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Colombia Médica v49n1 -Back cover PDF

Colombia Médica Colombia Médica 1-8

EDITORIAL
Epidemiology of cancer in Colombia Luis
Eduardo Bravo, Nubia Muñoz 9-12

Public health and epidemiology of cancer in Colombia


Carolina Wiesner 13-15

ORIGINAL ARTICLES
Cancer incidence estimates and mortality for the top five cancer in
Colombia, 2007-2011
Constanza Pardo, Ricardo Cendales 16-22

Reliable information for cancer control in Cali, Colombia


Luis Eduardo Bravo, Luz Stella García, Paola Collazos, Edwin 23-34
Carrascal, Oscar Ramírez, Armando Cortés, Marcela Nuñez,
Erquinovaldo Millán

Trends in cancer incidence and mortality over three decades in Quito -


Ecuador
Fabian Corral Cordero, Patricia Cueva Ayala, José Yépez Maldonado, 35-41
Wilmer Tarupi Montenegro

Trends in cancer incidence, and mortality in Pasto, Colombia. 15 years


experience
María Clara Yepez Chamorro, Daniel Marcelo Jurado Fajardo, Luisa 42-54
Mercedes Bravo Goyes, Luis Eduardo Bravo

Cancer incidence and mortality in Barranquilla, Colombia. 2008-2012


Rusvelt Vargas Moranth, Edgar Navarro-Lechuga 55-62

Health inequities and cancer survival in Manizales, Colombia: a


population-based study

Nelson Enrique Arias-Ortiz, Esther De Vries 63-72

Cancer incidence and mortality in Bucaramanga, Colombia. 2008-2012


Claudia Janeth Uribe Pérez, Sergio Serrano-Gómez, Claudia Milena 73-80
Hormiga Sánchez

Cancer incidence and mortality in Medellin-Colombia, 2010-2014


Mary Ruth Brome Bohórquez, Diego Montoya Restrepo, Liseth Amell 81-88

Oncology services supply in Colombia


Eliana Marcela Murcia Monroy, Jairo Aguilera, Carolina Wiesner, 89-96
Constanza Pardo

Pediatric oncology services in Colombia


Amaranto Suarez Mattos, Jairo Aguilera, Edgar Augusto Salguero, 97-101
Carolina Wiesner

Breast and cervical cancer survival at Instituto Nacional de


Cancerología, Colombia
Constanza Pardo, Esther de Vries 102-108

TECHNICAL REPORT
Cali Cancer Registry Methods

Luz Stella Garcia, Luis Eduardo Bravo, Paola Collazos, Oscar 109-120
Ramirez, Edwin Carrascal, Marcela Nuñez, Nelson Portilla,
Erquinovaldo Millan

Quality of death certification in Colombia


Ricardo Cendales, Constanza Pardo 121-127

Cancer risk management in Colombia, 2016


Paula Ramírez-Barbosa, Lizbeth Acuña Merchan 128-136
Bravo LE/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)

Editorial

Epidemiology of cancer in Colombia


Epidemiología del cáncer en Colombia

Luis Eduardo Bravo1, Nubia Muñoz2


1
Editor asociado, Revista Colombia Médica, Universidad del Valle, Cali, Colombia.
2
Professor Emérita del Instituto de Cancerología de Colombia

Bravo LE, Muñoz N . Epidemiology of cancer in Colombia. Colomb Med (Cali). 2018; 49(1): 09-12. doi:10.25100/cm.v49i1.3877.

© 2018. Universidad del Valle. This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use,
distribution, and reproduction in any medium, provided the original author and source are credited.

In this special issue dedicated to cancer, Colombia Medica discloses In this issue of Colombia Medica, the PBCR-Cali describes the
an analysis of the cancer situation in Colombia and Ecuador. The principles and methods used to analyze 50 years of incidence
analysis is based on the data collected and analyzed by several (1962-2012), 30 years of mortality (1984-2014) and 15 years of
Population-based Cancer Registries (PBCR), carried out with survival data (1995-2009)5. Six Colombian PBC-Registries and one
an inter-institutional collaborative effort of public and private Ecuadorian PBC-Registry show the collection, classification and
Colombian universities, Municipal and Provincial Secretaries of analysis of all new cancer cases and cancer deaths that occurred
Health, and the Ministry of Health and Social Protection through in Quito, Cali, Pasto, Bucaramanga, Manizales, Barranquilla and
the National Institute of Cancer of Colombia; and of the Fight Medellín during the period 2008-20126-12.
Cancer Foundation of Ecuador, SOLCA-Core of Quito. This
valuable contribution of the academic sector to the control and The Population-based Cancer Registries of Cali, Quito and Pasto
surveillance of cancer in Colombia needs reciprocity from the have at least 15 years of good quality information and present
Ministry of Health. It is necessary to regulate the participation of valid results of cancer incidence and mortality trends in their
RPC in the cancer information system; and to assign permanent respective populations6-8.
resources to guarantee their sustainability.
The PBCR-Cali 7, PBC-Manizales10 and the hospital-based cancer
For forty years the Population-based Cancer Registry of Cali (RPC- registry (HBC-Registry) of the NCI-Colombia13, the only HBC-
Cali) was the only source of valid information on the incidence Registry in the country, present survival data for the types of
of cancer in Colombia1. To increase coverage, the National cancer with the highest morbidity in Colombia: prostate, breast,
Cancer Institute of Colombia (NCI-Col), with the advisory of cervix, colon and stomach.
the Universidad del Valle, promoted during the first decade of
Data analysis shows that there is a significant decrease in the
the XXI century the creation of PBCR in strategic regions of the
incidence and mortality rates of the infectious-related cancers and
country. Thanks to this effort, the incidence information of the
tobacco-related cancers; and an increase in the incidence rates
Colombian cities of Pasto, Manizales and Bucaramanga was added
of cancers related to early detection activities (breast, prostate,
to that of Cali and published since 2012 in Cancer Incidence in
colon) and new diagnostic techniques (thyroid cancer)6-8.
Five Continents2, and the four Colombian RPC participated
in the CONCORD3  study, the global monitoring program for Barranquilla and Medellín report for the first-time data on the
cancer survival. Due to advances in cancer control and the great incidence of cancer11,12. Barranquilla, a coastal city and the main
strength of its RPC, Cali is the first city in the world to implement economic center of the Colombian Caribbean region, shows the
the initiative “C/Can 2025: Challenge of Cities Against Cancer;” highest incidence rates of breast and cervix uteri cancer, while
a project of the Union for International Cancer Control (UICC) its rates for gastric cancer and all cancer sites are the lowest in
that seeks to increase the coverage and quality of oncological care Colombia. It is important to conduct specific investigations to
in cities with more than one million inhabitants in low and middle determine if these differences are the result of including non-
income countries4. resident cases, duplication and/or information under reporting.

Corresponding author:
Luis Eduardo Bravo: Director Registro Poblacional de Cáncer de Cali, Escuela de Medicina,
Universidad del Valle, Cali, Colombia. e-mail: luis.bravo@correounivalle.edu.co
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Bravo LE/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)
Medellín, located in the Andean mountains of northwestern To estimate risk measures, PBC-Registries must have a delimited
Colombia, is the second most populated city in the country, with registry area and a clear definition of “case”. In this definition, it
particular demographic characteristics; it presents the incidence is critical to include only the new cancer cases diagnosed in the
for cancers prioritized by the Ten-Year Plan for Cancer Control permanent residents of the city and to exclude the cancer cases
in Colombia. It should be noted that nearly 100% of new cases of patients referred to the city for diagnostic and/or treatment
of cancer registered have morphological verification12, so that the procedures. The data collection must be both passive and active in
results correspond more to a Population Registry of Pathology. the different sources of information.
In this sense, the information on the risk of cancer in Medellín is
most probably underestimated since it does not include cases with PBC-Registries require adequate and sustained resources to be
a clinical or imaging diagnosis and those whose only evidence of successful. In Colombia, the per capita registration cost varies
cancer is the death certificate. Therefore, the rates for Medellín are between US $0.05 to US $0.22. Between 20% and 45% of the total
cost is due to activities with a fixed cost. Universities have been
not comparable with those of other Colombian PBC-Registries.
the main source of financial resources and of both scientific and
The NCI-Colombia characterizes the current situation of the technical personnel, which has allowed them to be successful.
supply of oncological services in Colombia14, and it demonstrates Another success factor of the PBC-Registries is the social
that the certification of cancer deaths in Colombia is of good recognition in the city, facilitating the process of data collection.
quality15. The NCI-Colombia uses the information from four
cancer registers7-10and the official mortality figures, to make valid The report of NCI-Colombia14 shows this reality concerning
estimates of cancer incidence for the entire country and for each oncological services in the country, the system serves 63,000 new
one of the provinces in Colombia15. The cancer risk estimates cases of cancer annually 16. Colombia has 1,780 habilitated services,
for Colombia will be more precise when the information from but only 25 providers offer joint chemotherapy, radiotherapy and
Barranquilla11 and Medellín12 can be included in the future. surgery services. Nearly 50% of the offer is concentrated in Bogotá,
and the provinces of Antioquia and Valle del Cauca; 87.8% is
Figure 1 shows the location of the RPC-Colombians, and Table offered by Institutions, and 12.2% by independent (health)
1 the incidence rates for the five leading causes of cancer morbidity professionals. 66.7% of the oncology services are outpatient,
in Colombia, prioritized by the Ten-Year Plan for Cancer Control, 17.4% of diagnostic support and therapeutic complementation
2012-2025. services, and 15.9% of surgical services; 87.9% of the offer of

Barranquilla
1,224,000 h

Venezuela
Bucaramanga
1,100,000 h

Medellín
2,400,000 h

Manizales
400,000 h

Cali
2,300,000 h

Pasto
350,000 h

Quito

Brasil
Ecuador

Perú

Figure 1. Location of the Population-based Cancer Registries in Colombia. The physical location of the RPC-Colombians
is linked to their administrative dependency; all are in universities, except for the PBC-Antioquia, which is located in
the Provincial Health Secretariat. The universities have been the main source of financial resources and of scientific and
technical personnel for the PBC-Colombians; its directors have academic and research experience Data are inhabitant.

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Bravo LE/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)
Table 1. Rates of cancer incidence (100,000 persons-year) for the most frequent cancers, prioritized in the Ten-Year Plan for Cancer
Control in Colombia.
Colon C18-C21 Stomach C16
Region Breast C50 Prostate C61 Cervix C53
♂ ♀ ♂ ♀
1. Cali 44.3 59.7 15.3 16.2 14.0 20.2 10.7
2. Pasto 27.7 27.3 18.0 8.4 9.0 26.7 11.8
3. Bucaramanga 41.2 40.9 13.0 14.3 13.7 17.1 10.2
4. Manizales 37.2 44.1 17.5 14.7 14.7 20.3 9.7
5. Barranquilla 65.7 43.0 26.6 9.6 9.8 4.4 2.2
6. Medellín 36.5 38.6 8.5 7.5 6.9 12.4 8.1
7. Colombia-INC 33.8 46.5 19.3 12.2 12.3 18.5 10.3
8. Quito-Ecuador 38.8 62.9 18.6 13.2 11.9 20.3 14.5

oncological services in Colombia is in the private sector. There is Conflict of interest: 


clear evidence of fragmentation in the provision, so it is necessary None to declare
to redefine the services and to make a comprehensive oncological
care approach for the diagnosis and treatment of patients with Referencias
cancer, in order to improve clinical outcomes.
1. Bravo LE, Collazos T, Collazos P, García LS, Correa P. Trends
Despite this wide range of services, the 5-year global survival of of cancer incidence and mortality in Cali, Colombia. 50 years
childhood cancer in Cali (51%) is between 26% and 32% below experience. Colomb Med (Cali). 2012; 43(4): 246-55.
the reported results for affluent countries (77% to 83%). This
means that, if around 1,500 to 1,600 children with cancer are 2. Forman D, Bray F, Brewster DH, Gombe MC, Kohler B, Piñeros
treated in Colombia each year, 765 to 816 die within 5 years after M, et al (eds). Cancer Incidence in Five Continents, Vol. X. Lyon:
diagnosis. Of these, 390 to 512 deaths per year would be avoidable. International Agency for Research on Cancer; 2013. Available
This survival gap is maintained in all groups of neoplasms, except from: http://ci5.iarc.fr. 
for Hodgkin’s lymphoma (88% vs 95%). In adults, the situation
is similar; the 5-year net survival to prostate, cervix and breast 3. Allemani C, Matsuda T, Di Carlo V, Harewood R, Matz M,
cancer is between 20 and 30 points below that observed in North Nikšić M, et al. Global surveillance of trends in cancer survival
America and Europe. During the period 2000-2004, the 5-year 2000-14 (CONCORD-3): analysis of individual records for
net survival improved for cancers of the breast, cervix, prostate, 37 513 025 patients diagnosed with one of 18 cancers from 322
melanoma and thyroid, although in the period 2005-2009, it was population-based registries in 71 countries. Lancet. 2018 Mar
observed a stagnation. In stomach, liver and lung cancer, the 17;391(10125):1023-1075. doi: 10.1016/S0140-6736(17)33326-3.
5-year net survival was less than 15%7.
4. Bravo LE, Arboleda OI, Ramirez O, Durán A, Lesmes MC, Rendler-
The PBC-Manizales  analyzed the differences in the survival for
10 García M, et al Cali, Colombia, Key learning City C/Can 2025: City
breast, cervix, lung, prostate and stomach cancers; it highlights Cancer Challenge. Colomb Med (Cali). 2017;48(2):39-40
the existence of important inequities in cancer survival related
5. García LS, Bravo LE, Collazos P, Ramírez O, Carrascal E, Nuñez
to health insurance and socioeconomic status, attributable to the
M, Portilla N, Millán E. Cali Cancer Registry Methods. Colomb
barriers and delays in obtaining diagnostic care that are associated
Med (Cali). 2018; 49(1): 109-20.
with more advanced stages at the time of diagnosis.

The HBC-Registry of NCI-Colombia13, Colombia’s only hospital- 6. Cueva AP, Yepes MJ, Turupi MW. Trends in cancer incidence
and mortality over three decades in Quito - Ecuador. Colomb
based cancer registry, analyzed survival in 1,928 cases of breast
Med (Cali). 2018; 49(1): 35-41
cancer and 1,189 cases of cervix uteri cancer. The estimated overall
survival probability was 79.6% for breast cancer and 63.3% for cervix
7. Bravo LE, García LS, Collazos P, Carrascal E, Ramírez O, Cortés
uteri cancer. Overall survival was 32.2% for stage IV breast cancer A, Nuñez M, Millán E . Reliable information for cancer control in
and 22.6% for stage IV cervical cancer. These survival estimates are Cali, Colombia. Colomb Med (Cali). 2018; 49(1): 23-34.
like those reported by the cancer-registries4,7,10; It would be expected
that the survival estimates in a cancer center would be higher than 8. Yepez MC, Jurado DM, Bravo LM, Bravo LE. Trends in cancer
the estimates observed by the cancer registries. It is necessary to incidence, and mortality in Pasto, Colombia. 15 years experience.
review the guidelines for clinical management in cancer patients Colomb Med (Cali). 2018; 49(1): 42-54.
treated at the NCI-Colombia.
9. Uribe PCJ, Serrano GSE, Hormiga SCM. Cancer incidence and
In Conclusion, the pioneer effort of the population-based Cancer mortality in Bucaramanga, Colombia. 2008-2012. Colomb Med
registry of Cali and of the Universidad del Valle and their (Cali). 2018; 49(1): 73-80.
collaboration with other academic and public institutions has
made possible a precise estimation of the cancer burden in various 10. Arias-Ortiz NE, de Vries E. Health inequities and cancer
regions of Colombia and in Quito, Ecuador; this information is survival in Manizales, Colombia: a population-based study.
basic and essential in the planning of strategies for cancer control. Colomb Med (Cali). 2018; 49(1): 63-72.
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Bravo LE/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)
11. Vargas Moranth R, Navarro Lechuga E. Cancer incidence and 14. Cendales R, Pardo C. Quality of death certification in
mortality in Barranquilla, Colombia. 2008-2012. Colomb Med Colombia. Colomb Med (Cali). 2018; 49(1):121-127
(Cali). 2018; 49(1): 55-62.
15. Pardo C, Cendales R. Cancer incidence estimates and mortality
12. Brome Bohórquez MR, Montoya Restrepo DM, Salcedo LA. for the top five cancer in Colombia, 2007-2011. Colomb Med
Cancer incidence and mortality in Medellin-Colombia, 2010- (Cali). 2018; 49(1): 16-22.
2014. Colomb Med (Cali). 2018; 49(1): 81-88.
16. Pardo C, de Vries E. Breast and cervical cancer survival in
13. Suarez MA, Aguilera J, Salguero EA, Wiesner C. Pediatric Instituto Nacional de Cancerología, Colombia. Colomb Med
oncology services in Colombia. Colomb Med (Cali). 2018; 49(1): (Cali). 2018; 49(1): 102-108.
97-101.

Colomb Med. (Cali) 49(1): 9-12

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Editorial

Public health and epidemiology of cancer in Colombia


Salud pública y epidemiología del cáncer en Colombia

Carolina Wiesner
Directora. Instituto Nacional de Cancerología de Colombia, Bogota, Colombia

Wiesner C. Public health and epidemiology of cancer in Colombia. Colomb Med (Cali). 2018; 49(1): 13-15. doi: 10.25100/cm.v49i1.3885

© 2018. Universidad del Valle. This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use,
distribution, and reproduction in any medium, provided the original author and source are credited.

Understanding the epidemiology of cancer has been a relatively Since then the International Agency for the Research on Cancer
recent challenge for health systems of middle and low-income (IARC) has emphasized promoting a validated methodology such
countries, since the predominant pathological profiles, up to the as population-based cancer registries (RCBP)4. These registries
second half of the XX century, had been acute and communicable constitute a strategy that allows us to collect data reliably on the
diseases and therefore cancer was not given sufficient visibility1. incidence in a designated population which in addition allows us
The epidemiology of communicable diseases requires a specific to make comparisons between countries6. Frequently, we believe
epidemiological approach, with information that is almost in real that with hospital and clinic registries it is possible to obtain data
time, or maximum up to one year; it also requires information on incidence since the diagnosis of the patients that visit them is
based on the classification of the causal agent, with the primary registered on these. However, the objective of these registries is
objective of controlling epidemiological outbreaks2. In contrast, mainly administrative and to register the clinical evaluation. For
the objectives of the epidemiological surveillance of cancer are: this reason, hospital registries are not useful to generate or provide
monitoring the behavior of different risk factors, estimating the measures on the appearance of cancer in a specific population
population risk of developing the illness, -in a designated area and environment, precisely because it is not possible to define the
and time-, as well as measuring the impact of interventions by population where the cases occur. Currently, 35% of all countries
analyzing survival and mortality2. Since modifying the incidence in the world have high quality RCBP to report cancer incidence
or mortality by cancer requires interventions which imply a and in Latin America only 22 % of countries count on these2.
minimum of five years, generating information in cancer is
generally done every five years. Colombia was a pioneer in the development of RCBP with the
registry in Cali (RCPB-Cali), at the Universidad del Valle founded
In high-income countries, the epidemiological transition towards in 1962 under the boost of Pelayo Correa, an investigator focused
the predominance of chronic illnesses began in the XVIII on establishing causal hypotheses of stomach cancer and William
century3. Since cancer started to become a significant public Haenszel from the National Cancer Institute of the United States7.
health problem in these countries, it was imperative to be able to Based on their creation, the RCPB-Cali has generated high quality
measure cancer incidence. Different methodologies were used for information about cancer incidence, as the only one in the regional
this, such as surveys sent to physicians and passive registries that context, which has a population base of such a long trajectory7-9.
were not effective since we found that they only reported a third
of the cases 4. This situation was very worrying because it makes it The RCPB-Cali had a limited scope to demonstrate the reality
difficult to determine the population risk as well as the possibility of the entire country because Colombia has great geographical,
to establish causal hypotheses in investigation4. It was in 1946, demographical, social and cultural differences between its
when a Commission of international experts on the subject, regions10. Based on the expertise and trajectory of the RCBP in
suggested to the World Health Organization that they establish Cali, Pasto generated a second RCBP. Subsequently and with the
cancer registries with a standard methodology that was valid additional support of the National Cancer Institute of Colombia
and reliable. This was the most significant precedent to form the (INC-Colombia) they created the RCBP of Bucaramanga,
International Association of Cancer Registries (IACR) in 19765. Barranquilla, Manizales, so that at the end of 2010 there were

Corresponding author:
Carolina Wiesner. Directora Instituto Nacional de Cancerología de Colombia.
Calle 1 No.9-85 Bogotá. Telefono +57 1 4320160. E-mail: cwiesner@cancer.gov.co

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Wiesner /et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)
already five RCBP, four of which have been endorsed by the IARC, nature. Private companies as well as some insurers in Colombia
and its information circulated in the “Cancer Incidence in Five open oncological services, especially for external consultation
Continents”11  book. Other department registries in Antioquia, and chemotherapy, without guaranteeing comprehensiveness
Cesar and Huila, have worked in generating information with but prioritizing those services in which the use of cutting-edge
difficulties in its implementation12. Based on this information technology represents a favorable business opportunity such as
about municipal RCBP as well as information on mortality, supplying expensive medications19.
the INC-Colombia applies the estimation methodology of the
incidence used by the IARC as the main input to estimate cancer Likewise, and according to the articles presented, it is worrying
incidence in the different departments and for the country13. that the Ministry of Health and Social Protection uses the same
instrument to activate functional units for cancer treatment in
In addition, the RCBP allows us to generate survival information adults and Childhood Cancer Comprehensive Care Units20. It is
as the most important outcome to evaluate the comparative clear that to guarantee the comprehensiveness for these two types
effectiveness of health systems regarding the control of the cancer14. of populations there must be a differential approach in which the
Global survival is also the most important outcome to evaluate fundamental variable is the frequency of the illness19. It is not the
the effectiveness of the treatments an health system. Undoubtedly, same to guarantee the comprehensiveness for 1,312 new cases
the comprehensive care of patients improves survival in that the of cancer in children under 14 years of age than for the close to
cancer treatment requires a multidisciplinary look. 62,000 cases of cancer in adults annually.

This issue of Colombia Médica Magazine highlights the work We expect that this issue of Colombia Medica contributes to
done through the methodology based on the RCBP to obtain promoting a unification of concepts relevant to the field of public
valid estimates of cancer incidence in a population. It is important health and epidemiological surveillance of cancer considering that
to highlight this trajectory because since the year 2014, cancer it is the most important health challenge that we will have to face,
incidence figures have been published in Colombia that have their moving forward, and therefore it is important to count on analysis
source of information in the administrative database of the health instruments for health decision making.
system in Colombia (BDA-SSC for its initials in Spanish). These
publications, which demonstrate the advantage of having national Conflict of interest:
coverage, have generated controversies due to the magnitude of None declared
the differences in cancer incidence figures when compared to
those generated by the RCBP15. The sub-registry and the non- Referencias
validation of the information generated by the BDA-SSC16  are
not useful to evaluate the population risk nor do they measure 1. McKeown RE. The epidemiologic transition: changing patterns
the impact policies, or the health system have had on controlling of mortality and population dynamics. Am J Lifestyle Med. 2009;
cancer in the country17,18. 3(1 Suppl):19s-26s.

Based on the information of the RCBP and the mortality 2. Pineros M, Znaor A, Mery L, Bray F. A global cancer surveillance
information from the DANE (National Administrative framework within noncommunicable disease surveillance:
Department of Statistics); the INC-Colombia generates incidence making the case for population-based cancer registries. Epidemiol
estimates in the different departments of the country applying the Rev. 2017; 39(1):161-9.
methodology used by the IARC. The TIEE (initials in Spanish for
incidence rates) for all cancers except skin cancer, were 151.5 in 3. dos Santos SI. Cancer epidemiology: principles and methods.
men and 145.6 in women, which contrasts with the rates in the Lyon: International Agency for Research on Cancer, World Health
United States of 347.0 in men and 297.4 in women. Organization; 1999.

Considering that survival rates is an outcome that must be 4. Wagner G. History of cancer registration. Jensen OM, Parkin
evaluated for the health systems not only in terms of population DM, MacLennan R, Muir RC, Skeet RG. Cancer registration:
but also institutionally, it shows survival data for patients treated principles and methods. Scientific Publication No. 95. IARC
for the first time for breast cancer and cervical cancer in the Scientific Publications. Lyon: IARC, WHO; 1991.
National Cancer Institute in the years 2007, 2010, and 2012. The
2-year survival rate of cervical cancer registered in the INC- 5. Muir CS. The International Association of Cancer Registries. The
Colombia is similar to the one registered in the Colombian and benefits of a worldwide network of tumor registries. Connecticut
United States RPCC14. On the contrary, the 24-month survival med. 1985;49(11):713-7.
rate of breast cancer in the INC was 79.6% when for the five-year
period of 2010- 2014 in the United States it reaches 90%. 6. Olsen J, Basso O, Sorensen HT. What is a population-based
registry? Scandin J Public Health. 1999; 27(1):78.
Finally, and from a public health perspective, Colombia Medica
Journal presents an analysis of oncological services carried out by 7. Muñoz N, Knaul F, Lazcano E. 50 años del Registro Poblacional
the surveillance performed by the National Cancer Institute. In de Cáncer de Cali, Colombia. Sal Publ Mexico. 2014; 56(5): 421-2.
this sense, there is an analysis of services for adults as well as for
children. Regarding the first group we find that in Colombia 87.9% 8. Correa P. The Cali cancer registry an example for Latin America.
of the provision of oncological services in Colombia is private in Colomb Med (Cali). 2012; 43(4):244-5.

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of cancer incidence and mortality in Cali, Colombia. 50 years J. Incidence and prevalence of cancer in Colombia: The
experience. Colomb Med (Cali). 2012; 43(4): 246-55. methodology used matters. J Global Oncol. 2017; 4:1-7. doi:
10.1200/JGO.17.00008.
10. Piñeros M, Murillo R. Incidencia de cáncer en Colombia
Importancia de las fuentes de información en la obtención de 16. Benchimol EI, Manuel DG, To T, Griffiths AM, Rabeneck L,
cifras estimativas. Rev Colomb Cancerol. 2004; 8(1): 5-14. Guttmann A. Development and use of reporting guidelines for
assessing the quality of validation studies of health administrative
11. Curado M-P, Edwards B, Shin HR, Storm H, Ferlay J, Heanue data. J Clin Epidemiol. 2011;64(8):821-9.
M, et al. Cancer incidence in five continents, Volume IX. IARC
Scientific Publication No. 160. Lyon: IARC, WHO; 2007. 17. de Vries E, Pardo C, Henríquez G, Piñeros M. Discrepancies in
the handling of cancer data in Colombia. Rev Colomb Cancerol.
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Colombia, Chile y Brasil. Facultad Nacional Salud Pública. 2013;
31(1): 127-35. 18. de Vries E, Pardo C, Wiesner C. Active versus passive cancer
registry methods make the difference: case report from Colombia.
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por cáncer en Colombia 2007-2011. Bogotá DC: Instituto Nacional 19. Murillo MRH, Wiesner CC, Acosta PJA. Modelo de atención
de Cancerología, Ministerio de Salud y Protección Social; 2015. de cáncer. Bogota: Instituto Nacional de Cancerología; 2014.

14. Allemani C, Matsuda T, Di Carlo V, Harewood R, Matz M, 20. Ministerio de Salud y Protección Social. Resolución 1477 de 2016.
Nikšić M, et al. Global surveillance of trends in cancer survival Por la cual se define el procedimiento, los estándares y los criterios
2000–14 (CONCORD-3): analysis of individual records for para la habilitación de las Unidades Funcionales para la Atención
37 513 025 patients diagnosed with one of 18 cancers from Integral de Cáncer del Adulto “UFCA” y de las Unidades de Atención
322 population-based registries in 71 countries. Lancet. 2018; de Cáncer Infantil “UACAI” y se dictan otras disposiciones. Bogota:
391(10125):1023-75. Ministerio de Salud y Protección Social; 2016.

Colomb Med. (Cali) 49(1): 13-15

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Pardo C/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)

Original article

Cancer incidence estimates and mortality for the top five cancer in Colombia, 2007-2011
Estimaciones de incidencia y mortalidad para los principales cinco tipos de cáncer en Colombia, 2007-2011

Constanza Pardo, Ricardo Cendales

Grupo de Vigilancia Epidemiológica del Cáncer, Instituto Nacional de Cancerología, Bogotá, Colombia

Pardo C, Cendales R. Cancer incidence estimates and mortality in the five first types of cancer in Colombia 2007-2011. Colomb Med (Cali). 2018; 49(1): 16-22.
Doi: 10.25100/cm.v49i1.3596.

© 2018 Universidad del Valle. This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use,
distribution and reproduction in any medium, provided that the original author and the source are credited.

Article history: Abstract Resumen


Received: 6 October 2017 Objectives: To describe the incidence and mortality for the five main Objetivos: Describir la incidencia y mortalidad para los cinco principa-
Revised: 15 November 2017 types of cancer in Colombia, from 2007-2011. les tipos de cáncer en Colombia, de 2007-2011.
Accepted: 22 February 2018 Methods: We estimated cases and cancer incidence rates standardised Métodos: Se estimaron casos y tasas de incidencia de cáncer ajustadas
by age, based on incidence/mortality ratios; and we calculated the ob- por edad a partir de razones incidencia/mortalidad y se calcularon las
Keywords: served deaths and mortality rates standardised by age in Colombia, both muertes observadas y tasas de mortalidad ajustadas por edad en Co-
Incidence; mortality; cancer; differentiated by province, type of cancer and sex. Incidence estimates lombia, ambas diferenciadas por departamentos, tipo de cáncer y sexo.
epidemiology; Colombia were generated based on information from four cancer population reg- Las estimaciones de incidencia se generaron con base en la información
istries (Cali, Pasto, Bucaramanga and Manizales), published in Cancer
Palabras clave: de cuatro registros poblacionales de cáncer (Cali, Pasto, Bucaramanga
Incidence in Five Continents, volume X, and the official mortality and
Incidencia; mortalidad; y Manizales), publicada en Cancer Incidence in Five Continents, volu-
population information of the National Administrative Province of Sta-
cáncer; epidemiología; men X, y la información oficial de mortalidad y población del Departa-
Colombia tistics (DANE, for its initials in Spanish).
Results: The annual number of expected cases (all cancers) was 62,818 mento Administrativo Nacional de Estadística (DANE).
in men and women; and there were 32,653 recorded deaths. The main Resultados: El número anual de casos esperados (todos los cánceres)
incidental cancers were prostate (46.5 per 100,000 person-years) in fue 62,818 en hombres y en mujeres y se registraron 32,653 muertes.
men, and breast (33.8 per 100,000 person-years) in women. The high- Los principales cánceres incidentes fueron próstata (46.5 por 100,000
est mortality figures were for stomach cancer in men (14.2); and breast años-persona) en hombres y mama (33.8 por 100,000 años-persona) en
cancer in women (9.9). mujeres. La mortalidad más alta en hombres se presentó en estómago
Conclusions: The highest incidence and mortality estimates in Co- (14.2) y mama en mujeres (9.9).
lombia were for breast and prostate cancers, as well as a proportion of Conclusiones: Las estimaciones de incidencia y mortalidad más altas
infection-related cancers, such as stomach and cervical cancer. These
en Colombia fueron para los cánceres de mama y próstata, además de
four neoplasms were responsible for more than 50% of the burden of the
una proporción de cánceres relacionados con la infección como son el
disease. Only through good quality, long-duration cancer registries, can
cáncer de estómago y de cuello uterino. Estas cuatro neoplasias fueron
information be obtained about the changes in incidence trends.
responsables de más del 50% de la carga de la enfermedad. Solamente
a través de los registros de cáncer de buena calidad y de larga trayec-
toria podrá tenerse información sobre el cambio en las tendencias de
incidencia..

Corresponding author:
Constanza Pardo, Grupo de Vigilancia Epidemiológica del Cáncer, Instituto
Nacional de Cancerología, Calle 1 No. 9-85, Tel.: 57 (1) 4320160 extensión
4806, Bogotá D.C., Colombia. Correo electrónico cpardo@cancer.gov.co
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Pardo C/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)

Introduction Materials and Methods


Colombia is considered to be a country with an intermediate The geographic ordering of the country is defined by regions (two
incidence of cancer within the world panorama, with rates or more provinces), provinces (set of several municipalities),
standardised by age estimated by the International Agency for special districts, municipalities and metropolitan areas (two
Research on Cancer (IARC) of 175.2 cases per 100,000 men, and or more municipalities). Based on this distribution, there were
151.5 cases per 100,000 women, excluding non-melanoma skin estimates made for cancer discriminated by sex, for 25 locations,
tumors1. For cancer, there are established methods to measure in 27 provinces, the Capital District and a region that grouped the
the incidence and mortality by location at the population level: provinces of Amazonas, Guainía, Guaviare, Vaupés and Vichada.
the population-based cancer registries (RCBP, for its initials in Incidence information included four RCBP, with information
Spanish), which collect information on the incidence and the vital from 2003-2007: Cali, Metropolitan Area of ​​Bucaramanga,
statistics systems of the countries that provide mortality data2. Manizales and Pasto. The mortality information was obtained
from the official mortality databases of DANE for the period
Achieving national coverage through a group of cancer registries 2003-2011. The population information for the same period was
generates a high cost3; therefore, a viable alternative is to use obtained from the national and province estimates and projections
information from a few RCBP located in strategic areas and the disaggregated by sex, area and five-year age groups of DANE17.
mortality data available at national level. The purpose is to obtain
reliable national estimates with a model that assumes that the The incidence/mortality ratio was calculated with the groups by
incidence of cancer in a region can be estimated from the number cancer location, based on the tenth edition of the International
of cancer deaths observed in that region, and from the observed Classification of Diseases. This methodology is available in the
incidence/mortality ratio in a region with similar characteristics4. base publication of this manuscript8. For this article, we analyzed
In the country, there are currently five RCBP (Cali, Pasto, five locations corresponding to stomach (C16), colon, rectum and
Bucaramanga, Manizales and Barranquilla); these cover 12% of anus (C18-21), female breast (C50), cervix (C53), and prostate
the population. (C61) in the provinces. The complete information for the country
is presented in Tables S1and S2.
The national estimate developed by the International Agency
Mortality
for Research on Cancer - IARC1 is based on these two methods;
Cancer mortality information required some quality adjustments
but it does not offer, at province level, the disaggregation that
in which deaths of non-residents in Colombia, deaths without sex
is required for the country5. Due to regional variations in the
or age information, and those certified by persons other than a
country, three studies have been carried out by the National
physician were excluded8. Deaths due to other ill-defined causes
Cancer Institute (INC, for its initials in Spanish) under this
were not redistributed, nor were cancer cases or deaths from ill-
perspective: the magnitude of the disease, incidence and mortality
defined sites, with the exception of uterine cancer of unspecified
at province level6-8, information that is useful for planning human
site (C55), which was redistributed among deaths from uterine
resource training, acquisition of equipment and provision of
cancer of specified site (C53-C54), as it is recommended by the
cancer prevention, detection, diagnosis and treatment services9. In
standard methodology18. The information of the province of
addition to the estimates generated by IARC, cancer information residence was imputed by the province of occurrence of death,
at national level also comes from other sources that do not in those cases in which this information was not available. This
match each other. On the one hand, there are the INC estimates allocation was not applied to the cities in which the records are
based on the data from the RCBP in Cali, Manizales, Pasto and located, due to the errors that could be generated when correcting
Bucaramanga; and the national system of vital statistics. The data this information in small geographical areas. No adjustment was
used from RCBP comply with international quality standards made for under registration of mortality.
endorsed by the IARC10. The vital statistics system provides
information on mortality, with a coverage according to data from Estimation of incident cases
the World Health Organization of 98.5% for 200911, and a quality A specific generalized linear model was used for each location,
of 92.8% according to the analysis of the certification of mortality which assumes that the number of cancer cases follows a Poisson
in Colombia, which was carried out for the 2002-2006 period12. distribution and uses a logarithmic transformation as a link
On the other hand, it has been necessary to have information function. The model considered as independent variables sex and
on the quality of cancer care, which is why passive (often age group (0-14, 15-44, 45-54, 55-64 and ≤65 years), in addition to
administrative) records on patient care have been created. From mortality as an offset variable, and it assumes that the incidence/
these administrative records, reports13,14 which are more updated mortality ratio is a constant value that is related through survival 19.
than those from RCBP have been made, but with incidence and The resulting model was the following:
mortality data with large differences and low reliability15,16. Ln(cancer cases) - Ln(deaths for cancer) + Bc + B sex + B2 
The objective of this article is to present estimates of cancer (age groups) + B3 (sex * age groups)
incidence and mortality observed in Colombia8, for the first five
cancers in men and women (prostate, stomach, breast, cervix and The model assumed that the incidence/mortality ratios would
colon-rectum) in the provinces, during the 2007-2011 period. be constant in the last five years. The national estimates for each

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Pardo C/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)

location were the result of the sum of estimated cases in each 2). Table S1shows the totality of locations in greater detail.
province. Readers can consult the book already published to
review more details of the methodology8. Prostate cancer corresponded to 29.8% of cancer cases among
men; it presented the highest ASIR in the provinces of San Andrés
Validation of the models and Providencia (90.0), Cesar (60.8), Atlántico (60.4) and Valle
The number of cases observed in each population registry was del Cauca (59.8) Similarly, breast cancer presented the highest
compared with that estimated from six different models in which ASIR in Valle del Cauca (43.5), Atlántico (42.8) and San Andrés y
the data from the registry or records not included as predictors are Providencia (41.9). Provinces such as Arauca (38.7), Meta (37.6)
assumed to be unknown, making the estimate from the remaining and Caquetá (30.8) had the highest incidence rates for cervical
records. Each of the first five models was weighed based on the cancer (Fig. 1a-e).
square root of the population of each record; the sixth model
corresponds to estimated data without considering weighing. The Age-standardised cancer incidence rates for stomach in men
accurate fit of the models was not evaluated because they were all predominated in Quindío (32.1), Huila (30.2) and Cauca (26.8);
saturated. in women, they were higher in Cauca (16.9), Norte de Santander
(15.9) and Quindío (15.6). In contrast, the Caribbean region
To evaluate the statistical validity of each model, the difference presented the lowest ASIR, in a range of 3.3 -10.7 in men and
between the number of cases detected by the registry and the 2.4 - 6.0 in women (Table 2S). ASIR for colorectal cancer were
number of cases estimated by the model was calculated; based on very similar for both sexes. In men, Quindío (18.3), Bogotá (18.0)
these differences, the sum of squared errors was calculated. Table and Risaralda (16.0) predominated; in women, Quindío (18.5),
1 shows the model used for the estimations, which was generated Risaralda (16.6) and Caldas (16.2).
from the weighted model with combined information from the
Cali, Pasto, Manizales and Bucaramanga cancer registries, which Table S2 shows the highest province rates for all cancers; 55%
obtained the lowest values of the sum of squared errors ​​- SSE. of cancers occurred in five provinces (Antioquia, Bogotá,
Cundinamarca, Santander and Valle del Cauca). In men, the
Crude rates (CR) were calculated for cancer incidence and largest ASIR were in Quindío (195.5), Risaralda (182.4), Valle
mortality per 100,000 person-years for each of the cancer sites, del Cauca (179.6) and Antioquia (173.1); in women, Quindío
according to sex and provinces of the country. The CR were (193.3), Caldas (170.4), Risaralda (168.6) and Meta (167.9). The
standardised by age (ASR) using the direct method with the world incidence of cancer in Bogotá and nine other provinces was above
reference population (SEGI population). the national average (151.5). Men had a lower incidence ratio than
women only in the provinces of Tolima (M: F; 0.9: 1) and Nariño
Results (M: F; 0.9: 1).

Incidence of cancer Mortality from cancer


The annual national estimate of incident cases for 2007-2011 was Annual cancer deaths in men and women were 32,653; 16,081 in
62,818 cases of cancer, 29,734 in men and 33,084 in women. Age- men and 16,572 in women, with an age-standardised mortality
standardised cancer incidence rates (ASIR) per 100,000, in men rate (ASMR) of 82.3 in men and 73.2 in women (Table S1). The
were 151.5 and 145.6 in women (Table S1). Women had a lower incidence / mortality ratio was 1.8 in men and 2.0 in women.
incidence ratio than men in stomach cancer (M: F: 1.8: 1), and a Cancers in men with the highest ASMR occurred in stomach
similar incidence ratio in colorectal cancer (M: F; 1: 1). (14.2), prostate (12.6), and colorectal (6.0). In women, breast
(9.9), cervix (8.2) and colorectal (6.1) (Table 2).
In men, the highest ASIR were for prostate (46.5), followed by
stomach (18.5) and colorectal cancer (12.2). Among women, the Age-standardised mortality rate for provinces showed notable
highest ASIR were for breast (33.8), cervix (19.3), colorectal (12.3) differences. 56.0% of the deaths occurred in the provinces of
and stomach (10.3). The incidence of breast cancer was twice as Antioquia, Bogotá, Cundinamarca, Santander and Valle del
high as cervical cancer, and it accounted for 23.0% of all cancer Cauca. The largest ASMR for men were found in Quindío (111.2),
cases in women and 37.6% together with cervix. The five cancers Risaralda (103.2), Antioquia (99.7) and Valle del Cauca (96.8); for
(prostate, breast, cervix, stomach and colorectal) are responsible women, Quindío (91.5), Caldas (85.5), Risaralda (91.0) and Meta
for more than 50% of new cancer cases in Colombia (Table (86.2) (Table S2).

In men, the provinces with the highest ASMR for stomach were
Table 1. Sum of the differences between the observed cancer cases
in Quindío (24.4), Huila (23.2) and Cauca (20.5). In women,
and the estimated cases squared (sum of squared errors - SSE).
the highest were in Cauca (12.8), Norte de Santander (12.1) and
SSE according to the RPC
included in the model
Men Women Total Quindío (11.8). Prostate cancer predominated in San Andrés
SSE RPCC 229,603 230,699 460,302 (25.5), Atlántico and Valle del Cauca, both with ASMR of 16.6.
SSE RPCC, RPCB 113,099 200,271 313,370 Mortality per breast cancer represented 13.4% among all cancer
SSE RPCC, RPCP 193,892 182,835 376,727 deaths in women; the highest rates presented in San Andrés
SSE RPCC, RPCM 190,927 173,383 364,311
SSE RPCC, RPCP, RPCM, RPCB 113,296 142,270 255,566
(13.3), Valle del Cauca (12.7) and Atlántico (12.5). Provinces such
SSE RPCC, RPCP, RPCM, RPCB* 126,325 145,327 271,652 as Meta (16.5), Arauca (15.9) and Caquetá (13.2) also had the
* Not weighted RPC: Population Registry of Cancer;
RPCC: Population Registry of Cancer, Cali;
highest mortality rates from cervical cancer. For colon-rectum,
RPCB: Population Registry of Cancer, Bucaramanga; the highest mortality rates occurred in Bogotá and the Old Caldas
RPCP: Population Registry of Cancer, Pasto;
RPCM: Population Registry of Cancer, Manizales. region (Fig. 1 a-e).
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Pardo C/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)

Table 2. Cancer incidence and mortality, five first locations, Colombia, 2007-2011.
Characteristics Stomach Colorectal Breast Cervix Prostate
C16 C18-C20 C50 C53 C61
5,955 5,185 7,627 4,462 8,872
Incident cases (year) Men 3,613 2,401 … … 8,872
Women 2,342 2,784 7,627 4,462 …
16.3 10.8 … … 40.0
Rates (men)
ASR 18.5 12.2 … … 46.5
10.3 12.2 33.5 19.6 …
Rates (women)
ASR 10.3 12.3 33.8 19.3 …
4,537 2,544 2,226 1,861 2,416
Observed Men 2,767 1,168 … … 2,416
deaths (year)
Women 1,770 1,376 2,226 1,861 …
12.5 5.3 … … 10.9
Rates (Men)
ASR 14.2 6.0 … … 12.6
Rates (Women) CR 7.8 6.0 9.8 8.2 …

AAR ASR 7.8 6.1 9.9 8.2 …


CR, crude rate
ASR, age-standardised rate (per 100,000 years - person)

Discussion In general, for Colombia, standardized rates of both incidence and


mortality were lower than in countries such as the United States,
According to these estimates, the five main locations of incidental Australia, New Zealand and countries of South America22. In turn,
cancers in Colombia are stomach, colorectal, breast, cervical, these five types of cancer were also the main incidental cancers
and prostate cancer. This is the third time that this exercise has and the leading cause of mortality in Central and South America.
been done for Colombia by provinces8, with the incorporation of However, it is highlighted that stomach cancer and cervical cancer
the recommendations made in past editions. For the first time, have much higher rates than in other Latin America countries,
data from four cancer registries, Cali, Pasto, Manizales and the such as Brazil, Argentina and Mexico, among others23.
Metropolitan Area of ​​Bucaramanga are included in the estimation
models, in addition to the official mortality data registered for The first three locations with the highest incidence (of cancer)
Colombia, with 92.8% of quality in the certification. The importance in men were prostate, stomach and colon-rectum; and breast,
of this incorporation lies in the fact that the current estimates reflect cervix and colon-rectum in women. It is noteworthy that all the
the diversity in the risk profiles for cancer incidence more for each five main locations are characterized by having surgical treatment
region. A relevant factor is the quality of the information produced as a fundamental element in the comprehensive management of
by the records included in the model, because they already complied the disease. By geographical location, these cancers occur in five
with international quality standards2. of the main provinces of Colombia, such as Antioquia, Bogotá,
Cundinamarca, Santander and Valle del Cauca, which have
The differences in the numbers incidence estimated by Globocan the largest population. This situation implies in absolute terms
2012 are related to the model selected, which includes data from (frequencies), the basis to make decisions about the number
cancer registries in South America and also for the use of estimated of health institutions needed in the different areas. In fact, this
mortality in the country. Estimating the incidence/mortality is corroborated in the panorama of oncology services enabled,
ratio based on the last available year of the registry generated mainly in surgery, and in these provinces of the country24.
very volatile figures, so for these locations the information from
The incidence and mortality from stomach cancer is one of the
the five-year period was used. However, for breast and prostate
first causes in the country, and this behavior is similar in Latin
cancer, Globocan 2012 considered that this assumption would not
American countries such as Argentina, Brazil, Chile and Costa
be met with the relative recent introduction of screening for these
Rica23. It is highlighted that despite the behavior, the tendency has
pathologies, with a fluctuating result in the incidence/mortality
been to decrease in recent decades25,26. This decrease is attributed to
ratios for these pathologies. This way, Globocan 2012 based the
the improvement in hygiene conditions and food preservation24,27.
incidence/mortality ratio only on the result of the most recent
In gastric cancer, the smallest difference between mortality rates
year of reporting of population registries20. On the other hand, versus incidence rates occurs because it is a highly fatal cancer.
the estimated annual figures for 2007-2011 were lower when
compared with the annual figures of incidence estimated in 2002- Colorectal cancer corresponds to 8.3% of the incident cases in
2006, because in this study the correction for under-registration the country, and its behavior in other Latin American countries
of mortality was not incorporated21. turns out to be much higher than in Colombia, even with higher
rates than for stomach cancer, in countries such as the United
When contrasting the incidence and mortality information States, Brazil and Argentina23. Obesity is one of its risk factors,
generated in Colombia using other sources13,14, a great difference in and its behavior in the country was of high figures of overweight
figures is evident, both in absolute numbers and rates. Probably this according to the survey of nutritional status (ENSIN, for its
discrepancy is due to the different methods used in the collection, Spanish acronym) from 2010. The highest prevalence of excess
processing and analysis of the data, sometimes resulting in less than weight occurred in urban areas (52.5%) and in women (84.1%),
50% of the real number of patients present in the country15. which may explain the behavior of the rates.

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Pardo C/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)

1b. Colorectal Age-Standarized Rate x 100,000 person-year


1a. Stomach Age-Standarized Rate x 100,000 person-year
25 20 15 10 5 0 5 10 15 20 25
40 30 20 10 0 10 20
Quindío 32.1 15.6 Quindío 18.3 18.5
24.4 11.8 8.4 8.5
Huila 30.2 13.2 Bogotá 18.0 15.9
23.2 10.2 9.0 7.8
Cauca 26.8 16.9 Risaralda 16.0 16.6
20.5 12.8 7.7 8.1
Nariño 26.1 14.8 Caldas 15.9 16.2
20.2 11.1 7.6 8.0
Norte de Santander 25.0 15.9 Valle del Cauca 14.9 15.3
19.4 12.1 7.3 7.5
Boyacá 24.7 13.1 Meta 14.0 15.0
19.0 10.0 7.1 7.6
Tolima 24.7 12.1 Santander 13.8 12.5
19.0 9.0 6.8 6.1
Caldas 24.5 12.2 Antioquia 13.5 13.5
18.6 9.2 6.7 6.7
Risaralda 24.5 13.4 Cundinamarca 13.5 9.9
18.8 10.2 6.6 4.9
Casanare 23.0 12.6 Tolima 11.9 13.3
17.3 8.7 5.8 6.7
Colombia 18.5 10.3
Colombia 12.2 12.3
14.2 7.8 6.0 6.1

Men Incidence Mortality Women Men Incidence Mortality Women

Age-Standarized Rate x 100,000 person-year Age-Standarized Rate x 100,000 person-year


1c. Breast
0 5 10 15 20 25 30 35 40 45 50 1d. Cervix Uteri 0 5 10 15 20 25 30 35 40 45

Valle del Cauca 43.5 Arauca 38.7


12.7 15.9
Atlántico 42.8
12.5 Meta 37.6
16.5
San Andrés 41.9 Caquetá 30.8
13.3 13.2
Arauca 39.9
10.7 Casanare 30.6
13.2
Quindío 38.9
11.5 Tolima 28.2
11.5
Caldas 38.4
11.2 Cesar 28.1
11.6
Bogotá 37.2
11.0 Quindío 26.7
10.4
Huila 36.9
10.6 Grupo Amazonas 25.9
11.7
Risaralda 36.4
10.9 Norte de Santander 25.5
10.4
Meta 36.4
10.8 Incidence Magdalena 23.9
10.2
Incidence
Colombia 33.8
9.9
Mortality
Colombia 19.3
8.2 Mortality

Age-Standarized Rate x 100,000 person-year


1e. Prostate
0 10 20 30 40 50 60 70 80 90 100

San Andrés 90.0


25.5
Cesar 60.8
16.0
Atlántico 60.4
16.6
Valle del Cauca 59.8
16.6
Arauca 58.3
12.8
Casanare 54.4
14.6
Magdalena 53.0
14.4
Chocó 52.1
13.1
Meta 50.6
12.9
Norte de Santander 50.0
13.6 Incidence
Colombia 46.5
12.6
Mortality

Figure 1(a-e). Cancer incidence and mortality, according to provinces, five main locations, Colombia, 2007-2011.

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Pardo C/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)

In relation to prostate cancer, it is the first diagnosis most Acknowledgements:


frequent in men, whose incidence rate (46.5) is below the rate The authors thank Dr. Esther de Vries for reviewing the
for South America (60.1), but above the rate for Central America manuscript and for her valuable comments. This article is part of
(28.4)23. In addition, it is the second cause of cancer mortality in the publications “Incidence, mortality and prevalence of cancer
Colombia, with the highest mortality rates in the coastal region in Colombia 2007-2011” - http://www.cancer.gov.co/files/libros/
and Valle del Cauca. The wide incidence ranges may be due to archivos/incidencia1.pdf “Incidence, mortality and prevalence
screening programs (prostate-specific antigen tests - PSA), to the of cancer in Colombia 2007-2011, attached tables “- http://www.
availability of treatment services in the different regions since cancer.gov.co/files/libros/archivos/incidencia2.pdf
these provinces coincide with those with the highest percentage
of Afro-Colombian population. Conflict of interest: 
The authors declare no conflicts of interest for this study
Something similar occurs with regional differences in breast
cancer incidence rates, provinces with a large proportion of Funding:
Afro-Colombian population; as well as being influenced by the The work was carried out with resources administered by the
availability of early detection services; and reproductive and National Cancer Institute (Epidemiological Cancer Surveillance
hormonal risk associated factors, such as overweight or obesity, Program
post-menopause, the use of menopausal hormone therapy,
physical inactivity and alcohol consumption28,29. References
A downward trend in cervical cancer has also been found , with the
26
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for this population. According to vaccination campaigns against Agency for Research on Cancer; 2013. Accessed: 24 May 2017.
HPV, coverage in 2012 was above 95% in the whole country, with Available from: http://globocan.iarc.fr.
the exception of Caquetá (82.2%), Vichada (74.4%) and Putumayo
(86.1%) for the first phase; Guainía, Vaupés and Caquetá, among 2. Piñeros M, Znaor A, Mery L, Bray F. A global cancer surveillance
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5. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo
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M et al. Cancer incidence and mortality worldwide: sources,
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de Cancerología; 2010.
surveillance, burden measurement and evaluation of the impact of
the disease32,33 present the difficulty of having a national coverage, 8. Pardo C, Cendales R. Incidencia estimada, mortalidad y
a situation that lies in viability and long-term sustainability3,34. prevalencia por cáncer en Colombia 2007-2011. Bogotá, D.C:
Instituto Nacional de Cancerología; 2015.
Population registries of cancer and vital statistics - DANE, provide
sufficient information to produce estimates at the national and 9. WHO. National cancer control programmes: policies and
province levels. It would be desirable to improve the quality of managerial guidelines. Second ed. Geneva, Switzerland: World
some existing cancer registries in other areas of the country, so Health Organization; 2002.
they can be included in the estimates, and to establish some other
registries, in order to expand the current coverage (12%). Only 10. Forman D, Bray F, Brewster DH, Gombe Mbalawa C, Kohler B,
through RCBP of good quality and long trajectory can information Piñeros M, et al. (eds) Cancer Incidence in Five Continents, Vol X. Lyon:
be obtained about changes in the incidence trends. IARC; 2013. Available from: http://ci5.iarc.fr/CI5-X/Default.aspx.
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11. WHO. Demographic and socioeconomic statistics: Census and 24. Murillo R, Wisner C, Acosta J, Piñeros M; Pérez JJ, Orozco M.
civil registration coverage. Data by country. Global Health Observatory Modelo de cuidado del paciente con cáncer. Bogotá D.C: Instituto
data repository, WHO; 2017. Accessed: 21 Juneo de 2017. Available nacional de Cancerología; 2015.
from: http://apps.who.int/gho/data/node.main.121?lang=en.
25. Ferro A, Peleteiro B, Malvezzi M, Bosetti C, Bertuccio P, Levi
12. Cendales R, Pardo C. La calidad de certificación de la mortalidad F et al. Worldwide trends in gastric cancer mortality (1980–2011),
en Colombia, 2002-2006. Rev Salud Publica . 2011;13(2):229-38. with predictions to 2015, and incidence by subtype. Eur J Cancer.
2014;50(7): 1330–1344.
13. Alvis LF, Acuña ML, Sánchez QP. Información preliminar
sobre el reporte de cáncer y el proceso de atención en Colombia. 26. Piñeros M, Pardo C, Gamboa O, Hernández G. Atlas de
Boletín de información técnica especializada. 2015; 1(4):1-12. mortalidad por cáncer en Colombia. Bogotá D.C: Instituto
Nacional de Cancerología; 2010.
14. Valencia, O, Lopes G, Sánchez P, Acuña L, Uribe D, González J.
Incidence and prevalence of cancer in Colombia: the methodology 27. Cueva P, Sierra MS, Bravo LE, Forman D. Etiology of stomach
used matters. J Glob Oncol. 2018; 4: 1-7. cancer (C16) in Central and South America. In: Cancer in Central
and South America. Lyon: International Agency for Research on
15. de Vries E, Pardo C, Henríquez G, Piñeros M. Discrepancias Cancer; 2016. Assessed:: 9 June 2017. Available from: http://www-
en manejo de cifras de cáncer en Colombia. Rev Colomb Cancerol. dep.iarc.fr/CSU_resources.htm.
2016;20(1):45–7.
28. Chlebowski RT, Manson JE, Anderson GL, Cauley JA, Aragaki
16. de Vries E, Pardo C, Wiesner C. Active versus passive cancer
AK, Stefanick ML, et al. Estrogen plus progestin and breast,
registry methods make the difference: case report from Colombia.
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29. Kabat GC, Jones JG, Olson N, Negassa A, Duggan C, Ginsberg
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%202014.pdf.
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Tieulent J, Bruni L, et al. Global burden of human papillomavirus
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Coebergh JW, Comber H, Forman D, Bray F. Cancer incidence
and mortality patterns in Europe: estimates for 40 countries in 32. Bray F, Znaor A, Cueva P, Korir A, Swaminathan R, Ullrich
2012. Eur J Cancer. 2013;49(6):1374-403. A, et al. Planning and Developing Population-Based Cancer
Registration in Low- and Middle-Income Settings. Lyon, France:
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de cáncer en el orden departamental en Colombia, 2002-2006.
Rev Colomb Cancerol. 2012;16(1):5-15. 33. Parkin DM. The evolution of the population-based cancer
registry. Nat Rev Cancer. 2006;6(8):603–12.
22. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A.
Global cancer statistics, 2012. CA Cancer J Clin. 2015;65(2):87-108. 34. Tangka FK, Subramanian S, Edwards P, Cole-Beebe M,
Parkin DM, Bray F, et al. Resource requirements for cancer
23. Sierra MS, Soerjomataram I, Antoni S, Laversanne M, Piñeros registration in areas with limited resources: analysis of cost data
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Colomb Med. (Cali) 49(1): 16-22

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Bravo LE/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)

Original article

Reliable information for cancer control in Cali, Colombia


Información fiable para el control del cáncer en Cali, Colombia

Luis Eduardo Bravo1,2, Luz Stella García1, Paola Collazos1, Edwin Carrascal1,2, Oscar Ramírez1,3,4, Tito Collazos1, Armando Cortés2,
Marcela Nuñez1, Erquinovaldo Millan5

1
Registro Poblacional de Cáncer de Cali. Cali, Colombia
2
Departamento de Patología, Facultad de Salud, Universidad del Valle, Cali, Colombia.
3
Fundación POHEMA. Cali, Colombia
4
Sistema de Vigilancia Epidemiologica de Cáncer Pediátrico (VIGICANCER), Cali, Colombia.
5
Secretaria de Salud Pública Municipal de Cali, Cali, Colombia.

Bravo LE, García LS, Collazos P, Carrascal E, Ramírez O, Cortés A, Nuñez M, Millán E. Reliable nformation for cancer control in Cali, Colombia. Colomb Med (Cali). 2018;
49(1): 23-34. doi: 10.25100/cm.v49i1.3689

© 2018 Universidad del Valle. This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use,
distribution and reproduction in any medium, provided that the original author and the source are credited.

History article Abstract Resumen


Received: 13 December 2017 Background: The Cali Population Cancer Registry (RPCC) has been in Antecedentes: El Registro Poblacional de Cáncer de Cali (RPCC) está en
Revised: 20 January 2018 continuous operation since 1962 with the objective of producing valid operación continua desde 1962 con el objetivo de producir estadísticas
Accepted: 13 February 2018
statistics on the incidence of cancer, its patterns, trends and survival rates. válidas sobre la incidencia de cáncer, sus patrones, tendencias y
Keywords: Methods: During the period 2008-2012, 23,046 new cases were supervivencia.
Cancer registry, incidence, registered and during 2011-2015 there were 12,761 cancer deaths. The Métodos: Durante el periodo 2008-2012, se registraron 23,046 casos
mortality, survival, methods, trend of the rates was described with the APC average annual change nuevos y durante 2011-2015 se registraron 12,761 defunciones por
Cali, Colombia rate and with the Joinpoint analysis. We analyzed the individual data cáncer. La tendencia de las tasas se describió con el porcentaje de cambio
of 38,671 adults (15-99 years) diagnosed with cancer between 1995- medio anual APC y con el análisis de Joinpoint. Se analizaron los datos
Palabras clave:
2009, and we calculated the standardized net survival by age for the individuales de 38,671 adultos (15-99 años) con diagnóstico de cáncer
Registro de cáncer, incidencia, 14 most common cancer body sites, using the Pohar-Perme method. entre 1995-2009, y se calculó la supervivencia neta estandarizada por
mortalidad, supervivencia,
métodos, Cali, Colombia Results: Prostate and breast cancer were the first cause of cancer edad para las 14 localizaciones más comunes de cáncer, con el método
morbidity. The incidence rates in these susceptible to early detection, de Pohar-Perme.
tumors stabilized after decades of growth, while an increase in the Resultados: Próstata y mama fueron la primera causa de morbilidad por
incidence of colon cancer and papillary thyroid carcinoma was cáncer. Las tasas de incidencia en estos tumores susceptibles de detección
observed. The incidence rates of cervical and stomach cancer, temprana se estabilizaron tras décadas de crecimiento, mientras que se
conditions related to infectious agents, decreased, although the observó un incremento de la incidencia de cáncer de colon y carcinoma
number of absolute cases increased, due to the growth and aging papilar de tiroides. Las tasas de incidencia de cáncer de cuello uterino y
of the population. Gastric cancer was responsible for the highest estómago, afecciones relacionados con agentes infecciosos, disminuyeron,
number of cancer deaths. The types of cancer related to tobacco aunque el número de los casos absolutos aumentó, debido al crecimiento
consumption (lung, oral cavity, esophagus, pancreas, urinary y envejecimiento de la población. El cáncer gástrico fue responsable del
bladder) showed low numbers and a tendency to decrease. During mayor número de muertes por cáncer. Los tipos de cáncer relacionados
the period 2000-2004, the 5-year net survival improved for cancers con el consumo de tabaco (pulmón, cavidad oral, esófago, páncreas, vejiga
of the breast, cervix, prostate, melanoma and thyroid, although in urinaria) mostraron cifras bajas y con tendencia al descenso. Durante
the period 2005-2009 a stagnation was observed. In stomach, liver el periodo 2000-2004, la supervivencia neta a 5 años mejoró para los
and lung cancer, the 5-year net survival was less than 15%. The cánceres de mama, cuello uterino, próstata, melanoma y tiroides, aunque
5-year overall survival in children was 51.0% (95% CI: 47.5, 54.3) en el periodo 2005-2009 se observó un estancamiento. En cáncer de
and in adolescents 44.6% (95% CI: 36.0, 52.8). estómago, hígado y pulmón, la supervivencia neta a 5 años fue inferior al
Comment: RPCC has been an advisor to the Colombian government 15%. La supervivencia global a 5 años en niños fue de 51.0% (IC 95%: 47.5,
in the evaluation of CPRs in the country and its data have contributed 54.3) y en adolescentes de 44.6% (IC 95%: 36.0, 52.8).
significantly to different aspects of cancer control in Colombia. Comentario: El RPCC ha sido asesor del gobierno colombiano en la
evaluación de RPCs en el país y sus datos han contribuido significativamente
Corresponding author: a diferentes aspectos del control del cáncer en Colombia.
Luis Eduardo Bravo, Director Registro Poblacional de Cáncer de Cali. Calle 4B 31-00
Oficina 4003, Edificio 116, Cali, Colombia. E-mail: luis.bravo@correounivalle.edu.co.

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Introduction females15. The infrastructure for cancer care includes 165 oncology
functioning services 16, these services are in the urban area where
Comprehensive cancer control is a strategic approach that brings 95% of the population resides in an area of ​​approximately 110
together the main associations and organizations of a community km2 that corresponds to 20% of the extension of the municipality
to prevent or minimize its impact and to develop a plan to reduce of Cali (503 km2).
the number of citizens who become ill or die from cancer. The
plans are specific, based on an analysis of the cancer situation in Incidence and mortality information
each country1. It is essential that the information on incidence, Information on the incidence of cancer was obtained from the
mortality and survival be of high quality because it will help database of the RPCC (2008-2012) and information on general
monitor and evaluate the programs. Population-based cancer mortality was obtained in the Municipal Public Health Secretary
registries (RCPobs) represent the gold standard for providing of Cali (2006-2015). Details on the history, objectives, logistics
cancer incidence and survival figures in a region and are a key and coverage of the RPCC have been previously described5,17.
element in cancer control because they provide indicators for This same issue of Colombian Medical describes in detail the
planning and evaluating cancer control activities and carrying out procedures and methods for estimating incidence, mortality
cancer research2. The information disclosed by these information and survival in adults18. In summary, the RPCC was established
systems in Colombia indicates that cancer is a public health in 1962, it is a population-based cancer registry which provides
problem that causes 63,000 new cases and 33,000 deaths each year3. continuous information on new cases of all types of cancer in
To face this threat, the Colombian government has formulated a permanent residents of Cali through active search and notification.
Ten-Year Plan for Cancer Control in Colombia (PDCC)4 focusing
on activities to control and reduce mortality from cancer of cervix, Implementation of a childhood cancer outcomes surveillance
stomach, prostate, breast, colon and acute pediatric leukemias. system (VIGICANCER) within Cali’s population-based cancer
registry was carried-out in 2009; methodological details have been
Colombia lacks an RCPobs with national coverage and for several published recently19,20. Briefly, children and adolescents (<19 years
decades the only source of valid cancer incidence information for of age) with new diagnosis of cancer and treated in a pediatric
the country was the Cali Population Registry of Cali (RPCC)5. oncology unit of the city, are registered by the system and included
Now it has three additional regional RCPobs that provide in an active follow-up. VIGICANCER includes both children living
quality cancer incidence information in Pasto6, Manizales7  and in the city as well as children from other Colombian municipalities
Bucaramanga8; and two new ones in the process of consolidation and provinces but treated in Cali. Vital status, relapse, treatment
in Barranquilla9 and Medellín10. The coverage of these six regional abandonment, and second neoplasms are the primary outcomes.
RCBPs is less than 12.9% of the Colombian population. To
overcome this limitation, health authorities use GLOBOCAN Results
methods to make national and regional cancer incidence estimates
1. New cases of cancer (incidence)
based on mortality information11. The incidence/mortality ratio
In the quinquennium 2008-2012, 23,046 new cases of cancer were
of the period of interest of each regional RCPob is incorporated
diagnosed among the permanent residents of Cali, for an average
into a mathematical model that uses this information and the
of 4,500 cases per year; 55% (12,613) occurred in females and the
mortality observed in each department as inputs to estimate
sex ratio was 1:2. The incidence rates standardized by age for all
the departmental and national incidence3,11. The validity of the
cancer sites per 100,000 person-years were 204.6 in men; and 185.1
estimates depends on the quality of the information and also on
in females. In the absence of other causes of death, the cumulative
the accurate quality of the certification of general mortality and
risk of developing cancer before reaching the age of 75 was 23.8%
cancer in Colombia and the coverage of the certification is close
and 20.5% in males and females in Cali.
to 100%12.
Cancer incidence rates per 100,000 person-year by sex and cancer
In this article, the Cali Population Registry discloses the most
location are shown in  Table 1. In men, the five primary sites of
recent cancer statistics in Cali, Colombia, for incidence and
primary cancer were prostate (ASR: 59.7), stomach (ASR: 20.2),
mortality rates standardized by age (ASR) for all cancers for the
colorectal (ASR: 16.2), lung (ASR: 14.5), and lymphomas (ASR:
periods 2008-2012 and 2008-2015, respectively; and the 5-year net
11.3). Together they constituted 58.8% of all new cancer cases
survival estimates standardized by age for the 14 most common
diagnosed between 2008 and 2012. Prostate cancer accounted for
cancer sites from 1995 to 2009. Estimating the incidence of
28.2% of all incident cases, (n: 2,937).
cancer in Colombia and creating some of the baseline indicators
of the current PDCC in the city is a contribution made by the In females, the most frequent locations for cancer according to
Universidad del Valle to the health authorities. their ASR were in descending order: breast (44.3), cervix (15.3),
colorectal (14.0), thyroid (13.2), and stomach (10.7). These
Materials and Methods
locations together accounted for 52.9% of all new cases of cancer
Population and registration area diagnosed during the five-year period. Breast cancer alone
Cali is the third largest city in Colombia, capital of the Department accounted for 23.6% of incident cases (n: 2,972).
of Valle del Cauca. According to the 2005 census and according
to the projections of the DANE13, the estimated population for 2. Mortality from cancer
2010 was 2.3 million inhabitants. 52% are females, and 26.2% Table 2  shows cancer deaths that occurred in Cali in two
self-identify as belonging to the black ethnic group14. The life quinquennial periods; 2006-2010 and 2011-2015. During this
expectancy at birth is 73.1 years for men, and 78.5 years for decade there were 122,014 deaths, (56.8% in males and 43.2% in

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Table 1. Cali, Colombia. Incidence rates standardized by age (World Population) per 100,000 person-year and the annual percentage
change (APC) by sex during the period 2008-2012
Male Female Male Female Code
Site n ASR n ASR APC 95% IC APC 95% IC ICD 10
Oral cavity and pharynx 279 5.4 233 3.4 -1.2* -1.7;-0.7 -1.1* -1.6;-0.5 C00 14
Oesophagus 90 1.7 72 1.0 -1.3* -2.1;-0.5 C15
Stomach 1,041 20.2 769 10.7 -1.9* -2.1;-1.7 -1.9* -2.1;-1.6 C16
Small intestine 39 0.7 37 0.5 C17
Colon and Rectum 831 16.2 996 1.4 2.4* 2.0;2.7 1.9* 1.5;2.3 C18 20
Anus 48 1.0 126 1.9 C21
Liver 249 5.0 218 3.1 1.7* 0.9;2.4 0.4 -0.5;1.2 C22
Gallbladder 120 2.4 264 3.7 -1.3* -1.9;-0.6 -1.8* -2.4;-1.2 C23 24
Pancreas 222 4.4 257 3.6 0.0 -0.5;0.5 C25
Nose, sinuses, etc. 38 0.7 18 0.3 C30 31
Larynx 202 4.0 37 0.6 -1.1* -1.6;-0.6 C32
Trachea, bronchi and lung 731 14.5 585 8.2 -0.6* -1.1;-0.1 0.5* 0.0;1.1 C33 34. C38 39
Bone 75 1.4 84 1.3 0.8 -0.1;1.6 0.1 -0.9;1.1 C40 41
Connective tissue 135 2.6 134 2.1 0.4 -0.2;1.0 C47 49
Mesothelioma 9 0.2 7 0.1 C45
Kaposi sarcoma 92 1.6 10 0.1 C46
Skin melanoma 145 2.8 179 2.6 1.1* 0.5;1.7 C43
Other skin 28 0.5 41 0.6 C44
Breast 26 0.5 2,972 44.3 1.4* 1.1;1.6 C50
Vulva 60 0.8 -1.6* -2.4;-0.8 C51
Vagina 44 0.7 C52
Uterus unspecified 37 0.5 C55
Uterine cervix 1,037 15.3 -3.0* -3.2;-2.8 C53
Corpus uteri 347 5.3 0.3 -0.1;0.7 C54
Ovary 513 7.7 -0.1 -0.5;0.2 C56
Other females genital organs 22 0.4 C57 58
Penis 74 1.3 C60
Prostate 2,937 59.7 3.0* 2.5;3.5 C61
Testicle 154 2.6 1.7* 1.0;2.5 C62
Other male genital organs 8 0.1 C63
Kidney 250 5.1 209 3.2 2.8* 2.1;3.4 2.3* 1.7;2.9 C64 66
Bladder 319 6.2 121 1.6 -0.7* -1.1;-0.3 -1.2* -1.7;-0.6 C67
Other urinary organs 3 0.0 4 0.1 C68
Eye 48 0.9 37 0.6 C69
Central Nervous System 271 5.2 269 4.3 1.2* 0.5;1.9 2.3* 1.2;3.4 C70 72
Thyroid 173 3.2 893 13.2 0.7 -0.1;1.5 2.6* 2.1;3.1 C73
Other endocrine 25 0.5 21 0.4 C74 75
Hodgkin's disease 91 1.7 63 1.0 -1.6* -2.2;-0.9 -0.6 -1.4;0.2 C81
Non-Hodgkin lymphoma 502 9.6 511 7,5 2.3* 1.7;2.8 2.1* 1.6;2.7 C82 85. 96
Multiple myeloma 156 3.1 142 2,1 C90
Lymphocytic leukaemia 205 4.0 211 3,6 2.1* 1.6;2.7 C91
Myeloid and monocytic leukaemia 172 3.3 173 2,6 0.0 -0.6;0.7 1.1* 0.5;1.6 C92 94
Non-specific leukaemia 53 1.0 53 0,7 C95
Unknown primary site 581 11.3 797 11,3 -0.3 -0.7;0.1 -0.8* -1.2;-0.4 **
All the sites 10,433 204.6 12,613 185,1 0.6* 0.4;0.8 -0.1 -0.2;0.1 C00 96
All sites * 10,405 204.1 12,572 184,5 0.6* 0.4;0.8 -0.1 -0.2;0.1 C00 43.45 96
** C26.39.48.76.80 - CIE O: 998_ / 3
Number of cases (n); Standardized incidence rate by age (ASR, by its acronym in English).
APC: For its acronym in English Annual Percent Change. APC is calculated for period 1962-2012
* All sites excluding non-melanoma skin cancer

females). Overall mortality from cancer corresponded to 19.6% higher among males (107.0) than among females (85.9). Cancer of
(23,873 deaths) of all deaths in that period and the number of stomach, lung, colorectal, breast and prostate were the main causes
deaths from this cause was greater among females (53.0%, 12,663) of cancer-related death, together they represent approximately
than among males (47.0%, 11,219). For the analysis of cancer half of all cancer deaths (47.9%).
mortality, emphasis was placed on the results of the quinquennium
2011-2015. Based on mortality rates standardized by age, prostate cancer (ASR:
17.4), was the leading cause of death among tumors in males in the
Cancer was the third cause of death in Cali after mortality due to
five-year period 2011-2015, followed by cancer of stomach (ASR:
cardiovascular diseases (26.0%) and unintentional or intentional
14.4), lung (ASR: 14.4), colorectal (ASR: 10.2) and lymphomas
injuries (20.1%).
(ASR: 6.0). Breast cancer was the leading cause of death in females
In contrast to the number of deaths, standardized cancer mortality (ASR: 13.8), followed by cancer of stomach (ASR: 8.2), colorectal
rates for all combined locations per 100,000 person-years were (ASR: 7.5), lung (ASR: 7.3) and cervix (ASR: 6.5).

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Table 2. Cali, Colombia. Mortality rates standardized by age (World Population) per 100,000 person-year and the annual percentage
change (APC) by sex during the period 2006-2015
2006-2010 2011-2015 APC
Code
Site Male Female Male Female Male Female
n ASR n ASR n ASR n ASR APC 95% IC APC 95% IC ICD 10
Mouth and oropharynx 90 1.9 82 1.2 115 2.0 104 1.3 -2.7* (-3.5 ; -1.9) 0.0 (-1.2 ; 1.2) C00-14
Oesophagus 91 1.9 54 0.8 95 1.7 52 0.7 -3.5* (-4.4 ; -2.5) -3.9* (-5.1 ; -2.7) C15
Stomach 801 16.6 607 9.0 807 14.4 659 8.2 -2.3* (-2.7 ; -2.0) -2.5* (-2.9 ; -2.1) C16
Colon and rectum 421 8.6 483 7.1 570 10.2 607 7.5 2.0* (1.4 ; 2.7) 0.4 (-0.2 ; 1.1) C18-21
Liver 305 6.4 311 4.7 317 5.7 372 4.5 -0.2 (-0.8 ; 0.5) -1.5* (-2.1 ; -0.8) C22
Pancreas 180 3.8 235 3.5 252 4.5 300 3.7 -0.6 (-1.3 ; 0.2) -1.2* (-2 ; -0.5) C25
Lung 714 14.8 531 8.0 799 14.4 602 7.3 -1.8* (-2.2 ; -1.4) -0.8* (-1.3 ; -0.3) C33-34
Skin melanoma 105 2.1 102 1.4 152 2.7 126 1.6 2.2* (1.2 ; 3.2) 1.2 (-0.1 ; 2.5) C43-44
Breast 8 0.2 904 14.1 7 0.1 1,055 13.8 0.1 (-0.4 ; 0.6) C50
Cervix uteri 471 7.4 487 6.5 -3.9* (-4.3 ; -3.5) C53
Corpus uteri 115 1.7 138 1.9 -2.3* (-3.5 ; -1.1) C54-C55
Ovary 297 4.7 302 4.0 -0.6 (-1.5 ; 0.3) C56
Prostate 847 16.7 1,012 17.4 -0.1 (-0.5 ; 0.4) C61
Bladder 100 2.0 58 0.8 113 2.0 75 0.9 -1.2* (-2.4 ; -0.1) -2.5* (-3.9 ; -1.1) C67
Lymphoma 256 5.3 237 3.8 330 6.0 290 3.7 -0.8* (-1.5 ; 0.0) -1.1* (-1.9 ; -0.3) C81-C90,C96
Leukaemia 259 5.1 286 4.6 270 4.6 246 3.5 -0.6 (-1.2 ; 0.0) -0.6 (-1.5 ; 0.3) C91-95
Other sites 1,003 20.6 1,159 17.8 1,191 2.1 1,316 1.7 -0.7* (-1.1 ; -0.3) -1.2* (-1.6 ; -0.9) **
All sites 5,180 10.6 5,932 90.7 6,030 10.7 6,731 85.9 -0.9* (-1.1 ; -0.6) -1.3* (-1.4 ; -1.1) C00-C97
**C17, C23, C24, C26-C32, C37-C41, C45-C49, C51, C52,C57-C60, C62-C66, C68-C80, C97
Number of cases (n); Mortality rate standardized by age (ASR).
APC: Annual Percent Change. APC is calculated for the period 1984-2015.
* The APC is significantly different from zero (p <0.05).

3. Changes in cancer morbidity and mortality Trend in cancer mortality rates (1984-2015)
Tables 1 and  2 show the APC that represents the average percentage Mortality from cancer shows a favorable trend. There was only an
of annual increase or decrease in cancer incidence and mortality rates increase in mortality rate from melanoma and colorectal cancer
during the periods 1962-2012 and 1984-2015, respectively. In describing in men. In the rest of the neoplasms, there was evidence of a
the change, three well-defined patterns were detected: increased or decrease in mortality rates for ten of the 17 main body locations.
decreased when the APC was significantly different from zero (two- The decrease was observed in both males and females with cancer
tailed values ​​p <0.05); otherwise the term stable or flat was used. of the esophagus, stomach, lung, urinary bladder, lymphomas and
multiple myeloma; only in males with cancer of the oral cavity and
The incidence rates for all cancer body sites increased in male an
pharynx; and only in females with cancer of liver, pancreas, cervix
annual average of 0.6% (95% CI: 0.4 - 0.8) and remained stable in
females. In contrast, mortality for all cancer body sites has been and uterine body.
significantly decreasing at an annual average of 0.9% in male; (95%
There were no changes in leukemia mortality in the entire
CI: -1.1; -0.6); and 1.3% in females, (95% CI: -1.4, -1.1).
population of Cali. Mortality rates for liver, pancreas, and prostate
Trend in cancer incidence rates (1962-2012) cancer remained stable in males; and females, there were no
The incidence of cancer decreased in both males and females in changes in mortality rates for breast, colorectal, ovarian and
the following sites: oral cavity and pharynx, esophagus, stomach, melanoma cancer.
larynx, urinary bladder and leukemia of unspecified type. The
decrease was only observed in male with pancreatic cancer and 4. Five-year net survival
with Hodgkin’s disease; and in females with cervical cancer. For the analysis, a total of 38,671 patients diagnosed with cancer
were included through 1995-2009. The distribution of the most
In contrast, increased incidence rates of colorectal cancer, frequent malignancies corresponded to breast (17.7%), prostate
melanoma, non-Hodgkin’s lymphoma and lymphoid leukemia (17.3%), stomach (13.1%) and colorectal cancer (9.4%), while a
were found in both males and females; breast and thyroid cancer smaller number of records were reported for liver cancer (2.2%),
increased in females only; and liver, prostate and testicular cancer
melanoma (1.8%), multiple myeloma (1.5%) and Hodgkin’s
in males only.
lymphoma (1.0%). The median age at diagnosis for the period
In females, there was no change in the risk of morbidity due considered was 64 years. There has been an increase in the
to cancer of the liver, pancreas, lung, uterine body, ovary and number of patients diagnosed for the last study period 2005-2009.
Hodgkin’s lymphoma and in males the incidence of thyroid cancer The trend of net survival for certain types of cancer by sex and
and myeloid leukemia remained stable. diagnosis period 1995-2009 is shown in Figure 1.

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Figure 2  shows the 5-year net survival standardized by age for Childhood cancer
three quinquennial periods: 1995-1999, 2000-2004 and 2005- VIGICANCER registered 1,428 children (<15 years of age) and
2009. When compared with previous periods, patients diagnosed adolescents (15 to 18.9 years of age) between 2010 and 2016.
with cancer in the most recent period (2005-2009) marked Ninety-six percent (n: 1,379) contributed to the follow-up (673
improvements in net survival of 5 years were observed for most hemato-lymphoid tumors y 706 solid tumors). Children 5-year
cancer sites. The proportions of increased cancer survival in overall survival (OS) was 52.0% (95% CI: 48.7, 55.3) and 44.0%
females could be explained in part by common types of cancer (95% CI: 35.4, 52.2) in adolescents.
in females (e.g. thyroid, breast, and cervical cancers) that have a
relatively good prognosis. When examined by year of diagnosis Table 3  shows OS by the International Childhood Cancer
and localization of cancer, in general terms it was evident that in Classification 3rd version21  cancer group. Group I was the most
the last period which includes the years 2005-2009 there was an frequent both in children (39.7%) and adolescents (30.3%).
increase in survival for most of the cancer locations except for Within this group 79.1% were acute lymphoblastic leukemia
stomach cancer and colorectal cancer. (ALL). Among group II, 38.4% were Hodgkin disease, 38.3% non-
Hodgkin lymphoma (without Burkitt) and 23.3% Burkitt. From
In the case of liver cancer, age standardization was not carried all groups, 17.2% were central nervous system tumors (group III);
out, because some of the age-specific 5-year net survival estimates being the most frequent (26.5%) in the <1 year of age group.
necessary to carry out standardization were not available (very low
survival, first year of follow-up, about 90% of patients with liver Infancy and early childhood malignant solid tumors frequency
cancer died). was 2.3% for neuroblastoma (and other group IV tumors), 4.2%
for retinoblastoma (group V), 3.9% for Wilms tumor (and other
On the other hand, the highest estimates of net survival for the groups VI tumors), and 1.3% hepatoblastoma (group VII).
period 2005-2009 were seen for thyroid cancer (89.3%), prostate
(83.2%), breast (74.4%) and melanoma (65.8%). In the case of Malignant bone tumors (group VIII) were more frequent
hematolymphoid neoplasms, survival was better in patients with in adolescents (14.9%) than in children (5.6%), with 58.9%
Hodgkin lymphoma (64.4%) than in non-Hodgkin lymphoma osteosarcomas and 32.7% Ewing sarcoma. Group IX (soft tissue
(43.3%). In leukemia and multiple myeloma survival was lower, with sarcomas) was similar in children and adolescents (5.0% vs. 5.9%).
estimates for the 2005-2009 period of 28.1% and 22.8% respectively. Germ cell tumors (group X) showed an overall frequency of 5.2%;

1995-1999 2000-2004 2005-2009

Thyroids 68.9 (56.7 ; 81.2) 67.8 (56.6 ; 79) 90.8 (81.3 ; 98.4)

Prostate 68.1 (64.1 ; 72.1) 81.1 (78.3 ; 84) 83.2 (80.7 ; 85.8)

Hodgkin´s Lymphoma 60.7 (48.2 ; 73.2) 66.3 (55.5 ; 77.1) 61.9 (50.6 ; 73.2)

Melanoma 48.8 (34.3 ; 63.3) 55.7 (44.7 ; 66.7) 61.9 (51.0 ; 72.8)

Non-Hodgkin´s Lymphoma 22.8 (16.6 ; 29.1) 34.4 (27.5 ; 41.2) 40.3 (33.2 ; 47.4)

Colorectal 29.5 (23.2 ; 35.8) 40.7 (35.2 ; 46.2) 39.2 (34.0 ; 44.3)

Multiple myeloma 18.8 (9.4 ; 28.1) 23.0 (11.3 ; 34.7) 23.8 (15.9 ; 31.6)

Leukaemia* 11.1 (5.9 ; 16.4) 20.9 (13.6 ; 28.2) 20.5 (14.2 ; 26.7)

Stomach 16.8 (13.6 ; 20.1) 17.6 (14.4 ; 20.8) 16.8 (13.8 ; 19.7)

Lung 7.7 (5.1 ; 10.3) 7.4 (4.9 ; 9.9) 8.8 (6.3 ; 11.3)

0 10 20 30 40 50 60 70 80 90 100
Five-year net survival (%)
Figure 1a. Cali, Colombia. Cali, Net standardized survival in male by age at 5 years for the most frequent locations by period of interest and sex, between 1995 and 2009.

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1995-1999 2000-2004 2005-2009

Thyroids 70.0 (62.9 ; 77.1) 88.7 (83.6 ; 93.7) 88.4 (84.3; 92.5)

Breast 65.7 (61.3 ; 70.1) 69.7 (66.4 ; 73.1) 74.4 (71.1; 77.6)

48.9 (36.0 ; 61.8) 66.7 (58.8 ; 74.7) 68.8 (59.6; 77.9)


Melanoma

Hodgkin´s Lymphoma 52.0 (36.3 ; 67.7) 64.3 (51.9 ; 76.7) 61.8 (48.6; 75.0)

Ovary 26.0 (19.8 ; 32.2) 32.3 (27.0 ; 37.7) 34.3 (29.1; 39.5)

Non-Hodgkin´s Lymphoma 23.2 (18.1 ; 28.4) 43.4 (37.2 ; 49.7) 46.2 (40.4; 51.9)

Colorectal 27.5 (22.7 ; 32.4) 43.4 (38.5 ; 48.3) 42.2 (37.8; 46.7)

Leukaemia* 17.0 (10.0 ; 24.1) 24.4 (17.2 ; 31.5) 34.5 (28.1; 41.0)

Cervix 50.5 (46.5 ; 54.5) 56.9 (53.2 ; 60.7) 57.7 (54.0; 61.5)

26.4 (16.4 ; 36.4) 17.5 (9.0 ; 25.9) 18.3 (10.5; 26.0)


Multiple myeloma
14.0 (10.7 ; 17.3) 18.2 (14.6 ; 21.7) 18.3 (15.0; 21.5)
Stomach
5.5 (3.0 ; 8.1) 11.2 (7.7 ; 14.7) 11.1 (7.8; 14.3)
Lung

0 10 20 30 40 50 60 70 80 90 100
Five-year net survival (%)
Figure 1b. Cali, Colombia. Cali, Net standardized survival in female by age at 5 years for the most frequent locations by period of interest and sex, between 1995 and 2009.

1995-1999 2000-2004 2005-2009


Thyroids 69.6 (63.2 ; 75.9) 86.3 (81.4 ; 91.1) 89.3 (85.4 ; 93.2)

Prostate 68.1 (64.1 ; 72.1) 81.1 (78.3 ; 84.0) 83.2 (80.7 ; 85.8)

Breast 65.7 (61.3 ; 70.1) 69.7 (66.4 ; 73.1) 74.4 (71.1 ; 77.6)

Melanoma 49.1 (38.7 ; 59.6) 62.3 (55.7 ; 68.8) 65.8 (58.8 ; 72.8)

Hodgkin´s Lymphoma 54.4 (44.5 ; 64.3) 65.5 (57.2 ; 73.8) 64.4 (56.2 ; 72.7)

Cervix 50.5 (46.5 ; 54.5) 56.9 (53.2 ; 60.7) 57.7 (54.0 ; 61.5)

Colorectal 28.9 (25.0 ; 32.9) 42.3 (38.6 ; 45.9) 40.6 (37.2 ; 43.9)

22.3 (18.4 ; 26.3) 39.1 (34.4 ; 43.8) 43.3 (38.8 ; 47.9)


Non-Hodgkin’s Lymphoma
26.0 (19.8 ; 32.2) 32.3 (27.0 ; 37.7) 34.3 (29.1 ; 39.5)
Ovary
12.3 (8.1 ; 16.5) 22.3 (17.1 ; 27.5) 28.1 (23.2 ; 32.9)
Leukaemia*

Multiple myeloma 20.6 (13.8 ; 27.3) 21.0 (13.6 ; 28.3) 22.8 (16.9 ; 28.8)

Stomach 15.7 (13.3 ; 18.1) 17.9 (15.5 ; 20.3) 17.4 (15.2 ; 19.6)

Lung 6.6 (4.7 ; 8.6) 9.0 (6.8 ; 11.1) 9.6 (7.6 ; 11.7)

Liver 4.1 (0.3 ; 8.0) 3.8 (0.7 ; 6.8) 5.0 (1.9 ; 8.0)

0 10 20 30 40 50 60 70 80 90 100
Five-year net survival (%)
Figure 2. Cali, Colombia. Five-year net survival standardized by age after diagnosis by period of interest, both sexes between 1995 and 2009.

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Table 3. Cali, Colombia, 2010-2015. Frequency of children and adolescent cancer cases and 5-year overall survival by ICCC-3 groups 21
Group ICCC-3 Children % Adolescents % OS 95% CI
I 453 39.7 87 30.3 48.3 43.3 53.2
II 112 9.8 34 11.9 74.1 65.5 81.0
III 209 18.3 36 12.6 40.2 32.4 47.7
IV 32 2.8 1 0.3 39.2 21.5 56.6
V 60 5.3 0 0.0 74.8 61.1 84.2
VI 56 4.9 0 0.0 62.5 47.3 74.5
VII 19 1.7 0 0.0 47.8 9.6 79.3
VIII 64 5.6 43 15.0 29.4 18.9 40.5
IX 57 5.0 17 5.9 32.3 19.9 45.3
X 39 3.4 27 9.4 61.2 45.2 73.8
XI 27 2.4 37 12.9 76.2 59.8 86.6
XII 13 1.1 5 1.7 56.3 20.9 80.9
Total 1,141 100.0 287 100.0 50.8 47.7 53.8
ICCC-3: International Classification of Childhood Cancer version 3
OS: 5-year overall survival. 95% CI: 95% Confidence interval

in children 3.4% and in adolescents 9.4%. Epithelial malignant for the last 55 years, which allows detailed analyses of the 50
tumors (group XI) had higher frequency in adolescents (12.9%) year-incidence (1962-2012), 30 year-mortality (1984-2015) and
than in children (2.4%). In this group, thyroid tumor was the most 15-year-survival (1995-2009) of cancer in the region.
frequent 51.5%. Non-specified cancers (group XII) were 1.3%.
Cali has experienced profound epidemiological and demographic
Discussion changes in the last half of the century. The population has
quadrupled and has aged, and the life expectancy at birth increased
The RPCC of Universidad del Valle provides unique information from 56.7 to 68.4 years13,15; Currently there are 33 persons 65 years
of the statistics of cancer in Cali, during the 2008-2015 period. old or over per 100 persons under 15 (Ageing index)13.
This information is necessary for health authorities to make
estimates of cancer risk for other regions of Colombia that are The offer of oncology care services in Cali corresponds to one
lacking cancer registries. These statistics complement previous sixth of the country’s installed capacity16 and attends around 9,000
reports5,22  and provides uninterrupted continuous monitoring new cases of cancer per year, half are permanent residents and the
Infection-related Cancer Screening-related Cancer Tobacco-related Cancer
Age-standardized rate (World population) x 100,000 person-year

A
80 80 80
60 60 60
40 40 40

20 20 20

10 10 10

5 5 5

1 1 1
1965 1975 1985 1995 2005 2015 1965 1975 1985 1995 2005 2015 1965 1975 1985 1995 2005 2015

Stomach Prostate Lung


Cervix Uteri Breast Oral Cavity
Colorectal Pancreas

B
80 80 80
60 60 60
40 40 40

20 20 20

10 10 10

5 5 5

1 1 1
1965 1975 1985 1995 2005 2015 1965 1975 1985 1995 2005 2015 1965 1975 1985 1995 2005 2015

Stomach Prostate Lung


Cervix Uteri Breast Oral Cavity
Colorectal Pancreas

Figure 3. Cali, Colombia. Trend in cancer rates


Calendar in the last 55 years
Years
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rest are patients from the south-west, a region that represents 20% that estimates of gastric cancer survival in Ecuador and Cuba may
of the Colombian population13. Eighty five percent of the oncology be overestimated24,25.
services in Cali are private16, the care is not comprehensive and
there are several barriers to accessing quality oncological care Despite the continuous decline in the incidence and mortality of
services. Government measures aimed at stabilizing the health infection-related cancers, rates remain high and the number of
system have been unsuccessful and there has been evidence of cases continues to increase due to aging and population growth30.
discriminatory behavior and risk selection of the oncological It is very likely that this downward trend will continue, even
patients by the health care provider entities responsible for without additional interventions, in the years to come; however,
managing the risks related to the disease23. Therefore, the clinical under natural conditions, it will likely take many decades, if not
outcomes remain unfavorable primarily because patients present centuries, before the incidence and mortality rates reach the
late with in advanced stages of the disease and, thus, survival is low values ​​currently observed in the United States and Europe. It is
for most types of cancer compared to that observed in Europe and a priority to implement additional measures to accelerate the
the United States24,25. decline, improve survival and achieve control30.
Coinciding with demographic changes there are significant The perspectives for the control of gastric cancer are uncertain
variations in trends, patterns and differences in incidence rates and because therapeutic advances are insufficient, the pre-clinical
cancer mortality. The increase or decrease in the risk of morbidity results of efforts to develop vaccines against H. pylori have been
and mortality due to this group of diseases is determined by
disappointing31; and the early detection of gastric cancer in
different factors. So far, some are recognized and most are still to
Latin America has shown unreliable results32,33  and low cost-
be identified. These changes may be the result of variations in the
effectiveness34. During the first stages of tumor growth, cancer
exposure of the population to different risk factors, better access
is clinically silent. Therefore, an alternative to control, is the
to health services and improvement in diagnostic and treatment
techniques26,27. implementation of primary prevention programs which would
help eradicate H. pylori infection by reducing the risk of developing
Although several threats persist, the available information shows gastric cancer in people without precursor lesions30,34,35. Due to
evidence of advances in the control of some types of cancer in Cali. the above, it is necessary to develop 1) monotherapies to facilitate
Overall cancer mortality decreased significantly in both males adherence to antibiotic treatment and 2) accurate non-invasive
and females with an annual change rate of 1% during the period tests to identify premalignant gastric lesions and thus serve as a risk
1984-2015 ((APC: -0.9, 95% CI: -1.1; -0.6) and (APC: -1.3, 95% CI: stratification tool of patients. The simultaneous detection of serum
-1.4; -1.1)). The magnitude of the decrease was greater in patients pepsinogens and antibodies against  H. pylori  has achieved this
with cancer related to tobacco consumption, infectious agents goal in Japan35,36. This strategy has not been adequately validated
and hematolymphoid neoplasms where important therapeutic in Latin America and continues to be an option that requires
advances have been made (Fig. 3). exploration with a well-founded project of implementation.
Cancer related to infectious agents The picture is different and more favorable for females with cervix
The incidence and mortality rates for stomach and cervix uteri uteri cancer (CUC). Mortality rates in Cali are close to the PDPCC
cancer have decreased significantly over the last 55 years (Fig. goal4, but they are still three times higher compared to the United
3). The descent is monotonic, continuous and began before States and Europe; where the risk of cervix uteri cancer is half
knowing the prominent role in the processes of carcinogenesis of that observed in Cali. The incidence and mortality rates have
of Helicobacter pylori28 and the Human Papilloma Virus (HPV)29.
declined for many reasons, including declining fertility rates,
These changes are not related to specific interventions against
improved socio-economic conditions and the establishment of a
these infectious agents, they are the result of progress in the
citywide program to prevent cervix uteri cancer via a widespread
development and improvement of sanitary conditions. Economic
use of pap smear29,37.
development determined changes in lifestyles and modifications of
the known risk factors for gastric cancer. Refrigeration facilitates
the consumption of fresh foods and limits the use of chemical- The knowledge that certain genotypes of VPH infection are
based food preservation methods (salting, desiccation, smoking, necessary to cause cervix uteri cancer has created new strategies
and acidification). for its prevention in the current PDPCC. As of 2012, the national
guidelines for vaccination against VPH are established and coverage
In the 21st century, gastric cancer still represents a great social
of 80% has been achieved, which unfortunately is now below 10%
burden in Cali and Colombia because it causes the highest number
because of a mismanaged episode of massive psychogenic reaction
of deaths from cancer3,5,22. The disease is fatal when discovered
clinically because the diagnosis is usually made in the advanced in Carmen de Bolívar, a Colombian rural region. This reaction
stages. From 1995 to 2009, the 5-year net survival of patients with was supposedly associated with the VPH vaccine38. To increase
gastric cancer in Cali was less than 20%, with a healing fraction of the accuracy of cervix uteri screening, the Ministry of Health of
15% and an average survival time of 6 months for uncured cases22; Colombia incorporated HPV testing in cervical cancer screening
similar results were observed in Chile and Costa Rica. But in other programs. It is expected to achieve coverage of 80% of the target
Latin American countries with equal or lesser development, the population in 20214. These measures are essential to accelerate the
control of this disease because the 5-year net survival of females
survival estimates were around 30%, which are comparable to with cervix uteri cancer in Cali was 57%, 10% points below that
those observed in the United States and Europe. It is also possible observed in affluent countries24,25.

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Cancer related opportunity screening activities the 21st century. The incidence rates of lung cancer for both sexes
Prostate and breast cancer are the leading cause of cancer-related in Cali reflect the end of a tobacco-related epidemic that began in
morbidity in males and females in Cali, respectively5. In Colombia the 1970s and was interrupted around the 1980s5,42,43. Since then,
there are no organized screening programs for either cancer there has been a significant decrease in tobacco-related cancer
and cancer control is based on specific opportunistic screening incidence and mortality: oral cavity and pharynx, esophagus,
activities. Mammography, digital rectal examination and PSA pancreas, lung and urinary bladder. The decrease was more
allowed us to detect cases of disease that were previously unknown consistent in the oral cavity and lung cancer in both males and
and contributed to increasing the incidence rates before the first females.
quinquennium of the 21st century and since then, it has begun
to decline. Most, but not all, of the increase may be due to earlier Net survival estimates
detection of the disease. Once the use of screening tests had been Surveillance of cancer survival is important for health
established the rates tended to stabilize as long as other factors organizations, civil society and research agencies because it serves
causing the disease had not changed. to formulate strategies and prioritize cancer control measures, and
to evaluate effectiveness, as well as the cost effectiveness of these
These changes were more evident in the population subject to strategies 1.
screening, the group of 50-69 years of age, where there was also
a turning point in the trend of incidence. Similar changes were At the beginning of the 21st century, we began to monitor trends
documented in Costa Rica and Ecuador at the end of the first in cancer survival in Cali. The relative survival (without age-
decade of the 21st century and were observed in Europe and the adjustment) was estimated for 16,064 patients diagnosed with
United States 20 years earlier. prostate, breast, colorectal, cervical, stomach and lung cancer
through 1995-200422. The present study, covers 38,671 patients
Mortality from prostate cancer has decreased consistently since diagnosed with invasive primary cancer in 14 body locations
1984 with an average annual percentage decrease of 2%; the decline representing around 71.8% of the global cancer burden in Cali
occurred earlier than expected. This could not be attributed (15-year period 1995-2009). Furthermore, the accuracy of the
exclusively to the screening activities (Fig. 3). An influential and previous estimates was improved through the implementation of
perhaps determining factor is the evolution of treatments with the new unbiased Pohar-Perme estimator44-46.
curative intent; it is likely that the use of PSA and digital rectal
examination have contributed to maintaining and consolidating Coinciding with the implementation of the new health system in
this trend39. However, mortality from breast cancer remained the 1990s, survival improved for most of the neoplasms in the first
stable during the study period (Fig. 3). five-year period of the 21st century compared to the 1995-1999
period. This trend stagnated in the five-year period 2005-2009.
The United States and Europe have made great advances in the The 5-year net survival was like that found in Argentina, Chile,
control of prostate and breast cancer. Despite the high incidence Ecuador and Costa Rica and very low compared to that observed
rates (ASR: 119.8 and ASR: 124.9, respectively); the 5-year net in developed countries24.
survival is around 98.9% and 89.7%; and mortality rates around
(ASR: 20.1, ASR: 21.2), respectively11,24. In Cali, 5-year net survival Certification of cancer mortality
for the same neoplasms was 83.2% and 74.4%; and the mortality Information on cancer mortality in liver, lung, brain and bones
rates around (ASR: 17.4 and ASR: 13.8), respectively. The should be interpreted with caution, because in these sites, the
existence of a gap of 15 percentage points in 5-year net survival in occurrence of metastasis is frequent. In the Cali cancer registry,
a population where incidence rates are half of those observed in we found evidence that the primary site of some of these cancers
affluent countries40, suggests that the diagnosis of cases is made at came from locations different than these organs. It is important
more advanced stages and / or that the tumors are more aggressive. to understand that 45% of liver cancer cases corresponded to
This will remain an area of future investigation. metastasis. It was also established that cancers of the bone (46%),
lung (15%) and CNS (10%) corresponded to metastasis. There
The incidence and mortality due to colorectal cancer continues were 2,447 new cases and 450 deaths from cancer. The coding of
to rise in males and females in Cali. The reasons are that the the body locations made by the vital statistics office and the cancer
screening activities are incipient, and the risk factors are difficult registry were compared. The concordance (Landis criteria47 for the
to control or are not clearly identified41; it is a priority to promote coding of cases of liver, bone and lung cancer were considerable
an organized screening program to reverse the current trend. (Kappa = 0.64, 0.67 and 0.79, respectively) and the highest was for
Until this intervention occurs, oncological care services must be malignant tumors of the CNS (Kappa = 0.90).
oriented to the early diagnosis of suspected cases.
Childhood cancer
Cancer related to tobacco use About 200,000 new childhood cancer cases per year are diagnosed
The trend in the incidence of lung cancer correlates with the historical in the world48, 84% occurring in low and middle-income
patterns of prevalence of cigarette smoking and there is sufficient countries49,50. Taken into account that cancer in children is not
evidence of a causal relationship between cigarette smoking and amenable to primary or secondary prevention, survival is the most
various types of cancer. The reduction in the number of cancer cases relevant metric to evaluate efforts aimed to control cancer burden
related to tobacco use in Cali, has been interpreted as a successful in this population group. Cali’s 5-year OS (51%) is 26% to 32%
example of cancer control. This was due to the implementation of lower to outcomes reported in more affluent countries (77% to
a very strong anti-smoking government campaign implemented in 83%)51,52. This implies that if in Colombia 1,500 to 1,600 children
the seventies and that has been consolidated in are treated for cancer per year then after 5 years 765 to 816 had
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Original article

Trends in cancer incidence and mortality over three decades in Quito - Ecuador
Tendencias en incidencia y mortalidad por cáncer durante tres decadas en Quito - Ecuador

Fabián Corral Cordero1, Patricia Cueva Ayala2,3, José Yépez Maldonado2,3, Wilmer Tarupi Montenegro4

1
Director Honorífico de los Registros de Cáncer del Ecuador – Fundador del Registro Nacional de Tumores
2
Registro Nacional de Tumores. Quito, Ecuador
3
Sociedad de Lucha contra el Cáncer. SOLCA. Quito, Ecuador
4
Facultad de Ciencias de la Salud, Universidad Tecnológica Equinoccial, Ecuador.

Corral CF, Cueva AP, Yepez MJ, Tarupi MW. Trends in cancer incidence and mortality over three decades in Quito - Ecuador. Colomb Med (Cali). 2018; 49(1): 35-41.
Doi: 10.25100/cm.v49i1.3785.

© 2018 Universidad del Valle. This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use,
distribution and reproduction in any medium, provided that the original author and the source are credited.

Article history: Abstract Resumen


Received: 01 March 2018 Introduction: The National Registry of Tumors has collected, Introducción: El Registro Nacional de Tumores ha recolectado,
Revised: 14 March 2018 processed, analyzed and regularly disseminated information on new procesado, analizado y divulgado regularmente la información de los
Accepted: 23 March 2018
cases of cancer diagnosed in the city of Quito, Ecuador over the last casos nuevos de cáncer diagnosticados en la ciudad de Quito, Ecuador
three decades. durante las últimas tres décadas.
Keywords:
Aim: This article analyzed the trend of cancer incidence and Objetivo: Analizar la tendencia de las tasas de incidencia y mortalidad
Incidence, mortality, cancer,
Ecuador, Latin America. mortality rates for the period 1985-2013. por cáncer durante el periodo 1985-2013.
Methods: Incidence and mortality rates standardized by age Métodos: Se estimaron las tasas de incidencia y mortalidad
were estimated by the direct method, using the world standard estandarizadas por edad a través del método directo, utilizando la
Palabras clave:
population. Analysis of the time trends, from selected locations, the población estándar mundial. Para el análisis de la tendencia de las
Incidencia, mortalidad,
cáncer, Ecuador, América joinpoint regression was used. tasas, de localizaciones seleccionadas, se utilizó la regresión joinpoint.
latina Results: A decrease in the incidence and mortality rates of cervical Resultados: Se documentó un descenso de las tasas de incidencia y
and stomach cancers were documented. There was an increase in mortalidad de los tipos de cáncer de cuello uterino y estómago. Existe
breast and colorectal cancer rates. The increase of the incidence incremento de las tasas de cánceres de mama y colon-recto. Es notorio
rate of thyroid cancer in women was notorious. Lung cancer also el crecimiento de la tasa de incidencia de cáncer de tiroides en mujeres.
increased in women while in men their values remained stable. El cáncer de pulmón se incrementó en las mujeres en tanto que en los
Conclusion: There are important variations in the evolution of varones sus valores se mantuvieron estables.
cancer in Quito; the information presented is an instrument for Conclusión: Se evidencian importantes variaciones en la evolución del
monitoring and evaluating the interventions that are developed in cáncer en Quito, la información presentada constituye un instrumento
the Country. para el seguimiento y evaluación de las intervenciones que se
desarrollen.

Corresponding author:
Directora del Registro Nacional de Tumores (RNT) – Sociedad de Lucha
contra el Cáncer. SOLCA Quito. Hospital Oncológico "Solón Espinosa
Ayala". Av. Eloy Alfaro 5394 y Los Pinos (QUITO). Phone: (593 2) 2419775.
Casilla 17-11-4965 C.C.I. Quito, Ecuador. E-mail: patycuev@hotmail.com.

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Corral CF/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)

Introduction extension of the tumor. Staging is performed for the eight most
frequent locations (cervix, breast, prostate, lung, colon-rectum,
The experience and consolidation of cancer population registries stomach, thyroid and lymphomas).
had their beginning in Hamburg, Germany in 19291. Its greatest
impulse comes from the Conference of Copenhagen which took A Case is considered to be any invasive or in situ neoplasia incident
place in 1946, and recommended the establishment of Cancer in the year, with or without histological verification which occurs
Registries Worldwide. In 1966 the International Association of in the population of inhabitants in the city of Quito.
Cancer Registries (IACR) was created as part of the International
Agency for Research on Cancer (IARC). This entity brings Tumors of an uncertain nature are not recorded. Since 2005, the
together, supports and sets the guidelines for the development and information has been collected and processed with the CIEO3
implementation of cancer registries in humans across the world. Classification. Tumors are recorded, not patients. The definition of
multiple tumors is established using the criteria defined by the IACR4.
In Latin America, the first cancer registry appeared in the 1950s2 in
Puerto Rico, and the second one in Cali, Colombia in 1962. This The information collected is validated through quality controls
encouraged the consolidation of the proposal in Ecuador. In 1984, checked between registrars and resolution of doubts is consulted
within the Cancer Fighting Society (SOLCA) Quito Nucleus, the with the doctors of the Registry and/or the occasional support
National Tumor Registry (NTR) was created3. Since its establishment of a pathologist. At the end of each year, the validation tool is
it has collected, processed, analyzed and regularly disseminated applied: IARCcrgTools 2.05, to establish the coherence of the main
information on new cases of cancer diagnosed in the city of Quito. variables that should be a population register.
The present study analyzes the trend of incidence and mortality of
The NTR has a 4th version computer system adjusted to the needs of
the main types of cancer in the city of Quito, from 1985 to 2013.
the implemented methodology. The data is presented according to
Materials and Methods the International Classification of Diseases ICD 10, and analyzed, by
sex, incidence and mortality rates standardized by age (using a world
The NTR registers all cases of cancer diagnosed in the city of Quito standard population and direct method). Analysis data included
using a methodology which is adopted internationally (IACR). The the following six periods: 1985-1988, 1989-1993, 1994-1998, 1999-
information is obtained through an active process, in which a group 2003, 2004-2008 and 2009-2013, in selected locations of the body.
of technicians goes to the pathology, hematology and cytology To study the trend of cancer incidence and mortality rates during
laboratories of all public and private health center establishments in the 1985-2013 period, the average annual percentage change (APC)
Quito. They review the clinical records to detect diagnosed cancer was estimated. In describing the change, the terms ‘’ increase ‘’ or ‘’
cases, and then read the clinical history or contact the treating doctor decrease ‘’ were used when the APC was significantly different from
to obtain more information about the patient. This methodology zero (p <0.05); otherwise, the term “stable” was used. Significance
guarantees that there are no duplication of cases. tests were performed using the Monte Carlo permutation technique.
All analysis were performed in the Joinpoint Regression Program
The cases that never underwent microscopic examination are version 4.5.0.1 of the Surveillance Research Program of the National
captured in the National Institute of Statistics and Census (INEC) Cancer Institute of the United States.
through the review of “Hospital discharges” and in the “Deaths by
cancer” occurred in the city of Quito, which constitute approximately Population
6% of new cases of cancer. A limitation of hospital discharges is not The city of Quito is the capital of Ecuador, it is the second largest
designed to adequately discriminate the multiple occasions that the and most populated city in the country. It is located at latitude
same patient enters and leaves a hospital or for cancer cases that 0 (0°13’23” South), west of the Andes Mountain Range, at 2,800
do not require hospitalization. Hospital discharges and deaths are meters above sea level. The extension of the city is 127 Km2 and its
compared with the registry database, with the aim of identifying new population for the year 2013, according to the Census Projections
cases or updating the vital status of previously registered patients. of the year 2010 was: 1,694,086 inhabitants5.

The variables that are collected are organized into three areas: The population of Ecuador in general and of Quito city in particular,
identification of the patient, description of the tumor and clinical has experienced important changes in demographic composition.

75+ 75+
70-74 70-74
65-69 65-69
60-64 60-64
55-59 55-59
50-54 50-54
45-49 45-49
40-44 40-44
35-39 35-39
30-34 30-34
25-29 25-29
20-24 20-24
15-19 15-19
10-14 10-14
5-9 5-9
0-4 0-4
14.0 12.0 10.0 8.0 6.0 4.0 2.0 0.0 2.0 4.0 6.0 8.0 10.0 12.0 14.0 14.0 12.0 10.0 8.0 6.0 4.0 2.0 0.0 2.0 4.0 6.0 8.0 10.0 12.0 14.0
Men (%) Women (%) Men (%) Women (%)

Figure 1. Quito Population structure by age and sex: 1985-2013.

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Corral CF/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)

Ecuador, over the last three decades, has developed censuses in interval, the values of the annual percentage change, and the
the years 1982, 1990, 2001 and 2010. Through its data it can be statistical significance are also presented.
seen that the broad base of its population pyramid decreases while
the older group increases. In Quito in 1985, 54% of its population In Figure 2 we can observe trends in the incidence and mortality
was under 25 years of age, while in 2013 this group was reduced of the main body locations. In men, a significant increase in the
to 44%. Those aged 65 and over accounted for 4.3% in 1985 and overall incidence rate of cancer was observed, with APC of 1.4%
in 2013, 6.5% (Fig. 1). The projection of population data of the (Fig. 2a). The stomach cancer incidence rate reached its highest
intercensal years are provided by the INEC. point in the first two periods, although it was later overtaken
by prostate cancer. Also, in women, the cancer global incidence
The age variation and the increase in life expectancy (75 years rate increased significantly with an APC of 1% (Fig. 2b). In the
old for females, 70 years old for males) is closely linked to the first two periods, the most frequent cancer was the cervix, and in
frequency of presentation and temporary tendency of cancer. the following periods, breast cancer presented the highest rate.
In the last two periods, thyroid cancer appears in second place,
Results surpassing cervical cancer.

Table 1 shows the cancer standardized incidence rates per 100,000 In men, the cancer that caused the most deaths until the period
inhabitants according to sex, main body locations and the six time of 1994-1998 was stomach cancer. In the last three quinquennial
periods studied. The trends of the incidence and its confidence periods, the highest mortality rate was that of prostate cancer. At
Table 1. Quito, Ecuador. Incidence. Standardized rates by age for locations selected by sex. 1985-2013.
Trend of the incidence rate
1985-1988 1989-1993 1994-1998 1999-2003 2004-2008 2009-2013
Location ♂ ♀
♂ ♀ ♂ ♀ ♂ ♀ ♂ ♀ ♂ ♀ ♂ ♀ APC 95% IC APC 95% IC
Lip, oral cavity, pharynx 2.0 1.6 1.8 1.1 2.4 1.7 1.7 1.3 1.9 2.0 2.1 1.6 0.0 (-1.2; 1.3) 0.9 (-1.4; 3.2)
Esophagus 3.4 0.6 3.0 1.2 2.4 0.6 2.0 0.8 2.4 0.6 1.4 0.7 -3.1* (-4.6; -1.5) ~
Stomach 28.5 21.7 32.7 20.0 24.5 16.9 22.2 13.2 22.9 14.9 20.3 14.5 -1.7 (-5.3; 2.1) -1.6* (-2.7; -0.5)
rectal colon 7.3 8.2 7.4 9.0 8.7 8.1 8.9 8.7 11.3 10.2 13.2 11.9 2.5* (1.7; 3.3) 1.4* (0.6; 2.2)
Pancreas 4.4 3.6 3.7 4.2 3.8 3.5 3.2 3.1 2.8 3.6 3.2 3.9 -1.3* (-2.3; -0.3) 0.2 (-1.2; 1.5)
Larynx 2.0 0.2 1.3 0.2 1.5 0.1 1.3 0.1 1.5 0.2 1.6 0.2 -0.1 (-1.9; 1.7) ~
Bronchi Lung 7.9 3.3 10.1 3.7 8.3 4.8 8.4 4.4 8.0 5.8 8.0 6.4 -0.5 (-1.3; 0.4) 2.8* (1.7; 3.9)
Cervix - 31.0 - 32.6 - 24.8 - 19.5 - 18.6 - 18.6 - - -2.6* (-3.2; -2.0)
Uterine body - 4.8 - 5.3 - 4.5 - 4.4 - 4.4 - 5.6 - - 0.3 (-0.6; 1.3)
Breast - 25.4 - 26.6 - 28.4 - 31.4 - 36.8 - 38.8 - - 1.9* (1.4; 2.3)
Ovary - 5.7 - 6.2 - 7.5 - 6.5 - 7.8 - 7.5 - - 1.2* (0.4; 2.0)
Prostate 22.7 - 23.1 - 31.7 - 43.5 - 53.5 - 62.9 - 3.8* (2.2; 5.3) - -
Testicle 2.6 - 4.0 - 3.3 - 4.2 - 5.2 - 5.7 - 3.0* (2.0; 4.1) - -
Bladder 4.3 2.0 5.9 1.4 5.0 1.3 5.3 1.5 5.1 2.0 6.1 2.2 0.8 (-0.3; 1.9) 1.4 (-0.2; 3.0)
Thyroid 3.1 6.3 2.1 7.6 2.2 8.7 2.4 10.5 3.9 19.6 6.6 35.0 3.6 (-0.6; 8.1) 8.5* (5.6; 11.5)
Lymphoma 8.9 7.2 8.8 7.5 11.4 8.4 10.5 9.1 12.6 9.9 16.1 13.1 2.2* (1.4; 3.1) 1.7 (-1.9; 5.3)
Leukemia 7.1 5.5 6.7 5.2 8.4 7.2 7.7 6.2 7.7 6.6 8.6 7.0 0.8 (-0.1; 1.8) 1.1* (0.2: 2.1)
Melanoma 2.3 3.3 3.5 3.6 2.2 3.0 2.5 3.0 3.7 3.8 4.1 3.8 1.8* (0.2; 3.4) 1.2 (-0.3; 2.7)
All - no melanoma skin 142.3 185.9 146.8 190.1 1476 1773 158.5 167.2 182.1 201.2 200.8 207.9 1.4* (0.9; 2.0) 1.0* (0.5; 1.5)
Rates x 100,000
APC: Annual percentage change. *The APC is significantly different from zero (p <0.05)
~ It is not possible to calculate

Table 2. Quito, Ecuador. Mortality Rates Standardized by age for selected locations by gender 1985 - 2013.
Trend of mortality rate
1985-1988 1989-1993 1994-1998 1999-2003 2004-2008 2009-2013
Localization ♂ ♀
♂ ♀ ♂ ♀ ♂ ♀ ♂ ♀ ♂ ♀ ♂ ♀ APC 95% IC APC 95% IC
Lip, oral cavity, pharynx 0.8 0.5 0.8 0.3 0.8 1.0 1.0 0.8 1.0 0.7 1.3 0.8 2.4* (0.1; 4.7) ~
Esophagus 2.6 0.3 2.0 0.6 1.8 0.4 1.7 0.4 1.4 0.5 1.3 0.6 -2.3* (-3.8; -0.7) ~
Stomach 16.7 13.8 18.4 11.5 16.2 11.6 15.8 10.2 15.9 10.6 15.2 10.0 -0.5* (-0.9; -0.1) -0.9* (-1.7; -0.1)
rectal colon 3.3 2.9 3.5 3.8 4.4 4.9 5.5 4.7 5.9 5.5 7.0 6.4 3.5* (2.4; 4.6) 4.2* (0.3; 8.2)
Pancreas 2.7 2.6 2.8 3.3 3.1 2.7 2.5 2.5 2.5 3.3 2.6 3.1 -0.1 (-1.3; 1.1) 0.6 (-0.6; 1.9)
Larynx 1.0 0.0 0.4 0.2 0.4 0.1 0.7 0.0 1.0 0.0 0.9 0.1 ~ ~
Bronchi Lung 5.2 2.8 7.2 2.9 6.7 3.5 7.0 3.6 6.7 4.6 6.2 4.9 0.4 (-0.6; 1.4) 2.7* (1.6; 3.7)
Cervix - 8.6 - 10.7 - 10.5 - 10.2 - 10.3 - 8.2 - - 0.1 (-5.3; 5.8)
Uterine body - 0.4 - 1.2 - 1.5 - 1.4 - 1.6 - 1.6 - - ~
Breast - 6.5 - 7.8 - 9.6 - 12.1 - 12.4 - 12.3 - - 2.7* (1.5; 4.0)
Ovary - 2.2 - 2.4 - 4.1 - 3.5 - 4.0 - 4.2 - - 2.7* (1.3; 4.0)
Prostate 9.3 - 10.8 - 12.7 - 16.3 - 18.7 - 1.9-1.9 - 3.7* (3.0; 4.4) - -
Testicle 0.6 - 0.7 - 0.6 - 8.0 - 0.9 - 0.7 - 1.1 (-1.4; 3.8) - -
Bladder 1.0 0.5 1.9 0.6 1.8 0.6 2.7 1.0 2.4 0.7 2.6 1.2 5.7* (1.0; 10.5) 2.9* (0.1; 5.7)
Thyroid 1.1 1.4 0.9 1.7 0.9 1.2 8.0 1.3 0.9 2.0 0.9 2.2 0.3 (-2.2; 2.8) 1.8 (-1.5; 5.2)
Lymphoma 2.0 1.8 3.3 2.2 5.2 3.7 5.4 4.6 6.9 5.2 7.9 5.9 5.4* (3.9; 6.9) 5.8* (2.7; 9.0)
Leukemia 3.3 2.3 3.0 2.0 4.7 4.3 5.2 3.6 5.3 4.1 5.2 3.9 2.6* (1.5; 3.8) 2.2 (-3.5; 8.1)
Melanoma 0.3 0.7 0.8 0.6 1.0 0.9 1.1 0.9 1.4 1.4 2.0 1.5 ~ 4.7* (2.0; 7.5)
All - no melanoma skin 68.4 69.0 73.0 75.1 78.9 83.6 88.1 83.1 93.7 90.3 101.2 89.4 1.7* (1.4; 2.0) 1.2* (0.8; 1.5)
Rates x 100,000
APC: Annual percentage change.. * The APC is significantly different from zero (p <0.05)
~ It is not possible to calculate

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Corral CF/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)

A B
Stomach Colorectal Stomach Colorectal
100 100
APC= Incidence : -1.7 ( -5,3; 2,1) APC= Incidence : 2.5* (1,7; 3,3) APC= Incidence : -1.6* ( -2,7; -0,5) APC= Incidence : 1.4* (0,6; 2,2)
Mortality : -0.5 (-0,9; -0,1) Mortality : 3.5* (2,4; 4,5) Mortality : -0.9* (-1,7; -0,1) Mortality : 4.2* (0,3; 8,2)

10 10

1 1
85-88 89-93 94-98 99-03 04-08 09-13 85-88 89-93 94-98 99-03 04-08 09-13 85-88 89-93 94-98 99-03 04-08 09-13 85-88 89-93 94-98 99-03 04-08 09-13

Incidence Mortality Incidence Mortality

Lip, Oral Cavity, Pharynx Bronchi Lung Lip, Oral Cavity, Pharynx Bronchi Lung

100 10
APC= Incidence : 0.0 (-1,2; 1,3) APC= Incidence : -0.5 (-1,3; 0,4) APC= Incidence : 0.9 (-1,4; 3,2)
Mortality : 2.4* (0,1; 4,7) Mortality : 0.4 (-0,6; 1,4) Mortality : ~

10

1
APC= Incidence : 2.8* (1,7; 3,9)
Mortality : 2.7* (1,6; 3,7)
1

0.1 0,1
85-88 89-93 94-98 99-03 04-08 09-13 85-88 89-93 94-98 99-03 04-08 09-13 85-88 89-93 94-98 99-03 04-08 09-13 85-88 89-93 94-98 99-03 04-08 09-13

Incidence Mortality Incidence Mortality

Breast Cervix Uteri


Prostate Testicle 100
APC= Incidence : 1.9* (1,4; 2,3) APC= Incidence : -2.6* (-3,2; -2,0)
100 Mortality : 2.7* (1,5; 4,0) Mortality : 0.1 (-5,3; 5,8)
APC= Incidence : 3.0* (2,0; 4,1)
Mortality : 1.1 (-1,4; 3,8)

10
10
APC= Incidence : 3.8* (2,2; 5,3)
Mortality : 3.7* (3,0; 4,4)
1

0.1 1
85-88 89-93 94-98 99-03 04-08 09-13 85-88 89-93 94-98 99-03 04-08 09-13 85-88 89-93 94-98 99-03 04-08 09-13 85-88 89-93 94-98 99-03 04-08 09-13

Incidence Mortalidty Incidence Mortality

C
Thyroids Men Thyroids Women
All cancers - Men All cancers - Women
100
APC= Incidence : 3.6 (-0,6; 8,1) APC= Incidence : 8.5* (5,6; 11,5) 1000
APC= Incidence : -1.7 ( -5,3;2,1) APC= Incidence : 1.0* (0,5; 1,5)
Mortality : 0.3 (-2,2; 2,8) Mortality : 1.8 (-1,5; 5,2) Mortality : 1.2* (0,8; 1,5)
Mortality : -0.5 (-0,9;-0,1)

10 100

1 10

0.1 1
85-88 89-93 94-98 99-03 04-08 09-13 85-88 89-93 94-98 99-03 04-08 09-13
85-88 89-93 94-98 99-03 04-08 09-13 85-88 89-93 94-98 99-03 04-08 09-13
Incidence Mortality
Incidence Mortality

Calendar Year
Figura 2. Quito, Ecuador. Rates of cancer incidence. 1985–2013 (Location selected). 2a: Men. 2b. Women. 2c: thyroides and all cancer

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the national level, the situation was different in terms of mortality, Discussion
since stomach cancer until 2013 was the leading cause of death
among malignant tumors. In women residing in Quito, the The incidence rate in certain body locations is reflected by the
behavior of mortality from gastric cancer is similar to that of men demographic, social and economic change that is occurring
with two specificities: a) the rates had lower values and b) in the in Quito and Ecuadorian society. It is essential to highlight the
period of 1999-2003, breast cancer surpassed that of the stomach importance of the cancer active registry that has been kept by the
as the main cause of cancer deaths. RNT over the last three decades. This has allowed identifying the
trends of both incidence and mortality of the main types of cancer
In Figure 2 we can observe trends in the incidence and mortality in the city of Quito6.
of the main body locations.
While breast cancer is on the increase among women in Quito,
Incidence rates of gastric cancer decreased in women significantly cervical cancer on the other hand is decreasing. This behavior
with a APC of -1.6. In men, the overall decrease was not significant. indicates the important changes in the lifestyle that women
However, when applying joinpoint regression, an increase was have had, especially in the urban area and in the cities of greater
observed in the first phase and from the period 1994-1998 until economic development. The inclusion of women in the national
economy has led to an increase in the “estrogen window of risk”
2013, the decrease was significant. (APC -2.4, 95% CI: -3.8; -1.1).
due to late pregnancies, fewer pregnancies, reduced lactation
Mortality rates decreased significantly in men and women (-0.5
or caloric overload7. On the other hand, the improved access to
and -0.9, respectively).
health services8, a better educational level of women in the city9,
Colon-rectal cancer had a significant upward trend in both and campaigns of prevention, are changes that should have an
impact on the decrease in the incidence of cancer of the cervix.
APC, men (2.5) and women (1.4). The values were very similar
The same tendency occurs more slowly in other places within the
for both genders. Mortality rates, in men and women, increased
country due to sanitary, educational and life style changes.
significantly (3.5 and 4.2, respectively)
Thyroid cancer, which is much more frequent in women, is notable
In the 29 years of analysis, the incidence and mortality rates from
for its tendency to increase. Comparing the increase of incidence
lung cancer among men have remained stable. However, in women from 10 to 35 over the last ten years places this area among one of
the increase was significant with a APC of 2.8 in incidence and 2.7 the highest positions in the world10.
in mortality. There was a sustained and large increase in both the
incidence rate and the mortality rate of prostate cancer with an This increase is due to papillary cancer which represents 44% of
APC of 3.8 and 3.7 respectively. the cases (1985-1988) and 89% between the period 2009-2013.
Whereas in men, the increase of these rates was moderate and also
Breast cancer had an incidence and mortality rates that increased given in papillary cancer (from 40% to 84% in the same periods).
significantly (APC 1.9 and 2.7), however in the last three
quinquennial periods the mortality rates remained stable. One explanation for this phenomenon is over diagnosis established
through different researches in various countries throughout the
There was a significant downward trend in the incidence rates of world11. Increased medical surveillance and the introduction
cervical cancer (APC 2.6). The mortality rates, analyzed globally, of new diagnostic techniques, such as neck ultrasound (since
did not show a significant decrease. the 1980s) and, more recently, computed tomography (CT) and
magnetic resonance imaging (MRI), have made it possible to
The incidence rates for thyroid cancer have large differences in detect a large number of asymptomatic and non-lethal diseases
magnitude between Men and women which accentuated with the that exist in abundance in the thyroid gland of healthy people of
passing of time. Initially, a ratio of 1:2 was detected and in the final all ages. On the other hand, little is known about the aetiology of
years the ratio was 1:5. The incidence rates increased in both men thyroid cancer so far; exposure to ionizing radiation (especially
and women, especially in the last two quinquenial. In the case of during childhood) and a history of benign thyroid disease are
women, this increase was significant (APC 8.5). the only well-established risk factors for differentiated thyroid
carcinomas (the most common forms of thyroid cancer)12-14. Based
Mortality rates in both men and women remained low, with small on this data, IARC warns against the systematic detection of the
variations that were not significant. thyroid gland cancer and the study of small nodules, and suggests
careful monitoring for patients affected by low-risk tumors.
The incidence and mortality rates of lymphomas were slightly
higher in men. Among men, incidence rates increased over time Gastric cancer decreased in incidence and mortality in both men
significantly (APC 2.2). Mortality rates increase in both genders and women. Worldwide, Helicobacter pylori infection is recognized
(APC 5.4 men APC 5.8, women). as the primary cause of gastric cancer15. Several risk factors have
also been identified, such as socioeconomic level, high-salt and
The incidence rate of leukemia was higher among men. It also low-antioxidant diet, alcohol and, tobacco consumption16-18.
increased significantly among women (APC 1.1). On the other However, in Ecuador there are multiple geographical, physical,
hand, mortality had a significant tendency to rise among men biological, social, economic and cultural variables which could be
(APC 2.6). related to the occurrence and course of the disease. The equatorial

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Corral CF/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)

location, the ethnic diversity, multiculturalism, the phenotype Ecuador during the period 2000-2004 it was 13%, in 2005-2009
of miscegenation and the limited access to education and health it was 11% and in 2010-2014 it was 9%. In the specific case of the
services are issues that must be addressed in order to better RNT of Quito, the histological verification in men and women
understand the gastric cancer disease in our country. The decrease, increased from 71.0% to 87.0%, in the quinquennial periods 1986-
both in incidence and in mortality, is most probably linked to 1990 to 2006-2010.
better socioeconomic conditions, improvement of the quality
of food and its preservation19, rather than to the intervention of Finally, it is worth mentioning that during these three decades
health services in the early diagnosis. of monitoring, the RNT has provided accurate and relevant
information for the education of health professionals. It has
The significant increase in incidence and mortality of colorectal contributed to designing and establishing programs for the
cancer is probably a manifestation of changes in the lifestyles prevention and control of cancer. In addition, it has trained
of societies. It is known worldwide that its incidence is higher individuals in the implementation and development of other
in countries in economic transition, especially those that have cancer registries in the country that use the same standardized
adopted lifestyles typical of industrialized countries (diets with RNT methodology. Actually, there are registries in Quito,
a low intake of fruits and vegetables, greater consumption of Guayaquil, Manabí, Cuenca, Loja and Machala. The information
red or processed meat, physical inactivity, smoking and alcohol of the RNT has been included in the publication of the IACR
consumption)20. “Cancer Incidence in Five Continents”, (Volumes VI, VII, VIII, IX,
X and XI).
In men, the great increase in prostate cancer incidence rates is
associated with an improvement in early diagnosis, mainly due to Acknowledgements:
the use of prostate antigen. It would be expected that this very To Solón Espinosa, undisputed leader of the fight against cancer,
important increase is accompanied by a decrease in the mortality to Dr. Fabián Corral, founder of the RNT, to María Belén Morejón,
rate, however, as has been observed in other countries21, there was Mónica Galarza, Doris Chauca, Paulina Bedón and Silvia Jacho,
no impact on the decrease in mortality. for their patient and tenacious work in the RNT.

In women, the incidence and mortality rates of lung cancer have Conflict of interest:
increased significantly. But in men, little changes were observed The authors declare that there is no real or potential conflict of
in their rates. This behavior is probably due to the changes that interest regarding the possible publication of this work
occurred in the smoking behavior of both sexes. The application
of the WHO Framework Convention for the Control of Tobacco References
(FCTC) and its Protocol for the Elimination of Illicit Trade in
Ecuador, makes it possible to expand measures to avoid the risks 1. Parkin DM, Maclennan R, Muir CS, Skeet RG, Jensen
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2. Mirra AP. Registros de Cáncer en América Latina. Rev Brasileira
same year that protocol was ratified in Ecuador22.
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intermediary determinant of health inequities23, due to this registro Nacional de Tumores (RNT). Quito; 1984.
fact a reorganisation of the public care system Network and a
4. IARC. International Rules for multiple Primary Cancers ICD-O
Complementary Health Network24  was proposed through the
Third edition. Internal Report Nro. 200472. Lyon: IARC; 2004.
Integral Health Care Model in Families and Communities25.
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Original Article

Trends in cancer incidence, and mortality in Pasto, Colombia. 15 years experience


Tendencia de la incidencia y mortalidad por Cáncer en Pasto, Colombia. 15 años de experiencia

María Clara Yépez1, Daniel Marcelo Jurado1 , Luisa Mercedes Bravo1, Luis Eduardo Bravo2

1
Registro Poblacional de Cáncer del Municipio de Pasto, Grupo de investigación Salud Pública, Centro de Estudios en Salud (CESUN), Universidad de Nariño, Pasto, Colombia.
2
Departamento de Patología, Universidad del Valle, Cali, Colombia.

Yepez MC, Jurado DM, Bravo LM, Bravo LE. Trends in cancer incidence, mortality and survival in Pasto, Colombia. Colomb Med (Cali). 2018; 49(1): 42-54.
doi: 10.25100/cm.v49i1.3616.

© 2018 Universidad del Valle. This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use,
distribution and reproduction in any medium, provided that the original author and the source are credited.

Article history: Abstract Resumen

Received: 19 October 2017 Introduction: In Colombia it is necessary to continue producing Introducción: En Colombia es necesario que se continúe produciendo
Revised: 16 January 2018 quality and continuously updated information, on the magnitude información de calidad y actualizada sobre la magnitud del cáncer a
Accepted: 22 February 2018 of cancer, from cancer population registered data to contribute partir de datos de los registros poblacionales de cáncer para contribuir
to decision making, and implementation of strategies for health a la toma de decisiones e implementación de estrategias de promoción
Keywords: promotion, prevention and treatment of cancer, in order to reduce de la salud, prevención y tratamiento del cáncer con el objetivo de
Cancer, incidence, mortality, the impact on the population. disminuir el impacto en la población.
trends, disease prevention. Objective: To describe the incidence, mortality and cancer trends in Objetivo: Describir la incidencia, mortalidad y tendencia del cáncer en
Pasto-Colombia from 1998 to 2012. Pasto-Colombia durante 1998-2012.
Palabras clave: Methods: Observational descriptive study of morbi - mortality Métodos: Estudio observacional descriptivo de la morbi-mortalidad
Cáncer, incidencia, due to malignant tumors in Pasto. The collection, processing por tumores malignos en Pasto. La recolección, procesamiento y
mortalidad, tendencias,
and systematization of the data, was carried out according to sistematización de los datos se realizó de acuerdo a parámetros
Prevención de
Enfermedades. international standards for cancer population registries. The estandarizados internacionalmente para registros poblacionales de
incidence and mortality rates were calculated by period, sex, age and cáncer. Las tasas de incidencia y mortalidad se calcularon por periodo,
tumor location. sexo, edad y localización del tumor.
Results: for the period 1998-2012 there were 8,010 new cases of Resultados: En el período 1998-2012 se registraron 8,010 casos nuevos
cancer, of them, 57.7% occurred in women. There were 4,214 deaths de cáncer, de ellos, 57.7% se presentaron en mujeres. Se reportaron
reported, 52.0% in women. The incidence (p men= 0.7, p females= 4,214 muertes, 52.0% en mujeres. La incidencia (p hombres= 0.7;
0.3) and mortality (p men= 1.0, p females= 0.0) did not present p mujeres= 0.3) y mortalidad (p hombres= 1.0; p mujeres= 0.0) no
significant changes over 15 years of observation and the tumors that presentó cambios significativos durante 15 años de observación y los
cause greater morbi-mortality affect the stomach, cervix, breast and tumores que causan mayor morbi-mortalidad afectan al estómago,
prostate. cuello uterino, mama y próstata.
Conclusions: Cancer in general continues to be a serious health Conclusiones: El cáncer en general continúa siendo un importante
problem for the population of Pasto. problema de salud para la población de Pasto. El comportamiento
The global behavior of cancer incidence and mortality, identify global de la incidencia y la mortalidad por cáncer, evidencian la
the need to promote and strengthen promotion and prevention necesidad de fomentar y fortalecer programas de promoción y
programs, especially focused on tumors of the stomach, prostate, prevención, enfocados especialmente hacia los tumores de estómago,
breast and cervix that produce greater morbidity and mortality in próstata, mama y cuello uterino que producen mayor morbi-
the population mortalidad en la población.

Corresponding author:
María Clara Yépez Chamorro. Directora Registro Poblacional de Cáncer
del Municipio de Pasto. Universidad de Nariño, Ciudad Universitaria
Torobajo - Clle 18 Cr 50, Bloque Tecnológico CESUN, San Juan de Pasto –
Colombia, Tel y fax: 7312283, e-mail: cesun@udenar.edu.co.

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Yepez MC/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)

Introduction  malignant tumours in certain populations that correspond to


8.9% of the national population (Cali, Bucaramanga, Manizales,
In recent decades, cancer has become one of the leading Barranquilla and Pasto)6,7. For this period, Colombia estimated a
causes of mortality worldwide. According to the World Health total of 62,812 new cases of cancer per year, 29,734 cases in males
Organization (WHO), this disease represents 21% of total deaths and 33,084 cases in females were estimated for the country. In
due to non-communicable diseases, and it is the second cause of males, the highest incidence of tumours occurred in: prostate,
death after cardiovascular diseases (48%)1. Different agencies both stomach, colon and rectum. In females affect the: breast, cervix,
governmental and non-governmental organizations, have stressed uteri, colon and rectum. In the same period, there were 32,653
the importance of understanding the impact of this disease, cancer deaths, 16,081 deaths in men and 16,572 deaths in females.
not only in terms of mortality but also of morbidity (incidence, The main causes of cancer mortality in men were tumours of:
prevalence and burden) and have promoted the creation and stomach, prostate and lung; in females the tumours of: breast,
strengthening of epidemiological surveillance and information cervix uteri and stomach. According to this report, for the
systems of a regional and national nature, called Population- Department of Nariño, where is located Pasto, stomach cancer in
based Cancer Registries (PBCR)2. Thus, in 1966 the International both males and females produces the highest mortality rate8.
Association of Cancer Registries (IACR) was founded, whose main
objective is to promote the monitoring of cancer in populations The Cancer Registry of Pasto, processes information on cancer
through PBCR with internationally standardized methodological cases that occur in the rural and urban area of Pasto, Colombia,
guidelines that allow the production of scientific evidence with which according to the 2005 census has a population of 382,422
quality criteria such as: comparability, comprehensiveness, validity inhabitants, 47.8% males, 52.2% females. The population is spread
and timeliness in order to base public policies and interventions out 81.7% in the urban area, and 18.3% in the rural area. Previous
for the prevention and control of cancer, as well as to evaluate its studies conducted over 1998-2007 showed that the cancer which
effectiveness3,4. produces the highest morbi-mortality in males was the stomach,
and in females the cervix uteri.
According to estimations published by GLOBOCAN, an
epidemiological surveillance system derived from PBCR, cancer In order to observe the behaviour of the different types of tumours,
is not only a problem exclusively of high-income countries(HIC), the characterization of morbi-mortality due to cancer in Pasto was
low and middle-income countries (LMIC) allow more than half carried out over the period 1998-2012, and the analysis of the
of the annual cancer burden with 7 million new cases (56%) and trend of the incidence and mortality of the main types of tumours
4.8 millions of deaths (64%), although they are the least prepared over a period of fifteen years. This study was done to contribute to
to face this situation. Without planning and control interventions decision-making and the implementation of strategies to promote
in these populations, the burden of disease due to cancer will health, prevention and treatment of cancer that help to mitigate
increase by 70%. Therefore, cancer is considered a threat to human the impact of this disease in the region9,10.
and economic development in these countries. In Latin America
and the Caribbean it is estimated that each year there are around Materials and Methods
900,000 new cases, 542,000 deaths, and more than 2 million people
Design and population
living with cancer5.
A descriptive observational study of all the malignant tumours and
In Colombia, the National Cancer Institute (NCI) estimated that cancer deaths presented on residents of The Municipality of Pasto-
for the period 2007-2011 the morbi- mortality from cancer at Colombia during 1998-2012 was conducted. The city is located in
national and departmental level from the mortality information south western Colombia and by the middle of the study period
in combination with data produced by five PBCR that followed there were approximately 350,000 inhabitants (2005), of which
the methods of the IACR and that have produced information 74.7% with health care and 57.0% living in low socioeconomic
regarding the magnitude, distribution and tendency of the neighborhoods11,12 (Fig. 1).
n n
958 Males 85-+ Females 1,059
1,195 Total people Total people 1,567
80-84
182,889 199,533
1,992 75-79 2,613
2,858 70-74 3,939
3,775 65-69 4,687
4,904 60-64 5,893
6,187 55-59 7,206
7,441 50-54 9,161
9,284 45-49 11,176
11,461 40-44 13,618
13,270 35-39 15,519
12,956 30-34 15,581
15,722 25-29 17,095
18,472 20-24 19,063
18,451 15-19 18,708
18,978 10-14 18,890
18,136 5-9 18,046
16,849 0-4 16,712
5 4 3 2 1 0 0 1 2 3 4 5
Percentage
Figur 1. Average annual person-years by sex and age group. Colombia, Pasto 2005 Resource. General
Census -2005. Colombian National Administrative Department of Statistics (DANE).
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Ninety per cent of the tumours that were included were distributed between the category “cervix uteri” and “body of the
microscopically confirmed (histology, cytology, and bone marrow uterus” taking into account the proportion of deaths observed
aspiration); the rest, were identified using other methods valid by age, according to IACR guidelines3. 98.0% of the deaths were
for the IACR (imaging, exploratory surgery, endoscopy, clinical certified by medical personnel, the rest were certified by non-
and death certificate) in population-based studies. The percentage medical health personnel. The percentage of deaths with unknown
distribution of indices of data quality varies according to the age was 0.3%, and the percentage of deaths with unknown primary
primary site of the tumour and is shown in Table 1. site (C76-C80) was 5.0%. Incident and mortality cases do not
necessarily refer to the same person.
For mortality analysis all deaths recorded on the death
certificate with basic cause of death C00-C99 according to For each person with an incident tumour and cancer death recorded
ICD-10 (International Classification of Diseases 10th edition) in the period, information was collected on demographic (age, sex)
were included. Deaths coded as “non-specific uterus” (C55), and clinical conditions (date of incidence or death, primary site of
corresponding to 12% of deaths due to uterine cancer, were the tumour, cause of death). The date of incidence corresponds

Table 1. Indices of data quality. Males and females of Pasto, Colombia, 1998-2012
Males Females
Site ICD-10 code
n %MV %DCO %Others MI n % DCO %MV %Others MI
Oral cavity 39 84.6 7.7 7,7 0.4 45 6.7 77.8 15.6 0.3 C00-14
Oesophagus 73 86.3 12.3 1.4 1.0 36 16.7 77.8 5.6 0.9 C15
Stomach 804 80.7 12.6 6.7 0.7 495 17.2 75.2 7.7 0.8 C16
Small intestine 13 69.2 15.4 15.4 0.3 12 8.3 83.3 8.3 0.5 C17
Colon and rectum 177 84.2 6.2 9.6 0.5 242 8.7 80.6 10.7 0.6 C18-20
Anus 5 100 0.0 0.0 0.5 19 0.0 100.0 0.0 0.3 C21
Liver 82 47.6 25.6 26.8 1.4 92 38.0 37.0 25.0 1.4 C22
Gallbladder 57 45.6 14.0 40.4 0.4 154 16.2 59.1 24.7 0.6 C23-24
Pancreas 78 26.9 23.1 50.0 0.9 116 25.0 30.2 44.8 1.1 C25
Nose, sinuses etc. 7 100.0 0.0 0.0 0.7 5 20.0 60.0 20.0 1.0 C30-31
Larynx 34 85.3 8.8 5.9 0.6 2 0.0 100.0 0.0 0.0 C32
Lung 168 60.1 20.8 19.0 1.1 117 23.1 61.5 15.4 1.2 C33-34
Other thoracic organs 7 100 0.0 0.0 0.3 7 0.0 100.0 0.0 0.5 C37-38
Bone 19 94.7 5.3 0.0 0.6 21 9.5 81.0 9.5 0.9 C40-41
Melanoma of skin 56 98.2 0.0 1.8 0.2 108 0.0 99.1 0.9 0.2 C43
Other Skin 33 93.9 6.1 0.0 0.3 35 8.6 88.6 2.9 0.6 C44
Mesothelioma 6 100.0 0.0 0.0 1.0 4 0.0 100.0 0.0 0.0 C45
Kaposi sarcoma 9 100.0 0.0 0.0 0.0 1 0.0 100.0 0.0 - C46
Connective and soft tissue 66 95.5 0.0 4.5 0.3 41 0.0 97.6 2.4 0.4 C47,49
Breast 5 100 0.0 0.0 0.5 790 1.6 94.7 3.7 0.3 C50
Vulva 16 6.3 87.5 6.3 0.4 C51
Vagina 10 0.0 90.0 10.0 0.3 C52
Cervix uteri 733 4.8 91.8 3.4 0.4 C53
Corpus uteri 129 3.9 93.8 2.3 0.2 C54
Uterus unspecified 9 55.6 33.3 11.1 2.0 C55
Ovary 217 5.5 83.9 10.6 0.4 C56
Placenta 6 0.0 83.3 16.7 0.0 C58
Penis 36 91.7 2.8 5,6 0,3 C60
Prostate 626 82.3 8.3 9.4 0.3 C61
Testis 105 98.1 0.0 1.9 0.1 C62
Other male genital organs 3 100 0.0 0.0 0.0 C63
Kidney 45 71.1 8.9 20.0 0.2 41 7.3 85.4 7.3 0.2 C64
Renal Pelvis 1 100 0.0 0.0 0.0 2 0.0 100.0 0.0 0.0 C65
Bladder 92 88.0 6.5 5.4 0.3 52 5.8 82.7 11.5 0.5 C67
Other urinary organs 2 100 0.0 0.0 1.0 2 0.0 100.0 0.0 - C68
Eye 17 100 0.0 0.0 0.1 19 0.0 100.0 0.0 0.0 C69
Brain, nervous system 106 78.3 6.6 15.1 0.6 99 17.2 66.7 16.2 0.7 C70-72
Thyroid 60 91.7 5.0 3,3 0,2 302 1.7 95.7 2.6 0.1 C73
Adrenal gland 1 0.0 100 0.0 - 1 0.0 0.0 100 - C74
Other endocrine glands 1 0.0 100 0.0 - 2 0.0 100.0 0.0 0.0 C75
Lymphomas 259 96.5 1.2 2.3 0.4 210 1.0 97.1 1.9 0.4 C81-82,85,96
Multiple myeloma 39 89.7 0.0 10.3 0.6 42 4.8 83.3 11.9 0.7 C90
Leukemia 147 96.6 2.0 1,4 0,6 115 6.1 93.0 0.9 0.8 C90-95
Myelodysplastic syndromes 12 100 0.0 0.0 0.3 15 0.0 100.0 0.0 0.3 CIE-O-3: 998_/3
CIE-O3: 9950/3,
Myeloproliferative disorders 3 100 0.0 0.0 0.5 9 100 0.0 0.3
996_3/3, 9975/3
Other and unspecified 133 52.6 16.5 30.8 0.7 211 15.2 60.2 24.6 0.5 C26,39,48,76,80
All sites 3,423 80.6 9.3 10.1 0.6 4,584 8.5 83.0 8.5 0.5 C00-96
% MV: percentage of cases with microscopic verification (cytology-hematology and histology of the primary tumor)
% DCO: percentage of cases conducted on death certificate-only
% others: percentage of cases diagnosed by other methods (imaging, endoscopy and clinical)
MI: Mortality/Incidence

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to the first chronological event of diagnostic confirmation of the because they are diseases of great relevance for the region. Crude
disease or in case of lack of data the date of death was used. and standardised incidence and mortality rates are expressed per
100,000 males-year or females-year.
The information was collected in an active, continuous and
systematic way in all the health institutions that generate To assess the trend of incidence and mortality, a global analysis
information on cancer: hospitals, clinics, oncology units, pathology between five-year periods was made and the percentage change
and haematology laboratories, medical centers, specialized offices in rates between the last two periods was estimated. Additionally,
and the Municipal Health Secretariat, responsible for processing a trend analysis of annual incidence and mortality rates was
the death certificates. In addition, to guarantee the completeness performed using a segmented linear regression or joinpoint,
of the data, databases of hospital discharges, Beneficiaries Selection accepting a maximum of three change points (joinpoints) with
System for Social Programs (SISBEN in Spanish), National Attorney four linear segments respectively. The annual percentage of change
General’s Office, National Registry of Civil Status, Registry of (APC) was estimated in each possible segment generated between
patients of third level hospitals , the Solidarity and Guarantee Fund - each point and the average annual percentage change (AAPC) was
FOSYGA and the mortality database of the National Administrative calculated for the entire period. All possible models were adjusted
Department of Statistics (DANE in Spanish). with the weighted least squares method and the model selection
was made with the Montecarlo permutations test. All analyses
The cases were entered into the CanReg5 system for the were carried out in the SEER stat and Joinpoint 4.0 program
elimination of duplicates, processing and complementation of produced by the Surveillance Research Program of the National
data. The identification of primary multiple tumours follows the Cancer Institute of the United States16.
IACR standards13. For the validation of the internal consistency
between the variables, an automatic check was carried out with Ethical considerations
the IACRcrg Tools program version 2.05 and the rare cases were This study is classified as without risk research according to
resolved in a scientific committee formed by specialists or by resolution 8430 of 1993 of the Ministry of Health of Colombia,
consulting with the Cali Cancer Registry. since the information comes from secondary sources and has
no direct contact or intervention of the biological, physiological,
Analysis of the information psychological or social variables of the individuals studied.
For the analysis of incidence and mortality, frequencies were The handling of information follows the confidentiality rules
calculated such as absolute, relative, crude, specific rates (by established by the International Agency for Cancer Research
period, sex, age and site of the tumour or cause of death according (IACR) that regulate the use of data for scientific purposes without
to the ICD-10, grouped into large categories.) and standardised by the disclosure of personal data, guaranteeing respect and non-
age (ASR) to the world population standard (SEGI) by the direct maleficence towards patients. On the other hand, the Cancer
method7,14. The DANE population estimates and projections by Registry of Pasto and the investigations that derive from it have
the middle of the period were used as a denominator at risk for agreements with the sources of information to guarantee the
calculating the rates, which were calculated considering the basic adequate flow of the data.
components of the population dynamics: fertility, mortality, and
migration (internal and international) from the population base Results
determined in the 2005 census, and adjusted by conciliation of the
General Census (census 1985, 1993 and 2005)15. Cases without age Global incidence
(0.15%), basal cell carcinoma and squamous cell of the skin were During the period 1998-2012 in the municipality of Pasto, 8,010
excluded. cases of cancer were identified. (ASR 145.1 cases per 100,000
persons-year), 3,426 in males (ASR 139.1 cases per 100,000 males-
The incidence and mortality results are presented in specific year) and 4,584 cases in females (ASR: 150.3 cases) per 100,000
Tables or Charts and the analysis of the main sites was intensified females-year) (Tables 2 ​and 3).
170

Age-specific rate x 100,000 males or females - year


600 2,000

160 1,800
ASR x 100,000 males or females - year

500
1,600
Cancer Cases (n)

150 1,400
400
1,200
140
300 1,000

130 800
200
600
120 400
100
200
110
0 0
0-4 5-9 10-14 15-19 20-24 25-29 30-34 35-39 40-44 45-49 50-54 55-59 60-64 65-69 70-74 75-79 80-84 85 +
100
Age of diagnosis
1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012
Cases Cases
Modeled rate Modeled rate Males Females
Females Males ASpR ASpR
Observed rate Observed rate

Figure 2. Trend of age-standardized global rates of cancer incidence. Males and Figure 3. Cases and specific rates by age per 100,000 males or females-year of
females of Pasto, Colombia, 1998-2012. APC: Annual Percentage of change. ASR: incidence of cancer, Pasto, Colombia, 1998-2012. ASpR: age-specific Rates x 100,000
age-standardized Rates (SEGI world population standard) x 100,000 males or males or females-year
females-year

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By sex and period, in males there were in 1998-2002, 982 cases Incidence by age
(ASR: 135 cases per 100,000 males-year), for 2003-2007 1,174 cases Cases and cancer incidence rates increase by age; 55% of incident
(ASR: 147.1 cases per 100,000 males-year) and in 2008-2012 1,270 cases in males and 40% in females occurred after 65 years, while
cases (ASR 136.4 cases per 100,000 males-year). In females during 2% of cases in both genders occurred in children under 15 years of
1998-2002 there were 1,359 cases (ASR: 149.6 cases per 100,000 age (Fig. 3). The average age of diagnosis in males was 62.3 years
females-year), for 2003-2007: 1,541 cases (ASR: 156.1 cases per (Standard deviation SD= 18.7 years) and in females of 58.2 years
100,000 females-year) and in 2008-2012: 1,684 cases (ASR: 147.1 (SD= 18.1 years).
cases per 100,000 females-year). The percentage of change in the
global incidence rates between the last two periods was 0.2 in males Incidence by tumour site
and in females of 1.0%. The most frequent tumours over the 15 years in males were
The incidence trend indicates that there were no significant tumours of the: Stomach (23.5%), prostate (18.3%), lymphomas
changes in the incidence rates in both males and females during (7.6%) colon and rectum (5.2%) and lung (4.9%). In females were:
the analysed period (p-value males= 0.7, p-value females= 0.3), that breast (17.3%), cervix uteri (16.0%), stomach (10.8%), thyroid
means the incidence was stable. The average annual incidence rates (6.6%) and colon and rectum (5.3%). This behaviour was observed
standardised by age were 139.7 cases per 100,000 males-year and when analysing each of the three five-year periods that comprise
150.7 cases per 100,000 females-year (Fig. 2). the study period (Tables 2 and 3).

Table 2. Cancer incidence rates by tumour site, crude and age-standardized per 100,000 males-year. Pasto, Colombia, 1998-2002, 2003-
2007 and 2008-2012
PC(%) 2003-2007 ICD-10 code
1998-2002 2003-2007 2008-2012
Site and 2008-2012
n % CR ASR n % CR ASR n % CR ASR CR ASR
Oral cavity 15 1.5 1.8 2.3 13 1.1 1.4 1.7 11 0.9 1.1 1.1 -21.4 -35.3 C00-14
Oesophagus 35 3.6 4.1 4.6 23 2.0 2.5 3.0 15 1.2 1.5 1.5 -40.0 -50.0 C15
Stomach 296 30.1 34.8 42.6 258 22.0 28.2 32.6 250 19.7 25.3 26.7 -10.3 -18.1 C16
Small intestine 4 0.4 0.5 0.6 5 0.4 0.5 0.6 4 0.3 0.4 0.5 -20.0 -16.7 C17
Colon and rectum 42 4.3 4.9 5.9 57 4.9 6.2 7.3 78 6.1 7.9 8.4 27.4 15.1 C18-20
Anus 1 0.1 0.1 0.1 2 0.2 0.2 0.3 2 0.2 0.2 0.2 0.0 -33.3 C21
Liver 26 2.6 3.1 3.7 27 2.3 3.0 3.5 29 2.3 2.9 3 -3.3 -14.3 C22
Gallbladder 17 1.7 2.0 2.6 21 1.8 2.3 2.8 19 1.5 1.9 2.2 -17.4 -21.4 C23-24
Pancreas 18 1.8 2.1 2.6 36 3.1 3.9 4.4 24 1.9 2.4 2.8 -38.5 -36.4 C25
Nose, sinuses etc. 1 0.1 0.1 0.2 2 0.2 0.2 0.3 4 0.3 0.4 0.5 100.0 66.7 C30-31
Larynx 6 0.6 0.7 0.9 16 1.4 1.7 2.3 12 0.9 1.2 1.4 -29.4 -39.1 C32
Trachea, bronchus and lung 47 4.8 5.5 6.5 60 5.1 6.6 7.5 61 4.8 6.2 7.0 -6.1 -6.7 C33-34
Other thoracic organs 0 0.0 0.0 0.0 4 0.3 0.4 0.5 3 0.2 0.3 0.3 -25.0 -40.0 C37-38
Bone 8 0.8 0.9 0.9 6 0.5 0.7 0.8 5 0.4 0.5 0.5 -28.6 -37.5 C40-41
Melanoma of skin 11 1.1 1.3 1.4 16 1.4 1.7 2.1 29 2.3 2.9 3.1 70.6 47.6 C43
Other Skin 7 0.7 0.8 0.9 13 1.1 1.4 1.8 13 1.0 1.3 1.5 -7.1 -16.7 C44
Mesothelioma 1 0.1 0.1 0.2 2 0.2 0.2 0.2 3 0.2 0.3 0.3 50.0 50.0 C45
Kaposi sarcoma 0 0.0 0.0 0.0 1 0.1 0.1 0.1 8 0.6 0.8 0.8 700.0 700.0 C46
Connective and soft tissue 14 1.4 1.6 1.7 32 2.7 3.5 3.9 20 1.6 2.0 2.3 -42.9 -41.0 C47,49
Breast 0 0.0 0.0 0.0 2 0.2 0.2 0.2 3 0.2 0.3 0.4 50.0 100.0 C50
Penis 7 0.7 0.8 1.1 11 0.9 1.2 1.4 18 1.4 1.8 1.9 50.0 35.7 C60
Prostate 163 16.6 19.1 23.2 213 18.1 23.3 27.3 250 19.7 25.3 27.3 8.6 0.0 C61
Testis 21 2.1 2.5 2.3 43 3.7 4.7 4.3 41 3.2 4.1 3.6 -12.8 -16.3 C62
Other Male genital organs 1 0.1 0.1 0.2 1 0.1 0.1 0.1 1 0.1 0.1 0.1 0.0 0.0 C63
Kidney 15 1.5 1.8 2.1 15 1.3 1.6 1.7 15 1.2 1.5 1.8 -6.3 5.9 C64
Renal pelvis 0 0.0 0.0 0.0 0 0.0 0.0 0.0 1 0.1 0.1 0.1 C65 C65
Bladder 35 3.6 4.1 4.8 28 2.4 3.1 3.7 29 2.3 2.9 3.0 -6.5 -18.9 C67
Other urinary organs 0 0.0 0.0 0.0 1 0.1 0.1 0.1 1 0.1 0.1 0.1 0.0 0.0 C68
Eye 8 0.8 0.9 1.1 4 0.3 0.4 0.6 5 0.4 0.5 0.6 25.0 0.0 C69
Brain, nervous system 26 2.6 3.1 3.2 45 3.8 4.9 5.2 35 2.8 3.5 3.7 -28.6 -28.8 C70-72
Thyroid 12 1.2 1.4 1.5 20 1.7 2.2 2.7 28 2.2 2.8 2.6 27.3 -3.7 C73
Adrenal gland 0 0.0 0.0 0.0 1 0.1 0.1 0.1 0 0.0 0.0 0.0 -100.0 -100.0 C74
Other endocrine glands 0 0.0 0.0 0.0 1 0.1 0.1 0.1 0 0.0 0.0 0.0 -100.0 -100.0 C75
Lymphomas 72 7.3 8.5 9.0 87 7.4 9.5 10.9 100 7.9 10.1 10.6 6.3 -2.8 C81-82,85,96
Multiple myeloma 8 0.8 0.9 1.0 8 0.7 0.9 1.0 23 1.8 2.3 2.5 155.6 150.0 C90
Leukemia 40 4.1 4.7 4.5 52 4.4 5.7 6.1 55 4.3 5.6 5.9 -1.8 -3.3 C90-95
Myelodysplastic syndromes 0 0.0 0.0 0.0 3 0.3 0.3 0.4 9 0.7 0.9 0.8 200.0 100.0 CIE-O-3: 998_/3
 CIE-O3: 9950/3,
Myeloproliferative disorders 0 0.0 0.0 0.0 0 0.0 0.0 0.0 3 0.2 0.5 0.5
996_3/3, 9975/3
Other and unspecified 25 2.5 2.9 3.3 45 3.8 4.9 5.4 63 5.0 6.4 6.8 30.6 25.9 C26,39,48,76,80
All sites 982 100 115.3 135.0 1,174 100.0 128.3 147.1 1,270 100.0 128.6 136.4 0.2 -7.3 C00-96
All sites except C44 975 99.3 114.5 134.1 1,161 98.9 126.9 145.4 1,257 99.0 127.3 134.9 0.3 -7.2 C00-43,45-96
CR: Crude rate of incidence x 100,000 males-year;
ASR: Age-standardized rates (SEGI world population standard) x 100,000 males-year;
PC: Percentage of change

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Table 3. Cancer incidence rates by tumour site, crude and age-standardized per 100,000 females-year. Pasto, Colombia, 1998-2002, 2003-
2007 and 2008-2012
PC(%) 2003-2007
1998-2002 2003-2007 2008-2012 ICD-10 code
Localización and 2008-2012
n % CR ASR n % CR ASR n % CR ASR CR ASR
Oral cavity 17 1.3 1.9 1.9 21 1.4 2.1 2.1 7 0.4 0.7 0.6 -66.7 -71.4 C00-14
Oesophagus 12 0.9 1.3 1.3 13 0.8 1.3 1.2 11 0.7 1.0 1.0 -23.1 -16.7 C15
Stomach 183 13.5 20.2 20.2 175 11.4 17.6 17.1 137 8.1 12.8 11.8 -27.3 -31.0 C16
Small intestine 3 0.2 0.3 0.3 3 0.2 0.3 0.3 6 0.4 0.6 0.6 100.0 100.0 C17
Colon and rectum 63 4.6 7.0 6.8 75 4.9 7.5 7.5 104 6.2 9.7 9.0 29.3 20.0 C18-20
Anus 5 0.4 0.6 0.6 8 0.5 0.8 0.8 6 0.4 0.6 0.5 -25.0 -37.5 C21
Liver 26 1.9 2.9 2.7 32 2.1 3.2 3.0 34 2.0 3.2 2.8 0.0 -6.7 C22
Gallbladder 59 4.3 6.5 6.4 48 3.1 4.8 5.0 47 2.8 4.4 4.0 -8.3 -20.0 C23-24
Pancreas 21 1.5 2.3 2.3 54 3.5 5.4 5.5 41 2.4 3.8 3.7 -29.6 -32.7 C25
Nose, sinuses etc. 0 0.0 0.0 0.0 3 0.2 0.3 0.3 2 0.1 0.2 0.1 -33.3 -66.7 C30-31
Lung 0 0.0 0.0 0.0 1 0.1 0.1 0.1 1 0.1 0.1 0.1 0.0 0.0 C32
Trachea, bronchus and
23 1.7 2.5 2.3 37 2.4 3.7 3.8 57 3.4 5.3 4.8 43.2 26.3 C33-34
lung
Other thoracic organs 2 0.1 0.2 0.3 2 0.1 0.2 0.1 3 0.2 0.3 0.3 50.0 200.0 C37-38
Bone 5 0.4 0.6 0.6 8 0.5 0.8 0.7 8 0.5 0.7 0.7 -12.5 0.0 C40-41
Skin melanoma 31 2.3 3.4 3.3 32 2.1 3.2 3.2 45 2.7 4.2 4.0 31.3 25.0 C43
Other skin 10 0.7 1.1 1.1 10 0.6 1.0 1.1 15 0.9 1.4 1.2 40.0 9.1 C44
Mesothelioma 3 0.2 0.3 0.4 0 0.0 0.0 0.0 1 0.1 0.1 0.1 C45
Kaposi sarcoma 0 0.0 0.0 0.0 1 0.1 0.1 0.1 0 0.0 0.0 0.0 -100.0 -100.0 C46
Connective and soft
15 1.1 1.7 1.6 15 1.0 1.5 1.6 11 0.7 1 0.9 -33.3 -43.8 C47,49
tissue
Breast 219 16.1 24.2 24.4 258 16.7 25.9 27.1 313 18.6 29.3 27.7 13.1 2.2 C50
Vulva 5 0.4 0.6 0.5 5 0.3 0.5 0.6 6 0.4 0.6 0.5 20.0 -16.7 C51
Vagina 7 0.5 0.8 0.7 0 0.0 0.0 0.0 3 0.2 0.3 0.3 C52
Cervix uteri 251 18.5 27.7 27 272 17.7 27.3 27.4 210 12.5 19.6 18 -28.2 -34.3 C53
Corpus uteri 39 2.9 4.3 4.6 45 2.9 4.5 4.7 45 2.7 4.2 4.3 -6.7 -8.5 C54
Uterus unspecified 4 0.3 0.4 0.4 1 0.1 0.1 0.1 4 0.2 0.4 0.4 300.0 300.0 C55
Ovary 63 4.6 7.0 7.1 70 4.5 7.0 7.1 84 5.0 7.9 7.3 C56
Placenta 2 0.1 0.2 0.2 4 0.3 0.4 0.3 0 0.0 0.0 0.0 -100.0 -100.0 C58
Kidney 13 1.0 1.4 1.4 13 0.8 1.3 1.4 15 0.9 1.4 1.5 7.7 7.1 C64
Renal pelvis 1 0.1 0.1 0.1 0 0.0 0.0 0.0 1 0.1 0.1 0.1 C65
Bladder 18 1.3 2.0 2.0 14 0.9 1.4 1.5 20 1.2 1.9 1.7 35.7 13.3 C67
Other urinary organs 0 0.0 0.0 0.0 1 0.1 0.1 0.1 1 0.1 0.1 0.1 0.0 0.0 C68
Eye 10 0.7 1.1 1.2 7 0.5 0.7 0.7 2 0.1 0.2 0.2 -71.4 -71.4 C69
Brain, nervous system 23 1.7 2.5 2.7 27 1.8 2.7 2.8 49 2.9 4.6 4.4 70.4 57.1 C70-72
Thyroid 71 5.2 7.8 7.7 92 6.0 9.2 9.0 139 8.3 13.0 11.8 41.3 31.1 C73
Adrenal gland 1 0.1 0.1 0.2 0 0.0 0.0 0.0 0 0.0 0.0 0.0 C74
Other endocrine glands 0 0.0 0.0 0.0 0 0.0 0.0 0.0 2 0.1 0.2 0.2 C75
Lymphomas 64 4.7 7.1 6.6 71 4.6 7.1 7.3 75 4.5 7.0 6.3 -1.4 -13.7 C81-82,85,96
Multiple myeloma 7 0.5 0.8 0.8 19 1.2 1.9 2.1 16 1 1.5 1.4 C90
Leukemia 35 2.6 3.9 4.2 35 2.3 3.5 3.7 45 2.7 4.2 4.1 20.0 10.8 C90-95
Myelodysplastic
0 0.0 0.0 0.0 3 0.2 0.3 0.3 12 0.7 1.1 0.9 266.7 200.0 CIE-O-3: 998_/3
syndromes
Myeloproliferative CIE-O3: 9950/3, 996_3/3,
0 0.0 0.0 0.0 1 0.1 0.1 0.1 8 0.5 0.9 0.8 800.0 700.0
disorders 9975/3
Other and unspecified 48 3.5 5.3 5.6 65 4.2 6.5 6.4 98 5.8 9.2 8.8 41.5 37.5 C26,39,48,76,80
All sites 1359 100 149.9 149.6 1541 100 154.7 156.1 1684 100 157.7 147.1 1.9 -5.8 C00-96
All sites except C44 1349 99.3 148.8 148.5 1531 99.4 153.7 155.1 1669 99.1 156.3 145.9 1.7 -5.9 C00-43,45-96
CR: Crude rate of incidence x 100,000 males-year;
ASR: Age-standardized rates (SEGI world population standard) x 100,000 males-year;
PC: Percentage of change

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Stomach Cancer in Males Prostate Cancer


50 40
45 35
40

ASR x 100,000 Males - year

ASR x 100,000 Males - year


30
35
25
30
25 20
20 15
15
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5 APC= -4.58*
5
APC= 1.48
0 0

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Observerd rate Modeled rate Observerd rate Modeled rate

Breast Cancer in Females Cervix Uteri Cancer


40
40
35 35

ASR x 100,000 Females - year


ASR x 100,000 Females - year

30 30
25 25
20 20
15 15

10 10
5 APC 1998-2003 = 6.08
5
APC= 1.08 APC 2003-2012 = -8.56*
0 0

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Observerd rate Modeled rate Observerd rate Modeled rate


Figure 4. Trend of age-standardized incidence rates for the most frequent tumours. Pasto, Colombia, males and females 1998-2012.
APC: Annual percentage of change. ASR: Age-standardized Rate (SEGI world population standard) x 100,000 males-year. * Statistically
significant (p <0.005)

The incidence of stomach tumours in males decreased significantly females= 0.0), the average annual mortality rate standardised by
by 4.6% (p-value= 0.0) anwnually from an ASR of 41.5 in 1998 age was 78.5 deaths per 100,000 males-year. While in females
to 19.1 cases per 100,000 males-year in 2012. In females, the mortality rates reached 2.1% per year from an ASR: of 58.6 to 86.0
incidence of cervix uteri decreased 8.6% (p= 0.0) annually from deaths per 100,000 females-year, in 1998 and 2012 respectively
2003 from an ASR of 34.2 to 13.4 cases per 100,000 females-year (Fig. 5). The average in the three quinquennial periods of the ratio
in 2012. The incidence of prostate tumours (p= 0.2) and breast between the mortality-incidence rates (M: I) was 56 deaths per
(p= 0.3) was constant and the average of its annual incidence rates 100 diagnostic cases in males and 49 deaths per 100 diagnostic
standardised by age was 26 cases per 100,000 males-year and 26.4 cases in females.
cases per 100,000 females-year, respectively (Fig. 4).
Like the incidence, mortality showed the highest percentage of
Global mortality cases after 65 years old, both in males (63.9%) and in females
Over the period 1998-2012 in the municipality of Pasto there were (55.2%) (Fig. 6). The average age of death for males was estimated
4,221 deaths due to cancer (ASR: 75.9 deaths per 100,000 people- at 66 years (SD= 17.8 years) and for females at 63.7 years (SD:
year), 1,949 in males (ASR: 78 deaths per 100,000 males-year) and 17.1).
2,272 deaths in females (ASR: 74.4 deaths per 100,000 females-
year (Tables 4 ​and 5). Mortality by tumour site
Over 1998-2012, the main causes of cancer mortality in males
According to sex and period, over 1998-2002 period, 553 deaths were tumours of: Stomach (28.8%), prostate (12.3%) lung (9.7%),
occurred in males (ASR: 76.9 deaths per 100,000 males-year), for lymphomas and myelomas (7%) and liver (5.5%). In females
2003-2007, 648 deaths (ASR: 79.4 deaths per 100,000 males-year) were tumours of: Stomach (16.7%), cervix uteri (12.5%), breast
and in 2008-2012, 748 deaths (ASR: 79 per 100,000 males-year (11.3%), lung (6.2%), colon and rectum (6.2%). This behaviour
deaths). Over 1998-2002 there were 601 deaths in females (ASR: was observed during the three five-year periods that comprise the
65.6 deaths per 100,000 females-year), for 2003-2007, 701 deaths period of study (Tables 4 and 5).
(ASR: 71.2 deaths per 100,000 females-year) and in 2008-2012,
970 deaths (ASR: 84.3 deaths per 100,000 females-year). Mortality caused by stomach tumours in males decreased
significantly (p-value= 0.0) 2.18% annually from an ASR of 24.5
The trend in mortality indicates that there are no significant in 1998 to 19.9 deaths per 100,000 males-year in 2012. In females,
changes in mortality rates in males (p-value males= 1.0, p-value breast cancer mortality increased (p-value= 0.0) 3% annually from

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Table 4. Cancer mortality rates by tumour site, crude and age-standardized per 100,000 males-year. Pasto, Colombia, 1998-2002, 2003-
2007 and 2008-2012.
PC(%) 2003-2007
1998-2002 2003-2007 2008-2012
Localization and 2008-2012 ICD-10 code
N % CR ASR N % CR ASR N % CR ASR CR ASR
Oral cavity 3 0.5 0.4 0.4 4 0.6 0.4 0.4 9 1.2 0.9 0.9 125.0 125.0 C00-14
Oesophagus 22 4.0 2.6 3.2 25 3.9 2.7 3.1 25 3.3 2.5 2.6 -7.4 -16.1 C15
Stomach 190 34.4 22.3 26.6 172 26.5 18.8 21.5 200 26.7 20.2 21.5 7.4 0.0 C16
Small intestine 0 0.0 0.0 0.0 2 0.3 0.2 0.2 2 0.3 0.2 0.2 0.0 0.0 C17
Colon and rectum 15 2.7 1.8 1.9 34 5.2 3.7 4.2 50 6.7 5.1 5.3 37.8 26.2 C18-20
Liver 28 5.1 3.3 4.3 48 7.4 5.2 6.4 31 4.1 3.1 3.2 -40.4 -50.0 C22
Pancreas 20 3.6 2.3 3.1 28 4.3 3.1 3.4 27 3.6 2.7 3.0 -12.9 -11.8 C25
Lung 62 11.2 7.3 9.2 61 9.4 6.7 7.3 66 8.8 6.7 7.3 0.0 0.0 C34
Skin melanoma and Other skin 9 1.6 1.1 1.3 2 0.3 0.2 0.3 11 1.5 1.1 1.1 450.0 266.7 C43-44
Breast 2 0.4 0.2 0.2 1 0.2 0.1 0.1 0 0.0 0.0 0.0 -100.0 -100.0 C50
Prostate 66 11.9 7.7 9.4 81 12.5 8.9 9.2 92 12.3 9.3 9.0 4.5 -2.2 C61
Bladder 9 1.6 1.1 1.4 7 1.1 0.8 0.7 17 2.3 1.7 1.7 112.5 142.9 C67
Lymphomas and myelomas 37 6.7 4.3 4.4 45 6.9 4.9 5.7 55 7.4 5.6 6.0 14.3 5.3 C90 ,C81-82,85,96
Leukemias 25 4.5 2.9 2.8 21 3.2 2.3 2.4 42 5.6 4.2 4.3 82.6 79.2 C90-95
Other malignant tumours 65 11.8 7.6 8.8 117 18.1 12.8 14.4 121 16.2 12.2 12.9 -4.7 -10.4
All sites 553 100.0 64.9 76.9 648 100.0 70.8 79.4 748 100.0 75.6 79.0 6.8 -0.5 C00-96
CR: Crude rate of mortality x 100,000 males-year;
ASR: Age-standardized rates (SEGI world population standard) x 100,000 males-year;

Table 5. Cancer mortality rates by tumour site, crude and age-standardized per 100,000 females-year. Pasto, Colombia, 1998-2002, 2003-
2007 and 2008-2012.
PC (%) 2003-
1998-2002 2003-2007 2008-2012 2007 and 2008- ICD-10 code
Site 2012
n % CR ASR n % CR ASR n % CR ASR CR ASR
Oral cavity 2 0.3 0.2 0.2 3 0.4 0.3 0.3 7 0.7 0.7 0.6 133.3 100.0 C00-14
Oesophagus 8 1.3 0.9 1.0 11 1.6 1.1 1.0 13 1.3 1.2 1.1 9.1 10.0 C15
Stomach 131 21.8 14.5 14.1 121 17.3 12.1 12.0 128 13.2 12.0 10.9 -0.8 -9.2 C16
Small intestine 3 0.5 0.3 0.3 3 0.4 0.3 0.3 1 0.1 0.1 0.1 -66.7 -66.7 C17
Colon and rectum 25 4.2 2.8 2.5 41 5.8 4.1 4.1 74 7.6 6.9 6.3 68.3 53.7 C18-20
Liver 31 5.2 3.4 3.6 44 6.3 4.4 4.2 46 4.7 4.3 4.1 -2.3 -2.4 C22
Pancreas 36 6.0 4.0 4.0 52 7.4 5.2 5.3 43 4.4 4.0 3.7 -23.1 -30.2 C25
Lung 38 6.3 4.2 4.0 41 5.8 4.1 4.2 62 6.4 5.8 5.5 41.5 31.0 C34
Skin melanoma and other skin 13 2.2 1.4 1.4 11 1.6 1.1 1.0 17 1.8 1.6 1.4 45.5 40.0 C43-44
Breast 69 11.5 7.6 7.6 73 10.4 7.3 7.6 115 11.9 10.8 10.4 47.9 36.8 C50
Cervix uteri 107 17.8 11.8 11.6 65 9.3 6.5 6.6 111 11.4 10.4 9.5 60.0 43.9 C53
Corpus uteri 2 0.3 0.2 0.2 14 2.0 1.4 1.5 5 0.5 0.5 0.5 -64.3 -66.7 C54
Ovary 0 0.0 0.0 0.0 30 4.3 3.0 3.2 56 5.8 5.2 5.0 73.3 56.3 C56
Bladder 7 1.2 0.8 0.8 5 0.7 0.5 0.5 14 1.4 1.3 1.3 160.0 160.0 C67
Lymphomas and myelomas 34 5.7 3.8 3.8 34 4.9 3.4 3.5 48 4.9 4.5 4.2 32.4 20.0 C90 ,C81-82,85,96
Leukemias 30 5.0 3.3 3.3 24 3.4 2.4 2.5 41 4.2 3.8 3.5 58.3 40.0 C90-95
Other malignant tumours 65 10.8 7.2 7.2 129 18.4 13.0 13.2 189 19.5 17.7 16.3 36.2 23.5
All sites 601 100.0 66.3 65.6 701 100.0 70.4 71.2 970 100.0 90.7 84.3 28.8 18.4 C00-96
CR: Crude rate of mortality x 100,000 females-year;
ASR: Age-standardized rates (SEGI world population standard) x 100,000 females-year

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Figure 5. Trend of age-standardized global rates of cancer mortality. Males and females of Pasto, Colombia, 1998-
2012. APC: Annual percentage of change. ASR: Age-standardized rates (SEGI world population standard) x 100,000
males-year. * Statistically significant (p <0.005)

Age-specific rate x 100,000 males of females - year


350 2,000
1,800
300
1,600
Cancer Deaths (n)

250 1,400
1,200
200
1,000
150
800

100 600
400
50
200
0 0
0-4 5-9 10-14 15-19 20-24 25-29 30-34 35-39 40-44 45-49 50-54 55-59 60-64 65-69 70-74 75-79 80-84 85 +

Age of death

Deaths Deaths
Hombres Mujeres
ASpR ASpR
Figure 6. Deaths and death age-specific rates due to cancer per 100,000 males or females-year of Pasto, Colombia,
1998-2012. ASpR: Age-Specific rate x 100,000 Males or females-year

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Stomach Cancer in Males Prostate Cancer

35 14

30 12

ASR x 100,000 Males - year


ASR x 100,000 Males - year

25 10

20 8

15 6

10 4

5 APC= -2.18* 2 APC= -0.28

0 0

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Observerd rate Modeled rate Observerd rate Modeled rate

Stomach Cancer in Females Cervix Uteri Cancer

25 16
14
ASR x 100,000 Females - year

ASR x 100,000 Females - year


20
12

15 10
8
10 6
4
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APC= -1.60 2 APC= -1.60
0 0
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Observerd rate Modeled rate Observerd rate Modeled rate

Figure 7. Trend of age-standardized mortality rates for the most frequent tumours. Pasto, Colombia, males and females 1998-2012. APC: Annual percentage
of change. ASR: age-standardized Rate (SEGI world population standard) x 100,000 males-year. * Statistically significant (p-value <0.005).

an ASR of 6.3 in 1998 to 10.8 deaths per 100,000 females-year in At the regional level, thanks to the advances of the Cali Cancer
2012. Mortality from prostate tumours (p-value= 0.9), stomach Registry for the systematic reporting of data on incidence, mortality
tumours in females (p-value= 0.4) and cervix uteri (p-value= and survival to cancer, the Union for International Cancer Control
0.4) was constant and the average of their annual mortality rates (UICC), selected the city of Cali as one of the first cities in the
standardised by age was 9.3 deaths per 100,000 males-year, 12.3 world to implement the C/Can 2025 initiative: Challenge of cities
deaths per 100,000 females-years and 9.2 deaths per 100,000
against cancer, that consists of involving all the stakeholders of
females-year, respectively (Fig. 7).
each city in the design, planning and implementation of solutions
Discussion for cancer care. The data on the characterization of cancer morbi-
mortality provided by the Cali Cancer Registry for five decades
The population characterization on cancer incidence and will be the only source of evidence for evaluating the effects of the
mortality carried out by this study is part of the initiative to implementation of this strategy 21. Following the model of Cali, it
implement programs for its control promoted by the Organization is intended that the results presented in this study constitute the
of the United Nations, the World Health Organization (WHO), baseline about the cancer situation in the municipality of Pasto to
the specialized agency in cancer IARC and at the national level assess the effects of the implementation of the national program for
the Ministry of Health and Social Protection and the National cancer control that Colombia addressed in 20109.
Institute of Cancerology of Colombia10,17. These organizations
consider that the implementation of any program to control In general, it is considered that the global incidence rate for the
this disease and its outcomes should be supported by scientific Municipality of Pasto (ASR: 139.1 cases per 100,000 males-year
evidence and defined as: “approaches from public health, designed
and ASR: 150.3 cases per 100,000 females-year) and in other
to contribute to the reduction of cancer morbi-mortality, improve
the patients´quality of life with this condition through the systematic geographically close regions are low; Cali-Colombia (ASR: 205
and equitable implementation of strategies of prevention, early cases per 100,000 males-year and ASR: 186 cases per 100,000
diagnosis, treatment and palliation based on evidence, for the females-year), Manizales-Colombia (ASR: 156 cases per 100,000
optimal use of available resources; prioritizing in those vulnerable males-year and ASR: 165 cases per 100,000 females-year),
populations with greater cancer burden and intervening in those Bucaramanga-Colombia (ASR: 154 cases per 100,000 males-year
tumours that produce higher incidence and mortality”3,18-20. and ASR: 157 cases per 100,000 females-year), Quito-Ecuador

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(ASR: 193 cases per 100,000 males-year and ASR: 199 cases per North America and some European countries has increased very
100,000 females-year), Manabí-Ecuador (ASR: 89 cases per little, with an APC ranging between 3.3% and 1.5%. Only Indian
100,000 males-year and ASR: 102 cases per 100,000 females- populations (3 records) reported that the incidence trend of
year)24. The results observed are similar in other Latin American prostate cancer has decreased slightly with an APC of 0.2%. For
countries and contrary to those reported by the majority of North the Municipality of Pasto, incidence and mortality rates over time
American and oceanic registers 24. have remained constant without showing a statistically significant
change. The analysis of this behavior should be studied to establish
The behaviour of the global incidence rates of the populations can the factors related to early diagnosis and treatment.
be associated to lifestyles, diagnostic capacity in the health system,
but mainly to the demographic and epidemiological transition; in In females, the trend in the incidence of breast cancer is increasing
globally and is accentuated in populations of African and some
populations of North America, Oceania, Europe and Asia with a
European and Asian registries with an APC ranging between
significant population aging, the risk of chronic diseases increases,
5.3% and 2.2%, in Latin American, oceanic and some European
especially those of late presentation such as cancer, in contrast to
populations increased moderately with an APC that varies
those populations with a younger population structure such as between 2.1% and 1.3%, and very little in North American
in Latin America and Africa, which have greater public health populations and some Asians with an APC that ranges between
problems related to communicable diseases25,26. 0.3% and 1.2%. This behaviour is probably caused by the increase
in obesity, physical inactivity, and changes in reproductive and
When contrasting incidence rates with mortality rates, to establish other behavioural habits29. The tendency of the mortality by breast
the mortality-incidence ratio (M:I) it can be observed that, cancer varies between regions: populations of European and
although the majority of North American registries have higher North American countries show decreasing tendencies, contrary
rates of incidence in both males and females, the mortality and to the presented in the populations of South American countries.
incidence ratio reaches the lowest values (M:I: 30-40), which In Pasto the incidence rate remains constant and mortality has
means that for every 100 cases that are diagnosed there are a tendency to increase similar to other populations of South
between 30 and 40 cancer deaths in the same period. On the other American countries30.
hand, in Latin American countries the ratio M:I range between
60 and 80, its mean, for every 100 incident cases there are around The decrease in the incidence rates of cervical cancer worldwide is
80 deaths. This is an indirect indicator of the quality of the health very evident, with a greater decrease in Latin American, Oceanic
system in relation to diagnostic tests for the identification of new and some European populations with an APC that ranges between
cancer cases and oncological treatment services to avoid deaths 7. -2.7% and -8.6%, an average decrease in populations in North
America, some European and Asian with an APC that fluctuates
When comparing the incidence and mortality trends reported by between -1.4% and -2.6% and with a reduced decrease in some
other registries that have published at least 15 years consecutively European and Asian populations with an APC that oscillates
in IC5, it is observed that the incidence of stomach tumours between -0.3% and -1.1%, behaviour contrary to that reported by
decreased significantly in most populations, primarily in those African populations where the incidence trend increased with an
APC of 3.9%. In Pasto the tendency of the incidence of cervical
from European countries where the annual percentage of
cancer has lowered nevertheless the tendency of the mortality
change (APC) reported ranges between -5.1% and -3.1%, with
stays constant, results that reflect difficulties in the early detection
less decrease in North American, Oceanic and some European
and opportune treatment.
countries, the APC varies between -2.9% and -2.3% and with the
lowest decrease in Latin American populations with an APC that For the Municipality of Pasto the analysis of the incidence,
ranges between -2.2% and -0.9%. Only the registry of kyadondo mortality and behaviour of the tendency of the types of cancer of
county-Uganda and Goiania-Brazil, have reported an increase in greater occurrence becomes a base for the evaluation of the impact
the incidence of stomach cancer where the APC is 2.1% and 0.1% of the measures of prevention, treatment, implementation of new
respectively. In the Municipality of Pasto, the trend of incidence technologies and investigations that promote actions to control
and mortality from stomach cancer has achieved a significant the impact of the disease on the population.
decrease, this behaviour is explained by the study on the trend
of incidence and mortality from stomach cancer in Cali, which Acknowledgment
indicates that it is probably related to the decrease of the prevalent To the Cancer Population Registry team of the Municipality of
rates of infection by Helicobacter pylori, the improvement of life Pasto, Population Registry of Cancer of Cali, National Institute
of Cancerology of Colombia, Municipal Health Secretariat of
habits and early detection in the population, however, for the case
Pasto-Colombia and Hospitals, clinics, clinics and laboratories for
of the Municipality of Pasto, it is suggested to study in depth the
diagnosis and treatment of cancer in Pasto.
causes of this behaviour behaviour27,28.
Funding
The trend of the incidence of prostate tumours in the world has This research was done with funding from the Center for Health
increased significantly in most populations, in an accelerated Studies of the University of Nariño, the University of Nariño
way in Latin American populations, some European, Asian and (Agreement No. 076 of 2005), The Municipal Health Secretariat
oceanic with an APC that varies between 5.2% and 11.0%, has Pasto (Inter-institutional Cooperation Agreement August 25,
slightly increased in some European, Asian and Oceanic countries 2005) and the National Institute of Cancerology (Convention
with an APC that fluctuates between 3.4% and 3.9%, and in Africa, C0498 of 2010).

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Yepez MC/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)

Conflict of interest: 14. Dos Santos Silva I. Epidemiología del cáncer: principios y métodos.
The authors declare to have participated in the phases of International Agency for Research on Cancer. Lyon: IARC; 1999.
formulation, execution, processing and analysis of the investigation
that are exposed in this article and do not have conflicts of interest 15. Departamento Administrativo Nacional de Estadística.
in its development and diffusion. Estimaciones y proyecciones de población periodo 1985-2020.
Bogotá: DANE. Accessed: 2011. Available from: http://www.dane.
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proyecciones-de-poblacion.
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7. Forman D, Bray F, Brewster DH, Gombe Mbalawa C, Kohler 22. Curado MP, Voti L, Sortino-Rachou AM. Cancer registration
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8. Pardo C, Cendales R. Incidencia, mortalidad y prevalencia de 23. Murillo R, Quintero Á, Piñeros M, Bravo MM, Cendales R,
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de Cancerología. Plan nacional para el control del cáncer en 24. Bray F, Colombet M, Mery L, Piñeros M, Znaor A, Zanetti
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Vol. XI. Lyon: International Agency for Research on Cancer;
10. Piñeros M, Murillo R, Porras A. Guía para el análisis de la 2017. Accessed: October 2017. Available from: http://ci5.iarc.
situación del cáncer. Ministerio de la Protección Social. Instituto
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Nacional de Cancerología, E.S.E. Bogotá: MPS/INC; 2011.

11. Departamento Administrativo Nacional de Estadística. 25. Bongaarts J. Human population growth and the demographic
Población Ajustada Municipal y Omisión Censal: Censo tran­sition. Philos Trans R Soc Lond B Sci. 2009; 364(1532): 2985-90.
Básico 2005. Bogotá: DANE; Accessed: 2010. Available from:
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conciliacion_censal.pdf. 2004; 50(2): 127-144.

12. Alcaldía de Pasto. Dirección municipal de salud. Indicadores 27. Bravo L, Collazos T, Collazos P, Garcia L, Correa, P. Trends
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International Association of Cancer Registries. European network 28. Peleteiro B, La Vecchia C, Lunet N. The role of Helicobacter
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29. Althuis MD, Dozier JM, Anderson WF, Devesa SS, Brinton 30. Dibio A; Abriata G; Forman D; Sierra M. Female breast cancer
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Colomb Med. (Cali) 49(1): 47-54

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Original Article

Cancer incidence and mortality in Barranquilla, Colombia. 2008-2012


Incidencia y mortalidad por cáncer en Barranquilla, Colombia. 2008-2012

Rusvelt Vargas Moranth1,2,3, Edgar Navarro Lechuga1,4

1
Registro Poblacional de Cáncer de Barranquilla. Barranquilla, Colombia.
2
Grupo de Investigación en Economía de la Salud, Universidad de Cartagena, Cartagena, Colombia.
3
Grupo de Investigación Sanus Viventium, Barranquilla, Colombia.
4
Grupo de Investigación Proyecto UNI. Departamento de Salud Pública, Universidad del Norte, Barranquilla, Colombia.

Vargas MR, Navarro LE. Cancer incidence and mortality in Barranquilla, Colombia. 2008-2012 Colomb Med (Cali). 2018; 49(1): 55-62.
doi: 10.25100/cm.v49i1.3627

© 2018 Universidad del Valle. This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use,
distribution and reproduction in any medium, provided that the original author and the source are credited.

Article history: Abstract Resumen

Received: 30 October 2017


Objective: To describe the behavior of cancer incidence and mortality Objetivo: Describir el comportamiento de la incidencia y mortalidad
Revised: 07 December 2017
Accepted: 13 February 2018 during 2008-2012, in the Barranquilla District. del cáncer durante el período 2008-2012, en el Distrito de Barranquilla,
Methods: Incident cancer cases were collected, analyzed and processed Colombia.
Keywords: by the Barranquilla Cancer Population Registry during the study Métodos: La información fue obtenida del Registro Poblacional de
Cancer, incidence, mortality, period. The population structure was obtained from the National Cáncer de Barranquilla y el DANE. Se analizaron casos incidentes y
population registries Administrative Department of Statistics (DANE) and the mortality muertes por cáncer en residentes de Barranquilla, desde enero 1 de
from the Cancer Information System in Colombia. The total and 2008 hasta diciembre 31 de 2012. Los casos informados corresponden
Palabras clave:
specific crude and specific incidence rates and mortality by age and sex a tumores malignos primarios invasivos en todas las localizaciones,
Cáncer, incidencia,
were estimated, as well as by-age standardized incidence rates. excepto carcinomas de células escamosas y células basales en piel. Se
mortalidad, registros
poblacionales. Results: Were identified 8,182 cases of cancer, excluding non- verificó la consistencia interna de los datos y se aplicaron indicadores
melanoma skin (62.8% in women). 83.0% of the tumors had de calidad sugeridos por la IARC. La población en riesgo se obtuvo de
histological verification and only 5.2% were DCO. The adjusted proyecciones poblacionales (1985-2020, DANE). Se estimaron tasas
incidence rate for all tumors was 116.5 per 100,000 in men and 155.4 específicas por sexo y edad (grupos quinquenales) y se estandarizaron
per 100,000 in women. The most frequent locations were prostate por método directo utilizando como referencia población mundial.
and trachea-bronchi-lung in men, while in women breast and cervix Resultados: Se identificaron 8,182 casos de cáncer, (62.8% en mujeres).
occupied the first places. Breast and prostate had the highest mortality 83.0% tuvieron verificación histológica y 5.2% fueron capturados solo
rates in women and men, respectively. por certificado de defunción. La tasa global de incidencia de cáncer por
Conclusion: Specific behavior of cancer incidence and mortality in 100,000 personas /año ajustada por edad fue 116.5 en hombres y 155.4
Barranquilla has important increases in main types of tumors (breast en mujeres. Las localizaciones más frecuentes de neoplasias malignas
and prostate) with respect to the country and other population fueron: próstata y pulmón en hombres, y mama y cérvix para mujeres.
registries, provided data are key to showing a representative behavior Las mayores tasas de mortalidad se presentaron por los tumores de
of the Colombian Caribbean. mama en mujeres y próstata en hombres.
Conclusión: la incidencia y mortalidad por cáncer en Barranquilla
presentan aumentos importantes en los principales tumores (mama
y próstata) con respecto a otras regiones de Colombia. Los datos
aportados pueden considerarse representativos del comportamiento
epidemiológico del cáncer en el caribe colombiano.

Corresponding author:
Edgar Navarro Lechuga. Hospital Universidad del Norte, Calle 30 Autopista
Aeropuerto, Ciudadela Rotaria. E-mail: enavarro@uninorte.edu.co
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Introduction climate and with characteristic that include genetic, social and
cultural elements, a product of the miscegenation marked since
Cancer is a public health problem. In 2012, there were near of 14 the Spanish colonization and having been in previous centuries the
million incident cases worldwide, and the expectation is unfavorable recipient of European and Middle Eastern migrants, it is necessary
since this number is expected to increase to almost 24 million by to have a population register of cancer and analyze the behavior of
20301. Cancer is responsible for 17% of the deaths in the world, cancer in the city within the national scenario, which gave rise to
and about a third of them are due to five potentially modifiable risk the Barranquilla Population Cancer Registry (BPCR), the result
factors: high body mass index, low intake of fruits and vegetables, of a strategic alliance between the INC and the  Universidad del
cigarette smoking, sedentary lifestyle and consumption of alcohol2, Norte  to consolidate incidents in the population resident in the
which indicates that cancer is largely preventable. District of Barranquilla since January 1st, 2008, and have quality
information, which is necessary for cancer control.
In Colombia, cancer is the third cause of mortality3. For the 2002-
2006 period, the age-standardized incidence rate for all cancers The objective of present study is to describe cancer incidence and
(with the exception of skin) was 196.9/100,000 in women and mortality in Barranquilla for the 2008-2012 period. The BPCR
186.6 in men4, similar to international rates, noting that close to use international standards5,6  and the information consolidated
56% of new cases and about 70% of deaths from cancer occur in by the Sistema de Información de Cáncer en Colombia (Cancer
medium and low-income countries5. Information System in Colombia) to obtain valid information to
make timely and efficient decisions regarding the comprehensive
Some researchers point out that cancer mortality rates can be approach to cancer in the Colombian Caribbean region.
taken as an indicator of health care´s quality, due to the disease’s
high probability of being prevented or treated in a timely manner6. Material and Methods
Therefore, it is necessary to determine the behavior, not only of
the incidence, but also of the mortality, in the different regions of Type of study
the country7, due to diversity in sociocultural, geographical and Descriptive Population base
genetic characteristics in each area4.
Population at risk and area of influence
In Colombia, there are only five Population Base Registries BPCR covers the urban and rural population of the District of
endorsed by the  Instituto Nacional de Cancerología  (National Barranquilla, located in the northeastern vertex of the department
Cancer Institute of Colombia, INC): Cali, Bucaramanga, Pasto, (province) of  Atlántico, on the western shore of the Magdalena
Manizales and Barranquilla. Every one of the registers represents River, 7.5 km from its mouth in the Atlantic Ocean. Its geographical
the cultural, geographical and environmental differences of the position is: 10º59’16” north latitude, and 74º47’20” west longitude.
zones that each covers; nevertheless, the city of Barranquilla is The urban area is at a maximum height of 98 meters above sea
the only one that does not have direct environmental influences level to the west and 4 meters above sea level to the east. The city
and Andean customs, such as those of the interior of the country, limits to the north with the municipality of Puerto Colombia, to
palpable in the other Registries; being a coastal city, with a tropical the south with the municipality of Soledad, to the east with the

n n
6,601 Males 80-+ Females 11,243
6,095 Total people 75-79
Total people 9,226
9,066 290,383 70-74
327,032 12,627
12,003 65-69 14,809
17,431 60-64 20,311
23,588 55-59 26,802
29,644 50-54 34,987
35,779 45-49 40,690
35,993 40-44 41,706
36,677 35-39 40,726
43,784 30-34 47,521
50,726 25-29 54,969
53,855 20-24 52,630
53,741 15-19 51,616
53,554 10-14 51,797
53,417 5-9 51,147
52,442 0-4 50,109

10 5 0 0 5 10
Percentage
Figure 1. Population structure by age and gender. District of Barranquilla. Departamento Administrativo Nacional de Estadísticas (DANE)

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Vargas MR/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)

department of Magdalena and the Caribbean Sea, and to the Case definition
west with the municipalities of Galapa, Puerto Colombia and Every malignant tumor located anywhere, including benign
Tubará. The district of Barranquilla is divided into five localities neoplasms of the central nervous system that has been diagnosed
for administrative and political purposes: Riomar, Norte-Centro in permanent residents of the District of Barranquilla, since January
Histórico, Sur Occidente, Metropolitana,  and  Sur Oriente  These 1st  of 2008, regardless of the diagnosis method, including cases
localities are subdivided into 611  manzanas (blocks)  and 188 identified only by death certificate. Skin cases corresponding to
neighborhoods, approximately. Additionally, the District includes squamous and basal cell carcinomas are excluded (ICD code 10).
the corregimientos (small towns) of La Playa and Juan Mina8.
Primary cancer is understood as one which originates in a location
The extension of the city is 154 Km2, and the climate is dry or tissue that does not correspond to the extension, recurrence or
tropical, with an average temperature of 27.4° C. According to metastasis of another primary tumor11. The most valid basis for
DANE (Departamento Administrativo Nacional de Estadísticas- diagnosis is the clinical morphology (histopathological, aspiration
National Administrative Department of Statistics)) projections for cytology, flow cytometry, imaging, endoscopy) and death
the year 2010, Barranquilla had a total of 1,224,000 inhabitants, certificate only (DCO).
with a density of 7,945 inhabitants per km2. The economy is
mainly based on the industrial, port and tourism sectors9. Figure The main information sources of the registry are: pathology and
1 shows the population by gender and age for 2010. hematology laboratories, hospital discharges, imaging and early
detection centers, oncology centers, medical specialists, and
In 2012, the District of Barranquilla had 1,352 private health service individual death certificates. To confirm if a subject is a resident
providers (807 independent professionals and 463 IPS, which is of Barranquilla, or has a high probability of being a resident, the
Healthcare-Providing Institutions or Instituciones Promotoras de identification document number is used to validate residence;
Salud) and the public network, made up of 48 health institutions, is this is entered on the Registraduría Nacional (National Register)
managed by a private operator. These institutions have more than website (http://www.registraduria.gov.co/), and the subject that
70 oncological services (surgical, chemotherapy, radiotherapy, appears with an assigned voting location is considered as a habitual
among others)10  that give Barranquilla the status of reference resident of said place; the information is then cross-checked with
center for the Atlantic Coast and the Caribbean, which is an the official national database of beneficiaries of social programs
additional challenge for the BPCR’s aim of identifying cases from (https://www.sisben.gov.co/atencion-al-ciudadano/Paginas/
city residents that are served by the public and private hospital consulta-del-puntaje.aspx; http://roble.barranquilla.gov.co:8888/
network. This has been addressed by verifying the data from 74 SisbenIII/) and healthcare (http://ruafsvr2.sispro.gov.co/; http://
sources of information (pathology laboratories, imaging centers, www.adres.gov.co/BDUA/) which include addresses. Likewise,
clinics and hospitals), each with a different recollection dynamic, through specific projects, cases are selected that are analyzed in
and by cross-checking the information from all databases. depth regarding sociodemographic and clinical variables.

The BPCR collects data on malignant tumors (and benign tumors The cases obtained from hospital discharges on one hand and
of the central nervous system) in all topographic locations DCO on the other hand, are determined after a process of review
(in skin, only melanoma) and all age groups. The search is of clinical histories to verify their diagnosis. In the absence of
active, that is, the BPCR staff periodically visits the sources of clinical information, cases are labeled as “identified only by DCO”.
information: histopathology laboratories, hospitals and clinics,
diagnostic centers, and institutions specialized in oncological Classification and codification of cases
care in the city. Likewise, data on mortality, health insurance, The BPCR collects patient variables (identification number,
and other sociodemographic background is consulted in the name, gender, and age / date of birth) and tumor variables (date
official databases of the country, such as the National Registry of of incidence, valid basis of diagnosis, topography, morphology,
the Nation, the “Unique Registry of Affiliates” (Registro Único behavior and source of information). The coding is carried out
de Afiliados,  RUAF) and the “Identification System of Potential by personnel trained in the application of ICD-O-310 guidelines.
Beneficiaries of Social Programs” (Sistema de Identificación de The information was initially processed in an electronic sheet
Potenciales Beneficiarios de Programas Sociales, SISBEN), among and was migrated to Canreg5 in 2016. The coding of the cases
others. is carried out following the Third Edition of the International
Classification of Oncological Diseases (ICD-O-3)12 and the rules
Barranquilla Population Cancer Registry for multiple primary tumors of the International Agency for
It initiated activities in 2008, collecting data from the 2007 cases, Research on Cancer (IARC)13. For the definition of the incidence
which were considered as a pilot test adopting the guidelines date, the recommendations of the European Network of Cancer
suggested by the IARC for population-based records. The BPCR is Registries (ENCR)14  are considered. The database is reviewed
made up of a multidisciplinary team of 9 people: 3 physicians (one with IARCtools® and LinkPlus® to identify possible errors and
Master in Epidemiology, one Master in Public Health, and one duplications, and to verify the internal consistency between
Pathology specialist), one business administrator (coordinator) variables6. Cases with inconsistencies are reviewed in the sources
and 5 technicians (4 information collectors and 1 user) funded by of information and adjustments are made.
the Universidad del Norte and the INC.
Quality of the information
Collecting and processing information BPCR researchers, supported by the INC and the population
BPCR actively and passively searches for information regarding registries of Cali, Bucaramanga, Manizales, and Pasto, permanently
new cases of cancer. train the people participating in the RPCB in techniques and
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Table 1. Quality indexes by high incidence cancer location and gender. BPCR, 2008-2012
Male Female
Location
n %DCO %MV MI n %DCO %MV MI
Breast 2,094 1.0 93.0 0.2
Prostate 1,078 2.6 85.6 0.4
Cervix uteri 747 2.1 94.6 0.4
Lung 265 13.2 64.9 1.4 159 18.9 61.0 1.5
Thyroid 176 0.0 91.5 0.1
Leukaemia 156 4.5 96.2 2.4
Colon 137 10.2 73.0 0.6 175 7.4 74.3 0.7
Stomach 113 9.7 68.1 1.2
Total 3,042 6.5 80.0 0.5 5,140 3.9 85.9 0.7
DCO: only via death certificate
MV: microscopic verification.
MI: Mortality to incidence ratio

standards to collect, process and analyze information, while Lung and Stomach in men, and Lung in women, had values higher ​​
being aware of the fact that the quality of the data depends on than 1. On the other hand, there were no cases without information
the information obtained from the sources and of the mission in the gender and diagnostic basis variables. Table 1 shows the quality
processes of the BPCR. In addition, indicators suggested by the indicators for the locations with the highest incidence by gender.
IARC are used to evaluate the quality of the BPCR: percentage of
cases with microscopic verification, percentage of cases registered Incidence and mortality due to every cancer (all locations)
only by DCO, percentage of cases with unknown primary location, During the period of study, 8,182 new cases were registered, 62.8%
proportion of cases with unknown age at the time of diagnosis, of which corresponded to women. The average age at diagnosis
mortality / incidence ratio, and percentage of cases with unknown was 56.1 years old for women and 61.9 for men, and 2.3% of cases
diagnosis basis. Regarding confidentiality, the BPCR adopts the occurred in the pediatric population (younger than 15 years old).
standards of the IARC, considering the purpose of collecting, The Age-Standardized Incidence Rate per 100,000 people-year
processing and analyzing the information as epidemiological15. for all primary locations, including melanoma and excluding the
rest of skin tumors, was 116.5 in men and 155.4 in women and
Estimations of incidence the female / male incidence ratio was 1.3 (Table 2). Regarding
Every new case registered in residents of Barranquilla between mortality, it was higher in men: 82.4 compared to 75.9 deaths per
January 1st of 2008 and December 31st of 2012 was considered. The 100,000 people-years and the ratio of female to male mortality was
population at risk was calculated using the 1985-2020 projections 0.92 (Table 3).
prepared by DANE. The specific rates were estimated by gender
and age (five-year groups) and standardized using the direct Incidence and mortality by type of cancer
method when using the world population (WHO) as a reference. The five locations with the highest incidence in men were: prostate
The relative frequencies of incident cases were estimated by (43.0), trachea, bronchus and lung (10.4), colon and rectum (9.6),
specific locations. Incidence and mortality data are presented oral cavity (4.6) and stomach (4.4), corresponding to 61.3% of
grouped in ICD-10 codes for comparability purposes, following all the types of cancer. In women, the five most recurrent types
the methodology used by the IARC16. of cancer represent 72.0% of all types of cancer, and were: breast
(65.7), cervix (26.6), colon and rectum (9.8), thyroid (5.2), and
Estimations of mortality trachea, bronchi and lung (4.8). In terms of mortality, tumors in
All deaths occurred during the same period were included with the the lung, breast, prostate, colon and rectum and cervix represent
ICD-10 codes corresponding to malignant neoplasms, including 49.0% of all tumors, and the highest mortality rates standardized
DCOs and deaths occurred in the observation period. It was by age per 100,000 people / year were: prostate (17.4), lung (14.3),
based on the information consolidated in the Cancer Information leukemia (6.1) and stomach and lymphomas (5.1 each) in men,
System in Colombia17, which uses as population at risk the 1985- and breast (15.7), cervix (9.8), lung (7.1), colon and rectum (6.7),
2020 projections done by DANE. Mortality was also adjusted by and leukemia (4.4) in women. Tables 2 and ​3 show the incidence
the direct method using the same reference population used in the and mortality rates according to specific locations by gender,
standardization of incidence. and  Figure 2  shows the incidence rate by age for the two main
types of cancer in women (breast and cervix) and men.
Results
Discussion
Global quality indicators
The percentage of histological verification for all locations was of Regarding the quality criteria, the BPCR was found to be compliant
80.0% in men and of 85.9% in women; the five main locations by with the requirements defined by the IARC6: microscopic
gender showed that breast, cervix and thyroid (in women), and verification of at least 80% of the cases and less than 10% of the
leukemia (in men) had percentages higher than 90%. On the cases registered by DCO, and the same figure for tumors with
other hand, the percentage of registrations by DCO represented an unknown or a poorly defined primary location. It is possible
3.9% in women and 6.5% in men and had values lower ​​ than 5.0% that the M:I >1 ratio for some tumors may indicate the need to
for prostate and leukemia (men) and breast, cervix and thyroid strengthen the active search for incident cases, but it could also
(women). Regarding the Mortality-Incidence ratio, for men it had indicate an excessive registration of lung, leukemia and stomach
a value of 0.5 and for women of 0.7. It is striking that, Leukemia, cancer as causes of death in the DCOs.

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Tabla 2. Cancer incidence by location and gender. Barranquilla, 2008-2012


Males Females
Location n CR ASIR n CR ASIR ICD-10 Code
Oral cavity and pharynx 125 4.3 4.6 74 2.4 2.2 C00-C14
Esophagus 34 1.1 1.3 22 0.7 0.6 C15
Stomach 117 4.1 4.4 96 3.1 2.8 C16
Small intestine 10 0.3 0.3 10 0.3 0.2 C17
Colon and rectum 253 8.8 9.6 337 11.0 9.8 C18-C20
Anus 12 0.4 0.4 48 1.5 0.9 C21
Liver and bile ducts 51 1.9 2.1 56 1.9 1.8 C22
Gallbladder 19 0.7 0.8 34 1.3 1.9 C23-C24
Pancreas 41 1.1 1.2 66 1.2 1.0 C25
Nose. ear and paranasal sinus 10 0.3 0.4 9 0.2 3.2 C30-C31
Larynx 103 3.6 3.9 18 0.6 3.5 C32
Lung 268 9.4 10.4 159 5.4 4.8 C33-C34
Other thoracic organs 19 0.7 0.7 19 0.6 0.5 C37-C38
Bones and articulations 38 1.2 1.2 33 1.0 1.0 C40-C41
Melanoma of the skin 10 0.3 0.4 13 0.4 0.4 C43
Conjunctive and soft tissue 71 2.4 2.6 85 2.7 2.6 C47-C49
Breast 2,148 70.0 65.7 C50
Vulva 19 0.7 0.6 C51
Vagina 38 1.2 1.1 C52
Cervix uter 870 28.7 26.6 C53
Body of the uterus 100 3.1 2.9 C54
Ovary 143 4.7 4.4 C56
Other female organs Not Specified 8 0.3 0.3 C57
Penis 40 1.4 1.6 C60
Prostate 1,104 37.5 4.3 C61
Testícle 11 0.4 0.4 C62
Kidney 62 2.0 2.3 53 1.7 1.6 C64
Bladder 66 2.3 2.6 33 1.0 0.9 C67
Eyes and anexes 26 1.1 1.1 14 0.5 0.5 C69
Brain, CNS 107 3.7 3.9 100 3.2 3.0 C70-C72
Thyroid 31 1.0 1.1 182 5.8 5.2 C73
Other endocrine glands 10 0.3 0.3 9 0.2 0.2 C75
Hodgkin Lynphoma 35 1.1 1.1 26 0.9 0.8 C81
Non Hodgkin Lynphoma 107 3.8 4.0 9 2.6 2.4 C82-C85,C96
Multiple myeloma 17 0.6 0.6 18 0.6 0.5 C90
Lymphoid leukaemia 52 1.8 1.9 27 1.5 1.5 C91
Myeloid leukaemia 69 2.2 2.3 27 1.9 1.8 C92-C94
Leukaemia unspecified 37 1.4 1.5 27 0.9 0.8 C95
Other and unspecified 90 3.0 3.1 79 2.5 2.2 C26,C39,C48,C76,C80
All locations 3,063 105.9 116.5 5,133 168 155.4 C00-C96
CR: Crude rate per 100,000 people-year, ASIR: Age-standardized Incidence Rate (SEGI world population) per 100,000 people-year

Men Women
500 500

400 400

300 300
Rate per 100,000 people - year

Rate per 100,000 people - year

200 200

100 100

0 0
30 40 50 60 70 80 30 40 50 60 70 80
Age (years) Age (years)
Lung Prostate Breast Cervix

Figure 2. Specific incidence rates by age in women and men, first two locations. (Rates per 100,000 p-y). Barranquilla, 2008-2012

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Vargas MR/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)

Table 3. Annual average mortality due to cancer by location and gender. Barranquilla, 2008-2012
Males Females
Location n CR ASIR n CR ASIR ICD-10 Code
Oral cavity and pharynx 10 1.7 1.9 6 0.9 0.8 C00-C14
Esophagus 7 1.1 1.3 3 0.4 0.3 C15
Stomach 27 4.6 5.1 24 4.0 3.3 C16
Colon and rectum 33 5.7 6.0 49 7.9 6.7 C18-C20
Liver and bile ducts 18 3.1 3.4 23 3.7 3.1 C22
Pancreas 16 2.8 3.1 22 3.5 2.9 C25
Lung 75 13.0 14.3 49 8.1 7.1 C33-C34
Melanoma of the skin 2 0.3 0.4 2 0.2 0.2 C43
Breast 108 17.6 15.7 C50
Cervix uter 66 10.8 9.8 C53
Body of the uterus 6 0.9 2.9 C54
Ovary 21 3.4 3.1 C56
Prostate 95 16.6 17.4 C61
Bladder 7 1.3 1.3 5 0.8 0.6 C67
Lymphomas 27 4.7 5.1 24 3.9 3.5 C81-C90, C96
Leukemia 34 5.9 6.1 28 4.6 4.4 C91-C95
Thyroid 6 1.0 0.2 35 5.8 0.5 C73
Other and unspecified 24 4.1 4.4 32 5.3 4.5 C26, C39,C48,C76,C80
All locations 442 76.9 82.4 527 86.1 75.9 C00-C96
CR: Crude rate per 100,000 people-year, ASIR: Age-standardized Incidence Rate (Segi world population) per 100,000 people-year

With respect to the results of the analysis of the cases registered by the these tumors26, this information is validated to a great extent,
BPCR during the 2008-2012 period, the standardized rate in women although for future studies the effect of sociocultural factors (use
(155.4/100,000) was higher than that of men (116.5/100,000), as it of screening, self-care, etc.) environmental (climate, topography,
has occurred in other places, such as Guayaquil, Ecuador, whose altitude)25 and the composition of the population, a product not
Population Registry found rates of 110.0/100,000 and 146.0/100,000 only of miscegenation, but also of groups that migrated to the area
for men and women, respectively, during the 2003-2006 period18, since the nineteenth century (Arabs, Germans and English, etc.)27.
and in Khartoum, Sudan19, which also had larger rates for women:
124.3/100,000 and 90.8/100,000, during a period similar to the one In the case of men, prostate cancer presented a rate of 43 cases
reported in this article: 2009-2012. per 100,000 men-years, a value that could be considered as
intermediate when compared with Bucaramanga (50.5) and
On the other hand, more than 80% of the cases had pathological Manizales (32.7). In this regard, it is important to mention that, in
confirmation, and the percentages of cases identified only by DCO Colombia, the Ministerio de Salud y Protecciòn Social (Ministry
were 6.5% in men and 3.9% in women, these were values ​​lower of Health and Social Protection) and the  Sociedad Colombiana
than the maximum suggested by the IARC20. The cancers with de Urologìa  (Colombian Society of Urology) recommend early
higher incidence in women were: breast, cervix, colon-rectum, detection in men over 50 years of age or under 50 years of age if
thyroid, and trachea-bronchi-lung. For men, the malignant risk factors are present28, due to scientific evidence showing better
neoplasms of higher incidence were: prostate, trachea-bronchi- results for screening in this groups.
lung, colon-rectum, oral cavity, and stomach. The standardized
rate for all cancers, excluding non-melanoma skin cancer, was Regarding mortality, important differences have been found in
116.5 per 100,000 people-years in men and 155.4 per 100,000 some departments of Colombia, such as the case of  Atlántico,
person-years in women. where the District of Barranquilla is located, where mortality rates
for cancer were higher than the national average4; for the 2007-
Cervical tumors represented a significant percentage, which can 2011 period, the mortality rate standardized by age for breast
be attributed, to a large extent, to the early detection programs cancer per 100,000 inhabitants was 9.5 in the country, while for
in the country20, which have contributed to the inclusion of the department of  Atlántico  this indicator had a value of 12.0,
these cancers, along with breast cancer, as an epidemiological only exceeded by Valle del Cauca with 12.3, while for prostate at
surveillance object 21. It is worth noting the high incidence of breast national level the value was of 10.5 per 100,000 inhabitants, and
cancer (65.7/100,000), higher than those reported for different for the Department it was of 14.6, occupying the second place at
periods (2003-2007) by Manizales (33 / 100,000)22, Bucaramanga the national level4.
(41.9/100,000)23, and Cali (48.0/100,000)24. This data is related to
mortality from this tumor, since along with Armenia, Cali, and This study finds that the rates for breast and prostate cancers
Bucaramanga, Barranquilla has mortality rates which are higher are the highest: 15.7 and 17.4 per 100,000 inhabitants in each
than the national average: 10.525, and although mortality has case, as stated by the  Análisis de Situación de Salud del Distrito
been determined chronologically before the incidence, it could de Barranquilla  (Health Situation Analysis of the District of
be an indicator associated with the number of cases captured by Barranquilla)10, which also indicates that the mortality rate of breast
the BPCR, which is supported by the number of cases of breast cancer has progressively increased by 2.43 points from 2004 to 2014,
cancer estimated for the department of Atlántico by the INC4: 481 while in the same period, prostate cancer’s has fallen 5.36 points.
per year, compared to an annual average of 430 captured by the
BPCR. Likewise, the percentage of DCO is low for breast cancer, It is noteworthy that, this study is the first to take data from
and having carried out an exhaustive review of the residence for the  Sistema de Información de Cáncer en Colombia  to analyze

60
Vargas MR/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)

mortality. This tool is available to the general public as of 2017 5. Bray F, Znaor A, Cueva P, Korir A, Swaminathan R, Ullrich A, et al.
and is the result of the efforts of the INC and the Cancer Registries Planificación y desarrollo de registros de cáncer de base poblacional
of Colombia. Taking this source and not the DCOs of DANE en los países de ingresos bajos y medios. IARC, Publicaciones
“directly”, is an interesting challenge that allows us to glimpse the técnicas, N 43; 2015.
scope and potential of the information system as an important
resource for decision making in the country. Breast cancer was 6. Bray F, Parkin D. Evaluation of data quality in the cancer
found to be the leading cause of death among women, and in men, registry: principles and methods. Part I: comparability, validity and
cancer mortality was attributed mainly to prostate cancer. timeliness. Eur J Cancer. 2009; 45(5): 747–55.

Conclusions 7. Bravo L, Collazos T, Collazos P, García L, Correa P. Trends


of cancer incidence and mortality in Cali, Colombia. 50 years
The information obtained by the BPCR is reliable, in accordance experience. Colomb Med (Cali). 2012; 43(4): 246-55.
with the standards required by IARC, and constitutes an important
contribution to the National Information System of Cancer. The 8. Concejo Distrital de Barranquilla. Acuerdo N 006 del 10 de agosto
epidemiological behavior of cancer in Barranquilla has variations de 2006. Barranquilla; 2006.
with regards to what was found and reported during the previous
years in the country, although the risk of developing cancer or 9. Secretaría de Salud Pública Distrital. Plan de Salud Territorial del
dying due to it is considered intermediate when compared with distrito de Barranquilla 2008-2011. Alcaldía de Barranquilla; 2008.
the figures reported by other registries.
10. Secretaría Distrital de Salud. Análisis de Situación de Salud con
The estimates made for the 2008-2012 five-year period will serve el Modelo de los Determinantes Sociales de Salud 2012. Alcaldía
as a baseline for the construction of future trends. The information de Barranquilla; 2013.
generated by the BPCR provides a valuable contribution to the
11. Jensen O, Parkin D, MacLennan R, Muir C, Skeet R. Cancer
construction of reliable epidemiological information for the
registration: principles and methods. Scientific Publication N 95.
country, specifically in a representative city of the north coast
Lyon: IARC; 1991.
of Colombia, so that its sustainability must be guaranteed and
every day its objectives and strategies must be improved for both 12. OPS. Clasificación Internacional de Enfermedades para
medium and long term. Oncología. 3ª ed. Washington, DC: Organización Panamericana de
la Salud/Organización Mundial de la Salud; 2003.
Funding:
Universidad del Norte, Instituto Nacional de Cancerología. Code 13. Working Group Report. International rules for multiple
No. 0147 of 2017 primaries cancer. ICD-O third edition. Eur J Cancer Prev. 2005;
14(4): 307-8.
Conflict of interest:
None 14. Red Europea de Registros de Cáncer. Recomendaciones para la
codificación de la fecha de incidencia. Available from: http://www.
References encr.com.fr/incidspa.pdf. Accessed: octubre de 2017.

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and major patterns in GLOBOCAN 2012. Internat J Cancer. 2015; of data.  Springfield, IL: North American Association of Central
136(5): 359-386. Cancer Registries. 2004.

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assessment of 79 behavioural, environmental and occupational, and IARC; 2013.
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systematic analysis for the Global Burden of Disease Study 2013. 17. Sistema de Información de cáncer de Colombia. Tomado de:
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Lancet. 2015; 386(10010): 2287-2323.
18. Tanca J, Arreaga C. Incidencia del cáncer en Guayaquil 2003-
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Nacional de Cancerología-ESE, Ministerio de la Protección Social; 19. Saeed I, Weng H, Mohamed K, Mohammed S. Cancer incidence
2010. Available from: https://www.minsalud.gov.co/sites/rid/ in Khartoum, Sudan: first results from the Cancer Registry, 2009–
Lists/BibliotecaDigital/RIDE/IA/INCA/plan-nacional-control- 2010. Cancer Med. 2014; 3(4): 1075–1084.
cancer-2012-2020.pdf.
20. Ministerio de la Protección Social. Recomendaciones para
4. Pardo C, Duarte R. Incidencia estimada por cáncer en Colombia la tamización de neoplasias del cuello uterino en mujeres sin
2002-2006. Bogotá: Instituto nacional de Cancerología, 2010. antecedentes de patología cervical (preinvasora o invasora) en
Available from: http://www.cancer.gov.co/files/libros/archivos/ Colombia. Bogotá: Ministerio de la Protección Social-Instituto
incidencia1.pdf. Nacional de Cancerología; 2007.

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21. Martínez J, Martínez V. Protocolo de Vigilancia en Salud Pública: 26. Vargas R, Gámez H. Localidad de residencia como posible
Cáncer de mama y cuello uterino. Bogotá: INS, 2016. determinante de la incidencia de cáncer de mama en la ciudad de
Barranquilla. Rev Colomb Cancerología. 2017; 21(1): 76-77.
22. López G, Arias N, Arboleda W. Cancer incidence and mortality
in Manizales 2003-2007. Colomb Med (Cali). 2012; 43(4), 281-9 27. Villalón, J. Colonias extranjeras en Barranquilla. Barranquilla:
Colombia; 2008.
23. Uribe C, Osma S, Herrera V. Cancer incidence and mortality
in the Bucaramanga metropolitan area, 2003-2007. Colomb Med 28. Instituto Nacional de Cancerología, Sociedad Colombiana
(Cali). 2012; 43(4): 290-7.
de Urología. Guía de práctica clínica para la detección temprana,
24. Ministerio de Salud y Protección Social. Indicadores diagnóstico, tratamiento, seguimiento y rehabilitación del cáncer
de Mortalidad. Available from: http://rssvr2.sispro.gov.co/ de próstata. Guia n° GPC-2013-21. Bogotá: Ministerio de Salud y
reportesAsis2/. Accessed: October 2017. Protección Social; 2013.

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Colomb Med. (Cali) 49(1): 55-62

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Original articles

Health inequities and cancer survival in Manizales, Colombia: a population-based study


Inequidades en salud y supervivencia al cáncer en Manizales, Colombia: un estudio de base poblacional

Nelson Enrique Arias-Ortiz1, Esther de Vries2

1
Departamento de Salud Pública, Universidad de Caldas. Manizales, Colombia
2
Departmento de Epidemiologia Clinica y Biostadistica, Pontificia Universidad Javeriana. Bogotá, Colombia.

Arias-Ortiz NE, de Vries E. Health inequities and cancer survival in Manizales, Colombia: a population-based study. Colomb Med (Cali). 2018; 49(1): 63-72.
doi: 10.25100/cm.v49i1.3629

© 2018 Universidad del Valle. This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use,
distribution and reproduction in any medium, provided that the original author and the source are credited.

Article history: Abstract Resumen


Objective: To analyze differences in survival of breast, cervical, Objetivo: Analizar la supervivencia de pacientes con cáncer de
Received: 31 October 2017
Revised: 9 February 2018 lung, prostate and stomach cancer by health insurance regime mama, cuello uterino, pulmón, próstata y estómago según régimen
Accepted: 13 March 2018 (HIR) and socioeconomic position (SEP) in an intermediate city de aseguramiento en salud (RAS) y posición socioeconómica (PSE)
in a middle-income country. en una ciudad intermedia de un país de medianos ingresos.
Keywords: Methods: All patients with breast, cervix uteri, lung, prostate Métodos: Se incluyeron todos los pacientes con cáncer de mama,
Malignant neoplasms, and stomach cancer diagnosed between 2003 and 2007 and cuello uterino, pulmón, próstata y estómago diagnosticados entre
survival analysis, characterized by the Manizales population-based Cancer Registry 2003 y 2007 y caracterizados por el Registro Poblacional de Cáncer
socioeconomic factors, (MCR) were included and followed up to a maximum of 5 years for de Manizales, quienes fueron seguidos hasta un máximo de cinco
insurance, health
identifying deaths. Survival probabilities estimated by HIR were años para identificar los fallecimientos. Las probabilidades de
Palabras clave: defined according to the type of affiliation at the date of diagnosis, supervivencia estimada según RAS fueron definidas de acuerdo
neoplasias malignas, and by socioeconomic stratification of residence (SS) as indicator con el tipo de afiliación al momento del diagnóstico, y según el
análisis de sobrevida, of SEP, stratifying for other prognostic factors using Kaplan- estrato socioeconómico de la residencia como indicador de PSE,
factores socioeconómicos, Meier methods. Cox proportional hazard models were fitted for estratificando por otros factores pronósticos y utilizando el método
aseguramiento, salud
multivariate analysis. de Kaplan-Meier. Para el análisis multivariado se ajustaron modelos
Results: A total of 1,384 cases and 700 deaths were analyzed. Five- de riesgos proporcionales de Cox.
year observed survival was 71.0% (95% IC: 66.1-75.3) for breast, Resultados: Se analizaron en total 1.384 casos y 700 muertes. La
51.4% (95% IC: 44.6-57.9) for cervix, 15.4% (95% IC: 10.7-20.8) supervivencia observada a cinco años fue 71.0% (IC 95%: 66.1-
for lung, 71.1% (95% IC: 65.3-76.1) for prostate and 23.8% (95% 75.3) para cáncer de mama, 51.4% (44.6-57.9) para cuello uterino,
IC: 19.3-28.6) for stomach. Statistically significant differences 15.4% (10.7-20.8) para pulmón, 71.1% (65.3-76.1) para próstata,
in survival by HIR were observed for breast, lung, prostate, and y 23.8% (19.3-28.6) para estómago. Se observaron diferencias
stomach - with poorer survival for the subsidized and uninsured estadísticamente significativas en la supervivencia según RAS para
patients. Differences by SS were observed for lung and prostate. mama, pulmón, próstata y estómago, con supervivencia más pobre en
Differences in survival by HIR were independent of SS, and los pacientes del régimen subsidiado y no asegurados. Se observaron
viceversa. diferencias por estrato socioeconómico en los cánceres de pulmón y
Conclusions: Important inequities in cancer survival exist próstata. Las diferencias por RAS fueron independientes del estrato
related to HIR and SEP. Possible explanations include underlying socioeconómico y viceversa.
comorbidities, late stage at diagnosis, or barriers to timely and Conclusiones: Existen importantes inequidades en la supervivencia de
effective treatment. pacientes con cáncer relacionadas con el RAS y con la PSE. Las posibles
explicaciones incluyen comorbilidades subyacentes, diagnóstico tardío
y barreras para el acceso al tratamiento oportuno y efectivo.

Corresponding author:
Nelson Enrique Arias-Ortiz. ORCID: Carrera 25 Nº 48-57, Manizales, Caldas,
Colombia,. Sede Versalles Universidad de Caldas. Phone: +57 (6)8783060 ext
31255; +573125836563. https://orcid.org/0000-0001-5093-3384. E-mail: nelson.
arias@ucaldas.edu.co

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Introduction in breast, cervical, lung, prostate and stomach cancer survival


as a result of health insurance and socioeconomic status in this
Socio-economic differences in cancer survival have been well intermediate, Andean city in Colombia.
documented in the last two decades1. Disparities in stage at
diagnosis have been considered as the main underlying factor Materials and Methods
of those differences. However, there is evidence that differential
access to timely and adequate treatment by socio-economic groups Type of study
also determines cancer survival inequities1. Estimations of relative Exploratory population-based cohort study.
risk of dying comparing the most deprived groups with the best-off
Patients and follow up
groups have been around 1.3 to 1.5-fold; factors underlying these
All 1,482 patients resident in Manizales with breast, cervix uteri,
differences include tumour- and patient conditions, and access
lung, prostate or stomach cancer diagnosed between 2003 and
to and quality of care1. In countries with universal health care
2007 and characterized at baseline by Manizales’ Cancer Registry
insurance like Canada, socioeconomic position (SEP) remained
- MCR (information regarding data quality of MCR was published
associated with cancer survival, the differences are not being
previously19,22) were included: 380 female-breast cancer cases
due to stage at diagnosis2. Inequalities and inequities have been
(5 male cases were excluded), 226 cervix uteri, 230 lung, 296
reported for all cancer sites combined1, but also for specific sites
prostate, and 347 stomach cancer patients. The percentages of
including breast3, cervix4, lung5, prostate6 and stomach7,8 cancers.
microscopically verified cases were 95.8%, 96.9%, 78.6%, 92.5% and
For breast and cervical cancer, large differences were observed
89.4% for breast, cervix, lung, prostate, and stomach, respectively.
between developed and developing countries but also between
developed countries and within countries9. For female cancers, All cases were followed up until 60 months or until December 31th
place of residence, income, socioeconomic and educational level, 2013 since diagnosis for identifying the event of study (deaths due
ethnicity, and migration status have been associated with inequities to all causes) and time to event through matching personal identity
in survival9. numbers and names of incident cases with the local vital statistics
provided by the local health authority; also, we performed manually
In Colombia, health insurance financed through contributions of
searching in electoral rolls and health insurance databases. Active
both workers and employers (contributory regime) is mandatory
follow-up was performed by consultation of medical records where
for dependent employees and partially voluntary for independent
available. When only data for year was available, month and day
workers. A small proportion (<5%) of the population, working in
were assigned to June 30th. Patients without event were censored
certain public sectors, has exceptional or special health insurance
at five years of follow-up. Subjects were considered alive if they
plans (special or exceptional regime). The poor population is
were eligible to vote or if they were reported as “active” in health
covered by a subsidized health system founded through taxes
insurance databases on December 31th 2013. Survival time was
(subsidized regime)10. In 2005, contributory and subsidized
calculated as the difference between incidence date and date of
regimes covered 36.3% and 43.3% of the population, respectively,
death, date of last contact with health system, date of loss to follow
while about 20% of population had no health insurance11. In
up, or date they were censored. For incidence data, MCR uses rules
theory, special and contributory regimes offer the best access to
from European Network of Cancer Registries23.
care, but in practice special/exceptional regimes have shown some
problems that could make the conditions of its affiliates worse than Sixteen subjects with a clinical cancer diagnosis were lost to follow
those of the contributory regime12,13. Recent laws (years 201114 and up at day of diagnosis and were therefore treated the same as DCO
201515) have advocated for universal health care access without cases. There were 77 cases identified only by their death certificate
differences by SEP. However, those legislative changes have not (DCO), representing 5.2% of all cases (breast: n= 5 (1.3%); cervix
been fully implemented, and patients diagnosed prior to 2010 may uteri: n= 5 (2.2%); lung: n= 29 (12.6%); prostate: n=19 (6.4%)
have experienced different survival rates depending on their health and stomach: n=19 (5.5%). According to international registry
insurance status and their SEP. Large socioeconomic disparities in standards, a case is flagged as DCO when death certificate is the
gastric cancer survival were recently documented in other cities in only source of data for the case, i.e, there is no other data from
Colombia, despite improvements in health insurance coverage 8 and pathological reports, medical images, or hospitals. Since DCO
therefore it is not surprising that large inequities in population- cases by definition do not have information about time to event,
based cancer mortality exist17,18. Hardly any population-based they were excluded from survival analyses.
information by socioeconomic indicators is available for other
cities and other cancers in Colombia. Clinical and demographic characteristics
Information on histological subtype coded according to the
Manizales is a middle-size Andean city in Colombia with a projected International Classification of Diseases for Oncology, 3rd revision
population in 2005 (mid-term year) of 379,794 inhabitants 18. Since -ICDO-3- was available for 95.2% of cases; clinical stage at diagnosis
2003, the city hosts a population-based cancer registry that meets according to TNM system was available in usable proportions of
international standards proposed by IARC19  and has reported patients only for breast (62%) and cervix (42%) cancer. For other
incidence rates that are slightly higher than national estimations, sites, clinical stage was available in less than 30% of cases and could
mainly for breast, lung and stomach cancers20,21 - coinciding with therefore not be used. There were no patients with missing data
a higher smoker rate and position in the Andes. With incidences for age at diagnosis. More than 85% of patients had complete date
known, there is a need to evaluate population-based survival for of birth, and their ages in clinical records were consistent with
this population, and evaluate the effect of health insurance and SEP calculated ages. For patients without date of birth, age in clinical
on its survival rates. The aim of this paper is to analyze differences records was assumed as correct.

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Differences in diagnostic methods were observed only for CI: 46.4-51.7) for the five sites combined. By cancer site, 5-year OS
prostate and stomach cancers, which “only clinical” and “clinical were 71.0% (95% IC: 66.1-75.3), 51.4% (95% CI: 44.6-57.9), 15.4%
procedures” methods were observed only for patients in (95% CI: 10.7-20.8), 71.1% (95% CI: 65.3-76.1) and 23.8% (95%
contributory and subsidized regimes and uninsured, while 100% CI: 19.3-28.6) for breast, cervix uteri, lung, prostate, and stomach,
of the cancers diagnosed in patients affiliated to the special regime respectively (Table 1).
were histologically confirmed.
Statistically significant differences in survival by HIR were
Socioeconomic indicators observed for breast, lung, prostate, and stomach - with poorer
Variables for socioeconomic position and health insurance were survival for the subsidized and uninsured patients. Differences by
defined following categories previously used for a Colombian SS were observed for lung and prostate. (Figs. 1 and 2). One and
population by de Vries et al8. Socioeconomic stratum (SS) of the five-years OS proportions were significantly lower in uninsured
place of residence at diagnosis was used as indicator of SEP. In or subsidized patients versus patients with special or contributory
Colombia, SS is defined according to external and internal physical HIR, with exception of cervix uteri cancer. Regarding SS, differences
characteristics of dwellings and wards, ranging from the purely statistically significant were only observed in lung and prostate
functional and indispensable to the aesthetic, ornamental and cancers, with poorer survival proportions in patients for low/
sumptuous characteristics. SS is reported in categories from 1 to middle versus high SS and low versus middle/high SS, respectively.
6, where 1 and 2 corresponds to “low” social stratum, 3 and 4 to However, survival proportions for cervix uteri and lung cancer of
“middle”, and 5 and 6 to “high”. patients affiliated to the special/ exceptional HIR were lower than
in the other categories, even lower than in uninsured population.
Health Insurance Regime (HIR) at the date of diagnosis was used
grouping the special and exceptional regimes into one unique As expected, overall survival was higher in younger patients for all
category, contributory regime, subsidized regime, and a group of sites studied, but those differences were not statistically significant.
uninsured people. According to literature, clinical stage at diagnosis showed a strong
association with survival (Table 1 and Fig. 3). Survival was better
Statistical analysis for women diagnosed with ductal breast carcinoma vs. other
Observed survival proportions at different times were obtained histological subtypes. Non-significant differences in survival
using Kaplan-Meier analyses, stratifying analyses by HIR and SS, were observed by histological subtypes of cervix, lung, prostate
age, sex, histological subtype and, for breast and cervical cancer and stomach cancers. For lung and stomach cancers no survival
only, clinical stage at diagnosis. Cox multivariate proportional differences by sex were observed.
hazard assumption was checked by visual evaluation of log-log
plots; the assumption was not violated. Three Cox multivariate Table 2  shows results from Cox models by HIR and SS and by
regression models for each cancer were fitted for both HIR and SS: cancer site. For prostate cancer, HIR hazard ratios (HR) remained
i) a univariate (null) model; ii) a multivariate model A with age, sex significant after adjusting for age and histological subtype, with
(lung and stomach), histological subtype, and clinical stage (breast lower hazard of dying for special HIR group in comparison with
and cervix) as covariates ; and iii) a model B containing all variables the subsidized regime (HR: 0.17 (95% IC: 0.04-0.80)). These results
of model A plus an additional term for SS in the HIR model and remained significant in multivariate analyses. For stomach cancer,
vice versa8. All calculations were performed using STATA™ SE 12.0. patients in contributory regime had better survival in all, univariate
and multivariate, models, with about 30% lower hazard of dying
Ethical considerations in comparison with patients in subsidized HIR. With respect to
This research was approved by the Research Ethics Committees of socioeconomic position, prostate cancer patients from middle SS
the Universidad del Valle, Universidad de Caldas, and the National showed about 47% lower hazard of dying than patients from low
Cancer Institute of Colombia. SS (HR 0.53, 95% CI: 0.31-0.88), independently of health insurance
regime. Other sites did not reach statistical significance, possibly
Results due to the low number of cases in each group.
Patient and tumour characteristics for all 1,405 incident cases are Unsurprisingly, advanced clinical stages for breast and cervix had
shown in Supplementary Table 1S. increased HRs. In line with the Kaplan-Meier results, cervical
cancer patients affiliated to the special regime had a higher hazard
For the five cancer sites studied, 1,384 cases were finally analyzed.
than women affiliated to the subsidized regime after adjusting by
Lost of follow-up was 1.7% for five sites studied (0.8% for breast,
age, histological subtype and clinical stage.
2.3% for cervix, 1.9% for lung, 1.8% for prostate, and 2.1% for
stomach). In Manizales, HIR coverage among cancer patients was Model B showed that inclusion of both terms HIR and SS in the
88.8%, except for gastric cancer, in which 18.3% had no affiliation same model modified HR estimates in all cancers combined and
to HIR. Breast and prostate patients without HIR tended to be older by cancer site, indicating independent effects of HIR and SS on
at diagnosis than affiliated, but differences were not statistically survival.
significant.
Discussion
At five-years follow-up, 700 deaths (all causes) were observed.
Mean follow-up time for overall sites was 38.4 months (95% CI: This population-based study on population-based survival for
37.2; 39.7), varying from 18.5 months for lung to 50.8 months for five cancer sites in Manizales, Colombia, demonstrated significant
breast cancer. Five-year observed survival (OS) was 49.1% (95% differences in observed survival. Differences by HIR varied from 8

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Table 1. Survival estimations by cancer site and prognostic factors. Manizales, 2003-2013
Proportion surviving after (%)
Cases (n) Deaths (n) WBG test*
12 m 36 m 60 m
All cases 375 108 93.8 81.0 71.0
Age at diagnosis
0 a 49 116 29 96.5 85.2 74.8 X2=1.63
50+ 258 79 92.6 79.1 69.3 p=0.20
Histology
Breast Ductal Ca. 307 82 95.1 83.1 73.3 X 2 =6.19
Other and NOS 67 26 87.9 71.2 60.4 p=0.013
Clinical stage
Stage I 25 0 100.0 100.0 100.0 X 2 =80.76
Stage II 97 5 100.0 96.9 94.9 p=0.000
Stage III 82 19 100.0 89.0 76.8
Stage IV 29 11 93.1 69.0 55.2
Unknown 141 71 85.0 64.3 49.2
All cases 220 105 80.7 62.1 51.4
Age at diagnosis
0 a 49 101 42 83.0 68.0 58.0 X2=2.40
50+ 119 63 78.7 57.1 45.8 p=0.121
Histology
Squamos cell Ca. 167 80 80.1 60.7 51.6 X2= 1.99
AdenoCa. 38 16 83.9 70.3 56.8 p=0.369
Cervix
Other and NOS 15 9 79.4 57.8 36.1
Clinical stage
Stage I 16 2 100.0 93.8 87.5 X 2 = 13.75
Stage II 36 16 91.7 69.4 55.6 p=0.008
Stage III 30 19 80.0 53.3 36.7
Stage IV 13 10 69.2 38.5 23.1
Unknown 125 58 76.3 60.5 52.2
All cases 198 165 43.6 21.0 15.4
Sex
Women 81 67 50.6 28.4 17.3 X2= 3.25
Men 117 98 38.7 15.8 14.1 p=0.071
Age at diagnosis
0 a 59 59 46 40.7 27.1 22.0 X2=0.94
Lung
60+ 139 119 44.9 18.4 12.5 p=0.331
Histology
Squamous cell Ca. 71 54 49.3 22.5 16.9 X2=5.96
AdenoCa. 53 44 37.3 17.7 13.8 p=0.113
Small cell Ca. 16 13 56.3 31.2 18.7
Other and NOS 58 49 38.6 19.3 14.0
All cases 270 78 92.2 78.9 71.1
Age at diagnosis
0 a 59 43 8 95.4 83.7 81.4 X2=2.05
Prostate 60+ 227 70 91.6 77.8 69.2 p=0.152
Histology
Adeno Ca. 257 70 92.3 79.4 72.2 X2=2.30
Other and NOS 18 8 83.3 72.2 55.6 p=0.129
All cases 322 244 49.4 33.1 23.8
Sex
Women 114 83 57.6 39.0 26.6 X2=1.31
Men 208 161 44.9 30.0 22.2 p=0.252
Age at diagnosis
0 a 59 112 86 48.2 32.1 23.2 X2=0.03
Stomach
60+ 210 158 50.0 33.7 24.1 p=0.857
Histology
Adeno Ca, intestinal 146 111 54.5 33.8 23.5 X2=2.01
Difuse Ca. 73 59 41.7 26.4 18.1 p=0.569
Adeno Ca., others 48 35 47.9 37.5 27.1
Other and NOS 55 39 47.3 36.4 29.1
NOS: Non other specification *WBG: Wilcoxon -Breslow-Gehan test.

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Breast Cerviz uteri

1.00

1.00
0.75

0.75
Survival proportion

Survival proportion
0.50

0.50
0.25

0.25
WBG test = 9.6; p=0.035 WBG test = 6.1; p=0.108

0.00

0.00
0 20 40 60 0 20 40 60
Months Months
Special Contributory Special Contributory
Subsidized Not insurance Subsidized Not insurance

Lung Prostate

1.00
1.00
WBG test = 12.7; p=0.005

0.75
0.75

Survival proportion
Survival proportion

0.50
0.50

0.25
0.25

WBG test = 7.9; p=0.048

0.00
0.00

0 20 40 60 0 20 40 60
Months Month
Special Contributory Special Contributory
Subsidized Not insurance Subsidized Not insurance

Stomach
1.00

WBG test = 9.9; p=0.019


0.75
Survival proportion
0.50
0.25
0.00

0 20 40 60
Months
Special Contributory
Subsidized Not insurance

Figure 1. Observed survival by health insurance regime and cancer site. Manizales, 2003-2013. WBG:
Wilcoxon-Breslow-Gehan test.
Breast Cervix uteri
1.00
1.00

0.75
0.75
Survival proportion

Survival proportion
0.50

0.50
0.25

0.25

WBG test= 2.6; p=0.27


WBG test = 1.6; p=0.44
0.00

0.00

0 20 40 60 0 20 40 60
Months Months
High Intermediate Low High Intermediate Low

Lung Prostate
1.00
1.00

WBG test = 6.5; p=0.039


0.75
0.75

Survival proportion
Survival proportion

0.50

0.50
0.25

0.25

WBG test = 7.2; p=0.027


0.00

0.00

0 20 40 60 0 20 40 60
Months Months

High Intermediate Low High Intermediate Low

Stomach
1.00

WBG test = 3.2; p=0.198


0.75
Survival proportion
0.50
0.25
0.00

0 20 40 60
Months
High Intermediate Low

Figure 2. Observed survival by social strata and by cancer site. Manizales, 2003-2013. WBG:
Wilcoxon-Breslow-Gehan test.

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percent-points in stomach to 32 percent-points in prostate cancer. In general, 5-year OS by site was below that observed for most
Hazard Ratios estimated for HIR were in line with risks reported countries in the CONCORD27  and EUROCARE28  studies.
in other studies1. Absolute differences by SS were less noticeable, Disparities by HIR and SS for breast, prostate and stomach cancers
with differences between low versus high categories of about 16 were similar to reported by literature29-33.
percent-points for prostate, 10 for breast, 14 for cervix, 5 for lung, The survival proportion for women with a cancer of the cervix uteri
and 11 percent-points for stomach cancers. The magnitude of these was 3-fold lower among women affiliated to the special regime
disparities is similar with those found in U.S for the last quarter of compared to the other HIR groups. This surprising results - special
the past century24. regimes have, in theory, the most generous health care plan - are
in line with the observation of the worst stage at diagnosis in this
Colombian health system was radically reformed at the end of
group, which suggest that screening and early detection programs
the last century, resulting in a substantial increase in coverage of are not properly working in special regime entities. Regarding
health insurance which reached almost 100% around 2010. On socioeconomic stratification, survival rates or cervical cancer were
paper, this meant a substantial improvement in access to health 7 and 14 percent-points higher in low and middle social strata,
services. However, timely access to health care in cancer diagnosis respectively, in comparison with the richest group. Incidence rates
and treatment is still problematic, particularly because of the high were lower in the richest group, and the relative low frequency of
out-of-pocket cost and long waiting times to obtain permission to disease among the wealthiest part of the population may result in
use these services. In Colombia, access to health care is differential a lower awareness or lower participation rates in screening and
according to the health insurance regime, and inequities persist early treatment programs for cervical cancer. However, differences
between types of affiliation. Local researchers have pointed out that in clinical stage at diagnosis did not reach statistical significance -
universality in National Health System has not been achieved and perhaps because number of cases in the high strata was very low
there has been a stagnation in matters regarding access to services (see supplementary table). In this regard, Brookfield et al.34, found
and equality25. Additionally, enormous regional disparities have that, in women living in the state of Florida (USA), the independent
been described in Colombia, and the country has one of the worst predictors of poorer outcomes were insurance status, tumor stage,
distributions of per capita income in the world26. tumor grade, and treatment. Neither race, nor ethnicity, nor SES

Breast
1.00
0.75
Survival proportion

0.50
0.25
0.00

0 20 40 60
Months
Stage I Stage II Stage III Stage IV

Cervix uteri
1.00
0.75
Survival proportion

0.50
0.25
0.00

0 20 40 60
Months
Stage I Stage II Stage III Stage IV

Figure 3. Survival proportion by clinical stage at diagnosis for breast cancer (based on 233 cases
with known clinical stage) and cervix uteri cancer (based on 95 cases). Manizales, 2003-2013.

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Table 2. Proportional risks (Cox) survival models by cancer site.


Univariate analysis Multivariate analysis
Model A Model B
HR IC 95% HR 95% CI HR 95% CI
Health insurance *
Contributory 0.77 0.47-12.7 0.71 0.43-1.17 0.77 0.44-1.36
Special 0.89 0.38-2.09 0.47 0.20-1.13 0.52 0.20-1.34
Not insured 1.66 0.84-2.26 1.27 0.64-2.55 1.41 0.65-3.07
Breast cancer Cases (events) 370 (108) 370 (108) 345 (99)
Social Strataa
Middle 0.88 0.57-1.35 0.75 0.48-1.17 0.93 0.56-1.55
High 0.61 0.33-1.14 0.65 0.35-1.21 0.84 0.42-1.65
Cases (events) 347 (99) 347 (99) 345 (99)
Health insurance *
Contributory 0.78 0.51-1.22 1.76 0.85-3.64 2.12 0.99-4.55
Special 2.20 0.85-5.68 5.02 1.69-14.9 7.60 1.94-29.7
Not insured 0.92 0.46-1.81 0.94 0.25-3.58 0.90 0.23-3.51
Cervical cancer Cases (events) 217 (104) 92 (46) 87 (43)
Social Strataa
Middle 0.78 0.50-1.22 0.91 0.47-1.76 0.67 0.32-1.41
High 1.20 0.55-2.62 0.84 0.19-3-65 0.38 0.08-1.87
Cases (events) 197 (95) 88 (44) 87 (43)
Health insurance *
Contributory 0.69 0.47-1.02 0.75 0.51-1.12 0.89 0.58-1.36
Special 1.15 0.61-2.19 1.22 0.64-2.32 1.28 0.66-2.49
Not insured 1.04 0.54-2.01 1.32 0.66-2.62 1.77 0.83-3.77
Lung cancer Cases (events) 197 (165) 197 (165) 186 (157)
Social Strata a

Middle 1.00 0.72-1.39 0.99 0.71-1.38 1.03 0.74-1.46


High 0.58 0.32-1.05 0.60 0.33-1.09 0.67 0.36-1.24
Cases (events) 186 (157) 186 (157) 186 (157)
Health insurance *
Contributory 0.58 0.28-1.21 0.56 0.27-1.18 0.56 0.26-1.21
Special 0.17 0.04-0.80 0.20 0.04-0.95 0.12 0.02-0.99
Not insured 0.89 0.33-2.37 0.74 0.27-2.02 0.81 0.27-2.41
Prostate cancer Cases (events) 266 (77) 266 (77) 233 (70)
Social Strataa
Middle 0.52 0.31-0.87 0.53 0.31-0.88 0.54 0.32-0-92
High 0.63 0.32-1.26 0.71 0.36-1.44 0.78 0.38-1.60
Cases (events) 237 (71) 237 (71) 233 (70)
Health insurance *
Contributory 0.72 0.52-0.98 0.71 0.52-0.98 0.70 0.51-0.98
Special 0.70 0.36-1.38 0.72 0.36-1.41 0.75 0.38-1.50
Not insured 0.93 0.62-1.39 0.93 0.62-1.39 1.01 0.65-1.56
Stomach cancer Cases (events) 320 (243) 320 (243) 289 (221)
Social Strataa
Middle 0.80 0.61-1.06 0.80 0.60-1.05 0.82 0.62-1.09
High 0.75 0.46-1.20 0.76 0.47-1.23 0.89 0.55-1.45
Cases (events) 291 (222) 291 (222) 289 (221)
* Subsidized regime as reference a Low strata as reference. Models were adjusted by age, sex (lung and stomach), histological subtype, and stage at diagnosis (breast and cervix).

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was an independent predictor of poorer outcome. Similarly, Niu et Conclusions


al.35, found no significant differences in cervical cancer survival by
insurance status in New Jersey. Important inequities in cancer survival exist in Manizales related
to health insurance and socioeconomic position. Differences may
For lung cancer, 2.3 and 2-fold better survival rates were observed in be attributed to inequities in comorbidities, stage at diagnosis,
patients from contributory, subsidized and non-insured categories or barriers to timely access to effective treatment suggested by
in comparison with special regimes. These results are contradictory differences observed between health insurance regimes.
with those reported in US36 where uninsured and Medicaid patients
had poorer survival than patients with private insurance. This Acknowledgements:
pattern may be reflecting barriers to early diagnosis and treatment in We would like to thank the Local Health Authority in Manizales
this subgroup, which in Manizales is mostly composed by teachers, for providing death data, and to the National Cancer Institute for
and army and police members. However, this should be confirmed the technical and financial support to this research. To Manizales’
by studies with a larger number of patients. Survival proportions Cancer Registry staff for the cooperation to complete data, and all
were around five percent-points lower in the lowest socioeconomic the sources of MCR for allowing data query. To medical institutions
stratum in comparison with the most affluent group, which is in Manizales for their cooperation in data collection.
consistent with figures reported by Ou et al37.
Funding:
Disparities in cancer survival related to the health system can This study was funded by the National Cancer Institute of Colombia
be attributed to barriers and delays in obtaining diagnostic care, and University of Caldas through inter-administrative contract
associated with more advanced stages at diagnosis. In Colombia, number 0365-2014.
practically all medical procedures require authorization from the
insurer, which in many cases lead to substantial diagnostic and Referencias
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40. Tervonen HE, Roder D, Morrell S, You H, Currow DC.
38. Martinez S, Segura A, Arias S, Mateus G. Caracterización de los Does exclusion of cancers registered only from death-certificate
tiempos de atención y de mujeres con cáncer de mama que asistieron information diminish socio-demographic disparities in recorded
a un hospital de tercer nivel, 2005-2009. Rev Fac Nac Salud Pública. survival? Cancer Epidemiol. 2017;48:70-7.
2012;30(2):183-91.

Colomb Med. (Cali) 49(1): 63-72

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Original article

Cancer incidence and mortality in Bucaramanga, Colombia. 2008-2012


Incidencia y mortalidad por cáncer en Bucaramanga, Colombia. 2008-2012

Claudia Janeth Uribe Pérez1,2, Sergio Eduardo Serrano Gómez4, Claudia Milena Hormiga Sánchez3

1
Grupo de investigación Estudio Genético de Enfermedades Complejas, Universidad Autónoma de Bucaramanga. Bucaramanga, Colombia.
2
Directora del Registro Poblacional de Cáncer del Área Metropolitana de Bucaramanga. Bucaramanga, Colombia.
3
Grupo de investigación Observatorio de Salud Pública de Santander, Fundación FOSCAL- Universidad Autónoma de Bucaramanga. Bucaramanga, Colombia
4
Grupo de investigación Investigaciones Clínicas UNAB, Universidad Autónoma de Bucaramanga. Bucaramanga, Colombia

Uribe PCJ, Serrano GSE, Hormiga SCM. Cancer incidence and mortality in Bucaramanga, Colombia. 2008-2012. Colomb Med (Cali). 2018; 49(1): 73-80.
doi: 10.25100/cm.v49i1.3632.

© 2018 Universidad del Valle. This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use,
distribution and reproduction in any medium, provided that the original author and the source are credited.

Article history Abstract Resumen


Introduction: Cancer is a huge burden worldwide, especially for the
Received: 5 November 2017 least developed countries. Population-based cancer registries (PB­CRs) Introducción: El cáncer constituye una carga en el mundo, en especial
Revised: 16 January2018
are essential to know the cancer territorial profiles and the evaluation of para los países menos desarrollados. Los Registros Poblacionales de
Accepted: 15 March 2018
the impact of their control programs. Cáncer son fundamentales para conocer los perfiles territoriales del
Keywords: Aim: To estimate the cancer incidence and mortality in the Metropolitan cáncer y la evaluación del impacto de sus programas de control.
Cancer, incidence, mortality, Area of Bucaramanga over the period 2008-2012. Objetivo: Estimar la incidencia y mortalidad por cáncer en el Área
Records, Bucaramanga. Methods: A descriptive study of cancer incidence and mortality was Metropolitana de Bucaramanga en el período 2008-2012.
conducted in the Metropolitan Area of Bucaramanga. The cases of Métodos: Se realizó un estudio poblacional descriptivo de la incidencia
Palabras clave: primary invasive cancer from the period 2008-2012 were obtained from y mortalidad por cáncer en el Área Metropolitana de Bucaramanga. Los
Cáncer, incidencia, the base of the Population Registry of Cancer of the Metropolitan Area casos de cáncer invasivos primarios del periodo 2008-2012 se obtuvieron
mortalidad, registros,
of Bucaramanga. The National Administrative Department of Statistics de la base del RPC-AMB. Los datos de población y defunciones fueron
Bucaramanga.
provided population and death data. Crude rates of global and specific facilitados por el Departamento Administrativo Nacional de Estadística
incidence and mortality were estimated for each sex, and standardized (DANE). Se estimaron tasas crudas de incidencia y mortalidad globales
incidence and mortality rates. y específicas por sexo, y tasas de incidencia y mortalidad estandarizadas.
Results: During the five-year period, 8,775 incidents cases of cancer Resultados: Durante el quinquenio se registraron 8,775 casos incidentes
were recorded (excluding non-melanoma skin cancer). The global de cáncer (excluyendo cáncer de piel no melanoma). Las tasas de
standardized incidence rate was 151.7 per 100,000 men-year and 157.2 incidencia estandarizada globales por 100,000 personas-año fueron
per 100,000 women-year. The main locations were prostate, stomach de 151.7 en hombres y 157.2 en mujeres. Las principales localizaciones
and colorectal men in men, and breast, thyroid and colorectal in women. fueron próstata, estómago y colorrecto, en los hombres, y mama,
The standardized mortality rate by sex was 94.8 per 100,000 men-year tiroides y colorrecto en las mujeres. La tasa de mortalidad estandarizada
and 78.0 per 100,000 women-year. por 100,000 personas-año fue de 94.8 en hombres y de 78.0 en mujeres.
Conclusion: For the most part of neoplasms, the incidence and Conclusión: Las tasas de incidencia y mortalidad en la mayoría de
mortality rates in the Metropolitan Area of Bucaramanga are lower than localizaciones son inferiores a las nacionales y al quinquenio previo en el
the rates reported in Colombia and Metropolitan Area of Bucaramanga Área Metropolitana de Bucaramanga. El cáncer de tiroides, colorrectal,
in the five-year period 2003-2007, except for colorectal cancer, thyroid y las leucemias muestran una tendencia al aumento, lo cual demanda
cancer and leukemia showing a tendency to increase, which requires indagaciones posteriores.
further investigation.

Corresponding author:
Claudia Janeth Uribe Pérez. Universidad Autónoma de Bucaramanga.
Av. 42 #48 – 11. E-mail: curibep@unab.edu.co
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Introduction Geographic area


Metropolitan Area of ​​Bucaramanga is a geographical area made up
Cancer represents a huge burden in the world, causing about 14.1 of four municipalities in the province of Santander: Bucaramanga
million new cases and 8.2 million deaths in 2012. The burden of cancer (its capital city), Floridablanca, Girón and Piedecuesta. It is
is increasing in less developed countries, from which about 57% of the located in the Andean region and it has an area of ​​1,479 km2. Each
new cases come up as well as 65% of the deaths caused by this disease. municipality is independent in its political organization, but they
It is estimated that 48% of prevalent cases of cancer at five years of are completely related from an economic and social perspective14.
diagnosis occur in the regions with less economic development1,2.
According to population projections of DANE, AMB had 1,074,000
The incidence of cancer is increasing. It is expected that by 2025, inhabitants at the middle of the 2008-2012 period (53.5% of the
there will be more than 20 million new cases, and a greater burden provincial total); 94.3% were urban residents, 51.9% were women,
in low and middle income countries3,4. This trend is attributed to 24.5% were aged under 15 years, and 20.4% were older than 50
the growth and aging of the population, as well as to a growing years15.
prevalence of clearly established risk factors, such as smoking,
overweight, physical inactivity and changes in reproductive patterns AMB is an important reference center for the care of cancer patients
associated with urbanization and economic development1,2. in the northeastern part of the country, with state (hospitals) and
private institutions (clinics, specialized medical centers, diagnostic
To generate impact on the reduction of the problems generated by centers, oncology centers and medical specialists in all areas) that
this disease, the World Health Organization (WHO) promotes the provide various oncological services for diagnosis and treatment.
creation of effective programs that improve early detection, timely
diagnosis, and a specific and effective treatment5. The Population Registry of Cancer of the Metropolitan Area of​​
Bucaramanga (RPC-AMB)
It also leads cancer control programs with the promotion of RPC-AMB has carried out permanent activities since April 2000, as
national cancer control policies, plans and programs. One of the a result of the commitment assumed by La Universidad Autónoma
strategies has been the promotion, establishment and strengthening de Bucaramanga).  The economic resources are assigned in the
of the monitoring and evaluation of this disease through registries, research calls of the university, and it receives annual co-financing
as well as research aimed at the burden of the disease, as well as from the INC.
increasing the availability of resources for its care6.
Method of data collection and processing
Population Cancer Registries (RPC, for its initials in Spanish) are
RPC-AMB makes active collection of incident cases through
essential information systems for cancer control programs; these
periodic visits to information sources: pathology and hematology
allow determining frequencies, incidences, mortality and trends,
laboratories, hospital discharges, imaging centers, screening
which are the result of activities aimed at collecting, analyzing
centers, volunteer programs, oncology centers, medical specialists,
and continuously disseminating information on cancer cases that
autopsies and certificates of deaths that are obtained in the
occur in a specific population, with guarantee of the quality of the
Provincial Health Secretariat.
data (completeness, precision, and comparability)7,8.
A recordable case is any malignancy of any location including
In Colombia there are four RPC with international recognition. One
benign neoplasms of the Central Nervous System (CNS) and
of these is the Population Registry of Cancer of the Metropolitan Area
of ​​Bucaramanga (RPC-AMB), which has managed to consolidate a carcinomas in situ that have been diagnosed after January 1 of
continuous work during 18 years of operation9,10. the year 2000 in residents of AMB, both in urban and rural areas,
regardless of the diagnostic method used, so that cases identified
With the leadership of the Ministry for Health and Social by death certificate are also included. It excludes non-melanoma
Protection, the National Cancer Information System was set up skin cancer (basal cell and squamous cell).
and the National Cancer Observatory for Colombia was created,
led by the National Cancer Institute of Colombia (INC, for its The cases obtained by hospital discharge and death certificates
initials in Spanish), in order to know the territorial profile and follow a process of verification of the diagnosis, through the search
evaluate the impact of cancer control programs11. Population of the clinical history. When no additional information is obtained
Cancer Registries are a fundamental part of this initiative  12; from the case obtained by the death certificate, it is recorded as a case
through them, the epidemiology of the disease can be known; and identified only by its death certificate (death certificate only - DCO).
also the rate progress is being made in terms of fulfilling one of the
pillars of the Ten-Year Plan for Cancer Control13. The coding of cancer cases is carried out under the supervision
of the RPC Director, by personnel trained in the International
This study describes the total and specific incidence and Classification of Diseases for Oncology (ICD-O) - 3rd edition, 1st
mortality rates by sex, corresponding to the Metropolitan Area of​​ revision, published by the World Health Organization (WHO) ) in
Bucaramanga during the period 2008-2012. 2013, and the IARC criteria for multiple primary tumors16,17.

Materials and Methods RPC-AMB complies with confidentiality standards following the
parameters of the IARC and the research commitment ethics.
A descriptive population study was proposed, with the incident Only the staff of RPC-AMB accesses the information of each case,
cases of invasive cancer registered in the databases of the RPC- which allows exhaustive work in the control of the duplicity of the
AMB in the quinquennium 2008-2012. information8,18.

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The source of information on deaths was DANE, the official entity that around 55 years of age, with a magnitude 60% lower than that of
collects, organizes and codifies the basic causes of mortality using the breast cancer at this age (Fig. 1). In men, the incidence of gastric
tenth revision of the International Classification of Diseases (ICD 10)19. cancer increases after 30 years of age, and that of the prostate
increases after 40 years of age, but the latter presents a much steeper
The CanReg5 program20, designed for the RPC by the IARC, was upward curve, almost tripling the incidence of gastric cancer at 80
used to systematize the information of the incident cases, which years of age (Fig. 2).
allows eliminating duplicates and identifying multiple primary
tumors. Additionally, the data is also validated with the IARC During the 2008-2012 quinquennium, of 24,860 deaths registered in
Tools and Registry Plus™ Link Plus programs20,21. AMB, 4,998 (20.1%) corresponded to malignant neoplasms; 50.2%
occurred in women. For the general population, the mortality rate
For the estimation of the incidence rates, the population of the ardized by cancer was 84.6 per 100,000 persons-years. The most
AMB of the study period, projected by DANE, was used as the frequent cancers were: stomach (13.9%), lung (11.4%), colorectal
denominator. Crude and standardized rates were calculated by (9.0%), breast (7.1%), prostate (6.0%), leukemia (5.3%), liver
direct method using the global standard population proposed by (5.1%), lymphoma (5%), cervix (3.8%) and pancreas (3.5%).
Segi and corrected by Doll22. The analyses were performed in Stata
1423 and the program CanReg5©, version 5.00.42, software created Women had a standardized mortality rate by age of 78.0 per
by the International Agency for Research on Cancer (IARC), 100,000 women-year. The cancers that caused the greatest number
in collaboration with the International Association of Cancer of deaths were breast (13.3%), stomach (11.8%), colorectal (9.4%),
Registries (IACR), available for free all members of the IACR24. lung (8.7%), cervix (7.1%), liver (4.8%), leukemia and lymphomas.
(4.7% each). In men, the mortality rate standardized by age was
Results 94.8 per 100,000 men-year, cancers of stomach (15.9%), lung
(14.1%) and prostate (12.4%), colorectal (8.0%), liver (5.4%),
During the 2008-2012 quinquennium, there were 8,775 incident leukemia (6.0%) and lymphoma (5.4%) (Table 3 ).
cases of cancer in AMB (excluding non-melanoma skin cancer);
(57.2%) occurred in women, (84.2%) were verified by microscopy Discussion
(cytology, hematology or pathology), (7.6%) were detected only
by death certificate, and (7.2%) by clinical history (Table 1). The This study presents the results of cancer incidence and mortality in
percentage of cases identified by microscopy was higher in women the quinquennium 2008-2012, thus providing continuity with the
than in men (88.0 and 81.4 respectively p <0.0001); in contrast, data for the 2003-2007 quinquennium25. In general, the quality of
the percentage of cases identified by death certificate was higher in the data analyzed was better than for the previous quinquennium,
men than in women (9.1 and 6.5 p <0.0001). because the percentage of cases that were detected only by death
certificate decreased.
The average age at diagnosis was 57.3 years in women and 61.8
years in men (p  <0.0001). The location of the most frequent In the interpretation of data, it is important to bear in mind that the
malignant tumors in women were breast (26.1%), colorectal classification of the cases used in the current study was based on the
(9.1%), thyroid (9.1%), cervix (8.3%) and stomach (6.9%). In men, first revision of the ICD-O-3, which includes changes in the codes
the most frequent cancers were: prostate (26.1%), stomach (11.4%), related to the behavior of some tumor lesions and morphological
colorectal (9.4%), trachea bronchi and lung (6.7%), lymphoma and codes of hematolymphoid and central nervous system neoplasms,
myeloma (6.2%) (Table 2). which were not taken into account in the analysis of the previous
quinquennium.
Rates are expressed per 100,000 persons-years. The cancer
incidence rate standardized by age (ASR) was 151.7 in men, and When compared with the 2003-2007 quinquennium, the average
157.2 in women. The standardized rates of the five most frequent age at diagnosis moment was similar for both sexes. The total
cancers in men were prostate (40.9), stomach (17.1), colorectal number of new cases (excluding non-melanoma skin cancer)
(14.3), lung (10.3) and lymphoma (9.1). In women, they were increased 6.7%, as well as the percentage representation of women,
breast (41.2), thyroid (14.5), colorectal (13.7), cervix (13.0) and which went from 54.3% to 57.2%. However, the overall incidence
stomach (10.2). rate in men and women decreased, especially in men, because the
male/female ratio (m/f) was 1.0, showing a behavior contrary to
In women, the five tumor sites with a percentage of microscopic that reported by the Population Registry of Cali Cancer (RPCC,
diagnosis greater than 95.2% were: thyroid, lymphoma, leukemia, for its initials in Spanish) for the same period (ratio m/f of 1.1)26,
kidney and breast. In men, they were skin melanoma, leukemia, but similar to the behavior reported for previous years in countries
lymphoma, bladder and thyroid. The type of cancer with the such as Ecuador, Peru and Mexico27.
highest percentage of diagnosis by death certificate was: liver
(31.9% in women and 35.6% in men), pancreas (31.1% in women The standardized rates of incidence in the 2008-2012 period in AMB
and 33.3% in men) and lung (23.5% in women and 21.9% in men). were lower than those reported by RPCC in the same period26, as
well as those of the South American population (206.7 per 100,000
The behavior of the age-specific incidence of the two most frequent men-year and 180.6 per 100,000 women-year)27  and worldwide
types of cancer in women is different. Breast cancer rises sharply (182.0 per 100,000 men-year and 165.2 per 100,000 women-year) 26.
since the end of the third decade of life, reaching its peak at around
70 years of age; in contrast, the incidence of thyroid cancer begins Breast cancer was the most frequent in women from AMB, with
in the middle of the second decade of life, and reaches its peak at percentage representation and standardized incidence rate similar

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Table 1. Quality index by cancer location and sex. Metropolitan Area of ​​Bucaramanga, 2008-2012.
Men Women
Place CIE-10
n % DCO % MV n % DCO % MV
Oral cavity and pharynx 116 5.2 91.4 69 1.4 88.4 C00-C14
Esophagus 43 16.3 79.1 29 20.7 72.4 C15
Stomach 427 6.6 89.5 345 11.3 82.6 C16
Colorectal 353 5.9 91.0 457 4.8 92.3 C18-C21
Liver 90 35.6 46.7 69 31.9 44.9 C22
Pancreas 54 33.3 37.0 61 31.1 37.7 C25
Lung 251 21.9 66.1 200 23.5 64.0 C33-C34
Melanoma, skin 59 0.0 100.0 53 3.8 92.5 C43
Breast 12 8.3 83.3 1,309 1.4 95.3 C50
Cervix 0 - - 418 3.8 91.6 C53
Others in uterus 0 - - 222 4.1 94.1 C54-C55
Ovary 0 - - 215 8.4 85.1 C56
Prostate 980 7.3 76.8 0 - - C61
Urinary Bladder 83 3.6 95.2 39 5.1 87.2 C67
Thyroid 66 0.0 93.9 456 1.5 97.4 C73
Lymphoma 231 1.3 96.1 225 0.9 97.3 C81-C90;C96
Leukemia 180 1.7 96.1 151 2.6 96.7 C91-C95
Others 795 12.7 75.0 672 15.5 70.9
All locations without skin 3,754 9.1 88.0 5,021 6.5 81.4
DCO: death certificate as the only evidence
VM: microscopic verification

Table 2. Cases and crude and standardized incidence rates per 100,000 persons-year due to cancer and sex. Metropolitan Area
of Bucaramanga, 2008-2012
Both Men Women
Place CIE-10
n % CR ASR n % CR ASR n % CR ASR
Oral cavity and Pharynx 185 2.1 3.4 4.3 116 3.1 4.5 4.6 69 1.4 2.4 2.1 C00-C14
Esophagus 72 0.8 1.3 1.2 43 1.1 1.7 1.7 29 0.6 1.0 0.8 C15
Stomach 772 8.8 14.3 13.1 427 11.4 16.5 17.1 345 6.9 12.3 10.2 C16
Colorectal 810 9.2 15 13.9 353 9.4 13.6 14.3 457 9.1 16.3 13.7 C18-C20
Liver 159 1.8 2.9 2.7 90 2.4 3.5 3.7 69 1.4 2.4 2.0 C22
Pancreas 115 1.3 2.1 2.0 54 1.4 2.1 2.2 61 1.2 2.2 1.8 C25
Lung 451 5.1 8.4 7.8 251 6.7 9.7 10.3 200 4.0 7.2 5.9 C33-C34
Melanoma, skin 112 1.3 2.1 2.0 59 1.6 2.3 2.3 53 1.1 1.9 1.7 C43
Breast 1.321 15.1 24.3 23.0 12 0.3 0.5 0.5 1.309 26.1 46.3 41.2 C50
Cervix 418 4.8 7.8 7.1 0 0.0 0.0 0.0 418 8.3 15.0 13.0 C53
Others in uterus 222 2.5 4.1 3.9 0 0.0 0.0 0.0 222 4.4 7.8 7.1 C54-C55
Ovary 215 2.5 4.0 3.8 0 0.0 0.0 0.5 215 4.3 7.7 7.0 C56
Prostate 980 11.2 18.1 17.3 980 26.1 37.7 40.9 0 0.0 0.0 0.0 C61
Urinary Bladder 122 1.4 2.3 2.0 83 2.2 3.2 3.3 39 0.8 1.4 1.1 C67
Thyroid 522 5.9 9.7 8.9 66 1.8 2.5 2.4 456 9.1 16.3 14.5 C73
Lymphoma 456 5.2 8.4 8.1 231 6.2 8.9 9.1 225 4.5 8.0 7.3 C81-C90;C96
Leukemia 331 3.8 6.1 6.3 180 4.8 6.9 7.3 151 3.0 5.4 5.5 C91-C95
Other neoplasms 1.467 16.7 27.1 25.9 795 21.2 30.5 31.6 672 13.4 23.9 21.3
Total Cases without C44 8.775 100 162.2 153.1 3.754 100.0 144.5 151.7 5.021 100.0 178.7 157.2
CR: Crude rates per 100,000
ASR: Standardized rates by age per 100,000

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Tabla 3. Casos y tasas de mortalidad crudas y estandarizadas (población mundial Segi) por 100.000 personas-año, por localización y
sexo. Área Metropolitana de Bucaramanga, 2008-2012
Both Men Women
Place CIE-10
n % CR ASR n % CR ASR n % CR ASR
Oral cavity and Pharynx 112 2.2 2.1 1.9 81 3.4 3.1 3.3 31 1.2 1.1 0.9 C00-C14
Esophagus 94 1.9 1.7 1.5 60 2.5 2.3 2.3 34 1.3 1.2 1.0 C15
Stomach 686 13.7 12.8 11.6 379 15.9 14.7 15.2 307 11.8 11 9.0 C16
Colorectal 455 9.0 8.3 7.4 204 8.0 7.9 8.1 241 9.4 8.6 6.7 C18-C20
Liver 254 5.1 4.7 4.4 130 5.4 5.0 5.3 124 4.8 4.4 3.7 C22
Pancreas 175 3.5 3.3 2.9 80 3.3 3.1 3.2 95 3.6 3.4 2.7 C25
Lung 563 11.3 10.5 9.6 337 14.1 13.0 13.7 226 8.7 8.1 6.6 C33-C34
Melanoma, skin 50 1.0 0.9 0.8 26 1.1 1.0 1.0 24 0.9 0.8 0.7 C43
Breast 349 7.0 6.5 6.1 3 0.1 0.1 0.1 346 13.3 12.4 10.8 C50
Cervix 186 3.7 3.5 3.1 186 7.1 6.7 5.7 C53
Others in uterus 55 1.1 1.0 0.9 55 2.1 2.0 1.6 C54-C55
Ovary 128 2.6 2.4 2.2 128 4.9 4.6 4.0 C56
Prostate 297 5.9 5.5 4.6 297 12.4 11.5 11.3 C61
Urinary Bladder 63 1.3 1.2 1.0 36 1.5 1.4 1.4 27 1.0 1.0 0.7 C67
Lymphoma 251 5.0 4.7 4.3 129 5.4 5.0 5.1 122 4.7 4.4 3.7 C81-C90;C96
Leukemia 266 5.3 4.9 4.7 143 6.0 5.5 5.6 123 4.7 4.4 4.1 C91-C95
Other locations 1.013 20.3 18.8 17.3 480 20.1 18.5 19.1 533 20.4 19.1 16.0
Total cases of cancer 4,997 100.0 92.9 84.6 2,390 100.0 92.4 94.8 2,607 100.0 93.3 78.0

CR: Crude rates per 100,000


ASR: Standardized rates by age per 100,000

to those of the previous quinquennium (41.2 vs 41.9 per 100,000 According to the estimates of the National Health Observatory (ONS,
women-year)25, and the global behavior reported for the year for its initials in Spanish) in Colombia for the year 2012, breast cancer,
201226. However, the order of the other more frequent cancers followed by cervical cancer, continued to have the highest incidence
in women from AMB was modified, placing thyroid cancer in in women, with magnitudes higher than those of AMB (47.3 and 16.3
the second place, followed by colorectal cancer, and displacing per 100,000 women-year, respectively); while cancer of the colon,
cervix cancer to the fourth place; cervix cancer had occupied the rectum and anus (7.8 per 100,000 women-year), thyroid cancer
second place in the previous quinquennium, showing a sustained (11.2 per 100,000 women-year) and stomach cancer (9.6 per 100,000
tendency to decrease in its rate since 2000. Stomach cancer was women-year) had lower rates. Particularly, the latter showed a marked
the fifth cancer in frequency, with the same incidence as in the downward trend in the country during the 2010-2014 period28, in
previous quinquennium. contrast to the stability of its behavior in women from AMB.
Women Men
600 600
Specific rates per age ( 100,000 people - year)
Specific rates per age ( 100,000 people - year)

400
400

200
200

0
0 20 40 60 >=80 0
0 20 40 60 >=80
Age (years)
Age (years)
Thyroid Breast Stomach Prostate

Figure 1. Age-specific incidence rates of the most frequent Figure 2. Age-specific incidence rates of the most frequent cancers
cancers in women in the metropolitan area of Bucaramanga, in men in the metropolitan area of Bucaramanga, stratified by
stratified by quinquennial 2008-2012. quinquennial 2008-2012.

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In men, the order of the five cancers with the highest incidence consumption of fruits and vegetables is very low (94.9% did not
remains the same from one quinquennium to another; all but reach the recommended daily consumption)29, and gender and
colorectal cancer showed a decrease in the standardized incidence socioeconomic inequalities have been documented in the practice
rate compared to the quinquennium 2003-200725. These five types of physical activity, with women being less active, especially
of cancer were also the ones with the highest incidence for men those engaged in unpaid work30. Inequalities in lifestyles demand
in the country in 2012, although with standardized rates higher comprehensive approaches that deepen the role of social structures
than those of AMB and with an increasing tendency in the in the configuration of health decisions and practices, as these do
quinquennium 2010-2014; with the exception of stomach cancer, not depend solely on personal decisions31,32.
which showed a clear tendency to decrease at national level28.
Improving and promoting equity at all preventive levels in relation
In relation to mortality, the profile of AMB is similar to the to stomach cancer is also a priority for AMB, especially when
quinquennium 2003-2007, although with lower rates in most marked socio-economic inequalities have been documented in the
locations; especially stomach cancer, which decreased particularly survival of patients, despite the existence of the “universal” system
in men, from 20.1 to 15.2 per 100,000 men-year. In contrast, of social security in health33.
the death rate for colorectal cancer increased in men, as did the
mortality rate from leukemia, which increased in men and women, With regard to thyroid cancer, this presents an increase on
with mortality in the period 2008-2012 being 2.4 times higher than incidence rates similar to the data reported for several regions of
in the previous quinquennium25. the world and the country. In some countries such as the United
States, the increase in incidence rates was recorded three decades
The outlook in AMB contrasts with that of the country, which ago due to a greater use of diagnostic methods such as ultrasound,
according to ONS calculations had higher standardized mortality which allowed them to find very small nodules that would
rates and a tendency to increase in several locations. However, probably go unnoticed for a long time; that is, the relative increase
mortality from leukemia showed an opposite behavior compared in incidence could be influenced by the diagnosis.
to the national estimate for 2012, with AMB reaching a 46.5%
higher rate in men and 70.5% higher in women in the 2008- Finally, the behavior of hematolymphoid neoplasms, especially in
2012 quinquennium. Unlike the behavior of the country, whose leukemia, with mortality rates that have doubled the rates of the
mortality from cancer of the colon, rectum and anus increased in previous quinquennium in our region, raises concerns about the
men and women during the quinquennium 2010-2014, in AMB factors that have impacted this marked increase in mortality rates.
this behavior was only observed in men28. It is important to explore modifiable factors, especially those that
have been associated with barriers in the health care of patients
The behavior of the country reflects the double burden of cancer with cancer, such as administrative, economic and cultural factors,
faced by the Central and South America regions, which manifests with delays in the opportunity for diagnosis and treatment34.
in high rates of cancer related to infection (cervix, stomach and
liver) and an increase in cancers related to lifestyle (prostate, breast, Conclusions
colon and rectum), the latter ones possibly have to do with aspects
of economic development, such as the increase in the age of first This study presents the magnitude of cancer in the Metropolitan
pregnancy, lower parity, smoking and alcohol consumption, diets Area of ​​Bucaramanga during the quinquennium 2008-2012,
poor in fruits and vegetables, obesity and physical inactivity27. comparatively with the quinquennium 2003-2007. Positive
behaviors are revealed for several cancers, which show a decrease
Although in several locations of tumors, AMB has lower incidences in the incidence of one quinquennium to another, or magnitudes
compared to the total population of the country, here the double lower than those of the country; however, the magnitude and
burden is also appreciated. In addition, the magnitude of colorectal tendency to increase in colorectal cancer for both sexes is to
cancer and its tendency to increase in both sexes is noteworthy, as significant, as well as the high frequency of stomach cancer, and
well as the high frequency of stomach cancer and the increased the increased incidence of thyroid cancer in women. Likewise,
incidence of thyroid cancer in women. Also, although the risk of mortality from colon and rectal cancer in men, and from leukemia
dying from cancer is lower in AMB than in the rest of the country for both sexes has increased, which requires further investigation
for almost all locations, and it was lower than in the previous and the strengthening of preventive measures.
quinquennium, the increase in mortality from colon cancer and
rectum in men, and from leukemia for both sexes is significant. Conflicts of interest:
The authors declare that they have no conflicts of interest. Interests
This profile raises more attention to the prevention of colon and or values ​​different from the usual ones in an investigation have not
rectum cancer in AMB, where the magnitude of the incidence is influenced the elaboration of this manuscript
similar for both sexes, unlike what happens in much of the world.
This type of cancer shares with breast cancer several prevention Acknowledgements:
measures, such as the maintenance of body weight, increased The Population Registry of Cancer of the Metropolitan Area of​​
physical activity and decreased consumption of alcohol, red and Bucaramanga deeply thanks all the health institutions, the medical,
processed meats, and tobacco1. paramedical and administrative staff for their cooperation and
the support provided. The Population Registry of Cancer of the
It should be noted that the prevalence of overweight or obesity Metropolitan Area of ​​Bucaramanga (RPC-AMB) is a research
in the province of Santander is 50.1%, higher in men, although project of the Universidad Autónoma de Bucaramanga, UNAB,
abdominal obesity is higher in women (46.6% versus 40.11%), the funded by UNAB and the INC.
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Colomb Med. (Cali) 49(1): 73-80

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Original Article

Cancer incidence and mortality in Medellin-Colombia, 2010-2014


Incidencia y mortalidad por cáncer en Medellín, Colombia. 2010-2014

Mary Ruth Brome Bohórquez, Diego Mauricio Montoya Restrepo, Liseth Amell Salcedo

Registro Poblacional de Cáncer de Antioquia. Secretaría Seccional de Salud y Protección Social de Antioquia. MEdellin, Colombia

Brome BMR, Montoya RDM, Salcedo LA. Cancer incidence and mortality in Medellin, Colombia. 2010-20. Colomb Med (Cali). 2018; 49(1): 81-88. doi: 10.25100/cm.v49i1.3740

© 2018 Universidad del Valle. This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use,
distribution and reproduction in any medium, provided that the original author and the source are credited.

Article history: Abstract Resumen


Background: This study provides information on cancer incidence Antecedentes: Este estudio proporciona información sobre la
Received: 24 January 2018 and mortality in a Colombian population during 2010-2014, based on incidencia y mortalidad por cáncer en una población colombiana
Revised: 13 February 2018 the data and methodology of the Population-based Cancer Registry of durante 2010-2014, a partir de los datos y la metodología del Registro
Accepted: 6 April 2018 Antioquia to facilitate the implementation of cancer control strategies.
Poblacional de Cáncer de Antioquia para facilitar la implementación de
Methods: This is a descriptive study of cancer incidence and mortality estrategias para el control del cáncer.
Keywords:
in a population, residing in the urban area of the municipality of Medel- Métodos: Este estudio es un estudio descriptivo, cuya población objeto
Incidence, mortality, cancer,
Colombia. lin. The cancers included in the study are those prioritized in the cancer reside en el área urbana del municipio de Medellín. Se incluyeron para
control plan for Colombia (PDCC-cancers). The collection, processing el análisis los cánceres priorizados por el plan de control de cáncer de
Palabras clave: and systematization of the data were performed in accordance with in- Colombia (cánceres-PDCC). La recolección, el procesamiento y la
Incidencia, mortalidad, ternationally standardized parameters for population cancer registries. sistematización de los datos se realizaron de acuerdo con los parámetros
cáncer, Colombia. Incidence and mortality rates were calculated by gender, age and tumor estandarizados internacionalmente para los registros poblacionales de
location. cáncer. Las tasas de incidencia y mortalidad se calcularon por sexo, edad
Results: During 2010-2014 there were 22,379 new cancer cases record- y ubicación del tumor.
ed in the urban area of the municipality of Medellin, of which 43.5% Resultados: En el periodo 2010-2014 se registraron 22.379 casos
corresponded to the PDCC-cancers. During the same period, 14,922 nuevos de cáncer en el área urbana del municipio de Medellín, de ellos,
cancer deaths were reported, 23.5% related to the PDCC-cancers, 53.5% 43.5% corresponde a los cánceres-PDCC. Para el mismo periodo se
in women. Prostate cancer and breast cancer were the principal cause reportaron 14,922 muertes por cáncer, 23.5% pertenecen a cánceres-
of morbidity in men and women, respectively, and lung cancer was the PDCC, 53.5 %, ocurrieron en mujeres. El cáncer de próstata y el cáncer
principal cause of death for both sexes. de mama fueron la primera causa de morbilidad por cáncer en hombres
Conclusion: Cancer is a health problem for the population of Medel- y mujeres respectivamente, y el cáncer de pulmón fue la principal causa
lin. It is necessary to emphasize research and monitor risk factors, the de muerte por cáncer para los dos sexos.
health response and the capacity of the health provider network when Conclusión: El cáncer es un problema de salud para la población del
facing the growing demand caused by this epidemic. municipio de Medellín. Se requiere hacer énfasis en las investigaciones
y monitoreo de los factores de riesgo, así como hacer seguimiento a la
respuesta sanitaria y la capacidad de la red de prestadores frente a la
demanda creciente de esta epidemia.

Corresponding author:
Mary Ruth Brome Bohórquez. Calle 42 B 52-106. Piso 8. Oficina 801.
Teléfono: 383 54 01. e-mail: institucional: mary.brome@antioquia.gov.co

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Introduction Males 80-+ Females


75-79
70-74
Cancer is one of the principal causes of morbidity and mortality
65-69
around the world; in 2015 there were 8.8 million deaths. It 60-64
is estimated that the number of new cases will increase by 55-59
approximately 70% in the next 20 years1,2. In Colombia from 2007 50-54
45-49
to 2011 there were an estimated 29,734 new cancer cases (men) 40-44
and 33,084 (women) per year. The age standardized incidence rate 35-39
(ASIR) for every cancer, except skin, per 100,000 inhabitants was 30-34
151.5 in men and 145.6 in women3. 25-29
20-24
15-19
In response, the Ministry of Health and Social Protection and the 10-14
National Cancer Institute (or INC) implemented the  Model for 5-9
Cancer Control in Colombia  in 2006. This model defines cancer 0-4
control as a series of activities that seek to decrease the burden of the 10 8 6 4 2 0 0 2 4 6 8 10
Percentage
illness in Colombia. In order to execute the plan, a description of the
epidemiological situation and an evaluation of the determinant factors Figure 1. Medellin, Colombia. Population pyramid, 2013. Source: Based on projections from
is fundamental, which allows the health system to orient oncological the National Administrative Department of Statistics. DANE, Colombia, 2013.

service and ensure an adequate social response4. The Decade Cancer


Control Plan (or PDCC)5 focuses its actions on the control of breast, According to estimates from the National Administrative
cervix, prostate and colorectal cancer as well as acute pediatric Department of Statistics in Colombia (or DANE), in 2013 there
leukemia. These tumors, in addition to stomach cancer, correspond to were 2,386,233 inhabitants in the urban area and 31,092 in the
31.7% of cancer mortality in Colombia during 2007-20113. rural area, in total 52.9% of the population were women (Fig. 1).
The Aging Index jumped from 8 senior citizens per 100 minors
Since 2000 the mission of the Population-based Cancer Registry of below the age of 15 in 1964 to 51 seniors in 2013; life expectancy
Antioquia (or RPC-A) is to offer reliable and high-quality cancer increased from 60 years in the mid-20th century to 77.5 years in
data in the state of Antioquia and facilitate the implementation of 2013, 75.5 years for men and 78.7 years for women7.
prevention and diagnostic programs and integral cancer care to
diminish the burden of this disease in the region. Currently, the Registry area
RPC-A is part of the International Association of Cancer Registries The state capitol of Medellin is comprised of 105 km2 of urban area
(or IACR) and the Network of Population-based Cancer Registries and 270 km2 of rural area.
of Colombia, alongside the RPC of Cali, Bucaramanga, Pasto,
Manizales and Barranquilla. Case definition
For this study the RPC-A acts as a selective population registry. It
The present study aims to describe the cancer incidence and included all of the malignant, invasive tumors diagnosed for the
mortality in Medellin during 2010-2014, as both a contribution first time in the five year span between 2010-2014 (incidence) by the
from the RPC-A to understand better the epidemiological behavior locations prioritized in the strategic lines of the PDCC in Colombia
of cancer in the state of Antioquia and to come closer toward 2012-2020: breast (in women), cervical, prostate, colorectal and
achieving the objectives outlined in the PDCC. acute pediatric leukemia, in addition to stomach cancer. The basis
of diagnosis could be histological, clinical, bone marrow cytology
Materials and Methods or death certificate. The statistical analyses only included primary
Medellin is the second most populated city in Colombia, capital malignant tumors or multiple invasive. In the analysis pre-invasive
of the state of Antioquia. The city is situated in the middle of the cervical neoplasms will be taken into account. Benign tumors and
Central Mountain range of the Andes, 1,538 meters above sea those of uncertain behavior were excluded. The cases of patients that
level. The weather is warm with little variation in temperature arrived to the city for diagnosis and treatment were not considered
throughout the year. The Medellin River runs through the entire residents of Medellin. The incidence date corresponds to the first
length of the city. It is the nucleus of the metropolitan area in the chronological event of diagnosis, confirming the sickness.
Aburra Valley. The other neighboring municipalities from north
The information was collected by different means (active and
to south are Barbosa, Girardota, Copacabana, Bello, Envigado,
passive), continuous and systematic recollection in the health
Itagüí, Sabaneta, La Estrella and Caldas. Industry represents 43.6%
institutes that produce cancer data: hospitals, clinics, oncology
of the internal product. The industrial sectors in order of economic
units, pathology and hematology laboratories, medical centers,
participation are the textile industry (20%), chemical products
specialized practices, the DANE and the State Secretary of Health
and substances (14.5%), beverages (11.0%) and food (10.0%).
and organisms in charge of processing death certificates, which
The remaining 10.0% include sectors such as metal mechanics,
provide the base to tabulate official mortality. The data collected
electrical and electronic industries, among others6.
were correlated to the patient’s socio-demographic variables,
Population tumor clinic and follow up. The information was then processed
The inhabitants descend from a mixture of European, Indigenous according to the confidentiality criteria stipulated by the IACR for
and African origin, with a clear preponderance of the first. population-based cancer registries8,9.

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The cases were entered into the system designed by the RPC-A Results
to eliminate duplicates, process and complement the data. The
identification of multiple primary tumors follows the norms From 2010 to 2014, 56,650 new cancer cases were registered in the
established by the IACR10. Tumor topography (localization) and RPC-A, (60.1% in women); and 30,465 cancer deaths were certified
morphology (histology) were codified with the International in the state of Antioquia (48.4% in men). Forty-five percent of the
Classification of Diseases for Oncology Third Edition (or cases and 48.9% of cancer deaths occurred to permanent residents
CIE-O-3)11. In order to compare the data, some localizations were in the municipality of Medellin.
grouped together.
Of the 22,379 new cancer cases diagnosed in Medellin, 61.6%
To ensure quality the RPC-A employs a set of indicators, were women. The average age for cancer diagnosis was 63 for men
exhaustiveness indicators (percentage of incident cases identified and 55 for women. The specific rates, crude rates (CR) and age
by death certificate and cause of death/incidence) and validity standardized rates (ASR) with the world population are expressed
indicators (distribution of cases according to the most valid base per 100,000 people-year (p-y). For men the cancer incident rate per
for a cancer diagnosis and percentage of microscopically verified 100,000 people per year (p-y) for all localizations was 171.3 (CR)
cases). and 144.4 (ASR). In women the CR was 202.9 and the ASR 145.6.

The rates of incidence and mortality are calculated conventionally, Among men the five principle cancer localizations were prostate
utilizing the mid-year population estimates and projections (26.9%), colorectal (7.8%), stomach (7.3%), lung (6.1%) and bladder
denominator calculated by the official 2005 Census12.  Cases (6.1%). Among women the most frequent localizations were: breast
without age (0.5% 111/22,379) and in situ tumors were excluded (25.8%), thyroid (13.6%), colorectal (7%), cervix (5.5%) and lung
from the study. In the case of cervical cancer, the incidence rates (4.4%). In all, these localizations represented 54.7% of all the new
for invasive and pre-invasive neoplasms were calculated separately. cancer cases diagnosed during the five-year period.
The age adjusted rates were estimated by direct methods with
the world population standard (or SEGI), the specific rates were Of the 14,922 cancer-related death certificates issued in Medellin,
calculated by variable: gender, localization and five-year age ranges 53.4% were for women. The average age at the moment of death
(18 categories). The incidence and mortality results are presented was 68 for men and 67.2 for women. Among men the cancer
for the 2010-2014 time period in their corresponding tables and mortality rates per 100,000 p-y for all localizations was 123.3 (CR)
graphs. and 101.1 (ASR). Among women the CR was 126.0 and the ASR

Table 1. Municipality of Medellin, Colombia. Incidence and mortality data for malignant tumors prioritized by the Decade Cancer
Control Plan in Colombia, quality indicators (exhaustiveness and validity) distributed by sex and localization during 2010-2014. Incident
quality indicators.
Incidence Mortality
Localization Age Rate M:I VM% DCO% Rates
n % n %
Desc CR ASR CR ASR
Breast (C50) 3,286 25.7 14 51.9 36.5 0.33 97.4 0.1 1,075 13.5 17.0 12.9
Cervix (C53) 708 5.5 1 11.2 8.5 0.55 98.0 0.1 391 4.9 6.2 4.9
Prostate (C61) 2,571 26.8 15 45.7 38.6 0.31 99.3 0.2 798 11.5 14.2 14.6
Colorectal (C18-C20) 1,640 7.3 5 13.7 10.0 0.74 98.5 0.2 1,216 8.1 10.2 7.2
Men 747 7.8 3 13.3 11.0 0.77 98.4 0.0 575 8.3 10.2 8.4
Women 893 7.0 2 14.1 9.4 0.72 98.6 0.3 641 8.0 10.1 6.5
Colon (C18) 1,080 4.8 3 9.0 6.6 0.94 98.6 0.2 1,015 6.8 8.5 6.0
Men 474 4.9 3 8.5 7.0 1.00 98.5 0.0 476 6.9 8.5 6.9
Women 606 4.7 0 9.6 6.4 0.89 98.7 0.3 539 6.8 8.5 5.4
Rectum (C19-C20) 560 2.5 2 4.7 3.4 0.36 98.8 0.2 201 1.3 1.7 1.2
Men 273 2.8 0 4.8 4.0 0.36 98.8 0.0 99 1.4 1.8 1.5
Women 287 2.2 2 4.6 3.0 0.36 99.3 0.3 102 1.3 1.6 1.1
Stomach (C16) 1,209 5.4 12 10.2 10.1 1.21 98.3 0.4 1,467 9.8 12.3 10.3
Men 695 7.2 6 12.4 12.3 1.15 98.4 0.3 801 11.5 14.2 13.6
Women 514 4.0 6 8.2 8.1 1.30 98.1 0.6 666 8.3 10.5 8.0
All localizations‡ 22,379 111 187.1 143.4 0.67 96.3 0.2 14,922 124.7 89.7
Men 9,602 42.9 43 171.3 144.4 0.72 97.4 0.2 6,941 123.3 101.1
Women 12,777 57.1 68 202.9 145.6 0.62 95.5 0.2 7,980 126.0 82.6
Infantile Leukemia 77 0 0.6 1.1 0.60 98.7 1.3 46 0.4 0.6
Men 38 0 0.7 1.0 0.55 98.8 1.2 21 0.4 0.5
Women 39 0 0.6 1.1 0.64 98.6 1.4 25 0.4 0.7
Source: Population-based Cancer Registry of Antioquia. Vital Statistics SSSA - DANE.
n: number of cases;
M:I: Reason Mortality-Incidence;
VM%: Verified Microscopically (histology/hematology);
DCO%: Death Certificate Only.
The specific, crude (CR) and age standardized rates (ASR) with the world population are expressed per 100,000 p-y.
‡ All localizations, except C44 (Skin non melanoma)

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Incidence Cervix Colon cancer Stomach cancer
150 150
400
100

300 80

Rate per 100,000 people - year


Rate per 100,000 people - year
100 100

Rate per 100,000 people - year


Rate per 100,000 people - year

60
200

40
50 50
100

20

0
25 35 45 55 65 75
0 0 0
10 20 30 40 50 60 70 80 30 40 50 60 70 80 30 40 50 60 70 80
Age (year) Age (year) Age (year)
Prostate Breast Colon
Stomach Cervix Cancer Pre-invasive neoplasm Men Women Men Women

Figure 2. Medellin, Colombia, 2010-2014. Age and Sex specific incidence rates (per 100,000 p-y) for the 9,538 cancers prioritized in the PDCC in Colombia. Source: Population-based Cancer
Registry of Antioquia. A. The age specific incidence rates were higher for prostate cancer and lower for cervical cancer. The incidence of precursor lesions of cervical cancer peaked at approximately
40 years of age. B. The morbidity of gastric cancer was greater for men older than 45 years old, the difference was less apparent for colorectal cancer with a slightly higher rate in women below 50
years of age.

was 82.6. The age specific cancer incidence and mortality rates groups, half of the cases were diagnosed before 50 and only 4.3%
were higher in women below 55 years of age, while for men it was over 80 (Fig 2).
after 55 (Supplementary Tables 1S and ​2S).
Pre-invasive Cervical Neoplasms: The peak incidence rate for
Lung cancer (19%) was the first cause of death among men, followed pre-invasive cervical lesions occurred between 35 and 39 years old,
by stomach cancer (11.5%), prostate (11.5%), colorectal (8.3%) and 60.8% were diagnosed before 40.
liver (6.2%). Lung cancer was the principle cause of death among
women (15.1%), followed by breast cancer (13.5%), stomach (8.3%), Prostate cancer: The average age of diagnosis was 68, 65 for
colorectal (8.0%) and leukemia/lymphomas (7.6%). In all, these five colorectal cancer, 65 for stomach cancer and 7 for acute pediatric
principle causes constitute 52.5% of all cancer deaths that occurred leukemia (Fig 2).
in Medellin during the five-year interval from 2010 to 2014.

Cancers prioritized in the Decade Cancer Control Plan in Mortality by PDCC malignant tumors in Medellin
Colombia, 2012 - 2021. During 2010-2014, the PDCC-cancers represented 33.5% (4,993)
Of the total new cancer diagnoses in residents of Medellin, 9,538 of the total cancer deaths in Medellin (14,922); 2,798 (56.0%) of the
(42.6%) corresponded to stomach, prostate, breast, cervical, deaths occurred in women and 2,195 (44.0%) in men.
colorectal cancer and acute pediatric leukemia, that altogether will
be denominated for the analysis as PDCC-cancers; 4,075 (42.7%) The crude and standardized mortality rate (CMR and ASMR) by
cases were diagnosed in men and 5,463 (57.3%) in women. age for the PDCC-cancers was 38.9 and 31.6 in men and 44.2 and
29.7 in women.
For the PDCC-cancer group the CR and the ASR per 100,000 p-y
was 72.3 and 60.9 in men and 86.3 and 61.3 in women. The average age at the moment of death was 64 for breast cancer,
58 for cervical cancer, 78 for prostate cancer, 68 for colorectal and
During the 2010-2014 period there were 2,254 women with pre- stomach cancer. In the case of acute pediatric leukemia, the average
invasive cervical lesions, in 44 cases the age was unknown, CR was age of death was 9.
35.6 and the ASR 30.5.
Figure 3 describes the curves for age specific mortality rates. The
Quality criteria for incidence data mortality rate for breast cancer is higher for women below 65 years
Table 1 shows the quality indicators for the incidence information old. For older adult older than 65 years of age deaths are caused by
during 2010-2014 period for malignant tumors prioritized in prostate and stomach cancer. This is the reason why (M:I) is greater
the PDCC. The percentage of diagnosed cases with microscopic than 1 in women with cervical cancer and in men with prostate
verification (histology of primary tumor, cytology and bone marrow cancer over 70.
aspiration) for men and women was 99.8%; in this tumor group the
percentage of registered cases that only had a death certificate as its The specific mortality rates below 70 are higher in women with
only evidence was 0.2%. The global cause of mortality: incidence breast cancer. After 70 this is the reason why (M:I) is greater than 1
was 0.67 for the total population, 0.72 for men and 0.62 for women. in men with prostate cancer and women with cervical cancer

Breast Cancer: The average age of diagnosis was 58 years old, Discussion
42.5% in people below 50 years of age and only 12.5% over 80.
The Population-based Cancer Registry of Antioquia (or RPC-
Cervical Cancer: The specific incidence rates of invasive cervical Antioquia) compiled and classified all of the new cancer cases and
cancer reached a maximum value of 20 per 100,000 at approximately cancer-related deaths that occurred in Medellin, the second most
30 years of age and later leveled off and remained stable for all age populated city in Colombia. This article presents the incidence and
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Mortality Cervical cancer Breast cancer Prostate cancer
500 100 500 500

400 400 400

Rate per 100,000 people - year

Rate per 100,000 people - year


Rate per 100,000 people - year
Rate per 100,000 people - year

300
300 300

200
200 200

30
100
20 100 100

10
0
30 40 50 60 70 80 0 0 0
Age (year) 30 40 50 60 70 80 80 30 40 50 60 70 80 30 40 50 60 70 80
Age (year)
Age (year) Age (year)
Prostate Stomach Colorectal
Breast Cervix Incidence Motality Incidence Motality Incidence Motality

Figure 3. Medellin, Colombia, 2010-2014. Age and sex specific mortality rates (per 100,000 p-y). Source: Population-based Cancer Registry of Antioquia and Vital Statistics SSSA - DANE.

mortality rates for those cancers prioritized in the PDCC during with HER2 over-expression and higher rates of systemic relapse in
2010-2014. The PDCC-cancers were responsible for 42.4% of the any clinical stage in comparison with postmenopausal women21-23.
morbidity and 33.4% of the cancer-related mortality in Medellin.
This article is the product of a collaboration between the Secretary Prostate cancer was the first cause of morbidity and the second
of Health of Antioquia and the network of oncological service cause of cancer mortality in Medellin, 84.2% was concentrated
providers in the city. in the 60 to 80 age group. Prostate cancer affects older men more
frequently, which is an important health concern in developed
The information provided by the RPC-A indicates that cancer is a countries (Table 2S). In these countries 15% of cancers in men are
public health problem in Medellin. It was the second cause of death prostate cancer in contrast to 4% in developing countries24,25.
after circulatory system diseases and responsible for 25% of deaths that
occurred in the city13. During the 5-year period (2010-2014) cancer Malignant colorectal tumors in Medellin during 2010-2014
was diagnosed in 5,225 new cases and 2,963 deaths a year for residents affected more women than men. In both sexes, the cases increased
in the city of Medellin, according to the information provided by the after 55 years of age. Colombia can be classified as a country with
Sectional Secretary of Health and Social Protection of Antioquia. a low risk for colorectal cancer, but its incidence has increased,
coinciding with profound lifestyle changes. The majority of
The morbimortality risk for cancer in the region is determined by Colombians live in capital cities, few follow the recommendations
multiple factors. Cancer is part of a group of complex diseases of of exercising a minimum of 150 minutes a week and the prevalence
complex etiologies. Some factors are recognized, including genetic of overweightness is an increasing trend. This condition is more
factors and lifestyle choices, like smoking, diet and exercise; certain prevalent in women and in the 50 to 64 age group26,27.
types of infections and the exposition to some chemical substances
and radiation14. In Medellin, the majority of cancer determinants Gastric cancer is the principle cause of cancer mortality in
are yet to be identified. Colombia5, the risk is greater for men and the age specific rates
increase exponentially at 60 years of age (Table 2S and Figure 3).
Lung cancer is the primary cause of mortality in men and women The epidemiology of disease varies considerably by region and sex,
in Medellin during the five-year period. The prevalence of smoking due to the difference in eating habits, age and other risk factors
in the city reaches 25.5%, inversely proportional to the educational in the population28. In Colombia, gastric cancer has an annual
level and the proportion of smokers is greater in people that also incidence of 16.3/100,000 inhabitants and mortality is calculated
have a high consumption of alcohol. In Colombia, Medellin is at 14.2/100,000 inhabitants5. Five-year survival is less than 15%
recognized as the city with greatest level of air pollution, exceeding because patients are diagnosed at advanced stages29-31  The cause
the norms established by the WHO and posing as a risk to human M:I for gastric cancer was greater than 1, suggesting that incidence
health. Mortality from lung cancer is 2.4 times greater than in rates are underestimated (Table 1S).
Bogota and 1.7 times greater than the mortality in Colombia by
the same cause15,16. Table 2 shows the comparison of the ASIR for all cancer localizations
in Medellin with four other Colombian registries situated in Cali32,
Different Mexican studies indicate that 50% of women with breast Bucaramanga33, Manizales34 and Pasto35. The average annual ASR
cancer are younger than 50 years old at the time of diagnosis, in was 144 per 100,000 men and 145 per 100,000 women during 2010-
contrast to 22% to the Caucasian population17,18. In Medellin, the 2014. These findings are comparable to those observed in Pasto
data shows that during 2010-2014, 42.5% of the cases occurred (134 men and 146 women per 100,000), albeit lower than those in
in women younger than 50. This increased proportion of cases in Cali (205 men and 186 women); Bucaramanga (154 men and 157
young women is important because the diagnosis and behavior women) and Manizales (156 men and 165 women per 100,000). A
are generally more aggressive, with a disproportionately greater notable difference from other cancer registries is that Medellin has
number of years lost due to cancer19,20 This is a result of detection a high percentage of cases by microscopy, which suggests possibly
at advanced stages, a greater proportion of triple negative tumors considering a subregister.
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The comparison of the ASR of PDCC-cancers in Medellin, data Strengths


provided by the RPC-A, with the ASR reported by the RPC-Cali, The data was obtained based on the population in the nucleus of the
RPC-Bucaramanga, RPC-Manizales and RPC-Pasto shows that the municipality of Medellin. The technical and financial guidance was
ASIR for breast and prostate cancer were similar to those reported provided by the Sectional Secretary of Health and Social Protection
by RPC-Manizales and lower than other Colombian cities. For of Antioquia. The project was led by a medical doctor, a pathology
stomach cancer the ASR in women showed little variation from 8.1 specialist, an official of more than 30 years in this institution.
in Medellin and 11.9 in Pasto. In men there was greater contrast,
12.3 in Medellin to 26.5 in Pasto. In Medellin the incidence of Acknowledgements
colon cancer is lower than those reported in other registries with The authors manifest their acknowledgement to the team at the
the exception of Pasto that reported the lowest ASR in both sexes Population Cancer Registry of Antioquia, to the Sectional Secretary
for this malignant tumor. It is noteworthy that the ASR for cervical of Health and Social Protection of Antioquia and Dr. Luis Eduardo
cancer in Medellin is lower than those reported by other registries Bravo of the Population-based Cancer Registry in Cali.
(Table 2).
Conflict of interest:
In Medellin the incidence rate of cervical cancer is below the Nothing declarated
national average and the mortality rates are very close to the
goals proposed in the PDCC for 2021: Reduce the mortality rate References
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Registries in Colombia.
RPC. Incidence Rates 2008-2012
Localizations Cali 32
Bucaramanga 33
Manizales34 Pasto35 Medellín (RPC-A)2010-2014
Men Women Men Women Men Women Men Women Men Women
Stomach 20.3 10.8 17.3 10.3 20.3 9.7 26.5 11.9 12.3 8.1
Prostate 60.1 41.1 44.1 27.1 38.6
Colon 10.5 9.7 9.5 9.9 8.4 10.0 4.5 5.4 7.0 6.4
Rectum 5.7 4.4 5.0 3.8 6.3 4.7 3.8 3.6 4.7 3.4
Breast 44.5 41.3 37.2 27.8 36.5
Cervix 15.4 12.9 17.5 18.1 8.5
All 205.0 185.7 153.7 156.5 156.0 164.8 134.1 145.6 144.4 145.6
VM% 86.7 89.8 81.5 88.0 85.8 84.7 83.3 84.4 97.4 95.5
DCO% 1.9 1.4 9.1 6.6 3.8 3.0 5.0 4.5 0.2 0.2
M:I¶¶ 55.3 53.3 68.3 60.7 74.6 68.8 63.8 52.6 72.3 62.5
Source: ¶ Cancer Incidence in Five Continents, Volume XI. Cancer Incidence in Five Continents, Volume X.

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Colomb Med. (Cali) 49(1): 81-88

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Artículo original

Oncology services supply in Colombia


Servicios oncológicos en Colombia

Eliana Murcia1, Jairo Aguilera1, Carolina Wiesner2, Constanza Pardo3

1
Grupo Evaluación y Seguimiento de Servicios Oncológicos, Instituto Nacional de Cancerología, Bogotá. D.C., Colombia.
2
Dirección General, Instituto Nacional de Cancerología, Bogotá. D.C., Colombia.
3
Grupo Vigilancia Epidemiológica del Cáncer, Instituto Nacional de Cancerología, Bogotá, D.C., Colombia.

Murcia E, Aguilera J, Wiesner C, Pardo C. Oncology services in Colombia. Colomb Med (Cali). 2018; 49(1): 89-96. doi: 10.25100/cm.v49i1.3620

© 2018 Universidad del Valle. This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use,
distribution and reproduction in any medium, provided that the original author and the source are credited.

Article history: Abstract Resumen


Received:24 October 2017 Objective: To characterize the current status of oncological services Objetivo: Caracterizar la situación actual de la oferta de servicios
Revised: 22 February 2018 supply in Colombia. oncológicos en Colombia.
Accepted: 21 March 2018 Methods: A descriptive analysis of oncological services for cancer Métodos: Se realizó un análisis descriptivo de los servicios oncológicos
care in the adult and infant population that meet the requirements para la atención de cáncer en población adulta e infantil, que
Keywords:
for operation according to the Special Register of Health Service cumplieron con los requisitos para su funcionamiento de acuerdo
Health services; oncology Providers was carried out. The case – by - provider ratio was al Registro Especial de Prestadores de Servicios de Salud. La razón
service, hospital; cancer;
Colombia. calculated based on the cancer incidence estimated for Colombia by de casos por prestador se calculó a partir de la incidencia de cáncer
the National Cancer Institute. estimada para Colombia por el Instituto Nacional de Cancerología.
Results: Were identified 1,780 qualified oncology health services in Resultados: Se identificaron 1,780 servicios de salud oncológicos
Palabras clave:
the country related to specialties for providing care to cancer patients. habilitados en el país relacionados con especialidades para la atención
Servicios de salud; servicio
de oncología en hospital; Twenty five providers nationwide had all three qualified services: de pacientes con cáncer. 25 prestadores a nivel nacional contaron con
cáncer; Colombia. chemotherapy, radiotherapy and surgery. Nearly 50% of the offer was los tres servicios habilitados: quimioterapia, radioterapia y cirugía.
concentrated in Bogotá, Antioquia and Valle del Cauca. Putumayo Cerca del 50% de la oferta se concentró en Bogotá, Antioquia y Valle
and the Amazonas group departments, with the exception of del Cauca. Los departamentos de Putumayo y del grupo Amazonas,
Vaupés, did not show any oncological services. Healthcare Providers con excepción de Vaupés, no registraron servicios oncológicos. El
were responsible for 87.8%, and independent professionals provided 87.8% fue ofertado por Instituciones Prestadoras de Salud y el 12.2%
12.2%. Outpatient services were 66.7% of oncology services, 17.4% fue provisto por profesionales independientes. El 66.7% de los servicios
was diagnostic support services and therapeutic complementation, oncológicos eran de consulta externa, el 17.4% eran servicios de apoyo
and 15.9% was surgical services. 87.9% of the oncological service diagnóstico y complementación terapéutica y el 15.9% servicios
offer in Colombia takes place in the private sector. quirúrgicos. El 87.9% de la oferta de servicios oncológicos en Colombia
Conclusions: The ratio between the service groups is asymmetric, está en el sector privado.
with few providers jointly offering the basic services for oncology Conclusiones: La relación entre los grupos de servicios es asimétrica,
treatment, which reflects how provision is fragmented. It is necessary con pocos prestadores que ofertan de forma conjunta los servicios
to redefine the concept of oncology service under a comprehensive bases del tratamiento oncológico, lo cual refleja la fragmentación en
care approach and the importance of enabling functional units, la prestación. Es necesario redefinir el concepto de servicio oncológico
comprehensive treatment centers and other forms of care. bajo el enfoque de atención integral y la importancia de habilitar
unidades funcionales, centros integrales de tratamiento y otras formas
de atención.

Corresponding author:
Constanza Pardo MSc, Grupo Vigilancia Epidemiológica del Cáncer,
Instituto Nacional de Cancerología, Calle 1 No. 9-85, Tel.: 57 (1) 4320160
extensión 4806, Bogotá D.C., Colombia. Correo electrónico cpardo@cancer.
gov.co.
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Murcia E/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)

Introduction As of 2012 and after the Ministry of Health and Social Protection
regulated the price of oncological medicines, there was a gradual
About 14 million new cases of cancer1 were recorded in 2012, and decrease in the number of services provided9, a scenario that
the number of cases with cancer incidence is expected to increase possibly slowed down the supply of new oncology services. This was
by 70% over the next 20 years, facts that have made this disease joined by a new national regulation defining the procedures and
one of the main causes of morbidity and the second cause of death conditions for registration and authorization of health services, as
in the world2, accounting for at least one in every six deaths. In well as the declaration of mandatory requirement for institutions
2015, cancer caused an estimated 8.8 million deaths; close to 70% to obtain a verification by the Ministry of Health8 prior to opening
of deaths have been recorded in low and mid-income countries, their oncological services8, even though the mandatory nature of
where less than 30% of countries provide treatment to patients this verification does not imply that the Ministry regulates the
with an oncological pathology3. oncological service offering.

Comprehensive care for cancer patients requires bringing In order to avoid care fragmentation, aiming at promoting
together the various oncological specialties - medical, surgical, comprehensive care under the model of units or comprehensive
radio therapeutic - and it also requires the synergy of a variety treatment centers has been one of the ways in which the national
of diagnostic services (pathology, clinical laboratory, imaging, government has managed to organize the offer. New ways of
nuclear medicine, among others) as well as that of clinical and articulation between oncological services were defined by 2016:
social support services (nutrition, mental health, social work, Functional Units for Adult Cancer Care-UFCA and Childhood
pain control, among others) that are complementary4. According Cancer Care Units-UACAI10, and the creation of Health Service
to the recommendations made by high-income countries, which Suppliers’ Comprehensive Networks RIPSS, which the Oncology
have a high number of cancer patients, the oncological surgery, Services Delivery Network is part of11. Within this context, the
radiotherapy and chemotherapy services should be concentrated objective of this article is to characterize the current oncological
in comprehensive treatment centers, which can guarantee a high services supply status in Colombia and its distribution by
volume of patients with the same pathology, thus allowing to justify departments for the year 2017.
investment in complex treatment technologies, improve medical
expertise, and improve clinical outcomes. On the other hand, Materials and Methods
diagnostic and patient support services must be decentralized5.
A descriptive analysis of the distribution of oncology services that met
Colombia is a mid-income country, with a cancer incidence rate the requirements to provide health services for cancer care in the adult
of 151.5 per 100,000 men and 145.6 per 100,000 women6, with and infant population in Colombia, which required prior verification
a strong supply of oncological services in the private sector and by the Ministry of Health and Social Protection for its operation was
fragmentation among the services involved in cancer treatment4. conducted, according to information available in the REPS.
That is how, since cancer is a growing public health problem in
Colombia, the country placed the Ten-Year Plan for Cancer Control The set of oncological services included in the analysis is made
2012-2021 as part of its public policies, where several goals were up of: outpatient services specialized in the medical and surgical
defined, including: the need to update the eligibility standards and areas, surgical services, and diagnostic support and therapeutic
the oncological services verification modes, as well as the need to complementation services covering radiotherapy, chemotherapy
organize the service network for comprehensive care of cancer in and nuclear medicine (Table 1)8. The information was consulted
Colombia7. In meeting this goal, the procedures and conditions for with the report prepared by each department up to June 2017.
eligibility of health services, including oncology, were regulated in
We conducted the search by using the “guest” user access profile. We
2014, strengthening the requirements for compliance with quality
enter the “Current REPS” module, in the services item. Two search
standards8.
criteria were used: name and code of the services of interest, according
In Colombia, the Ministry of Health and Social Protection has to the service structure set forth in Resolution 2003 of 2014 (Table 1).
the power to verify compliance with standards, and technical-
We carried out an information selection process, which included
scientific conditions for opening and operating a new oncology
all the oncological services registered in the REPS, except those
service, identifying this as a “qualified” service in The Special
services that stated a “non-oncological” focus when registered,
Registry of Health Service Providers-REPS9. The REPS is the
that is, that the activities to be developed by them were not aimed
official source of information on the registered offer of health
at dealing with cancer patients. The services corresponding to
service providers that are authorized to provide health services
“other” name codes were incorporated into the analysis only in
in each territorial demarcation, which, for the Colombian case,
those cases in which the term oncological specialty was specified in
are called departments, according to the political-administrative
the service name. The variables defined in the analysis were those
division of the state. The country identifies two types of health
related to geographical distribution, service group, legal nature,
service providers: professionals who provide a single service
type of provider, level of care, territorial character, complexity and
independently in their private offices and health services provider
locations. Variables related to the provision mode were excluded
institutions that offer several health services. The latter group
based on incomplete information.
includes hospitals, clinics or similar establishments.
Based on this record, between 2004 and 2012 an increase in private The case-by-provider ratio was calculated from cancer incidence
oncological services and an expansion of non-integral services data estimated for Colombia, information published by the
became evident, a fact that clearly showed fragmentation of care4. National Institute of Cancer - INC6, on the number of qualified

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Table 1. Oncology services subject to prior verification by the provided 75% of the oncological offer; as for Santander, Bucaramanga
Ministry of Health and Social Protection. offers about half of all oncology services (48%) and the remaining offer
Group of services Service Service name is provided, in descending order, by the municipalities of Piedecuesta,
code
Floridablanca (Metropolitan Area) and Barrancabermeja.
210 Surgical oncology
227 Pediatric surgical oncology
Breast surgical oncology and soft tissue tumors
Offer of oncological services by type of provider, legal nature and
Surgical services group 232
surgery * level of care
237 Plastic surgery for the oncological patient Out of 1,780 qualified services provided in the country, 87.8%
217 Other surgeries* (1,563 services) was offered by Healthcare Providing Institutions
309 Pain and palliative care* - IPSs, and the remaining 12.2% (217 services) was provided by
336 Clinical oncology independent professionals - PI (Table 2).
346 Oncology rehabilitation
364 Breast and soft tissue tumor surgery* The IPSs group makes up 381 institutions and 443 care-providing
370 Plastic surgery for the oncological patient centers; this means that some of those IPSs enabled oncology
373 Surgical oncology services in more than one location. According to their legal
374 Pediatric surgical oncology nature, 91.1% of these institutions were private, 7.9% were public
375 Dermatological oncology
companies and only 1.0% were mixed entities. Regarding service
379 Gynecology oncology
Specialized Medical
381 Oncology and clinical hematology
provision, 362 IPSs (95%) stated to be medium and high complexity
Consultation group
390 Ophthalmic oncology and 19 low complexity IPSs. In addition, 21 IPSs recorded that
391 Pediatric hematology and oncology
they provide services in the third level of care, only 9 IPS in the
second level of care, and the rest of IPSs did not differentiate their
393 Orthopedic oncology
395 Urologic oncology
level of service provision.
408 Radiotherapy
383 Nuclear medicine*
As for the 347 existing private IPSs nationwide, they managed 1,374
394 Oncologic pathology of the 1,563 services authorized at IPSs, that is, 87.9% of the oncology
406 Hematological oncology services supply in Colombia is provided by private sector IPSs.
356 Other consultations*
709 Chemotherapy Public IPSs, which manage 180 services, correspond mostly to
Diagnostic and therapeutic 711 Radiotherapy institutions of departmental coverage (70%), and a smaller number
support Group
715 Nuclear Medicine (PET / Iodine therapy)* of entities have coverage at the national (10%), district (10%) and
* The REPS application has options for the provider to state whether the activities of
municipal (10%) levels. Likewise, the 30 public IPSs are entities
these services are aimed or not to cancer patients. Source: Resolution 2003 of 2014. that depend directly on the state or the departments, except for
two institutions belonging to the special regime of military health
oncological IPS. Calculations for 27 departments, the Capital and the national police.
District and the Amazonas group (Amazonas, Guainía, Guaviare,
Vaupés and Vichada) were made. In addition, the correlation Regarding independent professionals (195), it was found that
coefficient between new cancer cases per year and the number of several of them enabled more than one service or the same service
oncological IPS was calculated. in different locations. The average of independent professionals by
department is seven, it is important to note that in Arauca, Boyacá,
Results Casanare, Cesar, Chocó, Cundinamarca, La Guajira and San Andrés
and Providencia departments no oncology services enabled under
We identified 1,780 qualified health services in the national this type of providers (independent professionals) were found.
territory related to specialties for cancer patient care, as well as
close to 63,000 new patients per year, according to estimates of the In general, Colombia had 576 health service providers to serve the
INC regarding cancer incidences in the country. 62,818 new cases of cancer per year estimated in the country, with
an average of 2,166 cases of cancer per territory and 20 providers
Offer of health services by geographic location on average to meet this demand.
We found records of oncological services in 28 departments,
with at least one provider with an authorized service in each From the comprehensive care at the IPSs standpoint, there are an
territorial demarcation. The departments of Putumayo and the average of 13 IPSs per territory, with an average of 4.1 oncology
Amazonas group, with the exception of Vaupés, did not record services enabled per institution. This was the offer available for
any oncological services. Nearly 70% of the country’s offer was 165 new cases per year by IPS, with a range of variation between
concentrated in the Capital District, Bogotá D.C. (23.8%) and in 55 cases in institutions located in La Guajira and 1,052 cases to be
the departments of Antioquia (13.4%), Valle del Cauca (10.6%), addressed per IPSs located in Cundinamarca (Table 2).
Atlántico (8.3%), Santander (7.2%) and Bolívar (5.3%) (Fig. 1).
The number of new cancer cases estimated by department
With the exception of Chocó and Santander, capital cities in most showed a positive ratio with the number of oncology IPSs (r=
departments offered over 85% of oncological services available in 0.87). Some departments such as Antioquia, Valle del Cauca and
each territory. Bogotá, D.C., Medellin and Cali stood out as the Cundinamarca have new cases of cancer by IPS above the national
main urban centers with a high number of health services for average (165). The opposite is shown for the Departments of the
oncological diseases care. In the case of Chocó, its capital Quibdó Caribbean region and Santander (Fig. 2).

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Bogotá 337 86
Antioquia 202 36
Valle del Cauca 172 17
Atlántico 128 19
Santander 109 20
Bolívar 86 8
Risaralda 57 2
Magdalena 47 1
Nariño 42 1
Norte de Santander 40 4
Meta 39 4
Huila 36 3
Cesar 36
Córdoba 32 3
Tolima 31 2
Caldas 29 3
Sucre 28 1
Boyacá 25
Quindío 23 5
Cauca 18 1
Cundinamarca 16
La Guajira 15
Chocó 4
Caquetá 1
Grupo Amazonas 2
Casanare 2
Arauca 2
San Andrés y Providencia 1
Putumayo 0
0 50 100 150 200 250 300 350 400 450

Health Services Authorized in IPS* Health Services Authorized in PI**

Figure 1. Qualified Oncology Services by provider class and Department. Cut-off date: June 30, 2017. Source:
Database of the Special Register of Health Service Providers REPS. Ministry of Health and Social Protection.
* IPS: Institution providing health services,
** PI: Independent professional.

Table 2. Ratio between new cases of cancer and IPSs with oncology Offer according to health service groups
services in departments of Colombia. Cut-off date: June 30, 2017. When differentiating services according to the group classification
Estimated Oncology Cases/ *IPS structure, it was found that more than half of all oncology services
Department incidence IPS ratio were outpatient services (66.7%), and there was a lower percentage
Casanare 309 1 309 of participation in the offer for services related to the diagnostic
Antioquia 9,781 34 288
support and therapeutic support group (17.4%), and the surgical
Arauca 253 1 253
Boyacá 1,813 7 259 one (15.9%) (Table 3).
Cauca 1,521 6 254
Tolima 2,308 100 231 The outpatient group showed 1,187 services for 16 oncology specialties,
Valle del Cauca 7,639 353 218 among which clinical oncology, oncological gynecology, pain and
Córdoba 1,356 8 170 palliative care, and breast surgery and surgery of soft tissue tumors
Caldas 1,860 11 169 stands out because of their higher availability; these consultations
Norte de Santander 1,815 11 165 account for over 50% of the total offer of this group of services. 82.1%
Amazonas Group 164 14 164
of outpatient services were located in IPSs, and 17.9% of outpatient
Risaralda 1,723 11 157
Bogotá 11,068 72 154 consultations were provided by independent professionals.
Nariño 1,810 121 151
Caquetá 447 3 149 The diagnostic support and therapeutic support group are made
Quindío 1,172 8 147 up of services providing the traditional treatment modalities for
Huila 1,451 10 145 cancer: chemotherapy and radiotherapy and nuclear medicine.
Meta 1,206 9 134 In absolute figures, the services attached to this group were 310,
Chocó 279 2 140 discriminated as follows: chemotherapy (180), nuclear medicine
Sucre 737 67 123 (77) and radiotherapy (53). Participation of independent
Santander 2,961 25 118
Cesar 990 9 110
professionals in the offer of this group was 1.3%, which means that
Cundinamarca 3,157 3 105 98.7% of qualified diagnostic and therapeutic services in oncology
Magdalena 1,249 15 83 are provided by IPSs.
Bolívar 2,019 25 81
Atlántico 3,010 37 81 In addition, an offering consisting of six chemotherapy services
San Andrés y Providencia 78 1 78 was found in IPSs that did not have any outpatient services in
La Guajira 440 8 55 clinical oncology or hematology and pediatric oncology.
Putumayo 202 0 0
Colombia 62,818 38,118 165
Source: REPS database.* IPS: Institution providing health care services.

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12,000
Bogotá
R2 = 0.771

Antioquia
10,000

8,000 Valle del Cauca


New Cancer Cases (n)

6,000

4,000
Cundinamarca
Santander Atlántico
Tolima
Bolívar
Boyacá
2,000
Magdalena

La Guajira
0
0 10 20 30 40 50 60 70 80
IPSs Providing Oncology Services
Figure 2. Ratio of estimated incidence by departments and IPSs providing oncology services in Colombia. IPS:Institución prestadora de servicios de salud.
(Healthcare Provider Institution)

Table 3. Group of qualified (authorized) oncology services. Cut-off-date: June 30, 2017.
Number of services Number of services
Service group Service name enabled per IPS * enabled per PI**
Surgical oncology 105 0
Pediatric surgical oncology 20 0
Breast surgical oncology and surgery of soft tissue tumors * 122 0
Surgical services group Plastic surgery for the oncological patient 31 0
Other surgeries - Surgical oncology 3 0
Other surgeries- Gynecology oncology and mastology 1 0
Other surgeries- Orthopedic oncology 1 0
Pain and palliative care 132 15
Clinical oncology 182 37
Rehabilitation oncology 12 0
Breast and soft tissue tumor surgery 87 30
Plastic surgery for the oncological patient 24 8
Surgical oncology 83 21
Pediatric surgical oncology 10 0
Dermatological oncology 15 5
Gynecology oncology 113 44
Specialized medical
Oncology and clinical hematology 0 0
consultation group Ophthalmic oncology 13 4
Pediatric hematology and oncology 68 2
Orthopedic oncology 38 6
Urology oncology 33 10
Radiotherapy 46 14
Nuclear medicine 22 0
Oncologic pathology 0 0
Hematological oncology 87 8
Other consultations- Oncology 9 9
Diagnostic support Chemotherapy 180 0
and therapeutic Radiotherapy 51 2
complementation group
Nuclear Medicine (PET / Iodine therapy) 75 2
Source: REPS database.* IPS: Institution providing health services, ** PI: Independent professional.
**PI: Profesional independiente

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The surgical group showed a total of 283 services, where breast Likewise, countries such as the United Kingdom, which has an
and soft tissue surgery account for 43.1% of the total offered by incidence of 273 (APR per 100,000 person-years), states that
the group. Therefore, the availability of other surgical services, there must be a comprehensive treatment center for every 2.5 to
in descending order, was: general oncological surgery (37.1%), 3.6 million people13, a concept that if brought to the Colombian
oncological plastic surgery (11.0%), pediatric oncological surgery context, would mean having more or less 15 comprehensive
(7.1%), oncological gynecological surgery and mastology (0.4%), centers offering a multitude of oncological services, which is far
oncological orthopedics surgery (0.4%), and other oncological from the current situation in the country.
surgeries undifferentiated by specialty in the record (1.1%).
In the last decade, the offer of oncological health services in
With regard to comprehensiveness of health services involved Colombia showed a trend oriented to enabling services of the group
in conventional forms of cancer treatment (chemotherapy, of consultation of oncological medical specialties, with second and
radiotherapy, surgery), we found 257 providers offering these third places for services of diagnosis and therapeutic and surgical
services, of which 65.3% offered one of these three services, complementation support; as a result of this dynamics, over half
therefore 88 providers only offered surgical oncology services, 77 of oncology services are outpatient services, more than 65% of
providers only offered services to administer chemotherapy and providers offering cancer treatment services tend to offer only
9 providers had radiotherapy services exclusively for diagnostic one type of service, and only 6.5% of IPSs have comprehensive
support and therapeutic complementation. Also, a percentage of chemotherapy, radiotherapy and oncological surgery services. This
24.9% of this group of providers offered two services for treatment, lack of balance in the ratio of service groups and the low average of
which means that 49 providers had chemotherapy and oncological services provided by the IPSs suggests the existence of health centers
surgery services, and 15 providers offered chemotherapy and that do not integrate the basic oncological therapeutic modalities,
radiotherapy services. In summary, 25 providers nationwide had which hinders institutional coordination and sets up barriers to
the three services available: chemotherapy, radiotherapy and access as well as quality in the care provided14.
surgery.
Even though this article is not an analysis of sufficiency of
Discussion oncological services by specialty, since it includes variables
referring to the productive capacity of the services (infrastructure,
This descriptive study presents the characterization of oncological human talent, production, times and movements), the analysis
services in Colombia to provide care to cancer patients, based on certainly showed that the gynecology and breast surgery services
information available up to June 2017. A high concentration of as well as those for soft tissue tumors were the specialties with the
oncological services was found in the capital cities, out of which highest offer in consultation, data concomitant with the main types
more than half are related to outpatient services (67%) and 88% of cancer in women (breast and cervix). In the case of oncological
of them are private. Only 25 providers nationwide had the three gynecology, its high offer does reflect the priority granted to
services available: chemotherapy, radiotherapy and surgery. providing care for the pathologies treated by specialty, therefore,
Although the development of care models under the figure of with the current offer, each authorized oncology gynecology
comprehensive units of care and networks has been deemed as consultation service handles an average of 30 new cases of cervix
essential, it is worth noting that no records were found so far cancer per year out of the approximately 5,000 cases diagnosed;
regarding functional clinical units for adult cancer-UFCA, or units nevertheless, breast consultation is not necessarily enabled for
for Comprehensive Care of Childhood Cancer UACAI, and also cancer care, so the figures do not tacitly correspond to the offer for
no Comprehensive Networks for the Provision of Health Services treatment of an oncological pathology. In addition, if we consider
were found; according to this, thinking about a harmonization that of the 29,734 new cases of cancer per year that occur in men 6,
of the service network in the different levels of complexity that prostate cancer is the most frequent with around 9,000 cases, but
guarantees a quality and opportunity in the diagnosis of the the offer of outpatient care for oncological urology was low, since
oncological disease is still somehow complicated; this clearly a consultation service for this specialty examines an average of 210
shows the need the country has to classify and redefine what is new cases of prostate cancer per year, a number that is far away
currently defined as an oncological service12. from the figure observed for women’s care.

The study clearly shows that there are large differences in the Additionally, the record showed that, put together, the offer for
number of new cases of cancer in different regions, and that the consultations of the oncological specialties of dermatology,
largest numbers of cases are in the departments of Antioquia, rehabilitation, ophthalmology, nuclear medicine and pediatric
Atlántico, Valle del Cauca, Cundinamarca, and Bogotá. Incidence surgery, does not account for more than 5% of the total offer of the
estimates show that the demand for services varies according to outpatient services group.
the geographical characteristics, and this reason would usually
consider that the offer of oncological services should be in All the services of the surgical group were enabled by IPSs,
accordance with local demand. However, as it has already been otherwise this would not be feasible, given the criteria of the
shown in the world, a case-by-case ratio of 165 cases per IPS per interdependence standard for qualification of surgical services
year, as found in this study is very low to guarantee successful according to Resolution 2003 of 2014, a standard that regulates
health outcomes, considering that comprehensive treatment qualification of health services. Some radiotherapy and nuclear
centers such as the National Cancer Institute INC, handles about medicine services for diagnostic support and therapeutic
7,000 new cases per year; nevertheless, this fact is special because complementation were enabled by independent professionals;
this is a reference institution that offers care to patients from however, given the requirements of the human talent standard
all over the country and does not segment its offer to regions4. of the qualifying standard, this is a non-viable condition, since
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operation of these services involves several professionals and nuclei identified mainly in capital cities. The core of oncological
therefore cannot be offered by a single independent professional. services offer is concentrated in private providers with a minimum
This fact reflects discrepancies in the information system of the participation of public entities belonging to the Colombian state.
registry of providers in the REPS. In general, the ratio between groups of services is asymmetric,
the majority of them being oncological outpatient services with
In advanced oncological disease, pain relief and palliative care few providers that offer together the basic services for oncology
is the only realistic treatment option that allows for improving treatment, which reflects how fragmented provision is, a fact that
quality of life14. Palliative care along with other disciplines such as definitely does not benefit the patient. It is therefore necessary to
rehabilitation, nutrition and mental health are fundamental areas redefine the concept of oncology service under the comprehensive
of care in all phases of the disease and make up the oncological care approach and the importance of authorizing or enabling
support services, as proposed by the Cancer patient care Model4; units, comprehensive treatment centers and other forms of care
thus, pain and palliative care consultation was the third most that guarantee quality care with accessibility, comprehensiveness
offered and, among all consultations, oncological rehabilitation and continuity. The capacity of oncological services for the current
was the third least offered, these figures show the need to and future needs of the country is not yet exactly known.
strengthen these support services. Although this deduction is
subject exclusively to the classification of services in the registry Conflicts of interest:
of service providers, it does not exclude the fact that rehabilitation The authors state no conflicts of interest for this study
is incorporated during the service provided, and that services are
recorded as “general” rehabilitation. Similarly, palliative care and Funding:
pain counseling are not exclusive in cancer treatment, so the offer This study was carried out with national resources of investment of
for this specialty in oncology may be overrated. the National Institute of Cancer (National Cancer Network Program)

Strengths and limitations Referencias


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Original Article

Pediatric oncology services in Colombia


Servicios de oncología pediátrica en Colombia

Amaranto Suarez Mattos, Jairo Aguilera, Edgar Augusto Salguero, Carolina Wiesner

Instituto Nacional de Cancerología, Bogota, Colombia

Suarez MA, Aguilera J, Salguero EA, Wiesner C. Pediatric oncology services in Colombia. Colomb Med (Cali). 2018; 49(1): 97-101. doi: 10.25100/cm.v49i1.3377

© 2018 Universidad del Valle. This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use,
distribution and reproduction in any medium, provided that the original author and the source are credited.

Article history: Abstract Resumen


Received: 17 July 2017 Background: In low-income countries, a child diagnosed with Antecedentes: En los países de bajos ingresos un niño diagnosticado
Revised: 15 December 2017 cancer has an 80% chance of dying, while in high-income countries con cáncer tiene un 80% de probabilidad de morir mientras que en
Accepted: 12 January 2018 more than 80% survive the disease. In Colombia, a middle-income los países de ingresos altos más del 80% sobrevive a la enfermedad.
country, the government issued new legislation that promotes the En Colombia, un país de ingresos medios, el gobierno expidió una
Keywords:
generation of comprehensive care units; nevertheless, seven years nueva legislación que promueve la generación de unidades de atención
Medical care, comprehensive, after its expedition, no institution has been recognized as such by integral; sin embargo, siete años después de su expedición, ninguna
children, cancer, Colombia
the Ministry of Health. Institución ha sido reconocida como tal por el Ministerio de Salud.
Objective: To characterize the current offer of oncological services Objetivo: Caracterizar la actual oferta de servicios oncológicos para
Palabras clave:
for cancer care in children and to identify the institutions that atención de cáncer en niños e identificar las instituciones que podrían
Atención, integral, niños,
could be constituted in Units of Comprehensive Care of Childhood ser constituirse en Unidades de Atención Integral de Cáncer Infantil
cáncer, Colombia
Cancer in Colombia. en Colombia.
Methods: descriptive study of secondary source, it was consulted Métodos: estudio descriptivo de fuente secundaria, se consultó el
the Special Register of Health Providers of the Ministry of Health Registro Especial de Prestadores de Salud del Ministerio de Salud
and Social Protection, in order to identify the institutions that had y Protección Social; identificando las instituciones que tenían
enabled hospitalization services of medium or high complexity, habilitados servicio de hospitalización de mediana o alta complejidad,
chemotherapy, specialized consultation, emergencies, oncological quimioterapia, consulta especializada, urgencias, cirugía oncológica,
surgery, radiotherapy or nuclear medicine. The information is radioterapia o medicina nuclear. Se reporta la información en
reported in absolute frequencies. frecuencias absolutas.
Results: Seventy one institutions have hematology-oncology Resultados: Setenta y una instituciones cuentan con consulta de
consultation, 39 institutions have chemotherapy and hospitalization hemato-Oncología, 39 instituciones tienen servicios de quimioterapia
services of medium or high complexity, and 18 have radiotherapy y hospitalización de mediana o alta complejidad y 18 tienen habilitada
enabled. Only nine of the institutions include all the services that are radioterapia. Solo nueve de las instituciones incluyen la totalidad de los
necessary for comprehensive care. servicios necesarios para la atención integral.
Conclusion: Colombia has a sufficient supply of services for the care Conclusión: Colombia cuenta con una oferta suficiente de servicios para
of children with cancer. Only a minority are in institutions that have atención de niños con cáncer. Solo una minoría se encuentra en Instituciones
the capacity to guarantee the integrality of the attention. que tienen la capacidad de garantizar la integralidad de la atención.

Corresponding author:
Amaranto Suarez Mattos, Instituto Nacional de Cancerología . Cl. 1 #9-85,
Telefono +57 (1) 4320160. E-mail: asuarez@cancer.gov.co

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Introduction Materials and Methods


Cancer in children aged 0 to 14 is considered a rare disease, it This is a descriptive operational study that uses the Special
represents between 0.5% to 2% of all cancer cases in the world. Registry of Health Providers (SRHP) of the Ministry of Health and
It is estimated that 200,000 new cases of cancer in children aged Social Protection as a secondary source, consulted on August 29,
under 15 are diagnosed annually worldwide1. 84% of children 2016: This registry is permanently updated by the territorial health
dying from cancer live in countries with low or intermediate entities, which makes it changeable in time.
income, where there is limited access to health care and cancer
care2. Clinical results differ substantially; while in low-income To identify the institutions that provide health services (hereafter
countries a child diagnosed with cancer has an 80% chance of referred as  IPS) that can be constituted in CCCU, the technical
dying, in high-income countries over 80% survive the disease3,4. annex “Manual of Habilitation” was taken from the Ministry
of Health and Social Protection, which considers three central
In Colombia, cancer is the second cause of death after deaths for standards: organization or structure, management and health
external causes in the group of 0-14 years of age5. Each year, 1,322 outcomes13. The study defined in its scope of the first standard
new cases of cancer are diagnosed6. In the five-year period 1990- “Organization of the CCCU”.
95 the survival of children with Acute Lymphoblastic Leukemia in
Colombia was 40.9%; and for the five-year period 2005-9, it was The Habilitation manual describes the services with which CCCU
53.8%. Although it shows an improvement, the results are much meets the requirement of “it may provide” and have available for its
lower compared to other countries in America7. conformation: medium or high complexity hospitalization service
and chemotherapy service. In the same way and as a criterion in
The differences in the results between the countries have a the identification made in this study, the provider institutions that
multifactorial origin that involves a series of factors, such as the were enabled in the REPS services were taken into account such
social and economic determinants of each region6  Taking into as: Specialized external consultation, emergencies, oncological
account that it is a pathology of low frequency and high complexity, surgery, radiotherapy or nuclear medicine.
health systems need to organize their offer of services to guarantee
that access to the diagnosis and treatment of children with cancer The search was parameterized taking into account the following
is concentrated in institutions that have specialized human talent, variables: group of services, service code, name of the provider,
biomedical technologies and the necessary infrastructure for the level of complexity, legal nature of the provider and province. The
complexity of care. In this sense, twinning programs between search was oriented to IPSs and not to independent providers; the
hospitals located in countries with great experience and others search profile used was guest, the codes of the services consulted
located in low-income countries have allowed to improve survival8,9. were: 391 oncology and pediatric hematology consultation,
374 pediatric surgery consultations, 227 pediatric oncological
In Colombia there have been multiple barriers to access timely
surgeries, 709 chemotherapy, 711 radiotherapy, 715 nuclear
treatments for children with cancer: the delay by insurers in
medicine, 102 pediatric general hospitalizations, 501 emergency
the delivery of authorizations for care, the delay in the delivery
services.
of medicines, and the fragmentation of services and inter-
institutional transfers to achieve comprehensive care10,11. Due to The search strategy in the REPS focused on the following route:
these problems, the national government issued a new legislation
as legal support to reduce cases of death due to cancer in children 1. Identification of the initial universe of providers that prescribe
and persons aged under 1812,13. Colombian laws promote treatments in pediatric oncology: providers who had one of the
comprehensive treatment and they have delegated the Ministry following services enabled: pediatric hematology and oncology
of Social Protection to sector the services taking into account consultation and pediatric surgery consultation.
the demand needs and geographical location. They also created
the National Advisory Council for Childhood Cancer to follow- 2. Identification of qualified chemotherapy services in any form
up and monitor the implementation of these laws, as well as the of ambulatory or hospital care and pediatric hospitalization of
national policies and plans that derive from it. medium or high complexity.
Within the framework of this regulation, the creation of Child 3. 
Identification of support services and therapeutic
Cancer Care Units (CCCU) was defined as units “located in complementation of radiotherapy or nuclear medicine.
hospitals or clinics of level III and IV of pediatric complexity,
or with pediatric services of level III or IV”12. The definition of 4. Identification of emergency services and pediatric oncological
the concept of UACAI transformed the model of habilitation of surgery. This last result was converted for the study into the final
the pediatric oncological services towards a model in which the input that shows the potential number of institutions providing
provider institutions must guarantee the services related to the health services that can structure their services under a care
care of children with cancer, in order to guarantee the integrality strategy as CCCU (Fig. 1).
in the attention and the optimization of resources13. However,
seven years after its dissemination, the country does not have any For the analysis there were simple frequencies obtained by
UACAI recognized under that name by the Ministry of Health. province and by service. In a progressive manner, there were
In this sense, this article makes a descriptive analysis of the offer institutions excluded that did not have all the services that from a
of institutions providing health services in Colombia that could theoretical rather than a regulatory point of view should constitute
be constituted as Units of Comprehensive Care CCCU with the an UACAI, such as pediatric hospitalization, outpatient oncology
purpose of promoting its implementation.
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IPS with pediatric consultation of: The Province of Atlántico registers 13 institutions, a greater
Oncology, hematology and surgery. number than other Provinces that have capital cities with similar
Universe of Presenters with Pediatric Services (71 IPS) characteristics, such as Antioquia or Valle del Cauca, which register
a lower number of IPS, six and seven respectively; that way Atlántico
reports just the same number of IPS than the City of Bogotá D.C.
(Bogotá represents the entire Province of Cundinamarca).

IPS with hospital or outpatient chemotherapy and Among the 71 Healthcare Provider Institutions (IPS), 39
Pediatric hospitalization of medium or high complexity (39 IPS) institutions distributed in 15 Provinces “have/may provide”
chemotherapy and hospitalization services of medium or high
complexity (Table 1). The Provinces that did not meet the search
criteria for hospitalization services of medium and high complexity
IPS with radiotherapy or nuclear medicine services (21 IPS) and chemotherapy were Cesar, La Guajira, Magdalena and Meta.

Of the 39 registered IPS with qualified hospitalization services


of medium or high complexity and chemotherapy, the ones
that had support services and therapeutic complementation of
IPS with emergency services and pediatric radiotherapy or nuclear medicine were verified, being identified
oncological surgery. Potential UACAI (9 IPS) a total of 21 IPS distributed in 11 Provinces (Table 2). As it can
be seen, 18 IPS have enabled the radiotherapy service, 12 of them
Figura 1. Algorithm describing the results of the number of health service providers (IPS) in have enabled the nuclear medicine service and nine have the two
each of the searches carried out. services described above.

The number of institutions that met the requirements to establish


and pediatric hematology consultation and pediatric surgery themselves as CCCU were reviewed, that is to say, that they had the
consultation, chemotherapy in any form of ambulatory or hospital services to guarantee the integrality in the diagnosis and treatment
care and hospitalization, radiotherapy or nuclear medicine, of children with cancer. Table 3 shows that 9 of the IPS (located in
emergencies and pediatric oncological surgery. the Provinces of Atlántico, Santander, Valle del Cauca and Bogotá
City) met the criterion of concentrating the greatest number of
Results services in the same physical space. In relation to this, however, only
four of the nine IPS comply with pediatric oncological surgery offer,
According to the SRHP as of the cutoff date of August 29, 2016, eight with radiotherapy and seven with nuclear medicine.
there were 71 Provider Institutions of Health Services identified,
“Universe” of the country that has specialized consultation of Discussion
oncology and hematology or consultation of oncological surgery for
pediatric cancer care; they are distributed in 19 of the 32 provinces This study makes an analysis of the offer of pediatric cancer services
of the country. 69 IPS have a pediatric oncology and hematology in Colombia that fulfill the guarantees to establish a diagnosis and
consultation, and 11 also include oncological surgery (Table 1). comprehensive treatment for patients with cancer. According to

Table 1. Distribution by province of IPS with authorized services of pediatric oncological consultation, pediatric hospitalization of
medium or high complexity and chemotherapy.
IPS with Oncology and IPS with hospitalization IPS with both consultation
Province Number of IPS* IPS with oncologic surgery
hematology and chemotherapy services
Antioquia 6 6 4 0 0
Atlántico 13 12 5 2 1
Bogotá D.C** 13 12 9 4 3
Bolívar 3 3 3 1 1
Caldas 2 2 1 0 0
Cesar 2 2 NR 0 0
Córdoba 2 2 1 0 0
Huila 2 2 1 0 0
La Guajira 2 2 NR 0 0
Magdalena 1 1 NR 0 0
Meta 1 1 NR 0 0
Nariño 1 1 1 0 0
Norte de Santander 3 3 1 0 0
Quindío 1 1 1 0 0
Risaralda 4 4 3 0 0
Santander 4 4 3 2 2
Sucre 3 3 1 0 0
Tolima 1 1 1 0 0
Valle del Cauca 7 7 4 2 2
Total Colombia 71 69 39 11 9
Source: SRHP August 2016. Elaboration: self-made (study team)
* IPS with some service enabled under the SRHP service codes: 391, 374.
** Bogotá D.C. represents the Province of Cundinamarca.

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the study, it is found that of the 71 qualified institutions, that is, Table 2. Distribution by province of IPS with oncological consultation
guaranteed to offer oncological services for children with cancer, services, medium and high complexity pediatric hospitalization,
only 21 of them have hospitalization, a chemotherapy room, a chemotherapy, radiotherapy and/or nuclear medicine.
Hematology-oncology clinic and a pediatric oncological surgery Province
Number of
Radiotherapy
Nuclear
Both services
clinic; and only 9 (12%) of the institutions are able to guarantee the IPS Medicine
integrality of that care in Colombia. Antioquia 2 2 2 2
Atlántico 2 2 NR NR
High-income countries have defined the criteria that cancer Bogotá D.C 6 3 6 3
centers must fulfill in order to be able to offer care for inpatients Córdoba 1 1 NR NR
and outpatients diagnosed with childhood cancer. Emphasis Huila 1 1 NR NR
has been placed on the fact that the facilities must ensure timely Quindío 1 1 NR NR
Risaralda 1 1 NR NR
accurate diagnosis, the administration of intensive chemotherapy,
Santander 2 2 NR NR
emergency management for serious complications 24 hours a day,
Sucre 1 1 1 1
intensive care services, and timely and complete blood support
Tolima 1 1 NR NR
(blood bank) among others, and to have a network of hospitals
Valle del Cauca 321 3 3 3
that offer treatments as part of a shared attention14-16. This shared Total Colombia 21 18 12 9
network is important because the radiotherapy service is not always Source: SRHP August 2016.
found within the hospitals, and this does not stop the care from SRHP: Special Registry of Service Providers of the Ministry of Health and Social
Protection
being comprehensive, as long as the care is guaranteed if required, IPS:Institución prestadora de servicios de salud. (Healthcare Provider Institution)
particularly for cases of central nervous system tumors. This is the
case of the hospital network in Chile under the PINDA program16.
Faced with the objectives set in Colombia since 2010 11, the goal
Human talent is an essential requirement and institutions must of implementing comprehensive care for children with cancer has
have a multidisciplinary team led by pediatric hematologist/ not been achieved. In the first place, it is found that the resolution
oncologists with the support of pediatricians, subspecialists defining the rating of UACAI was only published in July 2016 12.
in some areas of pediatrics, pediatric surgeons, intensive Secondly, the authorization is voluntary, which means that the
pediatricians, rehabilitators, nurses and other professionals13,14. institutions do not have a motivation to do so, since a great effort
Since the number of cases of pediatric cancer is relatively low, to have all the required services is required. On the other hand,
the quality of treatment is guaranteed when the same institution it is allowed that the UACAI be located in centers of “medium
receives a significant volume of children with cancer. complexity,” and that they may have services outside the same
institution, which is a bit against the objective of having integral
Likewise, there must be available educational programs for patients treatment centers; with the exception of the service of radiotherapy,
and family members, school programs, including contact with which can certainly be shared by several institutions. This is how
teachers who teach students at home or hospital, as well as support the regulation states, for example, that the hospitalization service
with reincorporation to school, and social support programs to may be available outside the (health) institution if it only has
help families with their concerns about economic difficulties and ambulatory surgery enabled12.
about the treatment and expenses that are going to be incurred17.
A critical element that negatively affects the care of children and
Without compliance with these minimum conditions, it is very adolescents with cancer is that it allows potential CCCU not to have
difficult for children, adolescents and young adults to benefit 24-hour emergency services in the pediatric hematology-oncology
from the progress made in high income countries, due to the fact units as a requirement for habilitation, which is fundamental for
that an accurate diagnosis, adequate treatment, and medical and the care of children. In this regard, Dang-tan  et al.19, reported
social support care depend on a multidisciplinary team and an on the delays in the diagnosis of pediatric solid tumors that, in
infrastructure enabled in the institutions to treat cancer. general, the diagnosis was timelier when patients with suspicion
of cancer were treated for the first time in an emergency service.
According to the present study, 19 out of the 32 Provinces of On the other hand, and more importantly, is the need to have an
Colombia have a pediatric oncology service enabled, and these are immediate service for the complications caused by diseases or
concentrated in six provinces (Bogotá, Atlántico, Valle del Cauca, treatments that may endanger the lives of cancer patients.
Antioquia, Santander and Risaralda) which is adequate taking into
account that Cancer in children is a rare pathology. It is striking that Taking into account that the only source of information for
the Province of Atlántico, with a population approximately four times performing this study was the REPS, there are some limitations
smaller than the city of Bogotá, has the same number of institutions because only information related to infrastructure could be
with oncology services enabled. As a possible explanation to this included; the REPS does not allow to identify certain requirements
situation, it is found that most of the institutions that offer these demanded as “central of mixtures” or “program of pain and
services are private institutions that offer a broad service portfolio palliative care”; in the first case, the REPS does not identify these
regardless of their ability to guarantee integral conditions in the care physical environments; in the second case, it does not identify
of children with cancer. In Colombia, the authorization of health programs. The fact of being the only source of information
services has been allowed, such as outpatient services, chemotherapy constitutes its main weakness. It is desirable to supplement the
or hospitalization of children with cancer; without the need for information with other primary sources. It is also possible, even
them to be integrated within the same institution, which hardly though it is little feasible, for many providers to register authorized
guarantees a comprehensive and continuous care18. services that are not offering or that are inactive.
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Table 3. Distribution by Province of IPS with oncological consultation services, hospitalization and chemotherapy, radiotherapy or
nuclear medicine, pediatric surgery and emergency service.
Province Number of IPS Oncology and hematology Oncologic surgery Radiotherapy Nuclear Medicine Emergency services
Atlántico 2 2 0 2 2 2
Bogotá D.C 2 2 1 1 2 2
Santander 2 2 1 2 0 2
Valle del Cauca 3 3 2 3 3 3
Total Colombia 9 9 4 8 7 9
Source: SRHP August 2016
IPS: Institución prestadora de servicios de salud.

Conclusion 9. Rodriguez-Galindo C, Friedrich P, Alcasabas P, Antiñon F,


Branavali S, Castillo L, et al. Toward the cure of all children with
It is found that Colombia has an adequate offer of oncological cancer through collaborative efforts: Pediatric oncology as a global
services for children with cancer; however, this offer only challenge. J Clin Oncol. 2015; 33: 3065-73.
guarantees the integrality requirements in a small proportion.
10. Vera AM, Pardo C, Duarte MC, Suárez A. Análisis de la
Conflict of interest: mortalidad por leucemia aguda pediátrica en el Instituto Nacional
Nothing de Cancerología. Biomédica. 2012;32:355-64.

Referencias 11. Suárez A, Guzmán C, Villa B, Gamboa. Abandono del


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13. Ministerio de Salud y Protección Social. Resolución 1477 de
2016. “Por la cual se define el procedimiento, los estándares y los
2. Riveiro RC, Chantada GL, Arora RS, Antillon F, Kruger M, Barr
criterios para la habilitación de las Unidades Funcionales para la
RD. Pediatric oncology in country with limited resources. In: Pizzo
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SIOP PODC Initiative. Pediatr Blood Cancer. 2016; 63: 387–91. 16. Campbell M. Desarrollo de la oncología pediátrica en Chile.
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5. Piñeros M, Gamboa O, Suarez A. Mortalidad por cáncer infantil
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Publica. 2011; 30 (1): 15-21. of Care for Children with Cancer. Varsovia: SIOP Europa; 2009.
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Colomb Med. (Cali) 49(1): 97-101


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Original Article

Breast and cervical cancer survival at Instituto Nacional de Cancerología, Colombia


Supervivencia de cáncer de mama y cuello uterino en el Instituto Nacional de Cancerología, Colombia

Constanza Pardo1 and Esther de Vries2

1
Cancer Surveillance Group, Instituto Nacional de Cancerología, Bogota, Colombia.
2
Department of Clinical Epidemiology and Biostatistics, Pontificia Universidad Javeriana, Bogota, Colombia.

Pardo C, De Vries E. Breast and cervical cancer survival in Instituto Nacional de Cancerología, Colombia. Colomb Med (Cali). 2018; 49(1): 102-108. 10.25100/cm.v49i1.2840

© 2018 Universidad del Valle. This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use,
distribution and reproduction in any medium, provided that the original author and the source are credited.

Article history: Abstract Resumen

Received: 11 January 2017 Objective: to provide and compare estimations of two-year overall Objetivo: Describir las estimaciones de supervivencia global a dos
Revised: 19 February 2018 survival for cervical and female breast cancer in three cohorts (first años para mama (mujeres) y cuello uterino en tres cohortes (tratadas
Accepted: 06 March 2018 treated in 2007, 2010, 2012) at the Instituto Nacional de Cancerología por primera vez en 2007, 2010, 2012) en el Instituto Nacional de
of Colombia Cancerología de Colombia.
Keywords: Methods: All patients first treated at the Instituto Nacional de Métodos: Se incluyeron las pacientes tratadas por primera vez en el
Breast cancer, cancer of Cancerología for breast or cervical cancer in the years 2007, 2010, Instituto Nacional de Cancerología por cáncer de mama y de cuello
the uterine cervix, survival 2012, without a prior cancer diagnosis, were included for the uterino en los años 2007, 2010, y 2012, y quienes no habían tenido un
analysis, hospital-based,
registry, Colombia study. The hospital-based cancer registry was crosslinked with diagnóstico previo de otro cáncer. Se cruzaron las bases de datos del
governmental databases to obtain follow-up information on all registro hospitalario de cáncer con las gubernamentales para obtener
patients. Probability of surviving 24 months since the date of entry información de seguimiento de los casos. Se estimó la probabilidad
Palabras clave:
at the hospital was estimated using Kaplan-Meier methods, using the de sobrevivir a 24 meses a partir de la fecha de ingreso mediante el
Cáncer de mama, cáncer
de cuello uterino, análisis log-rank test to evaluate differences between groups. método de Kaplan-Meier. Se aplicó la prueba de rango logarítmico
de supervivencia, registro Results: We analyzed 1,928 breast cancer cases and 1,189 cervical para evaluar las diferencias entre los grupos.
hospitalario de cáncer, cancer cases, resulting in an overall survival probability at 24 months Resultados: Se analizaron 1,928 casos de cáncer de mama y 1,189 de
Colombia
of 79.6% (95% CI: 77.8-81.4) for BC and of 63.3% (95% CI: 60.6- cuello uterino. La estimación de la supervivencia global a 24 meses para
66.0) for cervical cancer, there were no differences in survival for year mama fue 79.6% (IC 95%: 77.8-81.4) y de 63.3% (IC 95%: 60.6-66.0)
of entry. Advanced clinical stage substantial affected overall survival, para cuello uterino, no se observaron tendencias en supervivencia con
being 32.2% (95% CI: 28.4-44.0) for stage IV breast cancer and 22.6% el año de ingreso. En los estadios clínicos avanzados la supervivencia
(95% CI: 11.4-33.8) for stage IV cervical cancer. global disminuyó en estadio clínico IV, tanto para cáncer de mama,
Conclusions: Breast cancer was the cancer with the best survival at 32.2% (IC 95% 28.4-44.0), como para cuello uterino 22.6% (IC 95%
Instituto Nacional de Cancerología; cervical cancer the one with the 11.4; 33.8).
lowest survival. Overall survival did not change over the years for Conclusiones: El cáncer de mama presentó mejor supervivencia en el
any of the cancers. Instituto Nacional de Cancerología frente al cáncer de cuello uterino.
La supervivencia global se comportó de manera estable con los años
para ambos tipos de cáncer.

Corresponding author:
Esther de Vries Department of Clinical Epidemiology and Biostatistics. Cra 7
No 40-62 Hospital San Ignacio. Piso 2, Bogotá, Colombia. Tel: (57-1)320 8320
Ext. 2813 Fax: (57-1) 320 8320 Ext. 2800. Email: estherdevries@javeriana.
edu.co
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Introduction Materials and Methods


The cancer burden among women in Latin-America is mostly All female invasive breast (C50) and cervical cancer (C53) cases
attributable to breast and cervical cancers1-3. In 2012 in Latin- first treated at the Colombian INC in the years 2007, 2010 and
America, age-adjusted breast cancer incidence rates reached levels 2012 were selected from the hospital-based cancer registry of
between 40-65 per 100,000 woman-years. Age-standardized breast the INC14. Only the first primary invasive cancer was considered
cancer mortality rates in Colombia increased substantially: from for each cancer, as the probability of survival of patients with
6.9 in the mid-1980´s (6.9) to 10.8 in 20124-6. Age-standardized previous primaries may be altered. The cases registered in each
cervical cancer mortality rates have come down from 13.2 in year were considered fixed cohorts. The hospital registry data was
1984-1988 to 8.7 in 20136. checked and completed using medical records and linked with
the hospital-based mortality database as well as government-
The Instituto Nacional de Cancerología of Colombia (INC) based information sources such as the National Civil Registry
estimated that in the period 2007-2011, around 7,600 new breast (Registraduría Nacional del Estado Civil (RNEC)) to determine
cancer cases were diagnosed annually, with 2,226 annual breast vital status at December 31st 2014 and date of death for deceased
cancer deaths. In the same period, there were 4,462 new cervical patients who died extramurally. This was necessary as the
cancer cases, and 1861 deaths. Both cancer types show strong Colombian legislation does not allow direct linkage between our
geographical variations between different parts of the country, patient databases and the cause- and date of death registry; if one
with breast cancer being more frequent in the cities and urbanized has the personal identification number, it is possible to check for
areas, and cervical cancer in the remote areas7. vital status and reporting of deaths in RNEC. Two-year overall
survival was calculated for the cohorts of women entering INC
The prognosis of these two cancer types depends on in 2007, 2010 and 2012, with start date of follow-up being the
sociodemographic characteristics but even more on the stage at date of entry at INC. Date of death was specified according to the
diagnosis, the available therapeutic options and the efficiency of death certificate in case this certificate was available, for those
the system in providing (access to) care. In general, cancer survival patients reported as deceased in the RNEC but without detailed
improves with Human Development Index (HDI) of countries or date of death, we determined the expected date of death as the
regions, probably through better access to efficient treatments and date of reported deceased at RNEC minus a correction factor.
potentially early detection. Colombia is currently categorized as a This correction was calculated based on data of deceased patients
high HDI country (0.720)8. Since 2003 the coverage of Colombia’s with available death certificates, where the real date of death
‘universal’ mandatory health insurance system has increased was compared with the date of reporting in RNEC; the median
substantially. This system consists mainly of two different regimes, difference between these dates was subtracted from the RNEC
each covering slightly under 50% of the population, in which date to obtain expected date of death15. This median number of
people are assigned on the basis of income: the contributory days of difference between date of death and reporting of the death
regime, covering workers and their families with an income decreased over time (for breast cancer it was 148 days in 2007,
above the cut-off and financed through the payroll and employer’s 66 in 2010 and 25 in 2012; corresponding number of days for
contributions and the subsidized regime, covering those identified cervical cancer were 184, 114 and 39 days), indicating substantial
as ‘poor’. Additionally, around 5% of the population, workers in improvements in the reporting systems. The detailed steps to
the petrol industry, teachers, military and police, is affiliated to determine date of last contact or date of death are described in
“special” and “exceptional” regimes; and is a remaining group of detail elsewhere, and summarized below15.
the population not being covered by the system (representing 2.6%
in 2015, according to the Ministry of Health)9,10. The insurance As this process is a bit complex, we described it in more detail below:
packages and methods are similar, but not equal between regimes
and providers within each regime. a) For patients who deceased within INC, the exact date of death
was known and assigned.
There are few available data on survival of these cancer types in
Latin American populations; the few population-based data do b) For patients with unknown vital status, we used the Colombian
not show survival by stage11,12. Trends in survival in hospital-based personal identification number (cédula) to check for vital status
settings are scarce13, with most existing reports aiming to determine in the databases of the RNEC - RNEC reports if persons are
the efficiency of the different therapeutic options. INC Colombia deceased. If the patients did not appear as “deceased” in any of the
designed a survival surveillance system, based on linkage with RNEC data sources, the 31st of December 2014 was assigned at
government databases, to produce comparable overall survival date of last follow-up.
estimates of its patients on an annual basis, with the objective of
evaluating changes in prognosis over time and contributing to the c) For those cases reported as deceased in RNEC but without death
improvement of the quality of cancer care within the institution certificate information, the date of death was estimated based on
and, through comparison of data, on a national level. the date of reporting of the death in RNEC, corrected for the
median difference between date of death and date of reporting of
In this manuscript we compare the demographical and clinical death at RNEC, as described above and in detail elsewhere15. If this
characteristics of breast and cervical cancer patients treated at procedure resulted in negative survival times, the date reported in
INC in the years 2007, 2010 and 2012 and report 2-year overall RNEC was assigned as date of death. This procedure generated the
survival estimated by age, clinical stage and type of affiliation to variable: calculated date of death.
the social security system.

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Table 1. Demographic and diagnostic characteristic of the study populationby cohorts


Breast cancer Cervical cancer
Characteristics
n (%) 2007 2010 2012 n (%) 2007 2010 2012
Total number 1,928 100 622 (32.3) 632 (32.8) 674 (35.0) 1,189 100 387 (32.5) 474 (39.9) 328 (27.6)
Age (yrs)
0 - 14 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0)
15 - 44 344 (17.8) 118 (19.0) 102 (16.1) 124 (18.4) 400 (33.6) 119 (30.7) 167 (35.2) 114 (34.8)
45 - 54 609 (31.6) 189 (30.4) 199 (31.5) 221 (32.8) 293 (24.6) 102 (26.4) 97 (20.5) 94 (28.7)
55 - 64 493 (25.6) 158 (25.4) 165 (26.1) 170 (25.2) 262 (22.0) 86 (22.2) 116 (24.5) 60 (18.3)
> 65 482 (25.0) 157 (25.2) 166 (26.3) 159 (23.6) 234 (19.7) 80 (20.7) 94 (19.8) 60 (18.3)
Social Security Scheme
Contributive 764 (39.6) 228 (36.7) 236 (37.3) 300 (44.5) 286 (24.1) 86 (22.2) 85 (17.9) 115 (35.1)
Subsidized 525 (27.2) 119 (19.1) 219 (34.7) 187 (27.7) 573 (48.2) 154 (39.8) 289 (61.0) 130 (39.6)
Special 168 (8.7) 50 (8.0) 50 (7.9) 68 (10.1) 45 (3.8) 9 (2.3) 9 (1.9) 27 (8.2)
Particular 256 (13.3) 90 (14.5) 80 (12.7) 86 (12.8) 98 (8.2) 30 (7.8) 39 (8.2) 29 (8.8)
Uninsured 215 (11.2) 135 (21.7) 47 (7.4) 33 (4.9) 187 (15.7) 108 (27.9) 52 (11.0) 27 (8.2)
Clinical stage
I 111 (5.8) 26 (4.2) 43 (6.8) 42 (6.2) 289 (24.3) 106 (27.4) 112 (23.6) 71 (21.6)
II 545 (28.3) 168 (27.0) 196 (31.0) 181 (26.9) 250 (21.0) 92 (23.8) 104 (21.9) 54 (16.5)
III 751 (39.0) 259 (41.6) 248 (39.2) 244 (36.2) 418 (35.2) 121 (31.3) 173 (36.5) 124 (37.8)
IV 141 (7.3) 34 (5.5) 54 (8.5) 53 (7.9) 54 (4.5) 14 (3.6) 21 (4.4) 19 (5.8)
No information 380 (19.7) 135 (21.7) 91 (14.4) 154 (22.8) 178 (15.0) 54 (14.0) 64 (13.5) 60 (18.3)

d) For those cases deceased according to RNEC but with only year of variables were assessed using the log-rank test. Univariate analyses
death known (no month or day available in RNEC), we assigned the were performed for year of entry, age in two categories (<50 y ≥50
30th of June of the provided year as date of death for patients with years), clinical stage and type of affiliation to the social security
date of entry in the first semester of a year, and 31st of December if system at the moment of entry at INC. Because of violation of the
patients entered INC in the second semester of a year. proportional hazard assumption for the variables year, age group,
and type of affiliation to the social security system, we did not report
e) For those cases for whom none of these methods could be results of the multivariate Cox Proportional Hazards models. All
applied, or who were not identified in the mentioned databases, data were analyzed using SPSS®, v19.
the last date of follow-up was assigned as the date of the last visit
according to the medical file at INC. Results
Statistical analysis Demographic and clinical characteristics of the patients
In order to assess differences in distribution of clinical stage by type We analyzed a total of 1,928 breast and 1,189 cervical cancer
of affiliation to the Colombian social security system, we performed patients.  Table 1  shows the characteristics by cancer type and
Fishers exact test. Survival time was calculated as the difference cohort; the distribution between breast and cervical cancer was
between the closing date of follow-up (December 31st, 2014), date shifting towards breast cancer over time. Breast cancer cases were
of last contact or calculated date of death and the date of entry at concentrated in the 45-54 years age group, and cervical cancer in the
the INC. The probability of surviving 24 months was calculated 15-44 years age group. The percentage of patients not affiliated to the
using Kaplan-Meier analysis, and differences in survival by several social security system decreased between 2007 and 2012 for both
90
Two years over all survival estimates (%)

80

70

60

50

40

30

20

10

0
2007 2010 2012 2007 2010 2012
Breast cancer Cervix uteri cancer.
Figure 1. Comparison of two year overall survival estimates for breast and cervical cancer by cohort

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Table 2. Distribution of cancer stage by type of affiliation to the social security system

Contributive Subsidized Uninsured Special Private


Tumour stage
% % % % %
Breast cancer stage
I 8.2 2.1 2.3 12.5 4.3
II 32.1 25.1 22.3 35.8 23.4
III 35.0 51.1 48.8 29.2 24.2
IV 6.9 8.6 13.5 3.0 3.5
No information 17.8 13.1 13.0 19.6 44.5
Cervical cancer stage
I 26.9 25.2 20.3 31.1 16.3
II 21.7 21.1 21.4 20.0 18.3
III 33.5 35.7 42.8 24.4 26.5
IV 5.2 4.4 5.4 2.2 3.0
No information 12.6 13.6 10.2 22.2 35.7
p-values for differences in stage distribution by regimen: Breast cancer: p= 0.01034, cervical cancer p <0.005

cancer types. There was an important proportion of cases without 1,535 cases were censored at follow-up. Two-year OS for breast
clinical stage information (19.7% for breast cancer, 15.0% for cervical cancer was 79.6%, with clear differences in survival between types
cancer); 100% of cases had a histologically confirmed diagnosis. of affiliation to the social security system, being highest for those
in the “special” regime (93.4%) (log-rank test 48.9, p <0.001). Few
Overall survival patients died in the first month of follow-up (1.9%). Two-year OS
Two-year overall survival did not vary between the different of stage I patients was very high (98.2%), declining to 36.2% for
cohorts, as shown in Figure 1. stage IV patients. No significant effects were found for year of or
age at entry at INC (Table 3, Fig. 2).
Breast cancer
The 1928 patients in the analyses had a median age at entry in Cervical cancer
INC of 55 years (range 17-99). Most (66%) patients were aged over The median age of the 1,189 women with cervical cancer was 51
50 and most of them (39.6%) were affiliated in the “contributive” years (range 19-92). Most were aged over 50, almost half (48.2%)
regime of the social security system. About half of the patients were affiliated to the subsidized part of the social security system,
had stage III-IV breast cancer at entry in INC. Stage distribution and almost 50.0% of patients presented at INC with stage I or II
differed substantially and statistically significantly between disease. The distribution by stage was similar between regimes,
regimes, with around 60.0% of women in the subsidized and with between 40 and 50.0% of women being diagnosed in stages
uninsured groups being diagnosed in stages III-IV, versus 42.0% I-II, with the exception of the privately insured women (34.6%),
in the contributive and around 30.0% in the special regime and who had a significantly better stage at entry (Table 2). At the end
privately insured group (Table 2). of the two years of follow-up, 435 (36.6%) had died, the remaining
754 cases were censored. The probability of surviving two years
At 24 months of follow-up, 393 (20.4%) had died, the remaining

Table 3. Univariate overall survival estimates of breast cancer and cervical cancer by cohorts
Breast cancer Cervical cancer
Number of Number of
Characteristics N % Surviving** CI 95% Log-rank test N % Surviving** CI 95% Log-rank test
deaths* deaths*
Total 1,928 393 79.6 77.8 - 81.4 N.A. 1,189 435 63.3 60.6 - 66.0 N.A.
Years of entry at INC
2007 622 32.3 122 80.4 77.3 - 83.5 X2= 4.1 387 32.5 135 65.0 60.3 - 69.7 X2= 3.7
2010 632 32.8 142 77.4 74.1 - 80.7 p= 0.127 474 39.9 177 62.6 58.3 - 66.9 p= 0.161
2012 674 35.0 129 80.8 77.9 - 83.7 328 27.6 123 62.3 57.0 - 67.6
Age (years)
<50 655 34.0 138 78.9 75.8 - 82.0 X2= 0.5 539 45.3 173 67.8 63.9 - 71.7 X²= 17.6
≥ 50 1273 66.0 255 80.0 77.8 - 82.2 p= 0.481 650 54.7 262 59.5 55.8 - 63.2 p= 0.000
Social Security Scheme
Contributive 764 39.6 147 80.8 78.1 - 83.5 X²= 48.9 286 24.1 102 64.2 58.7 - 69.7 X²=6.0
Subsidized 525 27.2 131 75.0 1.3 - 78.7 p= 0.000 573 48.2 201 64.8 60.9 - 68.7 p= 0.202
Special 168 8.7 11 93.4 89.7 - 97.1 45 3.8 16 64.4 50.5 - 78.3
Particular 256 13.3 52 79.6 74.7 - 84.5 98 8.2 46 52.6 42.6 - 62.6
Uninsured 215 11.2 52 75.8 70.1 - 81.5 187 15.7 70 62.4 55.3-69.5
Clinical stage
I 111 5.8 2 98.2 95.6 - 100.7 X2= 404.9 289 24.3 28 90.3 87.0 - 93.6 X2= 229.5
II 545 28.3 30 94.5 92.5 - 96.5 p= 0.000 250 21.0 61 75.6 70.3 - 80.9 p= 0.000
III 751 39.0 171 77.2 74.3 - 80.1 418 35.2 217 47.6 42.7 - 52.5
IV 141 7.3 90 36.2 28.4 - 44.0 54 4.5 41 22.6 11.4 - 33.8
No information 380 19.7 100 73.6 69.1 - 78.1 178 15.0 88 50.6 43.3 - 57.8
*Number of deaths in two years follow up
**Probability of surviving 2 years
N. A.= not applicable

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Breast cancer
a) b)
1 1
0.9 0.9
0.8 0.8
0.7 0.7

Global survival
0.6 0.6

Global survival
0.5 0.5
0.4 0.4
0.3 0.3
0.2 0.2
0.1 0.1
0 0
0 2 4 6 8 10 12 14 16 18 20 22 24 0 2 4 6 8 10 12 14 16 18 20 22 24
Time (months) Time (months)
I II III VI No information Contributive Subsidized Uninsured Special Particular

Cervix cancer
a) b)
1 1.0
0.9 0.9
0.8 0.8
0.7 0.7

Global survival
Global survival

0.6 0.6
0.5 0.5
0.4 0.4
0.3 0.3
0.2 0.2
0.1 0.1
0 0
0 2 4 6 8 10 12 14 16 18 20 22 24 0 2 4 6 8 10 12 14 16 18 20 22 24
Time (months) Time (months)
I II III VI No information Contributive Subsidized Uninsured Special Particular

Figura 2. Función de supervivencia a dos años (Kaplan – Meier) por estadio clínico y seguridad social, para
cáncer de mama (a y b) y de cuello uterino (c y d).

was 63.3%, with a better survival for women presenting at younger a bit lower than reports from USA-based studies, undoubtedly
ages (67.8%). During the first month of follow-up, 2.3% of patients related to a relatively late stage at entry in our patients, with 46%
died. There was a sharp gradient in survival by clinical stage at of women with stage III/IV disease.
presentation, between 90.3% in stage I and 22.6% in stage IV.
The quality of the Colombian death registry has improved
No differences in survival was observed by year or type of social substantially in recent years18, limiting, but not eliminating,
security (Table 3, Fig. 2). the possibility that some patients may have died without being
registered. In this case, the patient will have been censored alive
Discussion at her last visit in INC, which may have slightly over-estimated
survival rates. The improved quality is also reflected in the
These results are among the first of the overall survival surveillance diminishing of the time between date of death and reporting of
project of the INC; showing a stable two-year overall survival death in RNEC.
for breast and cervical cancer with the expec562-year survival
for breast (80%) and cervical cancer (63%) is not far from the The age distribution of our patients was as expected19,20. For the
population-based reports from Cali (3-year OS:breast 77%, cervix prognosis of breast cancer, early detection is important, as well as
63%)12. Survival in a specialized cancer hospital is expected to the time between first symptoms or abnormal screening test and
be a bit lower than the population-based survival data, because first consultation (according to a previous Colombian study this
specialized centers tend to receive “complicated” patients referred was >1 month in 34.1% of the patients) and the time between the
from other, less specialized hospitals. first consultation and treatment initiation (in 69.8% of patients
>3 months in a previous study)21. Cervical cancer patients were,
One limitation of our study is that we have no reliable incidence as expected, relatively young, and a substantial proportion (40%)
date, and therefore we had to use date of entry at the INC. The presented with late stage disease, a situation that could have been
survival time calculated from the date of diagnosis is certainly prevented by effective screening programs.
higher than our reported survival data, although we cannot know
how much higher: some patients come for their initial treatment to Unfortunately, we did not have information on clinical stage for
the INC - their date of entry will be close to their date of diagnosis; an important proportion of our patients (breast cancer 19.7% and
others come when initial treatment has failed or when they have cervical cancer 15.0%). However, our observations of around 50%
a recurrence, sometimes a long time after their initial diagnosis. of women being diagnosed in stage III/IV breast cancer and 40%
Considering this, our reported survival rates for cervical cancer in stage III/IV cervical cancer, despite this proportion of missing
are relatively similar to European estimates, lower than of the USA values, shows the very late stage at presentation of our patients. As
but higher than those for Brazil 11,12. Breast cancer survival is quite the proportional hazards assumption was violated, we did not run
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multivariate survival models. However, the differences in stage Worldwide: IARC CancerBase No. 11. Lyon, France: International
distribution by regime of affiliation, with lower stage at diagnosis Agency for Research on Cancer; 2013. Available from:  http://
of breast cancer in the contributive and special regimes as well globocan.iarc.fr. Accessed: 24/November/2016.
as privately insured women, explains the differences between
survival curves for breast cancer. Likewise, for cervical cancer, the 7. Pardo C, Cendales R. Incidencia, mortalidad y prevalencia de
better survival of the privately insured is most likely due to the cáncer en Colombia, 2007-2011. Primera edición. Bogotá, D.C:
earlier stage at diagnosis in this group of patients. Instituto Nacional de Cancerología; 2015. Available from: http://
www.cancer.gov.co/publicaciones?idpadre=1&idcategoria=59.
It is important to have a baseline idea of hospital-based cancer
survival, to evaluate tendencies and be able to act when necessary. 8. Selim J. Human development report 2015. New York, USA:
Counting with reliable data on cancer occurrence, stage and United Nations Development Programme; 2015. Available
survival is necessary for effective cancer control, at local and from: http://hdr.undp.org/sites/default/files/2015_human_
national level. development_report_1.pdf.

Conclusion 9. Guerrero R, Gallego AI, Becerril-Montekio V, Vásquez J. Sistema


de salud de Colombia. Salud pública Méx. 2011; 53(Suppl 2): s144-55.
Breast cancer and cervical cancer have, for international standards,
a poor survival, and this survival has not improved over time. 10. Ministerio de Salud y Protección Social. Informe al
The late stage at diagnosis undoubtedly plays an important role Congreso de la República 2014-2015. Sector Administrativo de
Salud y Protección Social. Bogotá: D.C: Ministerio de Salud y
in these relatively poor results and could be improved through
Protección Social; 2015. Available from:  https://www.minsalud.
changes in the early detection programs offered in Colombia.
gov.co/sites/rid/Lists/BibliotecaDigital/RIDE/DE/PES/informe-
The statistically significant differences in clinical stage by type of
congreso-2014-2015.pdf.
affiliation to the social security system is reflected in the survival
rates and shows the enormous potential for improvement in access 11. Allemani C, Weir HK, Carreira H, Harewood R, Spika D, Wang
to early detection, diagnosis and treatment of these cancer types. XS, et al. Global surveillance of cancer survival 1995-2009: analysis
of individual data for 25,676,887 patients from 279 population-
Acknowledgements:
based registries in 67 countries (CONCORD-2). Lancet. 2015;
We would like to thank Jenny Patricia Castro for her help in
385(9972): 977-1010.
searching and updating the information of the hospital-based
registry and linking the follow-up information. 12. Bravo LE, García LS, Collazos PA. Cancer survival in Cali,
Colombia: A population-based study, 1995-2004. Colomb Med
Conflicts of interests: (Cali). 2014; 45(3): 110-6.
We have no conflicts of interests to declare
13. Carneseca Mauad EC, de Araujo MA, Dalbó RM, Longatto
Funding:  Filho A, Vazquez Vde L. The Hospital de Câncer de Barretos
This work was performed with financial support of the Instituto Registry: an analysis of cancer survival at a single institution in
Nacional de Cancerología allocated to the Cancer Surveillance Brazil over a 10-year period. BMC Research Notes. 2013, 6:141.1
programme of this institution
14. Instituto Nacional de Cancerología. Registro institucional de
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Colomb Med. (Cali) 49(1): 102-108

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Technical report

Cali cancer registry methods


Métodos del Registro de Cáncer en Cali, Colombia

Luz Stella García1, Luis Eduardo Bravo1,2, Paola Collazos1, Oscar Ramírez1,4,5, Edwin Carrascal1,2, Marcela Nuñez1, Nelson Portilla1,
Erquinovaldo Millan3

1
Registro Poblacional de Cáncer de Cali. Cali, Colombia
2
Departamento de Patología, Facultad de Salud, Universidad del Valle, Cali, Colombia.
3
Secretaria de Salud Pública Municipal de Cali, Cali, Colombia.
4
Fundación POHEMA. Cali, Colombia
5
Sistema de Vigilancia Epidemiologica de Cáncer Pediátrico (VIGICANCER), Cali, Colombia

García LS, Bravo LE, Collazos P, Ramírez O, Carrascal E, Nuñez M, Portilla N, Millán E. Cancer Registration in Cali, Colombia. Colomb Med (Cali). 2018; 49(1): 109-120.
Doi: 10.25100/cm.v49i1.3853

© 2018 Universidad del Valle. This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use,
distribution and reproduction in any medium, provided that the original author and the source are credited.

Article history: Abstract Resumen


Received: 20 December 2017 Background: The Cali Population Registry of Cancer Registry of Cali Antecedentes: El Registro Poblacional de Cáncer de Cali (RPCC)
Revised: 30 January 2018 (RPCC) has operated since 1962, disseminating high quality information opera de manera continua desde 1962 divulgando información
Accepted: 13 February 2018 to provide a framework to assess and control the burden of cancer in Cali. de calidad para proporcionar un marco para valorar y controlar
Methods: The collection of new cancer cases in permanent residents el impacto del cáncer en Cali.
Keywords: of Cali is done through active search in and notification from hospi- Métodos: La recolección de los casos nuevos de cáncer en
Cancer registry, methods, tals, and public and private laboratories. The Secretary of Municipal residentes permanentes de Cali se hace mediante búsqueda
data management, Cali, Public Health provides individual information on general mortality activa y por notificación en los hospitales y laboratorios públicos
Colombia
and death from cancer. Tumors are coded with ICDO-3 and mortality y privados. La Secretaria de Salud Pública Municipal proporciona
with ICD-10. Presented rates are standardized by age and trends are la información individual de mortalidad general y por cáncer.
Palabras clave:
assessed by estimating the percentage annual change using the regres- Los tumores se codifican con la CIO-3 y la mortalidad con la
Registro de cáncer, métodos,
sion analysis in JoinPoint. The 5-year net survival was analyzed with CIE-10. Las tasas se estandarizan por edad y la tendencia se
manejo de datos, Cali,
Colombia the Pohar-Perme estimator. estudia con el porcentaje de cambio anual y con la regresión
Results: 88.5% of the registered cancers had morphological verifica- de JoinPoint. La supervivencia neta a 5 años se analizó con el
tion (MV). The proportion of unknown primary site represented 5% estimador de Pohar-Perme.
and the death certificate only cases (DCO) varied between 0 to3% de- Resultados: El 88.5% de los canceres tuvieron verificación
pending on the cancer site. All deaths were certified by a physician, morfológica (VM). La proporción de los casos codificada
94.2% of cancer deaths were correctly certified. The ill-defined site como de sitio mal definido representó el 5% y el certificado
proportion was 5.3% and that of uterine cancer not specified (C55) de defunción como única evidencia del diagnóstico de cáncer
was 0.5%. For survival analysis, existing data collection procedure (DCO) varió entre 0-3% dependiendo de la localización. Todas
and infrastructure ensures assessment of the patient’s vital status and las defunciones fueron certificadas por un médico, el 94.2% de
follow-up, with an average lost to follow-up of 13.2%. las muertes por cáncer fueron bien certificadas. La proporción
Comment: The information has been published in the eleven volumes de sitio mal definido fue 5.3% y la de cáncer de útero no
of "Cancer Incidence in Five Continents" confirming high quality of especificado (C55) fue 0.5%. En todos los casos de supervivencia
the collected data. The RPCC PCRC has also participated in the Con- fue posible el seguimiento y la proporción de censuras fue 13.2%
cord Study and is participating in SURVCAN-3. Comentario: La información ha sido publicada en los once
volúmenes de “Cancer Incidence in Five Continents”. El RPCC
participó en el Estudio Concord y está participando en SURVCAN-3.

Corresponding author:
Luz Stella García, Registro Poblacional de Cáncer de Cali. Calle 4B 31-00
Oficina 4003, Edificio 116, Cali, Colombia. E-mail: luz.garcia@correounivalle.
edu.co
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Introduction Obtaining new cases of cancer


Population and registration area
The Population Cancer Registry of Cali (RPCC) was started in Cali is the third largest city in Colombia, capital of the Province of
1962 as a research program of the Department of Pathology of Valle del Cauca, located by the Cauca river valley at coordinates
the Universidad del Valle. It was initially funded by a donation 3°27’00” N 76°32’00” W. The western limit is the Farallones of Cali,
from the Ana Fuller Fund. Later, La Universidad del Valle became which are part of the Western Cordillera of the Colombian Andes.
the main source of both financial and scientific resources of the According to both the 2005 census and National Administrative
registry. The RPCC began at the same time as Pan American
Department of Statistics of Colombia (DANE) projections, the
Health Organization (PAHO) conducted the Urban Mortality
estimated population for 2010 was 2.3 million inhabitants, 52%
Study, which examined in detail all the death certificates of the
are women, and 26.2% self-identify as belonging to the black
city 1. The systematic study of these certificates was part of the data
collection for the RPCC2. ethnic group5,6. The life expectancy at birth was 73.1 years for
men, and 78.5 years for women7. The facilities for oncological care
Cancer registries are systems that collect information in a includes165 oncology services8, located in the urban area, where
continuous and systematic way about each new cancer case 95% of the population resides in an area of ​​110 km2. This area
identified within a specific population in a given area and period3. corresponds to 20% of the extension of the municipality of Cali
There are two types of cancer registries that complement each (561.7 km2)9; Administratively Cali was divided into 22 communes,
other, although they have distinct procedures and objectives: the with a gross density of 4,094.7 inhabitants/km2. The rural land
population-based cancer registry (PBCR) and the hospital-based is approximately 424.4 km2  (divided into 15 corregimientos or
Cancer Registry (HBCR). The HBCR records all cases that go to designated areas)  9 with a gross density of 0.83 inhabitants/km2.
a health center or specialized service, regardless of their place In 2012, the municipality of Cali was defined as the cancer registry
of residence, for administrative and patient care purposes. The area. The geopolitical map is shown in Figure 1.
purpose of the PBCR is to identify all new cases of cancer that appear
among the inhabitants of a well-defined, natural or administrative Case definition
demographic area. The main objective is to produce information People of any age, residents in the urban area of ​​Cali, with
to provide a framework to assess and control the impact of cancer a diagnosis of invasive malignant tumor for the first time
on health of the community. Some registries might be specialized
(incident), of any anatomical location, that has been confirmed
on one or several tumor location(s) are called Monographic;
or treated in partial or in total. The basis for diagnosis can be both
and can be both hospital-based and population-based. Central
cancer registries gather and consolidate information from several microscopic (fluid cytology, peripheral blood and bone marrow,
registries that cover different areas, which can also be population- histology of primary tumors and autopsy); and non-microscopic
based or hospital-based3. (clinical, surgical and imaging diagnosis). The following cancers
were included: single or multiple primary malignant tumors, all
The value of the modern cancer registry and its ability to carry out tumors of the Central Nervous System and  in situ  breast and
cancer control activities depend to a large extent on the underlying cervical cancer. Excluded are benign tumors with uncertain
quality of its data and the established quality control procedures4. behavior, malignant tumors of metastatic sites, and basal cell
In this article, the Population-based Cancer Registry of Cali shows and epidermoid carcinoma of the skin (these were included until
a standardized methodological guide and maintains the quality 1986). The cases that arrived in the city for treatment or diagnosis
criteria for a reliable information system to estimate the burden purposes are not considered residents of Cali.
of cancer in Cali.

Yumbo

Rural
area of Cali
Palmira

Rural
area of Cali

Urban
area of Cali

Communes (administrative division)


Health care center
Rural area of Cali
Urban area of Cali

Figure 1. Cali-Valle del Cauca-Colombia geopolitical map. License: http: //creativecommons.org/licenses/by-sa/3.0/deed.es Modified by: Tejido
creativo Cali-Colombia

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Pediatric cancer head quarter (287 m² area) with 15 employees working in the
In 2009, an information system was setup within the RPCC for registry. The head of staff and his advisors are senior researchers
the continuous monitoring of clinical outcomes of children and pathology professors at the School of Medicine. The
with cancer treated in Cali (VIGICANCER). Details have been coordinator is a business administrator with a master’s degree
published earlier  10. In summary, the system, in addition to the in epidemiology and the information system is managed by an
registry of incident cases, actively follows children under 19 engineer with a master’s degree in engineering with emphasis in
years old treated in pediatric oncology units in Cali. The system systems engineering and computer science. There are three data
includes both residents of the city and patients referred from collectors. The staff has job stability due to university affiliation
other municipalities and departments. As part of the RPCC, it that provided permanent contracts. The RPCC assures stability
also receives information from secondary sources, achieving to the rest of the human resources using specific projects funds.
an exhaustiveness of around 94% and a follow-up of 95% of The Information Technology network includes an intranet
registered cases. The outcomes under surveillance are the vital with Internet access supported by the Office of Information
status, relapses, abandonment of treatment and second primary Technology and Telecommunications of Universidad del Valle.
cancers. This system continues to monitors patients who leave The local network includes a server, 11 computers and 5 laptops.
treatment and, if their vital status is unknown, they are included Backup copies are made twice a day by means of an automatic
as events for survival analyzes. The observed survival is reported, daily script and a monthly external copy. The technical team
using the Kaplan-Meier method. of the RPCC meets weekly to resolve the problem cases. The
software of the RPCC (Siscan) performs consistency checks when
Comparability of the basic data collected entering the data and the internal consistency is checked every
The basic information for the RPCC is collected in a pre-coded six months with IarcTools15. Before sending the information to
form that includes data of the person: name, sex, date of birth, age, international collaborators or external projects such as the IARC
and address. Neoplasms are described with anatomical location, and the CONCORD program, the whole data set is rechecked
morphology, behavior and, degree of differentiation, multiple with IarcTools15.
primary tumors, the extent of disease (breast and cervix) and the
most valid basis of cancer diagnosis. Periodic survey of medical specialists
The three-yearly survey of medical specialists in the city is a key
For the last 20 years, information on the outcomes has been activity in which several groups of students from the Faculty of
collected: date of last contact, vital status, date of death, and cause Health of the Universidad del Valle have participated. This survey
of death. Neoplasms in adults are coded with ICDO-311, whereas lasts for eight weeks and complements the continuous cancer data
in children with ICCC-312. collection by the RPCC. As an initial step, the inventories of sites
that have oncological services for the diagnosis and treatment of
To calculate date of incidence we used the guidelines of the cancer that are not covered during routine collection activities
European Network of Cancer Registries (ENCR)13  and this are updated. The Faculty of Health of the Universidad del Valle
corresponds to the date of the first histological or cytological is contacted, and the participating students are trained in biology,
confirmation of cancer. For the classification of multiple primary cancer nomenclature, and the methodology standardized to
tumors, the IARC / IACR guidelines14 were used, which are also obtain cancer cases. Each participant is assigned a supervisor
used elsewhere around the world, to report the incidence rates. (member of the RPCC) and support materials are provided that
include: 1) General recommendations; 2) minimum variables for
Confidentiality of information
collection; 3) list of malignant tumors; 4) manual for completing
The guidelines of the European Network of Cancer Registries
the form of the cancer morbidity survey; 5) list of assigned
(ENCR)13 are followed. The director of the RPCC is responsible
specialist physicians; 6) cover letters; and 7) collection forms. The
for the security of the information. All the staff members of
supervisor has permanent contact to clarify doubts and concerns
the RPCC sign an agreement to guarantee the protection of
and receive weekly update of the information collected.
the confidentiality of the data on the persons whose cancer
is informed to the RPCC. Access to the physical space of the Procedure for obtaining new cases of cancer
Registry is restricted to authorized persons only. The access to the Figure 2 summarizes the procedures for collecting information to
confidential information is carried out using personal passwords obtain new cancer cases among permanent residents of Cali. The
that permit access to the computers holding the classified information is in physical format and structured and unstructured
information and additionally closed files are used. Any data that digital formats; and the extraction of the variables of interest is
is not used is automatically destroyed. done in several phases manually or automatically.
A single person (administrator) makes initial matching between
Figure 3 shows the procedures for detection of duplicate cases,
databases to detect new cases and update vital status information.
multiple tumors, updating vital status, date of last contact,
A registration number is assigned to each case and the information
residence and identity of each new case of cancer. The procedures
that identifies a patient is deleted before the data is analyzed
involved three phases, which are as follow:
(name and other documents that can lead to identification of the
patient).
Phase 1. Extraction of information
Facilities This is done through active search and manually when the
Universidad del Valle has been the main source of financial information is in physical format and structured and unstructured
and technical resources. The research group at RPCC has a digital formats; or automatic to obtain structured and unstructured

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Linkage Linkage

Clinical and Data source:


Diagnostic Death Certificates
Hospital Public & Paper or Private Physicians
Labs
Private Electronic Forms

Triennial Annual

Diagnostic
Linkage Cali
Labs Periodic
Continuous Population-based
Collection Cancer Registry Collection

Discharges
Linkage
Summaries
3. Eliminates potential
Duplicate records

Figure 2. Population Cancer Registry of Cali (RPCC). Procedure to obtain new cases of cancer among permanent residents of the city through active
search and notification. Collection is continuous in diagnostic laboratories, hospitals and clinics; public and private. The collection is periodic (annual
and three-yearly) in the Municipal Public Health Secretariat (for death certificates), and in the physician office´s. The information is integrated into the
database of the RPCC, through individual search or with matching between databases (linkage).

Extraction list

WORD PDF EXCEL PLAIN

Phase 1
Extraction and Linkage
Linkage

Yes No Approximate
Exact Search ID Number
Search

R.P.C.C

Phase 2
Phase 3
Update
Incidence Case
No
Registered Search

Health Yes
Insurance Health
Insurance
No more No Get
Found Search
Information Mortality ID Verification
Mortality

Yes Discharges Discharges


Summaries Summaries
Clerical Review
Merge IARC 2004 (1)
Notification Berg (2) Rules
Systems Notification
Systems

Multiple
Identification Residence Vital Status Tumor

Record with input No


Found
data
No
Flag:
Yes No Identification
Alive
Residence Yes
Vital Status Yes

Complete
Update Duplicate
Identification

Residence

Vital Status

Incidence
Case

Figure 3. Exact search procedures (personal identity document) to detect duplicate cases, multiple tumors, update vital status, date of last contact,
residence and identity of each new case of cancer.

listings. Hospital expenditures are obtained periodically in a Phase 2. Update of the information
structured digital format. With an automatic process of data When the cases already exist in the base of the RPCC (prevalent
extraction, for each case a matching with the database of the cancers), additional information is sought in the health insurance
Population Cancer Registry is done in two methods: Exact search databases (public and private), general mortality in the city, and
(Fig. 3) and Search by approximation (Fig. 4). hospital discharges from clinics and hospitals in Cali. Information
of identification, residence, date of last contact and vital state is
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Aproximate Search
Linkage

Extraction
list Health Discharges
RPCC Mortality
Insurance Summaries
Dataset A
Dataset B

Splitting Names

Cleaning and Surnames Strong


Standardisation Field

Date of birth
Blocking
Indexing

Field
Comprasion Address
Optional
Phone Field
Weight Vector Number
Classification

Possible
Matches Non Matches Clerical Reviewt
Matches

Evaluation Flag

Figure 4. Approximate search procedures when there is no personal identity document.


Pairing with the Population Cancer Registry database using the approximate search method

recovered; these updated variables are marked as completed Procedures for the analysis of incidence and mortality
(Flag) and the case is excluded for future searches. The revised The International Classification of Diseases (ICD-10)17 is used for
rules of the IARC 200414 is used to allow detection of multiple the coding of cancer. The main locations were defined according
primary tumors. to the guidelines suggested by the IARC for the analysis of the
incidence information; and by the WHO to group the primary site
Phase 3. Inclusion of new cases of the tumor and the causes of (cancer) death18,19. The structure of
In phase 3, cases that are not found in the main database of the the population by sex and five-year age groups for each calendar
cancer registry are processed. First, the three additional data year was obtained in the DANE5. The incidence and mortality
sources are searched (Fig. 3) to find additional information that rates for the entire population were standardized by age (ASR) by
allows identification, residence and vital status to be completed. means of the direct method, using as reference the world standard
Afterwards they are entered into the main database as a new case population20,21. The global and specific rates by age and sex are
of cancer (incidence). If additional information is not retrieved in expressed by 100,000 person-years. Trends in incidence rates were
the auxiliary databases, the case enters with only the data obtained analyzed over ten 5-year period from 1962 to 2012; and those of
in the extraction phase. mortality during six five-year periods, from 1984 to 2015. The
summary measures to assess the trend of the rates over time was
Search by approximation the annual percentage change (APC), calculated by the minimum
It is used when there is no information on the personal method weighted squares22. For some locations and age groups it
identification document (Fig. 4). The two sets of data to be was impossible to estimate the APC because in some years there
compared are prepared namely data set (A) that are the extraction were no new cases or cancer deaths in these categories.
lists which contains the possible new cases of cancer and data set
(B) which is the database that contains the information system Procedure for survival analysis
of the RPCC. First the data set is divided into smaller groups to Selection criteria
optimize matching, then standardized and indexed by blocks of Individual data from 38,671 permanent residents of Cali during
similarity between two fields (names and date of birth), finally the period 1995-2009, aged between 15 and 99 years, with a
a weighted vector classification is made, where a threshold diagnosis of a first invasive malignant tumor in one of the following
of similarity, the result is two groups of records: those that are fourteen locations defined by the ICD-10 were included for the
estimated as potentially equal and those that are considered as a analysis. (WHO, 2012): Stomach (C16), colorectal (C18-C20),
possible match whose process continues with a manual review, liver (C22), lung (C34), melanoma (C43), breast (C50), cervix
the records are evaluated to be paired between the two data sets 16. (C53), ovary (C56), prostate (C61), thyroid (C73), Hodgkin’s
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lymphoma (C81), non-Hodgkin’s lymphoma (C82-C85, C96), Follow-up: To update the vital status and the date of last contact,
multiple myeloma (C90), and leukemia (C91-C95). Following links were established between the RPCC information system and
the Concord-2 study guidelines23, the groups of solid tumors the following databases: a) general mortality of the Municipal
were defined by the anatomical site and the leukemias by their Public Health Secretariat of Cali; b) hospital discharges from Level
morphology. The coding of the topography and morphology was III institutions; c) Identification System for Potential Beneficiaries
done with the International Classification of Disease for Oncology, of Social Programs (SISBEN, 2016); and d) Private health
third edition (ICD-O-3)11. All malignant haematopoietic diseases insurance companies (2014). Process is described in Figures 3 and ​
were included according to the range of morphological codes of and44.
the ICD-O-3 from 9.590 to 9.999.
Analysis plan
Excluded from the survival analysis are tumors identified as  in The response variable was the time between the diagnosis of cancer
situ, benign or of uncertain behavior, subjects with unknown and the death of each individual. The maximum observation time
ages, tumors detected during necropsy, cases diagnosed only for each subject for the failure to occur was five years. The censored
through death certificate, and the syndromes myelodysplastic and variable was applied for patients who did not present the fault
myeloproliferative neoplasms such as chronic myeloid leukemia. within the study period, and as a mechanism of censorship the loss
Patients with synchronous bilateral breast cancer were included was established during the follow-up and the end of the study. For
and treated as individual cases for the analysis. the analysis, survival times greater than five years were censored,
times after the loss to follow-up and / or as of December 31st, 2009.
Event definition, start and end date
Death from any cause was considered an event in the survival For the five-year periods 1995-1999 and 2000-2004, a cohort
analysis. The survival time of each case was determined by the analysis was performed because all patients diagnosed with cancer
difference in time (in days) between the date of diagnosis (index during that period had at least five years of follow-up data until
date) and the date of death, the date of last contact, or the date of December 31, 2009. For the 2005-2009 period, survival analysis
the end of the study, which was defined as December 31, 2009. was carried using the period method24, given that there is no
To compare the survival changes during the study period, the 15- complete 5-year follow-up for patients, as shown in Figure 5. The
year study period was divided into three: a first period between number in each cell indicates the minimum number of years of
January 1, 1995 and December 31, 1999 that coincided with the follow-up completed by patients at the end of a specific year.
implementation of the health reform in Colombia; and the other
two periods; 2000-2004 and 2005-2009; after the implementation For the 5-year net survival estimates, the Pohar-Perme estimator
and consolidation of Law 100. was used  25. Life tables of the general population of Cali in one-

Follow up Year
1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009
1995 1 1-2 2-3 3-4 4-5 5
1996 1 1-2 2-3 3-4 4-5 5
1997 1 1-2 2-3 3-4 4-5 5
1998 1 1-2 2-3 3-4 4-5 5
1999 1 1-2 2-3 3-4 4-5 5

2000 1 1-2 2-3 3-4 4-5 5


2001 Cohort approach 1 1-2 2-3 3-4 4-5 5
2002 1 1-2 2-3 3-4 4-5 5
Diagnosis Year

2003 1 1-2 2-3 3-4 4-5 5


Period approach

2004 1 1-2 2-3 3-4 4-5 5

2005 1 1-2 2-3 3-4 4-5


2006 1 1-2 2-3 3-4
2007 1 1-2 2-3
2008 Cohort approach 1 1-2
2009 Period approach 1

Figure 5. Cali Cancer Population Registry. Monitoring structure for the analysis of survival of cancer cases in permanent residents of Cali during the 1995-2009 interval
with follow-up until 2009-12-31. Three 5-year periods were analyzed: 1995-1999, 2000-2004 and 2005-2009. Cohort approach between 1995-2004 and between 2005-2009.
In contiguous cells the complete tracking of an interval was described. Example: All patients with a diagnosis in 1995 complete one year of follow-up in 1996, except for
those diagnosed in 1995-01-01.

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Table 1. International Cancer Survival Standards (ICSS) used for standardizing survival by age according to cancer site. Age classes and
weighting for three types of cancer incidence age patterns.
ICSS-1 ICSS-1* ICSS-2 ICSS-3
Group age Weight Group age Weight Group age Weight Group age Weight
15-44 0.07 15-54 0.19 15-44 0.28 15-44 0.6
45-54 0.12 55-64 0.23 45-54 0.17 45-54 0.1
55-64 0.23 65-74 0.29 55-64 0.21 55-64 0.1
65-74 0.29 75-84 0.23 65-74 0.2 65-74 0.1
75+ 0.29 85+ 0.06 75+ 0.14 75+ 0.1
Total 1   1   1   1
ICSS-1*: Prostate (C61)
ICSS-1: Stomach (C16), colorectal (C18-C20), liver (C22), lung (C34), breast (C50), ovary (C53), non-Hodgkin's lymphoma (C82-C85, C96), multiple myeloma
(C90), leukemia (C91-C95)
ICSS-2: Melanoma (C43), cervix (C53), thyroid (C73)
ICSS-3: Hodgkin's lymphoma (C81)

year age group, by sex and for each calendar year from 1995 to The percentage of cases with morphological verification (MV)
2010, were provided by the Concord-2 study23. Estimates of 5-year -histology, cytology, bone marrow aspiration and flow cytometry-,
net survival were standardized by age to allow comparisons over for all cancer sites was 88.5% ranging between 85-100%, except
time or with different cancer populations and with different age in the liver (68.3%) and lung (66.4%). In patients with leukemia,
distributions. The three main cancer sites with similar incidence Hodgkin’s lymphoma and melanoma the MV was 100%.
patterns by age were taken into account and the weights of the
International Standard for Survival of Cancer, International The percentage of cases with a death certificate only (DCO) varied
Cancer Survival Standard ICSS 26 (Table 1) were implemented. between 0-3%, except in the liver (4.5%) and in the lung (6.0%).
In general, for major cancer sites, they had a low percentage of
Exhaustiveness assessment by death certificate method cases obtained through death certificate only. Another indicator
To verify the exhaustiveness, the death certificate method of quality that is also usually considered is the proportion of
was used  27. The principle is illustrated in  Figure 6. Individual cancer cases that was coded as poorly defined site. Between the
certificates of general mortality from all causes are received years 2008-2012 these tumors represented 4.6% of new cases of
annually in a structured file in a digital format with information cancer in men and 5.4% in women.
on causes of death in text and the basic cause codified with ICD-
10  17. We reviewed the causes of death to detect cancer cases Quality indicators of survival information
that were not coded as cancer in the basic cause; and a variable During the 1995-2009 period, 40,354 cases of the selected cancers
is created to identify cancer cases (ICD-10: C00-C97; D05-D06, were registered, 1.73% occurred in patients under 15 years. In 2.4%
D32-D33, D45-D46, D47.1, D47.3). The initial pairing with the there was no age information and they were excluded from the
RPCC database allows to identify the prevalent cases that have analysis. All patients had follow-up and 13.2% of the observations
died, the vital status and the date of death are updated. New cases were censored; this proportion was higher in brain, melanoma,
reported annually through the death certificate are included in the colorectal and ovarian cancers. In cancers with poor survival:
RPCC database and are identified in a variable such as DCN. These stomach, lung, liver and pancreas; the censored rate was less
cases will then be updated when the RPCC data collectors obtain than 10%. In the most frequently diagnosed cancers the censored
newer information from the biopsy, the bone marrow aspirate, or percentage was 10.1%, 11.5% and 16.4%; for breast, prostate and
the flow cytometry; the diagnostic method is updated, from death cervix, respectively. In 15.3% of the cases the date of death and the
certificate to diagnosis by morphology. The active and continuous date of incidence were the same.
search of cases excludes some cases of mortality that are not
related to cancer; and which will be used to update, once more, Quality indicators of cancer mortality certification
the diagnostic method that will convert from death certificate Mortality due to cancer represented 18.0% (23,793 / 132,397) of
to diagnosis by clinical or by images. Finally, there is a remnant the total deaths that occurred in the city during the period 2006-
of cases whose only information came from death certificate 2015. 0.8% of the cases were not coded as cancer in the basic
(DCO). The proportion of unregistered cases that remained cause. All deaths were certified by a physician; the proportion
alive was estimated with the proportion of cases initiated by the of poorly defined site (C76-C80, C97) was 5.3% and that of the
death certificate (DCI) and the mortality: incidence ratio (M: I). uterine cancer not specified (C55) was 0.5%. Only 4 (0.02%) of
Exhaustivity = 1−DCI *(1M:I)/(1−DCI) the death certificate cases did not have age information. 94.2% of
cancer deaths were well certified.
Results
All patients died from cancer during the 2008-2012 period were
Indicators of quality of the incidence information
The main quality indicators for some selected cancer sites are found in the cancer registry database. For recognized sites of
presented in  Table 2. Age was known in 99.4% of patients. The metastasis; liver, lung, bone and brain; the ICD-10 (17) code of
mortality incidence ratio showed consistent values ​​except for liver the death certificate was compared with the topographic code of
(1.43) and lung (1.02). In these locations, the number of deaths the ICD-0-311 assigned by the cancer registry. Table 3 shows the
was greater than the number of cases recorded in the registry. concordance of the two systems to assign the code for each of the
described locations. 45% of the deaths coded as liver cancer in the

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Discharges No Extraction 1. Individual


Registered List Search
Summaries

Yes
Notification No Cancer
Systems TRACED

Update
Linkage
RPCC
There is not Trace to registered cases Cancer Register as
other source (via physician certificate) TRACED appropriate
Yes source
Wait

Different Not
Casa registered
source to TRACED
Death from this source
Registered (DC)
Certificates No Registered as

DCN Cases DCI Cases DCO Cases

Figure 6. Assessing the exhaustiveness. The annual matching between the mortality database and the cancer registry makes it possible to identify new cases notified by
means of the death certificate (DCN). The active and continuous search of the cases updates the most valid basis for the diagnosis and excludes some cases of mortality
that are not cancer (Tracking not cancer). The remaining are the cases initiated by a death certificate (DCI) that would not have been detected by another way. After all the
tracking maneuvers, there remains a residue of cases for which the only evidence of cancer was the death certificate (DCO).

death certificate corresponded to metastasis. In the RPCC there oncological services were visited, located in medical centers
was evidence (morphological and clinical verification) of having (64), private clinics (36) and private offices (5). Information was
made the diagnosis of cancer in the patient’s life in a different obtained that identified 2,215 new cases of cancer (27.8%) and
primary site. This proportion reached values ​​of 46%, 15% and 10% updated 5,750 cases (72.2%) that were already in the database of
for bone, lung and CNS locations. the RPCC.

Exhaustiveness assessment by death certificate method Discussion


The 54% of people who died from cancer in Cali during the
2008-2012 period were already included in the RPCC database. The Cali cancer registry is the only one registry in low and middle
The new cases notified by means of the death certificate (DCN) income countries that has accurately reported the cancer situation
corresponded to 46% of the deaths of the period. The proportion continuously over the last half century. The information is of high
was higher in cancers with high lethality as stomach (45%); and quality and has been included in all eleven volumes of Cancer
lower, in patients with breast cancer (12%), cervix (18%), prostate Incidence in Five Continents (CI5)21,28-37.
(14%) and childhood cancer (23%),  Table 4. The exhaustivity
For forty years, RPC-Cali and was the only valid source of
index was greater than 90%, except in cases of prostate cancer.
information on the incidence of cancer in Colombia  2. The
Periodic survey of oncological services National Cancer Institute of Colombia (INC-Col) with the
The last survey conducted in 2014 costed US $ 23,300, where 19 support of Universidad del Valle, promoted in the first decade of
students participated, each one received a bonus, transportation the 21st century the establishment of RPCs in strategic regions of
cost and one payment per survey. During the eight weeks, 107 the country to increase coverage. Due to this effort, the incidence

Table 2. Cali, Colombia. Indicators of the data quality of the incidence information for both sexes during the period 2008-2012
Cancer site n Age (%) M/I 1-NS MV (%) DCO (%) ICD-10
Stomach 1,810 99.7 0.78 0.83 85.1 3.0 C16
Colorectal 1,827 99.6 0.55 0.59 89.8 1.4 C18-20
Liver 467 99.8 1.43 0.95 68.3 4.5 C22
Lung 1,316 99.9 1.02 0.90 66.4 6.0 C33-34, C38-39
Skin melanoma 324 98.2 0.40 0.34 100.0 0.0 C43
Breast* 2,998 99.5 0.33 0.26 97.0 0.3 C50
Uterine cervix 1,037 99.5 0.45 0.42 94.4 1.2 C53
Ovary 513 100.0 0.59 0.66 87.1 0.6 C56
Prostate 2,937 99.2 0.32 0.17 89.2 2.0 C61
Thyroid 1,066 98.0 0.07 0.11 97.9 0.3 C73
Hodgkin's disease 154 100.0 0.20 0.36 100.0 0.0 C81
Non-Hodgkin lymphoma 1,013 99.9 0.35 0.57 99.6 0.0 C82-C85, C96
Multiple myeloma 298 99.7 0.55 0.77 99.7 0.0 C90
Leukemia 867 99.5 0.67 0.72 100.0 0.0 C91-C95
All sites 23,046 99.4 0.51   88.5 1.7  
M/I: Mortality:incidence ratio
MV: Proportion of cases verified microscopically
DCO: only evidence of death certificate
NS: Net survival
* 26 cases of breast in men are included

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Table 3. Cali, Colombia. Coding concordance for some selected sites between the Cali Population Registry of Cali and the Municipal
Public Health Secretariat. 2008-2012.
Information source Cancer registry
Liver (C22)
Location Kappa 95% CI
Yes No
Yes 341 284 0.638 0.60 0.68
Liver (C22) No 3 1,819
Lung (C33-C34)
Municipal Yes 980 250 0.790 0.75 0.83
Lung (C33-C34) No
Public Health 7 1,210
Secretary Bone (C40-C41)
Yes 50 43 0.671 0.63 0.71
Bone (C40-C41) No 4 2,350
SNC (C70-C72)
SNC (C70-C72) Yes 430 69 0.899 0.50 1.29
No 8 1,940
IC 95%: Interavalo de confianza 95%
Kappa: Concordancia: <0.00: Pobre; 0.00-0.20: Leve; 0.21-0.40: Aceptable; 0.41-0.60: Moderada; 0.61-0.80: Considerable; 0.81-1.00: Casi perfecta

information of the Colombian cities of Pasto, Manizales and at the top of the Colombian research system. With specific
Bucaramanga was added to that of Cali and published since projects, it provides solution to epidemiological problems and
2012 in CI536, and the four Colombian RPCs participated in the complements information gathering activities. The total cost per
CONCORD study23, the global program for global surveillance case in the RPCC was US $82, which included US $ 25 for fixed-
of cancer survival, led by the London School of Hygiene and cost activities, US $ 43 for central variable-cost activities, and US
Tropical Medicine. $ 14 for other activities38.

Currently, the RPC-Cali participates in SURVCAN-3, an initiative The RPCC has social recognition in the city, thus facilitating
of the IARC to produce reliable and comparable survival statistics the process of data collection that is made passively and actively
for countries in transition. Due to the great strength of the Cancer from the various sources of data information. The oncological
Registry, Cali is the first city in the world to implement the care facilities in Cali, include 165 oncology services enabled8  to
initiative “C/Can 2025: Challenge of Cities Against Cancer”; an offer accurate diagnosis and adequate treatment to 9,000 patients
initiative of the International Union for Cancer Control (UICC) per year  39. Since its foundation in 1962, the RPCC limited the
that seeks to increase the coverage and quality of oncological registration area to the urban area of ​​Cali and developed a clear
care in the cities of more than one million inhabitants of low and definition of “case”, including only the new cases of cancer
middle income countries. diagnosed in the permanent residents of the city; and excluding
the cases of patients referred to the city for diagnostic and/or
Success factors of the RPCC treatment procedures.
Several factors have contributed to the stability and continuity
over time of the Cali Cancer Registry. The RPCC has standardized To estimate the rates and to construct the life tables for the survival
definitions and procedures for the collection, analysis, storage, study, reliable denominators based on population censuses and
validation and dissemination of information. Universidad projections are required. The DANE facilitated the demographic
del Valle has been the main source of financial and technical structure of the population for the period 1962-2015.
resources. The four directors that the RPCC has had in the 55
years of operation have been academics and researchers of the Regulations for the notification of cancer in Colombia.
Department of Pathology, in charge of coordinating a trained The Colombian government positioned cancer as a primary
human resource that belongs to the plant of the Universidad del public health problem and established actions for comprehensive
Valle. The RPCC is constituted as a research group and ranked care to reduce morbidity and mortality due to this disease and

Table 4. Population Registry of Cancer of Cali, Colombia. Percentage of registered cases as DCN, DCO, and mortality ratio: incidence;
in selected locations. Period 2008-2012.
DCN DCN/M DCO DCO/M Incidence Mortality DCI DCI/M
Cancer site MI Exhaustiveness
n % n % n n n %
All 5,327 0.46 371 0.03 23,046 11,664 0.51 1,403 0.12 0.87
Stomach 625 0.45 53 0.04 1,810 1,374 0.72 99 0.07 0.97
Colorectal 332 0.34 25 0.03 1,827 987 0.53 68 0.07 0.94
Breast 115 0.12 7 0.01 2,972 941 0.32 32 0.03 0.92
Cervix 81 0.18 11 0.02 1,037 462 0.45 16 0.03 0.96
Prostate 126 0.14 54 0.06 2,937 913 0.31 103 0.11 0.72
Child <15 38 0.23 1 0.01 402 167 0.42 3 0.018 0.97
MI: Mortality:Incidence ratio
DCN: New cases notified annually to the RPCC through the death certificate
DCI: DCN - cases excluded from mortality that are not cance
DCO: New cases in the RPCC whose only evidence of cancer is the death certificate.
exhaustiveness: (1-DCI*(1/M:I))/(1-DCI
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improve the quality of life of cancer patients. Surveillance and the morphology of the tumor. A high proportion of new cases of
control mechanisms were implemented, and the National Cancer cancer based on a clinical diagnosis has the same interpretation.
Information System was organized. The model of care for these
diseases was defined in the Ten-Year Plan for Cancer Control Exhaustiveness
in Colombia 2012-202140, and the axis of this strategic plan is The incidence rates have been stable over time and the expected
surveillance, situational analysis and research. The Ministry values ​​are comparable with those reported by cancer registries
of Health and Protection of Colombia (Ministerio de Salud y that serve similar populations such as Quito (192.8 person-years
Protección Social) regulated the basic data that health insurers and 198.9 person-years in men and women, respectively) and
and health entities must report on the oncological services Costa Rica (173.9 person-years and 167.0 person-years in men
provided, whether they are promotion, prevention, diagnosis, and women, respectively)37.
treatment or rehabilitation (RIPS). For the management of
information on public health, the Public Health Surveillance The collaborative work with the SSPM of Cali facilitates access
System (SIVIGILA) was regulated for the surveillance of breast to information on general mortality and cancer; and allows us to
cancer, cervical cancer and childhood cancer. The objective is to have an independent source of verification of new cases of cancer.
determine the opportunity at the beginning of the treatment of Cancer deaths were well certified at about 94.2%. The M:I ratio
confirmed cases and to estimate the frequency of cases detected for all cancer sites during the period 2008-2012 was 51%; similar
at different stages. Since 2014, health insurers (EPS) must to that of other RPC-Latin American (range, 38.3% to 68%)36 and
report cancer information to the High Cost Account (CAC), a higher than that reported by the United States (34.8% in men, and
non-governmental organization that was created to guide the 36% in women)36 through the SEER (Surveillance, Epidemiology,
management of health risk and ensure the management of the and End Results Program). In many Latin American countries,
disease of the people affected. the M:I ratio is greater than one in tumors with high fatality such
as pancreas, liver, esophagus. Fatality of these cancers are due to
Strengths of the RPCC: Quality indices during the period 2008- lack of complete information and/or lack of diagnosis when the
2012 patient was alive.
The value of a cancer registry depends greatly on the quality of the
data and on the quality control procedures in force 4. The RPC- The exhaustivity index was 87% (method of death certificates IE-
Cali takes four dimensions into account to determine the quality CD) and in the cancers prioritized by the PNDC it was greater
indicators of the data collected: comparability, validity, timeliness than 90%, except in cases of prostate cancer (72%). This RPC-Cali
and exhaustiveness. index is higher than that reported by other international cancer
registers (82.8% in Japan, Miyagi, 80.4% in Germany, Münster
Comparability and 65.6% in the United Kingdom)41.
The RPCC uses standard methods to make the information
comparable to other regions of the country and the world. The The method depends on the availability of relatively good quality
neoplasms are coded with the ICD-O-3 for adults11 and the ICCC- certificates, which mention the cause of death (completely and
3 for children 12. For date of incidence, the guidelines of the ENCR accurately) in the area covered by the cancer registry. This method
(13) are followed and the IARC guidelines for the classification of has not been applied in other RPC-Latin American countries.
multiple primary tumors were used14.
Opportunity
Validity The statistics of the cancer situation in Cali are public access after
The main and most reliable sources of data for the cancer registry 36 months following the year of diagnosis. Data is also available
are the histopathology reports; but they are not enough to on the RPPC portal http://rpcc.univalle.edu.co. This information
guarantee clarity, such as poorly accessible tumors: those of the describes 50 years of incidence (1962-2012), 30 years of mortality
CNS, pancreas, lung, retroperitoneum and others; the basis of the (1984-2014) and 15 years of survival (1995-2009).
diagnosis can be imaging studies, clinical examination and DCO.
Limitations
The percentage of RPC-Cali cases with a morphologically verified The data of each service in each institution are handled
diagnosis (MV%) was 88.5%, similar to other RPC-Colombians autonomously and independently. because the information is
and RPC-Latin American; and inferior to the majority of PRC- managed on different platforms, generating duplication of data,
Europeans and North American RPCCs (90% -95%)37. Africa data transfer difficulties and a decrease in the quality and integrity
has the two contrasts (53.9% Uganda: Kyandono Country, 97.8% of the information.
Algeria: Sétif)37. In low and middle income countries, a large
The Colombian oncology services periodically notify to different
proportion of cases diagnosed through the pathology service may
dependencies of the ministry of health (SIVIGILA, RIPS, CAC).
suggest deficiencies in the search for cases and, therefore, evidence
These legacy systems are mostly local applications that lack
of incomplete registration.
interoperability for proper data management. Institutions begin
In the RPC-Cali, the percentage of cases known only by death to perceive notification as a burden and relegate them and
certificate (DCO%) was 1.7%; the lowest of all the RPC-Latin deprioritize data transfer to the cancer registry. This complexity
American; and like most RPC-North American and RPC- is a risk factor to guarantee completeness in the collection
European37. Some RPCs in Africa and Latin American have DCO% of information. Consequently, there are great possibilities of
greater than 10%; which indicate poor case detection and poor underestimating the cancer risk in the population. It is urgent
quality, because death certificates do not provide information on to modify the current Ministry of Health regulations so that the

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RPC-Colombians are incorporated into the cancer information 6. Krystosik AR, Curtis A, Buritica P, Ajayakumar J, Squires R,
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Colomb Med. (Cali) 49(1): 109-120

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Technical report

Quality of death certification in Colombia


Calidad del certificado de defunción en Colombia

Ricardo Cendales*, Constanza Pardo*

Grupo de Vigilancia Epidemiológica del Cáncer, Instituto Nacional de Cancerología, Bogotá, D.C., Colombia.

Cendales R, Pardo C. Colombia death certificate quality. Colomb Med (Cali). 2018; 49(1):121-127. doi: 10.25100/cm.v49i1.3155

© 2018 Universidad del Valle. This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use,
distribution and reproduction in any medium, provided that the original author and the source are credited. e Creative Commons Attribution License, which permits
unrestricted use, distribution and reproduction in any medium, provided that the original author and the source are credited.

Article history: Abstract Resumen


Objective: To evaluate overall quality of death certification and quality of Objetivo: Evaluar la calidad de la certificación de la muerte general y
Received: 7 June 2017
Revised: 19 February 2018 cancer mortality certification in Colombia. por cáncer en Colombia.
Accepted: 1 March 2018 Methods: Classic validity indexes were described through simple Métodos: Se describieron indicadores de validez para cada departamento
percentages for each department and five cities: Bogotá, Cali, Manizales, y las ciudades de Bogotá, Cali, Manizales, Pasto y Bucaramanga. Se
Keywords: Pasto and Bucaramanga. A factorial analysis of principal components realizó un análisis factorial de componentes principales con el fin de
Data collection, vital statistics, was performed in order to identify non-evident relationships. identificar relaciones no evidentes.
cause of death, developing
Results: 984,159 deaths were analyzed, 164,542 corresponding to cancer Resultados: Se analizaron 984,159 defunciones, dentro de las cuales
countries, data quality, health
information systems. deaths. 93.7% of the overall mortality was properly certified. Most errors había 164,542 muertes por cáncer. El 93.7% de la mortalidad general
were due to signs, symptoms and ill-defined conditions. 92.8% of the estaba bien certificada. Los errores predominantes fueron signos,
Palabras clave: cancer deaths were properly certified. Ill-defined cancers site certification síntomas y afecciones mal definidas. El 92.8% de la mortalidad por
Recolección de datos, prevailed as the most frequent cause of error. cáncer estaba bien certificada. Los errores predominantes fueron
estadísticas vitales, causas de
Conclusions: Colombia showed improvement in all indicators of quality cánceres de sitio mal definido.
muerte, países en desarrollo,
calidad del dato, sistemas de certification. Given the high performance of quality indicators for overall Conclusiones: Los indicadores de calidad de certificación en Colombia
información en salud. death and cancer death certification, it is considered that mortality data mejoraron. Ante el buen comportamiento de los indicadores de calidad
can be used in the cancer incidence estimation process. de la certificación de la muerte general y por cáncer, se considera que
esta es un insumo válido para la estimación de incidencia de cáncer.

Corresponding author:
Constanza Pardo, Grupo de Vigilancia Epidemiológica del Cáncer, Instituto
Nacional de Cancerología, Calle 1 No. 9-85, Teléfono y fax 4320160 ext. 4806,
Bogotá D.C., Colombia. Correo electrónico: cpardo@cancer.gov.co
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Introduction Indicators for the general evaluation of information quality

The measurement and monitoring of the quality of mortality The International Classification of Diseases (ICD-10) was used to
information is a very important component in the evaluation group and codify the causes of death.
of health information systems in each country1. Mortality is The following indicators were constructed: deaths from cancer
a fundamental input for the analysis of situations in health, certified as primary non-established, from poorly specified
monitoring results of public health programs, and planning sites, or as a consequence of metastatic tumors (C76-C80, C97);
needs in health services2; while also being an essential input for cardiovascular deaths of ill-defined etiology (I47.2, I49.0, I46,
estimating incidents of cancer3,4. I50, I51.4, I51.5, I51.6, I51.9, I70.9); injuries of indeterminate
intentionality (Y10-Y34, Y87.2); deaths that were recorded as signs,
In Colombia, around 12% of the population is covered by a group symptoms and ill-defined conditions (R00-R99); deaths without
of cancer population registries (RPC, for its acronym in Spanish): sex information; deaths that were not certified by physicians; and
Cali, Pasto, Bucaramanga, Manizales and Barranquilla5. The deaths that don’t have any cause of error in the certification.
RPC information and the available national mortality data allow
for national incidence estimates for cancer. On a first analysis, Indicators in the evaluation of quality of information on cancer
the National Cancer Institute (INC, for its acronym in Spanish) mortality
evaluated the quality of the certification of general mortality The following indicators were constructed: deaths from uterine
and cancer mortality as part of the validation process of the cancer of unspecified site (C55); deaths from cancer of non-stated
information sources6. This report reviews the progress of the primary, from poorly specified sites, or as a consequence of a
quality of the certification of general mortality and cancer based metastatic tumor without an established primary (C76-C80, C97);
on the official information of the national vital statistics registry deaths from cancer without age information; cancer deaths that
system of the National Administrative Department of Statistics were not certified by a physician; and well-certified cancer deaths.
(DANE, for its acronym in Spanish). This information is necessary
for the estimation of cancer incidences 2007-20117 and other types Analysis plan
of analysis with mortality8-10. In order to detect a possible underlying relationship structure, a
factorial analysis of the principal components was carried out, both
This publication presents the evaluation of the quality of the for the analysis of the certification quality of general mortality and
certification of death in Colombia during the period 2007-2011, for the analysis of the certification of cancer mortality; the Kaiser-
according to the province of occurrence; it also presents the results Meyer-Olkin statistic and the Bartlett sphericity test were used to
for the capital district (Bogotá) and the four cities in which the identify if there was an underlying relationship structure 12. Those
cancer population registries operate. factors that did not fit with the proposed solution of major factors
were excluded from the analysis; the number of factors was selected
Materials and Methods with the help of graphic analysis; in those cases in which it was
considered appropriate, an orthogonal rotation was made using the
A descriptive study of the quality of mortality information was
analysis of principal components as the extraction method, and the
made from death certificates in Colombia. The results are presented
varimax with Kaiser normalization as a rotation method based on
disaggregated according to the province or city where the death
graphic analysis.
occurred. For the provinces that have municipalities with RPC, the
data of these municipalities is excluded to avoid redundancy. Thirty Results
two provinces were included, the capital district (Bogotá) and the
cities of Manizales, Pasto, Cali and Bucaramanga (which comprise In the evaluation of the quality of the certification of general
the towns of Bucaramanga, Floridablanca, Girón and Piedecuesta) death for Colombia, there were 984,159 deaths considered for the
that have active cancer population registries, which are endorsed five-year period 2007-2011. For general mortality in the area of​​
by the International Agency for Research in Cancer (IARC, for its influence of the population registries of cancer in Bucaramanga,
acronym in English)  11, with a coverage of 12% of the population Cali, Manizales and Pasto, 138,716 deaths were analyzed (14.1% of
that represents the country. The source of information is the official the national mortality).
DANE mortality database for the five-year period 2007-2011.
Quality indicators of certification of death due to general causes
Statistical methods The national percentage of duly certified deaths was 93.7%. The
The description of the quality of the certification was made through indicators that most affected the quality of the certification were:
simple percentages. Each aspect related to the lack of quality in the signs, symptoms, ill-defined conditions (2.0%) and ill-defined
information was considered only once; for example, if the death cardiovascular deaths (1.9%). Ten provinces had a percentage of
was not certified by a physician, but it also had another certification deaths without errors in the certification lower than 90.1%, and they
problem, this record was not counted twice but only once as a represented only 6.6% of the deaths in the country. Vaupés was the
record that had faults in its certification quality. The results are province with the lowest indicators in certification, with 77.2%. The
presented in a logical order in such a way that those that appear quality of the general certification for deaths without errors ranged
in the first column of the tables correspond to the first reason of from 92.3% to 96.4% for the cities of Cali, Manizales, Bucaramanga
lack of quality; those that appear in the second column correspond and Pasto. The city of Bucaramanga showed a lower proportion in its
to records that have other faults different from the first; and so on indicators with respect to the other cities (Table 1).
(Tables 1 and ​2).

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1.0 1.0 Non medical

Ill-defined Cardiovascular Diseases


Sex Unk
0.5 Ill-defined Cancer 0.5

Component 2
Component 2

Ill-defined Uterus

0.0 0.0
Symptom Injuries
Ill-defined site
Age Unk
-0.5 -0.5

Non medical

-1.0 -1.0

-1.0 -0.5 0.0 0.5 1.0 -1.0 -0.5 0.0 0.5 1.0

Component 1 Component 1
Figure 1. Results of the analysis of principal components in the general Figure 2. Results of the analysis of principal components in the evaluation of
evaluation of the quality of the certification (rotated graph), Colombia, 2007- the quality of the certification by cancer (rotated graph), Colombia, 2007-2011.
2011. Extraction method: Principal component analysis and Rotation method: Extraction method: Principal component analysis and Rotation method: Varimax
Varimax standardization with Kayser. standardization with Kayser.

The analysis of principal components showed two that can explain for general mortality: proportions of deaths certified by a non-
the lack of quality: the first one is related to the lack of certification physician, without age, of unknown or nonspecific causes 14-16, and
by a physician and the consequent inadequate certification of the indicators of cancer mortality quality: percentages of deaths
death, either as a sign, symptom or ill-defined condition or as an due to poorly defined cancer site and deaths due to uterine cancer
undetermined intentionality injury (Amazonas, Cauca, Guainía, from non-specific sites17,18.
Vaupés); the second component has to do with the provinces in
which, despite having certification by a physician, there are errors in This report confirms that Colombia is classified by the World
the certification of cancer deaths and deaths due to cardiovascular Health Organization (WHO) -IARC as a class 2 country, with an
causes (Santander, Norte de Santander, Boyacá, Sucre) (Table average quality of mortality certification. According to this index,
1 and Fig. 1). the countries classified as medium quality have a percentage of
completeness that is between 70 and 90%; or have a percentage
Quality indicators of cancer death certification of completeness greater than 90% but with a percentage of deaths
Were analyzed 164,542 deaths. The percentage of cancer deaths certified as signs, symptoms and ill-defined conditions that are
duly certified was 92.8%. The indicators that most affected the between 10 and 20%; or have an  exhaustivity  (thoroughness)
quality of the certification were deaths due to poorly defined cancer greater than 90%, with less than 10% of deaths certified as signs,
sites (6.1%) and deaths from ill-defined site uterine cancer (0.9%). symptoms and ill-defined conditions, but do not use codes of an
international classification of diseases13,19. It is possible that the
The analysis disaggregated by provinces showed 10 provinces with classification of Colombia rises to that of a country with high
a percentage of deaths duly certified that were lower than 91.6%,
quality in the certification of mortality since we have a percentage
which represented 9% of the total deaths due to cancer; Amazonas
of deaths certified as signs, symptoms and ill-defined conditions
was the province that had the lowest indicators in the quality of
that is less than 10%, and the last WHO’s coverage report of death
cancer mortality certification (Table 2). In the analysis by cities,
reports that Colombia went from having coverage of 79.9% in the
Bucaramanga, Cali, Manizales and Pasto, showed a range of 92.8%
period 1990-1994 to 88.1% in 1995-1999, 93.1% in the period
to 94.5% for the certification of deaths. The lowest quality was
2000-2004, and 98.5% in 200920.
observed in the indicators of deaths due to unspecified uterine
cancer and cancer from poorly defined sites, mainly in Manizales An improvement in all the certification quality indicators in
and Bucaramanga. The analysis of principal components only Colombia was demonstrated, both globally and in the analysis
identified a principal component shared by all the provinces, so a disaggregated by provinces and some cities. The quality of the
reduction in the dimensions could not be made (Figure 2).
certification for general death was good with a percentage of deaths
Discussion duly certified (93.7%), which improved the figure observed for the
period 2002-2006 (92.8%). The results of the evaluation of the
Colombia is among the countries with medium-high status certification quality of cancer deaths (92.8%) also exceeded 91.5%
according to the quality of certification of the cause of death  13. that had been reported for this same period. Vaupés remained
Although there is a broad framework for evaluating the quality of the province with the lowest indicators of the overall quality of
certification of general mortality, the components contemplated certification, although its figures improved from 66.9% to 76.2%.
in this document do not differ from those considered for the The signs, symptoms and ill-defined conditions went from 1.5%
period 2002-2006; and we included the classic indicators of quality to 2.0%.

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Table 1. General evaluation of the quality of the certification according to the place of occurrence of the death, Colombia, 2007-2011.
Signs,
Deaths from Deaths that Deaths
Ill-defined Injuries of symptoms Deaths Deaths
Geographic cancer of were not without Total
cardiovascular undetermined and ill- without sex without age
ordering non-stated certified by errors in deaths
deaths intentionality defined information information
primary a physician certification
conditions
Amazonas* 0.4 1.1 2.8 7.2 0.0 0.0 7.3 81.2 848
Antioquia* 1.2 1.4 0.9 1.5 0.0 0.0 0.0 94.9 148,653
Arauca* 0.5 1.7 1.1 1.7 0.0 0.0 0.3 94.7 4,494
Atlántico* 0.9 2.0 0.5 1.9 0.0 0.0 0.0 94.6 46,182
Bogotá D.C.** 1.2 1.4 1.6 2.7 0.0 0.0 0.0 93.1 159,432
Bolivar* 1.2 2.4 0.8 2.9 0.0 0.0 0.4 92.3 29,089
Boyacá* 0.8 3.1 1.5 1.4 0.0 0.0 0.3 92.8 29,704
Caldas* 1.0 2.2 0.8 1.2 0.1 0.0 0.1 94.7 12,166
Manizales§ 1.2 1.1 0.4 0.9 0.0 0.0 0.0 96.4 15,651
Caquetá* 1.0 2.2 3.2 3.6 0.0 0.0 0.2 89.7 8,121
Casanare* 1.2 2.9 3.5 2.8 0.0 0.0 0.3 89.4 4,799
Cauca* 0.8 1.8 1.5 3.6 0.0 0.0 3.9 88.4 22,658
Cesar* 0.9 2.3 1.0 2.7 0.0 0.0 0.2 92.9 17,480
Chocó* 0.6 1.8 3.0 4.9 0.0 0.0 2.1 87.6 5,381
Córdoba* 0.6 2.4 0.7 2.1 0.0 0.0 0.8 93.3 26,801
Cundina-
0.8 2.6 1.4 3.0 0.0 0.0 0.0 92.1 43,956
marca*
Guainía* 0.0 2.3 1.4 1.4 0.0 0.0 7.6 87.3 353
Guajira* 0.5 1.8 1.0 2.2 0.1 0.0 0.8 93.6 7,227
Guaviare* 0.5 1.3 3.4 3.3 0.4 0.0 0.1 91.0 1,334
Huila* 1.1 1.8 1.5 2.1 0.0 0.0 0.2 93.3 25,036
Magdalena* 0.8 2.3 0.7 2.1 0.0 0.0 0.4 93.6 21,732
Meta* 0.9 1.3 1.2 1.3 0.0 0.0 0.0 95.1 20,611
Nariño* 0.6 2.4 1.9 3.8 0.0 0.0 0.9 90.4 16,746
Pasto¤ 0.9 1.6 0.9 0.8 0.0 0.0 0.0 95.8 14,671
N. Santander* 1.0 4.7 0.9 2.5 0.0 0.0 0.2 90.8 31,768
Putumayo* 0.4 1.2 4.7 2.1 0.1 0.0 1.7 89.8 3,572
Quindío* 1.2 1.4 0.2 0.4 0.0 0.0 0.0 96.7 16,577
Risaralda* 1.2 1.4 0.6 1.3 0.0 0.0 0.0 95.5 27,529
San Andrés* 0.3 2.5 0.2 0.9 0.0 0.0 0.1 95.9 952
Santander* 0.8 3.5 1.4 2.9 0.1 0.0 1.1 90.2 17,838
Bucara-
1.2 2.4 0.4 3.2 0.0 0.0 0.4 92.3 30,725
manga†
Sucre* 0.9 3.1 0.6 1.7 0.0 0.0 0.5 93.2 13,360
Tolima* 0.7 1.3 0.7 0.9 0.0 0.0 0.2 96.2 35,803
Valle* 0.9 1.6 1.0 2.0 0.0 0.0 0.2 94.3 44,184
Cali¤ 1.1 1.2 0.7 0.7 0.0 0.0 0.0 96.4 77,669
Vaupés* 0.0 0.8 3.8 3.2 0.0 0.0 15.0 77.2 474
Vichada* 0.2 2.4 2.9 3.1 0.7 0.0 1.0 89.7 583
Colombia 1.0 1.9 1.1 2.0 0.0 0.0 0.3 93.7 984,159
‡ The geographical order of the country is defined in regions (two or more provinces),
* provinces (several municipalities), followed by special districts
**, § municipalities and metropolitan areas
† (two or more municipalities).
† Metropolitan area of Bucaramanga (Bucaramanga, Floridablanca, Girón, Piedecuesta)

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Tabla 2. Evaluation of the quality of the certification by cancer according to the place of occurrence of the death, Colombia, 2007-2011.
Deaths from Deaths from Deaths from Deaths from cancer
Geographic Duly certified Total deaths
unspecified ill-defined cancer without that were not certified
ordering ‡ deaths from cancer from cancer
uterine cancer cancer site age information by a physician
Amazonas* 1.3 3.9 0.0 7.8 87.0 77
Antioquia* 0.7 6.4 0.0 0.0 92.9 27,411
Arauca* 1.6 4.3 0.0 0.2 93.9 507
Atlántico* 1.1 5.6 0.0 0.0 93.3 7,782
Bogotá D.C.** 0.6 5.8 0.0 0.0 93.6 33,332
Bolívar* 1.0 7.2 0.0 0.2 91.6 4,682
Boyacá* 1.0 6.2 0.0 0.1 92.7 4,024
Caldas* 0.9 6.7 0.0 0.0 92.4 1,876
Manizales¤ 0.4 6.4 0.0 0.0 93.2 3,000
Caquetá* 1.8 8.4 0.0 0.3 89.5 998
Casanare* 2.0 9.2 0.0 0.0 88.8 609
Cauca* 0.9 5.7 0.0 4.0 89.4 3,387
Cesar* 1.1 6.9 0.0 0.0 92.0 2,383
Chocó* 2.0 7.5 0.0 2.0 88.4 441
Córdoba* 1.6 4.7 0.0 1.1 92.6 3,321
Cundinamarca* 1.3 6.3 0.0 0.0 92.4 5,713
Guainía* 0.0 0.0 0.0 0.0 100.0 15
Guajira* 2.6 4.8 0.0 1.6 91.0 765
Guaviare* 3.1 7.2 0.0 0.0 89.7 97
Huila* 0.5 6.8 0.0 0.2 92.5 4,010
Magdalena* 2.3 5.6 0.0 0.5 91.6 3,043
Meta* 0.9 6.4 0.0 0.0 92.7 2,957
Nariño* 1.0 4.8 0.0 0.7 93.5 2,105
Pasto¤ 0.4 5.0 0.0 0.0 94.5 2,617
N. Santander* 1.3 6.5 0.0 0.1 92.1 4,881
Putumayo* 1.7 4.2 0.0 1.1 92.9 353
Quindío* 1.0 6.2 0.0 0.0 92.7 3,209
Risaralda* 0.7 6.9 0.0 0.0 92.4 4,946
San Andrés* 1.6 2.4 0.0 0.0 96.1 127
Santander* 1.3 7.1 0.0 1.1 90.5 1,947
Bucaramanga† 0.5 6.3 0.0 0.4 92.8 5,957
Sucre* 1.3 6.6 0.0 0.8 91.4 1,857
Tolima* 1.2 4.8 0.0 0.1 93.9 5,320
Valle* 1.5 6.3 0.0 0.1 92.2 6,546
Cali¤ 0.5 5.9 0.0 0.0 93.7 14,205
Vaupés* 0.0 0.0 0.0 0.0 100.0 16
Vichada* 0.0 3.8 0.0 3.8 92.3 26
Colombia 0.9 6.1 0.0 0.2 92.8 164,542
‡ The geographic ordering of the country is defined in regions (two or more provinces), provinces
* (set of several municipalities), followed by special districts
**, municipalities¤ and metropolitan areas
† (two or more municipalities).
† Metropolitan Area of Bucaramanga (Bucaramanga, Floridablanca, Girón, Piedecuesta)

Given the good performance of the quality indicators in these two and 9,986 deaths by cancer of ill-defined site (6.1%); of a total of
aspects, it was found that mortality in Colombia as an input for 152,753 deaths from well-certified cancer.
the estimation of incident cases of cancer is valid, and it does not
require adjustments for under-registration or correction for age, In the cities which have a working population registry of cancer,
sex or undefined causes of death; then, in total for the period, it was the indicators were substantially better than in the rest of their
only necessary to redistribute 101 deaths without sex information, provinces, and they were similar or exceeded the national average
1,180 deaths without age information, 2,800 deaths not certified by (Manizales 96.4%, Pasto 95.8% and Cali 96.4%), with the exception
physician and 19,937 deaths due to ill-defined causes among a total of Bucaramanga (92.3%). In the specific case of quality in the
of 921,967 deaths without errors in certification. certification of cancer mortality, the indicators of the cities were
also better than in the rest of their provinces (Manizales 93.2%,
For the specific case of cancer deaths, 1,452 deaths from ill- Pasto 94.5%, Bucaramanga 92.8%, Cali 93.7%), so it is considered
defined site uterine cancer (0.9% of total cancer deaths) should that the information of general death and death from cancer in
be redistributed according to standard methodologies; there these areas is valid and serves as an input for the estimation of the
would only remain 45 deaths by cancer without age (0.03%) to mortality incidence ratio necessary for the estimation of incident
redistribute; 347 deaths by cancer not certified by physician (0.2%); cases of cancer. It should be noted that there is a higher proportion
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of deaths in these cities than in the rest of the municipalities of 3. Ferlay J, Parkin MD, Steliarova-Fouche E. Estimates of the
their respective provinces. cancer incidence and mortality in Europe in 2008. Eur J Cancer.
2010;46:765-81.
A recommendation for cities with cancer population registries
would be that in the future, an analysis be performed in which 4. Dyba T, Hakulinen T. Comparison of different approaches to
the information about the diagnosis of cancer be crossed with the incidence prediction based on simple interpolation techniques. Stat
cause of death by cancer, in order to go deeper into the quality of Med. 2000;19:1741-52.
the specific cause of cancer. However, this requires permission to
cross databases with the identifier, which is not possible to perform 5. Pardo C, Bravo LE, Uribe C, Lopez G, Yepez MC, Navarro E, et al.
at the present time. This particular issue is a call to the health Comprehensive assessment of population-based cancer registries: an
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6. Cendales R, Pardo C. La calidad de certificación de la mortalidad en
This analysis was made in accordance with the site of occurrence Colombia, 2002-2006. Rev Salud Publica (Bogotá). 2011;13(2):229-38.
of death; however, the analysis of mortality and the calculation
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of residence of the deceased, so the quality of the certification five first types of cancer in Colombia. Colomb Med (Cali). 2018;
described here may be slightly different from that observed in the 49(1):116-22
analysis made in accordance with the place of habitual residence.
8. de Vries E, Arroyave I, Pardo C, Wiesner C, Murillo R, Forman
Phillips et al. , proposed a new methodology to establish the
21 D, et al. Trends in inequalities in premature cancer mortality by
overall performance of the vital statistics system (SEV, for its educational level in Colombia, 1998-2007. J Epidemiol Community
acronym in Spanish) in each country, with the inclusion of six Health. 2015;69(5):408–15.
complementary dimensions with their respective indicators, a
9. de Vries E, Arroyave I, Pardo C. Time trends in educational
methodology that seeks to obtain reliable mortality information
inequalities in cancer mortality in Colombia, 1998-2012. BMJ
and monitor changes in time. In a second publication,  Phillips
Open. 2016;6(4):e008985.
et al  defines the SEV performance index by ranges and for five
categories (very low, <0.25, low, 0.25-0.49, medium, 0.50-0.69, high, 10. de Vries E, Arroyave I, Pardo C. Re-emergence of educational
0.70-0.84, very high, ≥0.85). In this study, Colombia evaluated with inequalities in cervical cancer mortality, Colombia 1998–2015. J
the vital statistics information of 2008, presented an index of 82.5, Cancer Policy. 2017; 15:37-44. Doi: 10.1016/j.jcpo.2017.12.007.
with a high quality range22. In future work, the application of these
alternative estimation methods will be explored, according to the 11. Bray F, Colombet M, Mery L, Piñeros M, Znaor A, Zanetti R, Ferlay
available information on mortality in Colombia. J (Eds). Cancer Incidence in Five Continents. Vol XI, CancerBase
No. 14. Lyon: IARC; 2017. http://publications.iarc.fr/Databases/Iarc-
Conclusion Cancerbases/Cancer-Incidence-In-Five-Continents-Vol-Xi-2017.
Certification quality indicators in Colombia improved for the 12. Hutcheson GD, Sofroniou N. The multivariate social scientist.
studied period. Given the good performance of the quality London: Sage; 1999.
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is considered that this is a valid input for the estimation of cancer 13. Mahapatra P, Shibuya K, Lopez AD, Coullare F, Notzon FC,
incidence. Rao C, Szreter S. On behalf of the Monitoring Vital Events (MoVE)
writing group. Civil registration systems and vital statistics: successes
Acknowledgements: and missed opportunities. Lancet. 2007;370:1653–63.
The authors are grateful for the financial support of this work,
which was carried out with resources from the National Cancer 14. Núñez FML, Icaza NMG. Calidad de las estadísticas de mortalidad
Institute, Cancer Epidemiological Surveillance Program. en Chile, 1997-2003. Rev Med Chil. 2006;134(9):1191-6.
Conflict of interest 15. Paes NA. Qualidade das estatísticas de óbitos por causas
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2007;41(3):436-45.
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Technical report

Cancer risk management in Colombia, 2016


Gestión del riesgo de cáncer en Colombia, 2016

Paula Ramirez-Barbosa, Lizbeth Acuña Merchan

Cuenta de Alto Costo- Fondo Colombiano de Enfermedades de Alto Costo. Ministerio de Salud y Proteccion Social, Bogota, Colombia

Ramirez-Barbosa P, Acuña LA. Cancer risk management in Colombia, 2016. Colomb Med (Cali). 2018; 49(1): 128-136 DOI: 10.25100/cm.v49i1.3882

© 2018. Universidad del Valle. This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use,
distribution, and reproduction in any medium, provided the original author and source are credited.

Article history: Abstract Resumen


Recibido: 13 January 2018 Objective: To describe the outcomes of risk management indicators Objetivo: Describir los resultados de los indicadores de gestión del
Revisado: 25 February 2018 for five types of cancer in population that is affiliated to the General riesgo para cinco cánceres en la población afiliada al Sistema General
Aceptado: 20 March 2018 System of Social Security in Health, in six cities of Colombia. de Seguridad Social en Salud en Colombia en ciudades que tienen re-
Methods: Based on the data from the administrative cancer registry gistros de cáncer.
Keywords:
for the period 2016, the High Cost Disease Fund (CAC in Spanish) as Metodos: La Cuenta de Alto Costo (CAC) procesó y analizó la in-
Cancer, health records, a technical organization of the Colombian health system, processed formación del registro administrativo nacional de cáncer del periodo
quality indicators, health care
and analyzed the data for the calculation of risk management 2016 en Cali, Pasto, Bucaramanga, Manizales, Barranquilla y Mede-
indicators established in consensus based on the evidence found in llín; para calcular los indicadores de gestión del riesgo establecidos en
Palabras clave:
six cities el consenso basado en la evidencia para la atención en cáncer.
Cáncer, registros de salud,
Results: There is a diversity in the indicators results found among Resultados: Existe diversidad en los resultados de los indicadores
indicadores de calidad
the different cities, evidencing strengths and weaknesses in each of entre las diferentes ciudades, evidenciando fortalezas y debilidades
them for the different types of cancer. From the set of indicators, en cada una de ellas y para los diferentes tipos de cáncer. Los indica-
those with the best results presented are related to the greater dores que mejores resultados presentaron se relacionan con la mayor
detection of cancer in early stages or in situ, as well as a decrease detección del cáncer en estadios tempranos, así como disminución
in mortality, especially in colorectal and in gastric cancer. Most de la mortalidad, especialmente en cáncer de colorrectal y en cáncer
indicators in gastric cancer showed optimal results. Important gástrico. El cáncer gástrico fue aquel que mayor cantidad de indicado-
measurements such as the opportunity for diagnosis and treatment res obtuvieron resultados óptimos. Mediciones importantes como la
are below the proposed standard for most types in all the six cities. oportunidad de diagnóstico y de tratamiento se encuentran por de-
Conclusions: The descriptive analysis of cancer risk management bajo del estándar propuesto para la mayoría de los tipos de cáncer y
indicators shows certain weaknesses in the quality and timeliness de las ciudades.
of the care of cancer patients, the standards agreed upon in the Conclusiones:
consensus with the different actors of the system are not being Se evidencia ciertas debilidades en la calidad y la oportunidad de la
reached, situation which may be due to a reality of problems of the atención oncológica, no se están cumpliendo los estándares acordados
Colombian health system, as well as deficiencies in the quality of the en los consensos con los diferentes actores del sistema: puede deber-
report to the CAC. se a una realidad de problemas del sistema de salud colombiano, así
como a la necesidad de fortalecer la calidad del reporte por parte de
las entidades a la CAC.

Corresponding author:
Lizbeth Acuña. Cuenta de Alto Costo- Fondo Colombiano de Enfermedades de Alto
Costo. Ministerio de Salud y Proteccion Social, Bogota, Colombia. Carrera 45 N° 103-
34 Oficina 802, Tel. +57 1 6021820, E-mail: l.acuna@encuestadealtocosto.org

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Introduction Materials and Methods


Cancer is a public health problem in Colombia and the world, The High Cost Diseases Fund, is a technical body of the General
which requires decisive interventions to confront and contain System of Social Security in Health of Colombia with the mission
it. For this reason, different strategies and policies have been of Promoting risk management, the generation of health outcomes
developed in different countries and must be based not only on and knowledge management, through the articulation of different
clinical but also on epidemiological knowledge of cancer, which SGSSS actors to decrease the trend of High Cost events, stabilize
must also be tied to the administrative actions that are carried out the variability in their management, ensure technical-scientific
at the health insurance level. In order to accomplish this, the way quality and reduce the impact of the current disease burden,
to know and monitor these actions is through the measurement of through various mechanisms. The insurers and health providers
are mandated to report the data of all cancer patients to the CAC
indicators that account for the quality of health care1,2.
on an annual basis. The CAC is a source of information of the
In Colombia, information related to cancer has taken great SINCan responsible for integrating the information to form the
importance over the years and the country works to obtain National Administrative Registry of Cancer (RANC)
sufficient, real and accurate information with the objective SINCan
of analyzing and addressing it to the processes, evidencing The available sources within the SINCan are administrative and
strengths and weaknesses within the health system for the hospital records; as well as population studies and surveys. The data
formulation of strategies, programs and policies that define reported and collected from the local, territorial and national level
corrective interventions. To achieve this purpose, the Ministry are integrated into a data warehouse that allows interoperability of
of Health and Social Protection of Colombia (MSPS in Spanish) the sources, which is called the Social Protection Comprehensive
through Resolution 4496 of 2012 organizes the National Cancer Information System (SISPRO) (Fig. 1). The National Cancer
Information System (SINCan)3, in which the High Cost Diseases Observatory consolidates the information of the SISPRO, RANC
Fund (CAC in spanish) is part of these information sources, and Cancer Population Registries in order to build the indicators
analyzing data related to insurance and the provision of services to monitor the situation in the country, the analysis plans, and
to cancer patients in the country. Similarly, the MSPS-Colombia the information outputs as necessary tools to adequately manage
with Resolution 0247 of 2014, establishes the report for the knowledge about mortality, morbidity, access to services and
registration of cancer patients where the High Cost Diseases Fund actions for cancer control in Colombia.
is responsible for collecting and consolidating the information
that the healthcare payer, including those of the exception regime Case definition
and the public institutions, private, and mixed health service People with histopathological diagnosis of some type of in situ or
providers, as well as the departmental, district and municipal invasive cancer; people with clinical diagnosis of cancer, supported
and justified in clinical, biochemical, imaging or laboratory tests
health authorities, are mandated to report4.
appropriate in those for whom, due to any clinical condition
Therefore, Colombia has a national administrative registry in negative to its performance or contraindication, it was not possible
cancer (RANC in Spanish) since 2014, with clinical, administrative, to perform histopathological confirmation until the cutoff date, but
who are being managed as cancer patients. For specific cancers,
sociodemographic and cost components which, since 2015,
codes of the International Classification of Diseases, Tenth Revision
have been audited to guarantee the quality of the information
(ICD-10) were used as follows: stomach (C16); colorectal (C18 to
as a complement to other sources of information. Based on
C21); breast (C50); Cervix (C53) and prostate (C61).
this information, in 2016 the High Cost Diseases Fund began
the construction and development of processes to standardize Collection instrument
measurements in the cancer care process through consensus Structured form that collects information in the following aspects:
based on evidence for the formulation of indicators that measure General identification of the health insurer and the reported user
the management conducted by insurers and providers on people (Questions (Q) 1-16); General information related to diagnosis,
with cancer in the country. staging and treatment objectives (Q 17-41); antecedents that
precede the diagnosis of the cancer reported (Q 42-73);
Likewise, another source of information is population-based specific surgery information (Q 74-85); radiotherapy specific
cancer registries (RCBP in Spanish) in six cities of the country that information (Q 86-105); specific information on hematopoietic
collect and classify new cases of cancer in permanent residents of stem cell transplantation (Q 106-110); specific information on
Cali, Pasto, Bucaramanga, Manizales, Barranquilla and Medellin. complementary treatment (Q 111-124); current situation of the
They are members of the International Association of Cancer user at the cut-off date (Q 125-132)
Registries (IACR) and have disseminated information on incidence
and survival in Cancer Incidence in Five Continents5  and in the Information quality control in the High Cost Diseases Fund (CAC)
The CAC audits the information given by the EAPB against the
CONCORD study6 . The objective of this paper is to describe the clinical records. Its objective is to verify the authenticity of the
results of risk management indicators for five types of cancer data reported and to be able to accurately conclude the available
(stomach, colorectal, breast, cervix and prostate) in the population information. This process consists of two main components: the
that is affiliated with the Colombian General System of Social first refers to the audit carried out by the information system;
Security in Health (SGSSS in Spanish) in the six cities of Colombia through a validation mesh and the second, of the information
that have RCBP. against the medical record.
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Integration to SISPRO
Platform (Data highway)

Population Population-based
Studies Cancer Registry

Mortality and Web Portal MSPS


vitals statistics SISPRO
DANE
SQL
Data Storage Access to cubes
Administrative of information
and Hospital SISPRO
National SISPRO
Records
Cancer
Observatory Digital
Public Health (ONC) Institutional
Surveillance Repository

Cancer Registry
SISPRO
High Cost
Geographic
Account
Module
(CAC)

Public
Advocate

Quality
control
1 4
2 3
Information Access and
Data Knowledge
Sources Diffusion
Management Management
Management Channels

Figura 1. National Cancer Information System of Colombia

Process of creating the CAC indicators methodological and administrative. For the structuring of the
The development of the consensus done among the different actors question, the PICO strategy was taken into account10,11  , which
of the General System of Social Security in Health in Colombia was presented for each of the types of cancer worked on and
for the identification of indicators in cancer arose from the need then an online application created for the virtual development
to evaluate and monitor risk management in cancer carried out by of the consensus was designed, where the research question, the
insurance entities and health service providers, in order to be aligned objectives, the scope, and the limitations were socialized and there
and contribute to the strategies that the country has implemented was a space for participation for the actors involved.
for cancer control, such as the 10-year plan for cancer control in
Colombia1, clinical practice guidelines, and comprehensive care routes A search and critical reading of literature was carried out and it
for different types of cancer; this way generating control mechanisms was classified according to the type of scientific evidence, using
and providing a guide to health professionals, insurance entities, the AGREE II instrument12  for the qualification of the clinical
providers and other actors in the search for a better risk management practice guidelines and the recommendations of the GRADE
in health that contributes to decrease clinical variability, reduce the system  13  for the qualification of the review articles. Once the
complications of the disease, improve survival and the quality of life evidence was available, we extracted the recommendations and
of patients, and control spending on health. definitions of interest, which were reviewed and adjusted by the
participants through the virtual forum, from there the possible
The consensus has been developed by the High Cost Diseases Fund indicators were generated (the type of these: process or result), the
since 2016, giving priority to the most prevalent types of cancer in name, the description, the population object of application (total
Colombian society, and according to the priorities of the Ministry of cases or new cases) and the different guidelines and articles that
of Health; To this end, the concepts of the methodological manual supported the recommendation.
of deliberation and participation of the Institute of Technological
Evaluation in Health (IETS in Spanish) were adopted, and the Finally, a group of indicators was defined and evaluated through
methodology proposed by the methodological guide for the two virtual and a third face-to-face votes. The consensus
preparation of clinical practice guidelines was adapted. These participants determined if the proposed indicators were
guidelines present the technical processes for the formulation of appropriate and met three essential criteria: relevance of the
the research question, the review of the literature, the grading indicator; feasibility, understood as the possibility of accessing the
of the scientific evidence and the process for the selection sources of information from where the data will be obtained and
and construction of the indicators7,8  . For the selection and the validity of the content or measurement that reflects what is
construction of the indicators, an adaptation of the methodology intended to be measured, in this case, the indicator or indicators
“The RAND/UCLA Appropriateness Method (RAM)” was carried that allow evaluating risk management in patients with cancer.
out9, which allows combining the best available scientific evidence Risk management indicators for different types of cancer are
with the collective judgment of the experts, in this case, thematic, appended as a supplement.

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Table 1. High Cost Diseases Fund, Colombia. Number of new cancer cases for selected sites notified by health insurers during 2015.
Breast Prostate Cervix Colon Stomach Total
City
C50 C61 C53 C18-C21 C16
♂ ♀ ♂ ♀
Cali 235 273 59 69 80 51 42 809
Pasto 17 14 12 5 1 13 4 66
Bucaramanga 47 19 8 13 15 11 10 123
Manizales 58 29 15 13 27 20 8 170
Barranquilla 132 90 35 28 37 7 5 334
Medellín 498 250 134 103 134 80 71 1,270
Total 987 675 263 231 294 182 140 2,772
Source: Database High Cost Diseases Fund,

Analysis plan in the registry. These were divided into four large groups of
With the information reported to the CAC with a cutoff date indicators: diagnostic and staging (indicators 1 to 7), treatment
of January 1, 2015, the baseline was calculated for each of the (indicators 8 to 12), opportunity (indicators 13 to 17) and results
indicators with available information. According to the result, (indicators 18 to 19). It can be seen that the city of Cali had
the cut points were defined according to the quintiles of each the highest proportion of patients with breast cancer who were
indicator. For the indicators without baseline, the standards were diagnosed in situ or early stages, while Barranquilla and Pasto had
defined with the support of the clinical experts and the findings of the lowest proportions. Regarding the staging indicators, none of
the literature review. the six municipalities obtained the defined standard to consider
the result as optimal, However, Medellin, for the new cases, is the
The final indicators for the measurement of risk management were one with the highest proportion of staged cases registered. The
established with the agreement of all the participants in the third indicators related to the performance of diagnostic tests showed
virtual meeting and the consensus was finalized. Based on this, the a low proportion of women with breast cancer and who had
information is analyzed every year and weaknesses and strengths hormone test results, in terms of HER2 test results the proportion
of the cancer management process are identified. increased in the six cities, with Bucaramanga achieving the value
considered as optimal.
For this occasion, the results of the risk management indicators for
five types of cancer (breast (only in women), cervix, prostate, colon In the field of treatments such as radiotherapy, anti-Her2 therapy
and rectum and gastric) in a population that is affiliated with the or administration of hormonal block, the results were located in
General Social Security System in Health will be described in six the ranges considered as bad or moderate (red and yellow scored
cities of the country (Barranquilla, Bucaramanga, Cali, Manizales, card) in most of the municipalities selected according to the
Medellin and Pasto) where population registries operate, as a standard of measurement of the Consensus, Cali and Medellin
complement to the analysis and approach of interventions for presented the highest proportion of patients with carcinoma  in
cancer control. situ who underwent breast-conserving surgery.

The data comes from the administrative registry of cancer issued In the third group of indicators, related to opportunity times, none
by the Ministry of Health and Social Protection (Resolution 0247 of the cities analyzed presented a level considered optimal according
of 2014) and corresponds to the new cases reported (diagnosed) to the established standards, the times for diagnosis, medical care
between January 2, 2015 and January 1, 2016. and start of treatment presented prolonged times, above 60 days
for general care, that is, from the consultation for the presence of
We proceeded with the calculation of each of the indicators symptoms associated with cancer up to the first treatment, however,
included in the evidence-based consensus designed by the High cities such as Medellin and Pasto are close to the appropriate range.
Cost Diseases Fund, which measures risk management by insurers In terms of outcome indicators: mortality according to stage and
and providers for patients with each type of cancer previously mortality, the city with the best results was Medellin.
mentioned and that have defined standard cutoff points with a
color for each indicator, which reflects whether the result is good Prostate cancer
(green), moderate (yellow) or bad (red). A total of nine indicators were developed for prostate
cancer15  (Table 3), however 6 were susceptible to measurement,
Statistical software Stata 13 was used to process the data. due to the absence of information in the registry.

For prostate cancer, two opportunity times were measured: from


Results the medical suspicion for the first consultation until the diagnosis
and from this until the start of the first treatment. For each one it
Table 1  describes the number of new cancer cases prioritized was established that a time less than 30 days was adequate to be
in the Ten-Year Plan for Cancer Control in Colombia that were considered a good result. None of the cities obtained this result.
notified to the CAC during 2015 in the six cities studied.
The largest proportion of patients staged with the TNM system
Breast cancer occurred in the cities of Manizales and Medellin, and those with
A total of 21 indicators were included in the consensus14 (Table 2), the highest number of patients studied in localized stages were
however, 19 were measured due to the availability of information Bucaramanga and Medellin.
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Table 2. Risk management indicators in breast cancer by city of residence


1. Proportion of women 2. Proportion of women 3. Proportion of women 4. Proportion of women 5. Proportion of patients
with breast cancer who with breast cancer detected with breast cancer detected with breast cancer detected with histopathological
underwent TNM staging as carcinomas in situ at the in early stages at the time in advanced stages at the diagnosis before surgery
time of diagnosis of diagnosis time of diagnosis

< 71.5% < 6% < 42% > 58% < 38.6%


71.5 - 78.6% 6 - 11% 42 - 49% 50 - 57% 38.6 - 57.7%
City > 78.7% > 12% > 50% < 50% > 57.8%

Barranquilla 52.9% 10.0% 41.7% 58.3% 77.8%


Bucaramanga 66.3% 0.0% 44.1% 55.9% 52.6%
Cali 52.9% 16.9% 50.7% 49.3% 65.3%
Manizales 61.8% 4.9% 43.6% 56.4% 76.9%
Medellín 72.0% 8.0% 49.7% 50.3% 85.2%
Pasto 46.2% 9.1% 20.0% 80.0% 66.7%
Total 62.2% 8.8% 47.4% 52.6% 77.4%

6. Proportion of 8. Proportion of 8.1 Proportion of 9. Proportion of 10. Proportion of


women with breast women with breast women with invasive patients with breast women with positive
cancer resulting in 7. Proportion of cancer in situ who breast cancer who cancer who underwent hormone receptors who
hormone receptors patients with HER2 underwent breast-con- underwent breast-con- radiotherapy after are given hormonal
(estrogen / progestero- study serving surgery serving surgery breast-conserving blocking as treatment
ne) surgery
< 70% < 70% < 18.9% < 18.9% < 70% < 80%
70 - 89% 70 - 89% 18.9 - 65.3% 18.9 - 65.3% 70 - 89% 80 - 89%
City
> 90% > 90% > 65.4% > 65.4% > 90% > 90%

Barranquilla 56.8% 79.8% 33.3% 51.9% 27.3% 14.8%


Bucaramanga 70.2% 97.9% *** 40.0% 40.0% 21.1%
Cali 55.7% 76.5% 77.8% 61.5% 44.7% 18.1%
Manizales 50.0% 87.5% 100.0% 40.0% 0.0% 16.0%
Medellín 68.1% 87.9% 65.0% 63.9% 51.9% 13.4%
Pasto 47.1% 81.3% 0.0% 0.0% *** 28.6%
Total 62.3% 84.5% 64.7% 59.8% 45.7% 15.2%

12.1 Proportion of patients


11. Proportion of HER2 (+) with invasive breast cancer
13. Opportunity for 14. Opportunity for 15. Opportunity for care by
patients with anti-HER2 with assessment for general care cancer care the attending physician
therapy palliative care, advanced
stages (CNR)

< 34.1% > 75 days > 45 days > 30 days


34.1 - 69% to be decided 61 - 75 days 31 - 45 days 16 - 30 days
City > 70% < 60 days < 30 days < 15 days

Barranquilla 36.8% 2.4% 85.1 60.2 22.2


Bucaramanga 50.0% 5.3% 102.6 61.8 33.2
Cali 41.4% 5.9% 99.5 65.9 27.4
Manizales 25.0% 0.0% 82.8 45.8 19.5
Medellín 32.3% 9.2% 62.7 46.2 19.4
Pasto 0.0% 0.0% 61.3 50.8 33.8
Total 34.6% 6.6% 74.6 52.2 21.8

16. Opportunity to 17. Opportunity to start 18. Lethality of breast 18. Breast cancer lethality 19. General mortality
start treatment adjuvant therapy cancer (early stages) (late stages) in breast cancer

> 30 days > 56 days > 2% > 5% > 14.9 x 100000


16 - 30 days 43 - 56 days 1.3-2% 4.4-5% 9.9 -14.9 x 100000
City < 15 days < 42 days < 1.3 % < 4.4 % < 9.8 x 100000
Barranquilla 50.4 57.6 4.3% 6.4% 11.4
Bucaramanga 43.1 79.5 4.0% 5.0% 9.2
Cali 76.3 63.3 2.9% 8.2% 13.2
Manizales 34.4 64.2 2.7% 3.7% 7.5
Medellín 42.7 57.8 0.5% 3.8% 9.2
Pasto 31.2 44.0 9.5% 0.0% 6.5
Total 48.8 60.2 1.8% 5.1% 10.5

Source: High Cost Diseases Fund Database Resol 0247/14 - Cut-off date: January 01, 2016

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Table 3. Risk management indicators in prostate cancer by city of residence


1. Diagnostic opportunity in
3. Proportion of 4. Proportion of pa-
days; time between consulta- 6. Treatment opportu-
2. Proportion of pa- patients with locali- tients with locally ad- 5. Proportion of pa-
tions where remission is made nity in days, time
tients with prostate zed prostate cancer vanced and advanced tients staged in Glea-
due to clinical or paraclinical between diagnosis
cancer staged in TNM (patients in stage 0, I prostate cancer (stage son score
suspicion, associated with pros- until the first treat-
and II) III and IV patients)
tate cancer until diagnosis.

> 60 days < 50 % < 62% > 37% < 83% > 60 days
30 - 59 days 50 - 56% 62 - 69% 31 - 37% 83 - 87% 30 - 59 days
City
< 30 days > 56% > 69% < 31% > 87% < 30 days

Barranquilla 72 35.6% 56.3% 43.8% 79.3% 60


Bucaramanga 164 52.6% 70.0% 30.0% 85.7% 59
Cali 49 12.5% 61.8% 38.2% 60.0% 88
Manizales 112 62.1% 66.7% 33.3% 48.3% 61
Medellín 46 70.0% 74.3% 25.7% 93.1% 66
Pasto 43 7.1% 0.0% 100.0% 88.9% 64
Total 56 40.0% 69.6% 30.4% 78.4% 70

Source: High Cost Diseases Fund Database Resol 0247/14 - Cut-off date: January 01, 2016

The cities of Medellin and Pasto were the cities with the highest The cities of Pasto, Medellin and Barranquilla reported times
proportion of patients in the Gleason score, while the city of under 60 days between the time of clinical suspicion and the start
Manizales had the lowest proportion. of treatment. Considering the different opportunity times in a
disaggregated way, Pasto presented the shortest times between the
Cervical cancer different moments of attention.
The total number of indicators measured for cervical cancer were
12 out of a total of 14 from the consensus14 (Table 4), which, like Stomach cancer
the breast cancer indicators, were divided into four large groups: A total of 12 indicators of the 16 considered in the consensus
diagnostic (indicator 1), treatment (indicators 2 to 6), opportunity were measured 16 (Table 5). In terms of opportunity times for the
(indicators 7 to 10) and outcome (indicators 11 to 12). diagnosis, Barranquilla and Medellin had the shortest times with
23 and 25 days, respectively. Regarding the time for the start of the
Diagnostic measured the proportion of women who had clinical first treatment after confirmation of the diagnosis Medellin was
staging in the new cases, it being higher in Manizales and Pasto. On the city with the shortest time reported with 41 days, in contrast
the other hand, Barranquilla and Cali had the lowest proportions. to Barranquilla, which was the city where the entities reported the
In treatment, Bucaramanga was the city with the highest highest times with 84 days.
proportion of women who underwent some healing procedure
in stages IA-IB1, with respect to the supply of radiotherapy in Medellin was the city with the highest proportion of patients with
stages II to IV, Pasto reported 100% of their patients receiving this TNM staging and Barranquilla was the one with the highest proportion
therapy, the cities of Barranquilla and Bucaramanga presented the of staged patients in early stages. These two cities were those that in
highest proportions in terms of the number of women living in terms of treatment had the highest proportion of patients in stages 0
these cities receiving chemotherapy. to III who were subjected to surgery as a curative treatment.

Table 4. Risk management indicators in cervical cancer by city of residence


2. Proportion of women 5. Proportion of women
with cervical cancer in 6.1 Proportion of
1. Proportion of women with stage IA-IB1 3. Proportion of women 4. Proportion of women
stages II-IV who were women with cervical
with cervical cancer who cervical cancer who with stage II-IV cervical with cervical cancer in
given chemotherapy and cancer with assessment
underwent clinical received some curative cancer who were given stages II-IV who were
concomitant radiothera- for palliative care,
staging, CNR procedure (conization / radiotherapy given chemotherapy.
py with brachytherapy advanced stages CNR
surgery).
<69% <60% <45% <49% <60%
69-78% 60-89% 45-62% 49-65% 60-89% to be decided
City
>78% >90% >62% >65% >90%

Barranquilla 58.6% 25.0% 84.6% 92.3% 0.0% 7.7%


Bucaramanga 71.4% 100.0% 66.7% 66.7% 0.0% 0.0%
Cali 54.7% 0.0% 39.1% 21.7% 0.0% 8.7%
Manizales 84.6% 0.0% 77.8% 33.3% 22.2% 0.0%
Medellín 76.9% 67.4% 83.0% 61.7% 0.0% 17.0%
Pasto 100.0% 0.0% 100.0% 9.1% 0.0% 0.0%
Total 71.1% 55.7% 74.5% 49.1% 1.9% 10.4%

11. Proportion of
women with cervical 12. General mortality
7. Opportunity for 8. Opportunity for 9. Opportunity for 10. Opportunity to
cancer with new in women with
general care cancer care treating doctor start treatment
diagnosis (within the cervical cancer
reporting period)
> 75 days > 45 days > 45 days > 30 days > 8.2 x 100000
61 - 75 days 31 - 45 days 31 - 45 days 16 - 30 days to be decided 5.5 - 8.2 x 100000
City
< 60 days < 30 days < 30 days < 15 days < 5.5 x 100000

Barranquilla 56.3 65.6 18.1 41.1 7.9 4.0


Bucaramanga 91.3 60.3 18.6 37.5 5.8 4.3
Cali
97.3 86.9 35.8 50.7 7.2 6.0
Manizales 68.9 55.9 18.8 46.3 10.0 8.1
Medellín 55.0 42.8 18.7 32.2 13.1 5.2
Pasto
36.7 28.8 21.4 14.0 9.4 8.8
Total
62.3 51.9 21.8 35.6 9.6 5.6

Source: High Cost Diseases Fund Database Resol 0247/14 - Cut-off date: 01 January 2016

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Table 5. Risk management Indicators in stomach cancer by city of residence


2. Proportion of 3. Proportion of new 4. Proportion of 6. Opportunity
1. Diagnostic 5. Treatment
patients with gastric cases identified in patients with TNM between neodyuvance
opportunity opportunity
cancer classified in situ early stages staging and curative surgery

> 60 days < 1.8% < 8% < 55% > 60 days > 12 weeks
30 - 59 days 1.8 - 3.4% 8 - 12% 55 - 60% 30 - 59 days < 12 weeks (84
City
< 30 days > 3.4% > 12% > 60% < 30 days days)
Barranquilla 22.7 0.0% 66.7% 50.0% 84 ***
Bucaramanga 91.3 0.0% 11.1% 42.9% 71 49.0
Cali 40.0 2.9% 27.3% 36.6% 49 93.5
Manizales 31.9 0.0% 28.6% 50.0% 46 ***
Medellín 25.2 1.9% 29.7% 68.2% 41 50.5
Pasto 33.0 0.0% 16.7% 35.3% 42 ***
Total 34.1 1.7% 29.0% 53.4% 47 67.4

8. Proportion of stage 0 13. Proportion of


7. Opportunity between 12.Proportion of
to III patients post-surgical patients 15. Overall 16. Operative
surgery and the start patients with nutrition
undergoing surgery as a with nutritional mortality rate mortality
of adjuvant assessment
curative treatment support

> 12 weeks < 20% <14% < 22% > 20%


< 12 weeks 20-27% 14 - 17% 22 - 33% to be decided
City < 20%
(84 days) >27% > 17% > 33%
Barranquilla 69.0 40.0% 16.7% 0.0% 1.4 0.0%
Bucaramanga 20.0 25.0% 19.0% 0.0% 7.9 25.0%
Cali 52.3 7.1% 29.0% 26.7% 7.1 0.0%
Manizales *** 0.0% 0.0% 100.0% 8.5 0.0%
Medellín 54.2 40.7% 19.2% 14.3% 6.2 0.0%
Pasto 63.0 0.0% 5.9% 0.0% 4.9 0.0%
Total 54.1 29.2% 19.6% 16.4% 5.9 1.5%
Source: High Cost Diseases Fund Database Resol 0247/14 - Cut-off date: January 01, 2016

Bucaramanga was the only city to report cases of people with the In Colombia, the measurement of indicators for the evaluation and
disease who died within the first 30 days of the postoperative period. monitoring of risk management is of great importance in order to
determine whether the actions against cancer are being carried
Colon and rectum cancer out correctly in the country and otherwise, to take effective and
The total numbers of indicators included in the consensus were efficient measures to correct it.
1516 (Table 6), of which, due to the availability of the information,
12 were measured. In terms of opportunity times, Pasto and The results for each type of cancer in the different cities are
Barranquilla had the shortest time to confirm the diagnosis, 11 heterogeneous and show strengths and weaknesses for each of
and 27 days respectively; Bucaramanga presented the shortest the cities and within the processes of caring for a cancer patient.
time to start treatment. Manizales and Medellin were the cities The results can be approximated and be a reflection of the reality
with the highest proportion of patients with TNM staging. of the care process. However, there may also be weaknesses in
the reporting to the High Cost Diseases Fund, with incomplete
In terms of treatment, given by patients who underwent surgery information on the part of the insurers, especially since the
with curative intent, the highest proportion of cases occurred registry has been operating for a few years only. Likewise, the
in the city of Pasto. However, none of the cities reached the attention process is not only different according to illnesses but
established standard. they also manifest themselves in a different way in each person,
with certain particularities and therefore with specific times of
opportunity for each one of them. However, when observing the
Discussion defined standards in each of the consensus reached, a common
In different parts of the world, the development of indicators to agreement is obtained stating that for these solid characteristic
evaluate the quality of cancer care has gained great importance neoplasms, the average time that should elapse from the moment
due to the public health problem that it represents and how close to the first doctor who has the clinical and paraclinical tools makes
30% of cases with this group of diseases could be avoided. Likewise, the decision to refer the patient for diagnostic confirmation until
cancer is currently affecting countries especially in low and middle the first treatment is performed, there should be about 60 days in
levels in the Human Development Index, where more than 60% of total for it to be considered good management.
cases occur17. It is urgent that governments know and monitor the
actions carried out by the different factors that have influence in It is also important to mention that the differences between cities
patients having access to quality health services and on time. for certain types of cancer may be due to their geographical location

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Tabla 6. Risk management indicators in colon and rectal cancer by city of residence
7. Opportunity
9. Proportion of stage
between neoadjuvant 8. Opportunity 11. Proportion of
I to III patients under- 14. Overall 15. Incidence of colon
and curative surgery between surgery and patients with nutrition
going surgery as a mortality rate and rectum cancer
in patients with the start of adjuvant assessment
curative treatment
rectal cancer

> 12 weeks < 60% < 8%


> 8 weeks(56 days)
(84 days)
60 - 90% 8 - 11% to be decided to be decided
City 8-12 weeks < 8 weeks > 90% > 11%

Barranquilla *** 68.00 29.2% 9.2% 2.9 5.2


Bucaramanga 131.50 77.00 44.4% 7.1% 6.4 4.9
Cali *** 86.50 15.4% 10.7% 6.3 6.1
Manizales *** 49.00 29.4% 5.0% 9.3 10.1
Medellín 8.00 56.53 38.7% 13.1% 6.8 9.3
Pasto *** 76.00 50.0% 0.0% 2.2 1.3
Total 90.33 61.68 32.5% 10.9% 5.9 6.9
Source: High Cost Diseases Fund Database Resol 0247/14 - Cut-off date: January 01, 2016

in the country and the availability of specialized personnel for the The measured indicators show an overview of the situation in
number of inhabitants and people with the disease in each one the management of cancer by insurers in these cities, and this is
of them. According to figures from the National Cancer Institute considered the first step and an important input that contributes
in 2016  18  , the largest offer of oncological services in Colombia to generating information for making assertive decisions for
are concentrated in: Bogotá (25.1%), Antioquia (12.7%), Valle del the improvement of the quality of care for people with cancer
Cauca (10.7%), Atlántico (9.1%) and, to a lesser extent, Santander in these cities. This articulation with the population registers
(6.6%). Similarly, each capital city of these departments offers more for the realization of studies is crucial where causality analysis
than 88% of the cancer services available in their department 18. is carried out and each type of cancer is analyzed in detail. This
offers the possibility of extending it to other regions in order to
The indicators with the best results were those related to detection identify inequalities in the care process by regions but, above all,
in early stages, especially in gastric and colorectal cancer, these to intervene with the aim of achieving equity.
are cancers that require a specialized process for their diagnosis,
different from those of the breast and cervix. However, the Conflict of interest:
indicator that measures the proportion of patients with staging Authors report no conflicts of interest
was low for most types of cancer, this is possibly due to the lack
of reporting by insurers for this item, since staging is essential to References
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1. Ministerio de Salud y la Protección Social, Instituto Nacional de
With respect to treatment indicators, these usually vary by cities Cancerología E.S.E. Plan decenal para el control de cáncer en Colombia
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en Cáncer y se crea el Observatorio Nacional de Cáncer. 2012.
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5. Forman D, Bray F, Brewster DH, Mbalawa CG, Kohler B,
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6. Allemani C, Matsuda T, Di Carlo V, Harewood R, Matz M, Nikšić 14. Cuenta de Alto Costo. Consenso basado en evidencia:
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en Salud Colombiano. Bogota: Fundación Santa Fe; 2014. Available
indicadores de gestión del riesgo en pacientes con cáncer de próstata
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de Participación y deliberación. Bogotá D.C.: Instituto de 16. Cuenta de Alto Costo. Consenso basado en evidencia:
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iarc.fr/Non-Series-Publications/World-Cancer-Reports/World-
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12. Brouwers MC, Kho ME, Browman GP, Burgers JS, Cluzeau
files/libros/archivos/ Servicios Oncologicos Boletín.pdf.
F, Feder G, et al. AGREE II: Advancing guideline development,
reporting and evaluation in healthcare. Can Med Assoc J. 19. Bozzetti F, Mariani L, Lo Vullo S, Amerio ML, Biffi R,
2010;63(12):1308-11. Caccialanza R, et al. The nutritional risk in oncology: A study of 1,
453 cancer outpatients. Support Care Cancer. 2012;20(8):1919-28.
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Supplementary material. 
Table S1. Cancer incidence and mortality, 25 cancer categories. Colombia, 2007-2011
Incidence Cases (year) Rates (Men) Rates (Women) Observed deaths (year) Rates (men) Rates (women)
Cancer category
Total Men Women CR ASR CR ASR Total Men Women CR ASR CR ASR
All cáncer witout skin 62,818 29,734 33,084 133.9 151.5 145.3 145.6 32,653 16,081 16,572 72.4 82.3 72.8 73.2
Lips, Oral cavity and pharynx 1,494 787 707 3.5 4.0 3.1 3.1 501 295 206 1.3 1.5 0.9 0.9
Esophagus 864 573 291 2.6 3.0 1.3 1.3 664 451 213 2.0 2.3 0.9 0.9
Stomach 5,955 3,613 2,342 16.3 18.5 10.3 10.3 4,537 2,767 1,770 12.5 14.2 7.8 7.8
Colorrectal 2,401 2,784 10.8 12.2 12.2 12.3 2,544 1,168 1,376 5.3 6.0 6.0 6.1
Liver 1,138 541 597 2.4 2.8 2.6 2.6 1,621 762 859 3.4 3.9 3.8 3.8
Gallblader 1,098 281 817 1.3 1.4 3.6 3.6 776 228 548 1.0 1.2 2.4 2.4
Pancreas 1,191 512 679 2.3 2.6 3.0 3.0 1,269 583 686 2.6 3.0 3.0 3.0
Larynx 693 575 118 2.6 3.0 0.5 0.5 377 302 75 1.4 1.6 0.3 0.3
Trachea,, bronchi, lung 3,985 2,488 1,497 11.2 12.9 6.6 6.6 3,890 2,357 1,533 10.6 12.2 6.7 6.8
Skin melanoma 1,203 590 613 2.7 3.0 2.7 2.7 226 121 105 0.5 0.6 0.5 0.5
Breast 7,627 … 7,627 … … 33.5 33.8 2,226 … 2,226 … … 9.8 9.9
Cervix 4,462 … 4,462 … … 19.6 19.3 1,861 … 1,861 … … 8.2 8.2
Utero body 771 … 771 … … 3.4 3.5 187 … 187 … … 0.8 0.8
Ovary and others 1,279 … 1,279 … … 5.6 5.6 712 … 712 … … 3.1 3.2
Prostate 8,872 8,872 … 40.0 46.5 … … 2,416 2,416 … 10.9 12.6 … …
Testícle 507 507 … 2.3 2.2 … … 72 72 … 0.3 0.3 … …
Kidney 961 537 424 2.4 2.7 1.9 1.9 379 213 166 1.0 1.1 0.7 0.7
Bladder 1,144 863 281 3.9 4.5 1.2 1.3 401 266 135 1.2 1.4 0.6 0.6
Encephalon, SCN others 1,273 702 571 3.2 3.4 2.5 2.5 952 516 436 2.3 2.5 1.9 1.9
Thyroid 2,448 247 2,201 1.1 1.3 9.7 9.4 219 56 163 0.3 0.3 0.7 0.7
Lymphoma Hodgkin 339 229 110 1.0 1.0 0.5 0.5 119 74 45 0.3 0.4 0.2 0.2
Lymphoma no Hodgkin 2,744 1,542 1,202 6.9 7.5 5.3 5.3 939 518 421 2.3 2.6 1.8 1.9
Leukemia 2,473 1,256 1,217 5.7 6.0 5.3 5.4 1,610 869 741 3.9 4.2 3.3 3.3
Other places/not especified 5,112 2,618 2,494 11.8 13.1 11.0 11.0 4,155 2,047 2,108 9.2 10.4 9.3 9.3
CR:Crude rate
AAR:age-adjusted rate (per 100,000 year-person).

Cancer Incidence and mortality, Departments, Colombia, 2007-2011.


Departamet Total Men Women CR ASR CR ASR Total Men Women CR ASR CR ASR
Colombia 62,818 29,734 33,084 133.9 151.5 145.3 145.6 32,653 16,081 16572 72.4 82.3 72.8 73.2
Antioquia 9,781 4,606 5,175 157.4 173.1 169.0 159.9 5,419 2638 2781 90.2 99.7 90.8 86.2
Arauca 253 121 132 98.0 144.3 109.1 148.4 113 55 58 44.5 67.0 47.9 68.9
Atlántico 3,010 1,371 1,639 121.7 147.9 141.5 144.9 1,447 695 752 61.7 75.3 64.9 67.5
Bogotá 11,068 4,924 6,144 140.8 167.7 163.3 158.0 5,608 2607 3001 74.6 90.1 79.7 78.5
Bolívar 2,019 983 1,036 100.4 120.8 105.8 113.7 961 496 465 50.7 61.1 47.5 52.0
Boyacá 1,813 904 909 143.0 136.0 143.6 128.6 948 493 455 78.0 73.2 71.9 61.1
Caldas 1,860 871 989 182.2 171.2 198.5 170.4 1,008 499 509 104.4 97.5 102.2 85.5
Caquetá 447 229 218 102.6 132.0 99.6 127.4 226 117 109 52.4 68.6 49.8 66.4
Casanare 309 160 149 98.3 145.8 95.0 123.5 151 77 74 47.3 71.8 47.2 65.2
Cauca 1,521 726 795 109.5 122.2 123.2 128.6 788 394 394 59.5 66.0 61.0 63.2
Cesar 990 497 493 104.3 141.7 103.2 127.3 492 254 238 53.3 72.9 49.8 65.4
Chocó 279 145 134 61.8 99.7 56.5 78.2 128 66 62 28.1 45.0 26.2 37.1
Córdoba 1,356 687 669 87.8 105.5 86.2 97.6 661 330 331 42.2 50.6 42.6 49.0
Cundinamarca 3,157 1,546 1,611 127.0 135.0 132.0 129.9 1,649 851 798 69.9 74.2 65.4 63.7
Huila 1,451 740 711 137.9 160.3 133.6 145.9 773 410 363 76.4 88.9 68.2 74.6
La Guajira 440 214 226 54.7 83.0 56.6 72.6 201 100 101 25.5 38.8 25.3 33.5
Magdalena 1,249 634 615 105.5 133.0 104.2 122.2 633 329 304 54.8 69.5 51.5 61.6
Meta 1,206 594 612 138.5 166.9 144.3 167.9 616 313 303 73.0 88.7 71.4 86.2
Nariño 1,810 813 997 100.1 111.7 123.5 127.7 947 463 484 57.0 63.6 59.9 61.9
Norte de Santander 1,815 900 915 141.0 165.3 141.1 148.6 986 497 489 77.9 91.8 75.4 79.7
Putumayo 202 105 97 63.9 94.4 61.2 85.4 102 55 47 33.5 49.6 29.7 43.3
Quindío 1,172 557 615 207.7 195.5 220.9 193.3 616 318 298 118.6 111.2 107.1 91.5
Risaralda 1,723 828 895 184.7 182.4 189.9 168.6 958 469 489 104.6 103.2 103.8 91.0
San Andrés y Providencia 78 44 34 121.6 163.8 93.0 94.8 25 15 10 41.5 61.7 27.4 29.0
Santander 2,961 1,392 1,569 140.9 150.0 155.0 145.5 1,544 768 776 77.8 82.8 76.7 70.8
Sucre 737 360 377 88.5 100.4 95.2 103.6 379 186 193 45.7 52.0 48.7 53.4
Tolima 2,308 1,119 1,189 160.8 150.2 172.9 161.3 1,180 610 570 87.7 81.1 82.9 75.1
Valle del Cauca 7,639 3,582 4,057 170.1 179.6 181.7 167.1 4,015 1931 2084 91.7 96.8 93.3 85.1
Amazonas group * 164 82 82 50.6 82.1 54.0 83.4 79 45 34 27.8 47.4 22.4 37.3
TC: crude rate;
AAR: Age-adjusted rate (por 100,000)
*Amazonas, Guainía, Guaviare, Vichada y Vaupés

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Colomb Med. (Cali) 49(1): 16-22


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Supplementary material. 
Table S1. Municipality of Medellin, Colombia. Incidence data of malignant tumors prioritized in the Decade Cancer Control Plan in
Colombia during 2010-2014.
Age
Localization n 0-4 5-9 10-14 15-19 20-24 25-29 30-34 35-39 40-44 45-49 50-54 55-59 60-64 65-69 70-74 75-79 80 + Crude ASR
Desc
Breast (C50) 3,286 14 0.0 0.0 0.0 0.0 1.2 5.8 16.2 27.7 56.9 91.5 85.5 112.9 123.3 147.5 160.9 141.3 166.6 51.9 36.5
Cervix (C53) 708 1 0.0 0.0 0.0 0.2 1.4 9.0 12.9 20.0 18.0 17.2 17.4 21.2 16.6 20.7 15.0 9.2 19.1 11.2 8.5
Prostate (C61) 2,571 15 0.0 0.0 0.0 0.0 0.0 0.0 0.2 0.9 3.9 12.2 28.6 89.3 187.4 293.1 401.9 411.7 407.7 45.7 38.6
Colorrectal (C18-C20) 1,640 5 0.0 0.0 0.1 0.5 0.6 2.7 2.8 3.8 7.2 10.9 14.7 23.7 37.5 53.9 62.3 87.5 128.8 13.7 10.0
Men 747 3 0.0 0.0 0.0 0.6 0.6 3.1 3.5 2.0 5.2 11.6 14.3 24.1 40.7 66.1 72.4 99.0 149.7 13.3 11.0
Women 893 2 0.0 0.0 0.3 0.4 0.6 2.2 2.2 5.4 8.9 10.3 15.0 23.4 35.1 44.9 55.2 80.2 117.0 14.1 9.4
Colon (C18) 1,080 3 0.0 0.0 0.1 0.3 0.5 2.1 1.6 3.4 4.9 7.1 9.8 14.0 25.4 34.5 40.0 59.4 84.8 9.0 6.6
Men 474 3 0.0 0.0 0.0 0.4 0.6 2.5 1.7 1.7 3.6 7.7 10.4 13.3 27.0 39.5 47.4 60.4 90.6 8.5 7.0
Women 606 0 0.0 0.0 0.3 0.2 0.4 1.8 1.5 4.9 5.9 6.6 9.3 14.6 24.1 30.8 34.8 58.8 81.5 9.6 6.4
Rectum (C19-C20) 560 2 0.0 0.0 0.0 0.2 0.1 0.5 1.2 0.4 2.4 3.8 4.9 9.7 12.2 19.4 22.3 28.1 44.0 4.7 3.4
Men 273 0 0.0 0.0 0.0 0.2 0.0 0.6 1.7 0.3 1.6 3.9 4.0 10.8 13.7 26.5 25.0 38.6 59.1 4.8 4.0
Women 287 2 0.0 0.0 0.0 0.2 0.2 0.4 0.7 0.5 3.0 3.7 5.7 8.8 11.0 14.1 20.4 21.4 35.5 4.6 3.0
Stomach (C16) 1,209 12 0.0 0.0 0.0 0.0 0.4 1.6 3.6 3.8 4.6 7.7 10.4 17.4 25.2 35.8 60.9 66.0 88.0 10.2 10.1
Men 695 6 0.0 0.0 0.0 0.0 0.2 1.9 3.5 4.0 3.6 10.4 14.8 27.2 32.2 47.2 90.5 103.8 123.3 12.4 12.3
Women 514 6 0.0 0.0 0.0 0.0 0.6 1.4 3.7 3.6 5.4 5.4 6.9 9.8 19.7 27.3 40.2 42.0 68.1 8.2 8.1
All localizations 22,379 111 12.0 11.4 11.1 19.1 25.7 48.2 77.2 97.2 125.6 178.8 221.5 345.8 483.8 661.9 874.5 943.1 11,75.0 187.1 143.4
Men 9,602 43 13.9 11.7 11.1 18.0 22.7 33.7 48.6 52.6 71.4 116.8 160.7 309.5 524.3 793.8 1,125.0 1,295.0 15,74.0 171.3 144.4
Women 12,777 68 10.1 11.0 11.0 20.2 28.7 62.1 102.5 134.8 170.8 230.0 270.0 374.5 452.2 563.5 699.9 720.2 950.1 202.9 145.6
Non-invasive cervical
2,254 44 0.0 0.0 0.0 4.4 35.3 85.6 99.7 71.1 61.7 37.7 26.2 22.7 25.0 20.3 18.6 6.9 5.0 35.6 30.6
neoplasias
Infantile Leukemia 77 0 3.7 3.2 3.2 0.6 1.1
Men 38 0 3.7 3.4 2.7 0.7 1.0
Women 39 0 3.6 3.0 3.8 0.6 1.1
Source: Population-based Cancer Registry of Antioquia.

Table S2. Municipality of Medellin, Colombia. Mortality information of malignant tumors prioritized in the Decade Cancer Control
Plan in Colombia during 2010-2014.
10-
Localization n 0-4 5-9 15-19 20-24 25-29 30-34 35-39 40-44 45-49 50-54 55-59 60-64 65-69 70-74 75-79 80 + Crude ASR
14
Breast (C50) 1,075 0.0 0.0 0.0 0.2 0.0 1.2 2.6 7.5 11.3 19.1 24.5 27.1 41.6 51.1 73.2 62.6 129.7 17.0 12.9
Cervix (C53) 391 0.0 0.0 0.0 0.0 0.4 2.6 4.2 5.1 7.4 6.7 9.9 8.5 13.8 15.0 20.4 18.3 31.9 6.2 4.9
Prostate (C61) 798 0.0 0.0 0.0 0.0 0.0 0.0 0.2 0.0 0.5 0.2 1.7 7.1 25.4 46.6 99.2 142.4 489.5 14.2 14.6
Colorrectal (C18-C20) 1,216 0.0 0.0 0.1 0.3 0.4 0.9 1.9 1.8 3.7 6.3 8.3 14.0 21.7 37.6 62.3 63.6 142.4 10.2 7.2
Men 575 0.0 0.0 0.2 0.4 0.2 1.5 2.5 1.2 2.9 6.8 9.4 13.6 19.7 53.1 74.2 77.3 173.6 10.2 8.4
Women 641 0.0 0.0 0.0 0.2 0.6 0.4 1.3 2.4 4.3 5.8 7.5 14.4 23.2 26.0 54.0 55.0 124.8 10.1 6.5
Colon (C18) 1015 0.0 0.0 0.1 0.2 0.4 0.7 1.4 1.2 3.1 4.6 6.6 11.6 17.8 31.8 52.4 54.7 123.3 8.5 6.0
Men 476 0.0 0.0 0.2 0.2 0.2 1.0 2.2 0.6 2.6 5.4 7.2 11.4 16.9 44.8 58.6 64.0 148.5 8.5 6.9
Women 539 0.0 0.0 0.0 0.2 0.6 0.4 0.7 1.7 3.5 3.9 6.1 11.7 18.5 22.0 48.0 48.9 109.2 8.5 5.4
Rectum (C19-C20) 201 0.0 0.0 0.0 0.1 0.0 0.2 0.5 0.7 0.6 1.6 1.8 2.5 3.9 5.8 9.9 8.9 19.0 1.7 1.2
Men 99 0.0 0.0 0.0 0.2 0.0 0.4 0.2 0.6 0.3 1.4 2.2 2.2 2.8 8.3 15.5 13.3 25.2 1.8 1.5
Women 102 0.0 0.0 0.0 0.0 0.0 0.0 0.7 0.7 0.9 1.9 1.4 2.7 4.7 4.0 6.0 6.1 15.6 1.6 1.1
Stomach (C16) 1,467 0.0 0.0 0.0 0.0 0.3 1.3 2.9 4.2 4.7 8.2 13.2 16.1 27.5 39.8 71.1 87.9 151.0 12.3 10.3
Men 801 0.0 0.0 0.0 0.0 0.0 1.7 2.2 4.9 4.9 9.8 16.8 22.9 37.5 54.3 99.2 130.4 195.0 14.2 13.6
Women 666 0.0 0.0 0.0 0.0 0.6 1.0 3.5 3.6 4.6 6.9 10.3 10.7 19.7 29.1 51.6 61.1 126.2 10.5 8.0
All localizations 14,922* 5.3 5.3 5.2 10.0 8.1 10.0 20.9 27.3 37.9 65.6 106.3 172.2 282.4 450.0 703.6 897.7 1657.9 124.7 89.7
Men 6,941 4.5 5.5 3.6 12.2 9.0 10.0 17.3 20.5 27.5 58.5 98.3 178.4 318.4 520.7 845.1 1101.0 2129.0 123.3 101.1
Women 7,980 6.2 5.2 6.8 7.8 7.2 10.0 24.1 33.1 46.5 71.4 112.7 167.3 254.4 397.1 605.0 769.1 1391.8 126.0 82.6
Infantile Leukemia 46 1.2 2.3 2.5 0.4 0.6
Men 21 0.5 2.4 2.4 0.4 0.5
Women 25 2.0 2.2 2.5 0.4 0.7
*There is one case of mortality of unknown gender. Source: Population-based Cancer Registry of Antioquia.

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