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EDITORIAL
Epidemiology of cancer in Colombia Luis
Eduardo Bravo, Nubia Muñoz 9-12
ORIGINAL ARTICLES
Cancer incidence estimates and mortality for the top five cancer in
Colombia, 2007-2011
Constanza Pardo, Ricardo Cendales 16-22
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
Editorial
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
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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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.
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Editorial
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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9. Bravo LE, Collazos T, Collazos P, García LS, Correa P. Trends 15. Valencia O, Lopes G, Sánchez P, Acuña L, Uribe D, González
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.
12. Arias NE. Registros poblacionales de cáncer: avances en 2016; 20(1): 41-7.
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.
13. Pardo RC, Cendales DR. Incidencia, prevelancia y mortalidad J Global Oncol. 2017; 4: 1-3. doi: 10.1200/JGO.17.00093.
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.
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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
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.
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)
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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).
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).
18
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 …
19
Pardo C/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)
Figure 1(a-e). Cancer incidence and mortality, according to provinces, five main locations, Colombia, 2007-2011.
20
Pardo C/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)
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.
cancer incidence and mortality in the Women’s Health Initiative
J Glob Oncol. 2018; 4:1-3. doi: 10.1200/JGO.17.00093.
Observational Study. J Natl Cancer Inst. 2013;105:526-35.
17. Departamento Administrativo Nacional de Estadística.
29. Kabat GC, Jones JG, Olson N, Negassa A, Duggan C, Ginsberg
Estimaciones 1985-2005 y Proyecciones 2005-2020 nacional y
M, Rohan, TE. Risk factors for breast cancer in women biopsied
departamental desagregadas por sexo, área y grupos quinquenales
for benign breast disease: A nested case-control study. Cancer
de edad. Accessed: 30 June 2014. Available from: https://www.dane.
epidemiol. 2010;34(1):34-9.
gov.co/index.php/poblacion-y-demografia/series-de-poblacion.
30. Ministerio de Salud y Protección social. Sistemas de
18. Loos AH, Bray F, McCarron P, Weiderpass E, Hakama M,
Información –PAI. Presentación Coberturas PAI 2014. 2014.
Parkin DM. Sheep and goats: separating cervix and corpus uteri
Accessed: 10 November 2017. Available from: https://www.
from imprecisely coded uterine cancer deaths, for studies of
geographical and temporal variations in mortality. Eur J Cancer. minsalud.gov.co/sites/rid/Lists/BibliotecaDigital/RIDE/VS/PP/
2004; 40(18): 2794-803. PAI/Rol%20de%20la%20EAPB%20en%20PAI.%20Enero%20
%202014.pdf.
19. Capocaccia R. Relationships between incidence and mortality
in non-reversible diseases. Stat Med. 1993;12(24):2395-415. 31. Forman D, de Martel C, Lacey CJ, Soerjomataram I, Lortet-
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.
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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
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Bravo LE/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)
Original article
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.
23
Bravo LE/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)
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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Bravo LE/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)
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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Bravo LE/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)
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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Bravo LE/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)
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%;
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.
27
Bravo LE/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)
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)
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)
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.
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)
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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Bravo LE/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)
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
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
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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Bravo LE/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)
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
31
Bravo LE/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)
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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.
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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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 (%)
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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
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
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
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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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
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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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Care (Renewed Health, APS-R) as a basis for the organization el Ecuador. Quito; 2011. Available from: http://www.inec.gob.ec/
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Original Article
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.
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)
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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Yepez MC/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)
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
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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Yepez MC/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)
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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20
20
Observerd rate Modeled rate Observerd rate Modeled rate
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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20
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
48
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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
49
Yepez MC/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)
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)
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
50
Yepez MC/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)
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Observerd rate Modeled rate Observerd rate Modeled rate
25 16
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ASR x 100,000 Females - year
15 10
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APC= -1.60 2 APC= -1.60
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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
51
Yepez MC/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)
(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).
52
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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Vargas MR/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)
Original Article
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.
Corresponding author:
Edgar Navarro Lechuga. Hospital Universidad del Norte, Calle 30 Autopista
Aeropuerto, Ciudadela Rotaria. E-mail: enavarro@uninorte.edu.co
55
Vargas MR/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)
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)
56
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
57
Vargas MR/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)
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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Vargas MR/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)
Men Women
500 500
400 400
300 300
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
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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.
1. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, 15. Havener L. Standards for cancer registries volume III:
et al. Cancer incidence and mortality worldwide: sources, methods standards for completeness, quality, analysis, and management
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.
2. Forouzanfar H, Alexander L, Anderson R, Bachman V, Biryukov 16. Forman D, Bray F, Brewster D, Gombe Mbalawa C, Kohler B,
S, Brauer M, et al. Global, regional, and national comparative risk Piñeros M, et al. Cancer incidence in five continents, Vol. X Lyon:
assessment of 79 behavioural, environmental and occupational, and IARC; 2013.
metabolic risks or clusters of risks in 188 countries, 1990–2013: a
systematic analysis for the Global Burden of Disease Study 2013. 17. Sistema de Información de cáncer de Colombia. Tomado de:
http://www.infocancer.co/portal/#!/home. Accessed: Octubre 2017
Lancet. 2015; 386(10010): 2287-2323.
18. Tanca J, Arreaga C. Incidencia del cáncer en Guayaquil 2003-
3. Ministerio de la Protección Social. Plan nacional para el
2006. Rev Oncol. 2010; 1(2): 15-20.
control del cáncer en Colombia 2010-2019. Bogotá: Instituto
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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Original articles
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.
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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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
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
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
0.00
0 20 40 60 0 20 40 60
Months Months
High Intermediate Low High Intermediate Low
Lung Prostate
1.00
1.00
Survival proportion
Survival proportion
0.50
0.50
0.25
0.25
0.00
0 20 40 60 0 20 40 60
Months Months
Stomach
1.00
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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10. Congreso de la República. Ley 100 de 1993, Por la cual se crea el sistema 23. Tyczynski J, Demaret E, Parkin D. Standards and Guidelines for
de seguridad social integral y se dictan otras disposiciones. Diario Oficial Cancer Registration in Europe. IARC Technical Publication No. 40.
No. 41.148 de 23 de diciembre de 1993: Bogotá, D. C.; 1993. WHO: France; 2003.
11. Así vamos en Salud. Indicadores de aseguramiento [Internet]. 24. Singh GK, Miller BA, Hankey BF, Edwards B. Area socioeconomic
Así vamos en salud. Bogotá; 2017. Cited: 2017 Sep 15. Available variations in U.S CAncer incidence, mortality, stage, treatment and
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Uribe PCJ/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)
Original article
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.
Corresponding author:
Claudia Janeth Uribe Pérez. Universidad Autónoma de Bucaramanga.
Av. 42 #48 – 11. E-mail: curibep@unab.edu.co
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Uribe Pérez CJ/et al/Colombia Médica - Vol. 49 Nº1 2018 (Ene-Mar)
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
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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10. Shin HR, Curado MP, Ferlay J, Heanue M, Edwards B, Storm 26. Bray F, Colombet M, Mery L, Piñeros M, Znaor A, Zanetti R et
H. Chapter 5: Comparability and quality of data. Consultado: al. CI5 XI - Home; 2017. Available from: http://ci5.iarc.fr/CI5-XI/
noviembre 2 de 2017. Available from: : http://www.iarc.fr/en/ Default.aspx.
publications/pdfs-online/epi/sp160/CI5vol9-5.pdf
27. Sierra MS, Soerjomataram I, Antoni S, Laversanne M, Piñeros
11. Ospina ML, Huertas JA, Montaño JL, Rivillas JC. Observatorio Nacional M, de Vries E, et al. Cancer patterns and trends in Central and South
de Cáncer Colombia. Rev Fac Nac Salud Pública. 2015;33(2):262–176. America. Cancer Epidemiol. 2016;44:S23–42.
12. Parkin DM. The role of cancer registries in cancer control. Int J 28. Ministro de Salud y Protección Social. Quinto Informe ONS:
Clin Oncol. 2008;13(2):102–11. carga de enfermedad por enfermedades crónicas no transmisibles
y discapacidad en Colombia. Imprenta Nacional de Colombia,
13. Ministerio de Salud y Protección Social, Instituto Nacional de Bogotá, DC.; 2015.
Cancerología. Plan Nacional para el control del Cáncer en Colombia.
2012-2020. Bogotá: Ministerio de Salud y Protección Social; 2012 29. Hormiga CM, León MH, Otero JA, Rodríguez LA. Factores de
riesgo para enfermedades crónicas en Santander. Método STEPwise.
14. Corporación Autónoma Nacional para la Defensa de la Meseta de
1a ed. Bucaramanga: Secretaría de Salud de Santander, Observatorio
Bucaramanga. Área de Jurisdicción. 2017. Consultado: noviembre
de Salud Pública de Santander; 2010.
2 de 2017. Available from: http://www.cdmb.gov.co/web/asi-es-la-
cdmb/area-de-jurisdiccion
30. Hormiga CM, Alzate PML, Borrell C, Palència L, Rodríguez VLA,
15. DANE. Series de población. Consultado: noviembre 2 de 2017. Otero WJA, et al. Actividad física ocupacional, de transporte y de
Available from: http://www.dane.gov.co/index.php/estadisticas- tiempo libre: Desigualdades según género en Santander, Colombia.
por-tema/demografia-y-poblacion/series-de-poblacion. Rev Salud Pública. 2016;18(2):201–13.
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31. Hormiga CM. Influencia del género en la práctica regular de 33. De Vries E, Uribe C, Pardo C, Lemmens V, Van de Poel E,
actividad física en Santander, Colombia. Tesis doctoral. Universidad Forman D. Gastric cancer survival and affiliation to health insurance
Nacional de Colombia. 2015. Available from: http://www.bdigital. in a middle-income setting. Cancer Epidemiol. 2015;39(1):91–6.
unal.edu.co/52823/
34. Mantilla-Villabona LY, Ospina-Galeano DC, Maturana-Martínez
32. Álvarez LS. Los estilos de vida en salud: del individuo al contexto. DMA. Barreras para la atención en salud durante el diagnóstico y
Rev Fac Nac Salud Pública. 2012;30(1):95–101. tratamiento del cáncer gástrico. MedUNAB. 2017;19(3):211–20.
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Original Article
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.
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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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
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
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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Table 2. Age standardized incidence rates (world population) of the principle types of cancer. Data comparison among the Population
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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al. Carga de enfermedad en años de vida ajustados por discapacidad
Salud Pública Universidad de Antioquía; 2007 pp 79.
del cáncer gástrico en Colombia. Rev Colomb Gastroenterol.
17. Rodríguez-Cuevas S, Macías-Martínez CG, Labastida- 2017;32(4): 326-331.
Almendaro S. Breast cancer in Mexico. Is it a young women's
32. Bravo LE, García LS, Collazos P, Carrascal E, Ramírez O, Cortés
disease?. Ginecol Obstet Mex. 2000; 68: 185-190.
A, Nuñez M, Millán E . I. Reliable information for cancer control in
18. American Cancer Society. Breast cancer facts & figures 2011- Cali, Colombia. Colomb Med (Cali). 2018; 49(1): 23-34.
2012. Atlanta, Georgia: American Cancer Society; 2011. Accessed:
33. Uribe PCJ, Serrano GSE, Hormiga SCM. Cancer incidence and
26 December 2017. Available from: http://www.cancer.org/ acs/
mortality in Bucaramanga, Colombia. 2008-2012. Colomb Med
groups/content/@epidemiologysurveilance/documents/ document/
(Cali). 2018; 49(1): 73-80.
acspc-030975.pdf.
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34. Arias-Ortiz NE, De Vries E. Health inequities and cancer survival 36. INS. Guía de Control de Calidad para la toma, procesamiento e
in Manizales, Colombia: a population-based study. Colomb Med interpretación en Muestras de Citología de Cuello Uterino. Bogotá,
(Cali). 2018; 49(1): 63-72 INS. 2009. Accessed: 04 March 2018. Available from: https://
es.scribd.com/document/127882153.
35. Yepez MC, Jurado DM, Bravo LM, Bravo LE. Trends in cancer
incidence, and mortality in Pasto, Colombia. 15 years experience. 37. Ministerio de Salud y Protección Social. Profamilia. Encuesta
Colomb Med (Cali). 2018; 49(1): 42-54. Nacional de Demografía y Salud 2015.
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Artículo original
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.
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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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
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
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)
Colombia is a country with a wide and extensive range of 8. Ministerio de Salud y Protección Social. Resolución 2003/2014
oncological services throughout the national territory, with service del 28 de mayo. Por la cual se definen los procedimientos y
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condiciones de inscripción de los Prestadores de Servicios de 11. Ministerio de Salud y Protección Social. Resolución 1441/2016
Salud y de habilitación de servicios de salud. Diario Oficial, del 21 de abril. Por la cual se establecen los estándares, criterios
número 49.167, (30/05/14); 2014. Available from: y procedimientos para la habilitación de las Redes Integrales de
ht t p s : / / w w w. m i n s a lu d . g ov. c o / Nor m at i v i d a d _ Nu e v o / Prestadores de Servicios de Salud y se dictan otras disposiciones.
Resoluci%C3%B3n%202003%20de%202014.pdf. [Internet]. Diario Oficial, número 49.851, (21/04/16); 2016;
Available from: https://www.minsalud.gov.co/sites/rid/Lists/
9. Dirección de Servicios y Atención Primaria. Registro especial de BibliotecaDigital/RIDE/DE/DIJ/resolucion-1441-2016.pdf
prestadores de servicios de salud. 2017. Bogotá D.C.: Ministerio de
Salud y Protección Social; 2017. Accessed: 30 June 2017. Available 12. Suárez F, Quintero A. Conceptos preliminares sobre los
from: https://prestadores.minsalud.gov.co/habilitacion/ servicios oncológicos en Colombia. Rev Colomb Cancerol.
2008;12(1):12-22.
10. Ministerio de Salud y Protección Social. Resolución 1477/2016
del 22 de abril. Por la cual se define el procedimiento, los estándares 13. Commissioning support for London. A model of care for
y los criterios para la habilitación de las Unidades Funcionales cancer services. Clinical paper. London: National Health Service;
para la Atención Integral de Cáncer del Adulto "UFCA" y de las 2010.
Unidades de Atención de Cáncer Infantil "UACAI" y se dictan otras
disposiciones. Diario Oficial, número 49.852 (22/04/16); 2016. 14. González M. Diagnóstico de instituciones prestadoras de salud
Available from: https://www.minsalud.gov.co/Normatividad_ con habilitación de servicios oncológicos en Bogotá, Colombia.
Nuevo/Resoluci%C3%B3n%201477%20de%202016.pdf. Rev Gerenc Polit Salud. 2012;11(22):92-106.
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Original Article
Amaranto Suarez Mattos, Jairo Aguilera, Edgar Augusto Salguero, Carolina Wiesner
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.
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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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.
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.
Original Article
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.
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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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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Pardo C /et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)
Table 2. Distribution of cancer stage by type of affiliation to the social security system
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.
20. Rositch AF, Nowak RG, Gravitt PE. Increased age and 21. Piñeros M, Sánchez R, Perry F, García O, Ocampo R,
race-specific incidence of cervical cancer after correction for Cendales R. Demoras en el diagnóstico y tratamiento de mujeres
hysterectomy prevalence in the United States from 2000 to 2009. con cáncer de mama en Bogotá, Colombia. Salud Pública Méx.
Cancer. 2014; 120(13): 2032-8. 2011;53(6):478-85.
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Technical report
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.
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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Yumbo
Rural
area of Cali
Palmira
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
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
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
Multiple
Identification Residence Vital Status Tumor
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
Date of birth
Blocking
Indexing
Field
Comprasion Address
Optional
Phone Field
Weight Vector Number
Classification
Possible
Matches Non Matches Clerical Reviewt
Matches
Evaluation Flag
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
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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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
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.
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
118
García LS/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)
RPC-Colombians are incorporated into the cancer information 6. Krystosik AR, Curtis A, Buritica P, Ajayakumar J, Squires R,
system with an adequate budget allocation. Dávalos D, et al. Community context and sub-neighborhood scale
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The implementation of standards and transfer mechanism, pone.0181208.
shared information flows and adoption of tools are priorities
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level and administrative at the clinical level. The main objective supply in Colombia. Colomb Med (Cali). 2018; 49(1): 89-96.
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To all patients and to all oncology care services in Cali. This 10 Ramirez O, Aristizabal P, Zaidi A, Ribeiro RC, Bravo LE.
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Technical report
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.
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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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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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
authorities to allow these crossings with the different health related experience in Colombia. J Registry Manag. 2014;41(3):128-34.
information registries.
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
of the mortality incidence ratio are made according to the place 7. Pardo C, Cendales R. Cancer incidence estimates and mortality,
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.
indicators of both the certification of general death and cancer, it
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
Nothing desconhecidas dos Estados brasileiros. Rev Saude Publica.
2007;41(3):436-45.
References
16. Rao C, Lopez AD, Yang G, Begg S, Ma J. Evaluating national
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as an indicator of health system effectiveness. Health Policy. China. Bull World Health Organ. 2005;83(8):618-25.
2014;9(3):12-9.
17. Pérez-Gómez B, Aragonés N, Pollán M, Suárez B, Lope V, Llácer
2. Thacker SB, Stroup DF, Carande-Kulis V, Marks JS, Roy K, A, et al. Accuracy of cancer death certificates in Spain: a summary of
Gerberding JL. Measuring the public’s health. Public Health Rep. available information. Gac Sanit. 2006;20(Suppl 3):42-51.
2006;121(1):14-22. doi: 10.1177/003335490612100107.
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18. Cáffaro RM, Garau LI, Cabeza IE, Franch SP, Obrador AA. 21. Phillips DE, Lozano R, Naghavi M, Atkinson C, Gonzalez-
Validez de los certificados de defunción por cáncer en mallorca. Gac Medina D, Mikkelsen L, et al. A composite metric for assessing data
Sanit. 1995;9(48):166-73. on mortality and causes of death: the vital statistics performance
index. Population Health Metrics. 2014; 12:14.
19. Mathers CD, Fat DM, Inoue M, Rao C, Lopez AD. Counting the
dead and what they died from: an assessment of the global status of 22. Phillips DE, AbouZahr C, Lopez AD, Mikkelsen L, de Savigny
cause of death data. Bull World Health Organ. 2005;83(3):171-7. D, Lozano R, et al. Are well functioning civil registration and vital
statistics systems associated with better health outcomes? Lancet.
20. WHO. Demographic and socioeconomic statistics: Census and 2015; 386(10001):1386–94.
civil registration coverage. Data by country. WHO 2014. consultado
2014 junio 21. Available from: http://apps.who.int/gho/data/node.
main.121?lang=en.
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Technical report
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.
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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Population Population-based
Studies Cancer Registry
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
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.
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
Source: High Cost Diseases Fund Database Resol 0247/14 - Cut-off date: January 01, 2016
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> 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
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.
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
Source: High Cost Diseases Fund Database Resol 0247/14 - Cut-off date: 01 January 2016
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> 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
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
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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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).
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Pardo C/et al/Colombia Médica - Vol. 49 Nº1 2018 (Jan-Mar)
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.
16