ORIGINAL RESEARCH

Behavioural cancer risk factors in women diagnosed with primary

breast cancer
Mar
a Olivo Del Valle, Rub
en Martin-Payo, Alberto Lana, Juan Bautista Garcia, Mar
a Victoria
Folgueras & Mar
a Luisa Lopez
Accepted for publication 22 March 2014

Correspondence to M.O. Del Valle:

e-mail: delvalle@uniovi.es
Mar
a Olivo Del Valle MD PhD
Senior Lecturer
Department of Public Health & Medicine
Preventive, Faculty of Medicine & Health
Sciences, University of Oviedo, Spain
Rub
en Martin-Payo MSc PhD RN
Full time Lecturer
Department of Nursing, Faculty of
Medicine & Health Sciences, University of
Oviedo, Spain
Alberto Lana MSc PhD RN
Full time Lecturer
Department of Public Health & Medicine
Preventive, Faculty of Medicine & Health
Sciences, University of Oviedo, Spain
Juan Bautista Garcia MD PhD
Senior Lecturer
Department of Public Health & Medicine
Preventive, Faculty of Medicine & Health
Sciences, University of Oviedo, Spain
Mar
a Victoria Folgueras MD PhD
Specialist of the Pathologic Anatomy
Service,
Tumours Registry of the Central University
Hospital of Asturias Coordinator, Oviedo,
Spain
Mar
a Luisa Lopez MD PhD
Senior Lecturer
Department of Public Health & Medicine
Preventive, Faculty of Medicine & Health
Sciences, University of Oviedo, Spain

2810

DEL VALLE M.O., MARTIN-PAYO R., LANA A., GARCIA J.B., FOLGUERAS
M . V . & L O P E Z M . L . ( 2 0 1 4 ) Behavioural cancer risk factors in women diagnosed
with primary breast cancer. Journal of Advanced Nursing 70(12), 28102820.
doi: 10.1111/jan.12433

Abstract
Aims. To investigate behavioural risk factors and self-efficacy among women
diagnosed with breast cancer.
Background. The appearance of new tumours in breast cancer survivors is
influenced by risk behaviours. Knowing their prevalence and womens perceived
ability to adopt a healthy lifestyle would allow designing educational
interventions aimed at modifying these behaviours.
Design. An observational cross-sectional study of women diagnosed with breast
cancer.
Methods. The study was carried out in Asturias (Spain). A total of 2407 breast
cancer patients diagnosed between 19982008 were selected and 492 women
agreed to participate. Self-reported data on risk factors self-efficacy were gathered
through a telephone interview based on the European Code against Cancer
conducted between FebruaryJune 2010.
Results. A total of 16
1% of women in this study were regular smokers, 5%
drank alcohol excessively, 49% were overweight, 54% reported a lower level of
physical activity than recommended and 7
5% did not use sun protection. The
Total Cancer Behavioural Risk indicator was calculated by adding up the results
of all modifiable risks contained in the European Code against Cancer, with an
average score of 21
6 in a scale from 078 points (0 = null cancer risk,
78 = maximum cancer risk). Self-efficacy levels were very high among our
participants.
Conclusion. The results suggest that there is a need to design programmes to
promote a healthy lifestyle among women diagnosed with breast cancer. Nurses
have an important role to play in planning and implementing these programmes,
using the most efficient educational techniques.
Keywords: alcohol, behavioural risks, breast cancer, diet, nurses, obesity, physical activity, primary prevention, smoking, survivors

2014 John Wiley & Sons Ltd

JAN: ORIGINAL RESEARCH

Why is this research needed?

The survival rate for women diagnosed with breast cancer
is very high.
Behavioural risk factors increase the risk of new tumours
in women diagnosed with breast cancer.
There are very few studies on behavioural risk factors and
the self-efficacy to adopt a healthy lifestyle in women with
breast cancer.

What are the key findings?

The prevalence of behavioural risk factors among women
in this study was quite high.
These women had a high level of self-efficacy.

How should the findings be used to influence practice?

Our findings support the introduction of tailored health
promotion programmes targeting breast cancer survivors.
These programmes should be nurse-led and could be implemented during routine follow-up visits.

Introduction
Malignant tumours are one of the leading causes of death
worldwide. According to the World Health Organization
(WHO), deaths from cancer worldwide are projected to
continue to rise, reaching 13
1 million deaths in 2030
(WHO 2011a). Breast cancer is the most commonly diagnosed cancer in women worldwide, with more than 1
2 million cases diagnosed each year. Breast cancer affects 10
12% of the female population and accounts for approximately 500,000 deaths per year worldwide (Benson et al.
2009). Incidence rates are higher in developed countries
compared with less developed countries, but the same is
true for survival rates (WHO 2011b). Thus, mortality rates
in developed countries have remained stable or declined
due to early diagnosis, advances in pharmacological treatment (Jatoi & Mille 2003), a decrease in the use of hormone-replacement therapies (Kumle 2008) and a better
control of risk factors (Hellmann et al. 2010).
In the Principality of Asturias (a region in northern Spain
with a population of approximately 1
1 million), age-standardized (European standard) breast cancer incidence rate is
87
32 per 100,000 women (Direcci

on General de Salud
P

ublica. Consejer
a de Salud y Servicios Sanitarios. Principado de Asturias 2012a), lower than the average rate of the
European Union (94
2) and higher than that of Spain (84
9)
(Ferlay et al. 2013). The mortality rate among Asturian
women (18
1/105 women) (Direcci

on General de Salud P

ubli-

2014 John Wiley & Sons Ltd

Behavioural risk factors among women with breast cancer

ca. Consejer
a de Salud y Servicios Sanitarios. Principado de

Asturias 2012a) is also slightly higher than that of Spain
(16
7/105 women), which has the second lowest breast cancer
mortality rate in the European Union after Estonia (Ferlay
et al. 2013), with predicted rates for 2013 showing a continued downward trend (Malvezzi et al. 2013).

Background
One of the characteristics of women diagnosed with breast
cancer in Western countries is their high survival rate. Survival rates in Europe have increased in the past decades and
the 5-year survival rate is now 73%, with the rate being
slightly higher in Spain at 77% (Berrino et al. 2007, Coleman et al. 2008). However, the rate of second primary
tumours in these women is also high, ranging from 11
13% (Raymond & Hogue 2006, Yu et al. 2006) and showing an upward trend, as L

opez et al. (2009) found in a
study conducted in Asturias. Subsequent malignancies, following the primary breast cancer, are usually located in the
breast, genitourinary system and skin (Soerjomataram et al.
2005, Mariotto et al. 2007).
Evidence suggests that pharmacological treatments,
genetic factors and the presence of behavioural risk factors
contribute to the risk of developing a new malignancy
(S

anchez et al. 2008, Hellmann et al. 2010). However,
despite the critical importance of knowing these risk factors, it is noteworthy that there are very few studies on
their prevalence among breast cancer patients. This lack of
evidence led to the formulation of the research question in
our study: what is the prevalence of behavioural risk factors
among women with breast cancer and what are their levels
of self-efficacy?
Nurses play an important role in health promotion and
disease prevention. Knowing the prevalence of lifestyle factors related to malignant tumours in women diagnosed with
breast cancer will allow nurses working with breast cancer
patients to implement highly effective educational interventions, which will target specifically the most relevant
behavioural risk factors.

The study
Aim
The aim of the study was to describe the modifiable risk
factors among women diagnosed with breast cancer, and to
evaluate participants perceived self-efficacy in the adoption
of a healthy lifestyle to reduce the Total Cancer Behavioural

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Grant W.B. (2007) An ecologic study of cancer mortality rates in
Spain with respect to indices of solar UVB irradiance and
smoking. International Journal of Cancer 20(5), 11231128.
Hellmann S.S., Thygesen L.C., Tolstrup J.S. & Grnbk M.
(2010) Modifiable risk factors and survival in women
diagnosed with primary breast cancer: results from a
prospective cohort study. European Journal of Cancer
Prevention 19, 366373.
Holmes M.D., Chen W.Y., Feskanich D., Kroenke C.H. & Colditz
G.A. (2005) Physical activity and survival after breast cancer
diagnosis. JAMA 293(20), 24792486.
Instituto Nacional de Estad
stica. Ministerio de Sanidad, Pol
tica
Social e Igualdad, Madrid (2009) Encuesta Europea de salud en
Espa~
na 2009. Retrieved from http://www.msc.es/estadEstudios/
estadisticas/EncuestaEuropea/Principales_Resultados_Informe.pdf
on 09 July 2013.
Irwin M.L., Smith A.W., McTiernan A., Ballard-Barbash R.,
Cronin K., Gilliland F.D., Baumgartner R.N., Baumgartner K. &
Bernstein L. (2008) Influence of pre and post diagnosis physical
activity on mortality in breast cancer survivors. Journal of
Clinical Oncology 26(24), 39583964.
Jatoi I. & Mille A.B. (2003) Why is breast cancer mortality
declining? Lancet Oncology 4(4), 251254.
Kimman M.L., Bloebaum M.M.F., Dirksen C.D., Houben R.M.A.,
Lambin P. & Boersma L.J. (2010) Patient satisfaction with
nurse-led telephone follow-up after curative treatment for breast
cancer. BMC Cancer 10, 174. doi:10
1186/1471-2407-10-174.
Kimman M.L., Dirksen C.D., Voogd A.C., Falger P., Gijsen B.C.,
Thuring M., Lenssen A., van der Ent F., Verkeyn J., Haekens C.,
Hupperets C., Nuytinck J.K., van Riet Y., Brenninkmeijer S.J.,
Scheijmans L.J., Kessels A., Lambin P. & Boersma L.J. (2011a)
Nurse led-telephone follow-up and an educational group
programme after breast cancer treatment: results of a 2x2
randomised controlled trial. European Journal of Cancer 47(7),
10271036.
Kimman M.L., Dirksen C.D., Voogd A.C., Falger P., Gijsen B.C.,
Thuring M., Lenssen A., van der Ent F., Verkeyn J., Haekens C.,
Hupperets C., Nuytinck J.K., van Riet Y., Brenninkmeijer S.J.,
Scheijmans L.J., Kessels A., Lambin P. & Boersma L.J. (2011b)
Economic evaluation of a follow-up strategies after curative
treatment for breast cancer: results of an RCT. European Journal
of Cancer 47(8), 11751185.
Kumle M. (2008) Declining breast cancer incidence and decreased
HRT use. The Lancet 372(9639), 608610.
Lewis R., Neal R.D., Williams N.H., France B., Wilkinson C.,
Hendry M., Russell D., Russell I., Hughes D.A., Stuart N.S. &
Weller D. (2009) Nurse-led versus conventional physician-led
follow up for patients with cancer: systematic review. Journal of
Advanced Nursing 65(4), 706723.
Li C.I., Daling J.R., Porter P.L., Tang M.C. & Malone K.E. (2009)
Relationship between potentially modifiable lifestyle factors and
risk of second primary contralateral breast cancer among women
diagnosed with strogen receptor-positive invasive breast cancer.
Journal of Clinical Oncology 32(10), 53125318.
L

opez M.L., Comas A., Del Valle M.O., L

opez S., Garc
a J.B. &
Cueto-Espinar A. (2004) Psychosocial factors associated with
cancer behavioural risk in relatives of cancer patients. European
Journal of Cancer Prevention 13(2), 105111.

2014 John Wiley & Sons Ltd

Behavioural risk factors among women with breast cancer

L

opez M.L., Iglesias J.M., del Valle M.O., Comas A., Fern
andez
J.M., Lana A., Garc
a J.B., L

opez S., Cueto A. & FAPACAN
Working Group (2007) Impact of a primary care intervention on
smoking, drinking, diet, weight, sun exposure and work risk in
families with cancer experience. Cancer Causes and Control 18
(5), 525535.
L

opez M.L., Lana A., D
az S., Folgueras M.V., S
anchez L.,
Comendador M.A., Belyakova E., Rodr
guez J.M. & Cueto A.
(2009) Multiple primary cancer: an increasing health problem.
Strategies for prevention in cancer survivors. European Journal
of Cancer Care 18(6), 598605.
Malvezzi M., Bertuccio P., Levi F., La Vecchia C. & Negri E.
(2013) European cancer mortality predictions for the year 2013.
Annals of Oncology 24(3), 792800.
Mariotto A.B., Rowland J.H., Ries L.A.G., Scoppa S. & Feuer E.J.
(2007) Multiple cancer prevalence: a growing challenge in
long-term survivorship. Cancer Epidemiology, Biomarkers &
Prevention 16(3), 566571.
McEligot A.J., Largent J., Ziogas A., Peel D. & Anton-Culver H.
(2006) Dietary fat, fiber, vegetable and micronutrients are
associated with overall survival in postmenopausal women
diagnosed with breast cancer. Nutrition and Cancer 55(2), 132
140.
Morey M.C., Snyder D.C., Sloane R., Cohen H.J., Peterson B.,
Hartman T.J., Miller P., Mitchell T.C. & Demark-Wahnefried
W. (2009) Effects of home- based diet and exercise on functional
outcomes among older, overweight long- term survivors. JAMA
301(18), 18831891.
Norman S.A., Potashnik S.L., Galantino M.L., De Michele A.M.,
House L. & Localio A.R. (2007) Modificable risk factors for
breast cancer recurrence: what can we tell survivors? Journal of
Womens Health 16(2), 177191.
OECD (2012) Health at a Glance: Europe 2012. OECD
Publishing.
Retrieved
from
http://dx.doi.org/10
1787/
9789264183896-en on 09 July 2013.
Ott J.J., Ullrich A., Mascarenhas M. & Stevens G.A. (2011) Global
cancer incidence and mortality caused by behaviour and
infection. Journal of Public Health 33(2), 223233.
Physical Activity Guidelines Advisory Committee (2008) Physical
Activity Guidelines Advisory Committee Report, 2008. U.S.
Department of Health and Human Services, Washington, DC.
Pierce J.P., Newman V.A., Flatt S.W., Faerber S., Rock C.L.,
Natarajan L., Caan B.J., Gold E.B., Parker B.A., Hollenbach A.,
Wasserman L., Jones L.A., Ritenbaugh C., Stefacnick M.L.,
Thomson C.A. & Kealey S. (2004) Telephone counselling
intervention
increases
intakes
of
micronutrient
and
phytochemical-rich vegetables, fruit and fiber in breast cancer
survivors. The Journal of Nutrition 134(2), 452458.
Pierce J.P., Natarajan L., Caan B.J., Parker B.A., Greenberg B.R.,
Flatt S.W., Rock C.L., Kealey S., Al-Delaymi W.K., Bardwell
W.A., Carlson R.W., Edmon J.A., Faerber S., Gold E.B., Halek
R.A., Hollenbach A., Jones L.A., Karanja N., Madlensky L.,
Marshall J., Newman V.A., Ritenbaugh C., Thomson C.A.,
Wasserman L. & Stefacnick M.L. (2007) Influence of a diet very
high in vegetables, fruit and fiber and low in fat on prognosis
following treatment for breast cancer: the Womens Healthy
Eating and Living (WHEL) Randomized Trial. JAMA 298(3),
289298.

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Behavioural risk factors among women with breast cancer

Perceived self-efficacy to adopt each of these healthy

behaviours was assessed dichotomously (are you able yes/
no) and the total self-efficacy was estimated by means of
the average of the total scores obtained in all behaviours.
Finally, Body Mass Index (BMI) was calculated from selfreported weight and height.

The mean age of the participants was 55
74 years (range

3171 years) and the mean time since cancer diagnosis was
6
07 years (range 211 years). In terms of the level of
education, 48% of the participants had a primary level of
education or less, 28
7% had a secondary level of education
and 23
4% had a university level of education.

Ethical considerations

Behavioural risk factors

This study was approved by the Central University Hospital

of Asturiass Medical Ethics Committee. All participants
provided informed consent prior to the telephone interview.
Participants were informed that all information provided in
the study would remain confidential and any findings would
be reported anonymously.

A total of 79 women reported smoking regularly (16
1%),

although 41
8% of them wanted to quit smoking within
that month. A third of the participants (32
1%) reported
that they did not drink alcohol, whereas 62
8% drank alcohol occasionally or did not exceed the recommended limits,
i.e. no more than a unit a day (Boyle et al. 2003), equivalent to one glass of wine or one glass of beer or one single
small shot of spirits.
A substantial proportion (69
3%) undertook some physical activity, with an average of 5
04 days per week,
although less than half of them (45
7%) followed the health
authority recommendations of 5 days per week of moderate-intensity aerobic activity and at least 30 minutes each
of these days (Physical Activity Guidelines Advisory Committee 2008). Approximately half of the participants were
above the recommended weight (BMI >25 kg/m2): 36
8%
were overweight and 12
2% were obese as defined by the
WHO criteria (WHO 2011c).
Most women (92
5%) used sunscreen and all reported
that they either did not work or were not exposed to risks
in their workplaces. Table 2 shows the percentages of risk
behaviours by age, level of education and time since diagnosis in years, as well as the statistical significance.
When comparing the different behavioural risk factors by
age groups, significant smoking rates, excess weight and low
levels of physical activity were found to be significantly higher
in younger women. Women with a lower education level
smoked less, were more likely to be overweight and engaged
in more physical activity than those participants with a higher
level of education. These differences were significant.
Regarding time since cancer diagnosis, there was only one
statistically significant relationship: women were significantly
less likely to report being overweight 5 years after diagnosis.
No significant differences were found in alcohol intake or
sun protection. With regard to diet, the average number of
servings per year of healthy and unhealthy foods was
1593
4 and 341
21 respectively. Only 3
8% of the interviewed women showed values equal to or below the risk
threshold (0
9).
Table 3 lists the mean intake (expressed in servings/year)
of the different food groups by age, level of education and

Data analysis
The sample was divided into two age groups using the mean
age as the cut-off point (women aged 3155 were classed as
younger women and women aged 5671 were classed as
older women). This allowed for the statistical analysis of
the differences between age groups for all variables.
Descriptive statistics were performed for all variables.
Chi-square and MannWhitney and KruskalWallis nonparametric tests were used to analyse the possible differences between groups. Multivariate analysis was also carried out to establish which variables were significantly
associated with the highest TCBR. Multiple linear regression analysis (stepwise method) was performed using the
TCBR total scores as dependent variable and self-efficacy,
age, time since diagnosis and level of education as independent variables. SPSS version 18.0 (SPSS Inc., Chicago, IL,
USA) was used to analyse the data.

Validity and reliability

The survey instrument used had been previously validated
(L

opez et al. 2004).

Results
Participants
A total of 705 replies were received, which amounted to
34
4% (n = 2047) of the invitation letters. A total of 492
women (24
03%) agreed to participate, 109 (5
32%)
declined to participate, 8 women (0
39%) had died and 96
letters (4
69%) were returned as undeliverable due to an
address change.
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2813

M.O. Del Valle et al.

Table 2 Percentage of risk behaviours by patient characteristics.

Drink more
alcohol than the
recommended
limits

Have a BMI
>25 kg/m2

Yes

No

Yes

No

Yes

No

Yes

No

24
5
75
5
8
5
91
5
0
001***
10
6
89
4
20
6
79
4
21
7
78
3
0
006**
16
2
83
8

6
4
8
5

93
6
91
5

3
9
6
2

96
1
93
8

57
1
45
6

42
9
54
4

60
1
49

39
9
51

92
4
92
9
92
2

4
7
3
5
7
8

7
7

92
3

6
4

93
6

0
01**
62
7
37
3
44
56
27
73
0
001***
55
1
44
9

15
9

7
4

92
6

3
9

96
1

43
4

Smoke
Yes
<55 years
55 years
P
Primary
Secondary
University
P
5 years since
diagnosis
>5 years since
diagnosis
P

Undertake less
physical activity
than recommended

Sun exposure
without protection
No

84
1
0
916

0
399
7
6
7
1
7
8

0
305

0
972

95
3
96
5
92
2
0
276

0
89

0
201

56
6
0
009**

0
01**
47
5
58
9
62
6

52
5
41
1
37
4
0
01**

54
3

45
7

54
3

45
7
0
998

**P < 0
01; ***P < 0
001.

time since diagnosis. Significant differences were found in

the intake of raw and cooked vegetables without meat
(higher in younger women and the women with a higher
education level) and wholegrain cereal (higher in younger
women). Concerning unhealthy foods, major differences
were observed in the intake of vegetables cooked with meat
or meat products (which was higher in the shorter time
since diagnosis), in the intake of pork meat (higher in the
younger age group and the shorter time since diagnosis)
and that of cream, butter or margarine (higher in the younger age group). No significant differences were found in the
consumption of the rest of studied products.

Self-efficacy and TCBR

The level of self-efficacy was very high among the interviewed women, ranging from 85
5% (physical activity) to
95% (moderate alcohol consumption). The average score
for total self-efficacy was 0
94 (range 0
441). The mean
TCBR value among the interviewed women was 21
6 points
(range 569). No significant differences were found in the
TCBR by age group, level of education or time since cancer
diagnosis. The model of multiple linear regression explains
16
3% of the variability in the TCBR, which significantly
increases while self-efficacy decreases (Table 4).

Discussion
The studys participation rate was 24%. Other studies have
obtained similar (McEligot et al. 2006) or lower participation rates (11%) (Morey et al. 2009). Higher recruitment
2814

rates were achieved by means of a personal interview (Trentham-Dietz et al. 2007.

The percentage of women who smoked regularly (16
1%)
was lower in the studied sample than that of women in
Europe (18%) (OECD 2012), Spain (21%) (OECD 2012)
and Asturias (26
4%) (Direcci

on General de Salud P

ublica.
Consejer
a de Salud y Servicios Sanitarios. Principado de
Asturias 2012b). These differences could be due to a higher
level of awareness of harmful effects of smoking among
women with cancer. In any case, smoking is one of the
main risk factors associated with cancer mortality (Hellmann et al. 2010, Ott et al. 2011) and the appearance of a
new primary tumour in breast cancer patients (Li et al.
2009). This finding supports the need to develop smoking
cessation programmes targeting breast cancer patients, as
the percentage of smokers among this sample of women is
still undesirable.
The percentage of women in the sample who reported
not exceeding the recommended limits of alcohol (95%)
was higher than that of Spain (71
5%) and Asturias
(62
3%), as per the data in the latest European Health Survey for Spain (Instituto Nacional de Estad
stica. Ministerio
de Sanidad, Pol
tica Social e Igualdad, Madrid 2009) and
the Principality of Asturias Health Survey (Direcci

on General de Salud P

ublica. Consejer
a de Salud y Servicios Sanitarios. Principado de Asturias 2008). Higher consumption
rates of alcohol in women with breast cancer were found in
other studies (Hellmann et al. 2010). Scientific evidence
suggests that there is an association between alcohol consumption and cancer (Baan et al. 2007) and the appearance
of a new primary tumour in breast cancer patients (Li et al.
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Behavioural risk factors among women with breast cancer

Table 3 Average food servings per year by patient characteristics.

Healthy
food

Fresh
fruit

Raw
vegetables

Vegetables cooked
without meat or
meat products

Pulses cooked
without meat or
meat products

Wholemeal
cereal

<55 years
55 years
P
Primary
Secondary
University
P
5 years since
diagnosis
>5 years since
diagnosis
P

777
3
807
4
0
526
794
4
765
1
824
9
0
467
795
1

290
4
233
6
0
002**
240
4
281
7
275
0
035*
256

161
6
136
5
0
01**
126
1
170
1
166
8
0
005**
149
1

67
5
63
8
0
429
63
4
70
4
64
0
214
64
4

361
2
291
6
0
046*
293
3
344
7
364
0
104
336
7

791
4

264
7

147
8

66
6

313
7

Unhealthy
food
<55 years
55 years
P
Primary
Secondary
University
P
5 years since
diagnosis
>5 years since
diagnosis
P

0
96

0
646

0
89

Pork

Cold
cuts or
sausages

Cakes or
pastries

Cream,
butter or
margarine

10
8
6
7
0
152
8
9
9
4
7
1
0
743
7
2

38
4
32
1
0
003**
34
6
29
5
43
0
617
43
4

8
7
10
9
0
936
12
2
8
4
7
0
06
10
2

93
9
96
0
342
97
86
5
101
1
0
661
107
9

77
9
58
8
0
16
64
4
65
9
77
4
0
869
76
5

58
8
50
3
0
03*
48
2
60
6
59
2
0
065
48
3

10

27
6

9
5

83
3

60

59
8

Pulses cooked
with meat or
meat products

Bacon or
similar meat
products

32
9
33
2
0
988
28
3
38
7
36
0
492
42
8

35
43
8
0
928
41
8
39
4
35
5
0
268
41
5

24
3

38
0
534

0
217

Minced
meat with
pork

Vegetables cooked
with meat or
meat products

0
001***

0
847

0
1

0
01**

0
519

0
113

0
279

0
331

*P < 0
05; **P < 0
01; ***P < 0
001.

Table 4 Total Cancer Behavioural Risk (TCBR): multiple linear regression analysis.
Unstandardized coefficients
B
(Constante)
Age
Time since cancer diagnosis
Secondary
University
Self-efficacy

SE

84
711
0
107
0
326
0
958
0
767
58
552

6
993
0
079
0
231
1
447
1
503
6
157

Standardized
coefficients
Beta

0
064
0
059
0
032
0
024
0
398

95% CI
t

Sig.

12
114
1
357
1
412
0
662
0
511
9
510

0
001
0
176
0
159
0
508
0
610
0
001***

Min
70
971
0
261
0
780
3
800
3
720
70
650

Max
98
450
0
048
0
128
1
885
2
186
46
455

***P < 0
001.

Dependent variable: Total Cancer Behavioural Risk (TCBR).
Independent variables: age (years), time since breast cancer diagnosis, level of education and self-efficacy.

2009). This finding does not seem to support the need to

develop programmes or interventions to reduce alcohol consumption among the general population of women with
breast cancer; however, it would seem appropriate to target
women reporting high-risk patterns of consumption.
2014 John Wiley & Sons Ltd

The percentage of women reporting engaging in less

physical activity than recommended (54
3%) was higher
than that of the Spanish (41
6%) (Instituto Nacional de Estad
stica. Ministerio de Sanidad, Pol
tica Social e Igualdad,
Madrid 2009) and Asturian female population (33
4%)
2815

M.O. Del Valle et al.

(Direcci

on General de Salud P

ublica. Consejer
a de Salud y
Servicios Sanitarios. Principado de Asturias 2012b). (Instituto Nacional de Estad
stica. Ministerio de Sanidad, Pol
tica
Social e Igualdad, Madrid 2009). It is noteworthy that
physical inactivity was more prevalent among women with
higher educational levels; this is in contrast with the general
population in Spain, where physical inactivity is associated
with lower education attainment (Instituto Nacional de Estad
stica. Ministerio de Sanidad, Pol
tica Social e Igualdad,
Madrid 2009).
A sedentary lifestyle accounts for up to 25% deaths by
breast cancer (Ott et al. 2011), which underlines its
importance and the need to adopt measures to reduce its
prevalence. Educational interventions for people with cancer, aimed at increasing moderate-intensity physical activity, e.g. walking at a fast pace, have shown important
health benefits, including improved quality of life (Spence
et al. 2010), decreased cancer mortality (Irwin et al. 2008)
and a decreased incidence of recurrences (Holmes et al.
2005).
Being overweight was more prevalent in women who
were recently diagnosed with cancer. This result may be
due to the short period of time since diagnosis, as weight
loss associated with disease progression, its complications
and treatment might not have yet occurred. An alternative
explanation may be that women have not yet adopted a
healthier lifestyle.
It is also noteworthy that overweight was significantly
higher among women with a lower level of education. This
finding is consistent with national data showing a higher
prevalence of overweight and obesity among women with
lower levels of education (Instituto Nacional de Estad
stica.
Ministerio de Sanidad, Pol
tica Social e Igualdad, Madrid
2009). According to the 2008 Principality of Asturias
Health Survey (Direcci

on General de Salud P

ublica. Consejer
a de Salud y Servicios Sanitarios. Principado de Asturias
2008), 53% of Asturian women have weight problems and
in the Health Survey for Spain, a 44
5% value was
recorded (Instituto Nacional de Estad
stica. Ministerio de
Sanidad, Pol
tica Social e Igualdad, Madrid 2009). Overweight and obese women accounted for 49% of the sample.
This rate is lower than that of Asturias but higher than that
of Spain and similar (Hellmann et al. 2010) or even lower
(Actis et al. 2009) than other rates in people diagnosed
with cancer. This finding does not preclude the possibility
of improvement, especially considering that a high BMI and
weight gain after a breast cancer diagnosis are associated
with the appearance of new primary tumours (TrenthamDietz et al. 2007, Li et al. 2009) and higher mortality
(Norman et al. 2007).
2816

The average intake of healthy foods was greater than that

of unhealthy foods in our patients. The referenced literature
shows that, following breast cancer diagnosis, there is a
tendency to increase the consumption of healthy foods,
such as fruit and vegetables and decrease the intake of
unhealthy foods (Skeie et al. 2009, Valentzis et al. 2011).
Given the influence of diet on the outcome of these patients
(McEligot et al. 2006, Pierce et al. 2007) and the effectiveness of diet-related interventions in breast cancer survivors
(Pierce et al. 2004, Alexander et al. 2010), it would be
desirable to improve or strengthen this behaviour in women
with breast cancer.
The percentage of women with high-risk sun exposure
behaviours was higher than that in other studies of women
with breast cancer (Coups & Stroff 2005) and lower than
that found in healthy populations (L

opez et al. 2007).
Although some studies point to the inverse association
between breast cancer mortality and sun exposure, based
on vitamin D synthesis (Grant 2007, Chen et al. 2010), evidence shows that risk exposure is related to the appearance
of malignant melanoma, the incidence of which is increasing in Spain, Europe and worldwide (de Vries & Coebergh
2005, Godar 2011) and other types of skin cancer (Stein &
Colditz 2004).
The average score for the synthetic TCBR indicator (21
6
points out of a maximum of 78) is similar, although slightly
lower than the score of healthy relatives of patients with
cancer (L

opez et al. 2007). The reason behind this coincidence might be the close relationship between both sample
groups with this illness, which would mean a greater
knowledge of risk factors and a higher percentage of
healthy behaviours. This means that a direct relationship
could be established between the proximity to this illness
and the control of risks associated with behaviours. The
fact that the TCBR score was higher in younger women
might be related to the higher rate of smokers in this age
group, as this behaviour is the one that contributes the
most to the total risk score. In any case, it is desirable to
continue reducing the TCBR, given the special characteristics of this population group, that have already shown their
vulnerability to cancer and are at risk of developing a
potential second primary cancer.
Self-efficacy rates among these women were very high in
all preventive behaviours. It is possible that women in our
sample were able to adopt and maintain healthy behaviours due to having suffered from cancer and having the
belief that some risk behaviours could have led to its development. Self-efficacy has proven to be one of the best predictors of healthy behaviours (L

opez et al. 2007, Werrij
et al. 2011). Self-efficacy favours the intention of carrying
2014 John Wiley & Sons Ltd

JAN: ORIGINAL RESEARCH

out healthy behaviours in a very important way (de Vries

et al. 1988) and minimizes the risk of defensive reactions
to health messages (L

opez et al. 2007, Alexander et al.
2010, Werrij et al. 2011). The multiple regression analysis
showed an inverse relationship between the TCBR variable
and self-efficacy; thus, women reporting higher levels of
self-efficacy had lower behavioural risks and conversely,
women reporting low levels of self-efficacy had higher
behavioural risks.
Health professionals may be unaware of the prevalence
of behavioural risk factors among people with cancer, as
it is often assumed that a cancer diagnosis will automatically trigger behavioural change in patients. The evidence
shows that this is not the case and population studies have
shown little difference in the prevalence of unhealthy
behaviours between cancer survivors and healthy populations (Bellizzi et al. 2005, Caan et al. 2005, Coups &
Stroff 2005).
Our results are of particular relevance for nursing staff.
Because of their close involvement with people with cancer,
nurses are ideally placed to assess unhealthy behaviours
among recently diagnosed cancer patients. Our results could
contribute towards designing tailored health promotion
programmes to decrease cancer risk behaviours in people
with cancer, especially in breast cancer patients, who have
high survival rates and as our results support high selfefficacy, the best predictor of success. Nurses should play a
pivotal role in implementing such programmes, given that
health education and the implementation of effective health
promotion programmes are core competencies of nursing
staff.
In many countries, professional nurses have undertaken
and undertake regularly health prevention and promotion
activities aimed at improving the quality of life of people
with cancer (Ganz et al. 2008), which obtain high satisfaction levels among their users (Lewis et al. 2009, Kimman
et al. 2010). In these studies, activities carried out by professional nurses, such as telephone follow-up of patients,
were found to be both effective, in terms of health outcomes (Cox & Wilson 2003, Beaver et al. 2010, Kimman
et al. 2011a), and cost-effective (Kimman et al. 2011b).

Behavioural risk factors among women with breast cancer

response rate. Therefore, we cannot rule out some interviewer and response bias. Finally, healthy participant bias
cannot be ruled out, as early death and slow disease progression may have resulted in a sample healthier than the
general population of women with breast cancer.

Conclusion
Our study showed the prevalence of some undesirable
health behaviours among women with breast cancer; however, it also showed a high level of self-efficacy among these
women. Our results should help cancer nurses and primary
care nurses develop and implement health promotion interventions aimed at decreasing the risk of developing new primary tumours among women with breast cancer.
These programmes should be based on instruments and
resources that have been shown to be effective and may
lead to a significant reduction in the risk of developing new
primary cancers. Given the relevance that some of the
behaviours described in this article can have in the disease
progression, it would seem appropriate to add TCBR prevention programmes promoting a healthy lifestyle that have
proven their effectiveness, specially focused on tobacco,
diet, weight and physical activity.
Further research to assess behavioural risk factors in
other populations of breast cancer survivors is warranted.
Further research is also warranted among patients diagnosed with other cancers with high survival rates. The efficacy of health promotion interventions among people with
cancer should also be investigated, as strategies that have
been found to be effective in healthy populations might not
be effective among people with cancer. Finally, further
research should be conducted to determine whether the
large-scale implementation of such preventive programmes
results in a decrease in the development of new primary
tumours in the long term.

Acknowledgements
The authors thank all participating women for their contribution.

Limitations

Funding

There were some limitations to the study. As previously

described in the Data Collection section, data were gathered by means of a telephone interview and was selfreported; thus, accuracy issues cannot be discounted. In
addition, extrapolating these results to the population of
women with breast cancer is also limited by the low

The research was funded by the University of Oviedo, Spain

(grant number UNOV-09-MB-7).

2014 John Wiley & Sons Ltd

Conflict of interest
No conflict of interest has been declared by the authors.
2817

M.O. Del Valle et al.

Author contributions
All authors have agreed on the final version and meet at
least one of the following criteria [recommended by the ICMJE (http://www.icmje.org/ethical_1author.html)]:

substantial contributions to conception and design,

acquisition of data, or analysis and interpretation of
data;
drafting the article or revising it critically for important
intellectual content.

References
Actis A.M., Bergoc R.M., Quartucci A. & Outomuro D. (2009)
Factores de riesgo convencionales y emergentes en c
ancer de
mama: un estudio en pacientes postmenop
ausicas. Revista
Chilena de Obstetricia y Ginecologa 74(3), 135142.
Alexander G.L., McClure J.B., Calvi J.H., Divine G.W., Stopponi
M.A., Rolnick S.J., Heimendinger J., Tolsma D.D., Resnicow K.,
Campbell M.K., Strecher V.J. & Johnson C.C. (2010) A
randomized clinical trial evaluationg online interventions to
improve fruit and vegetable consumption. American Journal of
Public Health 100(2), 319326.
Baan R., Straif K., Grosse Y., Secretan B., El Ghissassi F., Bouvard
V., Altieri A. & Cogliano V. (2007) Carcinogenicity of alcoholic
beverages. The Lancet Oncology 8(4), 292293.
Bandura A. (1995) Exercise of personal and collective efficacy in
changing societies. In Self-efficacy in Changing Societies (Bandura
A., ed.), Cambridge University Press, New York, pp. 145.
Beaver K., Williamson S. & Chalmers K. (2010) Telephone followup after treatment for breast cancer: views and experiences of
patients and specialist breast care nurses. Journal of Clinical
Nursing 19(1920), 29162924.
Bellizzi K.M., Rowland J.H., Jeffery D.D. & McNeel T. (2005)
Health behaviors of cancer survivors: examining opportunities
for cancer control intervention. Journal of Clinical Oncology 23
(34), 88848893.
Benson J.R., Jatoi I., Keisch M., Esteva F.J., Makris A. & Jordan V.C.
(2009) Early breast cancer. The Lancet 373(9673), 14631479.
Berrino F., De Angelis R., Sant M., Rosso S., Lasota M.B.,
Coebergh J.W., Santaquilani M. & the EUROCARE Working
Group (2007) Survival for eight major cancers and all cancers
combined for European adults diagnosed in 1995-1999: results
of the EUROCARE- 4 study. Lancet Oncology 8(12), 773783.
Boyle P., Autier P., Bartelink H., Baselga J., Boffetta P., Burn J.,
Burns H.J.G., Christensen L., Denis L., Dicato M., Diehl V.,
Doll R., Franceschi S., Gillis C.R., Gray N., Griciute L.,
Hackshaw A., Kasler M., Kogevinas M., Kvinnsland M., La
Vecchia C., Levi F., McVie J.G., Maisonneuve P., MartinMoreno J.M., Newton Bishop J., Oleari F., Perrin P., Quinn M.,
Richards M., Ringborg U., Scully C., Siracka E., Storm H.,
Tubiana M., Tursz T., Veronesi U., Wald N., Weber W., Zaridze
D.G., Zatonski W. & Zur Hausen H. (2003) European Code
against Cancer and scientific justification: third version. Annals
of Oncology 14(7), 9731005.

2818

Caan B., Sternfeld B., Gunderson E., Coates A., Quesenberry C. &
Slattery M.L. (2005) Life After Cancer Epidemiology (LACE)
Study: a cohort of early stage breast cancer survivors (United
States). Cancer Causes and Control 16(5), 545556.
Chen W., Clements M., Rahman B., Zhang S., Qiao Y. &
Armstrong B.K. (2010) Relationship between cancer mortality/
incidence and ambient ultraviolet B irradiance in China. Cancer
Causes and Control 21(10), 17011709.
Coleman M.P., Quaresma M., Berrino F., Lutz J.M., De Angelis
R., Capocaccia R., Baili P., Rachet B., Gatta G., Hakulinen T.,
Micheli A., Sant M., Weir H.K., Elwood J.M., Tsukuma H.,
Koifman S., Azevedo e Silva G., Francisci S., Santaquilani M.,
Verdecchia A., Storm H.H., Young J.L. & the CONCORD
Working Group (2008) Cancer survival in five continents: a
Worldwide population- based study (CONCORD). Lancet
Oncology 9(8), 730756.
Coups E.J. & Stroff J.S. (2005) A population-based estimate of the
prevalence of behavioural risk factors among adult cancer survivors
and noncancer controls. Preventive Medicine 40(6), 702711.
Cox K. & Wilson E. (2003) Follow-up for people with cancer:
nurse-led services and telephone interventions. Journal of
Advanced Nursing 43(1), 5161.
Danaei G., Hoorn S.V., Lopez A.D., Murray C.J.L. & Ezzati M.
(2005) Causes of cancer in the World: comparative risk
assessment of nine behavioural and environmental risk factors.
The Lancet 366(9499), 17841793.
Direcci

on General de Salud P

ublica. Consejer
a de Salud y Servicios
Sanitarios. Principado de Asturias (2008) II Encuesta de Salud
para Asturias, a~
no 2008. Retrieved from http://www.asturias.es/
Astursalud/Ficheros/AS_Salud%20Publica/As_Vigilancia/Encuesta
%20de%20Salud/esa-2008-informe-preliminar.pdf on 09 July
2013.
Direcci

on General de Salud P

ublica. Consejer
a de Salud y Servicios
Sanitarios. Principado de Asturias (2012a) Documento T
ecnico
del Observatorio de Salud en Asturias. Anexo de Indicadores
ampliados. Mortalidad y Morbilidad Asturias, 2012. Retrieved
from http://www.obsaludasturias.com/obsa/wp-content/uploads/
ANEXO-Indicadores-Ampliados-OBSA2012VD.pdf on 09 July
2013.
Direcci

on General de Salud P

ublica. Consejer
a de Salud y Servicios
Sanitarios. Principado de Asturias (2012b) Documento T
ecnico
del Observatorio de Salud en Asturias. Documento de
Indicadores ampliados. Asturias, 2012. Retrieved from http://
www.obsaludasturias.com/obsa/wp-content/uploads/
Doc-Indicadores-ampliado-2012-VD.pdf on 09 July 2013.
Doll R. & Peto R. (1981) The causes of cancer: quantitative
estimates avoidable risk of cancer in United States today. Journal
of the National Cancer Institute 66(6), 11911308.
Ferlay J., Steliarova-Foucher E., Lortet-Tieulent J., Rosso S.,
Coebergh J.W.W., Comber H., Forman D. & Bray F. (2013)
Cancer incidence and mortality patterns in Europe: estimates for 40
countries in 2012. European Journal of Cancer 49(6), 13741403.
Ganz P.A., Casillas J. & Hahn E.E. (2008) Ensuring quality care
for cancer survivors: implementing the survivorship care plan.
Seminars in Oncology Nursing 24(3), 208217.
Godar D.E. (2011) Worldwide increasing incidences of cutaneous
malignant melanoma. Journal of Skin Cancer 2011, ID 858425.
doi: 10.1155/2011/858425.

2014 John Wiley & Sons Ltd

JAN: ORIGINAL RESEARCH

Grant W.B. (2007) An ecologic study of cancer mortality rates in
Spain with respect to indices of solar UVB irradiance and
smoking. International Journal of Cancer 20(5), 11231128.
Hellmann S.S., Thygesen L.C., Tolstrup J.S. & Grnbk M.
(2010) Modifiable risk factors and survival in women
diagnosed with primary breast cancer: results from a
prospective cohort study. European Journal of Cancer
Prevention 19, 366373.
Holmes M.D., Chen W.Y., Feskanich D., Kroenke C.H. & Colditz
G.A. (2005) Physical activity and survival after breast cancer
diagnosis. JAMA 293(20), 24792486.
Instituto Nacional de Estad
stica. Ministerio de Sanidad, Pol
tica
Social e Igualdad, Madrid (2009) Encuesta Europea de salud en
Espa~
na 2009. Retrieved from http://www.msc.es/estadEstudios/
estadisticas/EncuestaEuropea/Principales_Resultados_Informe.pdf
on 09 July 2013.
Irwin M.L., Smith A.W., McTiernan A., Ballard-Barbash R.,
Cronin K., Gilliland F.D., Baumgartner R.N., Baumgartner K. &
Bernstein L. (2008) Influence of pre and post diagnosis physical
activity on mortality in breast cancer survivors. Journal of
Clinical Oncology 26(24), 39583964.
Jatoi I. & Mille A.B. (2003) Why is breast cancer mortality
declining? Lancet Oncology 4(4), 251254.
Kimman M.L., Bloebaum M.M.F., Dirksen C.D., Houben R.M.A.,
Lambin P. & Boersma L.J. (2010) Patient satisfaction with
nurse-led telephone follow-up after curative treatment for breast
cancer. BMC Cancer 10, 174. doi:10
1186/1471-2407-10-174.
Kimman M.L., Dirksen C.D., Voogd A.C., Falger P., Gijsen B.C.,
Thuring M., Lenssen A., van der Ent F., Verkeyn J., Haekens C.,
Hupperets C., Nuytinck J.K., van Riet Y., Brenninkmeijer S.J.,
Scheijmans L.J., Kessels A., Lambin P. & Boersma L.J. (2011a)
Nurse led-telephone follow-up and an educational group
programme after breast cancer treatment: results of a 2x2
randomised controlled trial. European Journal of Cancer 47(7),
10271036.
Kimman M.L., Dirksen C.D., Voogd A.C., Falger P., Gijsen B.C.,
Thuring M., Lenssen A., van der Ent F., Verkeyn J., Haekens C.,
Hupperets C., Nuytinck J.K., van Riet Y., Brenninkmeijer S.J.,
Scheijmans L.J., Kessels A., Lambin P. & Boersma L.J. (2011b)
Economic evaluation of a follow-up strategies after curative
treatment for breast cancer: results of an RCT. European Journal
of Cancer 47(8), 11751185.
Kumle M. (2008) Declining breast cancer incidence and decreased
HRT use. The Lancet 372(9639), 608610.
Lewis R., Neal R.D., Williams N.H., France B., Wilkinson C.,
Hendry M., Russell D., Russell I., Hughes D.A., Stuart N.S. &
Weller D. (2009) Nurse-led versus conventional physician-led
follow up for patients with cancer: systematic review. Journal of
Advanced Nursing 65(4), 706723.
Li C.I., Daling J.R., Porter P.L., Tang M.C. & Malone K.E. (2009)
Relationship between potentially modifiable lifestyle factors and
risk of second primary contralateral breast cancer among women
diagnosed with strogen receptor-positive invasive breast cancer.
Journal of Clinical Oncology 32(10), 53125318.
L

opez M.L., Comas A., Del Valle M.O., L

opez S., Garc
a J.B. &
Cueto-Espinar A. (2004) Psychosocial factors associated with
cancer behavioural risk in relatives of cancer patients. European
Journal of Cancer Prevention 13(2), 105111.

2014 John Wiley & Sons Ltd

Behavioural risk factors among women with breast cancer

L

opez M.L., Iglesias J.M., del Valle M.O., Comas A., Fern
andez
J.M., Lana A., Garc
a J.B., L

opez S., Cueto A. & FAPACAN
Working Group (2007) Impact of a primary care intervention on
smoking, drinking, diet, weight, sun exposure and work risk in
families with cancer experience. Cancer Causes and Control 18
(5), 525535.
L

opez M.L., Lana A., D
az S., Folgueras M.V., S
anchez L.,
Comendador M.A., Belyakova E., Rodr
guez J.M. & Cueto A.
(2009) Multiple primary cancer: an increasing health problem.
Strategies for prevention in cancer survivors. European Journal
of Cancer Care 18(6), 598605.
Malvezzi M., Bertuccio P., Levi F., La Vecchia C. & Negri E.
(2013) European cancer mortality predictions for the year 2013.
Annals of Oncology 24(3), 792800.
Mariotto A.B., Rowland J.H., Ries L.A.G., Scoppa S. & Feuer E.J.
(2007) Multiple cancer prevalence: a growing challenge in
long-term survivorship. Cancer Epidemiology, Biomarkers &
Prevention 16(3), 566571.
McEligot A.J., Largent J., Ziogas A., Peel D. & Anton-Culver H.
(2006) Dietary fat, fiber, vegetable and micronutrients are
associated with overall survival in postmenopausal women
diagnosed with breast cancer. Nutrition and Cancer 55(2), 132
140.
Morey M.C., Snyder D.C., Sloane R., Cohen H.J., Peterson B.,
Hartman T.J., Miller P., Mitchell T.C. & Demark-Wahnefried
W. (2009) Effects of home- based diet and exercise on functional
outcomes among older, overweight long- term survivors. JAMA
301(18), 18831891.
Norman S.A., Potashnik S.L., Galantino M.L., De Michele A.M.,
House L. & Localio A.R. (2007) Modificable risk factors for
breast cancer recurrence: what can we tell survivors? Journal of
Womens Health 16(2), 177191.
OECD (2012) Health at a Glance: Europe 2012. OECD
Publishing.
Retrieved
from
http://dx.doi.org/10
1787/
9789264183896-en on 09 July 2013.
Ott J.J., Ullrich A., Mascarenhas M. & Stevens G.A. (2011) Global
cancer incidence and mortality caused by behaviour and
infection. Journal of Public Health 33(2), 223233.
Physical Activity Guidelines Advisory Committee (2008) Physical
Activity Guidelines Advisory Committee Report, 2008. U.S.
Department of Health and Human Services, Washington, DC.
Pierce J.P., Newman V.A., Flatt S.W., Faerber S., Rock C.L.,
Natarajan L., Caan B.J., Gold E.B., Parker B.A., Hollenbach A.,
Wasserman L., Jones L.A., Ritenbaugh C., Stefacnick M.L.,
Thomson C.A. & Kealey S. (2004) Telephone counselling
intervention
increases
intakes
of
micronutrient
and
phytochemical-rich vegetables, fruit and fiber in breast cancer
survivors. The Journal of Nutrition 134(2), 452458.
Pierce J.P., Natarajan L., Caan B.J., Parker B.A., Greenberg B.R.,
Flatt S.W., Rock C.L., Kealey S., Al-Delaymi W.K., Bardwell
W.A., Carlson R.W., Edmon J.A., Faerber S., Gold E.B., Halek
R.A., Hollenbach A., Jones L.A., Karanja N., Madlensky L.,
Marshall J., Newman V.A., Ritenbaugh C., Thomson C.A.,
Wasserman L. & Stefacnick M.L. (2007) Influence of a diet very
high in vegetables, fruit and fiber and low in fat on prognosis
following treatment for breast cancer: the Womens Healthy
Eating and Living (WHEL) Randomized Trial. JAMA 298(3),
289298.

2819

M.O. Del Valle et al.

Raymond J.S. & Hogue C.J.R. (2006) Multiple primary tumours in
women following breast cancer, 1973-2000. British Journal of
Cancer 94, 17451750.
S

anchez L., Lana A., Hidalgo A., Rodr
guez J.M., Del Valle Mdel
O., Cueto A., Folgueras M.V., Belyakova E., Comendador M.A.
& L

opez M.L. (2008) Risk factors for second primary tumours
in breast cancer survivors. European Journal of Cancer
Prevention 17(5), 406413.
Skeie G., Hjartaker A., Braaten T. & Lund E. (2009) Dietary
change among breast and colorectal cancer survivor and cancer
free women in the Norwegian Women and cancer Cohort Study.
Cancer Causes and Control 20(10), 19551966.
Soerjomataram I., Louwman W.J., Lemmens V.E.P.P., de Vries E.,
Klokman W.J. & Coebergh J.W.W. (2005) Risk of second
primary breast and urogenital cancer following female breast
cancer in the south of The Netherlands, 1972-2001. European
Journal of Cancer 41(15), 23312337.
Spence R.R., Heesch K.C. & Brown W.J. (2010) Exercise and
cancer rehabilitation: a systematic review. Cancer Treatment
Reviews 36(2), 185194.
Stein C.J. & Colditz G.A. (2004) Modifiable risk factors for
cancer. British Journal of Cancer 90(2), 299303.
Trentham-Dietz A., Newcomb P.A., Nichols H.B. & Hampton
J.M. (2007) Breast cancer risk factors and second primary
malignancies among women with breast cancer. Breast Cancer
Research and Treatment 105(2), 195207.
Valentzis L.S., Keshtgar M.R., Woodside J.V., Leathem A.J.,
Titcomb A., Perkins K.A., Mazurowska M., Anderson V.,

Wardell K. & Cantwell M.M. (2011) Significant changes in

dietary intake and supplement use after breast cancer diagnosis
in a UK multicentre study. Breast Cancer Research and
Treatment 128(2), 473482.
de Vries E. & Coebergh J.W. (2005) Melanoma incidence has risen
in Europe. BMJ 331(7518), 698.
de Vries H., Dijkstra M. & Kuhlman P. (1988) Self-efficacy: the
third factor besides attitude and subjective norm as a predictor
of behavioral intentions. Health Education Research 3(3), 273
282.
Werrij M.Q., Ruiter R.A.C., Vant Riet J. & De Vries H. (2011)
Self-efficacy as a potential moderator of the effects of
framed health messages. Journal of Health Psychology 16(2),
199207.
WHO (2011a) Cancer, Fact Sheet 297. World Health Organization
Media Centre, Geneve. Retrieved from http://www.who.int/
mediacentre/factsheets/fs297/es/index.html on 09 July 2013.
WHO (2011b) Breast Cancer: Prevention and control. World
Health Organization Media Centre, Geneve. Retrieved from
http://www.who.int/cancer/detection/breastcancer/en/index1.html
on 09 July 2013.
WHO (2011c) 10 facts on obesity. World Health Organization
Media Centre, Geneve. Retrieved from http://www.who.int/
features/factfiles/obesity/facts/es/index.html on 09 July 2013.
Yu G.P., Schantz S.P., Neugut A.I. & Zhang Z.F. (2006)
Incidences and trends of second cancers in female breast cancer
patients: a fixed inception cohort-based analysis (United States).
Cancer Causes and Control 17(4), 411420.

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