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Sport activity and the risk of breast cancer: Results from a case - Control study

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Abstract

A case – control study of 257 women with breast cancer and 565 control women was conducted to investigate the effect of life-time sport activity on breast cancer risk. Information was collected by questionnaire about sports played, frequency of participation and duration. The activity levels were determined using frequency variable weighted for metabolic equivalents of energy expenditure (MET). Multivariate logistic regression analyses were used to compute odds ratios (ORs) and 95% confidence intervals (CIs). A full assessment of confounding and effect modification was undertaken. The odds ratios for increasing tertiles of sport activity were 1.00 (referent), 0.50 (CI: 0.33-0.76) and 0.44 (CI: 0.28-0.64), respectively (P-trend = 0.000). Comparing sport active women to inactive women the OR was 0.49 (CI: 0.35-0.69). Models stratified according to body mass index, age at menarche, age at first full term pregnancy, intake of vegetables and fruits, and experience of stress were examined. In models stratified the risks of breast cancer were also reduced with higher levels of activity in sport. The conclusion is that women who participated in sports have a reduced risk of breast cancer.
Biology of Sport, Vol. 20 No3, 2003
.
SPORT ACTIVITY AND THE RISK OF BREAST CANCER: RESULTS
FROM A CASE CONTROL STUDY
J.Kruk
Institute of Physical Education, Faculty of Natural Science, University of Szczecin,
Szczecin, Poland
Abstract. A case control study of 257 women with breast cancer and 565 control
women was conducted to investigate the effect of life-time sport activity on breast
cancer risk. Information was collected by questionnaire about sports played,
frequency of participation and duration. The activity levels were determined using
frequency variable weighted for metabolic equivalents of energy expenditure
(MET). Multivariate logistic regression analyses were used to compute odds ratios
(ORs) and 95% confidence intervals (CIs). A full assessment of confounding and
effect modification was undertaken. The odds ratios for increasing tertiles of sport
activity were 1.00 (referent), 0.50 (CI: 0.33-0.76) and 0.44 (CI: 0.28-0.64),
respectively (P-trend = 0.000). Comparing sport active women to inactive women
the OR was 0.49 (CI: 0.35-0.69). Models stratified according to body mass index,
age at menarche, age at first full term pregnancy, intake of vegetables and fruits,
and experience of stress were examined. In models stratified the risks of breast
cancer were also reduced with higher levels of activity in sport. The conclusion is
that women who participated in sports have a reduced risk of breast cancer.
(Biol.Sport 20:243-259, 2003)
Key words: Breast cancer Sport activity Case-control study
Introduction
Breast cancer is the most common female cancer in the world and remains the
leading cause of cancer death in women [28], but few protective means of
preventing the dease, such as lifestyle have been identified [5,21]. For this reason it
is important to examine effective lifestyle modifications of preventing the disease,
in particular that there is growing number of evidences in so far as increased
physical activity may protect against tumor of colon, rectum, lung, prostate, breast
and female reproductive tract [2,13,24,31].
Reprint request to: Dr Joanna Kruk, Institute of Physical Education, University of Szczecin.
Al. Piastów 40b/6, 71-065 Szczecin, Poland
Fax: +48-91-4442734, E-mail: Joanna.Kruk@univ.szczecin.pl
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The relationship between physical activity and breast cancer risk has been
pointed out by several studies [for review see e.g. 19,20]; the strength of the
relationship was found in range from 10% to 70% decrease among women with
high levels of physical activity [9,12,23,35,38]. Also a dose response relation (i.e.,
that the risk decrease is greater when the more activity is performed) was showed
in several studies that examined the trend. Not withstanding, in the subject
literature we also find increase risk associated with higher levels of physical
activity, e.g. three-fold increase in the risk among the most active women was
reported by Sternfeld et al. [34].
It is well known that prevention strategies are hampered by established risk
factors, such as: older age, early age at menarche (11 years), nulliparity and late
age at first birth (30 years), late age at natural menopause (55 years) and
mutations in genes BRCA 1 and BRCA 2 [17].
The hypothesis that physical activity can reduced the breast cancer risk finds
ground from the biological point of view, as the activity has been reported to
modulate reproductive hormone levels and menstrual status, helps maintain lower
body weight, and may also to augment the defence of the immune system against
tumor growth [13,24].
Due to the great need to reduce the breast cancer risk, and since participation in
sports and exercise seems to be promising for this purpose a case-control study was
conducted to examine wheather participation in sports alters cancer risk of breast
cancer. Since the association between physical activity and breast cancer is quite
complex, the study was also designed to adjust risk estimates for potential
confounders.
Material and Methods
Subjects: A case-control study on breast cancer was conducted between October
1997 and October 1998 in Stettin province. Cases were identified from the
Szczecin Regional Cancer Registry. Case subjects were women aged between 35-
88 years (median age, 55.011.3) after radical mastectomy diagnosed with
histologically confirmed incident invasive or in-situ breast cancer and operated in
the Szczecin hospitals during 1993-1998. Controls were women aged between 35-
93 years (median age, 52.212.2) admitted to the hospitals or clinics in the same
areas of case subjects. Control subjects were selected to have an age distribution
similar to that of the cases; were free of any cancer diagnosis. To increase
statistical power, controls were oversampled. The overall response among those
who were achievable and provide any information on sport activity were 54.7%
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(n=257) cases and 84.3% (n=565) controls. Reason for not obtaining filed
questionnaires for cases included: death and illness 15.3%, patient refusal 28.5%
and lost to follow-up or moved out of the area (1.5%).
Risk factor questionnaire: All study subjects were asked to complete a
structured questionnaire (developed and tested for reliability in a pilot study that
preceded the case-control study), including information on socio-demographic
characteristics, such as education, occupation and socio-economic indicators;
gynaecological factors related to the risk of breast cancer (age at menarche, age at
the birth of the first child and total number of full-term pregnancies);
anthropometric measures (weight and height); medications taken; diet including
vegetables and fruits intake, alcohol intake; experience of stress. The section on
sport activity included questions dealing with sports in which women currently
participated: basket-ball, hand-ball, volley-ball, athletics, water activities
(swimming, sailing, kayaking, rowing), tennis, orienteering, sport gymnastics,
running/jogging, skating, participation in a dance group, and conditioning
exercises. Information gathered included duration (the number of years spent in
sport activity) and the frequency (times per week or month). Women were asked to
choose one from several intervals of the number of years sport/training and the
number of times per week that the best described their activity.
To study a possible dose-response relationship between the sport activitity and
breast cancer risk women were categorized into tertiles of the activity in two
separate analyses. The first analyse was based on frequency variable that was
weighted for metabolic equivalents of energy expenditure (MET) for each activity.
Frequency variable, i.e. appropriate calculation of average number episodes
performed per month in earlier period of lifetime was calculated, using the
following formula: [(number of years training) x (number of reported times per
week sport/training category) x (52 weeks in a year)] / (10 years in time period x
12 months/year). Ten year time period of participation in sports was considered as
this was the longest period reported by women and corresponds lifetime period
during child/young adulthood. The above given formula is a simple modification of
that given by Friedenreich et al. [10] for calculations average participation for each
activity in a given age / time period.
Daily or 6 times a week training was assigned 7 episodes; 3-5 times-4 episodes
once or twice-2 episodes, and less than once a week 0.5 episode. Engage in sports
for 0.51 year was assigned 0.5; 13 years 2; 35 years 4; 57 6; 79 years
8, and above 9 years 10.
The frequency variable was weighted for MET score using Ainsworth et al.
Compedium of Physical Activities [1]. An MET score classifies specific types of
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activities as the ratio of metabolic rate to resting metabolic rate. Examples of
intensity codes used in calculation are: running (7.5 MET), swimming (6.0 MET),
tennis (6.08.0 MET), dancing (4.8 MET), aerobic (6.5 MET), hand-ball (8.0
MET), conditioning exercise (5.5 MET), kayaking (5.0 MET), athletics (6.6 MET)
(calculated by averaging the individual MET scores from the activities: running;
high jump, long jump; race walking; shot, discus, hammer throw). A total MET
score was calculated for various sports weighted by the duration of each activity.
For example, a womam active for 2 years in running (MET score of 7.5) and also
active for 4 years in aerobic (MET score of 6.5) has a weighted MET score of [(7.5
x 2) + (6.5 x 4)] / 6 = 6.8. The frequency variable weighted for MET for a woman
who reported participation in the sports twice a week in this period was calculated
as follows: [(6 yrs) x (2 times/wk) x (52 wk/yr)] / [(10 yrs in time period) x (12
mo/yr)] = 5.2 episodes/month over the entire 10-yrs period. A running for 2 years
and an aerobic for 4 years have a MET value of 6.8 METs, then (6.8 METs) x (5.2
episodes/month) = 35.4 MET-episodes/month of running and aerobic averaged
over the entire 10-yrs period.
The range of the calculated MET-weighted frequency variable among active
women (2-108 MET-episodes/month) was divided into three categories of about 35
MET-episodes/month, but clustering in the data did not allow to categorize women
basing on percentiles. Regarding the distribution of the data among examined
women the sport activity was divided into three levels: the first level inactive
(women reporting no past sport participation) they determine the reference
category; the second level low-moderate active (235 MET-episodes/month), and
the third level as high active (35 MET-episodes/month). A distribution of total
past training volume among women shows that about 70% of subjects were
categorized as inactive or low-moderate active; the classification is comparable
with that of other studies [22]. To check the reliability of the above described
method of the women categorization the second measure of the sport activity levels
was used. In this method high activity level is defined when frequency participation
in sports was more than 2 times per week, duration (number of years training) 5
years and intensity 5.5 MET, score. Low-moderate level of the activity was
defined when all data concerning the sport activity were other than in the case of
the high activity level. Inactive level includes women reporting no past sport
participation. This technique categorization has been used by other authors and
occurs to be reliable [12,39]. The discrepancy between the two applied method of
classification was less than 5%.
Information on sport activity in a later period of lifetime was also gathered but
was minimal and incomplete; these data were used as an additional confounder. It
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was found that addition of this variable to the logistic regression models did not
significantly alter the association between the various confounders and risk for
breast cancer.
Statistical analysis: Multivariate logistic regression models were used to obtain
maximum likelihood estimates of the odds ratios (ORs) and associated 95%
confidence intervals (CIs) [4] as well as to evaluate the effects of confounding and
modifying factors on the association of sport activity with breast cancer.The
variables considered as confounders included age, body mass index (BMI)
(weight/height2), educational level, age at menarche, age at first full-term
pregnancy, number of full-term pregnancies, use of hormone replacement therapy,
use of oral contraceptives, intake of vegetables and fruits, and experience of stress.
There was very little confounding of the past sport activity in these data so most
final analysis has been controlled for age (35-44, 45-54, 55-64, 64 years), age at
menarche (12, 13, 14 years), pregnancy (20, 20-24, 25-29, 30 years), BMI
(22, 22-24, 24 kg/m2), intake of vegetables and fruits (very rarely, rarely,
frequently), and experience of stress (yes/no). Statistical analyses were carried out
on a PC using statistical package STATISTICA 5.1 (’97 Polish edition). P values
for trend were generated using the ordered categorical variables presented in the
tables. All P values reported are two-sided, and P values less than 0.05 were
considered statistically significant. P values equal to 0.0000 were marked in tables
as P=0.
Results
Selected characteristics and breast cancer risk factors among 257 breast cancer
cases and 565 control subjects are shown in Table 1. In the study cases were
somewhat older than the controls except for women who were 35 to 44 years of
age. Age at menarche of 13 years or older was associated with a reduced breast
cancer risk, compared with women at age 12 years or younger. A much lower
proportion of cases (6.2%) than controls (23.9%) was lean (body mass index,
BMI 22 kg/m2). Higher BMI were associated with increased risk of breast cancer.
Cases reported more frequent experience of stress (OR=3.18, 95% CI: 2.30-4.41
for stress experience yes versus no). Women who reported intake of vegetables and
fruits frequently compared with reporting very rarely had a risk of breast cancer
that was 86% lower (OR=0.14, 95% CI: 0.04-0.48). There was little difference
between cases and controls with regard to marital status, education, alcohol
ingestion, hormone use (data not shown).
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Table 1
Distribution of 257 cases of breast cancer and 565 women controls according to
selected characteristics
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Table 2
Univariate and multivariate ORs (95% CIs) for breast cancer associated with
participation in sport activities
ORs odds ratios; CIs confidence intervals; *denotes reference category:
aAdjusted for current age;
bAdjusted for categories of current age, age at menarche, age at first term
pregnancy, Quetelet’s index,
intake of vegetables and fruits, and experience of stress
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Table 2 presents findings of the relation between sport activity and breast
cancer unadjusted, adjusted only for age (aORs), and multivariate controlling for
possible confounding factors (bORs), which were significantly important in the
logistic model. Compared with women inactive, the ORs of breast cancer for
women low-moderate and high active are 0.50 (95% CI: 0.35-0.76) and 0.44 (95%
CI: 0.28-0.64), respectively. The inverse trend in risk was significant (P=0.000).
The OR for active women versus inactive was 0.49 (95% CI: 0.35-0.69). The ORs
unadjusted and adjusted for age were similar to those of the multivariate analysis.
Breast cancer risk associated with sport activity was also examined within
tertiles of BMI (22, 22-24, 24 kg/m2) (Table 3). Regardless of the level of sport
activity, cases were generally heavier than controls. The decreased risk of the
breast cancer among women with high activity was stronger in women whose BMI
was 22-24 kg/m2 (OR=0.32, 95% CI: 0.15-0.68). Stratification by age at menarche
also revealed some differences. The strongest protective effect of the sport activity
was seen for women who began their periods at age 12 years or younger (Table 3),
(OR=0.23, 95% CI: 0.09-0.62) for high active versus inactive, and strong trends
with increasing activity levels were observed (trend P=0.000). The protective effect
of sport activity in the case of women who began their periods at age 14 years or
older was weaker; risk was reduced 28% for those who were high active. The
apparent protective effect of sport activity was significant for women with a first
childbirth at age 29 years and less but not for the small group of women with later
age (30 years). The interaction between age at first full term pregnancy and sport
activity was not significant (P=0.13, 2=9.89, 6 degrees of freedom).
When the data were stratified according to intake of vegetables and fruits, the
reduction in risk of breast cancer associated with sport activity was greater for
women declaring intake of these products very rarely and rarely than for women
declaring an intake frequently (Table 4). Furthermore, the protective effect of sport
activity appeared to be stronger among women who did not experience of stress
than in women with the stress experience. The interaction was highly statistically
significant (P=0.000), but two-sided significance probability for interaction
between sport activity and experience of stress did not reach statistical significance
(P=0.60, 2=1.01, 2 degrees of freedom).
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Table 3
Multivariate odds ratios for sport activity of cases and controls by body
mass index (BMI), age at menarche, and age at full pregnancy
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Table 4
Odds ratios for sport activity of cases and controls by intake of vegetables and
fruits, and experience of stress
OR, odds ratio; CI, confidence interval; N1, number of cases; N2, number of
controls; *denotes reference category. Estimated were derived from multiple
logistic regression equations including for aOR current age, age at menarche, age at
first full term pregnancy, Quetelet’s index, and experience of stress; for bOR the
multivariate models included the same variables as in case of aOR, but the
experience of stress variable was replaced by intake of vegetables and fruits. Two-
sided significance probabilities for interaction of intake of vegetables, fruits and
sport activity 2=51.7, 4 df, P=0.000; for interaction of stress 2=1.01, 2 df, P=0.60
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Discussion
The present results support the hypothesis that sport activity protects women
against breast cancer; for women who had ever been engaged in sport activity
compared with inactive, sport activity was associated with at least a 50% reduction
in their risk. This is consist with the findings of Frisch et al. [11], some of recently
reported data of Sesso et al. [30], and Wyshak and Frisch [38]. Wyshak and Frisch
confirmed their earlier findings that former college athletes had a significantly
lower risk of breast cancer than nonathletes. They found that the OR for the 15-
year incidence of breast cancer is 0.605 (95% CI: 0.438-0.835) among all women.
These authors conclude that “athletic activity during the college and pre-college
years is protective against breast cancer through the life span, and more markedly
among women under 45”.
The results reported here have biological plausibility; controls were leaner, had
later menarche; both factors are protective. Early menarche represents more years
of exposure to ovarian hormones. There is a considerable amount of evidence
suggesting that estrogens and progesterone play a main role in the development of
breast cancer [3,31]. Although physical activity exerts diverse physiologic effects
through which it could decrease breast cancer risk, the most frequently reported
hypothesis is that physical activity may lower the risk via hormonal mechanisms.
Many epidemiologic studies have found that physical activity can influence some
of factors related to endogenous hormonal profiles, such as age at menarche,
number of ovulatory menstrual cycles, and age at menopause [18].
If breast cancer is related to ovarian hormones the observed reduction breast
cancer risk with a sport activity may be mediated through a reduction in the total
number of ovulation during the life of a woman, therefore women physically active
probably have less exposure to estrogens than inactive women. This finds a
confirmation in the study of Pirke et al. [29] who reported lower estradiol and
progesterone levels in their late thens and early twenties among female athletes
with and without menstrual disturbances.
Physically active women of all ages are leaner than women more sedentary
[33]. It is worth noting that exercise may reduce fat stores a substrate for
transformation of androgens to estrogens [32]. Thune et al. [35] found that the
greatest reduction of the breast cancer associated with physical activity occurrs
among lean women of all ages. Thus, exercise reducing obesity may help maintain
the balance in hormone release, and may decrease the endogenous production of
estrogens in postmenopausal women, thereby protect women against breast cancer
[25,36].
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Subgroup analysis showed that the reduction in risk was greater for lean women
(BMI <22 kg/m2) than for women with a higher BMI only in the low-moderate
active group (shown in Table 3). A somewhat stronger inverse relation was also
seen among high active women who were of average BMI (22-24 kg/m2), however
independly on the BMI value high active and low-moderate active had lower risk
than those inactive women. This result is in agreement with the study by
Friedenreich et al. [9] and Moradi et al. [27] of lifetime leisure-time and
occupational activities. There is insufficient evidence as yet to reach a conclusion
on effect modification by BMI on the dose-response aspects of the relationship
between physical activity and breast cancer risk. This situation may be because in
some studies stronger reduction of risk for active women was observed for women
with low BMI [7,35], while other authors reported these risk decreases more
clearly for women whose BMI was high [8] or founding no effect modification of
the risk by BMI [6,30].
A higher risk for breast cancer among women with low-medium level of sport
activity than those with high level (Table 3) may be due to the validity of data
obtained from physical activity questionnaires which is satisfactory for high
intensity and sedentary women but worse for a low and moderate levels of activity
[16].
Now known previous investigations have reported any effect modification by
stress experience or intake of fruits and vegetables on the dependence between
sport activity and breast cancer, as was found in this paper. The study was
suggested by a new program of the International Agency for Research Cancer,
initiated about six years ago, aimed at evaluating a wide range of potential cancer
preventive agents and strategies. Prevention strategies of the Unit except for
immunological, chemical, and dietery embrace behavioural interventions that may,
among others, reduce exposure to underlying risk factors [37]. It was found that
sport activity was stronger protective for women having diet poor in fruits and
vegetables (Table 4). Several studies [15,26,29,31,37] indicated that diet rich in
fruits, vegetables, vegetable oil and/or vitamins having antioxidant properties, such
as -carotene and vitamin E may be protective against breast cancer.
The collected information on sport activity and a stress experience
simultaneously in relation to the risk of breast cancer revealed that the effect of
sport activity was more pronounced among women who reported that they had
never experienced of the strong stress.
In conclusion, this study confirms that sport activity appears to be associated
with a reduction in the breast cancer risk. A new findings from the study concerns
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the importance of sport activity in reduction of breast cancer also in the case of
women of which diet was poor in fruits and vegetables or experienced stress.
To explore the interrelationships between physical activity, life-style
behaviours, breast cancer factors and breast cancer risk epidemiological and
controlled, clinical metabolic studies are needed. Therefore, the present study
provides a useful contribution to a still open problem.
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... In a similar fashion, life-time sport-active adult women have a reduced incidence of breast cancer (>50% reduction) compared with age-matched nonactive women with stronger protective effects observed in those with earlier sport engagement and higher activity level. 46 In amateur/collegiate athletes with higher training volume and intensity, a lower rate of cancer risk has also been observed. An early large-scale survey 47 in 5398 female former collegiate athletes and nonathletes indicated that long-term participation in organized sport activities was associated with a reduced risk of not only breast cancer but also gynecologic cancers; while a 15-year follow-up 48 of these subjects also indicated that previous college sports experience conferred a life-time prophylactic effect against breast cancer. ...
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... Classification of the occupational activity was done according to total years of work. The sport and occupational physical activity categorization of the examined women has been described in detail previously [30,31]. ...
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Background/Methods: Although several studies have suggested that physical activity is associated with a decreased risk of breast cancer, such a decrease has not been found consistently, perhaps because physical activity was assessed in different ways and for restricted periods. Few studies have assessed the risk of breast cancer in relation to lifetime physical activity. We used data from a population-based, case-control study, including 918 case subjects (aged 20-54 years) and 918 age-matched population control subjects, to examine associations between breast cancer risk and physical activity at ages 10-12 years and 13-15 years, lifetime recreational activity, and title of longest held job. Results: Women who were more active than their peers at ages 10-12 years had a lower risk of breast cancer (odds ratio [OR] = 0.68; 95% confidence interval [CI] = 0.49-0.94). Women who had ever engaged in recreational physical activity had a reduced risk of breast cancer compared with inactive women (OR = 0.70; 95% CI = 0.56-0.88). Neither very early recreational activity (before age 20 years) nor recent activity (last 5 years) was associated with a greater reduction in risk than recreational activity in the intermediate period. Furthermore, women who started recreational activities after age 20 years and women who started earlier and continued their activities throughout adult life experienced a similar reduction in risk. Lean women, i.e., women with a body mass index (weight in kg/[height in m] 2 ) less than 21.8 kg/m 2 , appeared to have a lower risk associated with recreational physical activity than women with a body mass index greater than 24.5 kg/m 2 (OR = 0.57 [95% CI = 0.40-0.82] and OR = 0.92 [95% CI = 0.65-1.29], respectively). Conclusions: Our findings support the hypothesis that recreational physical activity is associated with a decreased risk of breast cancer. Physical activity in early or recent life does not appear to be associated with additional beneficial effects.
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Physical activity is associated with a reduced risk of all-cause and colonic cancers, and it seems to exert a weaker effect on the risk of breast, lung and reproductive tract tumours. This review examines possible mechanisms behind the observed associations. Restriction of physical activity by pre-existing disease may contribute to the association with lung cancers, but seems a less likely explanation for other types of tumour. Indirect associations through activity-related differences in body build or susceptibility to trauma seem of minor importance. Potential dietary influences include overall energy balance and energy expenditure, the intake and/or bioavailability of minerals, antioxidant vitamins and fibre, and the relative proportions of protein and fat ingested. Links between regular exercise and other facets of lifestyle that influence cancer risks are not very strong, although endurance athletes are not usually smokers, and regular leisure activity is associated with a high socioeconomic status which tends to reduce exposure to airborne carcinogens, both at work and at home. Overall susceptibility to cancer shows a ‘U’-shaped relationship to body mass index (mass/height2) reflecting, in part, the adverse influences of cigarette smoking and a tall body build for those with low body mass indices and, in part, the adverse effect of obesity at the opposite end of the body mass index distribution. Obesity seems a major component in the exercise-cancer relationship, with a particular influence on reproductive tract tumours; it alters the pathways of estradiol metabolism, decreases estradiol binding and facilitates the synthesis of estrogens. Among the hormonal influences on cancer risk, insulin-like growth factors promote tumour development and exercise-mediated increases in cortisol and prostaglandin levels may depress cellular components of immune function. However, the most important change is probably the suppression of the gonadotropic axis. Apparent gender differences in the benefits associated with regular exercise reflect gender differences in the hormonal milieu and also a failure to adapt activity questionnaires to traditional patterns of physical activity in females. The immune system is active at various stages of tumour initiation, growth and metastasis. However, acute and chronic changes in immune response induced by moderate exercise are rather small, and their practical importance remains debatable. At present, the oncologist is confronted by a plethora of interesting hypotheses, and further research is needed to decide which are of practical importance.