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The Oncologist, Vol. 8, No. 4, 326–334, August 2003
© 2003 AlphaMed Press

ORIGINAL PAPER
Breast Cancer

Behavioral Risk Factors in Breast Cancer: Can Risk Be Modified?

Anne McTiernan

Cancer Prevention Research Program, Fred Hutchinson Cancer Research Center, Seattle, Washington, USA; Department of Epidemiology, School of Public Health and Community Medicine and Department of Medicine, School of Medicine, University of Washington, Seattle, Washington, USA

Correspondence: Anne McTiernan, M.D., Ph.D., Cancer Prevention Research Program, Fred Hutchinson Cancer Research Center, P.O. Box 19024, MP-900, Seattle, Washington 98109-1024, USA. Telephone: 206-667-7979; Fax: 206-667-7850; amctiern{at}fhcrc.org


   ABSTRACT
Top
 Abstract
Introduction
 Physical Activity
 Weight Control
 Diet
 Alcohol Use
 Conclusions
 References
 
The International Agency for Research on Cancer estimates that 25% of breast cancer cases worldwide are due to overweight/obesity and a sedentary lifestyle. The preponderance of epidemiologic studies indicates that women who engage in 3–4 hours per week of moderate to vigorous levels of exercise have a 30%-40% lower risk for breast cancer than sedentary women. Women who are overweight or obese have a 50%-250% greater risk for postmenopausal breast cancer. Alcohol use, even at moderate levels (two drinks per day) increases risk for both premenopausal and postmenopausal breast cancer. Certain dietary patterns, such as high fat, low vegetables/fruits, low fiber, and high simple carbohydrates, may increase risk, but definitive data are lacking. These lifestyle factors are likely associated with breast cancer etiology through hormonal mechanisms. The worldwide trends of increasing overweight and obesity and decreasing physical activity may lead to an increasing incidence of breast cancer unless other means of risk reduction counteract these effects. Thus, adoption of lifestyle changes by individuals and populations may have a large impact on the future incidence of this disease.

Key Words. Breast cancer • Physical activity • Exercise • Obesity • Diet • Nutrition • Alcohol


   INTRODUCTION
Top
 Abstract
 Introduction
Physical Activity
 Weight Control
 Diet
 Alcohol Use
 Conclusions
 References
 
That lifestyle changes can change the risk of developing breast cancer is supported by several lines of evidence. First, rates of breast cancer incidence vary widely by geographic areas around the world. Only a small part of these differences is due to genetics, few chemical or other carcinogen exposures have been linked to risk, and the remainder of cases are, therefore, due to individual health and lifestyle behaviors [1]. Second, within-country changes over time in breast cancer incidence have been paralleled by great lifestyle and health behavior changes [2]. Third, experimental animal and human models provide confirmation of observable effects of several lifestyle behaviors on breast biology [1].

The International Agency for Research on Cancer estimates that 25% of breast cancer cases worldwide are due to overweight/obesity and a sedentary lifestyle [1]. An American Cancer Society cohort study of 495,477 women followed for 16 years found that the risk of breast cancer mortality increased significantly with increasing level of obesity; compared with women with a body mass index (BMI) under 25.0, those with BMIs of 25–29.9, 30–34.9, 35–39.9, and >=40 had relative risks (RR) of breast cancer mortality of 1.34, 1.63, 1.7, and 2.12, respectively [3]. Thus, lifestyle changes to correct these factors might be expected to have a major impact on public health.

Most breast cancer prevention strategies involve some amount of behavioral change. Tamoxifen therapy to prevent breast cancer [4], for example, involves a behavioral change on the part of the individual. The implementation of this prevention method, therefore, depends on the individual being willing to change her daily routine to include taking this medication. Similarly, compliance with recommended breast cancer screening guidelines involves adopting behaviors. Self-exam of the breast requires frequent monitoring behaviors; undergoing mammography and clinical breast exams involve making and keeping clinic appointments. While these and other prevention methods require a great deal of behavioral change, a discussion of all of these is beyond the scope of the present paper.

The purpose of this paper is to outline behavioral strategies that show promise in the prevention of breast cancer. It covers the following major lifestyle behaviors that are relevant to breast cancer etiology and control: physical activity, weight control, diet, and alcohol use. This paper, however, does not review the implementation of behavioral changes.


   PHYSICAL ACTIVITY
Top
 Abstract
 Introduction
 Physical Activity
Weight Control
 Diet
 Alcohol Use
 Conclusions
 References
 
There is a quickly growing body of epidemiologic data on the association between exercise and breast cancer, which was recently reviewed in depth by Thune and Furberg [5]. Over 20 published cohort studies [6–26] have investigated the association between physical activity and risk of breast cancer, the majority of which showed clear evidence of a lower risk for breast cancer in women who were classified at the highest levels of physical activity [7, 9, 10, 12, 13, 16, 18, 20, 21, 23–27]. The reduction in risk ranged from 10%-70% for the most active women and, on average, was 30%-40% lower for women who exercised for 3–4 hours per week at moderate to vigorous levels. The definition of "most active" varied greatly by study and depended on the questions asked, the population studied, and the researchers’ choice of categories for amounts of activity.

In a study of over 25,000 Norwegian women, trends toward lower risks for breast cancer with greater levels of leisure time physical activity (trend p = 0.08) and physical activity at work (trend p = 0.004) were observed [23]. There have been two reports from the Nurses’ Health Study cohorts: one looked at recreational activity reported at just one point in time [19] and one looked at repeated measures of activity at several time points during follow-up [20]. While the former found no association between physical activity and risk for breast cancer, the latter found that women who engaged in an average of 7 or more hours per week of physical activity had an 18% lower chance (95% confidence interval [CI] = 3%-30%) of developing breast cancer than women who engaged in less than 1 hour per week of such activities. Activity other than leisure was not assessed, and there may be a considerable effect of occupational activity in a population of nurses.

Some cohort studies compared women according to participation in college sports, some looked at occupational physical activity only, several examined recreational exercise only, and others studied both occupational and recreational physical activity. Methods of assessment of physical activity were unique to each study, ranging from simply asking subjects questions such as, "In your usual day, aside from recreation, how active are you?," to a physician-administered questionnaire that ascertained how many hours per day the participant usually spent sleeping, resting, sedentary, or at slight, moderate, or heavy activities, to detailed questions involving the participants’ historical and current levels of regular participation in various sports and other recreational exercise activities at different life periods.

More than two dozen case-control studies have been published on the association between physical activity and risk of breast cancer [5], more than three-quarters of which support a lower risk for breast cancer in women who were the most active compared with sedentary women. Reduction in risk ranged from 10%-70%.

Lower risks associated with greater physical activity have been observed for both premenopausal and postmenopausal breast cancer. Most studies have been conducted in non-Hispanic white women, although data from some studies suggest that physical activity is associated with a lower risk for breast cancer in women of diverse races and ethnicities [26, 28–31].

It is not clear at what ages physical activity provides the most protection against breast cancer. In a small number of case-control studies [32–34], lifetime leisure activity was ascertained, while in other studies, activity levels at adolescence and discrete adult periods were obtained. Some studies found a lower risk with greater activity in adolescence, while in other studies, risk reduction was limited to adult activities. D’Avanzo et al. found similar effects of occupational physical activity occurring at ages 15–19, 30–39, and 50–59 on risk of breast cancer, but found a stronger negative association between recreational exercise and risk at ages 30–39 and 50–59 than at ages 15–19 [35]. Levi et al. found that greater occupational activity at any time between adolescence and the sixth decade of life was associated with a lower risk [36]. McTiernan et al. found a lower risk associated with adult activity and no effect of activity in adolescence [37]. Friedenreich et al. found that, while greater lifetime activity gave the most benefit, exercise in postmenopausal years was protective [38]. Most studies, however, looked at activity at just one time point, usually either right before diagnosis (for cases) or in the adolescent/young adulthood period.

It is important in studying the association between physical activity and breast cancer to control for potentially confounding factors to be sure that the association between physical activity and breast cancer is not due to extraneous factors. For example, women who exercise may follow different diets than nonexercisers. If the dietary patterns are related to breast cancer risk, the association between physical activity and breast cancer may be spurious. Most studies controlled for potential confounding factors such as age, reproductive history, and BMI. Since body mass may lie in the causal pathway between physical activity and breast cancer risk, simple adjustment may not give a complete picture. Indeed, some investigators found that risk reduction was limited to the leanest women [23, 34, 39, 40]. Adjustment for dietary macronutrient intake or caloric intake did not confound the physical activity/breast cancer relationship in studies that assessed dietary data [12, 23, 29, 35–37, 41].

Elucidation of the causal pathway between physical activity and cancer risk will help in determining optimum ages to exercise, and the dose, frequency, and intensity of physical activities needed to protect against breast cancer.

Early menarche (before age 12), greater frequency of ovulatory cycles, late first birth or multiparity, lack of lactation, late menopause, greater number of lifetime ovulatory cycles, greater interval between menarche and menopause, and high concentrations of endogenous sex hormones have been found to lead to a greater risk of breast cancer of 20% to >400% [42, 43]. Several of these reproductive and hormonal factors are affected to some degree by physical activity.

In observational studies, girls participating in vigorous sports, such as ballet dancing and running, have been noted to experience high incidences of primary and secondary amenorrhea, delayed menarche, and more irregular cycles, than nonathletic girls [44, 45]. A cross-sectional study of 174 girls aged 14–17 years found that girls who expended 600 or more kilocalories of energy per week (described by the authors as comparable with >=2 hours per week in activities such as aerobic exercise classes, swimming, jogging, or tennis) were two to three times more likely than less active girls to have anovulatory menstrual cycles [46]. However, the time course for this association is not clear from the observational data—does physical activity cause anovulatory menstrual cycles or are girls who are not ovulating and therefore experiencing lower hormone levels more likely to engage in physical activity?

In small intervention studies, it has been shown that exercise during the reproductive period of life alters the concentrations of sex hormones [47, 48]. A high-intensity exercise intervention in 28 untrained college women with normal ovulation and luteal adequacy resulted in reversible abnormal luteal function in two-thirds and loss of the luteinizing hormone surge in over half the subjects [48]. The most marked disturbances were observed during the periods of most intense training and in those women who had been randomized to a weight loss (versus weight maintenance) group. It may well be, therefore, that a low body weight is also required to reduce ovulation. Thus, intense prolonged exercise or caloric restriction, or some combination of these, may be required.

Most postmenopausal women produce estrogen through the peripheral conversion (mainly in fat cells) of adrenal androgens to estrogens [49]. Greater physical activity measured through self-reports and by movement monitors has been found to be associated with lower serum concentrations of estradiol, estrone, and androgens in postmenopausal women [50–52] and with greater concentrations of sex-hormone-binding globulin [53]. One clinical trial has shown that a moderate exercise program reduced endogenous sex hormones in postmenopausal women [54, 55].


   WEIGHT CONTROL
Top
 Abstract
 Introduction
 Physical Activity
 Weight Control
Diet
 Alcohol Use
 Conclusions
 References
 
Over 100 studies have examined the associations between weight or BMI at different ages, central fat distribution, or adult weight gain and breast cancer incidence [1, 56]. Taken together, those studies found that women who were overweight or obese had a 30%-50% greater risk for postmenopausal breast cancer development than leaner women. In contrast, overweight and obesity are associated with a lower risk of breast cancer developing during the premenopausal years.

The Women’s Health Initiative (WHI) Observational Study is a multiethnic, multisite cohort study of women aged 50–79 at study entry [57]. Women underwent several clinic measures of adiposity when entering the cohort, including height, weight, and waist and hip circumference measurements, and reported their lifetime weight history. Analysis of these data showed that anthropometric factors were associated with breast cancer risk, but only among those women who had never used hormone replacement therapy [58]. Among these latter women, women with BMIs >=31.1 had a statistically significant 2.5 times greater risk of developing breast cancer than women whose BMIs were <=22.6. The Nurses’ Health Study also found that the 60% greater risk for postmenopausal breast cancer associated with overweight and obesity was limited to women who had never used hormone replacement therapy [59]. In another large cohort, heavier women with a family history of breast cancer had a greater risk of developing breast cancer than heavier women without a family history [60]. Results from case-control studies mirror those of cohort studies [56].

Adult Weight Gain
Adult weight gain has been quite consistently associated with a greater risk for postmenopausal breast cancer [58, 59, 61–68]. Findings from two of the largest cohort studies suggest that the doubling of risk associated with a gain in BMI from age 18 of >9.7 (WHI) or a weight gain >20 kg (Nurses’ Health Study) was limited to women who had never used postmenopausal hormone replacement therapy [58, 59]. In those studies, a 20% greater risk was observed for BMI gains of 3.5–6.2 (WHI) or weight gains of 2–20 kg (Nurses Health Study), although these gains were not statistically significant. Weight gain has also been found to be a consistent predictor of greater risk in case-control studies [56].

Central Adiposity
Greater central adiposity has been associated with an approximate doubling of breast cancer risk among postmenopausal women in cohort studies [58, 60, 61, 64, 69], independent of BMI. In the WHI study, a statistically significant trend of increasing breast cancer risk with increasing waist and hip circumferences, but not waist/hip ratio, was observed, although this finding was limited to women who had never used hormone replacement therapy [58]. Women in the highest quintile of either circumference measure had approximately double the risk of women in the lowest quintile. In the Nurses’ Health Study, RR for women in the highest versus lowest quintile of waist circumference was 1.2 among women overall and 1.9 among women who had never used postmenopausal hormone replacement therapy [59]. Data are less consistent for case-control studies, probably because of the difficulty with obtaining reliable measures of prediagnostic body circumferences after women are diagnosed with cancer.

Evidence on Effect of Intended Weight Control or Weight Loss
Data on the association between weight loss and breast cancer risk are limited. In three studies, weight loss occurring over a prolonged interval was associated with a nonsignificant slightly lower risk [61, 62, 70]. In another, weight loss in the decade before diagnosis was associated with a nonsignificant lower risk [68]. One study in premenopausal women found a statistically significant 36% lower risk with weight loss from age 20 to interview (age 20–44) that was present only among cases with low-grade tumors [71]. One study in postmenopausal women found a statistically significant 24% lower risk with weight loss from age 18 to interview (age 50–74) [66]. These data suggest that weight loss may be beneficial but are difficult to interpret as it is not possible to determine the cause of weight loss in existing studies.

The majority of the studies on weight and breast cancer risk have been done in European and North American populations. Nevertheless, the available data suggest that greater adiposity increases the risk for breast cancer across race and ethnic groups [2].

Mechanisms
There are several likely mechanisms linking adiposity to risk for breast cancer. After menopause, adipose tissue is the main site of estrogen production through aromatization of androgens to estrogens [49]. Overweight and obese postmenopausal women have higher concentrations of estrone, estradiol, and testosterone and lower concentrations of sex-hormone-binding globulin than leaner women [52]. Testosterone concentrations are greater in both premenopausal and postmenopausal overweight/obese women than in their leaner counterparts, perhaps due to greater conversion of androstenedione to testosterone in adipose tissue [72].

Insulin promotes cancer cell growth and, therefore, could explain part of the link between adiposity and breast cancer risk [73]. Exercise reduces insulin resistance and, therefore, the circulating concentration of insulin both acutely and chronically.

Insulin-like growth factors (IGFs) stimulate cell turnover in most body tissues and have been associated with a greater risk of breast cancer [74]. IGF is downregulated by increased production of its binding protein (IGFBP-1), which can result from a greater level of exercise, lower caloric intake, and lower body weight [75, 76]. Decreased IGF activity may increase the hepatic synthesis of sex-hormone-binding globulin, resulting in diminished availability of free sex hormone. Thus, greater levels of exercise could result in lower levels of biologically available endogenous sex hormones via a cascade of metabolic events, and thus, a lower risk of breast cancer.


   DIET
Top
 Abstract
 Introduction
 Physical Activity
 Weight Control
 Diet
Alcohol Use
 Conclusions
 References
 
The large international variations in risk for breast cancer prompted interest in possible dietary causes of breast cancer [77]. Several investigators examined particular international and intercultural dietary differences and proposed that diets that are low in fat and high in fruits, vegetables, fiber, and complex carbohydrates might lower risk for breast cancer [78, 79]. Although prospective observational studies in humans have generally not supported this, several experimental studies have provided support for an association between certain dietary patterns and a lower risk for breast cancer [80]. Animal experimental studies have shown a higher rate of development (via promotion of tumorigenesis) of mammary tumors with greater polyunsaturated or saturated fats intake [77]. However, it is not clear if the dietary fat per se, or the greater energy intake, was responsible for the greater development of mammary tumors in those studies.

Human experimental evidence is available on the effects of low-fat and high-fiber diets on some breast cancer biomarkers. The effect of a low-fat, high vegetable and fruit diet on mammographic density, a breast cancer biomarker, was tested in a randomized clinical trial in 817 women [81]. Women randomized to the diet arm experienced a 6.1% decrease in mammographic density over 2 years compared with a 2.1% decrease in controls (p = 0.01). Several small clinical trials and other interventional studies have shown a reduction in circulating estrogen levels, as described in a recent review [82], although there is still a question regarding whether it was the diet per se, or the weight loss resulting from the dietary changes, that caused the reduction in hormones [83].

Definitive evidence of the effect of a low-fat dietary pattern on risk of breast cancer awaits the results of the WHI Dietary Modification clinical trial [57]. The trial includes over 48,000 postmenopausal women aged 50–79 from diverse geographic, cultural, race, and ethnic groups around the U.S. The WHI dietary goal is 20% of calories from fat, five servings of fruits/vegetables per day, and six servings of grains per day. The trial was begun in 1993 and will continue until 2005.

While intake of dietary fat per se has not been established as associated with risk for breast cancer, increased dietary fat typically increases caloric intake. This results in overweight and obesity, which are risk factors for breast cancer. Therefore, prudent advice for women wanting to avoid lifetime weight gain, overweight, and obesity, would be to follow a diet that is low in dietary fat.

Vegetables and Fruits
Early epidemiologic studies suggested a role for a high intake of vegetables and fruits in a low risk for breast cancer [77]. A combined analysis of eight cohort studies representing 351,825 women (7,377 breast cancer cases), however, found no association between intake of vegetables and fruits and risk of breast cancer [84].

Soy, Isoflavones, and Lignans
Epidemiologic data suggest that consumption of soy products is associated with a lower risk for breast cancer [82, 85]. Many soy-based foods are available in the U.S., including tofu, soy milk, soy cheeses, frozen "yogurt," breakfast shakes, soy nuts, meat substitutes, and salad dressings [86]. Recent evidence suggests that one component of soy, genistein, may promote the growth of some estrogen-sensitive tumors and reduce the efficacy of tamoxifen, which emphasizes the need for additional studies to determine whether soy is safe for women with breast cancer or who are at a greater risk for breast cancer [87, 88].

Phytoestrogens can act as weak estrogens and as estrogen antagonists, depending on the hormonal milieu of the host. Thus, high phytoestrogen intake can compete with endogenous estrogens in premenopausal women and reduce overall estrogen exposure to target tissue. Conversely, phytoestrogens can increase estrogen activities in women with low endogenous levels of estrogens, for example, postmenopausal women. These findings have been confirmed in animal experiments and in a small number of human experimental studies [77, 89–91].

Meat and Dairy
Some studies have pointed to a high intake of meats as a risk factor for breast cancer, but other studies have not supported this [77]. Part of the discrepancy in findings may be the different levels of carcinogens and mutagens included in meat in different areas around the world.

Intake of dairy foods has not been found to be associated with risk for breast cancer, and a recent report from a large cohort study suggests a lower risk with a greater intake of low-fat dairy products in premenopausal women [92]. In that study, the multivariate RR comparing the >1 serving/day with the <=3 servings/month intake categories were 0.68 (95% CI = 0.55–0.86) for low-fat dairy foods and 0.72 (95% CI = 0.56–0.91) for skim/low-fat milk. Dairy calcium (>800 mg/day versus <=200 mg/day; RR = 0.69, 95% CI = 0.48–0.98) and vitamin D (>500 IU/day versus <=150 IU/day; RR = 0.72, 95% CI = 0.55–0.94) intakes were also inversely associated with premenopausal breast cancer risk [92]. The fat content of dairy products may promote a greater risk for breast cancer through a greater energy intake in the diet. On the other hand, the high calcium and vitamin D contents of many dairy products may be protective against breast cancer [92].

Vitamins and Minerals
Several epidemiologic studies have investigated the association between dietary and supplement intakes of various vitamins and minerals and the risk of breast cancer. Specific micronutrients that have been associated with a lower risk include carotenoids, folate, calcium, vitamin D, lycopene, and vitamin C [77, 93–95]. Those studies have had mixed results, however, and because they have all been observational, are not conclusive. New analyses of prospective studies suggest that women with low folate intakes and greater alcohol intakes have a greater risk for breast cancer than nondrinkers with normal folate intakes [96, 97]. In the Nurses’ Health Study cohort, among women who consumed at least 15 g/day of alcohol, the risk of breast cancer was highest among those with low folate intakes [97]. For a total folate intake of at least 600 µg/day compared with 150–299 µg/day, the multivariate RR was 0.55 (95% CI = 0.39–0.76; trend p = 0.001).


   ALCOHOL USE
Top
 Abstract
 Introduction
 Physical Activity
 Weight Control
 Diet
 Alcohol Use
Conclusions
 References
 
Several meta-analyses and major reviews of epidemiologic data confirm a moderate, but statistically significant, association between moderate to heavy alcohol intake and subsequent risk of developing breast cancer [77, 98]. There is evidence of a dose-response relationship, e.g., as little as one to two drinks per day can increase risk. One combined analysis of data from 53 studies around the world estimated that the RR for breast cancer increased 7% for each additional 10 g of alcohol consumed daily [99]. The association between alcohol intake and greater breast cancer risk has been observed regardless of the type of alcohol consumed, and alcohol intake has been shown to be associated with a higher risk for both premenopausal and postmenopausal breast cancer [98]. Alcohol consumption may be particularly deleterious for individuals with suboptimal intake of some nutrients such as folate, beta-carotene, lutein/zeaxanthin, and vitamin C [98].

Alcohol intake could increase risk of breast cancer through several mechanisms. Observational and clinical trial data show that premenopausal women, and postmenopausal women taking oral or transdermal hormone replacement therapy, have higher concentrations of circulating estrogens if they drink alcohol, compared with abstainers [52, 100, 101]. Animal data suggest that alcohol could act as a cocarcinogen by stimulating conversion of inactive to active metabolites that can bind to or damage DNA, by inhibiting carcinogen detoxification, or by impairing liver clearance of carcinogens [98]. Alcohol, and its metabolite acetaldehyde could also inhibit repair of carcinogen-induced DNA damage.


   CONCLUSIONS
Top
 Abstract
 Introduction
 Physical Activity
 Weight Control
 Diet
 Alcohol Use
 Conclusions
References
 
Observational data show strong evidence that greater adiposity, a sedentary lifestyle, and moderate to high levels of alcohol use are associated with a greater risk for breast cancer. The evidence for specific dietary components is less clear, but a major clinical trial (the WHI Dietary Modification trial) will give a more definitive answer regarding a low-fat dietary pattern effect on breast cancer incidence. Animal and human experimental studies provide evidence that there are plausible biological mechanisms linking these lifestyle factors to breast cancer initiation and promotion, largely through hormonal pathways. The worldwide trends to increasing overweight and obesity and decreasing physical activity may lead to an increasing incidence of breast cancer unless other means of risk reduction counteract these effects. Thus, the impact of a population-wide adoption of greater physical activity and improved energy balance would likely be large. For individual women, counseling should include recommendation to increase physical activity and balance energy such that weight remains stable over lifetime, and, preferably, with a BMI remaining below 25.0. For women who are already overweight or obese, recommendations for weight loss should include increasing physical activity (working up to 60 minutes per day [102]) and changing their dietary patterns to ones that are high in nutritious foods, for example, high in vegetables and fruits (at least five servings per day, preferably more) and high-fiber carbohydrates and low in fats, low-fiber carbohydrates, and alcoholic beverages (i.e., less than two drinks per day on average).


   REFERENCES
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 Abstract
 Introduction
 Physical Activity
 Weight Control
 Diet
 Alcohol Use
 Conclusions
 References
 

  1. IARC Working Group on the Evaluation of Cancer-Preventive Agents. Weight Control and Physical Activity, IARC Handbooks of Cancer Prevention, Volume 6. Lyon, France: IARC, 2002.
  2. McTiernan A. Associations between energy balance and body mass index and risk of breast carcinoma in women from diverse racial and ethnic backgrounds in the U.S. Cancer 2000;88(suppl 5):1248–1255.[CrossRef][Medline]
  3. Calle EE, Rodriguez C, Walker-Thurmond K et al. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N Engl J Med 2003;348:1625–1638.[Abstract/Free Full Text]
  4. Fisher B, Costantino JP, Wickerham DL et al. Tamoxifen for prevention of breast cancer: report of the National Surgical Adjuvant Breast and Bowel Project P-1 Study. J Natl Cancer Inst 1998;90:1371–1388.[Abstract/Free Full Text]
  5. Thune I, Furberg AS. Physical activity and cancer risk: dose-response and cancer, all sites and site-specific. Med Sci Sports Exerc 2001;33(suppl 6):S530–S550.[CrossRef][Medline]
  6. Albanes D, Blair A, Taylor PR. Physical activity and risk of cancer in the NHANES I population. Am J Public Health 1989;79:744–750.[Abstract/Free Full Text]
  7. Breslow RA, Ballard-Barbash R, Munoz K et al. Long-term recreational physical activity and breast cancer in the National Health and Nutrition Examination Survey I epidemiologic follow-up study. Cancer Epidemiol Biomarkers Prev 2001;10:805–808.[Abstract/Free Full Text]
  8. Calle EE, Murphy TK, Rodriguez C et al. Occupation and breast cancer mortality in a prospective cohort of US women. Am J Epidemiol 1998;148:191–197.[Abstract/Free Full Text]
  9. Cerhan JR, Chiu BCH, Wallace RB et al. Physical activity, physical function, and the risk of breast cancer in a prospective study among elderly women. J Gerontol 1998;53A:M251–M256.
  10. Dirx MJ, Voorrips LE, Goldbohm RA et al. Baseline recreational physical activity, history of sports participation, and postmenopausal breast carcinoma risk in the Netherlands Cohort Study. Cancer 2001;92:1638–1649.[CrossRef][Medline]
  11. Dorgan JF, Brown C, Barrett M et al. Physical activity and risk of breast cancer in the Framingham Heart Study. Am J Epidemiol 1994;139:662–669.[Abstract/Free Full Text]
  12. Fraser GE, Shavlik D. Risk factors, lifetime risk, and age at onset of breast cancer. Ann Epidemiol 1997;7:375–382.[CrossRef][Medline]
  13. Frisch RE, Wyshak G, Albright NL et al. Lower prevalence of breast cancer and cancers of the reproductive system among former college athletes compared to non-athletes. Br J Cancer 1985;52:885–891.[Medline]
  14. Luoto R, Latikka P, Pukkala E et al. The effect of physical activity on breast cancer risk: a cohort study of 30,548 women. Eur J Epidemiol 2000;16:973–980.[CrossRef][Medline]
  15. Moore DB, Folsom AR, Mink PJ et al. Physical activity and incidence of postmenopausal breast cancer. Epidemiology 2000;11:292–296.[CrossRef][Medline]
  16. Moradi T, Nyren O, Zack M et al. Breast cancer risk and lifetime leisure-time and occupational physical activity (Sweden). Cancer Causes Control 2000;11:523–531.[CrossRef][Medline]
  17. Paffenbarger RS Jr, Lee IM, Wing AL. The influence of physical activity on the incidence of site-specific cancers in college alumni. Adv Exp Med Biol 1992;322:7–15.[Medline]
  18. Pukkala E, Poskiparta M, Apter D et al. Life-long physical activity and cancer risk among Finnish female teachers. Eur J Cancer Prev 1993;2:369–376.[Medline]
  19. Rockhill B, Willett WC, Hunter DJ et al. Physical activity and breast cancer risk in a cohort of young women. J Natl Cancer Inst 1998;90:1155–1160.[Abstract/Free Full Text]
  20. Rockhill B, Willett WC, Hunter DJ et al. A prospective study of recreational physical activity and breast cancer risk. Arch Intern Med 1999;159:2290–2296.[Abstract/Free Full Text]
  21. Sesso HD, Paffenbarger RS Jr, Lee IM. Physical activity and breast cancer risk in the College Alumni Health Study (United States). Cancer Causes Control 1998;9:433–439.[CrossRef][Medline]
  22. Steenland K, Nowlin S, Palu S. Cancer incidence in the National Health and Nutrition Survey I. Follow-up data: diabetes, cholesterol, pulse and physical activity. Cancer Epidemiol Biomarkers Prev 1995;4:807–811.[Abstract]
  23. Thune I, Brenn T, Lund E et al. Physical activity and the risk of breast cancer. N Engl J Med 1997;336:1269–1275.[Abstract/Free Full Text]
  24. Vena JE, Graham S, Zielezny M et al. Occupational exercise and risk of cancer. Am J Clin Nutr 1987;45:318–327.[Free Full Text]
  25. Wyshak G, Frisch RE. Breast cancer among former college athletes compared to non-athletes: a 15-year follow-up. Br J Cancer 2000;82:726–730.[CrossRef][Medline]
  26. Zheng W, Shu XO, McLaughlin JK et al. Occupational physical activity and the incidence of cancer of the breast, corpus uteri, and ovary in Shanghai. Cancer 1993;71:3620–3624.[CrossRef][Medline]
  27. Lee IM, Cook NR, Rexrode KM et al. Lifetime physical activity and risk of breast cancer. Br J Cancer 2001;85:962–965.[CrossRef][Medline]
  28. Gilliland FD, Li YF, Baumgartner K et al. Physical activity and breast cancer risk in hispanic and non-hispanic white women. Am J Epidemiol 2001;154:442–450.[Abstract/Free Full Text]
  29. Hirose K, Tajima K, Hamajima N et al. A large-scale, hospital-based case-control study of risk factors of breast cancer according to menopausal status. Jpn J Cancer Res 1995;86:146–154.[CrossRef][Medline]
  30. Hu YH, Nagata C, Shimizu H et al. Association of body mass index, physical activity, and reproductive histories with breast cancer: a case-control study in Gifu, Japan. Breast Cancer Res Treat 1997;43:65–72.[CrossRef][Medline]
  31. Ueji M, Ueno E, Osei-Hyiaman D et al. Physical activity and the risk of breast cancer: a case-control study of Japanese women. J Epidemiol 1998;8:116–122.[Medline]
  32. Bernstein L, Henderson BE, Hanisch R et al. Physical exercise and reduced risk of breast cancer in young women. J Natl Cancer Inst 1994;86:1403–1408.[Abstract/Free Full Text]
  33. Friedenreich CM, Rohan TE. Physical activity and risk of breast cancer. Eur J Cancer Prev 1995;4:145–151.[Medline]
  34. Verloop J, Rookus MA, van der Kooy K et al. Physical activity and breast cancer risk in women aged 20–54 years. J Natl Cancer Inst 2000;92:128–135.[Abstract/Free Full Text]
  35. D’Avanzo B, Nanni O, La Vecchia C et al. Physical activity and breast cancer risk. Cancer Epidemiol Biomarkers Prev 1996;5:155–160.[Abstract/Free Full Text]
  36. Levi F, Pasche C, Lucchini F et al. Occupational and leisure time physical activity and the risk of breast cancer. Eur J Cancer 1999;35:775–778.
  37. McTiernan A, Stanford JL, Weiss NS et al. Occurrence of breast cancer in relation to recreational exercise in women age 50–64 years. Epidemiology 1996;7:598–604.[Medline]
  38. Friedenreich CM, Courneya KS, Bryant HE. Influence of physical activity in different age and life periods on the risk of breast cancer. Epidemiology 2001;12:604–612.[CrossRef][Medline]
  39. Coogan PF, Clapp RW, Newcomb PA et al. Variation in female breast cancer risk by occupation. Am J Ind Med 1996;30:430–437.[CrossRef][Medline]
  40. McTiernan A, Kooperberg C, White E et al. A prospective study of recreational physical activity and the risk of breast cancer in women aged 50–79 years: the Women’s Health Initiative Cohort Study. JAMA 2003 (in press).
  41. Mezzetti M, La Vecchia C, Decarli A et al. Population attributable risk for breast cancer: diet, nutrition, and physical exercise. J Natl Cancer Inst 1998;90:389–394.[Abstract/Free Full Text]
  42. Hulka BS. Epidemiology of susceptibility to breast cancer. Prog Clin Biol Res 1996;395:159–174.[Medline]
  43. The Endogenous Hormones and Breast Cancer Collaborative Group. Endogenous sex hormones and breast cancer in postmenopausal women: reanalysis of nine prospective studies. J Natl Cancer Inst 2002;94:606–616.[Abstract/Free Full Text]
  44. Frisch RE, Wyshak G, Vincent L. Delayed menarche and amenorrhea in ballet dancers. N Engl J Med 1980;303:17–19.[Medline]
  45. Frisch RE, Gotz-Welbergen AV, McArthur JW et al. Delayed menarche and amenorrhea of college athletes in relation to age of onset of training. JAMA 1981;246:1559–1563.[Abstract/Free Full Text]
  46. Bernstein L, Ross RK, Lobo RA et al. The effects of moderate physical activity on menstrual cycle patterns in adolescence: implications for breast cancer prevention. Br J Cancer 1987;55:681–685.[Medline]
  47. Bonen A, Ling WY, MacIntyre KP et al. Effects of exercise on the serum concentrations of FSH, LH, progesterone, and estradiol. Eur J Appl Physiol Occup Physiol 1979;42:15–23.[CrossRef][Medline]
  48. Bullen BA, Skrinar GS, Beitins IZ et al. Induction of menstrual disorders by strenuous exercise in untrained women. N Engl J Med 1985;312:1349–1353.[Abstract]
  49. Siiteri PK. Adipose tissue as a source of hormones. Am J Clin Nutr 1987;45(suppl 1):277–282.[Abstract/Free Full Text]
  50. Cauley JA, Gutai JP, Kuller LH et al. The epidemiology of serum sex hormones in postmenopausal women. Am J Epidemiol 1989;129:1120–1131.[Abstract/Free Full Text]
  51. Nelson ME, Meredith CN, Dawson-Hughes B et al. Hormone and bone mineral status in endurance-trained and sedentary postmenopausal women. J Clin Endocrinol Metab 1988;66:927–933.[Abstract/Free Full Text]
  52. Verkasalo PK, Thomas HV, Appleby PN et al. Circulating levels of sex hormones and their relation to risk factors for breast cancer: a cross-sectional study in 1092 pre- and postmenopausal women (United Kingdom). Cancer Causes Control 2001;12:47–59.[CrossRef][Medline]
  53. Newcomb PA, Klein R, Klein BE et al. Association of dietary and life-style factors with sex hormones in postmenopausal women. Epidemiology 1995;6:318–321.[Medline]
  54. McTiernan A, Ulrich CM, Yancey D et al. The Physical Activity for Total Health (PATH) Study: rationale and design. Med Sci Sports Exerc 1999;31:1307–1312.[Medline]
  55. McTiernan A, Irwin M, Ulrich C et al. Energy balance—an etiologic factor in human cancer: randomized trial of exercise effect on breast cancer biomarkers. Int J Cancer 2002;100(suppl 13):64a.
  56. Friedenreich CM. Review of anthropometric factors and breast cancer risk. Eur J Cancer Prev 2001;10:15–32.[CrossRef][Medline]
  57. Women’s Health Initiative Study Group. Design of the Women’s Health Initiative clinical trial and observational study. Control Clin Trials 1998;19:61–109.[CrossRef][Medline]
  58. Morimoto LM, White E, Chen Z et al. Obesity, body size, and risk of postmenopausal breast cancer: the Women’s Health Initiative (United States). Cancer Causes Control 2002;13:741–751.[CrossRef][Medline]
  59. Huang Z, Hankinson SE, Colditz GA et al. Dual effects of weight and weight gain on breast cancer risk. JAMA 1997;278:1407–1411.[Abstract/Free Full Text]
  60. Sellers TA, Kushi LH, Potter JD et al. Effect of family history, body-fat distribution, and reproductive factors on the risk of postmenopausal breast cancer. N Engl J Med 1992;326:1323–1329.[Abstract]
  61. Ballard-Barbash R, Schatzkin A, Taylor PR et al. Association of change in body mass with breast cancer. Cancer Res 1990;50:2152–2155.[Abstract/Free Full Text]
  62. Brinton LA, Swanson CA. Height and weight at various ages and risk of breast cancer. Ann Epidemiol 1992;2:597–609.[Medline]
  63. Enger SM, Ross RK, Paganini-Hill A et al. Body size, physical activity, and breast cancer hormone receptor status: results from two case-control studies. Cancer Epidemiol Biomarkers Prev 2000;9:681–687.[Abstract/Free Full Text]
  64. Folsom AR, Kaye SA, Prineas RJ et al. Increased incidence of carcinoma of the breast associated with abdominal adiposity in postmenopausal women. Am J Epidemiol 1990;131:794–803.[Abstract/Free Full Text]
  65. Lubin F, Ruder AM, Wax Y et al. Overweight and changes in weight throughout adult life in breast cancer etiology. A case-control study. Am J Epidemiol 1985;122:579–588.[Abstract/Free Full Text]
  66. Magnusson C, Baron J, Persson I et al. Body size in different periods of life and breast cancer risk in post-menopausal women. Int J Cancer 1998;76:29–34.[CrossRef][Medline]
  67. Radimer K, Siskind V, Bain C et al. Relation between anthropometric indicators and risk of breast cancer among Australian women. Am J Epidemiol 1993;138:77–89.[Abstract/Free Full Text]
  68. Ziegler RG, Hoover RN, Nomura AM et al. Relative weight, weight change, height, and breast cancer risk in Asian-American women. J Natl Cancer Inst 1996;88:650–660.[Abstract/Free Full Text]
  69. Kaaks R, Van Noord PA, Den Tonkelaar I et al. Breast-cancer incidence in relation to height, weight and body-fat distribution in the Dutch "DOM" cohort. Int J Cancer 1998;76:647–651.[CrossRef][Medline]
  70. Trentham-Dietz A, Newcomb PA, Storer BE et al. Body size and risk of breast cancer. Am J Epidemiol 1997;145:1011–1019.[Abstract/Free Full Text]
  71. Coates RJ, Uhler RJ, Hall HI et al. Risk of breast cancer in young women in relation to body size and weight gain in adolescence and early adulthood. Br J Cancer 1999;81:167–174.[CrossRef][Medline]
  72. Corbould AM, Judd SJ, Rodgers RJ. Expression of types 1, 2, and 3 17 beta-hydroxysteroid dehydrogenase in subcutaneous abdominal and intra-abdominal adipose tissue of women. J Clin Endocrinol Metab 1998;83:187–194.[Abstract/Free Full Text]
  73. McTiernan A, Ulrich C, Slate S et al. Physical activity and cancer etiology: associations and mechanisms. Cancer Causes Control 1998;9:487–509.[CrossRef][Medline]
  74. Hankinson SE, Willett WC, Colditz GA et al. Circulating concentrations of insulin-like growth factor-I and risk of breast cancer. Lancet 1998;351:1393–1396.[CrossRef][Medline]
  75. McCarty MF. Up-regulation of IGF binding protein-1 as an anticarcinogenic strategy: relevance to caloric restriction, exercise, and insulin sensitivity. Med Hypotheses 1997;48:297–308.[CrossRef][Medline]
  76. Schmitz KH, Ahmed RL, Yee D. Effects of a 9-month strength training intervention on insulin, insulin-like growth factor (IGF)-I, IGF-binding protein (IGFBP)-1, and IGFBP-3 in 30–50-year-old women. Cancer Epidemiol Biomarkers Prev 2002;11:1597–1604.[Abstract/Free Full Text]
  77. World Cancer Research Fund Panel (Potter JD Chair). Food, Nutrition and the Prevention of Cancer: a Global Perspective. Washington, DC: American Institute for Cancer Research, 1997.
  78. Marshall JR, Qu Y, Chen J et al. Additional ecological evidence: lipids and breast cancer mortality among women aged 55 and over in China. Eur J Cancer 1992;28A:1720–1727.[CrossRef]
  79. Prentice RL, Kakar F, Hursting S et al. Aspects of the rationale for the Women’s Health Trial. J Natl Cancer Inst 1988;80:802–814.[Abstract/Free Full Text]
  80. Welsch CW. Relationship between dietary fat and experimental mammary tumorigenesis: a review and critique. Cancer Res 1992;52(suppl 7):2040s–2048s.[Abstract/Free Full Text]
  81. Boyd NF, Greenberg C, Lockwood G et al. Effects at two years of a low-fat, high-carbohydrate diet on radiologic features of the breast: results from a randomized trial. Canadian Diet and Breast Cancer Prevention Study Group. J Natl Cancer Inst 1997;89:488–496.[Abstract/Free Full Text]
  82. Wu AH, Ziegler RG, Nomura AM et al. Soy intake and risk of breast cancer in Asians and Asian Americans. Am J Clin Nutr 1998;68(suppl 6):1437S–1443S.[Abstract]
  83. Holmes MD, Schisterman EF, Spiegelman D et al. Re: Meta-analysis: dietary fat intake, serum estrogen levels, and the risk of breast cancer. J Natl Cancer Inst 1999;91:1511–1512.[Free Full Text]
  84. Smith-Warner SA, Spiegelman D, Yaun SS et al. Intake of fruits and vegetables and risk of breast cancer: a pooled analysis of cohort studies. JAMA 2001;285:769–776.[Abstract/Free Full Text]
  85. Greenwald P. Cancer prevention clinical trials. J Clin Oncol 2002;20(suppl 18):14S–22S.
  86. Pillow PC, Duphorne CM, Chang S et al. Development of a database for assessing dietary phytoestrogen intake. Nutr Cancer 1999;33:3–19.[Medline]
  87. Jones JL, Daley BJ, Enderson BL et al. Genistein inhibits tamoxifen effects on cell proliferation and cell cycle arrest in T47D breast cancer cells. Am Surg 2002;68:575–577; discussion 577–578.[Medline]
  88. Ju YH, Doerge DR, Allred KF et al. Dietary genistein negates the inhibitory effect of tamoxifen on growth of estrogen-dependent human breast cancer (MCF-7) cells implanted in athymic mice. Cancer Res 2002;62:2474–2477.[Abstract/Free Full Text]
  89. Adlercreutz H, Hamalainen E, Gorbach S et al. Dietary phyto-oestrogens and the menopause in Japan. Lancet 1992;339:1233.[CrossRef][Medline]
  90. Adlercreutz CH, Goldin BR, Gorbach SL et al. Soybean phytoestrogen intake and cancer risk. J Nutr 1995;125(suppl 3):757S–770S.
  91. Cassidy A, Bingham S, Carlson J et al. Biological effects of plant oestrogens in premenopausal women. FASEB J 1993;7:A866.
  92. Shin MH, Holmes MD, Hankinson SE et al. Intake of dairy products, calcium, and vitamin d and risk of breast cancer. J Natl Cancer Inst 2002;94:1301–1311.[Abstract/Free Full Text]
  93. Dorgan JF, Sowell A, Swanson CA et al. Relationships of serum carotenoids, retinol, alpha-tocopherol, and selenium with breast cancer risk: results from a prospective study in Columbia, Missouri (United States). Cancer Causes Control 1998;9:89–97.[CrossRef][Medline]
  94. Hulten K, Van Kappel AL, Winkvist A et al. Carotenoids, alpha-tocopherols, and retinol in plasma and breast cancer risk in northern Sweden. Cancer Causes Control 2001;12:529–537.[CrossRef][Medline]
  95. Sato R, Helzlsouer KJ, Alberg AJ et al. Prospective study of carotenoids, tocopherols, and retinoid concentrations and the risk of breast cancer. Cancer Epidemiol Biomarkers Prev 2002;11:451–457.[Abstract/Free Full Text]
  96. Sellers TA, Vierkant RA, Cerhan JR et al. Interaction of dietary folate intake, alcohol, and risk of hormone receptor-defined breast cancer in a prospective study of postmenopausal women. Cancer Epidemiol Biomarkers Prev 2002;11:1104–1107.[Abstract/Free Full Text]
  97. Zhang S, Hunter DJ, Hankinson SE et al. A prospective study of folate intake and the risk of breast cancer. JAMA 1999;281:1632–1637.[Abstract/Free Full Text]
  98. Singletary KW, Gapstur SM. Alcohol and breast cancer: review of epidemiologic and experimental evidence and potential mechanisms. JAMA 2001;286:2143–2151.[Abstract/Free Full Text]
  99. Hamajima N, Hirose K, Tajima K et al. Alcohol, tobacco and breast cancer—collaborative reanalysis of individual data from 53 epidemiological studies, including 58,515 women with breast cancer and 95,067 women without the disease. Br J Cancer 2002;87:1234–1245.[CrossRef][Medline]
  100. Ginsburg ES, Walsh BW, Gao X et al. The effect of acute ethanol ingestion on estrogen levels in postmenopausal women using transdermal estradiol. J Soc Gynecol Investig 1995;2:26–29.[CrossRef][Medline]
  101. Ginsburg ES, Mello NK, Mendelson JH et al. Effects of alcohol ingestion on estrogens in postmenopausal women. JAMA 1996;276:1747–1751.[Abstract/Free Full Text]
  102. Trumbo P, Schlicker S, Yates AA et al. Dietary reference intakes for energy, carbohydrate, fiber, fat, fatty acids, cholesterol, protein and amino acids. J Am Diet Assoc 2002;102:1621–1630.[CrossRef][Medline]
Received February 5, 2003; accepted for publication May 13, 2003.




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