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Recreational Physical Activity and Risk of Postmenopausal Breast Cancer Based on Hormone Receptor Status
Aditya Bardia, MD, MPH;
Lynn C. Hartmann, MD;
Celine M. Vachon, PhD;
Robert A. Vierkant, MS;
Alice H. Wang, BS;
Janet E. Olson, PhD;
Thomas A. Sellers, PhD;
James R. Cerhan, MD, PhD
Arch Intern Med. 2006;166:2478-2483.
ABSTRACT
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Background Physical activity is a potentially modifiable breast cancer risk factor. There is considerable recent evidence to suggest that risk factors for breast cancer differ based on its subtype, particularly estrogen receptor (ER)/progesterone receptor (PR) status, but this has been less well studied for physical activity. The objective of this study was to examine the association of physical activity with breast cancer incidence based on ER/PR status of the tumor.
Methods The Iowa Women's Health Study is a prospective cohort study of 41 836 postmenopausal women. Recreational physical activity was self-reported on the baseline questionnaire, and 3 levels (high, medium, and low) were defined. Breast cancer incidence and ER/PR status, through 18 years of follow-up, were ascertained by linkage with the Iowa Surveillance, Epidemiology, and End Results Cancer Registry. Cox proportional hazards models were used to estimate multivariate relative risks (RRs) and 95% confidence intervals (CIs) of breast cancer, adjusting for other breast cancer risk factors.
Results During 554 819 person-years of follow-up, 2548 incident cases of breast cancer were observed. Compared with low physical activity, high physical activity levels were inversely associated with risk of breast cancer (RR, 0.86; 95% CI, 0.78-0.96), and there were inverse associations for ER-positive (ER+)/PR-positive (RR, 0.87; 95% CI, 0.75-1.00), ER+/PR-negative (PR–) (RR, 0.67; 95% CI, 0.47-0.96), and ER-negative/PR– (RR, 0.80; 95% CI, 0.56-1.14) tumors. Further adjustment for body mass index attenuated the overall association with breast cancer (RR, 0.91; 95% CI, 0.82-1.01) and for ER+/PR-positive tumors (RR, 0.94; 95% CI, 0.81-1.08), while there was no change for ER+/PR– tumors (RR, 0.66; 95% CI, 0.46-0.94).
Conclusions Higher recreational physical activity might reduce the risk of postmenopausal breast cancer overall. Risk reduction varies by ER/PR status of the tumor, being most marked for ER+/PR– tumors, which, in general, have been associated with a clinically more aggressive tumor phenotype. If confirmed in additional studies, these results would suggest that additional mechanisms, besides an effect on body mass, may account for observed protective effects of physical activity in reducing breast cancer.
INTRODUCTION
Breast cancer is the most common noncutaneous cancer and is the second leading cause of cancer-related death among women in the United States.1-2 The incidence of breast cancer is increasing worldwide, and this seems to be partially related to an increase in some lifestyle risk factors for breast cancer, including obesity.3-9
Physical activity is a potentially modifiable breast cancer risk factor. Increased physical activity has been associated with a decreased risk of breast cancer among premenopausal and postmenopausal women.10-25 However, a few studies have reported no benefit26-31 or an increased risk.32 It is suggested that breast cancer may be biologically heterogeneous and, therefore, risk factor associations may differ based on the tumor characteristics, including estrogen receptor (ER) and progesterone receptor (PR) status.5, 33-48 Recent studies have found that various well-established risk factors for breast cancer vary by the ER/PR profile of the tumor, including age,34 menopausal status,34, 37 parity,33, 38-40 age at menarche,38, 41 age at first pregnancy,34, 37, 39-40 hormonal use,33-34,42-44 family history,42, 45 body mass index (BMI),33-34,38, 42, 46 waist-hip ratio,47 alcohol consumption,35, 42, 48 dietary fat intake,49 and folate level.5, 48 However, only 2 recent case-control studies46, 50 and 1 cohort study16 have evaluated the association of physical activity with postmenopausal breast cancer incidence defined by joint ER/PR status, and the single cohort study was small (411 cases) and only reported results for ER-positive (ER+)/PR-positive (PR+) tumors.16
The Iowa Women's Health Study is a large prospective cohort of postmenopausal women. A nonsignificant inverse association of physical activity with breast cancer was previously reported after 10 years of follow-up (adjusted relative risk [RR], 0.97; 95% confidence interval [CI], 0.87-1.08).31 We present the updated results of this previous study after an additional 8 years of follow-up, along with results stratified by ER/PR status of the tumor.
METHODS
STUDY POPULATION
The Iowa Women's Health Study is a prospective cohort study of 41 836 women aged 55 to 69 years initiated in 1986, and details about characteristics of the cohort have been described previously.51-52 Briefly, a 16-page questionnaire was mailed to 99 826 randomly selected women and returned by 41 836 women (41.9% response rate), with follow-up questionnaires mailed in 1987, 1989, 1992, 1997, and 2002.
MEASUREMENT OF RISK FACTORS
Physical activity during "free time" was ascertained using 2 questions that assessed frequency ("rarely or never," "a few times a year," "a few times a month," "about once a week," "two to four times a week," or "more than four times a week") and type of physical activity in the form of moderate activity (such as bowling, golf, light sports, gardening, or taking long walks) and of vigorous activity (such as jogging, racket sports, swimming, aerobics, or strenuous sports). This level of moderate physical activity generally requires fewer than 6 metabolic equivalent (resting metabolic rate or metabolic equivalent of energy expenditure) hours per week, and vigorous physical activity generally requires 6 or more metabolic equivalent hours per week.53
Based on these questions, 3 levels of physical activity were derived. High physical activity was defined as participation in vigorous activity 2 or more times per week or moderate activity more than 4 times per week. Medium physical activity was defined as participation in vigorous activity once per week or moderate activity 1 to 4 times per week. Low physical activity composed the rest of the cohort. This physical activity index has been indirectly validated in the cohort by the observation that BMI and mean energy intake vary by level of physical activity, and higher physical activity is inversely associated with overall and cardiovascular disease–related mortality.54-55
COHORT FOLLOW-UP
Incident cases of breast cancer, including ER/PR status, were identified through 2003 using the Iowa Cancer Registry, a member of the National Cancer Institute's Surveillance, Epidemiology, and End Results program.2 Each year, registry cases and cohort members were matched against registry files on name, maiden name, ZIP code, birth date, and social security number. Deaths were identified through annual linkage to Iowa death certificates, supplemented by linkage to the National Death Index.
EXCLUSION
Women who at baseline were premenopausal (n = 569), had cancer other than skin cancer (n = 3830), had undergone a total or partial mastectomy (n = 1884), or did not have data about physical activity (n = 742) were excluded from the analysis, leaving 36 363 participants for this analysis (exclusions are not mutually exclusive).
STATISTICAL ANALYSIS
Follow-up for incident events was calculated as the time from completion of the baseline questionnaire until the date of breast cancer diagnosis, date of move from Iowa, or date of death. Cox proportional hazards regression analysis was used to estimate RRs and 95% CIs of the association of physical activity with breast cancer risk based on ER/PR tumor subtype, controlling for potential confounding factors as outlined in Table 1. Because one of the mechanisms by which physical activity is postulated to decrease breast cancer risk is through decreasing adiposity,56-58 we modeled the association with and without controlling for obesity (BMI and BMI at the age of 18 years). Incidence was modeled as a function of age, because age is a better predictor of breast cancer risk in this cohort than length of follow-up.59 Tests for trend were calculated using an ordinal variable for level of physical activity, and including it in the Cox proportional hazards model as a linear variable. In the receptor-specific analyses, events not of that specific cancer type were considered censored observations. Population-attributable risk estimates were calculated based on the coefficients generated by the Cox proportional hazards models and the distribution of physical activity in the cohort.60 Confidence intervals were generated using the bootstrap resampling method.61 All statistical tests were 2-sided, and all analyses were performed using SAS statistical software (SAS Institute Inc, Cary, NC) and Splus software (Insightful, Inc, Seattle, Wash).
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Table 1. Selected Demographic and Breast Cancer Risk Factors According to Level of Physical Activity at Study Baseline: Iowa Women's Health Study (1986)
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RESULTS
There were 36 363 postmenopausal women aged 55 to 69 years at baseline in the analytic data set, and 99.2% were white. Compared with women with a low physical activity index, women with a high physical activity index had a lower BMI. They were also slightly more likely to be higher educated, to have a later age at first live birth, to consume alcohol, and to not smoke (Table 1). All other risk factors showed negligible differences with level of physical activity.
During 554 819 person-years of follow-up, 2548 incident cases of breast cancer were observed in the postmenopausal cohort. The mean age at diagnosis of breast cancer was 71.4 years. Estrogen receptor/PR status was available for 73.0% of the cases and of those with receptor status available, most were ER+/PR+ (71.1%), followed by ER+/PR negative (PR–) (13.5%), ER negative (ER–)/PR– (13.1%), and ER–/PR+ (2.3%). The availability of ER or PR was related to stage (highest for local and regional cases and lowest for in situ), but, of those cases with ER or PR, the percentage positive did not vary strongly with stage (eg, 73.1% of in situ, 85.9% of local, 82.7% of regional, and 75.0% of distant cases were ER+).
Compared with women with low physical activity levels, women with high physical activity levels had a 14% decreased risk of breast cancer after adjusting for major breast cancer risk factors, with the exception of the BMI variables (Table 2). This inverse association was strongest for ER+ and PR– tumors, while there were weaker inverse associations for ER– and PR+ tumors. Cross classification by receptor status showed an inverse relationship of physical activity with each breast cancer subtype except ER–/PR+, which showed a statistically nonsignificant positive association (P=.56); the fewer cases in this subtype limits interpretation of this result. The strongest association was seen for ER+/PR– tumors.
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Table 2. Association of Physical Activity With Breast Cancer Incidence: Iowa Women's Health Study (1986-2003)
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Next, we further adjusted the RRs for BMI at study baseline (1986) and for BMI at the age of 18 years (Table 2). The inverse association of physical activity attenuated for breast cancer overall and for ER+, PR+, and ER+/PR+ tumors. In contrast, the results changed little for ER–, PR–, and ER+/PR– tumors. Further adjustment for waist-hip ratio did not alter these results (data not shown).
There were no significant interactions between previously reported common effect modifiers for breast cancer48, 62 (BMI [P=.10], waist-hip ratio [P=.43], family history of breast cancer [P=.87], and smoking [P=.37]) and physical activity on incidence of breast cancer, either overall or by ER/PR status (results not shown).
Population-attributable risks (given in percentages) were calculated to estimate the potential public health significance if physical activity levels were increased to the high level of the physical activity index. Multivariate-adjusted population-attributable risks (not including BMI and BMI at the age of 18 years) were 10.9 (95% CI, 3.9-18.0) for all breast cancer, 7.9 (95% CI, 0-17.0) for ER+/PR+ tumors, 28.4 (95% CI, 7.4-49.4) for ER+/PR– tumors, and 21.9 (95% CI, 0-42.7) for ER–/PR– tumors; the latter estimate included no effect because the RR estimate for ER–/PR– tumors was not statistically significant.
COMMENT
This is the first large prospective cohort study, to our knowledge, to comprehensively report the association of physical activity on incidence of breast cancer by ER/PR status among postmenopausal women. We found that higher recreational physical activity was associated with about 14% decreased risk of breast cancer. The inverse association seemed to vary by ER/PR status and was most marked among ER+/PR– tumors (33% lower risk). Adjustment for BMI attenuated associations for all breast cancer and for ER+/PR+ tumors, but not for ER+/PR– tumors.
The study findings of a 14% lower risk of breast cancer among the most physically active women is within the range reported by most case-control and cohort studies10-25 involving postmenopausal women. A recent report25 from the Women's Health Initiative Cohort Study involving 74 171 women reported a 14% lower risk of breast cancer for women engaged in regular strenuous physical activity at the age of 35 years (95% CI, 0.78-0.95) and an 8% lower risk for women engaged in regular physical activity at the age of 50 years (95% CI, 0.83-1.01). Similar results were found for ER+ tumors, but results for PR and the joint classification of ER/PR were not conducted. Lee et al16 also reported an inverse association of physical activity with breast cancer among postmenopausal women (RR, 0.67; 95% CI, 0.44-1.02) in the Women's Health Study cohort, and results were similar when restricted to ER+/PR+ tumors (RR, 0.76; 95% CI, 0.43-1.34); no data were reported for other subtypes because of the small sample size.
Two case-control studies46, 50 have provided results for joint ER/PR status among postmenopausal women. Similar to our results, Enger et al46 found that higher physical activity had a stronger effect in reducing ER+/PR– tumors (odds ratio, 0.43; 95% CI, 0.19-0.98) than ER+/PR+ tumors (odds ratio, 0.69; 95% CI, 0.42-1.13). Another case-control study63 found the effect of vigorous physical activity to be slightly stronger among ER+ tumors (odds ratio, 0.79; 95% CI, 0.68-0.93) than ER– tumors (odds ratio, 0.86; 95% CI, 0.70-1.05), but did not further cross classify the tumors. Two other case-control studies found little evidence for causative heterogeneity for the association of physical activity with ER/PR subtypes among premenopausal50, 64 or postmenopausal64 women.
Our ER/PR subtype results for physical activity parallel those for reductions in fat intake seen in the Women's Health Initiative, a randomized trial of 48 835 postmenopausal women. Women who reduced intake of total fat to 20% of energy had a markedly lower risk of ER+/PR– tumors (RR, 0.64; 95% CI, 0.49-0.84), but not ER+/PR+ tumors (RR, 0.97; 95% CI, 0.86-1.10).36 The ER+/PR– tumors seem to represent a more clinically aggressive phenotype.65 For example, ER+/PR– tumors are often larger,65 have a higher grade,65 have more resistance to selective ER modulators,66-68 and have a worse prognosis,65, 68-70 compared with ER+/PR+ tumors.
Physical activity decreases the endogenous production of estrogen by reducing adipose tissue, the major source of estrogens in postmenopausal women.56-58 Lowering estrogen levels could lead to decreased ER+/PR+ tumors, the opposite of which is seen in obesity, in which increased circulating estrogens are associated with increased ER+/PR+ tumors.33-34,38, 41-42,46 Consistent with this mechanism, the association of physical activity with ER+/PR+ tumors attenuated after adjustment for BMI. In contrast, there was no change in the association for ER+/PR– tumors after adjustment for BMI, suggesting that additional mechanisms are likely to be important for this subtype. Higher levels of certain growth factors, particularly epidermal growth factor receptor or human growth factor receptor 2, have been associated with ER+/PR– tumors.70 Physical activity seems to impact growth factor levels,57, 71-72 and this might in part explain the ER+/PR– results.
This study had a few limitations. First, physical activity was measured as a single self-reported assessment at baseline (1986), with no update during follow-up. Also, it did not include detailed aspects of physical activity, such as lifetime activity, seasonal patterns, or occupational activity, and we were not able to calculate metabolic equivalents. However, previous reports54-55 from the Iowa Women's Health Study cohort have indicated that this physical activity index is sensitive enough to identify major disease trends. Second, information about ER/PR status of breast cancer was obtained through multiple pathological laboratories, rather than a single reference laboratory. However, the ER/PR distribution in our study was similar to that reported by other studies.34, 73 Finally, most of the population in the study was white. However, physical activity has been shown to have a beneficial effect on breast cancer among other races.63
In summary, higher physical activity was associated with about a 14% decreased risk of postmenopausal breast cancer. The inverse association was most marked for ER+ tumors, particularly ER+/PR– tumors; the latter, in general, have been associated with a more aggressive phenotype. The results also suggest that additional mechanisms, besides an effect on body mass, may account for observed effects of physical activity for this subtype. Further studies are needed to confirm these novel findings, and to evaluate similar relationships among premenopausal women. If found to be causally related to breast cancer, physical activity would have a substantial public health effect on the prevention of this disease, along with its other positive health benefits.74
AUTHOR INFORMATION
Correspondence: James R. Cerhan, MD, PhD, Department of Health Sciences Research, Mayo Clinic College of Medicine, 200 First St SW, Rochester, MN 55905 (cerhan.james{at}mayo.edu).
Accepted for Publication: September 1, 2006.
Author Contributions: Dr Cerhan had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Bardia, Sellers, and Cerhan. Acquisition of data: Bardia, Sellers, and Cerhan. Analysis and interpretation of data: Bardia, Hartmann, Vachon, Vierkant, Wang, Olson, and Cerhan. Drafting of the manuscript: Bardia, Vachon, Vierkant, and Cerhan. Critical revision of the manuscript for important intellectual content: Bardia, Hartmann, Vierkant, Wang, Olson, Sellers, and Cerhan. Statistical analysis: Vierkant, Wang, and Cerhan. Obtained funding: Sellers and Cerhan. Administrative, technical, and material support: Olson and Cerhan. Study supervision: Hartmann and Cerhan.
Financial Disclosure: None reported.
Funding/Support: This study was supported in part by grant R01 CA39742 from the National Cancer Institute.
Role of the Sponsor: The funding body had no role in data extraction and analyses, in the writing of the manuscript, or in the decision to submit the manuscript for publication.
Previous Presentation: This study was presented in part at the American Society of Clinical Oncology meeting; June 5, 2006; Atlanta, Ga.
Author Affiliations: Departments of Internal Medicine (Dr Bardia), Medical Oncology (Dr Hartmann), and Health Sciences Research (Drs Vachon, Olson, and Cerhan, Mr Vierkant, and Ms Wang), Mayo Clinic College of Medicine, Rochester, Minn; and Division of Cancer Prevention and Control, H. Lee Moffitt Cancer Center and Research Institute, Tampa, Fla (Dr Sellers).
REFERENCES
| |
1. Jemal A, Siegel R, Ward E, et al. Cancer statistics, 2006. CA Cancer J Clin. 2006;56:106-130.
FREE FULL TEXT
2. Ries LA, Eisner MN, Kosary CL, et al. SEER cancer statistics review, 1975-2002. http://seer.cancer.gov/csr/1975_2002. Accessed July 5, 2006.3. Edwards BK, Brown ML, Wingo PA, et al. Annual report to the nation on the status of cancer, 1975-2002, featuring population-based trends in cancer treatment. J Natl Cancer Inst. 2005;97:1407-1427.
FREE FULL TEXT
4. Smith-Warner SA, Spiegelman D, Yaun SS, et al. Alcohol and breast cancer in women: a pooled analysis of cohort studies. JAMA. 1998;279:535-540.
FREE FULL TEXT
5. Zhang SM, Hankinson SE, Hunter DJ, Giovannucci EL, Colditz GA, Willett WC. Folate intake and risk of breast cancer characterized by hormone receptor status. Cancer Epidemiol Biomarkers Prev. 2005;14:2004-2008.
FREE FULL TEXT
6. Fung TT, Hu FB, Holmes MD, et al. Dietary patterns and the risk of postmenopausal breast cancer. Int J Cancer. 2005;116:116-121.
FULL TEXT
|
ISI
| PUBMED
7. Cho E, Spiegelman D, Hunter DJ, et al. Premenopausal fat intake and risk of breast cancer. J Natl Cancer Inst. 2003;95:1079-1085.
FREE FULL TEXT
8. Huang Z, Hankinson SE, Colditz GA, et al. Dual effects of weight and weight gain on breast cancer risk. JAMA. 1997;278:1407-1411.
FREE FULL TEXT
9. Egan KM, Stampfer MJ, Hunter D, et al. Active and passive smoking in breast cancer: prospective results from the Nurses' Health Study. Epidemiology. 2002;13:138-145.
FULL TEXT
|
ISI
| PUBMED
10. 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.
FREE FULL TEXT
11. Coogan PF, Newcomb PA, Clapp RW, Trentham-Dietz A, Baron JA, Longnecker MP. Physical activity in usual occupation and risk of breast cancer (United States). Cancer Causes Control. 1997;8:626-631.
FULL TEXT
|
ISI
| PUBMED
12. D’Avanzo B, Nanni O, La Vecchia C, et al. Physical activity and breast cancer risk. Cancer Epidemiol Biomarkers Prev. 1996;5:155-160.
FREE FULL TEXT
13. Fraser GE, Shavlik D. Risk factors, lifetime risk, and age at onset of breast cancer. Ann Epidemiol. 1997;7:375-382.
FULL TEXT
|
ISI
| PUBMED
14. Friedenreich CM, Rohan TE. Physical activity and risk of breast cancer. Eur J Cancer Prev. 1995;4:145-151.
ISI
| PUBMED
15. Frisch RE, Wyshak G, Albright NL, et al. Lower lifetime occurrence of breast cancer and cancers of the reproductive system among former college athletes. Am J Clin Nutr. 1987;45(suppl):328-335.
FREE FULL TEXT
16. Lee IM, Rexrode KM, Cook NR, Hennekens CH, Burin JE. Physical activity and breast cancer risk: the Women's Health Study (United States). Cancer Causes Control. 2001;12:137-145.
FULL TEXT
|
ISI
| PUBMED
17. Marcus PM, Newman B, Moorman PG, et al. Physical activity at age 12 and adult breast cancer risk (United States). Cancer Causes Control. 1999;10:293-302.
FULL TEXT
|
ISI
| PUBMED
18. McTiernan A, Stanford JL, Weiss NS, Daling JR, Voigt LF. Occurrence of breast cancer in relation to recreational exercise in women age 50-64 years. Epidemiology. 1996;7:598-604.
ISI
| PUBMED
19. Mittendorf R, Longnecker MP, Newcomb PA, et al. Strenuous physical activity in young adulthood and risk of breast cancer (United States). Cancer Causes Control. 1995;6:347-353.
FULL TEXT
|
ISI
| PUBMED
20. 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.
FULL TEXT
|
ISI
| PUBMED
21. Thune I, Brenn T, Lund E, Gaard M. Physical activity and the risk of breast cancer. N Engl J Med. 1997;336:1269-1275.
FREE FULL TEXT
22. Ueji M, Ueno E, Osei-Hyiaman D, Takahashi H, Kano K. Physical activity and the risk of breast cancer: a case-control study of Japanese women. J Epidemiol. 1998;8:116-122.
PUBMED
23. Vena JE, Graham S, Zielezny M, Brasure J, Swanson MK. Occupational exercise and risk of cancer. Am J Clin Nutr. 1987;45(suppl):318-327.
FREE FULL TEXT
24. Zheng W, Shu XO, McLaughlin JK, Chow WH, Gao YT, Blot WJ. Occupational physical activity and the incidence of cancer of the breast, corpus uteri, and ovary in Shanghai. Cancer. 1993;71:3620-3624.
FULL TEXT
|
ISI
| PUBMED
25. McTiernan A, Kooperberg C, White E, et al, Women's Health Initiative Cohort Study. Recreational physical activity and the risk of breast cancer in postmenopausal women: the Women's Health Initiative Cohort Study. JAMA. 2003;290:1331-1336.
FREE FULL TEXT
26. Dosemeci M, Hayes RB, Vetter R, et al. Occupational physical activity, socioeconomic status, and risks of 15 cancer sites in Turkey. Cancer Causes Control. 1993;4:313-321.
FULL TEXT
|
ISI
| PUBMED
27. Hu YH, Nagata C, Shimizu H, Kaneda N, Kashiki Y. 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.
FULL TEXT
|
ISI
| PUBMED
28. Paffenbarger RS Jr, Hyde RT, Wing AL. Physical activity and incidence of cancer in diverse populations: a preliminary report. Am J Clin Nutr. 1987;45(suppl):312-317.
FREE FULL TEXT
29. Pukkala E, Poskiparta M, Apter D, Vihko V. Life-long physical activity and cancer risk among Finnish female teachers. Eur J Cancer Prev. 1993;2:369-376.
PUBMED
30. Taioli E, Barone J, Wynder EL. A case-control study on breast cancer and body mass: the American Health Foundation–Division of Epidemiology. Eur J Cancer. 1995;31A:723-728.31. Moore DB, Folsom AR, Mink PJ, Hong CP, Anderson KE, Kushi LH. Physical activity and incidence of postmenopausal breast cancer. Epidemiology. 2000;11:292-296.
FULL TEXT
|
ISI
| PUBMED
32. 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.
FREE FULL TEXT
33. Potter JD, Cerhan JR, Sellers TA, et al. Progesterone and estrogen receptors and mammary neoplasia in the Iowa Women's Health Study: how many kinds of breast cancer are there? Cancer Epidemiol Biomarkers Prev. 1995;4:319-326.
ABSTRACT
34. Colditz GA, Rosner BA, Chen WY, Holmes MD, Hankinson SE. Risk factors for breast cancer according to estrogen and progesterone receptor status. J Natl Cancer Inst. 2004;96:218-228.
FREE FULL TEXT
35. Suzuki R, Ye W, Rylander-Rudqvist T, Saji S, Colditz GA, Wolk A. Alcohol and postmenopausal breast cancer risk defined by estrogen and progesterone receptor status: a prospective cohort study. J Natl Cancer Inst. 2005;97:1601-1608.
FREE FULL TEXT
36. Prentice RL, Caan B, Chlebowski RT, et al. Low-fat dietary pattern and risk of invasive breast cancer: the Women's Health Initiative Randomized Controlled Dietary Modification Trial. JAMA. 2006;295:629-642.
FREE FULL TEXT
37. Rusiecki JA, Holford TR, Zahm SH, Zheng T. Breast cancer risk factors according to joint estrogen receptor and progesterone receptor status. Cancer Detect Prev. 2005;29:419-426.
FULL TEXT
|
ISI
| PUBMED
38. Huang WY, Newman B, Millikan RC, Schell MJ, Hulka BS, Moorman PG. Hormone-related factors and risk of breast cancer in relation to estrogen receptor and progesterone receptor status. Am J Epidemiol. 2000;151:703-714.
FREE FULL TEXT
39. Ursin G, Bernstein L, Lord SJ, et al. Reproductive factors and subtypes of breast cancer defined by hormone receptor and histology. Br J Cancer. 2005;93:364-371.
FULL TEXT
|
ISI
| PUBMED
40. Nichols HB, Trentham-Dietz A, Love RR, et al. Differences in breast cancer risk factors by tumor marker subtypes among premenopausal Vietnamese and Chinese women. Cancer Epidemiol Biomarkers Prev. 2005;14:41-47.
FREE FULL TEXT
41. Cotterchio M, Kreiger N, Theis B, Sloan M, Bahl S. Hormonal factors and the risk of breast cancer according to estrogen- and progesterone-receptor subgroup. Cancer Epidemiol Biomarkers Prev. 2003;12:1053-1060.
FREE FULL TEXT
42. Gapstur SM, Potter JD, Drinkard C, Folsom AR. Synergistic effect between alcohol and estrogen replacement therapy on risk of breast cancer differs by estrogen/progesterone receptor status in the Iowa Women's Health Study. Cancer Epidemiol Biomarkers Prev. 1995;4:313-318.
ABSTRACT
43. Li CI, Malone KE, Porter PL, et al. Relationship between long durations and different regimens of hormone therapy and risk of breast cancer. JAMA. 2003;289:3254-3263.
FREE FULL TEXT
44. Chen WY, Hankinson SE, Schnitt SJ, Rosner BA, Holmes MD, Colditz GA. Association of hormone replacement therapy to estrogen and progesterone receptor status in invasive breast carcinoma. Cancer. 2004;101:1490-1500.
FULL TEXT
|
ISI
| PUBMED
45. Tutera AM, Sellers TA, Potter JD, Drinkard CR, Wiesner GL, Folsom AR. Association between family history of cancer and breast cancer defined by estrogen and progesterone receptor status. Genet Epidemiol. 1996;13:207-221.
FULL TEXT
|
ISI
| PUBMED
46. Enger SM, Ross RK, Paganini-Hill A, Carpenter CL, Bernstein L. Body size, physical activity, and breast cancer hormone receptor status: results from two case-control studies. Cancer Epidemiol Biomarkers Prev. 2000;9:681-687.
FREE FULL TEXT
47. Sellers TA, Davis J, Cerhan JR, et al. Interaction of waist/hip ratio and family history on the risk of hormone receptor–defined breast cancer in a prospective study of postmenopausal women. Am J Epidemiol. 2002;155:225-233.
FREE FULL TEXT
48. 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.
FREE FULL TEXT
49. Kushi LH, Potter JD, Bostick RM, et al. Dietary fat and risk of breast cancer according to hormone receptor status. Cancer Epidemiol Biomarkers Prev. 1995;4:11-19.
ABSTRACT
50. Adams SA, Matthews CE, Hebert JR, et al. Association of physical activity with hormone receptor status: the Shanghai Breast Cancer Study. Cancer Epidemiol Biomarkers Prev. 2006;15:1170-1178.
FREE FULL TEXT
51. Folsom AR, Kaye SA, Prineas RJ, Potter JD, Gapstur SM, Wallace RB. Increased incidence of carcinoma of the breast associated with abdominal adiposity in postmenopausal women. Am J Epidemiol. 1990;131:794-803.
FREE FULL TEXT
52. Bisgard KM, Folsom AR, Hong CP, Sellers TA. Mortality and cancer rates in nonrespondents to a prospective study of older women: 5-year follow-up. Am J Epidemiol. 1994;139:990-1000.
FREE FULL TEXT
53. Pate RR, Pratt M, Blair SN, et al. Physical activity and public health: a recommendation from the Centers for Disease Control and Prevention and the American College of Sports Medicine. JAMA. 1995;273:402-407.
FREE FULL TEXT
54. Kushi LH, Fee RM, Folsom AR, Mink PJ, Anderson KE, Sellers TA. Physical activity and mortality in postmenopausal women. JAMA. 1997;277:1287-1292.
FREE FULL TEXT
55. Prineas RJ, Folsom AR, Kaye SJ. Central adiposity and increased risk of coronary artery disease mortality in older women. Ann Epidemiol. 1993;3:35-41.
PUBMED
56. McTiernan A, Ulrich C, Slate S, Potter J. Physical activity and cancer etiology: associations and mechanisms. Cancer Causes Control. 1998;9:487-509.
FULL TEXT
|
ISI
| PUBMED
57. Friedenreich CM, Orenstein MR. Physical activity and cancer prevention: etiologic evidence and biological mechanisms. J Nutr. 2002;132(suppl):3456S-3464S.
FREE FULL TEXT
58. Hoffman-Goetz L, Apter D, Demark-Wahnefried W, Goran MI, McTiernan A, Reichman ME. Possible mechanisms mediating an association between physical activity and breast cancer. Cancer. 1998;83(suppl):621-628.
FULL TEXT
|
ISI
| PUBMED
59. Korn EL, Graubard BI, Midthune D. Time-to-event analysis of longitudinal follow-up of a survey: choice of the time-scale. Am J Epidemiol. 1997;145:72-80.
FREE FULL TEXT
60. Benichou J. Methods for adjusting for estimating the population attributable risk in case-control studies: a review. Stat Med. 1991;10:1753-1773.
ISI
| PUBMED
61. Kahn MJ, O’Fallon WM, Sicks JD. Generalized Population Attributable Risk Estimation. Rochester, Minn: Dept of Health Sciences Research, Mayo Clinic; 1998. Technical Report series 54.62. Cerhan JR, Grabrick DM, Vierkant RA, et al. Interaction of adolescent anthropometric characteristics and family history on breast cancer risk in a Historical Cohort Study of 426 families (USA). Cancer Causes Control. 2004;15:1-9.
FULL TEXT
|
ISI
| PUBMED
63. Bernstein L, Patel AV, Ursin G, et al. Lifetime recreational exercise activity and breast cancer risk among black women and white women. J Natl Cancer Inst. 2005;97:1671-1679.
FREE FULL TEXT
64. Britton JA, Gammon MD, Schoenberg JB, et al. Risk of breast cancer classified by joint estrogen receptor and progesterone receptor status among women 20-44 years of age. Am J Epidemiol. 2002;156:507-516.
FREE FULL TEXT
65. Anderson WF, Chu KC, Chatterjee N, Brawley O, Brinton LA. Tumor variants by hormone receptor expression in white patients with node-negative breast cancer from the Surveillance, Epidemiology, and End Results database. J Clin Oncol. 2001;19:18-27.
FREE FULL TEXT
66. Bardou VJ, Arpino G, Elledge RM, Osborne CK, Clark GM. Progesterone receptor status significantly improves outcome prediction over estrogen receptor status alone for adjuvant endocrine therapy in two large breast cancer databases. J Clin Oncol. 2003;21:1973-1979.
FREE FULL TEXT
67. Ellis MJ, Coop A, Singh B, et al. Letrozole is more effective neoadjuvant endocrine therapy than tamoxifen for ErbB-1– and/or ErbB-2–positive, estrogen receptor–positive primary breast cancer: evidence from a phase III randomized trial. J Clin Oncol. 2001;19:3808-3816.
FREE FULL TEXT
68. Cui X, Schiff R, Arpino G, Osborne CK, Lee AV. Biology of progesterone receptor loss in breast cancer and its implications for endocrine therapy. J Clin Oncol. 2005;23:7721-7735.
FREE FULL TEXT
69. Balleine RL, Earl MJ, Greenberg ML, Clarke CL. Absence of progesterone receptor associated with secondary breast cancer in postmenopausal women. Br J Cancer. 1999;79:1564-1571.
FULL TEXT
|
ISI
| PUBMED
70. Arpino G, Weiss H, Lee AV, et al. Estrogen receptor–positive, progesterone receptor–negative breast cancer: association with growth factor receptor expression and tamoxifen resistance. J Natl Cancer Inst. 2005;97:1254-1261.
FREE FULL TEXT
71. Esposito K, Pontillo A, Di Palo C, et al. Effect of weight loss and lifestyle changes on vascular inflammatory markers in obese women: a randomized trial. JAMA. 2003;289:1799-1804.
FREE FULL TEXT
72. Bianchini F, Kaaks R, Vainio H. Weight control and physical activity in cancer prevention. Obes Rev. 2002;3:5-8.
FULL TEXT
| PUBMED
73. Grann VR, Troxel AB, Zojwalla NJ, Jacobson JS, Hershman D, Neugut AI. Hormone receptor status and survival in a population-based cohort of patients with breast carcinoma. Cancer. 2005;103:2241-2251.
FULL TEXT
|
ISI
| PUBMED
74. US Department of Health and Human Services. Physical activity and health: a report of the surgeon general. http://www.cdc.gov/nccdphp/sgr/pdf/sgrfull.pdf. Accessed July 5, 2006.
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