Abstract
Objective
Physical activity may decrease breast cancer risk. However, it is unclear what intensity of exercise and during which life periods this effect on decreasing risk is efficiently expressed, and whether the associations differ by the estrogen-/progesterone- receptor (ER/PR) status of tumors. We investigated associations between age- and intensity-specific leisure-time physical activity and ER/PR-defined breast cancer risk.
Methods
We conducted a hospital-based case–control study in Nagano, Japan. Subjects were 405 cases newly diagnosed (>99% known ER/PR) from 2001 to 2005, who were age-/area-matched with 405 controls. Activity was assessed with a self-reported questionnaire which considered intensity level (moderate and/or strenuous) at different ages (at 12 and 20 years, and in the previous 5 years). Odds ratios (ORs) and 95% confidence intervals were calculated using logistic regression.
Results
Strenuous but not moderate physical activity at age 12 was inversely associated with pre- and postmenopausal breast cancer risk across ER/PR subtypes [overall OR≥5 days/week vs. none = 0.24 (0.14–0.43)]. Moderate physical activity in the previous 5 years was significantly associated with a decrease in risk for postmenopausal ER + PR + tumors only [OR≥1 day/week vs. none = 0.35 (0.18–0.67)].
Conclusion
Strenuous activity in teens and moderate activity after menopause may contribute to a reduction in breast cancer risk.
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Abbreviations
- BMI:
-
Body mass index
- CIs:
-
Confidence intervals
- ER:
-
Estrogen receptor
- FFQ:
-
Food frequency questionnaire
- IGF-1:
-
Insulin-like growth factor 1
- OC:
-
Oral contraceptives
- OR:
-
Odds ratio
- PMH:
-
Postmenopausal hormones
- PR:
-
Progesterone receptor
- SHBG:
-
Sex hormone-binding globulin
- SD:
-
Standard deviation
References
Matsuda T, Marugame T, Kamo KI, Katanoda K, Ajiki W, Sobue T (2009) Cancer incidence and incidence rates in Japan in 2003: based on data from 13 Population-based Cancer Registries in the Monitoring of Cancer Incidence in Japan (MCIJ) Project. Jpn J Clin Oncol.hyp106 [pii]10.1093/jjco/hyp106
Maruti SS, Willett WC, Feskanich D, Rosner B, Colditz GA (2008) A prospective study of age-specific physical activity and premenopausal breast cancer. J Natl Cancer Inst 100:728–737
World Cancer Resarch Fund/American Institute for Cancer Resarch (2007) Food, nutrition, physical activity, and the prevention of cancer: a global perspective. AICR, Washington DC, p 289
Sternfeld B, Bhat AK, Wang H, Sharp T, Quesenberry CP Jr (2005) Menopause, physical activity, and body composition/fat distribution in midlife women. Med Sci Sports Exerc 37:1195–1202
van Gils CH, Peeters PH, Schoenmakers MC, Nijmeijer RM, Onland-Moret NC, van der Schouw YT, Monninkhof EM (2009) Physical activity and endogenous sex hormone levels in postmenopausal women: a cross-sectional study in the Prospect-EPIC Cohort. Cancer Epidemiol Biomarkers Prev 18: 377–383. 1055-9965.EPI-08-0823 [pii]10.1158/1055-9965.EPI-08-0823
Frisch RE, Gotz-Welbergen AV, McArthur JW, Albright T, Witschi J, Bullen B, Birnholz J, Reed RB, Hermann H (1981) Delayed menarche and amenorrhea of college athletes in relation to age of onset of training. JAMA 246:1559–1563
Bernstein L, Ross RK, Lobo RA, Hanisch R, Krailo MD, Henderson BE (1987) The effects of moderate physical activity on menstrual cycle patterns in adolescence: implications for breast cancer prevention. Br J Cancer 55:681–685
Regensteiner JG, Mayer EJ, Shetterly SM, Eckel RH, Haskell WL, Marshall JA, Baxter J, Hamman RF (1991) Relationship between habitual physical activity and insulin levels among nondiabetic men and women. San Luis Valley Diabetes Study, Diabetes Care 14:1066–1074
Raastad T, Bjoro T, Hallen J (2000) Hormonal responses to high- and moderate-intensity strength exercise. Eur J Appl Physiol 82:121–128
Bernstein L, Ross RK (1993) Endogenous hormones and breast cancer risk. Epidemiol Rev 15:48–65
Lawlor DA, Smith GD, Ebrahim S (2004) Hyperinsulinaemia and increased risk of breast cancer: findings from the British Women’s Heart and Health Study. Cancer Causes Control 15:267–275
Yu H, Rohan T (2000) Role of the insulin-like growth factor family in cancer development and progression. J Natl Cancer Inst 92:1472–1489
Hankinson SE, Willett WC, Colditz GA, Hunter DJ, Michaud DS, Deroo B, Rosner B, Speizer FE, Pollak M (1998) Circulating concentrations of insulin-like growth factor-I and risk of breast cancer. Lancet 351:1393–1396
Hoffman-Goetz L, e. (ed) (1996) Exercise and immune function. CRC Press, Boca Raton, FL
Ji LL (1996) Exercise, oxidative stress, and antioxidants. Am J Sports Med 24:S20–S24
Shephard RJ, Shek PN (1995) Cancer, immune function, and physical activity. Can J Appl Physiol 20:1–25
Lee IM, Rexrode KM, Cook NR, Hennekens CH, Burin JE (2001) Physical activity and breast cancer risk: the Women’s Health Study (United States). Cancer Causes Control 12:137–145
McTiernan A, Kooperberg C, White E, Wilcox S, Coates R, Adams-Campbell LL, Woods N, Ockene J (2003) Recreational physical activity and the risk of breast cancer in postmenopausal women: the Women’s Health Initiative Cohort Study. JAMA 290:1331–1336
Bardia A, Hartmann LC, Vachon CM, Vierkant RA, Wang AH, Olson JE, Sellers TA, Cerhan JR (2006) Recreational physical activity and risk of postmenopausal breast cancer based on hormone receptor status. Arch Intern Med 166:2478–2483
Chlebowski RT, Anderson GL, Lane DS, Aragaki AK, Rohan T, Yasmeen S, Sarto G, Rosenberg CA, Hubbell FA (2007) Predicting risk of breast cancer in postmenopausal women by hormone receptor status. J Natl Cancer Inst 99:1695–1705
Dallal CM, Sullivan-Halley J, Ross RK, Wang Y, Deapen D, Horn-Ross PL, Reynolds P, Stram DO, Clarke CA, Anton-Culver H, Ziogas A, Peel D, West DW, Wright W, Bernstein L (2007) Long-term recreational physical activity and risk of invasive and in situ breast cancer: the California teachers study. Arch Intern Med 167:408–415
Leitzmann MF, Moore SC, Peters TM, Lacey JV Jr., Schatzkin A, Schairer C, Brinton LA, Albanes D (2008) Prospective study of physical activity and risk of postmenopausal breast cancer. Breast Cancer Res 10: R92.bcr2190 [pii]10.1186/bcr2190
Peters TM, Schatzkin A, Gierach GL, Moore SC, Lacey JV Jr, Wareham NJ, Ekelund U, Hollenbeck AR, Leitzmann MF (2009) Physical activity and postmenopausal breast cancer risk in the NIH-AARP diet and health study. Cancer Epidemiol Biomarkers Prev 18:289–296
Enger SM, Ross RK, Paganini-Hill A, Carpenter CL, Bernstein L (2000) Body size, physical activity, and breast cancer hormone receptor status: results from two case-control studies. Cancer Epidemiol Biomarkers Prev 9:681–687
Britton JA, Gammon MD, Schoenberg JB, Stanford JL, Coates RJ, Swanson CA, Potischman N, Malone KE, Brogan DJ, Daling JR, Brinton LA (2002) Risk of breast cancer classified by joint estrogen receptor and progesterone receptor status among women 20–44 years of age. Am J Epidemiol 156:507–516
Bernstein L, Patel AV, Ursin G, Sullivan-Halley J, Press MF, Deapen D, Berlin JA, Daling JR, McDonald JA, Norman SA, Malone KE, Strom BL, Liff J, Folger SG, Simon MS, Burkman RT, Marchbanks PA, Weiss LK, Spirtas R (2005) Lifetime recreational exercise activity and breast cancer risk among black women and white women. J Natl Cancer Inst 97:1671–1679
Adams SA, Matthews CE, Hebert JR, et al (2006) Association of physical activity with hormone receptor status: the Shanghai Breast Cancer Study. Cancer Epidemiol Biomarkers Prev 15:1170–1178
Schmidt ME, Steindorf K, Mutschelknauss E, Slanger T, Kropp S, Obi N, Flesch-Janys D, Chang-Claude J (2008) Physical activity and postmenopausal breast cancer: effect modification by breast cancer subtypes and effective periods in life. Cancer Epidemiol Biomarkers Prev 17:3402–3410
Itoh H, Iwasaki M, Hanaoka T, et al (2009) Serum organochlorines and breast cancer risk in Japanese women: a case-control study. Cancer Causes Control 20:567–580
Inoue M, Yamamoto S, Kurahashi N, Iwasaki M, Sasazuki S, Tsugane S (2008) Daily total physical activity level and total cancer risk in men and women: results from a large-scale population-based cohort study in Japan. Am J Epidemiol 168:391–403
Tsugane S, Kobayashi M, Sasaki S (2003) Validity of the self-administered food frequency questionnaire used in the 5-year follow-up survey of the JPHC study cohort I: comparison with dietary records for main nutrients. J Epidemiol 13:S51–S56
Ishihara J, Inoue M, Kobayashi M, Tanaka S, Yamamoto S, Iso H, Tsugane S (2006) Impact of the revision of a nutrient database on the validity of a self-administered food frequency questionnaire (FFQ). J Epidemiol 16:107–116
The Council for Science and Technology: Ministry of Education C, S., Science and Technology, Japan (2005) ‘Standard Tables of Food Composition in Japan’, the fifth reviseed and enlarged edition Edition. National Printing Bureau, Tokyo
Marrett LD, Theis B, Ashbury FD (2000) Workshop report: physical activity and cancer prevention. Chronic Dis Can 21:143–149
Dreher D, Junod AF (1996) Role of oxygen free radicals in cancer development. Eur J Cancer 32A:30–38
Moradi T, Nyren O, Zack M, Magnusson C, Persson I, Adami HO (2000) Breast cancer risk and lifetime leisure-time and occupational physical activity (Sweden). Cancer Causes Control 11:523–531
Friedenreich CM, Courneya KS, Bryant HE (2001) Influence of physical activity in different age and life periods on the risk of breast cancer. Epidemiology 12:604–612
Cleland WH, Mendelson CR, Simpson ER (1985) Effects of aging and obesity on aromatase activity of human adipose cells. J Clin Endocrinol Metab 60:174–177
London S, Willett W, Longcope C, McKinlay S (1991) Alcohol and other dietary factors in relation to serum hormone concentrations in women at climacteric. Am J Clin Nutr 53:166–171
Goldin BR, Woods MN, Spiegelman DL, Longcope C, Morrill-LaBrode A, Dwyer JT, Gualtieri LJ, Hertzmark E, Gorbach SL (1994) The effect of dietary fat and fiber on serum estrogen concentrations in premenopausal women under controlled dietary conditions. Cancer 74:1125–1131
Singh A, Hamilton-Fairley D, Koistinen R, Seppala M, James VH, Franks S, Reed MJ (1990) Effect of insulin-like growth factor-type I (IGF-I) and insulin on the secretion of sex hormone binding globulin and IGF-I binding protein (IBP-I) by human hepatoma cells. J Endocrinol 124:R1–R3
Shephard RJ, Rhind S, Shek PN (1995) The impact of exercise on the immune system: NK cells, interleukins 1 and 2, and related responses. Exerc Sport Sci Rev 23:215–241
Cui X, Zhang P, Deng W, Oesterreich S, Lu Y, Mills GB, Lee AV (2003) Insulin-like growth factor-I inhibits progesterone receptor expression in breast cancer cells via the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin pathway: progesterone receptor as a potential indicator of growth factor activity in breast cancer. Mol Endocrinol 17:575–588
Wang M, Yu B, Westerlind K, et al (2009) Prepubertal physical activity up-regulates estrogen receptor beta, BRCA1 and p53 mRNA expression in the rat mammary gland. Breast Cancer Res Treat 115:213–220
Breslow NE, Day NE (1980) Volume 1- the analysis of case-control studies. In: Davis W (ed) Statistical methods in cancer research: IARC Scientific Publication No. 32. International Agency For Research On Cancer, Lyon, pp 84–280
Fransson E, Knutsson A, Westerholm P, Alfredsson L (2008) Indications of recall bias found in a retrospective study of physical activity and myocardial infarction. J Clin Epidemiol 61:840–847
Financial support
This study was supported by grants-in-aid for Cancer Research from the Ministry of Health, Labour and Welfare of Japan; and for Scientific Research on Priority Areas from the Ministry of Education, Culture, Sports, Science, and Technology of Japan. RS is an awardee of a Research Resident Fellowship from the Foundation for Promotion of Cancer Research (Japan) for the 3rd term Comprehensive 10-year Strategy for Cancer Control.
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Suzuki, R., Iwasaki, M., Kasuga, Y. et al. Leisure-time physical activity and breast cancer risk by hormone receptor status: effective life periods and exercise intensity. Cancer Causes Control 21, 1787–1798 (2010). https://doi.org/10.1007/s10552-010-9605-7
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DOI: https://doi.org/10.1007/s10552-010-9605-7