Breast Cancer Research and Treatment

, Volume 165, Issue 1, pp 201–213

Lifetime moderate-to-vigorous physical activity and ER/PR/HER-defined post-menopausal breast cancer risk

  • Joy Shi
  • Lindsay C. Kobayashi
  • Anne Grundy
  • Harriet Richardson
  • Sandip K. SenGupta
  • Caroline A. Lohrisch
  • John J. Spinelli
  • Kristan J. Aronson
Epidemiology

Abstract

Purpose

To assess the relationship of moderate-to-vigorous physical activity (MVPA) in leisure-time, household, and occupational domains across the total lifetime and in four age periods with breast cancer risk, as defined by estrogen receptor (ER)/progesterone receptor (PR) status and ER/PR/human epidermal growth factor-2 (HER2) status, among post-menopausal women.

Methods

Data were from 692 women with incident breast cancer and 644 controls in the Canadian Breast Cancer Study, a case–control study of women aged 40–80 years in British Columbia and Ontario. Mean metabolic equivalent (MET)-hours/week for questionnaire-assessed leisure-time, household, and occupational MVPA were calculated for the total lifetime and four age periods (12–17, 18–34, 45–49, and ≥50 years). Odds ratios (ORs) for the relationships between domain-specific MVPA at each lifetime period and risks of ER/PR-defined and ER/PR/HER2-defined breast cancers were estimated using polytomous logistic regression. Trend tests for dose–response relationships were calculated for the ORs across increasing tertiles of mean MET-hours/week of MVPA.

Results

Total lifetime leisure-time MVPA was associated with reduced risk of ER−/PR− breast cancer in a dose–response fashion (ptrend = 0.014). In contrast, total lifetime household MVPA was associated with reduced risk of ER+ and/or PR+ breast cancer (ptrend < 0.001). When further stratified by HER2 status, the effect of leisure-time MVPA appeared confined to HER2− breast cancers, and the effect of household MVPA did not differ according to HER2 status. Similar trends were observed when stratified by age period.

Conclusions

Lifetime leisure-time MVPA appeared to be associated with reduced risk of ER−/PR−/HER2− breast cancers and lifetime household MVPA was associated with reduced risk of ER+ and/or PR+ breast cancer, regardless of HER2 status.

Keywords

Physical activity Breast cancer Estrogen Progesterone HER2 

Supplementary material

10549_2017_4323_MOESM1_ESM.doc (331 kb)
Supplementary material 1 (DOC 331 kb)

References

  1. 1.
    Yang XR, Chang-Claude J, Goode EL, Couch FJ, Nevanlinna H, Milne RL et al (2011) Associations of breast cancer risk factors with tumor subtypes: a pooled analysis from the Breast Cancer Association Consortium studies. J Natl Cancer Ist 103:250–263. doi:10.1093/jnci/djq526 CrossRefGoogle Scholar
  2. 2.
    Boyle P (2012) Triple-negative breast cancer: epidemiological considerations and recommendations. Ann Oncol 23:vi7–vi12. doi:10.1093/annonc/mds187
  3. 3.
    Foulkes WD (2004) Estrogen receptor status in BRCA1- and BRCA2-related breast cancer: the influence of age, grade, and histological type. Clin Cancer Res 10:2029–2034CrossRefPubMedGoogle Scholar
  4. 4.
    Anderson WF, Chatterjee N, Ershler WB, Brawley OW (2002) Estrogen receptor breast cancer phenotypes in the surveillance, epidemiology, and end results database. Breast Cancer Res Treat 76:27–36. doi:10.1023/A:1020299707510 CrossRefPubMedGoogle Scholar
  5. 5.
    Trivers KF, Lund MJ, Porter P, Liff JM, Flagg EW, Coates RJ et al (2009) The epidemiology of triple-negative breast cancer, including race. Cancer Causes Control 20:1071–1082. doi:10.1007/s10552-009-9331-1 CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Parise CA, Bauer KR, Brown MM, Caggiano V (2009) Breast cancer subtypes as defined by the estrogen receptor (ER), progesterone receptor (PR), and the human epidermal growth factor receptor 2 (HER2) among women with invasive breast cancer in California, 1999-2004. Breast J 15:593–602. doi:10.1111/j.1524-4741.2009.00822.x CrossRefPubMedGoogle Scholar
  7. 7.
    Ma H, Wang Y, Sullivan-Halley J (2010) Use of four biomarkers to evaluate the risk of breast cancer subtypes in the Women’s Contraceptive and Reproductive Experiences Study. Cancer Res 70:575–587. doi:10.1158/0008-5472.CAN-09-3460 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Peters TM, Moore SC, Gierach GL, Wareham NJ, Ekelund U, Hollenbeck AR et al (2009) Intensity and timing of physical activity in relation to postmenopausal breast cancer risk: the prospective NIH-AARP Diet and Health Study. BMC Cancer 9:1–14. doi:10.1186/1471-2407-9-349 CrossRefGoogle Scholar
  9. 9.
    Leitzmann MF, Moore SC, Peters TM, Lacey JV, Schatzkin A, Schairer C et al (2008) Prospective study of physical activity and risk of postmenopausal breast cancer. Breast Cancer Res 10(5):R92. doi:10.1186/bcr2190 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Peplonska B, Lissowska J, Hartman TJ, Szeszenia-Dabrowska N, Blair A, Zatonski W et al (2008) Adulthood lifetime physical activity and breast cancer. Epidemiology 19:226–236. doi:10.1097/EDE.0b013e3181633bfb CrossRefPubMedGoogle Scholar
  11. 11.
    Slattery ML, Edwards S, Murtaugh MA, Sweeney C, Herrick J, Byers T et al (2007) Physical activity and breast cancer risk among women in the southwestern United States. Ann Epidemiol 17:342–353CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Bernstein L, Patel AV, Ursin G, Sullivan-Halley J, Press MF, Deapen D et al (2005) Lifetime recreational exercise activity and breast cancer risk among black women and white women. J Nat Cancer Inst 97:1671–1679CrossRefPubMedGoogle Scholar
  13. 13.
    Adams SA, Matthews CE, Hebert JR, Moore CG, Cunningham JE, Shu X-O et al (2006) Association of physical activity with hormone receptor status: the Shanghai Breast Cancer Study. Cancer Epidemiol Biomark Prev 15:1170–1178CrossRefGoogle Scholar
  14. 14.
    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 Biomark Prev 9:681–687Google Scholar
  15. 15.
    Suzuki R, Iwasaki M, Kasuga Y (2010) Leisure-time physical activity and breast cancer risk by hormone receptor status: effective life periods and exercise intensity. Cancer Causes Control 21:1787–1798. doi:10.1007/s10552-010-9605-7 CrossRefPubMedGoogle Scholar
  16. 16.
    Eliassen A, Hankinson S, Rosner B, Holmes M, Willett W (2010) Physical activity and risk of breast cancer among postmenopausal women. Arch Intern Med 170:1758–1764. doi:10.1001/archinternmed.2010.363 CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Rosato V, Bertuccio P, Bosetti C, Negri E, Edefonti V, Ferraroni M (2013) Nutritional factors, physical activity, and breast cancer by hormone receptor status. Breast 22:887–893. doi:10.1016/j.breast.2013.04.004 CrossRefPubMedGoogle Scholar
  18. 18.
    Schmidt ME, Steindorf K, Mutschelknauss E, Slanger T, Kropp S, Obi N et al (2008) Physical activity and postmenopausal breast cancer: effect modification by breast cancer subtypes and effective periods in life. Cancer Epidemiol Biomark Prev 17:3402–3410. doi:10.1158/1055-9965.EPI-08-0479 CrossRefGoogle Scholar
  19. 19.
    Bardia A, Hartmann LC, Vachon CM, Vierkant RA, Wang AH, Olson JE et al (2006) Recreational physical activity and risk of postmenopausal breast cancer based on hormone receptor status. Arch Intern Med 166:2478–2483CrossRefPubMedGoogle Scholar
  20. 20.
    Suzuki R, Iwasaki M, Yamamoto S, Inoue M, Sasazuki S (2011) Leisure-time physical activity and breast cancer risk defined by estrogen and progesterone receptor status—the Japan Public Health Center-based Prospective Study. Prev Med 52:227–233. doi:10.1016/j.ypmed.2011.01.016 PubMedGoogle Scholar
  21. 21.
    Dallal CM, Sullivan-Halley J, Ross RK, Wang Y, Deapen D, Horn-ross PL et al (2007) Long-term recreational physical activity and risk of invasive and in situ breast cancer. Arch Intern Med 167:408–415CrossRefPubMedGoogle Scholar
  22. 22.
    Wu Y, Zhang D, Kang S (2012) Physical activity and risk of breast cancer: a meta-analysis of prospective studies. Breast Cancer Res Treat 137(3):869–882. doi:10.1007/s10549-012-2396-7 CrossRefPubMedGoogle Scholar
  23. 23.
    Steindorf K, Ritte R, Eomois P, Lukanova A, Tjonneland A, Johnsen N et al (2012) Physical activity and risk of breast cancer overall and by hormone receptor status: the European prospective investigation into cancer and nutrition. Int J Cancer 132:1667–1678. doi:10.1002/ijc.27778 CrossRefPubMedGoogle Scholar
  24. 24.
    Phipps AI, Chlebowski RT, Prentice R (2011) Body size, physical activity, and risk of triple-negative and estrogen receptor—positive breast cancer. Cancer Epidemiol Biomark Prev 20:454–463. doi:10.1158/1055-9965.EPI-0974 CrossRefGoogle Scholar
  25. 25.
    Ma H, Xu X, Ursin G, Simon MS, Marchbanks PA, Malone KE et al (2015) Reduced risk of breast cancer associated with recreational physical activity varies by HER2 status. Cancer Med 4:1122–1135. doi:10.1002/cam4.465 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Ma H, Xu X, Clague J, Lu Y, Togawa K, Wang SS et al (2016) Recreational physical activity and risk of triple negative breast cancer in the California Teachers Study. Breast Cancer Res Treat 18:62. doi:10.1186/s13058-016-0723-3 CrossRefGoogle Scholar
  27. 27.
    Grundy A, Richardson H, Burstyn I, Lohrisch C, Sengupta SK, Lai AS et al (2013) Increased risk of breast cancer associated with long-term shift work in Canada. Occ Environ Med 70:831–838. doi:10.1136/oemed-2013-101482 CrossRefGoogle Scholar
  28. 28.
    Kobayashi LC, Janssen I, Richardson H, Lai AS, Spinelli JJ, Aronson KJ (2013) Moderate-to-vigorous intensity physical activity across the life course and risk of pre- and post-menopausal breast cancer. Breast Cancer Res Treat 139:851–861. doi:10.1007/s10549-013-2569-9 CrossRefPubMedGoogle Scholar
  29. 29.
    Friedenreich C, Courneya K, Bryant H (1998) The lifetime total physical activity questionnaire: development and reliability. Med Sci Sport Exerc 30:266–274CrossRefGoogle Scholar
  30. 30.
    Ainsworth BE, Haskell WL, Whitt MC, Irwin ML, Swartz ANNM, Strath SJ et al (2000) Compendium of physical activities: an update of activity codes and MET intensities. Med Sci Sport Exerc 32:S498–S516CrossRefGoogle Scholar
  31. 31.
    Harris L, Fritsche H, Mennel R, Norton L, Ravdin P, Taube S et al (2007) American Society of Clinical Oncology 2007 update of recommendations for the use of tumor markers in breast cancer. J Clin Oncol 25:5287–5312CrossRefPubMedGoogle Scholar
  32. 32.
    Smigal C, Jemal A, Ward E, Cokkinides V, Smith R, Howe HL et al (2006) Trends in breast cancer by race and ethnicity: update 2006. CA Cancer J Clin 56:168–183CrossRefPubMedGoogle Scholar
  33. 33.
    Mcpherson K, Steel CM, Dixon JM (2000) Breast cancer—epidemiology, risk factors, and genetics. BMJ 321:624–628CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Friedenreich CM (2011) Physical activity and breast cancer: review of the epidemiologic evidence and biological mechanisms. In: Senn H-J, Otto F (eds) Clinical cancer prevention. Springer, Berlin, pp 125–139Google Scholar
  35. 35.
    Friedenreich CM, Neilson HK, Woolcott CG, Wang Q, Yasui Y, Brant RF et al (2011) Mediators and moderators of the effects of a year-long exercise intervention on endogenous sex hormones in postmenopausal women. Cancer Causes Control 11:1365–1373. doi:10.1007/s10552-011-9809-5 CrossRefGoogle Scholar
  36. 36.
    Friedenreich C, Woolcott C, McTiernan A, Ballard-Barbash R, Brant R, Stanczyk F et al (2010) Alberta physical activity and breast cancer prevention trial: sex hormone changes in a year-long exercise intervention among postmenopausal women. J Clin Oncol 28:1458–1466. doi:10.1200/JCO.2009.24.9557 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Friedenreich CM, Neilson HK, Woolcott CG, Wang Q, Stanczyk FZ, McTiernan A et al (2011) Inflammatory marker changes in a yearlong randomized exercise intervention trial among postmenopausal women. Cancer Prev Res 5:98–108. doi:10.1158/1940-6207.CAPR-11-0369 CrossRefGoogle Scholar
  38. 38.
    Lynch BM, Friedenreich CM, Vallance JK, Eakin EG, Owen N (2011) Associations of objectively assessed physical activity and sedentary time with biomarkers of breast cancer risk in postmenopausal women: findings from NHANES (2003–2006). Breast Cancer Res Treat 130:183–194. doi:10.1007/s10549-011-1559-2 CrossRefPubMedGoogle Scholar
  39. 39.
    Pischon T, Hankinson SE, Hotamisligil GS, Rifai N, Rimm EB (2003) Leisure-time physical activity and reduced plasma levels of obesity-related inflammatory markers. Obesity 11:1055–1064CrossRefGoogle Scholar
  40. 40.
    Friedenreich CM, Neilson HK, Woolcott CG, Mctiernan A, Wang Q, Ballard-Barbash R et al (2011) Changes in insulin resistance indicators, IGFs, and adipokines in a year-long trial of aerobic exercise in postmenopausal women. Endocr Relat Cancer 18:357–369. doi:10.1530/ERC-10-0303 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Vona-Davis L, Rose DP (2007) Adipokines as endocrine, paracrine, and autocrine factors in breast cancer risk and progression. Endocr Relat Cancer 14:189–206CrossRefPubMedGoogle Scholar
  42. 42.
    Mantovani A, Allavena P, Sica A, Balkwill F (2008) Cancer-related inflammation. Nature 454:436–444. doi:10.1038/nature07205 CrossRefPubMedGoogle Scholar
  43. 43.
    Bruning PF, Bonfrèr JMG, van Noord PAH, Hart AAM, de Jong-Bakker M, Nooijen WJ (1992) Insulin resistance and breast cancer risk. Int J Cancer 52:511–516CrossRefPubMedGoogle Scholar
  44. 44.
    Jin Q, Esteva F (2008) Cross-talk between the ErbB/HER family and the type i insulin-like growth factor receptor signaling pathway in breast cancer. J Mammary Gland Biol Neoplasia 13(4):485–498CrossRefPubMedGoogle Scholar
  45. 45.
    Allen NE, Appleby PN, Kaaks R, Rinaldi S, Davey GK, Key TJ (2003) Lifestyle determinants of serum insulin-like growth-factor-I (IGF-I), C-peptide and hormone binding protein levels in British women. Cancer Causes Control 14:65–74CrossRefPubMedGoogle Scholar
  46. 46.
    McTiernan A, Sorensen B, Yasui Y, Tworoger SS, Ulrich CM, Irwin ML et al (2005) No effect of exercise on insulin-like growth factor 1 and insulin-like growth factor binding protein 3 in postmenopausal women: a 12-month randomized clinical trial. Cancer Epidemiol Biomark Prev 14:1020–1021CrossRefGoogle Scholar
  47. 47.
    Ridley K, Olds T (2008) Assigning energy costs to activities in children: a review and synthesis. Med Sci Sports Exerc 40(8):1439CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  1. 1.Department of EpidemiologyHarvard T. H. Chan School of Public HealthBostonUSA
  2. 2.Center for Population and Development StudiesHarvard T. H. Chan School of Public HealthCambridgeUSA
  3. 3.CRCHUM (Centre de recherche du Centre hospitalier de l’Université de Montréal)MontrealCanada
  4. 4.Department of Social and Preventive MedicineUniversité de MontréalMontrealCanada
  5. 5.Department of Public Health Sciences and Cancer Research InstituteQueen’s UniversityKingstonCanada
  6. 6.Department of Pathology and Molecular MedicineQueen’s UniversityKingstonCanada
  7. 7.Department of Medical OncologyBritish Columbia Cancer AgencyVancouverCanada
  8. 8.School of Population and Public HealthUniversity of British ColumbiaVancouverCanada
  9. 9.Department of Cancer Control ResearchBritish Columbia Cancer AgencyVancouverCanada

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