Advertisement

European Journal of Epidemiology

, Volume 29, Issue 6, pp 391–404 | Cite as

Association between physical activity and mortality in breast cancer: a meta-analysis of cohort studies

  • Shanliang Zhong
  • Tianchi Jiang
  • Tengfei Ma
  • Xiaohui Zhang
  • Jinhai Tang
  • Weixian Chen
  • Mengmeng Lv
  • Jianhua Zhao
META-ANALYSIS

Abstract

Previous studies concerning the association between physical activity (PA) and mortality in breast cancer yielded mixed results. We investigated the association by performing a meta-analysis of all available studies. Relevant studies were identified by searching PubMed and EMBASE to January 2014. We calculated the summary relative risk (RR) and 95 % confidence intervals (CIs) using random-effects models. The dose–response relationship was assessed by restricted cubic spline model and multivariate random-effect meta-regression. Sixteen cohort studies involving 42,602 patients of breast cancer were selected for meta-analysis. The analyses showed that patients who participated in any amount of PA before diagnosis had a RR of 0.82 (95 % CI 0.74–0.91) for breast cancer-specific mortality (vs. low PA). Those who participated in high PA and moderate PA before diagnosis had a RR of breast cancer-specific mortality of 0.81 (95 % CI 0.72–0.90) and 0.83 (95 % CI 0.73–0.94), respectively. Similar inverse associations of prediagnosis PA were found for all-cause mortality. Postdiagnosis PA on breast cancer-specific and all-cause mortality also showed the same results. Stratifying by body mass index (<25 vs. ≥25) or menopausal status, all the subgroups experienced benefits with PA, with a stronger mortality reduction among overweight women than normal weight women and among postmenopausal women than premenopausal women. A linear and significant dose–response association was only found for breast cancer-specific or all-cause mortality and prediagnosis PA (P for nonlinearity = 0.07 and 0.10, respectively). In conclusion, both prediagnosis and postdiagnosis PA were associated with reduced breast cancer-specific mortality and all-cause mortality.

Keywords

Physical activity Exercise Breast Cancer Mortality 

Notes

Acknowledgments

This study was supported by the National Natural Science Foundation of China (81272470).

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

10654_2014_9916_MOESM1_ESM.xls (28 kb)
Supplementary material 1 (XLS 27 kb)

References

  1. 1.
    Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin. 2013;63(1):11–30. doi: 10.3322/caac.21166.PubMedCrossRefGoogle Scholar
  2. 2.
    Keegan TH, Milne RL, Andrulis IL, et al. Past recreational physical activity, body size, and all-cause mortality following breast cancer diagnosis: results from the Breast Cancer Family Registry. Breast Cancer Res Treat. 2010;123(2):531–42. doi: 10.1007/s10549-010-0774-6.PubMedCentralPubMedCrossRefGoogle Scholar
  3. 3.
    Monninkhof EM, Elias SG, Vlems FA, et al. Physical activity and breast cancer: a systematic review. Epidemiology (Cambridge, Mass.). 2007;18(1):137–57. doi: 10.1097/01.ede.0000251167.75581.98.CrossRefGoogle Scholar
  4. 4.
    Friedenreich CM. The role of physical activity in breast cancer etiology. Semin Oncol. 2010;37(3):297–302. doi: 10.1053/j.seminoncol.2010.05.008.PubMedCrossRefGoogle Scholar
  5. 5.
    Ibrahim EM, Al-Homaidh A. Physical activity and survival after breast cancer diagnosis: meta-analysis of published studies. Med Oncol. 2011;28(3):753–65. doi: 10.1007/s12032-010-9536-x.PubMedCrossRefGoogle Scholar
  6. 6.
    Dal Maso L, Zucchetto A, Talamini R, et al. Effect of obesity and other lifestyle factors on mortality in women with breast cancer. Int J Cancer. 2008;123(9):2188–94. doi: 10.1002/ijc.23747.PubMedCrossRefGoogle Scholar
  7. 7.
    Friedenreich CM, Gregory J, Kopciuk KA, Mackey JR, Courneya KS. Prospective cohort study of lifetime physical activity and breast cancer survival. Int J Cancer. 2009;124(8):1954–62. doi: 10.1002/ijc.24155.PubMedCrossRefGoogle Scholar
  8. 8.
    West-Wright CN, Henderson KD, Sullivan-Halley J, et al. Long-term and recent recreational physical activity and survival after breast cancer: the California Teachers Study. Cancer Epidemiol Biomarkers Prev. 2009;18(11):2851–9. doi: 10.1158/1055-9965.epi-09-0538.PubMedCentralPubMedCrossRefGoogle Scholar
  9. 9.
    Emaus A, Veierod MB, Tretli S, et al. Metabolic profile, physical activity, and mortality in breast cancer patients. Breast Cancer Res Treat. 2010;121(3):651–60. doi: 10.1007/s10549-009-0603-y.PubMedCrossRefGoogle Scholar
  10. 10.
    Hellmann SS, Thygesen LC, Tolstrup JS, Gronbaek M. Modifiable risk factors and survival in women diagnosed with primary breast cancer: results from a prospective cohort study. Eur J Cancer Prev. 2010;19(5):366–73. doi: 10.1097/CEJ.0b013e32833b4828.PubMedCrossRefGoogle Scholar
  11. 11.
    Irwin ML, McTiernan A, Manson JE, et al. Physical activity and survival in postmenopausal women with breast cancer: results from the women’s health initiative. Cancer Prev Res (Phila). 2011;4(4):522–9. doi: 10.1158/1940-6207.capr-10-0295.CrossRefGoogle Scholar
  12. 12.
    Beasley JM, Kwan ML, Chen WY, et al. Meeting the physical activity guidelines and survival after breast cancer: findings from the after breast cancer pooling project. Breast Cancer Res Treat. 2012;131(2):637–43. doi: 10.1007/s10549-011-1770-1.PubMedCentralPubMedCrossRefGoogle Scholar
  13. 13.
    Cleveland RJ, Eng SM, Stevens J, et al. Influence of prediagnostic recreational physical activity on survival from breast cancer. Eur J Cancer Prev. 2012;21(1):46–54. doi: 10.1097/CEJ.0b013e3283498dd4.PubMedCentralPubMedCrossRefGoogle Scholar
  14. 14.
    Schmidt ME, Chang-Claude J, Vrieling A, et al. Association of pre-diagnosis physical activity with recurrence and mortality among women with breast cancer. Int J Cancer. 2013;133(6):1431–40. doi: 10.1002/ijc.28130.PubMedCrossRefGoogle Scholar
  15. 15.
    Rohan TE, Fu W, Hiller JE. Physical activity and survival from breast cancer. Eur J Cancer Prev. 1995;4(5):419–24.PubMedCrossRefGoogle Scholar
  16. 16.
    Wells G, Shea B, O’Connell D, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. 2010 www.ohri.ca/programs/clinical_epidemiology/oxford_web.ppt.
  17. 17.
    Holmes MD, Chen WY, Feskanich D, Kroenke CH, Colditz GA. Physical activity and survival after breast cancer diagnosis. JAMA. 2005;293(20):2479–86. doi: 10.1001/jama.293.20.2479.PubMedCrossRefGoogle Scholar
  18. 18.
    DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7(3):177–88.PubMedCrossRefGoogle Scholar
  19. 19.
    Abrahamson PE, Gammon MD, Lund MJ, et al. Recreational physical activity and survival among young women with breast cancer. Cancer. 2006;107(8):1777–85. doi: 10.1002/cncr.22201.PubMedCrossRefGoogle Scholar
  20. 20.
    Holick CN, Newcomb PA, Trentham-Dietz A, et al. Physical activity and survival after diagnosis of invasive breast cancer. Cancer Epidemiol Biomarkers Prev. 2008;17(2):379–86. doi: 10.1158/1055-9965.epi-07-0771.PubMedCrossRefGoogle Scholar
  21. 21.
    Enger SM, Bernstein L. Exercise activity, body size and premenopausal breast cancer survival. Br J Cancer. 2004;90(11):2138–41. doi: 10.1038/sj.bjc.6601820.PubMedCentralPubMedGoogle Scholar
  22. 22.
    Irwin ML, Smith AW, McTiernan A, et al. Influence of pre- and postdiagnosis physical activity on mortality in breast cancer survivors: the health, eating, activity, and lifestyle study. J Clin Oncol. 2008;26(24):3958–64. doi: 10.1200/jco.2007.15.9822.PubMedCentralPubMedCrossRefGoogle Scholar
  23. 23.
    Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21(11):1539–58. doi: 10.1002/sim.1186.PubMedCrossRefGoogle Scholar
  24. 24.
    Hedges LV, Pigott TD. The power of statistical tests in meta-analysis. Psychol Methods. 2001;6(3):203–17.PubMedCrossRefGoogle Scholar
  25. 25.
    Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315(7109):629–34.PubMedCentralPubMedCrossRefGoogle Scholar
  26. 26.
    Orsini N, Li R, Wolk A, Khudyakov P, Spiegelman D. Meta-analysis for linear and nonlinear dose-response relations: examples, an evaluation of approximations, and software. Am J Epidemiol. 2012;175(1):66–73. doi: 10.1093/aje/kwr265.PubMedCentralPubMedCrossRefGoogle Scholar
  27. 27.
    Orsini N, Bellocco R, Greenland S. Generalized least squares for trend estimation of summarized dose-response data. Stata J. 2006;6:40–57.Google Scholar
  28. 28.
    Jackson D, White IR, Thompson SG. Extending DerSimonian and Laird’s methodology to perform multivariate random effects meta-analyses. Stat Med. 2010;29(12):1282–97. doi: 10.1002/sim.3602.PubMedCrossRefGoogle Scholar
  29. 29.
    Pierce JP, Stefanick ML, Flatt SW, et al. Greater survival after breast cancer in physically active women with high vegetable-fruit intake regardless of obesity. J Clin Oncol. 2007;25(17):2345–51. doi: 10.1200/jco.2006.08.6819.PubMedCentralPubMedCrossRefGoogle Scholar
  30. 30.
    Borugian MJ, Sheps SB, Kim-Sing C, et al. Insulin, macronutrient intake, and physical activity: are potential indicators of insulin resistance associated with mortality from breast cancer? Cancer Epidemiol Biomarkers Prev. 2004;13(7):1163–72.PubMedGoogle Scholar
  31. 31.
    Sternfeld B, Weltzien E, Quesenberry CP Jr, et al. Physical activity and risk of recurrence and mortality in breast cancer survivors: findings from the LACE study. Cancer Epidemiol Biomarkers Prev. 2009;18(1):87–95. doi: 10.1158/1055-9965.epi-08-0595.PubMedCentralPubMedCrossRefGoogle Scholar
  32. 32.
    Bertram LA, Stefanick ML, Saquib N, et al. Physical activity, additional breast cancer events, and mortality among early-stage breast cancer survivors: findings from the WHEL Study. Cancer Causes Control. 2011;22(3):427–35. doi: 10.1007/s10552-010-9714-3.PubMedCentralPubMedCrossRefGoogle Scholar
  33. 33.
    Chen X, Lu W, Zheng W, et al. Exercise after diagnosis of breast cancer in association with survival. Cancer Prev Res (Phila). 2011;4(9):1409–18. doi: 10.1158/1940-6207.capr-10-0355.CrossRefGoogle Scholar
  34. 34.
    Rodriguez San Felipe MJ, Aguilar Martinez A, Manuel YKB. Influence of body weight on the prognosis of breast cancer survivors. Nutritional approach after diagnosis. Nutr Hosp. 2013;28(6):1829–41. doi: 10.3305/nutrhosp.v28in06.6981.PubMedGoogle Scholar
  35. 35.
    Etemadi A, Abnet CC, Kamangar F, et al. Impact of body size and physical activity during adolescence and adult life on overall and cause-specific mortality in a large cohort study from Iran. Eur J Epidemiol. 2014;. doi: 10.1007/s10654-014-9883-6.PubMedGoogle Scholar
  36. 36.
    Calle EE, Kaaks R. Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms. Nat Rev Cancer. 2004;4(8):579–91. doi: 10.1038/nrc1408.PubMedCrossRefGoogle Scholar
  37. 37.
    Fontein DB, de Glas NA, Duijm M, et al. Age and the effect of physical activity on breast cancer survival: a systematic review. Cancer Treat Rev. 2013;39(8):958–65. doi: 10.1016/j.ctrv.2013.03.008.PubMedCrossRefGoogle Scholar
  38. 38.
    Ligibel JA, Campbell N, Partridge A, et al. Impact of a mixed strength and endurance exercise intervention on insulin levels in breast cancer survivors. J Clin Oncol. 2008;26(6):907–12. doi: 10.1200/JCO.2007.12.7357.PubMedCrossRefGoogle Scholar
  39. 39.
    Autenrieth C, Schneider A, Doring A, et al. Association between different domains of physical activity and markers of inflammation. Med Sci Sports Exerc. 2009;41(9):1706–13. doi: 10.1249/MSS.0b013e3181a15512.PubMedCrossRefGoogle Scholar
  40. 40.
    Friedenreich CM, Neilson HK, Woolcott CG, et al. Inflammatory marker changes in a yearlong randomized exercise intervention trial among postmenopausal women. Cancer Prev Res (Phila). 2012;5(1):98–108. doi: 10.1158/1940-6207.CAPR-11-0369.CrossRefGoogle Scholar
  41. 41.
    Morris PG, Hudis CA, Giri D, et al. Inflammation and increased aromatase expression occur in the breast tissue of obese women with breast cancer. Cancer Prev Res (Phila). 2011;4(7):1021–9. doi: 10.1158/1940-6207.CAPR-11-0110.CrossRefGoogle Scholar
  42. 42.
    Cher MD, Louise AB, Charles EM, et al. Is accelerometer-measured physical activity associated with urinary estrogens and estrogen metabolites among postmenopausal women? Cancer Res. 2013;73(8 Suppl). doi: 10.1158/1538-7445.AM2013-2519.
  43. 43.
    Friedenreich CM, Woolcott CG, McTiernan A, et al. Alberta physical activity and breast cancer prevention trial: sex hormone changes in a year-long exercise intervention among postmenopausal women. J Clin Oncol. 2010;28(9):1458–66. doi: 10.1200/JCO.2009.24.9557.PubMedCentralPubMedCrossRefGoogle Scholar
  44. 44.
    Folkerd E, Dowsett M. Sex hormones and breast cancer risk and prognosis. Breast. 2013;22(Suppl 2):S38–43. doi: 10.1016/j.breast.2013.07.007.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Shanliang Zhong
    • 1
  • Tianchi Jiang
    • 2
  • Tengfei Ma
    • 1
  • Xiaohui Zhang
    • 1
  • Jinhai Tang
    • 3
  • Weixian Chen
    • 4
  • Mengmeng Lv
    • 4
  • Jianhua Zhao
    • 1
  1. 1.Center of Clinical Laboratory ScienceJiangsu Cancer Hospital Affiliated to Nanjing Medical UniversityNanjingChina
  2. 2.Clinical College of Nanjing Medical UniversityNanjingChina
  3. 3.Department of General SurgeryJiangsu Cancer Hospital Affiliated to Nanjing Medical UniversityNanjingChina
  4. 4.The Fourth Clinical College of Nanjing Medical UniversityNanjingChina

Personalised recommendations