Tumor Biology

, Volume 35, Issue 11, pp 11065–11073 | Cite as

Nonoccupational physical activity and risk of ovarian cancer: a meta-analysis

  • Shanliang Zhong
  • Lin Chen
  • Mengmeng Lv
  • Tengfei Ma
  • Xiaohui Zhang
  • Jianhua Zhao
Research Article

Abstract

Previous studies concerning the association between nonoccupational physical activity (PA) and risk of ovarian cancer yielded mixed results. We investigated the association by performing a meta-analysis. Relevant studies were identified by searching PubMed and EMBASE to June 2014. We calculated the summary relative risks (RRs) 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. Nine cohort studies and ten case–control studies involving 730,703 participants and 9,459 cases of ovarian cancer were selected for meta-analysis. The analyses showed that individuals who participated in any amount of nonoccupational PA had a RR of 0.92 (95 % CI = 0.84–1.00) for risk of ovarian cancer. Those who participated in high or moderate nonoccupational PA had a RR of ovarian cancer risk of 0.89 (95 % CI = 0.79–1.01) and 0.91 (95 % CI = 0.85–0.99), respectively. Stratifying by study design and cancer subtype (borderline and invasive tumors), inverse association was only found in case–control studies. A linear but not significant dose–response relationship was found between nonoccupational PA and ovarian cancer risk. In conclusion, a weak inverse association exists between nonoccupational PA and the risk of ovarian cancer. Regarding the significant heterogeneity among included studies, confirmation in further prospective cohort studies with more accurate assessment of PA level is essential.

Keywords

Physical activity Exercise Ovarian Cancer Incidence 

Notes

Acknowledgments

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

Conflicts of interest

None

Supplementary material

13277_2014_2385_MOESM1_ESM.xls (26 kb)
Table S1 Methodological quality of the case-control studies, based on the NOS for assessing the quality of epidemiological studies. (XLS 26 kb)
13277_2014_2385_MOESM2_ESM.xls (20 kb)
Table S2 Methodological quality of the cohort studies, based on the NOS for assessing the quality of epidemiological studies. (XLS 20 kb)

References

  1. 1.
    Sankaranarayanan R, Ferlay J. Worldwide burden of gynaecological cancer: the size of the problem. Best Pract Res Clin Obstet Gynaecol. 2006;20(2):207–25. doi: 10.1016/j.bpobgyn.2005.10.007.PubMedCrossRefGoogle Scholar
  2. 2.
    Sueblinvong T, Carney ME. Current understanding of risk factors for ovarian cancer. Curr Treat Options Oncol. 2009;10(1–2):67–81. doi: 10.1007/s11864-009-0108-2.PubMedCrossRefGoogle Scholar
  3. 3.
    Olsen CM, Bain CJ, Jordan SJ, Nagle CM, Green AC, Whiteman DC, et al. Recreational physical activity and epithelial ovarian cancer: a case-control study, systematic review, and meta-analysis. Cancer Epidemiol Biomarkers Prev. 2007;16(11):2321–30. doi: 10.1158/1055-9965.EPI-07-0566.PubMedCrossRefGoogle Scholar
  4. 4.
    Wells G, Shea B, O’Connell D, Robertson J, Peterson J, Welch V et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. www.ohri.ca/programs/clinical_epidemiology/oxford_web.ppt. 2010.
  5. 5.
    Rossing MA, Cushing-Haugen KL, Wicklund KG, Doherty JA, Weiss NS. Recreational physical activity and risk of epithelial ovarian cancer. Cancer Causes Control CCC. 2010;21(4):485–91. doi: 10.1007/s10552-009-9479-8.PubMedCentralPubMedCrossRefGoogle Scholar
  6. 6.
    DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7(3):177–88. doi: 10.1016/0197-2456(86)90046-2.PubMedCrossRefGoogle Scholar
  7. 7.
    Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21(11):1539–58. doi: 10.1002/sim.1186.PubMedCrossRefGoogle Scholar
  8. 8.
    Hedges LV, Pigott TD. The power of statistical tests in meta-analysis. Psychol Methods. 2001;6(3):203–17.PubMedCrossRefGoogle Scholar
  9. 9.
    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
  10. 10.
    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
  11. 11.
    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
  12. 12.
    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
  13. 13.
    Bertone ER, Newcomb PA, Willett WC, Stampfer MJ, Egan KM. Recreational physical activity and ovarian cancer in a population-based case-control study. Int J Cancer. 2002;99(3):431–6. doi: 10.1002/ijc.10365.PubMedCrossRefGoogle Scholar
  14. 14.
    Patel AV, Rodriguez C, Pavluck AL, Thun MJ, Calle EE. Recreational physical activity and sedentary behavior in relation to ovarian cancer risk in a large cohort of US women. Am J Epidemiol. 2006;163(8):709–16. doi: 10.1093/aje/kwj098.PubMedCrossRefGoogle Scholar
  15. 15.
    Lee AH, Su D, Pasalich M, Wong YL, Binns CW. Habitual physical activity reduces risk of ovarian cancer: a case-control study in southern China. Prev Med. 2013;57(Suppl):S31–3. doi: 10.1016/j.ypmed.2012.11.009.PubMedCrossRefGoogle Scholar
  16. 16.
    Moorman PG, Jones LW, Akushevich L, Schildkraut JM. Recreational physical activity and ovarian cancer risk and survival. Ann Epidemiol. 2011;21(3):178–87. doi: 10.1016/j.annepidem.2010.10.014.PubMedCentralPubMedCrossRefGoogle Scholar
  17. 17.
    Bertone ER, Willett WC, Rosner BA, Hunter DJ, Fuchs CS, Speizer FE, et al. Prospective study of recreational physical activity and ovarian cancer. J Natl Cancer Inst. 2001;93(12):942–8.PubMedCrossRefGoogle Scholar
  18. 18.
    Riman T, Dickman PW, Nilsson S, Nordlinder H, Magnusson CM, Persson IR. Some life-style factors and the risk of invasive epithelial ovarian cancer in Swedish women. Eur J Epidemiol. 2004;19(11):1011–9.PubMedCrossRefGoogle Scholar
  19. 19.
    Biesma RG, Schouten LJ, Dirx MJ, Goldbohm RA, van den Brandt PA. Physical activity and risk of ovarian cancer: results from the Netherlands Cohort Study (The Netherlands). Cancer Causes Control CCC. 2006;17(1):109–15. doi: 10.1007/s10552-005-0422-3.PubMedCrossRefGoogle Scholar
  20. 20.
    Mink PJ, Folsom AR, Sellers TA, Kushi LH. Physical activity, waist-to-hip ratio, and other risk factors for ovarian cancer: a follow-up study of older women. Epidemiol (Cambridge, Mass). 1996;7(1):38–45.CrossRefGoogle Scholar
  21. 21.
    Zhang M, Holman CD, Binns CW. Intake of specific carotenoids and the risk of epithelial ovarian cancer. Br J Nutr. 2007;98(1):187–93. doi: 10.1017/s0007114507690011.PubMedCrossRefGoogle Scholar
  22. 22.
    Leitzmann MF, Koebnick C, Moore SC, Danforth KN, Brinton LA, Hollenbeck AR, et al. Prospective study of physical activity and the risk of ovarian cancer. Cancer Causes Control CCC. 2009;20(5):765–73. doi: 10.1007/s10552-008-9291-x.PubMedCentralPubMedCrossRefGoogle Scholar
  23. 23.
    Sanchez-Zamorano LM, Salazar-Martinez E, Escudero-De Los Rios P, Gonzalez-Lira G, Flores-Luna L, Lazcano-Ponce EC. Factors associated with non-epithelial ovarian cancer among Mexican women: a matched case-control study. Int J Gynecol Cancer. 2003;13(6):756–63.PubMedCrossRefGoogle Scholar
  24. 24.
    Zhang M, Lee AH, Binns CW. Physical activity and epithelial ovarian cancer risk: a case-control study in China. Int J Cancer. 2003;105(6):838–43. doi: 10.1002/ijc.11165.PubMedCrossRefGoogle Scholar
  25. 25.
    Hannan LM, Leitzmann MF, Lacey Jr JV, Colbert LH, Albanes D, Schatzkin A, et al. Physical activity and risk of ovarian cancer: a prospective cohort study in the United States. Cancer Epidemiol Biomarkers Prev. 2004;13(5):765–70.PubMedGoogle Scholar
  26. 26.
    Xiao Q, Yang HP, Wentzensen N, Hollenbeck A, Matthews CE. Physical activity in different periods of life, sedentary behavior, and the risk of ovarian cancer in the NIH-AARP diet and health study. Cancer Epidemiol Biomarkers Prev. 2013;22(11):2000–8. doi: 10.1158/1055-9965.epi-13-0154.PubMedCrossRefGoogle Scholar
  27. 27.
    Dosemeci M, Hayes RB, Vetter R, Hoover RN, Tucker M, Engin K, et al. Occupational physical activity, socioeconomic status, and risks of 15 cancer sites in Turkey. Cancer Causes Control CCC. 1993;4(4):313–21.PubMedCrossRefGoogle Scholar
  28. 28.
    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(5):369–76.PubMedCrossRefGoogle Scholar
  29. 29.
    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(11):3620–4.PubMedCrossRefGoogle Scholar
  30. 30.
    Pieta B, Chmaj-Wierzchowska K, Opala T. Life style and risk of development of breast and ovarian cancer. Ann Agric Environ AAEM. 2012;19(3):379–84.Google Scholar
  31. 31.
    Anderson JP, Ross JA, Folsom AR. Anthropometric variables, physical activity, and incidence of ovarian cancer: the Iowa Women’s Health Study. Cancer. 2004;100(7):1515–21. doi: 10.1002/cncr.20146.PubMedCrossRefGoogle Scholar
  32. 32.
    Schnohr P, Gronbaek M, Petersen L, Hein HO, Sorensen TI. Physical activity in leisure-time and risk of cancer: 14-year follow-up of 28,000 Danish men and women. Scand J Public Health. 2005;33(4):244–9. doi: 10.1080/14034940510005752.PubMedCrossRefGoogle Scholar
  33. 33.
    Weiderpass E, Margolis KL, Sandin S, Braaten T, Kumle M, Adami HO, et al. Prospective study of physical activity in different periods of life and the risk of ovarian cancer. Int J Cancer. 2006;118(12):3153–60. doi: 10.1002/ijc.21800.PubMedCrossRefGoogle Scholar
  34. 34.
    Lahmann PH, Friedenreich C, Schulz M, Cust AE, Lukanova A, Kaaks R, et al. Physical activity and ovarian cancer risk: the European Prospective Investigation into Cancer and Nutrition. Cancer Epidemiol Biomarkers Prev. 2009;18(1):351–4. doi: 10.1158/1055-9965.epi-08-0958.PubMedCrossRefGoogle Scholar
  35. 35.
    Chionh F, Baglietto L, Krishnan K, English DR, MacInnis RJ, Gertig DM, et al. Physical activity, body size and composition, and risk of ovarian cancer. Cancer Causes Control CCC. 2010;21(12):2183–94. doi: 10.1007/s10552-010-9638-y.PubMedCrossRefGoogle Scholar
  36. 36.
    Weiderpass E, Sandin S, Inoue M, Shimazu T, Iwasaki M, Sasazuki S, et al. Risk factors for epithelial ovarian cancer in Japan—results from the Japan Public Health Center-based prospective study cohort. Int J Oncol. 2012;40(1):21–30. doi: 10.3892/ijo.2011.1194.PubMedGoogle Scholar
  37. 37.
    Carnide N, Kreiger N, Cotterchio M. Association between frequency and intensity of recreational physical activity and epithelial ovarian cancer risk by age period. Eur J Cancer Prev. 2009;18(4):322–30. doi: 10.1097/CEJ.0b013e32832bf3fa.PubMedCrossRefGoogle Scholar
  38. 38.
    Pan SY, Ugnat AM, Mao Y. Physical activity and the risk of ovarian cancer: a case-control study in Canada. Int J Cancer. 2005;117(2):300–7. doi: 10.1002/ijc.21157.PubMedCrossRefGoogle Scholar
  39. 39.
    Tavani A, Gallus S, La Vecchia C, Dal Maso L, Negri E, Pelucchi C, et al. Physical activity and risk of ovarian cancer: an Italian case-control study. Int J Cancer. 2001;91(3):407–11.PubMedCrossRefGoogle Scholar
  40. 40.
    Cottreau CM, Ness RB, Kriska AM. Physical activity and reduced risk of ovarian cancer. Obstet Gynecol. 2000;96(4):609–14.PubMedCrossRefGoogle Scholar
  41. 41.
    Cust AE. Physical activity and gynecologic cancer prevention. Recent Results Cancer Res. 2011;186:159–85. doi: 10.1007/978-3-642-04231-7_7.PubMedCrossRefGoogle Scholar
  42. 42.
    Autenrieth C, Schneider A, Doring A, Meisinger C, Herder C, Koenig W, 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
  43. 43.
    Kaaks R, Lukanova A, Kurzer MS. Obesity, endogenous hormones, and endometrial cancer risk: a synthetic review. Cancer Epidemiol Biomarkers Prev. 2002;11(12):1531–43.PubMedGoogle Scholar
  44. 44.
    Modugno F, Ness RB, Chen C, Weiss NS. Inflammation and endometrial cancer: a hypothesis. Cancer Epidemiol Biomarkers Prev. 2005;14(12):2840–7. doi: 10.1158/1055-9965.EPI-05-0493.PubMedCrossRefGoogle Scholar
  45. 45.
    Brown JC, Winters-Stone K, Lee A, Schmitz KH. Cancer, physical activity, and exercise. Compr Phys. 2012;2(4):2775–809. doi: 10.1002/cphy.c120005.Google Scholar
  46. 46.
    Kruk J, Czerniak U. Physical activity and its relation to cancer risk: updating the evidence. Asian Pac J Cancer Prev. 2013;14(7):3993–4003.PubMedCrossRefGoogle Scholar

Copyright information

© International Society of Oncology and BioMarkers (ISOBM) 2014

Authors and Affiliations

  • Shanliang Zhong
    • 1
  • Lin Chen
    • 2
  • Mengmeng Lv
    • 3
  • Tengfei Ma
    • 1
  • Xiaohui Zhang
    • 1
  • Jianhua Zhao
    • 1
  1. 1.Center of Clinical Laboratory ScienceJiangsu Cancer Hospital Affiliated to Nanjing Medical UniversityNanjingChina
  2. 2.Departments of OncologyXuzhou Medical CollegeXuzhouChina
  3. 3.The Fourth Clinical CollegeNanjing Medical UniversityNanjingChina

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