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Epidemiology

Physical activity during adolescence and risk of colorectal adenoma later in life: results from the Nurses’ Health Study II

Abstract

Background

Physical activity during adulthood has been consistently associated with lower risk of colorectal cancers, but whether physical activity during adolescence may also play a role in colorectal carcinogenesis is unclear.

Methods

We included 28,250 women in the Nurses’ Health Study II who provided data on physical activity during adolescence (ages 12–22 years) in 1997 and underwent lower bowel endoscopy (1998–2011). We used logistic regression models for clustered data to examine the association between physical activity during adolescence and risk of adenoma later in life.

Results

Physical activity during adolescence was inversely associated with risk of colorectal adenoma (2373 cases), independent of physical activity during adulthood. The multivariable-adjusted odds ratio (OR) of adenoma was 0.89 (95% CI 0.77–1.02; Ptrend = 0.03) comparing women with ≥ 72 metabolic equivalent of tasks-hours/week (MET-h/week) to < 21 MET-h/week. Women with high physical activity during both adolescence (≥53.3 MET-h/week) and adulthood (≥23.1 MET-h/week) had significantly lower risk of adenoma (all adenomas: OR 0.76; 95% CI 0.66–0.88; advanced adenoma: OR 0.61; 95% CI 0.45–0.82) compared to women with low physical activity during both stages of life.

Conclusions

Our findings suggest that physical activity during adolescence may lower the risk of colorectal adenoma later in life.

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References

  1. 1.

    World Cancer Research Fund/American Institute for Cancer Research. Physical activity and risk of cancer. Continuous Update Project Expert Report 2018. (WCRF/AICR, London, UK, 2018).

  2. 2.

    Leslie, A., Carey, F. A., Pratt, N. R. & Steele, R. J. The colorectal adenoma-carcinoma sequence. Br. J. Surg. 89, 845–860 (2002).

  3. 3.

    Vogelstein, B., Fearon, E. R., Hamilton, S. R., Kern, S. E., Preisinger, A. C., Leppert, M. et al. Genetic alterations during colorectal-tumor development. N. Engl. J. Med. 319, 525–532 (1988).

  4. 4.

    Siegel, R. L., Miller, K. D., Fedewa, S. A., Ahnen, D. J., Meester, R. G. S., Barzi, A. et al. Colorectal cancer statistics, 2017. CA Cancer J. Clin. 67, 177–193 (2017).

  5. 5.

    Clarke, M. A. & Joshu, C. E. Early Life Exposures and Adult Cancer Risk. Epidemiol. Rev. 39, 11–27 (2017).

  6. 6.

    Nimptsch, K., Giovannucci, E., Willett, W. C., Fuchs, C. S., Wei, E. K. & Wu, K. Body fatness during childhood and adolescence, adult height, and risk of colorectal adenoma in women. Cancer Prev Res 4, 1710–1718 (2011).

  7. 7.

    Nimptsch, K., Malik, V. S., Fung, T. T., Pischon, T., Hu, F., Willett, W. et al. Dietary patterns during high school and risk of colorectal adenoma in a cohort of middle-aged women. Int. J. Cancer 134, 2458–2467 (2014).

  8. 8.

    Nimptsch, K., Bernstein, A. M., Giovannucci, E., Fuchs, C. S., Willett, W. C. & Wu, K. Dietary intakes of red meat, poultry, and fish during high school and risk of colorectal adenomas in women. Am. J. Epidemiol. 178, 172–183 (2013).

  9. 9.

    International Agency for Research on Cancer (IARC). Weight Control and Physical Activity. (IARC press, Lyon, 2002).

  10. 10.

    Rezende, L. F. M., Sá, T. H., Markozannes, G., Rey-López J. P., Lee, I. M., Tsilidis, K.K. et al. Physical activity and cancer: an umbrella review of the literature including 22 major anatomical sites and 770 000 cancer cases. Br. J. Sports Med. 52, 826–833 (2018).

  11. 11.

    Wolin, K. Y., Yan, Y. & Colditz, G. A. Physical activity and risk of colon adenoma: a meta-analysis. Br. J. Cancer 104, 882–885 (2011).

  12. 12.

    Strum, W. B. Colorectal Adenomas. N. Engl. J. Med. 374, 1065–1075 (2016).

  13. 13.

    Lee, I. M., Paffenbarger, R. S. Jr. & Hsieh, C. Physical activity and risk of developing colorectal cancer among college alumni. J. Natl. Cancer. Inst. 83, 1324–1329 (1991).

  14. 14.

    Levi, F., Pasche, C., Lucchini, F., Tavani, A. & La Vecchia, C. Occupational and leisure-time physical activity and the risk of colorectal cancer. Eur. J. Cancer Prev. 8, 487–493 (1999).

  15. 15.

    Tavani, A., Braga, C., La Vecchia, C., Conti, E., Filiberti, R., Montella, M. et al. Physical activity and risk of cancers of the colon and rectum: an Italian case-control study. Br. J. Cancer 79, 1912–1916 (1999).

  16. 16.

    Nurses’ Health Study [internet]. Available at http://nurseshealthstudy.org/. Acessed Feb 27, 2018 (2018).

  17. 17.

    Bao, Y., Bertoia, M. L., Lenart, E. B., Stampfer, M. J., Willett, W. C. & Speizer, F. E. Origin, Methods, and Evolution of the Three Nurses’ Health Studies. Am. J. Public Health 106, 1573–1581 (2016).

  18. 18.

    Ainsworth, B. E., Haskell, W. L., Herrmann, S. D., Meckes, N., Bassett, D. R. Jr., Tudor-Locke, C. et al. 2011 Compendium of Physical Activities: a second update of codes and MET values. Med. Sci. Sports. Exerc. 43, 1575–1581 (2011).

  19. 19.

    Ainsworth, B. E., Haskell, W. L., Leon, A. S., Jacobs, D. R. Jr, Montoye, H. J., Sallis, J. F. et al. Compendium of physical activities: classification of energy costs of human physical activities. Med. Sci. Sports. Exerc. 25, 71–80 (1993).

  20. 20.

    Wolf, A. M., Hunter, D. J., Colditz, G. A., Manson, J. E., Stampfer, M. J., Corsano, K. A. et al. Reproducibility and validity of a self-administered physical activity questionnaire. Int. J. Epidemiol. 23, 991–999 (1994).

  21. 21.

    Hu, F. B., Leitzmann, M. F., Stampfer, M. J., Colditz, G. A., Willett, W. C. & Rimm, E. B. Physical activity and television watching in relation to risk for type 2 diabetes mellitus in men. Arch. Intern. Med. 161, 1542–1548 (2001).

  22. 22.

    Hu, F. B., Li, T. Y., Colditz, G. A., Willett, W. C. & Manson, J. E. Television watching and other sedentary behaviors in relation to risk of obesity and type 2 diabetes mellitus in women. JAMA 289, 1785–1791 (2003).

  23. 23.

    Maruti, S. S., Willett, W. C., Feskanich, D., Rosner, B. & Colditz, G. A. A prospective study of age-specific physical activity and premenopausal breast cancer. J. Natl Cancer. Inst. 100, 728–737 (2008).

  24. 24.

    Baer, H. J., Schnitt, S. J., Connolly, J. L., Byrne, C., Willett, W. C., Rosner, B. et al. Early life factors and incidence of proliferative benign breast disease. Cancer Epidemiol. Biomarkers. Prev. 14, 2889–2897 (2005).

  25. 25.

    Jacobs, D. R. Jr., Ainsworth, B. E., Hartman, T. J. & Leon, A. S. A simultaneous evaluation of 10 commonly used physical activity questionnaires. Med Sci Sports Exerc 25, 81–91 (1993).

  26. 26.

    Chasan-Taber, S., Rimm, E. B., Stampfer, M. J., Spiegelman, D., Colditz, G. A., Giovannucci, E. et al. Reproducibility and validity of a self-administered physical activity questionnaire for male health professionals. Epidemiology 7, 81–86 (1996).

  27. 27.

    Yuan, C., Spiegelman, D., Rimm, E. B., Rosner, B. A., Stampfer, M. J., Barnett, J. B. et al. Relative validity of nutrient intakes assessed by questionnaire, 24-hour recalls, and diet records as compared with urinary recovery and plasma concentration biomarkers: findings for women. Am. J. Epidemiol. 187, 1051–1063 (2018).

  28. 28.

    Yuan, C., Spiegelman, D., Rimm, E. B., Rosner, B. A., Stampfer, M. J., Barnett, J. B. et al. Validity of a Dietary Questionnaire Assessed by Comparison With Multiple Weighed Dietary Records or 24-Hour Recalls. Am. J. Epidemiol. 185, 570–584 (2017).

  29. 29.

    Maruti, S.S., Feskanich, D., Rockett, H.R., Colditz, G.A., Sampson, L.A. & Willett, W.C. Validation of adolescent diet recalled by adults. Epidemiology 4, 226–229 (2006).

  30. 30.

    East, J. E., Vieth, M. & Rex, D. K. Serrated lesions in colorectal cancer screening: detection, resection, pathology and surveillance. Gut 64, 991–1000 (2015).

  31. 31.

    Therneau, T. M. & Grambsch, P. M. Modeling Survival Data: Extending the Cox Model. (Springer, New York, 2000).

  32. 32.

    World Health Organization (WHO). Global Recommendations on Physical Activity for Health. (World Health Organization, Geneva, 2010).

  33. 33.

    Bibbins-Domingo, K., Grossman, D. C., Curry, S. J., Davidson, K. W., Epling, J. W. Jr., García, F. A. R. et al. Screening for Colorectal Cancer: US Preventive Services Task Force Recommendation Statement. JAMA 315, 2564–2575 (2016).

  34. 34.

    Johns, L. E. & Houlston, R. S. A systematic review and meta-analysis of familial colorectal cancer risk. Am. J. Gastroenterol. 96, 2992–3003 (2001).

  35. 35.

    McTiernan, A. Mechanisms linking physical activity with cancer. Nat. Rev. Cancer 8, 205–211 (2008).

  36. 36.

    Giovannucci, E. A framework to understand diet, physical activity, body weight, and cancer risk. Cancer Causes Control. https://doi.org/10.1007/s10552-017-0975-y (2018). Epub ahead of print 9 Nov 2017.

  37. 37.

    Friedenreich, C. M. & Orenstein, M. R. Physical activity and cancer prevention: etiologic evidence and biological mechanisms. J. Nutr. 132, 3456S–3464S (2002).

  38. 38.

    Giovannucci, E. Insulin, insulin-like growth factors and colon cancer: a review of the evidence. J. Nutr. 131, 3109S–3120S (2001).

  39. 39.

    Yoon, Y. S., Keum, N., Zhang, X., Cho, E. & Giovannucci, E. L. Hyperinsulinemia, insulin resistance and colorectal adenomas: A meta-analysis. Metabolism 64, 1324–1333 (2015).

  40. 40.

    Verheggen, R. J., Maessen, M. F., Green, D. J., Hermus, A. R., Hopman, M. T. & Thijssen, D. H. A systematic review and meta-analysis on the effects of exercise training versus hypocaloric diet: distinct effects on body weight and visceral adipose tissue. Obes. Rev. 17, 664–690 (2016).

  41. 41.

    Clarke, S. F., Murphy, E. F., O’Sullivan, O., Lucey, A. J., Humphreys, M., Hogan, A. et al. Exercise and associated dietary extremes impact on gut microbial diversity. Gut 63, 1913–1920 (2014).

  42. 42.

    O’Sullivan, O., Cronin, O., Clarke, S. F., Murphy, E. F., Molloy, E. F., Shanahan, F. et al. Exercise and the microbiota. Gut Microbes 6, 131–136 (2015).

  43. 43.

    Blottière, H. M. The gut microbiota and obesity. In: Energy Balancer and Obesity (eds. Romieu, I., Dossus, L. & Willet, W. C.) 89–94 (IARC press, Lyon, 2017).

  44. 44.

    Boyle, T., Keegel, T., Bull, F., Heyworth, J. & Fritschi, L. Physical activity and risks of proximal and distal colon cancers: a systematic review and meta-analysis. J. Natl. Cancer. Inst. 104, 1548–1561 (2012).

  45. 45.

    Murphy, N., Ward, H. A., Jenab, M., Rothwell, J. A., Boutron-Ruault, M.-C., Carbonnel, F. et al. Heterogeneity of colorectal cancer risk factors by anatomical subsite in 10 european countries: a multinational cohort study. Clin. Gastroenterol. Hepatol. https://doi.org/10.1016/j.cgh.2018.07.030 (2018).

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Acknowledgements

The authors would like to thank the Channing Division of Network Medicine, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School. The authors would like to thank the participants and staff of the Nurses’ Health Study II for their valuable contributions as well as the following state cancer registries for their help: AL, AZ, AR, CA, CO, CT, DE, FL, GA, ID, IL, IN, IA, KY, LA, ME, MD, MA, MI, NE, NH, NJ, NY, NC, ND, OH, OK, OR, PA, RI, SC, TN, TX, VA, WA and WY. The authors assume full responsibility for analyses and interpretation of these data. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Author information

L.F.M.R., D.H.L. and N.K. had full access to all of the data and take responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: L.F.M.R., D.H.L., N.K., E.G., K.W. Acquisition, analysis or interpretation of data: L.F.M.R., D.H.L., N.K., E.G., K.W., K.N., M.S., I.L., J.E.N., S.O., C.F., J.M., A.T.C., W.W. Drafting of manuscript: L.F.M.R., D.H.L. Critical revision of the manuscript for important intellectual content: all authors. Statistical analysis: L.F.M.R., D.H.L. and N.K. Obtained funding: W.W. and K.W. Study supervision: K.W. 

Correspondence to NaNa Keum.

Ethics declarations

Competing interests

Dr. Fuchs reports consulting role for Agios, Bain Capital, Bayer, Celgene, Dicerna, Five Prime Therapeutics, Gilead Sciences, Eli Lilly, Entrinsic Health, Genentech, KEW, Merck, Merrimack Pharmaceuticals, Pfizer, Sanofi, Taiho, and Unum Therapeutics. He also serves as a Director for CytomX Therapeutics and owns unexercised stock options for CytomX and Entrinsic Health. Dr. Meyerhardt reports consulting role for Ignyta, COTA, Taiho Pharmaceutical (all <$5 K). All other authors declare no competing interests relevant in relation to the work described.

Ethics approval and consent to participate

The study protocol was approved by the institutional review boards of the Brigham and Women’s Hospital and Harvard T.H. Chan School of Public Health, and those of participating registries as required. Completion of the questionnaire was considered to imply informed consent.

Consent to publish

Not applicable.

Data availability

Further information including the procedures to obtain and access data from the Nurses' Health Study and Health Professionals Follow-up Study is described at https://www.nurseshealthstudy.org/researchers (email: nhsaccess@channing.harvard.edu) and https://sites.sph.harvard.edu/hpfs/for-collaborators.

Note

This work is published under the standard license to publish agreement. After 12 months the work will become freely available and the license terms will switch to a Creative Commons Attribution 4.0 International (CC BY 4.0).

Funding

The Nurses’ Health Study II was funded by the National Cancer Institute (NCI), National Institutes of Health (UM1 CA176726 to WW). Leandro Fórnias Machado de Rezende receives a doctoral fellowship from the Coordination for the Improvement of Higher Education Personnel (CAPES) and the Sao Paulo Research Foundation (FAPESP), grant #2016/21390–0 and #2014/25614-4. NCI grants R03 CA197879 to KW, R21 CA222940 to K.W. and Reiko Nishihara, R21 CA230873 to K.W. and S.O., R35 CA197735 to S.O., P50 CA127003 to C.S.F. The American Cancer Society (grant number MRSG-17-220-01 – NEC to M.S.). The National Institutes of Health grants K99 CA215314 and R00 CA215314 to M.S. N.K. was supported by grants from the National Research Foundation of Korea (NRF-2018R1C1B6008822; NRF-2018R1A4A1022589); the Dongguk University Research Grant of 2017. This work was also in part supported by an Investigator Initiated Grant from the American Institute for Cancer Research (AICR) to KW.

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