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Physical activity, diabetes, and risk of thyroid cancer: a systematic review and meta-analysis

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Abstract

Thyroid cancer incidence has been increasing more rapidly over time than the occurrence of cancers of other sites, and interest in potential adverse relations of diabetes and lack of physical activity to thyroid cancer risk is accumulating. We conducted a systematic review and meta-analysis of published epidemiologic studies on the relations of physical activity and diabetes to thyroid cancer according to the Meta-analysis of Observational Studies in Epidemiology guidelines. Published studies were identified through a search in MEDLINE and EMBASE. Random-effects models were used to summarize thyroid cancer risk estimates comparing high versus low levels of physical activity, and separately, comparing individuals with diabetes versus those without diabetes. Meta-regression analyses were performed to evaluate potential effect modification by study design and thyroid cancer risk factors. Information was extracted from seven studies of physical activity and thyroid cancer and from six studies of diabetes and thyroid cancer. The number of individuals from studies on physical activity was 939,305 (yielding 2,250 incident thyroid cancer cases) and from studies on diabetes it was 960,840 (yielding 1,230 cases). The summary relative risk (RR) estimate from cohort and case–control studies combined indicated no association between physical activity and thyroid cancer (summary RR 1.06, 95 % confidence interval (CI) 0.79–1.42). Subgroup-analyses revealed a significant positive association between physical activity and thyroid cancer in cohort studies (summary RR 1.28; 95 % CI 1.01–1.63), whereas the relation was suggestively inverse in case–control studies (summary RR 0.70; 95 % CI 0.48–1.03; p for heterogeneity = 0.005). Individuals with diabetes showed a borderline statistically significant increased risk of thyroid cancer compared with those without diabetes (summary RR 1.17; 95 % CI 0.99–1.39). The relations of physical activity and diabetes to thyroid cancer were not modified by sex, number of adjustment factors, and adjustments for adiposity, smoking, and study quality. In this comprehensive systematic review and meta-analysis, no significant association between physical activity and thyroid cancer was found. Diabetes showed a suggestive positive relation with risk of thyroid cancer.

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References

  1. Kilfoy BA, Devesa SS, Ward MH, Zhang YW, Rosenberg PS, Holford TR, et al. Gender is an age-specific effect modifier for papillary cancers of the thyroid gland. Cancer Epidemiol Biomar. 2009;18(4):1092–100. doi:10.1158/1055-9965.Epi-08-0976.

    Article  Google Scholar 

  2. Kent WD, Hall SF, Isotalo PA, Houlden RL, George RL, Groome PA. Increased incidence of differentiated thyroid carcinoma and detection of subclinical disease. CMAJ. 2007;177(11):1357–61. doi:10.1503/cmaj.061730.

    Article  PubMed  Google Scholar 

  3. Centers for Disease Control and Prevention (CDC). Facts about physical activity. http://www.cdc.gov/physicalactivity/data/facts.html. Accessed 16 Mar 2013.

  4. King H, Aubert RE, Herman WH. Global burden of diabetes, 1995–2025: prevalence, numerical estimates, and projections. Diabetes Care. 1998;21(9):1414–31.

    Article  PubMed  CAS  Google Scholar 

  5. Zhao ZG, Guo XG, Ba CX, Wang W, Yang YY, Wang J, et al. Overweight, obesity and thyroid cancer risk: a meta-analysis of cohort studies. J Int Med Res. 2012;40(6):2041–50.

    Article  PubMed  CAS  Google Scholar 

  6. Renehan AG, Tyson M, Egger M, Heller RF, Zwahlen M. Body-mass index and incidence of cancer: a systematic review and meta-analysis of prospective observational studies. Lancet. 2008;371(9612):569–78. doi:10.1016/S0140-6736(08)60269-X.

    Article  PubMed  Google Scholar 

  7. Kitahara CM, Platz EA, Freeman LE, Hsing AW, Linet MS, Park Y, et al. Obesity and thyroid cancer risk among U.S. men and women: a pooled analysis of five prospective studies. Cancer Epidemiol Biomarkers Prev. 2011;20(3):464–72. doi:10.1158/1055-9965.EPI-10-1220.

    Article  PubMed  Google Scholar 

  8. Kolonel LN, Hankin JH, Wilkens LR, Fukunaga FH, Hinds MW. An epidemiologic study of thyroid cancer in Hawaii. Cancer Causes Control. 1990;1(3):223–34.

    Article  PubMed  CAS  Google Scholar 

  9. Lee SM, Kwak KH. Risk factors and a predictive model for thyroid cancer in Korean women. Cancer Nurs. 2010;33(4):310–9. doi:10.1097/NCC.0b013e3181cd2844.

    Article  PubMed  Google Scholar 

  10. Rossing MA, Remler R, Voigt LF, Wicklund KG, Daling JR. Recreational physical activity and risk of papillary thyroid cancer (United States). Cancer Causes Control. 2001;12(10):881–5.

    Article  PubMed  CAS  Google Scholar 

  11. Kitahara CM, Platz EA, Beane Freeman LE, Black A, Hsing AW, Linet MS, et al. Physical activity, diabetes, and thyroid cancer risk: a pooled analysis of five prospective studies. Cancer Causes Control. 2012. doi:10.1007/s10552-012-9896-y.

  12. Kabat GC, Kim MY, Thomson CA, Luo J, Wactawski-Wende J, Rohan TE. Anthropometric factors and physical activity and risk of thyroid cancer in postmenopausal women. Cancer Causes Control. 2012;23(3):421–30. doi:10.1007/s10552-011-9890-9.

    Article  PubMed  Google Scholar 

  13. Robsahm TE, Hestvik UE, Veierod MB, Fagerlie A, Nystad W, Engebretsen L, et al. Cancer risk in Norwegian world class athletes. Cancer Causes Control. 2010;21(10):1711–9. doi:10.1007/s10552-010-9600-z.

    Article  PubMed  Google Scholar 

  14. Cash SW, Ma H, Horn-Ross PL, Reynolds P, Canchola AJ, Sullivan-Halley J, et al. Recreational physical activity and risk of papillary thyroid cancer among women in the California Teachers Study. Cancer Epidemiol. 2013;37(1):46–53. doi:10.1016/j.canep.2012.09.003.

    Article  PubMed  Google Scholar 

  15. Inoue M, Iwasaki M, Otani T, Sasazuki S, Noda M, Tsugane S. Diabetes mellitus and the risk of cancer: results from a large-scale population-based cohort study in Japan. Arch Intern Med. 2006;166(17):1871–7. doi:10.1001/archinte.166.17.1871.

    Article  PubMed  Google Scholar 

  16. Wideroff L, Gridley G, Mellemkjaer L, Chow WH, Linet M, Keehn S, et al. Cancer incidence in a population-based cohort of patients hospitalized with diabetes mellitus in Denmark. J Natl Cancer Inst. 1997;89(18):1360–5.

    Article  PubMed  CAS  Google Scholar 

  17. Chodick G, Heymann AD, Rosenmann L, Green MS, Flash S, Porath A, et al. Diabetes and risk of incident cancer: a large population-based cohort study in Israel. Cancer Causes Control. 2010;21(6):879–87. doi:10.1007/s10552-010-9515-8.

    Article  PubMed  Google Scholar 

  18. Adami HO, McLaughlin J, Ekbom A, Berne C, Silverman D, Hacker D, et al. Cancer risk in patients with diabetes mellitus. Cancer Causes Control. 1991;2(5):307–14.

    Article  PubMed  CAS  Google Scholar 

  19. Kuriki K, Hirose K, Tajima K. Diabetes and cancer risk for all and specific sites among Japanese men and women. Eur J Cancer Prev Off J Eur Cancer Prev Org. 2007;16(1):83–9. doi:10.1097/01.cej.0000228404.37858.40.

    Article  Google Scholar 

  20. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of Observational Studies in Epidemiology (MOOSE) group. JAMA, J Am Med Assoc. 2000;283(15):2008–12.

    Article  CAS  Google Scholar 

  21. Wells SB, O’Connell D, Peterson J, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomized studies in meta-analyses. www.ohri.ca/programs/clinical_epidemiology/oxford.asp. Accessed 16 Mar 2013.

  22. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21(11):1539–58. doi:10.1002/sim.1186.

    Article  PubMed  Google Scholar 

  23. 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.

    Article  PubMed  CAS  Google Scholar 

  24. Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50(4):1088–101.

    Article  PubMed  CAS  Google Scholar 

  25. Viechtbauer W. Conducting meta-analyses in R with the metafor package. J Stat Softw. 2010;36(3):1–48.

    Google Scholar 

  26. Leitzmann MF, Brenner A, Moore SC, Koebnick C, Park Y, Hollenbeck A, et al. Prospective study of body mass index, physical activity and thyroid cancer. Int J Cancer. 2010;126(12):2947–56. doi:10.1002/ijc.24913.

    PubMed  CAS  Google Scholar 

  27. Meinhold CL, Ron E, Schonfeld SJ, Alexander BH, Freedman DM, Linet MS, et al. Nonradiation risk factors for thyroid cancer in the US Radiologic Technologists Study. Am J Epidemiol. 2010;171(2):242–52. doi:10.1093/aje/kwp354kwp354.

    Article  PubMed  Google Scholar 

  28. Marcello MA, Sampaio AC, Geloneze B, Vasques AC, Assumpcao LV, Ward LS. Obesity and excess protein and carbohydrate consumption are risk factors for thyroid cancer. Nutr Cancer. 2012;64(8):1190–5. doi:10.1080/01635581.2012.721154.

    Article  PubMed  CAS  Google Scholar 

  29. Aschebrook-Kilfoy B, Sabra MM, Brenner A, Moore SC, Ron E, Schatzkin A, et al. Diabetes and thyroid cancer risk in the National Institutes of Health-AARP Diet and Health Study. Thyroid Off J Am Thyroid Assoc. 2011;21(9):957–63. doi:10.1089/thy.2010.0396.

    Article  Google Scholar 

  30. Tseng CH. Thyroid cancer risk is not increased in diabetic patients. PLoS ONE. 2012;7(12):e53096. doi:10.1371/journal.pone.0053096.

    Article  PubMed  CAS  Google Scholar 

  31. Chiou WK, Huang BY, Chou WY, Weng HF, Lin JD. Incidences of cancers in diabetic and non-diabetic hospitalized adult patients in Taiwan. Asian Pac J Cancer Prev APJCP. 2011;12(6):1577–81.

    Google Scholar 

  32. Lee MY, Lin KD, Hsiao PJ, Shin SJ. The association of diabetes mellitus with liver, colon, lung, and prostate cancer is independent of hypertension, hyperlipidemia, and gout in Taiwanese patients. Metabolism. 2012;61(2):242–9. doi:10.1016/j.metabol.2011.06.020.

    Article  PubMed  CAS  Google Scholar 

  33. Ismail I, Keating SE, Baker MK, Johnson NA. A systematic review and meta-analysis of the effect of aerobic vs. resistance exercise training on visceral fat. Obes Rev. 2012;13(1):68–91. doi:10.1111/j.1467-789X.2011.00931.x.

    Article  PubMed  CAS  Google Scholar 

  34. Shih SR, Chiu WY, Chang TC, Tseng CH. Diabetes and thyroid cancer risk: literature review. Exp Diabetes Res. 2012;2012:578285. doi:10.1155/2012/578285.

    Article  PubMed  Google Scholar 

  35. La Vecchia C, Ron E, Franceschi S, Dal Maso L, Mark SD, Chatenoud L, et al. A pooled analysis of case-control studies of thyroid cancer. III. Oral contraceptives, menopausal replacement therapy and other female hormones. Cancer Causes Control. 1999;10(2):157–66.

    Article  PubMed  Google Scholar 

  36. Mitsiades N, Pazaitou-Panayiotou K, Aronis KN, Moon HS, Chamberland JP, Liu X, et al. Circulating adiponectin is inversely associated with risk of thyroid cancer: in vivo and in vitro studies. J Clin Endocrinol Metab. 2011;96(12):E2023–8. doi:10.1210/jc.2010-1908jc.2010-1908.

    Article  PubMed  CAS  Google Scholar 

  37. Sigurdson AJ, Hauptmann M, Alexander BH, Doody MM, Thomas CB, Struewing JP, et al. DNA damage among thyroid cancer and multiple cancer cases, controls, and long-lived individuals. Mutat Res. 2005;586(2):173–88. doi:10.1016/j.mrgentox.2005.07.001.

    Article  PubMed  CAS  Google Scholar 

  38. Sato Y, Nanri H, Ohta M, Kasai H, Ikeda M. Increase of human MTH1 and decrease of 8-hydroxydeoxyguanosine in leukocyte DNA by acute and chronic exercise in healthy male subjects. Biochem Biophys Res Commun. 2003;305(2):333–8.

    Article  PubMed  CAS  Google Scholar 

  39. Rundle A. Molecular epidemiology of physical activity and cancer. Cancer Epidemiol Biomarkers Prev. 2005;14(1):227–36.

    PubMed  Google Scholar 

  40. Ludlow AT, Zimmerman JB, Witkowski S, Hearn JW, Hatfield BD, Roth SM. Relationship between physical activity level, telomere length, and telomerase activity. Med Sci Sports Exerc. 2008;40(10):1764–71. doi:10.1249/MSS.0b013e31817c92aa.

    Article  PubMed  CAS  Google Scholar 

  41. Ivanov MK, Akushevich I, Gorski AI, Korelo AM, Kravchenko JS, Maksioutov MA, Tsyb AF. Risk of thyroid cancer after irradiation in children and adults. Curr Oncol. 2005;12(2):55–64.

    Google Scholar 

  42. Wang C, Wang X, Gong G, Ben Q, Qiu W, Chen Y, et al. Increased risk of hepatocellular carcinoma in patients with diabetes mellitus: a systematic review and meta-analysis of cohort studies. Int J Cancer. 2012;130(7):1639–48. doi:10.1002/ijc.26165.

    Article  PubMed  CAS  Google Scholar 

  43. Ben Q, Xu M, Ning X, Liu J, Hong S, Huang W, et al. Diabetes mellitus and risk of pancreatic cancer: a meta-analysis of cohort studies. Eur J Cancer. 2011;47(13):1928–37. doi:10.1016/j.ejca.2011.03.003.

    Article  PubMed  Google Scholar 

  44. Friberg E, Orsini N, Mantzoros CS, Wolk A. Diabetes mellitus and risk of endometrial cancer: a meta-analysis. Diabetologia. 2007;50(7):1365–74. doi:10.1007/s00125-007-0681-5.

    Article  PubMed  CAS  Google Scholar 

  45. Deng L, Gui Z, Zhao L, Wang J, Shen L. Diabetes mellitus and the incidence of colorectal cancer: an updated systematic review and meta-analysis. Dig Dis Sci. 2012;57(6):1576–85. doi:10.1007/s10620-012-2055-1.

    Article  PubMed  CAS  Google Scholar 

  46. Liao S, Li J, Wei W, Wang L, Zhang Y, Wang C, et al. Association between diabetes mellitus and breast cancer risk: a meta-analysis of the literature. Asian Pac J Cancer Prev APJCP. 2011;12(4):1061–5.

    Google Scholar 

  47. Larsson SC, Orsini N, Brismar K, Wolk A. Diabetes mellitus and risk of bladder cancer: a meta-analysis. Diabetologia. 2006;49(12):2819–23. doi:10.1007/s00125-006-0468-0.

    Article  PubMed  CAS  Google Scholar 

  48. Lee JY, Jeon I, Lee JM, Yoon JM, Park SM. Diabetes mellitus as an independent risk factor for lung cancer: a meta-analysis of observational studies. Eur J Cancer. 2013;49(10):2411–23. doi:10.1016/j.ejca.2013.02.025.

    Article  PubMed  Google Scholar 

  49. Castillo JJ, Mull N, Reagan JL, Nemr S, Mitri J. Increased incidence of non-Hodgkin lymphoma, leukemia, and myeloma in patients with diabetes mellitus type 2: a meta-analysis of observational studies. Blood. 2012;119(21):4845–50. doi:10.1182/blood-2011-06-362830.

    Article  PubMed  CAS  Google Scholar 

  50. Giovannucci E, Harlan DM, Archer MC, Bergenstal RM, Gapstur SM, Habel LA, et al. Diabetes and cancer: a consensus report. Diabetes Care. 2010;33(7):1674–85. doi:10.2337/dc10-0666.

    Article  PubMed  Google Scholar 

  51. Gallagher EJ, LeRoith D. Diabetes, cancer, and metformin: connections of metabolism and cell proliferation. Ann N Y Acad Sci. 2011;1243:54–68. doi:10.1111/j.1749-6632.2011.06285.x.

    Article  PubMed  CAS  Google Scholar 

  52. Thakkar B, Aronis KN, Vamvini MT, Shields K, Mantzoros CS. Metformin and sulfonylureas in relation to cancer risk in type II diabetes patients: a meta-analysis using primary data of published studies. Metabolism. 2013;62(7):922–34. doi:10.1016/j.metabol.2013.01.014.

    Article  PubMed  CAS  Google Scholar 

  53. Soranna D, Scotti L, Zambon A, Bosetti C, Grassi G, Catapano A, et al. Cancer risk associated with use of metformin and sulfonylurea in type 2 diabetes: a meta-analysis. Oncologist. 2012;17(6):813–22. doi:10.1634/theoncologist.2011-0462.

    Article  PubMed  CAS  Google Scholar 

  54. Habib SL, Rojna M. Diabetes and risk of cancer. ISRN Oncol. 2013;2013:583786. doi:10.1155/2013/583786.

    PubMed  Google Scholar 

  55. Okura Y, Urban LH, Mahoney DW, Jacobsen SJ, Rodeheffer RJ. Agreement between self-report questionnaires and medical record data was substantial for diabetes, hypertension, myocardial infarction and stroke but not for heart failure. J Clin Epidemiol. 2004;57(10):1096–103. doi:10.1016/j.jclinepi.2004.04.005.

    Article  PubMed  Google Scholar 

  56. Tseng CH. Diabetes and thyroid cancer mortality: a 12-year prospective follow-up of Taiwanese. Eur J Clin Invest. 2013;43(6):595–601. doi:10.1111/eci.12086.

    Article  PubMed  Google Scholar 

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  1. Department of Epidemiology and Preventive Medicine, University of Regensburg, Franz-Josef-Strauss-Allee 11, 93053, Regensburg, Germany

    Daniela Schmid, Gundula Behrens, Carmen Jochem, Marlen Keimling & Michael Leitzmann

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Schmid, D., Behrens, G., Jochem, C. et al. Physical activity, diabetes, and risk of thyroid cancer: a systematic review and meta-analysis. Eur J Epidemiol 28, 945–958 (2013). https://doi.org/10.1007/s10654-013-9865-0

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