European Journal of Epidemiology

, Volume 31, Issue 9, pp 893–904 | Cite as

Overweight duration in older adults and cancer risk: a study of cohorts in Europe and the United States

  • Melina Arnold
  • Heinz Freisling
  • Rachael Stolzenberg-Solomon
  • Frank Kee
  • Mark George O’Doherty
  • José Manuel Ordóñez-Mena
  • Tom Wilsgaard
  • Anne Maria May
  • Hendrik Bas Bueno-de-Mesquita
  • Anne Tjønneland
  • Philippos Orfanos
  • Antonia Trichopoulou
  • Paolo Boffetta
  • Freddie Bray
  • Mazda Jenab
  • Isabelle Soerjomataram
  • on behalf of the CHANCES consortium
CANCER

Abstract

Recent studies have shown that cancer risk related to overweight and obesity is mediated by time and might be better approximated by using life years lived with excess weight. In this study we aimed to assess the impact of overweight duration and intensity in older adults on the risk of developing different forms of cancer. Study participants from seven European and one US cohort study with two or more weight assessments during follow-up were included (n = 329,576). Trajectories of body mass index (BMI) across ages were estimated using a quadratic growth model; overweight duration (BMI ≥ 25) and cumulative weighted overweight years were calculated. In multivariate Cox models and random effects analyses, a longer duration of overweight was significantly associated with the incidence of obesity-related cancer [overall hazard ratio (HR) per 10-year increment: 1.36; 95 % CI 1.12–1.60], but also increased the risk of postmenopausal breast and colorectal cancer. Additionally accounting for the degree of overweight further increased the risk of obesity-related cancer. Risks associated with a longer overweight duration were higher in men than in women and were attenuated by smoking. For postmenopausal breast cancer, increased risks were confined to women who never used hormone therapy. Overall, 8.4 % of all obesity-related cancers could be attributed to overweight at any age. These findings provide further insights into the role of overweight duration in the etiology of cancer and indicate that weight control is relevant at all ages. This knowledge is vital for the development of effective and targeted cancer prevention strategies.

Keywords

CHANCES Ageing Cohort Obesity Cancer Prevention 

Supplementary material

10654_2016_169_MOESM1_ESM.docx (49 kb)
Supplementary material 1 (DOCX 49 kb)

References

  1. 1.
    Finucane MM, Stevens GA, Cowan MJ, et al. National, regional, and global trends in body-mass index since 1980: systematic analysis of health examination surveys and epidemiological studies with 960 country-years and 9.1 million participants. Lancet. 2011;377(9765):557–67.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Collaboration NRF, Di Cesare M, Bentham J, et al. Trends in adult body-mass index in 200 countries from 1975 to 2014: a pooled analysis of 1698 population-based measurement studies with 19.2 million participants. Lancet. 2016;387(10026):1377–96. doi:10.1016/S0140-6736(16)30054-X.CrossRefGoogle Scholar
  3. 3.
    Ogden CL, Carroll MD, Kit BK, Flegal KM. Prevalence of childhood and adult obesity in the United States, 2011–2012. JAMA. 2014;311(8):806–14. doi:10.1001/jama.2014.732.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Stevens GA, Singh GM, Lu Y, et al. National, regional, and global trends in adult overweight and obesity prevalences. Popul Health Metr. 2012;10(1):22.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Overweight and obesity—BMI statistics [database on the Internet]. Eurostat. 2015 [cited 28-08-2015]. http://ec.europa.eu/eurostat/statistics-explained/index.php?title=Overweight_and_obesity_-_BMI_statistics&oldid=120144.
  6. 6.
    Lakdawalla DN, Goldman DP, Shang B. The health and cost consequences of obesity among the future elderly. Health Aff. 2005;24(Suppl 2):W5R30–41. doi:10.1377/hlthaff.w5.r30.Google Scholar
  7. 7.
    Arnold M, Pandeya N, Byrnes G, et al. Global burden of cancer attributable to high body-mass index in 2012: a population-based study. Lancet Oncol. 2015;16(1):36–46. doi:10.1016/S1470-2045(14)71123-4.CrossRefPubMedGoogle Scholar
  8. 8.
    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.CrossRefPubMedGoogle Scholar
  9. 9.
    Arnold M, Leitzmann M, Freisling H, et al. Obesity and cancer: an update of the global impact. Cancer Epidemiol. 2016;41:8–15. doi:10.1016/j.canep.2016.01.003.CrossRefPubMedGoogle Scholar
  10. 10.
    Abdullah A, Stoelwinder J, Shortreed S, et al. The duration of obesity and the risk of type 2 diabetes. Public Health Nutr. 2011;14(1):119–26. doi:10.1017/S1368980010001813.CrossRefPubMedGoogle Scholar
  11. 11.
    Abdullah A, Amin FA, Stoelwinder J, et al. Estimating the risk of cardiovascular disease using an obese-years metric. BMJ Open. 2014;4(9):e005629. doi:10.1136/bmjopen-2014-005629.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Abdullah A, Wolfe R, Stoelwinder JU, et al. The number of years lived with obesity and the risk of all-cause and cause-specific mortality. Int J Epidemiol. 2011;40(4):985–96.CrossRefPubMedGoogle Scholar
  13. 13.
    Bianchini F, Kaaks R, Vainio H. Overweight, obesity, and cancer risk. Lancet Oncol. 2002;3(9):565–74.CrossRefPubMedGoogle Scholar
  14. 14.
    Boffetta P, Bobak M, Borsch-Supan A, et al. The Consortium on Health and Ageing: network of Cohorts in Europe and the United States (CHANCES) project–design, population and data harmonization of a large-scale, international study. Eur J Epidemiol. 2014;29(12):929–36. doi:10.1007/s10654-014-9977-1.CrossRefPubMedGoogle Scholar
  15. 15.
    World Cancer Research Fund. Food, nutrition, physical activity and the prevention of cancer: a global perspective: a project of World Cancer Research Fund International. Washington, D.C.: American Institute for Cancer Research; 2007.Google Scholar
  16. 16.
    Heo M, Faith MS, Mott JW, Gorman BS, Redden DT, Allison DB. Hierarchical linear models for the development of growth curves: an example with body mass index in overweight/obese adults. Stat Med. 2003;22(11):1911–42. doi:10.1002/sim.1218.CrossRefPubMedGoogle Scholar
  17. 17.
    Naumova EN, Must A, Laird NM. Tutorial in biostatistics: evaluating the impact of ‘critical periods’ in longitudinal studies of growth using piecewise mixed effects models. Int J Epidemiol. 2001;30(6):1332–41.CrossRefPubMedGoogle Scholar
  18. 18.
    Harris RJ, Bradburn MJ, Deeks JJ, Harbord RM, Altman DG, Sterne JAC. Metan: fixed- and random-effects meta-analysis. Stata J. 2008;8(1):3–28.Google Scholar
  19. 19.
    Rockhill B, Newman B, Weinberg C. Use and misuse of population attributable fractions. Am J Public Health. 1998;88(1):15–9.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Hanley JA. A heuristic approach to the formulas for population attributable fraction. J Epidemiol Community Health. 2001;55(7):508–14.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Miettinen OS. Proportion of disease caused or prevented by a given exposure, trait or intervention. Am J Epidemiol. 1974;99(5):325–32.PubMedGoogle Scholar
  22. 22.
    Greenland S, Drescher K. Maximum likelihood estimation of the attributable fraction from logistic models. Biometrics. 1993;49(3):865–72.CrossRefPubMedGoogle Scholar
  23. 23.
    Reeves GK, Pirie K, Beral V, et al. Cancer incidence and mortality in relation to body mass index in the Million Women Study: cohort study. BMJ. 2007;335(7630):1134. doi:10.1136/bmj.39367.495995.AE.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    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.CrossRefPubMedGoogle Scholar
  25. 25.
    Morimoto LM, White E, Chen Z, et al. Obesity, body size, and risk of postmenopausal breast cancer: the Women’s Health Initiative (United States). Cancer Causes Control. 2002;13(8):741–51.CrossRefPubMedGoogle Scholar
  26. 26.
    Food, Nutrition, Physical activity, and the Prevention of Breast Cancer. Continuous Update Project Report: World Cancer Research Fund/American Institute for Cancer Research; 2010.Google Scholar
  27. 27.
    Reeves KW, Carter GC, Rodabough RJ, et al. Obesity in relation to endometrial cancer risk and disease characteristics in the Women’s Health Initiative. Gynecol Oncol. 2011;121(2):376–82. doi:10.1016/j.ygyno.2011.01.027.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Bhaskaran K, Douglas I, Forbes H, Dos-Santos-Silva I, Leon DA, Smeeth L. Body-mass index and risk of 22 specific cancers: a population-based cohort study of 5·24 million UK adults. Lancet. 2014;. doi:10.1016/s0140-6736(14)60892-8.PubMedCentralGoogle Scholar
  29. 29.
    Wang Y, Jacobs EJ, Teras LR, et al. Lack of evidence for effect modification by estrogen of association between body mass index and colorectal cancer risk among postmenopausal women. Cancer Causes Control. 2007;18(8):793–9. doi:10.1007/s10552-007-9009-5.CrossRefPubMedGoogle Scholar
  30. 30.
    Slattery ML, Ballard-Barbash R, Edwards S, Caan BJ, Potter JD. Body mass index and colon cancer: an evaluation of the modifying effects of estrogen (United States). Cancer Causes Control. 2003;14(1):75–84.CrossRefPubMedGoogle Scholar
  31. 31.
    Keimling M, Renehan AG, Behrens G, et al. Comparison of associations of body mass index, abdominal adiposity, and risk of colorectal cancer in a large prospective cohort study. Cancer Epidemiol Biomarkers Prev. 2013;22(8):1383–94. doi:10.1158/1055-9965.EPI-13-0353.CrossRefPubMedGoogle Scholar
  32. 32.
    Food, Nutrition, Physical activity, and the Prevention of Colorectal Cancer. Continuous Update Project Report: World Cancer Research Fund/American Institute for Cancer Research; 2011.Google Scholar
  33. 33.
    Ford ES, Li C, Zhao G, Tsai J. Trends in obesity and abdominal obesity among adults in the United States from 1999–2008. Int J Obes. 2011;35(5):736–43. doi:10.1038/ijo.2010.186.CrossRefGoogle Scholar
  34. 34.
    Rose DP, Komninou D, Stephenson GD. Obesity, adipocytokines, and insulin resistance in breast cancer. Obes Rev. 2004;5(3):153–65. doi:10.1111/j.1467-789X.2004.00142.x.CrossRefPubMedGoogle Scholar
  35. 35.
    Smith L, Brinton LA, Spitz MR, et al. Body mass index and risk of lung cancer among never, former, and current smokers. J Natl Cancer Inst. 2012;104(10):778–89. doi:10.1093/jnci/djs179.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Aune D, Greenwood DC, Chan DS, et al. Body mass index, abdominal fatness and pancreatic cancer risk: a systematic review and non-linear dose–response meta-analysis of prospective studies. Ann Oncol. 2012;23(4):843–52. doi:10.1093/annonc/mdr398.CrossRefPubMedGoogle Scholar
  37. 37.
    Henley SJ, Flanders WD, Manatunga A, Thun MJ. Leanness and lung cancer risk: fact or artifact? Epidemiology. 2002;13(3):268–76.CrossRefPubMedGoogle Scholar
  38. 38.
    Calle EE, Rodriguez C, Walker-Thurmond K, Thun MJ. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N Engl J Med. 2003;348(17):1625–38. doi:10.1056/NEJMoa021423.CrossRefPubMedGoogle Scholar
  39. 39.
    Olson JE, Yang P, Schmitz K, Vierkant RA, Cerhan JR, Sellers TA. Differential association of body mass index and fat distribution with three major histologic types of lung cancer: evidence from a cohort of older women. Am J Epidemiol. 2002;156(7):606–15.CrossRefPubMedGoogle Scholar
  40. 40.
    Stolzenberg-Solomon RZ, Schairer C, Moore S, Hollenbeck A, Silverman DT. Lifetime adiposity and risk of pancreatic cancer in the NIH-AARP Diet and Health Study cohort. Am J Clin Nutr. 2013;98(4):1057–65. doi:10.3945/ajcn.113.058123.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Ostbye T, Malhotra R, Landerman LR. Body mass trajectories through adulthood: results from the National Longitudinal Survey of Youth 1979 Cohort (1981–2006). Int J Epidemiol. 2011;40(1):240–50. doi:10.1093/ije/dyq142.CrossRefPubMedGoogle Scholar
  42. 42.
    Botoseneanu A, Liang J. Latent heterogeneity in long-term trajectories of body mass index in older adults. J Aging Health. 2013;25(2):342–63. doi:10.1177/0898264312468593.CrossRefPubMedGoogle Scholar
  43. 43.
    Decaria JE, Sharp C, Petrella RJ. Scoping review report: obesity in older adults. Int J Obes. 2012;36(9):1141–50. doi:10.1038/ijo.2012.29.CrossRefGoogle Scholar
  44. 44.
    Moore LL, Bradlee ML, Singer MR, et al. BMI and waist circumference as predictors of lifetime colon cancer risk in Framingham Study adults. Int J Obes Relat Metab Disord. 2004;28(4):559–67. doi:10.1038/sj.ijo.0802606.CrossRefGoogle Scholar
  45. 45.
    Janssen I, Katzmarzyk PT, Ross R. Waist circumference and not body mass index explains obesity-related health risk. Am J Clin Nutr. 2004;79(3):379–84.PubMedGoogle Scholar
  46. 46.
    Peto J. That the effects of smoking should be measured in pack-years: misconceptions 4. Br J Cancer. 2012;107(3):406–7. doi:10.1038/bjc.2012.97.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Hernan MA. The hazards of hazard ratios. Epidemiology. 2010;21(1):13–5. doi:10.1097/EDE.0b013e3181c1ea43.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Thomas DC. Invited commentary: is it time to retire the “pack-years” variable? Maybe not! Am J Epidemiol. 2014;179(3):299–302. doi:10.1093/aje/kwt274.CrossRefPubMedGoogle Scholar
  49. 49.
    Zamboni M, Mazzali G, Zoico E, et al. Health consequences of obesity in the elderly: a review of four unresolved questions. Int J Obes. 2005;29(9):1011–29. doi:10.1038/sj.ijo.0803005.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Melina Arnold
    • 1
  • Heinz Freisling
    • 2
  • Rachael Stolzenberg-Solomon
    • 3
  • Frank Kee
    • 4
  • Mark George O’Doherty
    • 4
  • José Manuel Ordóñez-Mena
    • 5
    • 6
  • Tom Wilsgaard
    • 7
  • Anne Maria May
    • 8
  • Hendrik Bas Bueno-de-Mesquita
    • 9
    • 10
    • 11
    • 12
  • Anne Tjønneland
    • 13
  • Philippos Orfanos
    • 14
  • Antonia Trichopoulou
    • 14
    • 15
  • Paolo Boffetta
    • 14
    • 16
  • Freddie Bray
    • 1
  • Mazda Jenab
    • 17
  • Isabelle Soerjomataram
    • 1
  • on behalf of the CHANCES consortium
  1. 1.Section of Cancer SurveillanceInternational Agency for Research on CancerLyonFrance
  2. 2.Section of Nutrition and Metabolism, Dietary Exposure Assessment GroupInternational Agency for Research on CancerLyonFrance
  3. 3.Division of Cancer Epidemiology and Genetics, Nutritional Epidemiology BranchNational Cancer Institute (NCI/DCEG)BethesdaUSA
  4. 4.UKCRC Centre of Excellence for Public Health, School of Medicine, Dentistry and Biomedical SciencesQueen’s University BelfastBelfastNorthern Ireland, UK
  5. 5.Network Aging Research (NAR)Heidelberg UniversityHeidelbergGermany
  6. 6.Division of Clinical Epidemiology and Aging ResearchGerman Cancer Research Center (DKFZ)HeidelbergGermany
  7. 7.Department of Community MedicineThe Arctic University of NorwayTromsøNorway
  8. 8.Juliu Center for Health Sciences and Primary Care, EpidemiologyUniversity Medical Center UtrechtUtrechtThe Netherlands
  9. 9.Department for Determinants of Chronic Diseases (DCD)National Institute for Public Health and the Environment (RIVM)BilthovenThe Netherlands
  10. 10.Department of Gastroenterology and HepatologyUniversity Medical CentreUtrechtThe Netherlands
  11. 11.Department of Epidemiology and Biostatistics, The School of Public HealthImperial College LondonLondonUK
  12. 12.Department of Social and Preventive Medicine, Faculty of MedicineUniversity of MalayaKuala LumpurMalaysia
  13. 13.Danish Cancer Society Research CenterCopenhagen ØDenmark
  14. 14.Hellenic Health FoundationAthensGreece
  15. 15.Department of Hygiene, Epidemiology and Medical StatisticsUniversity of Athens Medical SchoolAthensGreece
  16. 16.Institute for Translational Epidemiology and Tisch Cancer InstituteIcahn School of Medicine at Mount SinaiNew YorkUSA
  17. 17.Section of Nutrition and Metabolism, Nutritional Epidemiology GroupInternational Agency for Research on CancerLyonFrance

Personalised recommendations