Anthropometric measures of body fat and obesity-related cancer risk: sex-specific differences in Framingham Offspring Study adults

Abstract

Background/objective

Obesity has been associated with the risk of developing certain cancers. A limited number of studies have examined effects of various anthropometric measures of body composition on cancer risk. The aim of this study was to estimate the sex-specific effects of various anthropometric measures on risk of obesity-related cancers (ObCa).

Subjects/methods

Data on body mass index (BMI), waist circumference (WC), waist-to-height ratio (WHtR), and hip circumference (HC) among 3818 45–69-year olds in the Framingham Offspring Study were included. Cox proportional hazards models were used to estimate adjusted risks of 16 obesity-related cancers, with the most common being postmenopausal breast, endometrial, and colon cancers.

Results

Obesity as measured by BMI in both men and women was a predictor of ObCa; those in the highest quintile (Q5) of BMI (>30.07 in women; >30.80 kg/m2 in men) had more than twice the risk of ObCa (HR = 2.07; 95% CI: 1.06–4.07 (women) and HR = 2.25; 95% CI: 1.08–4.69 (men)). Waist-related measures (WC, WHtR) were stronger predictors of ObCa in men than in women, and HC confounded the relations between waist size and cancer risk. After adjusting for HC, men in Q5 of WC had more than a threefold increased risk of ObCa (HR: = 3.22; 95% CI: 1.39–7.45). Comparable effects in women were weak and non-statistically significant. Results were similar for WHtR. Finally, an inverse J-shaped relation was found between HC and ObCa after adjusting for WC among men but not in women.

Conclusions

These results suggest that obesity as measured by BMI is a predictor of obesity-related cancer risk in men and women. They also suggest that waist and hip circumference measures are interrelated and confound the independent effects of each measure. Among men, a large waist size and a small hip size are independent predictors of cancer risk.

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References

  1. 1.

    World Cancer Research Fund, American Institute for Cancer Research (AICR). Food, nutrition, physical activity, and the prevention of cancer: a global perspective. 2007. https://discovery.ucl.ac.uk/id/eprint/4841/1/4841.pdf

  2. 2.

    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;371:569–78. https://doi.org/10.1016/S0140-6736(08)60269-X

  3. 3.

    Moore LL, Bradlee ML, Singer MR, Splansky GL, Proctor MH, Ellison RC, et al. BMI and waist circumference as predictors of lifetime colon cancer risk in Framingham Study adults. Int J Obes. 2004;28:559–67. https://doi.org/10.1038/sj.ijo.0802606

  4. 4.

    Snijder MB, Dekker JM, Visser M, Bouter LM, Stehouwer CDA, Kostense PJ, et al. Association of hip and thigh circumferences independent of waist circumference with the incidence of type 2 diabetes: the Hoorn Study. Am J Clin Nutr. 2003;77:1192–7

  5. 5.

    Yim J-E, Heshka S, Albu JB, Heymsfield S, Gallagher D. Femoral-gluteal subcutaneous and intermuscular adipose tissues have independent and opposing relationships with CVD risk. J Appl Physiol. 2008;104:700–7. https://doi.org/10.1152/japplphysiol.01035.2007

  6. 6.

    Parker ED, Pereira MA, Stevens J, Folsom AR. Association of hip circumference with incident diabetes and coronary heart disease: the atherosclerosis riskin communities study. Am J Epidemiol. 2009;169:837–47. https://doi.org/10.1093/aje/kwn395

  7. 7.

    Garrison RJ, Kannel WB, Stokes J, Castelli WP. Incidence and precursors of hypertension in young adults: the Framingham Offspring Study. Prev Med. 1987;16:235–51. https://doi.org/10.1016/0091-7435(87)90087-9

  8. 8.

    McMillan D, Sattar N, Lean M, McCardle C. ABC of obesity. Obesity and cancer. Br Med J. 2006;333:1109–11.

  9. 9.

    Ahn J, Schatzkin A, Lacey JV Jr, Albanes D, Ballard-Barbash R, Adams KF, et al. Adiposity, adult weight change, and postmenopausal breast cancer risk. Arch Intern Med. 2007;167:2091–102. https://doi.org/10.1001/archinte.167.19.2091

  10. 10.

    Sun B, Karin MObesity. inflammation, and liver cancer. J Hepatol. 2012;56:704–13. https://doi.org/10.1016/j.jhep.2011.09.020

  11. 11.

    Abnet CC, Freedman ND, Hollenbeck AR, Fraumeni JF, Leitzmann M, Schatzkin A. A prospective study of BMI and risk of oesophageal and gastric adenocarcinoma. Eur J Cancer. 2008;44:465–71. https://doi.org/10.1016/j.ejca.2007.12.009

  12. 12.

    Guh DP, Zhang W, Bansback N, Amarsi Z, Birmingham CL, Anis AH. The incidence of co-morbidities related to obesity and overweight: a systematic review and meta-analysis. BMC Public Health. 2009;9:1–20. https://doi.org/10.1186/1471-2458-9-88

  13. 13.

    Olsen CM, Green AC, Whiteman DC, Sadeghi S, Kolahdooz F, Webb PM. Obesity and the risk of epithelial ovarian cancer: a systematic review and meta-analysis. Eur J Cancer. 2007;43:690–709. https://doi.org/10.1016/j.ejca.2006.11.010

  14. 14.

    Yang P, Zhou Y, Chen B, Wan H-W, Jia G-Q, Bai H-L, et al. Overweight, obesity and gastric cancer risk: Results from a meta-analysis of cohort studies. Eur J Cancer. 2009;45:2867–73. https://doi.org/10.1016/j.ejca.2009.04.019

  15. 15.

    Kreger BE, Splansky GL, Schatzkin A. The cancer experience in The Framingham Heart Study cohort. Cancer. 1991;67:1–6. 10.1002/1097-0142(19910101)67:1<1:AID-CNCR2820670102>3.0.CO;2-W

  16. 16.

    Fritz A, Percy C, Jack A, Shanmugaratnam K, Sobin L, Parkin DM, et al. International classification of diseases for oncology. 3rd ed. 2013. https://doi.org/10.1136/jcp.30.8.782-c

  17. 17.

    Kannel WB, Sorlie P. Some health benefits of physical activity: the Framingham Study. Arch Intern Med. 1979;139:857–61. https://doi.org/10.1001/archinte.1979.03630450011006

  18. 18.

    Freisling H, Arnold M, Soerjomataram I, O’Doherty MG, Ordóñez-Mena JM, Bamia C, et al. Comparison of general obesity and measures of body fat distribution in older adults in relation to cancer risk: Meta-analysis of individual participant data of seven prospective cohorts in Europe. Br J Cancer. 2017;116:1486–97. https://doi.org/10.1038/bjc.2017.106

  19. 19.

    Moore LL, Chadid S, Singer MR, Kreger BE, Denis GV. Metabolic health reduces risk of obesity-related cancer in framingham study adults. Cancer Epidemiol Biomarkers Prev. 2014;23:2057–65

  20. 20.

    De Mutsert R, Sun Q, Willett WC, Hu FB, Van Dam RM. Overweight in early adulthood, adult weight change, and risk of type 2 diabetes, cardiovascular diseases, and certain cancers in men: a cohort study. Am J Epidemiol. 2014;179:1353–65. https://doi.org/10.1093/aje/kwu052

  21. 21.

    Reeves GK, Pirie K, Beral V, Green J, Spencer E, Bull D. Cancer incidence and mortality in relation to body mass index in the Million Women Study: cohort study. Br Med J. 2007;335:1134–9. https://doi.org/10.1136/bmj.39367.495995.AE

  22. 22.

    Manolopoulos KN, Karpe F, Frayn KN. Gluteofemoral body fat as a determinant of metabolic health. Int J Obes. 2010;34:949–59. https://doi.org/10.1038/ijo.2009.286

  23. 23.

    Lahmann PH, Hoffmann K, Allen N, van Gils TH, Khaw AT, Tehard B, et al. Body size and breast cancer risk: Findings from the European Prospective Investigation into Cancer and Nutrition (EPIC). Int J Cancer. 2004;111:762–71. https://doi.org/10.1002/ijc.20315

  24. 24.

    Morimoto LM, White E, Chen Z, Chlebowski RT, Hays J, Kuller L, et al. Obesity, body size, and risk of postmenopausal breast cancer: the Women’s Health Initiative. Cancer Causes Control. 2002;13:741–51

  25. 25.

    Kitahara CM, Platz EA, Park Y, Hollenbeck AR, Schatzkin A, Berrington De González A. Body fat distribution, weight change during adulthood, and thyroid cancer risk in the NIH-AARP Diet and Health Study. Int J Cancer. 2012;130:1411–9. https://doi.org/10.1002/ijc.26161

  26. 26.

    Pischon T, Lahmann PH, Boeing H, Friedenreich C, Norat T, Tjønneland A, et al. Body size and risk of colon and rectal cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC). J Natl Cancer Inst. 2006;98:920–31. https://doi.org/10.1093/jnci/djj246

  27. 27.

    Aune D, Navarro Rosenblatt DA, Chan DSM, Vingeliene S, Abar L, Vieira AR, et al. Anthropometric factors and endometrial cancer risk: a systematic review and dose-response meta-analysis of prospective studies. Ann Oncol. 2015;26:1635–48. https://doi.org/10.1093/annonc/mdv142

  28. 28.

    Sponholtz TR, Palmer JR, Rosenberg L, Hatch EE, Adams-Campbell LL, Wise LA. Body size, metabolic factors, and risk of endometrial cancer in black women. Am J Epidemiol. 2016;183:259–68. https://doi.org/10.1093/aje/kwv186

  29. 29.

    Cameron AJ, Magliano DJ, Söderberg S. A systematic review of the impact of including both waist and hip circumference in risk models for cardiovascular diseases, diabetes and mortality. Obes Rev. 2013;14:86–94. https://doi.org/10.1111/j.1467-789X.2012.01051.x

  30. 30.

    Divella R, De Luca R, Abbate I, Naglieri E, Daniele A. Obesity and cancer: The role of adipose tissue and adipo-cytokines-induced chronic inflammation. J Cancer. 2016;7:2346–59. https://doi.org/10.7150/jca.16884

  31. 31.

    Pollak M. The insulin and insulin-like growth factor receptor family in neoplasia: an update. Nat Rev Cancer. 2012;12:159–69. https://doi.org/10.1038/nrc3215

  32. 32.

    Hursting SD, Dunlap SM. Obesity, metabolic dysregulation, and cancer: a growing concern and an inflammatory (and microenvironmental) issue. Ann N Y Acad Sci. 2012;1271:82–87. https://doi.org/10.1111/j.1749-6632.2012.06737.x

  33. 33.

    Baniyash M, Sade-Feldman M, Kanterman J. Chronic inflammation and cancer: suppressing the suppressors. Cancer Immunol Immunother. 2014;63:11–20. https://doi.org/10.1007/s00262-013-1468-9

  34. 34.

    Maury E, Brichard SM. Adipokine dysregulation, adipose tissue inflammation and metabolic syndrome. Mol Cell Endocrinol. 2010;314:1–16. https://doi.org/10.1016/j.mce.2009.07.031

  35. 35.

    Spoto B, Di Betta E, Mattace-Raso F, Sijbrands E, Vilardi A, Parlongo RM, et al. Pro- and anti-inflammatory cytokine gene expression in subcutaneous and visceral fat in severe obesity. Nutr Metab Cardiovasc Dis. 2014;24:1137–43. https://doi.org/10.1016/j.numecd.2014.04.017

  36. 36.

    Fox CS, Massaro JM, Hoffmann U, Pou KM, Maurovich-Horvat P, Liu C-Y, et al. Abdominal visceral and subcutaneous adipose tissue compartments: Association with metabolic risk factors in the framingham heart study. Circulation. 2007;116:39–48. https://doi.org/10.1161/CIRCULATIONAHA.106.675355

  37. 37.

    Liu J, Fox CS, Hickson DMA, May WD, Hairston KG, Carr JJ, et al. Impact of abdominal visceral and subcutaneous adipose tissue on cardiometabolic risk factors: the Jackson Heart Study. J Clin Endocrinol Metab. 2010;95:5419–26. https://doi.org/10.1210/jc.2010-1378

  38. 38.

    Tchernof A, Despres J-P. Pathophysiology of human visceral obesity: an update. Physiol Rev. 2013;93:359–404. https://doi.org/10.1152/physrev.00033.2011

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Funding

This work is supported by NHLBI, Framingham Heart Study, (NHLBI/NIH contract #HHSN268201500001I) and the Boston University School of Medicine. Dr. Chadid was supported by a National Cancer Institute Training Grant (T32) CA009314 at the Johns Hopkins Bloomberg School of Public Health.

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Correspondence to Lynn L. Moore.

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Chadid, S., Kreger, B.E., Singer, M.R. et al. Anthropometric measures of body fat and obesity-related cancer risk: sex-specific differences in Framingham Offspring Study adults. Int J Obes (2020). https://doi.org/10.1038/s41366-020-0519-5

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