Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

Epidemiology and Population Health

Sex differences in the rate of abdominal adipose accrual during adulthood: the Fels Longitudinal Study

Abstract

Objectives:

The purpose of this analysis was to evaluate sex differences in the rate of visceral adipose tissue (VAT) and subcutaneous adipose tissue (SAT) accrual in adults. Secondary analyses examined differences in the rate of VAT and SAT accrual in premenopausal, perimenopausal and postmenopausal women.

Subjects/Methods:

Participants were 472 (60% female) non-Hispanic whites and aged 18–84 years at baseline in whom abdominal VAT and SAT were assessed using multiple-image magnetic resonance imaging at two time points, with an average follow-up of 7.3±2.6 years. Linear regression models were used to examine the effects of sex, baseline age and their interaction on rate of change per year in body composition measures (ΔBMI, ΔVAT and ΔVAT/SAT ratio (ΔVSR)) independent of baseline body composition measures, visit year, income, marital status, physical activity, smoking and alcohol intake. Secondary analyses examined differences in the rate of fat change by menopausal status (premenopausal, perimenopausal, postmenopausal).

Results:

Levels of body mass index (BMI), VAT and VSR all increased over the 7-year period on average (P<0.001); however, the change in BMI (mean ΔBMI=+0.5%) was far smaller than for VAT (mean ΔVAT=+6.8%), SAT (mean ΔSAT=+2.4%) and VSR (mean ΔVSR=+3.6%). ΔBMI, ΔVAT and ΔSAT decreased linearly with age in both sexes (P<0.01), such that older individuals had lower rates of BMI, VAT and SAT gain, and this deceleration in BMI, VAT and SAT accrual was greater in men than women (P for interaction <0.05). ΔVSR did not vary with age in either sex but remained higher in men than women throughout adulthood. There were no differences in rate of weight or fat gain by menopausal status after adjustment for age.

Conclusions:

Men and women continue to accrue abdominal adiposity with age, but the rate of weight and fat gain decreases over time, particularly in men.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1

Similar content being viewed by others

References

  1. Despres JP, Lemieux I . Abdominal obesity and metabolic syndrome. Nature 2006; 444: 881–887.

    Article  CAS  PubMed  Google Scholar 

  2. Kuk JL, Katzmarzyk PT, Nichaman MZ, Church TS, Blair SN, Ross R . Visceral fat is an independent predictor of all-cause mortality in men. Obesity (Silver Spring) 2006; 14: 336–341.

    Article  Google Scholar 

  3. Boyko EJ, Fujimoto WY, Leonetti DL, Newell-Morris L . Visceral adiposity and risk of type 2 diabetes: a prospective study among Japanese Americans. Diabetes Care 2000; 23: 465–471.

    Article  CAS  PubMed  Google Scholar 

  4. Hayashi T, Boyko EJ, Leonetti DL, McNeely MJ, Newell-Morris L, Kahn SE et al. Visceral adiposity is an independent predictor of incident hypertension in Japanese Americans. Ann Intern Med 2004; 140: 992–1000.

    Article  PubMed  Google Scholar 

  5. Misra A, Vikram NK . Clinical and pathophysiological consequences of abdominal adiposity and abdominal adipose tissue depots. Nutrition 2003; 19: 457–466.

    Article  PubMed  Google Scholar 

  6. Nguyen-Duy TB, Nichaman MZ, Church TS, Blair SN, Ross R . Visceral fat and liver fat are independent predictors of metabolic risk factors in men. Am J Physiol Endocrinol Metab 2003; 284: E1065–E1071.

    Article  CAS  PubMed  Google Scholar 

  7. Tchernof A, Despres JP . Pathophysiology of human visceral obesity: an update. Physiol Rev. 2013; 93: 359–404.

    Article  CAS  PubMed  Google Scholar 

  8. Abraham TM, Pedley A, Massaro JM, Hoffman U, Fox CS . Association between visceral and subcutaneous adipose depots and incident cardiovascular disease risk factors. Circulation 2015; 132: 1639–1647.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Gast KB, den Heijer M, Smit JW, Widya RL, Lamb HJ, de Roos A et al. Individual contributions of visceral fat and total body fat to subclinical atherosclerosis: the NEO study. Atherosclerosis 2015; 241: 547–554.

    Article  CAS  PubMed  Google Scholar 

  10. Wajchenberg BL . Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome. Endocr Rev 2000; 21: 697–738.

    Article  CAS  PubMed  Google Scholar 

  11. Enzi G, Gasparo M, Biondetti PR, Fiore D, Semisa M, Zurlo F . Subcutaneous and visceral fat distribution according to sex, age, and overweight, evaluated by computed tomography. Am J Clin Nutr 1986; 44: 739–746.

    Article  CAS  PubMed  Google Scholar 

  12. Kotani K, Tokunaga K, Fujioka S, Kobatake T, Keno Y, Yoshida S et al. Sexual dimorphism of age-related changes in whole-body fat distribution in the obese. Int J Obes Relat Metab Disord 1994; 18: 207–2.

    CAS  PubMed  Google Scholar 

  13. Kuk JL, Lee S, Heymsfield SB, Ross R . Waist circumference and abdominal adipose tissue distribution: influence of age and sex. Am J Clin Nutr 2005; 81: 1330–1334.

    Article  CAS  PubMed  Google Scholar 

  14. Machann J, Thamer C, Schnoedt B, Stefan N, Stumvoll M, Haring HU et al. Age and gender related effects on adipose tissue compartments of subjects with increased risk for type 2 diabetes: a whole body MRI/MRS study. MAGMA 2005; 18: 128–137.

    Article  CAS  PubMed  Google Scholar 

  15. Kuk JL, Saunders TJ, Davidson LE, Ross R . Age-related changes in total and regional fat distribution. Ageing Res Rev 2009; 8: 339–348.

    Article  PubMed  Google Scholar 

  16. Lara-Castro C, Weinsier RL, Hunter GR, Desmond R . Visceral adipose tissue in women: longitudinal study of the effects of fat gain, time, and race. Obes Res 2002; 10: 868–874.

    Article  PubMed  Google Scholar 

  17. Lovejoy JC, Champagne CM, de Jonge L, Xie H, Smith SR . Increased visceral fat and decreased energy expenditure during the menopausal transition. Int J Obes (Lond) 2008; 32: 949–958.

    Article  CAS  Google Scholar 

  18. Abdulnour J, Doucet E, Brochu M, Lavoie JM, Strychar I, Rabasa-Lhoret R et al. The effect of the menopausal transition on body composition and cardiometabolic risk factors: a Montreal-Ottawa New Emerging Team group study. Menopause 2012; 19: 760–767.

    Article  PubMed  Google Scholar 

  19. Ho SC, Wu S, Chan SG, Sham A . Menopausal transition and changes of body composition: a prospective study in Chinese perimenopausal women. Int J Obes (Lond) 2010; 34: 1265–1274.

    Article  CAS  Google Scholar 

  20. Janssen I, Powell LH, Kazlauskaite R, Dugan SA . Testosterone and visceral fat in midlife women: the Study of Women's Health Across the Nation (SWAN) fat patterning study. Obesity (Silver Spring) 2010; 18: 604–610.

    Article  CAS  Google Scholar 

  21. Guthrie JR, Dennerstein L, Taffe JR, Ebeling PR, Randolph JF, Burger HG et al. Central abdominal fat and endogenous hormones during the menopausal transition. Fertil Steril 2003; 79: 1335–1340.

    Article  PubMed  Google Scholar 

  22. Kanaley JA, Giannopoulou I, Tillapaugh-Fay G, Nappi JS, Ploutz-Snyder LL . Racial differences in subcutaneous and visceral fat distribution in postmenopausal black and white women. Metabolism 2003; 52: 186–191.

    Article  CAS  PubMed  Google Scholar 

  23. van der Leeuw J, Wassink AM, van der Graaf Y, Westerveld HE, Visseren FL . Second manifestations of ADSG. Age-related differences in abdominal fat distribution in premenopausal and postmenopausal women with cardiovascular disease. Menopause 2013; 20: 409–417.

    PubMed  Google Scholar 

  24. Wells JC . Sexual dimorphism of body composition. Best Pract Res Clin Endocrinol Metab 2007; 21: 415–430.

    Article  PubMed  Google Scholar 

  25. Shah RV, Murthy VL, Abbasi SA, Blankstein R, Kwong RY, Goldfine AB et al. Visceral adiposity and the risk of metabolic syndrome across body mass index: the MESA Study. JACC Cardiovasc Imaging 2014; 7: 1221–1235.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Muller MJ, Lagerpusch M, Enderle J, Schautz B, Heller M, Bosy-Westphal A . Beyond the body mass index: tracking body composition in the pathogenesis of obesity and the metabolic syndrome. Obes Rev 2012; 13 (Suppl 2): 6–13.

    Article  PubMed  Google Scholar 

  27. Demerath EW, Ritter KJ, Couch WA, Rogers NL, Moreno GM, Choh A et al. Validity of a new automated software program for visceral adipose tissue estimation. Int J Obes (Lond) 2007; 31: 285–291.

    Article  CAS  Google Scholar 

  28. Demerath EW, Shen W, Lee M, Choh AC, Czerwinski SA, Siervogel RM et al. Approximation of total visceral adipose tissue with a single magnetic resonance image. Am J Clin Nutr 2007; 85: 362–368.

    Article  CAS  PubMed  Google Scholar 

  29. Lohman TG, Roche AF, Martorell R . Anthropometric Standardization Reference Manual. Human Kinetics: Champaign, IL, USA, 1988.

    Google Scholar 

  30. Baecke JA, Burema J, Frijters JE . A short questionnaire for the measurement of habitual physical activity in epidemiological studies. Am J Clin Nutr 1982; 36: 936–942.

    Article  CAS  PubMed  Google Scholar 

  31. Droyvold WB, Nilsen TI, Kruger O, Holmen TL, Krokstad S, Midthjell K et al. Change in height, weight and body mass index: longitudinal data from the HUNT Study in Norway. Int J Obes (Lond) 2006; 30: 935–939.

    Article  CAS  Google Scholar 

  32. Shen W, Punyanitya M, Silva AM, Chen J, Gallagher D, Sardinha LB et al. Sexual dimorphism of adipose tissue distribution across the lifespan: a cross-sectional whole-body magnetic resonance imaging study. Nutr Metab (Lond) 2009; 6: 17.

    Article  Google Scholar 

  33. Lim U, Ernst T, Buchthal SD, Latch M, Albright CL, Wilkens LR et al. Asian women have greater abdominal and visceral adiposity than Caucasian women with similar body mass index. Nutr Diabetes 2011; 1: e6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Douchi T, Yonehara Y, Kawamura Y, Kuwahata A, Kuwahata T, Iwamoto I . Difference in segmental lean and fat mass components between pre- and postmenopausal women. Menopause 2007; 14: 875–878.

    Article  PubMed  Google Scholar 

  35. Pansini F, Cervellati C, Guariento A, Stacchini MA, Castaldini C, Bernardi A et al. Oxidative stress, body fat composition, and endocrine status in pre- and postmenopausal women. Menopause 2008; 15: 112–118.

    Article  PubMed  Google Scholar 

  36. Cervellati C, Pansini FS, Bonaccorsi G, Pascale G, Bagni B, Castaldini C et al. Body mass index is a major determinant of abdominal fat accumulation in pre-, peri- and post-menopausal women. Gynecol Endocrinol 2009; 25: 413–417.

    Article  PubMed  Google Scholar 

  37. Kanaley JA, Sames C, Swisher L, Swick AG, Ploutz-Snyder LL, Steppan CM et al. Abdominal fat distribution in pre- and postmenopausal women: the impact of physical activity, age, and menopausal status. Metabolism 2001; 50: 976–982.

    Article  CAS  PubMed  Google Scholar 

  38. Demerath EW, Rogers NL, Reed D, Lee M, Choh AC, Siervogel RM et al. Significant associations of age, menopausal status and lifestyle factors with visceral adiposity in African-American and European-American women. Ann Hum Biol 2011; 38: 247–256.

    Article  PubMed  Google Scholar 

  39. Toth MJ, Tchernof A, Sites CK, Poehlman ET . Effect of menopausal status on body composition and abdominal fat distribution. Int J Obes Relat Metab Disord 2000; 24: 226–231.

    Article  CAS  PubMed  Google Scholar 

  40. Tchernof A, Desmeules A, Richard C, Laberge P, Daris M, Mailloux J et al. Ovarian hormone status and abdominal visceral adipose tissue metabolism. J Clin Endocrinol Metab 2004; 89: 3425–3430.

    Article  CAS  PubMed  Google Scholar 

  41. Franklin RM, Ploutz-Snyder L, Kanaley JA . Longitudinal changes in abdominal fat distribution with menopause. Metabolism 2009; 58: 311–315.

    Article  CAS  PubMed  Google Scholar 

  42. Lee DC, Sui X, Church TS, Lee IM, Blair SN . Associations of cardiorespiratory fitness and obesity with risks of impaired fasting glucose and type 2 diabetes in men. Diabetes Care 2009; 32: 257–262.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Mongraw-Chaffin ML, Anderson CA, Allison MA, Ouyang P, Szklo M, Vaidya D et al. Association between sex hormones and adiposity: qualitative differences in women and men in the multi-ethnic study of atherosclerosis. J Clin Endocrinol Metab 2015; 100: E596–E600.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Nielsen TL, Hagen C, Wraae K, Brixen K, Petersen PH, Haug E et al. Visceral and subcutaneous adipose tissue assessed by magnetic resonance imaging in relation to circulating androgens, sex hormone-binding globulin, and luteinizing hormone in young men. J Clin Endocrinol Metab 2007; 92: 2696–2705.

    Article  CAS  PubMed  Google Scholar 

  45. Seidell JC, Bjorntorp P, Sjostrom L, Kvist H, Sannerstedt R . Visceral fat accumulation in men is positively associated with insulin, glucose, and C-peptide levels, but negatively with testosterone levels. Metabolism 1990; 39: 897–901.

    Article  CAS  PubMed  Google Scholar 

  46. Seifarth JE, McGowan CL, Milne KJ . Sex and life expectancy. Gend Med 2012; 9: 390–401.

    Article  PubMed  Google Scholar 

  47. Ross R, Janiszewski PM . Is weight loss the optimal target for obesity-related cardiovascular disease risk reduction? Can J Cardiol 2008; 24 (Suppl D): 25D–31D.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Ross R, Dagnone D, Jones PJ, Smith H, Paddags A, Hudson R et al. Reduction in obesity and related comorbid conditions after diet-induced weight loss or exercise-induced weight loss in men. A randomized, controlled trial. Ann Intern Med 2000; 133: 92–103.

    Article  CAS  PubMed  Google Scholar 

  49. Ross R, Janssen I, Dawson J, Kungl AM, Kuk JL, Wong SL et al. Exercise-induced reduction in obesity and insulin resistance in women: a randomized controlled trial. Obes Res 2004; 12: 789–798.

    Article  PubMed  Google Scholar 

  50. Demerath EW, Reed D, Rogers N, Sun SS, Lee M, Choh AC et al. Visceral adiposity and its anatomical distribution as predictors of the metabolic syndrome and cardiometabolic risk factor levels. Am J Clin Nutr 2008; 88: 1263–1271.

    CAS  PubMed  Google Scholar 

  51. Janssen I, Powell LH, Jasielec MS, Kazlauskaite R . Covariation of change in bioavailable testosterone and adiposity in midlife women. Obesity (Silver Spring) 2015; 23: 488–494.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by grants R01HD012252, R01DK064870 and R01DK064391 from the National Institutes of Health. KMW was supported in part by research training grant T32 HL007779 from the National Heart, Lung and Blood Institute. We thank the investigators, the staff and the participants of the Fels Longitudinal Study for their valuable contributions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to K M Whitaker.

Ethics declarations

Competing interests

The authors declare no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Whitaker, K., Choh, A., Lee, M. et al. Sex differences in the rate of abdominal adipose accrual during adulthood: the Fels Longitudinal Study. Int J Obes 40, 1278–1285 (2016). https://doi.org/10.1038/ijo.2016.48

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ijo.2016.48

This article is cited by

Search

Quick links