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Epidemiology and Population Health

Adult weight change in relation to visceral fat and liver fat at middle age: The Netherlands epidemiology of obesity study



We aimed to investigate the associations between weight change during adulthood and the amount of abdominal subcutaneous fat, visceral fat, and liver fat at middle age.


The Netherlands Epidemiology of Obesity (NEO) study is a population-based cohort of 6671 middle-aged men and women. We calculated the percentage of weight change during adulthood based on body weight at middle age and recalled body weight at age 20. Abdominal subcutaneous and visceral adipose tissue were assessed by magnetic resonance imaging (MRI), in addition to hepatic triglyceride content by 1H-MR spectroscopy in a random subgroup (maximum of n = 2580). With multivariable linear regression analysis, we examined the associations between categories of adult weight change, body mass index (BMI) at age 20 and measures of abdominal adiposity at middle age, adjusted for age, sex, ethnicity, lifestyle factors, menopausal status, parity, use of medication and total body fat at middle age.


In 2399 participants (54% women), individuals who gained more than 50% of body weight during adulthood had 1.96 (95% CI: 1.64; 2.33) times more visceral adipose tissue at middle age and 2.39 (95% CI: 1.70, 3.36) times more hepatic triglyceride content than weight maintainers (weight change between −5% and 5%). Associations with abdominal subcutaneous adipose tissue were weaker: participants who gained more than 50% of their body weight had 1.54 (95% CI: 1.38, 1.72) times more abdominal subcutaneous adipose tissue compared with weight maintainers.


In this population-based study, adult weight gain was associated with relatively more visceral adipose tissue and hepatic triglyceride content at middle age than abdominal subcutaneous adipose tissue. Overall, our study suggests that weight maintenance during adulthood plays an important role in limiting excess visceral adipose tissue and hepatic triglyceride content at middle age.

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Fig. 1


  1. 1.

    Tirosh A, Shai I, Afek A, Dubnov-Raz G, Ayalon N, Gordon B, et al. Adolescent BMI trajectory and risk of diabetes versus coronary disease. N Engl J Med. 2011;364:1315–25.

    CAS  Article  Google Scholar 

  2. 2.

    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.

    Article  Google Scholar 

  3. 3.

    Chan JM, Rimm EB, Colditz GA, Stampfer MJ, Willett WC. Obesity, fat distribution, and weight gain as risk factors for clinical diabetes in men. Diabetes Care. 1994;17:961–9.

    CAS  Article  Google Scholar 

  4. 4.

    Colditz GA, Willett WC, Rotnitzky A, Manson JE. Weight gain as a risk factor for clinical diabetes mellitus in women. Ann Intern Med. 1995;122:481–6.

    CAS  Article  Google Scholar 

  5. 5.

    Sun W, Shi L, Ye Z, Mu Y, Liu C, Zhao J, et al. Association between the change in body mass index from early adulthood to midlife and subsequent type 2 diabetes mellitus. Obesity (Silver Spring). 2016;24:703–9.

    Article  Google Scholar 

  6. 6.

    Koh-Banerjee P, Wang Y, Hu FB, Spiegelman D, Willett WC, Rimm EB. Changes in body weight and body fat distribution as risk factors for clinical diabetes in US men. Am J Epidemiol. 2004;159:1150–9.

    Article  Google Scholar 

  7. 7.

    Adams KF, Leitzmann MF, Ballard-Barbash R, Albanes D, Harris TB, Hollenbeck A, et al. Body mass and weight change in adults in relation to mortality risk. Am J Epidemiol. 2014;179:135–44.

    Article  Google Scholar 

  8. 8.

    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;44:739–46.

    CAS  Article  Google Scholar 

  9. 9.

    Kvist H, Chowdhury B, Grangard U, Tylen U, Sjostrom L. Total and visceral adipose-tissue volumes derived from measurements with computed tomography in adult men and women: predictive equations. Am J Clin Nutr. 1988;48:1351–61.

    CAS  Article  Google Scholar 

  10. 10.

    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  PubMed Central  Google Scholar 

  11. 11.

    Shimokata H, Tobin JD, Muller DC, Elahi D, Coon PJ, Andres R. Studies in the distribution of body fat: I. Effects of age, sex, and obesity. J Gerontol. 1989;44:M66–73.

    CAS  Article  Google Scholar 

  12. 12.

    Krotkiewski M, Bjorntorp P, Sjostrom L, Smith U. Impact of obesity on metabolism in men and women. Importance of regional adipose tissue distribution. J Clin Invest. 1983;72:1150–62.

    CAS  Article  Google Scholar 

  13. 13.

    Gustafson B. Adipose tissue, inflammation and atherosclerosis. J Atheroscler Thromb. 2010;17:332–41.

    CAS  Article  Google Scholar 

  14. 14.

    Thamer C, Machann J, Haap M, Stefan N, Heller E, Schnodt B, et al. Intrahepatic lipids are predicted by visceral adipose tissue mass in healthy subjects. Diabetes Care. 2004;27:2726–9.

    Article  Google Scholar 

  15. 15.

    Fabbrini E, Magkos F, Mohammed BS, Pietka T, Abumrad NA, Patterson BW, et al. Intrahepatic fat, not visceral fat, is linked with metabolic complications of obesity. Proc Natl Acad Sci USA. 2009;106:15430–5.

    CAS  Article  Google Scholar 

  16. 16.

    Bergman RN, Kim SP, Catalano KJ, Hsu IR, Chiu JD, Kabir M, et al. Why visceral fat is bad: mechanisms of the metabolic syndrome. Obesity (Silver Spring). 2006;14:16S–9S.

    CAS  Article  Google Scholar 

  17. 17.

    Jensen MD. Is visceral fat involved in the pathogenesis of the metabolic syndrome? Human model. Obesity (Silver Spring). 2006;14:20S–4S.

    CAS  Article  Google Scholar 

  18. 18.

    Miranda PJ, DeFronzo RA, Califf RM, Guyton JR. Metabolic syndrome: definition, pathophysiology, and mechanisms. Am Heart J. 2005;149:33–45.

    CAS  Article  Google Scholar 

  19. 19.

    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;88:1263–71.

    CAS  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Despres JP. Excess visceral adipose tissue/ectopic fat the missing link in the obesity paradox? J Am Coll Cardiol. 2011;57:1887–9.

    Article  Google Scholar 

  21. 21.

    Preis SR, Massaro JM, Robins SJ, Hoffmann U, Vasan RS, Irlbeck T, et al. Abdominal subcutaneous and visceral adipose tissue and insulin resistance in the Framingham heart study. Obesity (Silver Spring). 2010;18:2191–8.

    Article  Google Scholar 

  22. 22.

    Kelley DE, Thaete FL, Troost F, Huwe T, Goodpaster BH. Subdivisions of subcutaneous abdominal adipose tissue and insulin resistance. Am J Physiol Endocrinol Metab. 2000;278:E941–8.

    CAS  Article  Google Scholar 

  23. 23.

    Fox CS, Massaro JM, Hoffmann U, Pou KM, Maurovich-Horvat P, Liu CY, et al. Abdominal visceral and subcutaneous adipose tissue compartments: association with metabolic risk factors in the Framingham Heart Study. Circulation. 2007;116:39–48.

    Article  Google Scholar 

  24. 24.

    Fujioka S, Matsuzawa Y, Tokunaga K, Tarui S. Contribution of intra-accumulation to the impairment of glucose and lipid metabolism in human obesity. Metabolism. 1987;36:54–9.

    CAS  Article  Google Scholar 

  25. 25.

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

    CAS  Article  Google Scholar 

  26. 26.

    Despres JP, Lemieux I. Abdominal obesity and metabolic syndrome. Nature. 2006;444:881–7.

    CAS  Article  Google Scholar 

  27. 27.

    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;10:868–74.

    Article  Google Scholar 

  28. 28.

    Bouchard C, Tremblay A, Despres JP, Nadeau A, Lupien PJ, Theriault G, et al. The response to long-term overfeeding in identical twins. N Engl J Med. 1990;322:1477–82.

    CAS  Article  Google Scholar 

  29. 29.

    Kimura T, Deshpande GA, Urayama KY, Masuda K, Fukui T, Matsuyama Y. Association of weight gain since age 20 with non-alcoholic fatty liver disease in normal weight individuals. J Gastroenterol Hepatol. 2015;30:909–17.

    Article  Google Scholar 

  30. 30.

    Gast KB, Smit JW, den Heijer M, Middeldorp S, Rippe RC, le Cessie S, et al. Abdominal adiposity largely explains associations between insulin resistance, hyperglycemia and subclinical atherosclerosis: the NEO study. Atherosclerosis. 2013;229:423–9.

    CAS  Article  Google Scholar 

  31. 31.

    Despres JP. Abdominal obesity as important component of insulin-resistance syndrome. Nutrition. 1993;9:452–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  32. 32.

    Singh P, Somers VK, Romero-Corral A, Sert-Kuniyoshi FH, Pusalavidyasagar S, Davison DE, et al. Effects of weight gain and weight loss on regional fat distribution. Am J Clin Nutr. 2012;96:229–33.

    CAS  Article  Google Scholar 

  33. 33.

    Szczepaniak LS, Nurenberg P, Leonard D, Browning JD, Reingold JS, Grundy S, et al. Magnetic resonance spectroscopy to measure hepatic triglyceride content: prevalence of hepatic steatosis in the general population. Am J Physiol Endocrinol Metab. 2005;288:E462–8.

    CAS  Article  Google Scholar 

  34. 34.

    Korn EL, Graubard BI. Epidemiologic studies utilizing surveys: accounting for the sampling design. Am J Public Health. 1991;81:1166–73.

    CAS  Article  Google Scholar 

  35. 35.

    Lumley T. Analysis of complex survey samples. J Statist Softw. 2004;9:1–19.

    Article  Google Scholar 

  36. 36.

    Ministerie van VWS. Hoveel mensen hebben overgewicht? Accessed at on January 16, 2018.

  37. 37.

    World Health Organization (WHO). Obesity and overweight. Fact sheet No 311. Accessed at on January 16, 2018.

  38. 38.

    Casey VA, Dwyer JT, Berkey CS, Coleman KA, Gardner J, Valadian I. Long-term memory of body weight and past weight satisfaction: a longitudinal follow-up study. Am J Clin Nutr. 1991;53:1493–8.

    CAS  Article  Google Scholar 

  39. 39.

    Spalding KL, Arner E, Westermark PO, Bernard S, Buchholz BA, Bergmann O, et al. Dynamics of fat cell turnover in humans. Nature. 2008;453:783–7.

    CAS  Article  Google Scholar 

  40. 40.

    Brochu M, Tchernof A, Dionne IJ, Sites CK, Eltabbakh GH, Sims EA, et al. What are the physical characteristics associated with a normal metabolic profile despite a high level of obesity in postmenopausal women? J Clin Endocrinol Metab. 2001;86:1020–5.

    CAS  PubMed  PubMed Central  Google Scholar 

  41. 41.

    Muscelli E, Camastra S, Gastaldelli A, Natali A, Masoni A, Pecori N, et al. Influence of duration of obesity on the insulin resistance of obese non-diabetic patients. Int J Obes Relat Metab Disord. 1998;22:262–7.

    CAS  Article  Google Scholar 

  42. 42.

    Tamakoshi K, Yatsuya H, Kondo T, Hirano T, Hori Y, Yoshida T, et al. The accuracy of long-term recall of past body weight in Japanese adult men. Int J Obes Relat Metab Disord. 2003;27:247–52.

    CAS  Article  Google Scholar 

  43. 43.

    de Mutsert R, den Heijer M, Rabelink TJ, Smit JW, Romijn JA, Jukema JW, et al. The Netherlands Epidemiology of Obesity (NEO) study: study design and data collection. Eur J Epidemiol. 2013;28:513–23.

    Article  Google Scholar 

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We express our gratitude to all individuals who participate in the Netherlands Epidemiology of Obesity study. We are grateful to all participating general practitioners for inviting eligible participants. We furthermore thank P.R. van Beelen and all research nurses for collecting the data and P.J. Noordijk and her team for sample handling and storage and I. de Jonge, M.Sc. for data management of the NEO study.


The NEO study is supported by the participating Departments, the Division and the Board of Directors of the Leiden University Medical Centre, and by the Leiden University, Research Profile Area ‘Vascular and Regenerative Medicine’. D.v.H. was supported by the European Commission funded project HUMAN (Health-2013-INNOVATION-1-602757).

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Correspondence to Renée de Mutsert.

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Verkouter, I., Noordam, R., de Roos, A. et al. Adult weight change in relation to visceral fat and liver fat at middle age: The Netherlands epidemiology of obesity study. Int J Obes 43, 790–799 (2019).

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