Predictors of abdominal adipose tissue compartments: 18-year follow-up of young men with and without family history of diabetes

Published:December 17, 2015DOI:


      • 18-year follow-up study of insulin sensitivity
      • Adipose tissue compartments evaluated with CT at follow-up
      • Traditional cardiovascular risk markers are predictors of abdominal adipose tissue.
      • Family history of diabetes increases unfavorable adipose tissue.
      • Current cardiometabolic status is most important for those without family diabetes.



      Abdominal adipose tissue (AAT) consists of visceral adipose tissue (VAT) and subcutaneous adipose tissue (SAT), which can be further divided into superficial and deep SAT. Despite being a key factor in the development of metabolic and cardiovascular diseases, what predicts future amount of AAT is largely unknown.


      To determine long-term predictors of amount of AAT.


      This was a mean 18-year follow-up study of a cohort of 94 healthy young Caucasian men, with and without a family history of diabetes (FHD). Cardiovascular risk markers were examined both at baseline and at follow-up. At follow-up, computed tomography (CT) of AAT was conducted to assess amount of superficial and deep SAT, and VAT.


      In multiple regression analyses, baseline body mass index (BMI) remained a positive predictor of future amount of superficial and deep SAT, while high-density lipoprotein (HDL) cholesterol was a negative predictor of all three sub-compartments. Baseline risk markers were generally stronger predictors among men with FHD, than among men without. In addition, FHD had greater impact on amount of deep SAT and VAT, than on amount of superficial SAT.


      Our data suggest that the traditional cardiovascular risk markers BMI, HDL cholesterol and family history of diabetes are long-term predictors of the different abdominal adipose tissue compartments from young towards middle age in healthy men. In men with family history of diabetes, cardiovascular risk markers at a young age seem to be of greater importance to future amount of abdominal adipose tissue, than among men without.


      AAT (abdominal adipose tissue), BP (blood pressure), CT (computed tomography), FHD (family history of diabetes), GDR (glucose disposal rate), HT (hypertension), MST (mental stress test), SAT (subcutaneous adipose tissue), TGs (triglycerides), VAT (visceral adipose tissue)


      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'


      Subscribe to European Journal of Internal Medicine
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect


        • World Health Organization
        Obesity and overweight.
        (Internet) (Accessed 20 March 2015)
        • Tchernof A.
        • Despres J.P.
        Pathophysiology of human visceral obesity: an update.
        Physiol Rev. 2013; 93: 359-404
        • Golan R.
        • Shelef I.
        • Rudich A.
        • Gepner Y.
        • Shemesh E.
        • Chassidim Y.
        • et al.
        Abdominal superficial subcutaneous fat: a putative distinct protective fat subdepot in type 2 diabetes.
        Diabetes Care. 2012; 35: 640-647
        • Kelley D.E.
        • Thaete F.L.
        • Troost F.
        • Huwe T.
        • Goodpaster B.H.
        Subdivisions of subcutaneous abdominal adipose tissue and insulin resistance.
        Am J Physiol Endocrinol Metab. 2000; 278: E941-E948
        • Smith S.R.
        • Lovejoy J.C.
        • Greenway F.
        • Ryan D.
        • de Jonge L.
        • dela Bretonne J.
        • et al.
        Contributions of total body fat, abdominal subcutaneous adipose tissue compartments, and visceral adipose tissue to the metabolic complications of obesity.
        Metabolism. 2001; 50: 425-435
        • Henninger A.M.
        • Eliasson B.
        • Jenndahl L.E.
        • Hammarstedt A.
        Adipocyte hypertrophy, inflammation and fibrosis characterize subcutaneous adipose tissue of healthy, non-obese subjects predisposed to type 2 diabetes.
        PLoS One. 2014; 9: e105262
        • Masuo K.
        • Lambert G.W.
        Relationships of adrenoceptor polymorphisms with obesity.
        J Obes. 2011; 2011: 609485
        • Grassi G.
        • Dell'Oro R.
        • Facchini A.
        • Quarti Trevano F.
        • Bolla G.B.
        • Mancia G.
        Effect of central and peripheral body fat distribution on sympathetic and baroreflex function in obese normotensives.
        J Hypertens. 2004; 22: 2363-2369
        • Reims H.M.
        • Fossum E.
        • Høieggen A.
        • Moan A.
        • Eide I.
        • Kjeldsen S.E.
        Adrenal medullary overactivity in lean, borderline hypertensive young men.
        Am J Hypertens. 2004; 17: 611-618
        • Flaa A.
        • Sandvik L.
        • Kjeldsen S.E.
        • Eide I.K.
        • Rostrup M.
        Does sympathoadrenal activity predict changes in body fat? An 18-y follow-up study.
        Am J Clin Nutr. 2008; 87: 1596-1601
        • Tong J.
        • Fujimoto W.Y.
        • Kahn S.E.
        • Weigle D.S.
        • McNeely M.J.
        • Leonetti D.L.
        • et al.
        Insulin, C-peptide, and leptin concentrations predict increased visceral adiposity at 5- and 10-year follow-ups in nondiabetic Japanese Americans.
        Diabetes. 2005; 54: 985-990
        • Moan A.
        • Nordby G.
        • Rostrup M.
        • Eide I.
        • Kjeldsen S.E.
        Insulin sensitivity, sympathetic activity, and cardiovascular reactivity in young men.
        Am J Hypertens. 1995; 8: 268-275
        • Høieggen A.
        • Fossum E.
        • Moan A.
        • Rostrup M.
        • Eide I.K.
        • Kjeldsen S.E.
        Effects of hyperinsulinemia on sympathetic responses to mental stress.
        Am J Hypertens. 2000; 13: 21-28
        • Fossum E.
        • Høieggen A.
        • Moan A.
        • Rostrup M.
        • Nordby G.
        • Kjeldsen S.E.
        Relationship between insulin sensitivity and maximal forearm blood flow in young men.
        Hypertension. 1998; 32: 838-843
        • Reims H.M.
        • Sevre K.
        • Fossum E.
        • Høieggen A.
        • Mellem H.
        • Kjeldsen S.E.
        Relations between insulin sensitivity, fitness and autonomic cardiac regulation in healthy, young men.
        J Hypertens. 2004; 22: 2007-2015
        • Høieggen A.
        • Fossum E.
        • Moan A.
        • Rostrup M.
        • Eide I.K.
        • Kjeldsen S.E.
        Biphasic effect of epinephrine on blood glucose during hyperinsulinemia in borderline hypertensive young men.
        Am J Hypertens. 2001; 14: 539-545
        • DeFronzo R.A.
        • Tobin J.D.
        • Andres R.
        Glucose clamp technique: a method for quantifying insulin secretion and resistance.
        Am J Physiol. 1979; 237: E214-E223
        • Aksnes T.A.
        • Reims H.M.
        • Guptha S.
        • Moan A.
        • Os I.
        • Kjeldsen S.E.
        Improved insulin sensitivity with the angiotensin II-receptor blocker losartan in patients with hypertension and other cardiovascular risk factors.
        J Hum Hypertens. 2006; 20: 860-866
        • Moan A.
        • Nordby G.
        • Os I.
        • Birkeland K.I.
        • Kjeldsen S.E.
        Relationship between hemorrheologic factors and insulin sensitivity in healthy young men.
        Metabolism. 1994; 43: 423-427
        • Fossum E.
        • Høieggen A.
        • Moan A.
        • Nordby G.
        • Kjeldsen S.E.
        Insulin sensitivity relates to other cardiovascular risk factors in young men: validation of some modifications of the hyperinsulinaemic, isoglycaemic glucose clamp technique.
        Blood Press Suppl. 1997; 2: 113-119
        • Skårn S.N.
        • Flaa A.
        • Kjeldsen S.E.
        • Rostrup M.
        • Brunborg C.
        • Reims H.M.
        • et al.
        High screening blood pressure at young age predicts future masked hypertension: a 17 year follow-up study.
        Blood Press. 2015; 24: 131-138
        • World Health Organization
        Obesity: preventing and managing the global epidemic. Report of a WHO consultation.
        World Health Organ Tech Rep Ser. 2000; 894: 1-253
        • Katz M.H.
        Multivariable analyses: a practical guide for clinicians and public health researchers.
        Cambridge University Press, UK2011
        • Skårn S.N.
        • Flaa A.
        • Kjeldsen S.E.
        • Rostrup M.
        • Brunborg C.
        • Reims H.M.
        • et al.
        Family history of hypertension and triglycerides predict future insulin sensitivity: a 17-year follow-up study of young men.
        J Hypertens. 2015; 33: 1845-1852
        • Alexopoulos N.
        • Katritsis D.
        • Raggi P.
        Visceral adipose tissue as a source of inflammation and promoter of atherosclerosis.
        Atherosclerosis. 2014; 233: 104-112
        • Cederberg H.
        • Stancakova A.
        • Kuusisto J.
        • Laakso M.
        • Smith U.
        Family history of type 2 diabetes increases the risk of both obesity and its complications: is type 2 diabetes a disease of inappropriate lipid storage?.
        J Intern Med. 2014; 277: 540-551
        • Jones A.
        • McMillan M.R.
        • Jones R.W.
        • Kowalik G.T.
        • Steeden J.A.
        • Deanfield J.E.
        • et al.
        Adiposity is associated with blunted cardiovascular, neuroendocrine and cognitive responses to acute mental stress.
        PLoS One. 2012; 7: e39143
        • Wardle J.
        • Chida Y.
        • Gibson E.L.
        • Whitaker K.L.
        • Steptoe A.
        Stress and adiposity: a meta-analysis of longitudinal studies.
        Obesity. 2011; 19: 771-778
        • Carroll D.
        • Phillips A.C.
        • Der G.
        Body mass index, abdominal adiposity, obesity, and cardiovascular reactions to psychological stress in a large community sample.
        Psychosom Med. 2008; 70: 653-660
        • Hassellund S.S.
        • Flaa A.
        • Sandvik L.
        • Kjeldsen S.E.
        • Rostrup M.
        Long-term stability of cardiovascular and catecholamine responses to stress tests: an 18-year follow-up study.
        Hypertension. 2010; 55: 131-136
        • Huggett R.J.
        • Hogarth A.J.
        • Mackintosh A.F.
        • Mary D.A.
        Sympathetic nerve hyperactivity in non-diabetic offspring of patients with type 2 diabetes mellitus.
        Diabetologia. 2006; 49: 2741-2744
        • Skretteberg P.T.
        • Grundvold I.
        • Kjeldsen S.E.
        • Erikssen J.E.
        • Sandvik L.
        • Liestol K.
        • et al.
        HDL-cholesterol and prediction of coronary heart disease: modified by physical fitness? A 28-year follow-up of apparently healthy men.
        Atherosclerosis. 2012; 220: 250-256
        • Riserus U.
        • Arnlov J.
        • Berglund L.
        Long-term predictors of insulin resistance: role of lifestyle and metabolic factors in middle-aged men.
        Diabetes Care. 2007; 30: 2928-2933
        • Wilsgaard T.
        • Jacobsen B.K.
        • Schirmer H.
        • Thune I.
        • Lochen M.L.
        • Njolstad I.
        • et al.
        Tracking of cardiovascular risk factors: the Tromso study, 1979–1995.
        Am J Epidemiol. 2001; 154: 418-426
        • Eisenmann J.C.
        • Welk G.J.
        • Wickel E.E.
        • Blair S.N.
        Stability of variables associated with the metabolic syndrome from adolescence to adulthood: the Aerobics Center Longitudinal Study.
        Am J Hum Biol. 2004; 16: 690-696
        • Wolfs M.G.
        • Rensen S.S.
        • Bruin-Van Dijk E.J.
        • Verdam F.J.
        • Greve J.W.
        • Sanjabi B.
        • et al.
        Co-expressed immune and metabolic genes in visceral and subcutaneous adipose tissue from severely obese individuals are associated with plasma HDL and glucose levels: a microarray study.
        BMC Med Genomics. 2010; 3: 34
        • Sam S.
        • Haffner S.
        • Davidson M.H.
        • D'Agostino Sr., R.B.
        • Feinstein S.
        • Kondos G.
        • et al.
        Relationship of abdominal visceral and subcutaneous adipose tissue with lipoprotein particle number and size in type 2 diabetes.
        Diabetes. 2008; 57: 2022-2027
        • Voight B.F.
        • Peloso G.M.
        • Orho-Melander M.
        • Frikke-Schmidt R.
        • Barbalic M.
        • Jensen M.K.
        • et al.
        Plasma HDL cholesterol and risk of myocardial infarction: a Mendelian randomisation study.
        Lancet. 2012; 380: 572-580
        • Skretteberg P.T.
        • Grytten A.N.
        • Gjertsen K.
        • Grundvold I.
        • Kjeldsen S.E.
        • Erikssen J.
        • et al.
        Triglycerides–diabetes association in healthy middle-aged men: modified by physical fitness? A long term follow-up of 1962 Norwegian men in the Oslo Ischemia Study.
        Diabetes Res Clin Pract. 2013; 101: 201-209
        • Marinou K.
        • Hodson L.
        • Vasan S.K.
        • Fielding B.A.
        • Banerjee R.
        • Brismar K.
        • et al.
        Structural and functional properties of deep abdominal subcutaneous adipose tissue explain its association with insulin resistance and cardiovascular risk in men.
        Diabetes Care. 2014; 37: 821-829
        • Papadopoulos D.P.
        • Makris T.K.
        • Perrea D.
        • Papazachou O.
        • Daskalaki M.
        • Sanidas E.
        • et al.
        Adiponectin–insulin and resistin plasma levels in young healthy offspring of patients with essential hypertension.
        Blood Press. 2008; 17: 50-54
        • Sull J.W.
        • Kim H.J.
        • Yun J.E.
        • Kim G.
        • Park E.J.
        • Kim S.
        • et al.
        Serum adiponectin is associated with family history of diabetes independently of obesity and insulin resistance in healthy Korean men and women.
        Eur J Endocrinol Eur Fed Endocr Soc. 2009; 160: 39-43
        • Furuhashi M.
        • Ura N.
        • Higashiura K.
        • Miyazaki Y.
        • Murakami H.
        • Hyakukoku M.
        • et al.
        Low adiponectin level in young normotensive men with a family history of essential hypertension.
        Hypertens Res. 2005; 28: 141-146
        • Vega G.L.
        • Grundy S.M.
        Metabolic risk susceptibility in men is partially related to adiponectin/leptin ratio.
        J Obes. 2013; 2013: 409679
        • Matsuzawa Y.
        Adiponectin: a key player in obesity related disorders.
        Curr Pharm Des. 2010; 16: 1896-1901
        • Hu G.
        • Jousilahti P.
        • Tuomilehto J.
        Joint effects of history of hypertension at baseline and type 2 diabetes at baseline and during follow-up on the risk of coronary heart disease.
        Eur Heart J. 2007; 28: 3059-3066
        • Jandeleit-Dahm K.
        • Cooper M.E.
        Hypertension and diabetes: role of the renin–angiotensin system.
        Endocrinol Metab Clin North Am. 2006; 35 (vii): 469-490
        • Nazare J.A.
        • Smith J.D.
        • Borel A.L.
        • Haffner S.M.
        • Balkau B.
        • Ross R.
        • et al.
        Ethnic influences on the relations between abdominal subcutaneous and visceral adiposity, liver fat, and cardiometabolic risk profile: the International Study of Prediction of Intra-Abdominal Adiposity and Its Relationship With Cardiometabolic Risk/Intra-Abdominal Adiposity.
        Am J Clin Nutr. 2012; 96: 714-726
        • Arner P.
        • Arner E.
        • Hammarstedt A.
        • Smith U.
        Genetic predisposition for Type 2 diabetes, but not for overweight/obesity, is associated with a restricted adipogenesis.
        PLoS One. 2011; 6: e18284
        • Laaksonen D.E.
        • Lindstrom J.
        • Lakka T.A.
        • Eriksson J.G.
        • Niskanen L.
        • Wikstrom K.
        • et al.
        Physical activity in the prevention of type 2 diabetes: the Finnish diabetes prevention study.
        Diabetes. 2005; 54: 158-165
        • Mayes J.S.
        • Watson G.H.
        Direct effects of sex steroid hormones on adipose tissues and obesity.
        Obes Rev. 2004; 5: 197-216