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:

Adipocyte and Cell Biology

Abdominal subcutaneous adipose tissue cellularity in men and women

International Journal of Obesity volume 41, pages 1564–1569 (2017)Cite this article

Subjects

Abstract

Background/Objective:

Differences in subcutaneous abdominal adipose tissue (SAT) fat cell size and number (cellularity) are linked to insulin resistance. Men are generally more insulin resistant than women but it is unknown whether there is a gender dimorphism in SAT cellularity. The objective was to determine SAT cellularity and its relationship to insulin sensitivity in men and women.

Methods:

In a cohort study performed at an outpatient academic clinic in Sweden, 798 women and 306 men were included. Estimated SAT mass (ESAT) was derived from measures of dual-energy X-ray absorptiometry and a formula. SAT biopsies were obtained to measure mean fat cell size; SAT adipocyte number was obtained by dividing ESAT with mean fat cell weight. Fat cell size was also compared with level of insulin sensitivity in vivo.

Results:

Over the entire range of body mass index (BMI) both fat cell size and number correlated positively with ESAT in either sex. On average, fat cell size was larger in men than in women, which was driven by significantly larger fat cells in non-obese men compared with non-obese women; no gender effect on fat cell size was seen in obese subjects. For all subjects fat cell number was larger in women than men, which was driven by a gender effect among non-obese individuals (P<0.0001). The relationship between fat cell size and insulin resistance was significant in both genders (P<0.0001) but steeper in men than in women (F=19, P<0.0001).

Conclusions:

Although both fat cell size and number determine SAT mass, adipocyte number contributes more and size less in women than in men and this is most evident in non-obese subjects. Over the entire BMI range, fat cell size contributes stronger to insulin resistance in men.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1
Figure 2

Similar content being viewed by others

References

  1. Salans LB, Cushman SW, Weismann RE . Studies of human adipose tissue. Adipose cell size and number in nonobese and obese patients. J Clin Invest 1973; 52: 929–941.

    Article  CAS  Google Scholar 

  2. Bjorntorp P . Sjostrom L,+SJOSTROM L: Number and size of adipose tissue fat cells in relation to metabolism in human obesity. Metabolism 1971; 20: 703–713.

    Article  CAS  Google Scholar 

  3. Hirsch J, Batchelor B . Adipose tissue cellularity in human obesity. Clin Endocrinol Metab 1976; 5: 299–311.

    Article  CAS  Google Scholar 

  4. Arner E, Westermark PO, Spalding KL, Britton T, Ryden M, Frisen J et al. Adipocyte turnover: relevance to human adipose tissue morphology. Diabetes 2010; 59: 105–109.

    Article  CAS  Google Scholar 

  5. Ktotkiewski M, Sjostrom L, Bjorntorp P, Smith U . Regional adipose tissue cellularity in relation to metabolism in young and middle-aged women. Metabolism 1975; 24: 703–710.

    Article  CAS  Google Scholar 

  6. Stern JS, Batchelor BR, Hollander N, Cohn CK, Hirsch J . Adipose-cell size and immunoreactive insulin levels in obese and normal-weight adults. Lancet 1972; 2: 948–951.

    Article  CAS  Google Scholar 

  7. Salans LB, Knittle JL, Hirsch J . The role of adipose cell size and adipose tissue insulin sensitivity in the carbohydrate intolerance of human obesity. J Clin Invest 1968; 47: 153–165.

    Article  CAS  Google Scholar 

  8. Weyer C, Foley JE, Bogardus C, Tataranni PA, Pratley RE . Enlarged subcutaneous abdominal adipocyte size, but not obesity itself, predicts type II diabetes independent of insulin resistance. Diabetologia 2000; 43: 1498–1506.

    Article  CAS  Google Scholar 

  9. Lonn M, Mehlig K, Bengtsson C, Lissner L . Adipocyte size predicts incidence of type 2 diabetes in women. FASEB J 2010; 24: 326–331.

    Article  Google Scholar 

  10. Arner P, Andersson DP, Thorne A, Wiren M, Hoffstedt J, Naslund E et al. Variations in the size of the major omentum are primarily determined by fat cell number. J Clin Endocrinol Metab 2013; 98: E897–E901.

    Article  Google Scholar 

  11. Tchoukalova YD, Votruba SB, Tchkonia T, Giorgadze N, Kirkland JL, Jensen MD . Regional differences in cellular mechanisms of adipose tissue gain with overfeeding. Proc Natl Acad Sci USA 2010; 107: 18226–18231.

    Article  CAS  Google Scholar 

  12. Knittle JL, Timmers K, Ginsberg-Fellner F, Brown RE, Katz DP . The growth of adipose tissue in children and adolescents. Cross-sectional and longitudinal studies of adipose cell number and size. J Clin Invest 1979; 63: 239–246.

    Article  CAS  Google Scholar 

  13. Geer EB, Shen W . Gender differences in insulin resistance, body composition, and energy balance. Gender Med 2009; 6: 60–75.

    Article  Google Scholar 

  14. Sattar N . Gender aspects in type 2 diabetes mellitus and cardiometabolic risk. Best Pract Res Clin Endocrinol Metab 2013; 27: 501–507.

    Article  CAS  Google Scholar 

  15. Bjorntorp P, Bengtsson C, Blohme G, Jonsson A, Sjostrom L, Tibblin E et al. Adipose tissue fat cell size and number in relation to metabolism in randomly selected middle-aged men and women. Metabolism 1971; 20: 927–935.

    Article  CAS  Google Scholar 

  16. Sjostrom L, Smith U, Krotkiewski M, Bjorntorp P . Cellularity in different regions of adipose tissue in young men and women. Metabolism 1972; 21: 1143–1153.

    Article  CAS  Google Scholar 

  17. Tchoukalova YD, Koutsari C, Votruba SB, Tchkonia T, Giorgadze N, Thomou T et al. Sex- and depot-dependent differences in adipogenesis in normal-weight humans. Obesity (Silver Spring) 2010; 18: 1875–1880.

    Article  Google Scholar 

  18. Lee K, Lee S, Kim YJ . Waist circumference, dual-energy X-ray absortiometrically measured abdominal adiposity, and computed tomographically derived intra-abdominal fat area on detecting metabolic risk factors in obese women. Nutrition 2008; 24: 625–631.

    Article  Google Scholar 

  19. Kaul S, Rothney MP, Peters DM, Wacker WK, Davis CE, Shapiro MD et al. Dual-energy X-ray absorptiometry for quantification of visceral fat. Obesity (Silver Spring) 2012; 20: 1313–1318.

    Article  Google Scholar 

  20. Andersson DP, Eriksson Hogling D, Thorell A, Toft E, Qvisth V, Naslund E et al. Changes in subcutaneous fat cell volume and insulin sensitivity after weight loss. Diabetes Care 2014; 37: 1831–1836.

    Article  CAS  Google Scholar 

  21. Strawbridge RJ, Laumen H, Hamsten A, Breier M, Grallert H, Hauner H et al. Effects of genetic loci associated with central obesity on adipocyte lipolysis. PLoS One 2016; 11: e0153990.

    Article  Google Scholar 

  22. Gallagher D, Visser M, Sepulveda D, Pierson RN, Harris T, Heymsfield SB . How useful is body mass index for comparison of body fatness across age, sex, and ethnic groups? Am J Epidemiol 1996; 143: 228–239.

    Article  CAS  Google Scholar 

  23. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC . Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985; 28: 412–419.

    Article  CAS  Google Scholar 

  24. Bolinder J, Ostman J, Arner P . Postreceptor defects causing insulin resistance in normoinsulinemic non-insulin-dependent diabetes mellitus. Diabetes 1982; 31: 911–916.

    Article  CAS  Google Scholar 

  25. Hoffstedt J, Andersson DP, Eriksson Hogling D, Theorell J, Naslund E, Thorell A et al. Long-term protective changes in adipose tissue after gastric bypass. Diabetes Care 2017; 40: 77–84.

    Article  CAS  Google Scholar 

  26. Ryden M, Andersson DP, Bergstrom IB, Arner P . Adipose tissue and metabolic alterations: regional differences in fat cell size and number matter, but differently: a cross-sectional study. J Clin Endocrinol Metab 2014; 99: E1870–E1876.

    Article  CAS  Google Scholar 

  27. Goldrick RB, McLoughlin GM . Lipolysis and lipogenesis from glucose in human fat cells of different sizes. Effects of insulin, epinephrine, and theophylline. J Clin Invest 1970; 49: 1213–1223.

    Article  CAS  Google Scholar 

  28. Tchoukalova YD, Harteneck DA, Karwoski RA, Tarara J, Jensen MD . A quick, reliable, and automated method for fat cell sizing. J Lipid Res 2003; 44: 1795–1801.

    Article  CAS  Google Scholar 

  29. Cushman SW, Salans LB . Determinations of adipose cell size and number in suspensions of isolated rat and human adipose cells. J Lipid Res 1978; 19: 269–273.

    CAS  PubMed  Google Scholar 

  30. McLaughlin T, Sherman A, Tsao P, Gonzalez O, Yee G, Lamendola C et al. Enhanced proportion of small adipose cells in insulin-resistant vs insulin-sensitive obese individuals implicates impaired adipogenesis. Diabetologia 2007; 50: 1707–1715.

    Article  CAS  Google Scholar 

  31. Spalding KL, Arner E, Westermark PO, Bernard S, Buchholz BA, Bergmann O et al. Dynamics of fat cell turnover in humans. Nature 2008; 453: 783–787.

    Article  CAS  Google Scholar 

  32. Hellevik O . Linear versus logistic regression when the dependent variable is a dichotomy. Qual Quant 2009; 43: 59–74.

    Article  Google Scholar 

  33. Tchoukalova YD, Koutsari C, Karpyak MV, Votruba SB, Wendland E, Jensen MD . Subcutaneous adipocyte size and body fat distribution. Am J Clin Nutr 2008; 87: 56–63.

    Article  CAS  Google Scholar 

  34. Karastergiou K, Smith SR, Greenberg AS, Fried SK . Sex differences in human adipose tissues - the biology of pear shape. Biol Sex Differ 2012; 3: 13.

    Article  Google Scholar 

  35. White UA, Tchoukalova YD . Sex dimorphism and depot differences in adipose tissue function. Biochim Biophys Acta 2014; 1842: 377–392.

    Article  CAS  Google Scholar 

  36. Bonora E, Moghetti P, Zancanaro C, Cigolini M, Querena M, Cacciatori V et al. Estimates of in vivo insulin action in man: comparison of insulin tolerance tests with euglycemic and hyperglycemic glucose clamp studies. J Clin Endocrinol Metab 1989; 68: 374–378.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Katarina Hertel, Britt-Marie Leijonhufvud and Yvonne Widlund for performing clinical examinations and technicians Elisabeth Dungner, Eva Sjölin and Kerstin Wåhlen for their measures of fat cell diameter throughout the study. This work was supported by grants from the Swedish Research Council, The Swedish Diabetes Foundation, Center for Innovative Medicine, the Diabetes Theme Center at Karolinska Institutet, the Tore Nilsson Foundation, the Stockholm County Council and the Novo Nordisk Foundation including the Tripartite Immuno-metabolism Consortium (TrIC) Grant Number NNF15CC0018486 and the MSAM consortium NNF15SA0018346.

Author contributions

PA conceived the study, collected all the data, wrote the first version of the manuscript and is the guarantor of the data. EA, MR, DEH and DPA generated data and prepared figures/tables. EA; MR, DPA and PA, analyzed data. All authors read and contributed to the final version of the manuscript.

Author information

Authors and Affiliations

  1. Department of Medicine, Karolinska Institutet and Karolinska University Hospital, Stockholm, Sweden

    D P Andersson, E Arner, D E Hogling, M Rydén & P Arner

  2. RIKEN Center for Life Science Technologies, Molecular Network Control Genomics Unit, Yokohama, Kanaga-wa, Japan

    E Arner

Authors
  1. D P Andersson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E Arner
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D E Hogling
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M Rydén
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. P Arner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P Arner.

Ethics declarations

Competing interests

The authors declare no conflict of interest.

Additional information

Supplementary Information accompanies this paper on International Journal of Obesity website

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Andersson, D., Arner, E., Hogling, D. et al. Abdominal subcutaneous adipose tissue cellularity in men and women. Int J Obes 41, 1564–1569 (2017). https://doi.org/10.1038/ijo.2017.148

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ijo.2017.148

This article is cited by

Search

Advanced search

Quick links