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Sex Differences

Defining CMR - Visceral Adipose Tissue: the Culprit? Causes and Correlates of Visceral Obesity

Key Points

There is a definite sex difference in adipose tissue distribution:

  • Men accumulate adipose tissue in the visceral cavity (apple pattern).
  • Women accumulate adipose tissue in the gluteal/femoral depots (pear pattern).
  • Visceral adipose tissue accumulation—the adipose tissue distribution pattern generally found in men—predicts greater obesity-related health risks.
  • Pre-menopausal women have less visceral adipose tissue and a more favourable metabolic risk profile than men with similar total body fat. This protection against visceral fat accumulation is lost when women enter menopause.

A Question of Sex: Apples and Pears…

It is well known that visceral adipose tissue increases with age, regardless of sex [1]. It is also known that adipose tissue distribution differs markedly between men and women. Men are more likely to accumulate adipose tissue in the upper body (trunk, abdomen), whereas women usually accumulate adipose tissue in the lower body (hips, thighs) [2-4].

In the 1940s, professor Jean Vague of the University of Marseille was the first to highlight the importance of regional adipose tissue distribution as a correlate of obesity complications [4]. He used the term “android obesity” to refer to adipose tissue accumulation in the trunk area and the term “gynoid obesity” to refer to adipose tissue accumulation in the hips and thighs, typically in pre-menopausal women. This adipose tissue distribution is also associated to the apple and pear shapes (Figure). Vague also emphasized the health hazards associated with the android pattern of adipose tissue distribution usually observed in men as compared to the lower-risk gynoid pattern mostly observed in women. In fact, even in the absence of sophisticated laboratory methods, Vague was the first to propose that android obesity was more frequently associated with type 2 diabetes and coronary heart disease than gynoid obesity.

Thirty-five years later, Krotkiewski et al. [5] suggested that sex hormones might be involved in regulating the typical sex differences in regional body fat distribution. Their seminal work suggested that these differences were mainly due to the number of local fat cells: men had more fat cells in the abdominal region while women had more fat cells in the gluteal/femoral adipose depots [5]. They also observed that this regional adipose tissue distribution was unrelated to the presence or absence of obesity.

Abdominal adipose tissue is composed of visceral and subcutaneous adipose tissue, both of which can be accurately measured using imaging techniques. Anthropometric measurements such as waist circumference are useful tools in clinical practice to estimate the amount of abdominal fat, but these measurements cannot differentiate between subcutaneous and visceral adipose tissue compartments. Using computed tomography, it was found that the amount of visceral adipose tissue is, on average, twice as high in men as in pre-menopausal women [6]. In men, visceral accumulation generally increases with the amount of total body fat whereas in women, the volume of visceral adipose tissue is less affected by the amount of total body fat compared to men [6].

In another study [7], even after correcting for total body fat mass, women had a lower ratio of visceral adipose tissue to total body fat mass as compared to men. Estimated total visceral adipose tissue volume was 5.23 ± 2.39 L in men and 3.61 ± 1.91 L in women. Women had less visceral adipose tissue even though they had higher body mass index, total body fat, and abdominal subcutaneous adipose tissue values.

Pre-menopausal women can therefore “afford” to accumulate a substantial amount of total body fat. However, for the same increase in total body fat mass, subcutaneous adipose tissue accumulation has been found to be comparable in both sexes, although men have more visceral adipose tissue. These results support the idea that, in pre-menopausal women, subcutaneous adipose tissue is more likely to accumulate in both the abdominal and gluteal/femoral adipose depots.

Through computed tomography and magnetic resonance imaging, several groups [8-10] have suggested using waist circumference measurement as an index of abdominal adipose tissue deposition in both men and women. Similarly, using anthropometric measurement to predict visceral adiposity, it has been found that for a given waist circumference, women generally have greater body fat mass and abdominal subcutaneous adipose tissue than men [10,11]. Moreover, through magnetic resonance imaging, Kuk et al. [11] demonstrated that for the same waist circumference, men had more visceral adipose tissue than women. They also found that for a given increase in waist girth, men had a greater accumulation of visceral adiposity than did women.

Kotani et al. [1] also noted a clear sex difference when comparing regional adipose tissue distribution—abdominal adipose tissue accumulation in particular—across age groups. For instance, visceral adipose tissue deposition was found to increase with age mostly in men and menopausal and post-menopausal women. The influence of age and menopause will be discussed elsewhere (Influence of Age and Influence of Menopause).

Figure:
Adipose tissue distribution in men and women

Metabolic Consequences of Sex Differences in Regional Adipose Tissue Distribution

Men generally have more visceral adipose tissue than women, and women have more subcutaneous fat than men. It has been shown that visceral adipose tissue is a significant correlate of alterations in glucose tolerance and plasma lipoprotein-lipid levels, independent of total adiposity and abdominal subcutaneous adipose tissue [12-16]. In this regard, it has been suggested that the sex difference in the cardiovascular disease risk observed between men and pre-menopausal women could be explained, at least in part, by the sex difference in body fat distribution [17-19].

Lemieux et al. [20] have studied sex differences in visceral adipose tissue and cardiovascular disease risk profile using computed tomography. They found that though pre-menopausal women had more total body fat than men, they also had lower visceral adipose tissue accumulation and a better metabolic risk profile. After controlling for both total body fat and visceral adipose tissue as potential confounders of the sex difference in the metabolic risk profile, sex differences in plasma triglyceride and apolipoprotein B levels and the HDL2 cholesterol/HDL3 cholesterol ratio were eliminated. However, plasma HDL cholesterol levels remained significantly lower and fasting plasma glucose concentrations significantly higher in men than in women. These results suggest that visceral adipose tissue accumulation is an important correlate of the sex difference observed in some—but not all—variables predictive of type 2 diabetes and cardiovascular disease risk.

Many studies [21-23] have shown that higher levels of small, dense LDL particles increase coronary heart disease (CHD) risk. A sex difference in LDL particle size—women have larger LDL particles than men—is also a well established phenomenon [24-27]. However, Lemieux et al. [28] have reported that men’s higher visceral adipose tissue accumulation and plasma triglyceride levels—the best correlate of LDL particle size [24,29,30]—could not entirely explain the sex difference in LDL particle size. Carr et al. [27] have suggested that higher hepatic lipase activity in men, which affects LDL and HDL heterogeneity, may also explain the sex difference in the cardiovascular risk profile.

In addition to LDL size, HDL particle size is another marker of the sex difference in the lipid profile. Women have larger HDL particles than men, and large HDL particles help ensure a better overall lipoprotein-lipid profile [31]. In both sexes , HDL particle size has been associated with CHD risk factors such as triglyceride, HDL cholesterol, and apolipoprotein B levels as well as with the cholesterol/HDL cholesterol ratio. When men and women with similar HDL particle size were compared, the sex difference in the lipoprotein-lipid profile was virtually eliminated, despite the fact that women had higher levels of total body fat and lower visceral adiposity than men.

In summary, men’s tendency to accumulate visceral adipose tissue appears to be a key factor in predicting why obesity is much more hazardous in men than in pre-menopausal women. However, differences in male and female visceral adipose tissue accumulation cannot entirely explain the sex difference in the metabolic risk profile. It has been suggested that plasma sex hormones may play a significant role in modulating metabolic risk parameters beyond their effects on visceral fat accumulation.

References

  1. Kotani K, Tokunaga K, Fujioka S, et al. Sexual dimorphism of age-related changes in whole-body fat distribution in the obese. Int J Obes 1994; 18: 207-12.

    PubMed ID: 8044194

  2. Kvist H, Chowdhury B, Grangard U, et al. 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.

    PubMed ID: 3202084

  3. Sjostrom L, Rissanen A, Andersen T, et al. Randomised placebo-controlled trial of orlistat for weight loss and prevention of weight regain in obese patients. European Multicentre Orlistat Study Group. Lancet 1998; 352: 167-72.

    PubMed ID: 9683204

  4. Vague J. La différenciation sexuelle : facteur déterminant des formes de l’obésité. Presse Med 1947; 339-40.

    PubMed ID: 18918084

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

    PubMed ID: 6350364

  6. Kvist H, Chowdhury B, Grangård U, Tylén U, Sjöström 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.

    PubMed ID: 3202084

  7. Lemieux S, Prud’homme D, Bouchard C, et al. Sex differences in the relation of visceral adipose tissue accumulation to total body fatness. Am J Clin Nutr 1993; 58: 463-7.

    PubMed ID: 8379501

  8. Seidell JC, Oosterlee A, Deurenberg P, et al. Abdominal fat depots measured with computed tomography: effects of degree of obesity, sex, and age. Eur J Clin Nutr 1988; 42: 805-15.

    PubMed ID: 3181112

  9. Ross R, Léger L, Morris D, et al. Quantification of adipose tissue by MRI: relationship with anthropometric variables. J Appl Physiol 1992; 72: 787-95.

    PubMed ID: 1559959

  10. Pouliot MC, Després JP, Lemieux S, et al. Waist circumference and abdominal sagitttal diameter: best simple anthropometric indexes of abdominal visceral adipose tissue accumulation and related cardiovascular risk in men and women. Am J Cardiol 1994; 73: 460-8.

    PubMed ID: 8141087

  11. Kuk JL, Lee S, Heymsfield SB, et al. Waist circumference and abdominal adipose tissue distribution: influence of age and sex. Am J Clin Nutr 2005; 81: 1330-4.

    PubMed ID: 15941883

  12. Després JP, Ferland M, Moorjani S, et al. Role of hepatic-triglyceride lipase activity in the association between intra-abdominal fat and plasma HDL cholesterol in obese women. Arteriosclerosis 1989; 9: 485-92.

    PubMed ID: 2751477

  13. Pouliot MC, Després JP, Nadeau A, et al. Visceral obesity in men. Associations with glucose tolerance, plasma insulin, and lipoprotein levels. Diabetes 1992; 41: 826-34.

    PubMed ID: 1612197

  14. Ross R, Aru J, Freeman J, et al. Abdominal adiposity and insulin resistance in obese men. Am J Physiol Endocrinol Metab 2002; 282: E657-63.

    PubMed ID: 11832370

  15. Ross R, Freeman J, Hudson R, et al. Abdominal obesity, muscle composition, and insulin resistance in premenopausal women. J Clin Endocrinol Metab 2002; 87: 5044-51.

    PubMed ID: 12414870

  16. Lemieux S and Després JP. Metabolic complications of visceral obesity: contribution to the aetiology of type 2 diabetes and implications for prevention and treatment. Diabete Metab 1994; 20: 375-93.

    PubMed ID: 7843469

  17. Freedman DS, Jacobsen SJ, Barboriak JJ, et al. Body fat distribution and male/female differences in lipids and lipoproteins. Circulation 1990; 81: 1498-506.

    PubMed ID: 2110035

  18. Larsson B, Bengtsson C, Bjorntorp P, et al. Is abdominal body fat distribution a major explanation for the sex difference in the incidence of myocardial infarction? The study of men born in 1913 and the study of women, Goteborg, Sweden. Am J Epidemiol 1992; 135: 266-73.

    PubMed ID: 1546702

  19. Seidell JC, Cigolini M, Charzewska J, et al. Fat distribution and gender differences in serum lipids in men and women from four European communities. Atherosclerosis 1991; 87: 203-10.

    PubMed ID: 1854366

  20. Lemieux S, Després JP, Moorjani S, et al. Are gender differences in cardiovascular disease risk factors explained by the level of visceral adipose tissue? Diabetologia 1994; 37: 757-64.

    PubMed ID: 7988777

  21. Shen MM, Krauss RM, Lindgren FT, et al. Heterogeneity of serum low density lipoproteins in normal human subjects. J Lipid Res 1981; 22: 236-44.

    PubMed ID: 7240955

  22. Krauss RM and Burke DJ. Identification of multiple subclasses of plasma low density lipoproteins in normal humans. J Lipid Res 1982; 23: 97-104.

    PubMed ID: 7057116

  23. St-Pierre AC, Cantin B, Dagenais GR, et al. Low-density lipoprotein subfractions and the long-term risk of ischemic heart disease in men: 13-year follow-up data from the Quebec Cardiovascular Study. Arterioscler Thromb Vasc Biol 2005; 25: 553-9.

    PubMed ID: 15618542

  24. McNamara JR, Jenner JL, Li Z, et al. Change in LDL particle size is associated with change in plasma triglyceride concentration. Arterioscler Thromb 1992; 12: 1284-90.

    PubMed ID: 1420088

  25. Nikkila M, Pitkajarvi T, Koivula T, et al. Women have a larger and less atherogenic low density lipoprotein particle size than men. Atherosclerosis 1996; 119: 181-90.

    PubMed ID: 8808495

  26. Li Z, McNamara JR, Fruchart JC, et al. Effects of gender and menopausal status on plasma lipoprotein subspecies and particle sizes. J Lipid Res 1996; 37: 1886-96.

    PubMed ID: 8895054

  27. Carr MC, Hokanson JE, Zambon A, et al. The contribution of intraabdominal fat to gender differences in hepatic lipase activity and low/high density lipoprotein heterogeneity. J Clin Endocrinol Metab 2001; 86: 2831-7.

    PubMed ID: 11397895

  28. Lemieux I, Pascot A, Lamarche B, et al. Is the gender difference in LDL size explained by the metabolic complications of visceral obesity? Eur J Clin Invest 2002; 32: 909-17.

    PubMed ID: 12534450

  29. Austin MA, King MC, Vranizan KM, et al. Atherogenic lipoprotein phenotype. A proposed genetic marker for coronary heart disease risk. Circulation 1990; 82: 495-506.

    PubMed ID: 2372896

  30. Tchernof A, Lamarche B, Prud’homme D, et al. The dense LDL phenotype. Association with plasma lipoprotein levels, visceral obesity, and hyperinsulinemia in men. Diabetes Care 1996; 19: 629-37.

    PubMed ID: 8725863

  31. Pascot A, Lemieux I, Bergeron J, et al. HDL particle size: a marker of the gender difference in the metabolic risk profile. Atherosclerosis 2002; 160: 399-406.

    PubMed ID: 11849664
Reference 1 CLOSECLOSE

Kotani K, Tokunaga K, Fujioka S, et al. Sexual dimorphism of age-related changes in whole-body fat distribution in the obese. Int J Obes 1994; 18: 207-12.

PubMed ID: 8044194
Reference 2 CLOSECLOSE

Kvist H, Chowdhury B, Grangard U, et al. 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.

PubMed ID: 3202084
Reference 3 CLOSECLOSE

Sjostrom L, Rissanen A, Andersen T, et al. Randomised placebo-controlled trial of orlistat for weight loss and prevention of weight regain in obese patients. European Multicentre Orlistat Study Group. Lancet 1998; 352: 167-72.

PubMed ID: 9683204
Reference 4 CLOSECLOSE

Vague J. La différenciation sexuelle : facteur déterminant des formes de l’obésité. Presse Med 1947; 339-40.

PubMed ID: 18918084
Reference 5 CLOSECLOSE

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

PubMed ID: 6350364
Reference 6 CLOSECLOSE

Kvist H, Chowdhury B, Grangård U, Tylén U, Sjöström 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.

PubMed ID: 3202084
Reference 7 CLOSECLOSE

Lemieux S, Prud’homme D, Bouchard C, et al. Sex differences in the relation of visceral adipose tissue accumulation to total body fatness. Am J Clin Nutr 1993; 58: 463-7.

PubMed ID: 8379501
Reference 8 CLOSECLOSE

Seidell JC, Oosterlee A, Deurenberg P, et al. Abdominal fat depots measured with computed tomography: effects of degree of obesity, sex, and age. Eur J Clin Nutr 1988; 42: 805-15.

PubMed ID: 3181112
Reference 9 CLOSECLOSE

Ross R, Léger L, Morris D, et al. Quantification of adipose tissue by MRI: relationship with anthropometric variables. J Appl Physiol 1992; 72: 787-95.

PubMed ID: 1559959
Reference 10 CLOSECLOSE

Pouliot MC, Després JP, Lemieux S, et al. Waist circumference and abdominal sagitttal diameter: best simple anthropometric indexes of abdominal visceral adipose tissue accumulation and related cardiovascular risk in men and women. Am J Cardiol 1994; 73: 460-8.

PubMed ID: 8141087
Reference 11 CLOSECLOSE

Kuk JL, Lee S, Heymsfield SB, et al. Waist circumference and abdominal adipose tissue distribution: influence of age and sex. Am J Clin Nutr 2005; 81: 1330-4.

PubMed ID: 15941883
Reference 12 CLOSECLOSE

Després JP, Ferland M, Moorjani S, et al. Role of hepatic-triglyceride lipase activity in the association between intra-abdominal fat and plasma HDL cholesterol in obese women. Arteriosclerosis 1989; 9: 485-92.

PubMed ID: 2751477
Reference 13 CLOSECLOSE

Pouliot MC, Després JP, Nadeau A, et al. Visceral obesity in men. Associations with glucose tolerance, plasma insulin, and lipoprotein levels. Diabetes 1992; 41: 826-34.

PubMed ID: 1612197
Reference 14 CLOSECLOSE

Ross R, Aru J, Freeman J, et al. Abdominal adiposity and insulin resistance in obese men. Am J Physiol Endocrinol Metab 2002; 282: E657-63.

PubMed ID: 11832370
Reference 15 CLOSECLOSE

Ross R, Freeman J, Hudson R, et al. Abdominal obesity, muscle composition, and insulin resistance in premenopausal women. J Clin Endocrinol Metab 2002; 87: 5044-51.

PubMed ID: 12414870
Reference 16 CLOSECLOSE

Lemieux S and Després JP. Metabolic complications of visceral obesity: contribution to the aetiology of type 2 diabetes and implications for prevention and treatment. Diabete Metab 1994; 20: 375-93.

PubMed ID: 7843469
Reference 17 CLOSECLOSE

Freedman DS, Jacobsen SJ, Barboriak JJ, et al. Body fat distribution and male/female differences in lipids and lipoproteins. Circulation 1990; 81: 1498-506.

PubMed ID: 2110035
Reference 18 CLOSECLOSE

Larsson B, Bengtsson C, Bjorntorp P, et al. Is abdominal body fat distribution a major explanation for the sex difference in the incidence of myocardial infarction? The study of men born in 1913 and the study of women, Goteborg, Sweden. Am J Epidemiol 1992; 135: 266-73.

PubMed ID: 1546702
Reference 19 CLOSECLOSE

Seidell JC, Cigolini M, Charzewska J, et al. Fat distribution and gender differences in serum lipids in men and women from four European communities. Atherosclerosis 1991; 87: 203-10.

PubMed ID: 1854366
Reference 20 CLOSECLOSE

Lemieux S, Després JP, Moorjani S, et al. Are gender differences in cardiovascular disease risk factors explained by the level of visceral adipose tissue? Diabetologia 1994; 37: 757-64.

PubMed ID: 7988777
Reference 21 CLOSECLOSE

Shen MM, Krauss RM, Lindgren FT, et al. Heterogeneity of serum low density lipoproteins in normal human subjects. J Lipid Res 1981; 22: 236-44.

PubMed ID: 7240955
Reference 22 CLOSECLOSE

Krauss RM and Burke DJ. Identification of multiple subclasses of plasma low density lipoproteins in normal humans. J Lipid Res 1982; 23: 97-104.

PubMed ID: 7057116
Reference 23 CLOSECLOSE

St-Pierre AC, Cantin B, Dagenais GR, et al. Low-density lipoprotein subfractions and the long-term risk of ischemic heart disease in men: 13-year follow-up data from the Quebec Cardiovascular Study. Arterioscler Thromb Vasc Biol 2005; 25: 553-9.

PubMed ID: 15618542
Reference 24 CLOSECLOSE

McNamara JR, Jenner JL, Li Z, et al. Change in LDL particle size is associated with change in plasma triglyceride concentration. Arterioscler Thromb 1992; 12: 1284-90.

PubMed ID: 1420088
Reference 25 CLOSECLOSE

Nikkila M, Pitkajarvi T, Koivula T, et al. Women have a larger and less atherogenic low density lipoprotein particle size than men. Atherosclerosis 1996; 119: 181-90.

PubMed ID: 8808495
Reference 26 CLOSECLOSE

Li Z, McNamara JR, Fruchart JC, et al. Effects of gender and menopausal status on plasma lipoprotein subspecies and particle sizes. J Lipid Res 1996; 37: 1886-96.

PubMed ID: 8895054
Reference 27 CLOSECLOSE

Carr MC, Hokanson JE, Zambon A, et al. The contribution of intraabdominal fat to gender differences in hepatic lipase activity and low/high density lipoprotein heterogeneity. J Clin Endocrinol Metab 2001; 86: 2831-7.

PubMed ID: 11397895
Reference 28 CLOSECLOSE

Lemieux I, Pascot A, Lamarche B, et al. Is the gender difference in LDL size explained by the metabolic complications of visceral obesity? Eur J Clin Invest 2002; 32: 909-17.

PubMed ID: 12534450
Reference 29 CLOSECLOSE

Austin MA, King MC, Vranizan KM, et al. Atherogenic lipoprotein phenotype. A proposed genetic marker for coronary heart disease risk. Circulation 1990; 82: 495-506.

PubMed ID: 2372896
Reference 30 CLOSECLOSE

Tchernof A, Lamarche B, Prud’homme D, et al. The dense LDL phenotype. Association with plasma lipoprotein levels, visceral obesity, and hyperinsulinemia in men. Diabetes Care 1996; 19: 629-37.

PubMed ID: 8725863
Reference 31 CLOSECLOSE

Pascot A, Lemieux I, Bergeron J, et al. HDL particle size: a marker of the gender difference in the metabolic risk profile. Atherosclerosis 2002; 160: 399-406.

PubMed ID: 11849664