Interrelationships between intraabdominal fat and total serum testosterone levels in obese women

doi:10.1016/0026-0495(94)90110-4

Metabolism

Volume 43, Issue 3, March 1994, Pages 390-395

https://doi.org/10.1016/0026-0495(94)90110-4 Get rights and content

Abstract

Thirty-six women aged 18 to 52 years with body mass indexes (BMIs) between 27 and 52 were studied. Visceral and subcutaneous fat areas and body fat were evaluated by computerized tomography with a single scan at the IV-V lumbar vertebra level. Glucose, insulin, and C-peptide levels were measured before and after a glucose load. Total and free serum testosterone and 24-hour urinary cortisol excretion were measured. A stepwise multiple regression equation showed the visceral to subcutaneous fat area ratio to be the most powerful predictor for glucose alterations both during fasting and after a glucose load, and showed BMI to be the most powerful predictor for insulin and C-peptide levels. Total serum testosterone, after matching for age and BMI, demonstrates a significant negative correlation with visceral fat area. We conclude that in obese women, as in men, intraabdominal fat negatively correlates with serum testosterone levels.

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Citation Excerpt :
In fertile-aged women, the relation between body composition and serum androgen concentrations is not clear. Some studies have found a positive correlation between circulating free testosterone and waist to hip –ratio [12–14], and other studies a negative [15,16] or no correlation [12] between serum total testosterone levels and central accumulation of fat. Genetic factors and age appear to explain much of the variability in serum concentrations of steroid hormones [17,18], and both of these are important determinants of body composition too, which may have confounded many previous studies.
Obesity may alter serum steroid concentrations and metabolism. We investigated this in healthy young women with increased body fat and their leaner co-twin sisters.
Age and genetic background both strongly influence serum steroid levels and body composition. This is a cross-sectional study of 13 female monozygotic twin pairs (age, 23–36 years), ten of which were discordant for body mass index (median difference in body weight between the co-twins, 19 kg).
We determined body composition by dual energy X-ray absorptiometry and magnetic resonance imaging, serum androgens by liquid chromatography-tandem mass spectrometry, and mRNA expression of genes in subcutaneous adipose tissue and adipocytes.
The heavier women had lower serum dehydroepiandrosterone (DHEA), dihydrotestosterone (DHT), and sex hormone-binding globulin (SHBG) (P < 0.05 for all) compared to their leaner co-twins with no differences in serum testosterone or androstenedione levels. Serum DHEA correlated inversely with %body fat (r = −0.905, P = 0.002), and DHT positively with SHBG (r = 0.842, P = 0.002). In adipose tissue or adipocytes, expressions of STS (steroid sulfatase) and androgen-related genes were significantly higher in the heavier compared to the leaner co-twin, and within pairs, correlated positively with adiposity but were not related to serum androgen levels. None of the serum androgen or SHBG levels correlated with indices of insulin resistance.
Serum DHEA levels were best predicted by %body fat, and serum DHT by SHBG. These or other serum androgen concentrations did not reflect differences in androgen-related genes in adipose tissue. General or intra-abdominal adiposity were not associated with increased androgenicity in young women.
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Androgens modulate adipocyte function and affect the size of adipose tissue compartments in humans. Aldo-keto reductase 1C (AKR1C) enzymes, especially AKR1C2 and AKR1C3, through local synthesis and inactivation of androgens, may be involved in the fine regulation of androgen availability in adipose tissue. This review article summarizes recent findings on androgen metabolism in adipose tissue. Primary culture models and whole tissue specimens of human adipose tissue obtained from the abdominal subcutaneous and intra-abdominal (omental) fat compartments were used in our studies. The non-aromatizable androgen dihydrotestosterone (DHT) inhibits adipocyte differentiation in subcutaneous and omental adipocytes in humans. This inhibitory effect is partially reversed by anti-androgens. Activity and mRNA expression of AKR1C1, 2 and 3 were detected in SC and OM adipose tissue, in men and women, with higher levels in the SC depot than the omental depot of both sexes. The abundance of AKR1C enzyme mRNAs was particularly elevated compared to other steroid-converting enzymes. Significant positive associations were observed between AKR1C enzyme mRNA levels or DHT inactivation rates and visceral fat accumulation as well as OM adipocyte size in women and in men, at least in the normal weight to moderately obese range. Mature adipocytes had significantly higher DHT inactivation rates compared to preadipocytes. Accordingly, adipocyte differentiation significantly increased AKR1C enzyme expression and DHT inactivation rates. Treatment of preadipocytes with dexamethasone alone led to significant increases in the formation of 5α-androstan-3α,17β-diol. This stimulation was completely abolished by RU486, suggesting that androgen inactivation is stimulated by a glucocorticoid receptor-dependent mechanism. In conclusion, higher AKR1C activity and expression in mature adipocytes may explain the associations between these enzymes and obesity. We speculate that glucocorticoid-induced androgen inactivation could locally decrease the exposure of adipose cells to active androgens and partially remove their inhibitory effect on adipogenesis. We hypothesize that body fat distribution patterns likely emerge from the local adipose tissue balance between active androgens and glucocorticoids in each fat compartment.
Androgens and body fat distribution
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An important sex difference in body fat distribution is generally observed. Men are usually characterized by the android type of obesity, with accumulation of fat in the abdominal region, whereas women often display the gynoid type of obesity, with a greater proportion of their body fat in the gluteal-femoral region. Accordingly, the amount of fat located inside the abdominal cavity (intra-abdominal or visceral adipose tissue) is twice as high in men compared to women. This sex difference has been shown to explain a major portion of the differing metabolic profiles and cardiovascular disease risk in men and women. Association studies have shown that circulating androgens are negatively associated with intra-abdominal fat accumulation in men, which explains an important portion of the link between low androgens and features of the metabolic syndrome. In women, the low circulating sex hormone-binding globulin (SHBG) levels found in abdominal obesity may indirectly indicate that elevated free androgens are related to increased visceral fat accumulation. However, data on non SHBG-bound and total androgens are not unanimous and difficult to interpret for total androgens. These studies focusing on plasma levels of sex hormones indirectly suggest that androgens may alter adipose tissue mass in a depot-specific manner. This could occur through site-specific modulation of preadipocyte proliferation and/or differentiation as well as lipid synthesis and/or lipolysis in mature adipocytes. Recent results on the effects of androgens in cultured adipocytes and adipose tissue have been inconsistent, but may indicate decreased adipogenesis and increased lipolysis upon androgen treatment. Finally, adipose tissue has been shown to express several steroidogenic and steroid-inactivating enzymes. Their mere presence in fat indirectly supports the notion of a highly complex enzymatic system modulating steroid action on a local basis. Recent data obtained in both men and women suggest that enzymes from the aldoketoreductase 1C family are very active and may be important modulators of androgen action in adipose tissue.
The androgenic sex hormone profile is an essential feature of metabolic syndrome in premenopausal women: A controlled community-based study
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To evaluate sex hormones in premenopausal white women with metabolic syndrome (MBS).
Cross-sectional controlled community-based study.
Pieksämäki District Health Center, Pieksämäki, Finland.
Five hundred forty-three women, aged 34 to 54 years, were screened according to National Cholesterol Education Program criteria: waist >88 cm, hypertension ≥130/≥85 mm Hg, hypertriglyceridemia ≥1.7 mmol/L, high-density lipoprotein (HDL)-cholesterol <1.3 mmol/L, and fasting glucose ≥6.1 mmol/L. Sixty-three women fulfilled at least three of the above-mentioned criteria and were enrolled. Eighty-eight age-matched women without MBS served as controls.
None.
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A markedly lower insulin sensitivity index and higher free androgen index were detected in the women with MBS than in the controls. Abdominal obesity and increased diastolic blood pressure were significantly associated with high free androgen index in multiple regression analysis.
A hyperandrogenic hormone profile appeared to be a typical feature of premenopausal female MBS even without polycystic ovary syndrome (PCOS).
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^☆: Supported in part by grants from the Ministero dell'Universitá e della Ricerca Scientifica e Tecnologica and the Consiglio Nazionale delle Ricerche Project Prevenzione e Controllo dei Fattori di Malattia (C179037N).

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Interrelationships between intraabdominal fat and total serum testosterone levels in obese women☆

Abstract

Am J Clin Nutr

Metabolism

Am J Cardiol

J Clin Epidemiol

Metabolism

Metabolism

Metabolism

Clin Radiol

Am J Clin Nutr

Metabolism

J Clin Epidemiol

Relationship of anthropometric measurements of body fat distribution to the metabolic profile in premenopausal women

Acta Med Scand

Adipose tissue distribution and plasma lipoprotein levels in obese women. Importance of intra-abdominal fat

Arteriosclerosis

Receptor and postreceptor effects of free fatty acids (FFA) on hepatocyte insulin dynamics

Int J Obes

Body fat distribution in pre- and post-menopausal women: Metabolic and anthropometric variables and their inter-relationships

Int J Obes

Blood pressure, metabolic variables and adipose tissue distribution in pre- and post-menopausal women

Acta Obstet Gynecol Scand

Alcohol consumption, smoking habits and body fat distribution in Italian men and women aged 20–60 years

Eur J Clin Nutr

Splanchnic insulin metabolism in obesity: Influence of body fat distribution

J Clin Invest

Changed adipose tissue distribution after treatment of Cushing's syndrome

The effects of testosterone treatment on body composition and metabolism in middle-aged obese men

Int J Obes

The effects of androgens on the regulation of lipolysis in adipose precursor cells

Endocrinology

Effect of testosterone on abdominal adipose tissue in men

Int J Obes

Body fat distribution measured with CT: Correlations in healthy subjects, patients with anorexia nervosa and patients with Cushing syndrome

Radiology