Article

Biochemistry/Physiology

Plasma steroids, body composition, and fat distribution: effects of age, sex, and exercise training

Received:
Revised:
Accepted:
Published online:

Abstract

Background/objectives

Plasma steroid hormone levels vary between men and women, but their associations with BMI and adiposity are controversial. Furthermore, little is known about the role of exercise programs on the relationship between steroid hormones and adiposity. This report evaluates these relationships for plasma levels of adrenal, gonadal, and conjugated steroids with body composition and fat distribution in sedentary men and women, aged 17–65 years, and their responses to an exercise program.

Subjects/methods

In the sedentary state, 270 men (29% Blacks) and 304 women (34% Blacks) from the HERITAGE Family Study were available. Among them, 242 men and 238 women completed a 20-week fully standardized exercise program. Fourteen steroid hormones and SHBG concentrations were assayed in a fasted state and were compared for their associations with adiposity in men and women and in response to the exercise program. Covariates adjusted for in partial correlation analysis were age, ancestry, menopause status (women), and oral contraceptives/hormone replacement treatment status (women) at baseline, as well as baseline value of the trait for the training response. Differences among normal weight, overweight, and obese subjects were also considered. Statistical significance was set at P < 0.0001.

Results

Baseline levels of dihydrotesterone (DHT), 17 hydroxy progesterone (OHPROG), sex hormone-binding globulin (SHBG), and testosterone (TESTO) were negatively associated with fat mass and abdominal fat (P < 0.0001) in men and for SHBG in women (P < 0.0001). TESTO was not correlated with fat-free mass in men or women, but was significantly associated with % fat-free mass in men. No association was detected between baseline steroid hormone levels and changes in adiposity traits in response to 20 weeks of exercise.

Conclusion

In men, low DHT, OHPROG, SHBG, and TESTO were associated with higher adiposity and abdominal and visceral fat. A similar adiposity profile was observed in women with low SHBG.

  • Subscribe to International Journal of Obesity for full access:

    $652

    Subscribe

Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.

References

  1. 1.

    Gates MA, Mekary RA, Chiu GR, Ding EL, Wittert GA, Araujo AB. Sex steroid hormone levels and body composition in men. J Clin Endocrinol Metab. 2013;98:2442–50.

  2. 2.

    Bann D, Wu FC, Keevil B, Lashen H, Adams J, Hardy R, et al. Changes in testosterone related to body composition in late midlife: findings from the 1946 British birth cohort study. Obes (Silver Spring). 2015;23:1486–92.

  3. 3.

    Vandenput L, Mellstrom D, Karlsson MK, Orwoll E, Labrie F, Ljunggren O, et al. Serum estradiol is associated with lean mass in elderly Swedish men. Eur J Endocrinol. 2010;162:737–45.

  4. 4.

    Tchernof A, Despres JP, Belanger A, Dupont A, Prud’homme D, Moorjani S, et al. Reduced testosterone and adrenal C19 steroid levels in obese men. Metabolism. 1995;44:513–9.

  5. 5.

    Lee K, Sung J, Song YM. Genetic and environmental influence on the association between testosterone, sex hormone-binding globulin and body composition in Korean men. Clin Endocrinol (Oxf). 2015;83:236–45.

  6. 6.

    Keller JL, Casson PR, Toth MJ. Relationship of androgens to body composition, energy and substrate metabolism and aerobic capacity in healthy, young women. Steroids. 2011;76:1247–51.

  7. 7.

    Casson PR, Toth MJ, Johnson JV, Stanczyk FZ, Casey CL, Dixon ME. Correlation of serum androgens with anthropometric and metabolic indices in healthy, nonobese postmenopausal women. J Clin Endocrinol Metab. 2010;95:4276–82.

  8. 8.

    Crewther BT, Heke TL, Keogh JW. The effects of a resistance-training program on strength, body composition and baseline hormones in male athletes training concurrently for rugby union 7’s. J Sports Med Phys Fit. 2013;53:34–41.

  9. 9.

    Mouser JG, Loprinzi PD, Loenneke JP. The association between physiologic testosterone levels, lean mass, and fat mass in a nationally representative sample of men in the United States. Steroids. 2016;115:62–66.

  10. 10.

    Roy TA, Blackman MR, Harman SM, Tobin JD, Schrager M, Metter EJ. Interrelationships of serum testosterone and free testosterone index with FFM and strength in aging men. Am J Physiol Endocrinol Metab. 2002;283:E284–94.

  11. 11.

    Trabert B, Graubard BI, Nyante SJ, Rifai N, Bradwin G, Platz EA, et al. Relationship of sex steroid hormones with body size and with body composition measured by dual-energy X-ray absorptiometry in US men. Cancer Causes Control. 2012;23:1881–91.

  12. 12.

    Blouin K, Despres JP, Couillard C, Tremblay A, Prud’homme D, Bouchard C, et al. Contribution of age and declining androgen levels to features of the metabolic syndrome in men. Metabolism. 2005;54:1034–40.

  13. 13.

    Cao Y, Zhang S, Zou S, Xia X. The relationship between endogenous androgens and body fat distribution in early and late postmenopausal women. PLoS ONE. 2013;8:e58448.

  14. 14.

    Liedtke S, Schmidt ME, Vrieling A, Lukanova A, Becker S, Kaaks R, et al. Postmenopausal sex hormones in relation to body fat distribution. Obes (Silver Spring). 2012;20:1088–95.

  15. 15.

    Paxton RJ, King DW, Garcia-Prieto C, Connors SK, Hernandez M, Gor BJ, et al. Associations between body size and serum estradiol and sex hormone-binding globulin levels in premenopausal African American women. J Clin Endocrinol Metab. 2013;98:E485–90.

  16. 16.

    De Simone M, Verrotti A, Iughetti L, Palumbo M, Farello G, Di Cesare E, et al. Increased visceral adipose tissue is associated with increased circulating insulin and decreased sex hormone binding globulin levels in massively obese adolescent girls. J Endocrinol Invest. 2001;24:438–44.

  17. 17.

    Muller M, den Tonkelaar I, Thijssen JH, Grobbee DE, van der Schouw YT. Endogenous sex hormones in men aged 40-80 years. Eur J Endocrinol. 2003;149:583–9.

  18. 18.

    Mahabir S, Baer DJ, Johnson LL, Hartman TJ, Dorgan JF, Campbell WS, et al. Usefulness of body mass index as a sufficient adiposity measurement for sex hormone concentration associations in postmenopausal women. Cancer Epidemiol Biomark Prev. 2006;15:2502–7.

  19. 19.

    Couillard C, Gagnon J, Bergeron J, Leon AS, Rao DC, Skinner JS, et al. Contribution of body fatness and adipose tissue distribution to the age variation in plasma steroid hormone concentrations in men: the HERITAGE Family Study. J Clin Endocrinol Metab. 2000;85:1026–31.

  20. 20.

    van den Beld AW, de Jong FH, Grobbee DE, Pols HA, Lamberts SW. Measures of bioavailable serum testosterone and estradiol and their relationships with muscle strength, bone density, and body composition in elderly men. J Clin Endocrinol Metab. 2000;85:3276–82.

  21. 21.

    Cote JA, Lessard J, Mailloux J, Laberge P, Rheaume C, Tchernof A. Circulating 5alpha-dihydrotestosterone, abdominal obesity and adipocyte characteristics in women. Horm Mol Biol Clin Investig. 2012;12:391–400.

  22. 22.

    De Pergola G, Triggiani V, Giorgino F, Cospite MR, Garruti G, Cignarelli M, et al. The free testosterone to dehydroepiandrosterone sulphate molar ratio as a marker of visceral fat accumulation in premenopausal obese women. Int J Obes Relat Metab Disord. 1994;18:659–64.

  23. 23.

    Barrett-Connor E, Ferrara A. Dehydroepiandrosterone, dehydroepiandrosterone sulfate, obesity, waist-hip ratio, and noninsulin-dependent diabetes in postmenopausal women: the Rancho Bernardo Study. J Clin Endocrinol Metab. 1996;81:59–64.

  24. 24.

    Williams DP, Boyden TW, Pamenter RW, Lohman TG, Going SB. Relationship of body fat percentage and fat distribution with dehydroepiandrosterone sulfate in premenopausal females. J Clin Endocrinol Metab. 1993;77:80–5.

  25. 25.

    Hawkins VN, Foster-Schubert K, Chubak J, Sorensen B, Ulrich CM, Stancyzk FZ, et al. Effect of exercise on serum sex hormones in men: a 12-month randomized clinical trial. Med Sci Sports Exerc. 2008;40:223–33.

  26. 26.

    Webborn N, Williams A, McNamee M, Bouchard C, Pitsiladis Y, Ahmetov I, et al. Direct-to-consumer genetic testing for predicting sports performance and talent identification: consensus statement. Br J Sports Med. 2015;49:1486–91.

  27. 27.

    McTiernan A, Tworoger SS, Rajan KB, Yasui Y, Sorenson B, Ulrich CM, et al. Effect of exercise on serum androgens in postmenopausal women: a 12-month randomized clinical trial. Cancer Epidemiol Biomark Prev. 2004;13:1099–105.

  28. 28.

    Hayes LD, Grace FM, Sculthorpe N, Herbert P, Kilduff LP, Baker JS. Does chronic exercise attenuate age-related physiological decline in males? Res Sports Med. 2013;21:343–54.

  29. 29.

    Rosner W, Auchus RJ, Azziz R, Sluss PM, Raff H. Position statement: utility, limitations, and pitfalls in measuring testosterone: an Endocrine Society position statement. J Clin Endocrinol Metab. 2007;92:405–13.

  30. 30.

    Bouchard C, Leon AS, Rao DC, Skinner JS, Wilmore JH, Gagnon J. The HERITAGE family study. Aims, design, and measurement protocol. Med Sci Sports Exerc. 1995;27:721–9.

  31. 31.

    Siri WE. The gross composition of the body. Adv Biol Med Phys. 1956;4:239–80.

  32. 32.

    Lohman TG. Applicability of body composition techniques and constants for children and youths. Exerc Sport Sci Rev. 1986;14:325–57.

  33. 33.

    Schutte JE, Townsend EJ, Hugg J, Shoup RF, Malina RM, Blomqvist CG. Density of lean body mass is greater in blacks than in whites. J Appl Physiol Respir Environ Exerc Physiol. 1984;56:1647–9.

  34. 34.

    Ortiz O, Russell M, Daley TL, Baumgartner RN, Waki M, Lichtman S, et al. Differences in skeletal muscle and bone mineral mass between black and white females and their relevance to estimates of body composition. Am J Clin Nutr. 1992;55:8–13.

  35. 35.

    Wilmore JH, Stanforth PR, Domenick MA, Gagnon J, Daw EW, Leon AS, et al. Reproducibility of anthropometric and body composition measurements: the HERITAGE Family Study. Int J Obes Relat Metab Disord. 1997;21:297–303.

  36. 36.

    Sjostrom L, Kvist H, Cederblad A, Tylen U. Determination of total adipose tissue and body fat in women by computed tomography, 40K, and tritium. Am J Physiol. 1986;250:E736–45.

  37. 37.

    Stanforth PR, Jackson AS, Green JS, Gagnon J, Rankinen T, Despres JP, et al. Generalized abdominal visceral fat prediction models for black and white adults aged 17-65 y: the HERITAGE Family Study. Int J Obes Relat Metab Disord. 2004;28:925–32.

  38. 38.

    Lee YH, Hsiao HF, Yang HT, Huang SY, Chan WP. Reproducibility and repeatability of computer tomography-based measurement of abdominal subcutaneous and visceral adipose tissues. Sci Rep. 2017;7:40389

  39. 39.

    Ukkola O, Gagnon J, Rankinen T, Thompson PA, Hong Y, Leon AS, et al. Age, body mass index, race and other determinants of steroid hormone variability: the HERITAGE Family Study. Eur J Endocrinol. 2001;145:1–9.

  40. 40.

    Grasa MD, Gulfo J, Camps N, Alcala R, Monserrat L, Moreno-Navarrete JM, et al. Modulation of SHBG binding to testosterone and estradiol by sex and morbid obesity. Eur J Endocrinol. 2017;176:393–404.

  41. 41.

    Blouin K, Nadeau M, Perreault M, Veilleux A, Drolet R, Marceau P, et al. Effects of androgens on adipocyte differentiation and adipose tissue explant metabolism in men and women. Clin Endocrinol (Oxf). 2010;72:176–88.

  42. 42.

    O’Reilly MW, House PJ, Tomlinson JW. Understanding androgen action in adipose tissue. J Steroid Biochem Mol Biol. 2014;143:277–84.

  43. 43.

    Blouin K, Boivin A, Tchernof A. Androgens and body fat distribution. J Steroid Biochem Mol Biol. 2008;108:272–80.

  44. 44.

    Saad F, Aversa A, Isidori AM, Gooren LJ. Testosterone as potential effective therapy in treatment of obesity in men with testosterone deficiency: a review. Curr Diabetes Rev. 2012;8:131–43.

  45. 45.

    Despres JP, Nadeau A, Tremblay A, Ferland M, Moorjani S, Lupien PJ, et al. Role of deep abdominal fat in the association between regional adipose tissue distribution and glucose tolerance in obese women. Diabetes. 1989;38:304–9.

  46. 46.

    Plymate SR, Matej LA, Jones RE, Friedl KE. Inhibition of sex hormone-binding globulin production in the human hepatoma (Hep G2) cell line by insulin and prolactin. J Clin Endocrinol Metab. 1988;67:460–4.

  47. 47.

    Tchernof A, Brochu D, Maltais-Payette I, Fouad Mansour M, Marchand GB, Carreau AM, Kapeluto J. Androgens and the regulation of adiposity and body fat distribution in humans. Compr Physiol 2018; In press.

  48. 48.

    Sonksen P. Determination and regulation of body composition in elite athletes. Br J Sports Med. 2018;52:219–229

  49. 49.

    LeBlanc ES, Wang PY, Lee CG, Barrett-Connor E, Cauley JA, Hoffman AR, et al. Higher testosterone levels are associated with less loss of lean body mass in older men. J Clin Endocrinol Metab. 2011;96:3855–63.

Download references

Acknowledgements

The HERITAGE Family Study has been supported over the years by multiple grants from the National Institute for Heart, Lung and Blood Diseases of the National Institutes of Health (HL45670, CB and TR; HL47323, ASL; HL47317, DC Rao; HL47327, JS Skinner; HL47321, JH Wilmore, deceased). CB is partially funded by the John W. Barton Sr. Chair in Genetics and Nutrition, and by the NIH-funded COBRE grant (NIH 8 P30GM118430-01). ZH is funded by the China Scholarship Council (file no. 201603620001) and China Institute of Sport Science (2015-01, 2016-01). We would like to express our gratitude to Dr. Alain Belanger (retired) and his staff from the Molecular Endocrinology Laboratory of the Laval University Medical Center in Quebec City, Canada, for the assays of the steroids and their dedication to the HERITAGE Family Study.

Author information

Affiliations

  1. Human Genomics Laboratory, Pennington Biomedical Research Center, Baton Rouge, LA, USA

    • Zihong He
    • , Tuomo Rankinen
    •  & Claude Bouchard
  2. Department of Biology, China Institute of Sport Science, Beijing, China

    • Zihong He
  3. School of Kinesiology, University of Minnesota, Minneapolis, MN, USA

    • Arthur S. Leon
  4. Department of Kinesiology, Indiana University, Bloomington, IN, USA

    • James S. Skinner
  5. School of Nutrition, Laval University, Quebec City, QC, Canada

    • André Tchernof

Authors

  1. Search for Zihong He in:

  2. Search for Tuomo Rankinen in:

  3. Search for Arthur S. Leon in:

  4. Search for James S. Skinner in:

  5. Search for André Tchernof in:

  6. Search for Claude Bouchard in:

Conflict of interest

AT receives research funding from Johnson & Johnson Medical Companies for studies unrelated to the present paper. The remaining authors declare that they have no conflict of interest.

Corresponding author

Correspondence to Claude Bouchard.

Electronic supplementary material