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Journal of Endocrinological Investigation

, Volume 36, Issue 4, pp 227–232 | Cite as

Circulating free testosterone in obese men after bariatric surgery increases in parallel with insulin sensitivity

  • J. I. Botella-CarreteroEmail author
  • J. A. Balsa
  • J. M. Gómez-Martin
  • R. Peromingo
  • L. Huerta
  • M. Carrasco
  • F. Arrieta
  • I. Zamarron
  • A. Martin-Hidalgo
  • C. Vazquez
Original Article

Abstract

Background and aim: Male hypogonadism has been linked to obesity and diabetes. We aimed to study the association of changes in insulin sensitivity and testosterone levels in severe obese patients submitted to bariatric surgery. Subjects and methods: Prospective intervention study with twenty consecutive patients who underwent bariatric surgery studied before and after significant weight loss. Serum testosterone, SHBG, fasting glucose, and insulin were measured among others. Free testosterone was calculated with the Vermeulen formula and insulin sensitivity with the homeostatic model assessment (HOMA). Results: At baseline, thirteen patients had low total testosterone levels, whereas eight of these patients also had free testosterone levels below the reference range obtained from the control group. After bariatric surgery total testosterone, SHBG, and free testosterone significantly increased and achieved normal values in all evaluated patients. Insulin sensitivity improved in all of them. Multivariate linear regression showed that changes in fasting glucose (β=−1.868, p= 0.001), insulin (β=−3.782, p= 0.001), weight (β=−0.622, p= 0.002), and SHBG (β=−0.635, p= 0.022) were associated with changes in free testosterone (adjusted R2 =0.936, F=26.613, p= 0.001). When insulin resistance calculated by HOMA was in the model instead of insulin and glucose, it also was associated (β=−3.488, p= 0.008) with free testosterone (adjusted R2 =0.821, F=11.111, p= 0.005). Conclusion: Circulating testosterone in obese men increases after bariatric surgery in parallel with an improvement in insulin sensitivity.

Key-words

Insulin sensitivity male hypogonadism obesity surgery testosterone 

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References

  1. 1.
    Kohn GP, Galanko JA, Overby DW, Farrell TM. Recent trends in bariatric surgery case volume in the United States. Surgery 2009, 146: 375–80.PubMedCrossRefGoogle Scholar
  2. 2.
    Shah M, Simha V, Garg A. Review: long-term impact of bariatric surgery on body weight, comorbidities, and nutritional status. J Clin Endocrinol Metab 2006, 91: 4223–31.PubMedCrossRefGoogle Scholar
  3. 3.
    Fontaine KR, Redden DT, Wang C, Westfall AO, Allison DB. Years of life lost due to obesity. JAMA 2003, 289: 187–93.PubMedCrossRefGoogle Scholar
  4. 4.
    Sjostrom L. Bariatric surgery and reduction in morbidity and mortality: experiences from the SOS study. Int J Obes (Lond) 2008, 32(Suppl 7): S93–7.CrossRefGoogle Scholar
  5. 5.
    Sjostrom L, Gummesson A, Sjostrom CD, et al. Effects of bariatric surgery on cancer incidence in obese patients in Sweden (Swedish Obese Subjects Study): a prospective, controlled intervention trial. Lancet Oncol 2009, 10: 653–62.PubMedCrossRefGoogle Scholar
  6. 6.
    Sugerman HJ, Wolfe LG, Sica DA, Clore JN. Diabetes and hypertension in severe obesity and effects of gastric bypass-induced weight loss. Ann Surg 2003, 237: 751–6.PubMedCentralPubMedGoogle Scholar
  7. 7.
    Sjostrom L, Narbro K, Sjostrom CD, et al. Effects of bariatric surgery on mortality in Swedish obese subjects. N Engl J Med 2007, 357: 741–52.PubMedCrossRefGoogle Scholar
  8. 8.
    Escobar-Morreale HF, Botella-Carretero JI, Alvarez-Blasco F, Sancho J, San Millan JL. The polycystic ovary syndrome associated with morbid obesity may resolve after weight loss induced by bariatric surgery. J Clin Endocrinol Metab 2005, 90: 6364–9.PubMedCrossRefGoogle Scholar
  9. 9.
    Glass AR, Swerdloff RS, Bray GA, Dahms WT, Atkinson RL. Low serum testosterone and sex-hormone-binding-globulin in massively obese men. J Clin Endocrinol Metab 1977, 45: 1211–9.PubMedCrossRefGoogle Scholar
  10. 10.
    Amatruda JM, Harman SM, Pourmotabbed G, Lockwood DH. Depressed plasma testosterone and fractional binding of testosterone in obese males. J Clin Endocrinol Metab 1978, 47: 268–71.PubMedCrossRefGoogle Scholar
  11. 11.
    Hofstra J, Loves S, van Wageningen B, et al. High prevalence of hypogonadotropic hypogonadism in men referred for obesity treatment. Neth J Med 2008, 66: 103–9.PubMedGoogle Scholar
  12. 12.
    Mollar Puchades MA, Gomez RC, del Olmo Garcia MI, et al. Hypogonadotropic hypogonadism in a patient with morbid obesity. Obes Surg 2007, 17: 1127–31.PubMedCrossRefGoogle Scholar
  13. 13.
    Hammoud A, Gibson M, Hunt SC, et al. Effect of Roux-en-Y gastric bypass surgery on the sex steroids and quality of life in obese men. J Clin Endocrinol Metab 2009, 94: 1329–32.PubMedCentralPubMedCrossRefGoogle Scholar
  14. 14.
    Rao SR, Kini S, Tamler R. Sex Hormones and Bariatric Surgery in Men. Gend Med 2011, 5: 300–11.CrossRefGoogle Scholar
  15. 15.
    Zitzmann M. Testosterone deficiency, insulin resistance and the metabolic syndrome. Nat Rev Endocrinol 2009, 5: 673–81.PubMedCrossRefGoogle Scholar
  16. 16.
    Yeap BB, Chubb SA, Hyde Z, et al. Lower serum testosterone is independently associated with insulin resistance in non-diabetic older men: the Health In Men Study. Eur J Endocrinol 2009, 161: 591–8.PubMedCrossRefGoogle Scholar
  17. 17.
    Dandona P, Dhindsa S, Chaudhuri A, et al. Hypogonadotropic hypogonadism in type 2 diabetes, obesity and the metabolic syndrome. Curr Mol Med 2008, 8: 816–28.PubMedCrossRefGoogle Scholar
  18. 18.
    Vikan T, Schirmer H, Njolstad I, Svartberg J. Low testosterone and sex hormone-binding globulin levels and high estradiol levels are independent predictors of type 2 diabetes in men. Eur J Endocrinol 2010, 162: 747–54.PubMedCrossRefGoogle Scholar
  19. 19.
    Khoo J, Piantadosi C, Worthley S, Wittert GA. Effects of a low-energy diet on sexual function and lower urinary tract symptoms in obese men. Int J Obes (Lond) 2010, 34: 1396–403.CrossRefGoogle Scholar
  20. 20.
    NIH conference. Gastrointestinal surgery for severe obesity. Consensus Development Conference Panel. Ann Intern Med 1991, 115: 956–61.CrossRefGoogle Scholar
  21. 21.
    Vermeulen A, Verdonck L, Kaufman JM. A critical evaluation of simple methods for the estimation of free testosterone in serum. J Clin Endocrinol Metab 1999, 84: 3666–72.PubMedCrossRefGoogle Scholar
  22. 22.
    Matthews DR, Hosker JP, Rudenski AS, et al. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985, 28: 412–9.PubMedCrossRefGoogle Scholar
  23. 23.
    Belanger C, Luu-The V, Dupont P, Tchernof A. Adipose tissue intracrinology: potential importance of local androgen/estrogen metabolism in the regulation of adiposity. Horm Metab Res 2002, 34: 737–45.PubMedCrossRefGoogle Scholar
  24. 24.
    Luboshitzky R, Aviv A, Hefetz A, et al. Decreased pituitary-gonadal secretion in men with obstructive sleep apnea. J Clin Endocrinol Metab 2002, 87: 3394–8.PubMedCrossRefGoogle Scholar
  25. 25.
    Isidori AM, Caprio M, Strollo F, et al. Leptin and androgens in male obesity: evidence for leptin contribution to reduced androgen levels. J Clin Endocrinol Metab 1999, 84: 3673–80.PubMedGoogle Scholar
  26. 26.
    Loves S, Ruinemans-Koerts J, de Boer H. Letrozole once a week normalizes serum testosterone in obesity-related male hypogonadism. Eur J Endocrinol 2008, 158: 741–7.PubMedCrossRefGoogle Scholar
  27. 27.
    Santamaria JD, Prior JC, Fleetham JA. Reversible reproductive dysfunction in men with obstructive sleep apnoea. Clin Endocrinol (Oxf) 1988, 28: 461–70.CrossRefGoogle Scholar
  28. 28.
    Meston N, Davies RJ, Mullins R, et al. Endocrine effects of nasal continuous positive airway pressure in male patients with obstructive sleep apnoea. J Intern Med 2003, 254: 447–54.PubMedCrossRefGoogle Scholar
  29. 29.
    Zhuravlev VN, Frank MA, Gomzhin AI. Sexual functions of men with obstructive sleep apnoea syndrome and hypogonadism may improve upon testosterone administration: a pilot study. Andrologia 2009, 41: 193–5.PubMedCrossRefGoogle Scholar
  30. 30.
    Bastounis EA, Karayiannakis AJ, Syrigos K, et al. Sex hormone changes in morbidly obese patients after vertical banded gastroplasty. Eur Surg Res 1998, 30: 43–7.PubMedCrossRefGoogle Scholar
  31. 31.
    Globerman H, Shen-Orr Z, Karnieli E, Aloni Y, Charuzi I. Inhibin B in men with severe obesity and after weight reduction following gastroplasty. Endocr Res 2005, 31: 17–26.PubMedCrossRefGoogle Scholar
  32. 32.
    Ly LP, Sartorius G, Hull L, et al. Accuracy of calculated free testosterone formulae in men. Clin Endocrinol (Oxf) 2010, 73: 382–8.CrossRefGoogle Scholar
  33. 33.
    Guay AT. The emerging link between hypogonadism and metabolic syndrome. J Androl 2009, 30: 370–6.PubMedCrossRefGoogle Scholar
  34. 34.
    Katabami T, Kato H, Asahina T, et al. Serum free testosterone and metabolic syndrome in Japanese men. Endocr J 2010, 57: 533–9.PubMedCrossRefGoogle Scholar
  35. 35.
    Lewis JG, Borowski KK, Shand BI, George PM, Scott RS. Plasma sex hormone-binding globulin, corticosteroid-binding globulin, cortisol, and free cortisol levels in outpatients attending a lipid disorders clinic: a cross-sectional study of 1137 subjects. Horm Metab Res 2010, 42: 274–9.PubMedCrossRefGoogle Scholar
  36. 36.
    Dhindsa S, Miller MG, McWhirter CL, et al. Testosterone concentrations in diabetic and nondiabetic obese men. Diabetes Care 2010, 33: 1186–92.PubMedCentralPubMedCrossRefGoogle Scholar
  37. 37.
    Cohen PG. Obesity in men: the hypogonadal-estrogen receptor relationship and its effect on glucose homeostasis. Med Hypotheses 2008, 70: 358–60.PubMedCrossRefGoogle Scholar
  38. 38.
    Fischer-Posovszky P, Wabitsch M, Hochberg Z. Endocrinology of adipose tissue — an update. Horm Metab Res 2007, 39: 314–21.PubMedCrossRefGoogle Scholar
  39. 39.
    Kapoor D, Clarke S, Stanworth R, Channer KS, Jones TH. The effect of testosterone replacement therapy on adipocytokines and C-reactive protein in hypogonadal men with type 2 diabetes. Eur J Endocrinol 2007, 156: 595–602.PubMedCrossRefGoogle Scholar

Copyright information

© Italian Society of Endocrinology (SIE) 2013

Authors and Affiliations

  • J. I. Botella-Carretero
    • 1
    • 2
    Email author
  • J. A. Balsa
    • 1
    • 2
  • J. M. Gómez-Martin
    • 1
  • R. Peromingo
    • 3
  • L. Huerta
    • 2
    • 4
  • M. Carrasco
    • 1
  • F. Arrieta
    • 1
    • 2
  • I. Zamarron
    • 1
    • 2
  • A. Martin-Hidalgo
    • 2
    • 4
  • C. Vazquez
    • 1
    • 2
  1. 1.Unit of Clinical Nutrition and Obesity, Department of Endocrinology and NutritionHospital Universitario Ramón y Cajal, IRYCISMadridSpain
  2. 2.Centro de Investigación Biomédica en Red de Fisiopatología de Obesidad y Nutrición (CIBERobn)Hospital Universitario Ramón y Cajal, IRYCISMadridSpain
  3. 3.Department of General SurgeryHospital Universitario Ramón y Cajal, IRYCISMadridSpain
  4. 4.Department of Biochemistry-InvestigationHospital Universitario Ramón y Cajal, IRYCISMadridSpain

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