World Journal of Urology

, Volume 29, Issue 4, pp 541–546

The influence of age on bioavailable and free testosterone is independent of body mass index and glucose levels

  • Graziele Halmenschlager
  • Ernani Luis Rhoden
  • Charles Edison Riedner
Original Article



To evaluate the influence of age on serum levels of total testosterone (TT), bioavailable testosterone (BT), free testosterone (FT), and sex-hormone binding globulin (SHBG), considering the presence of fasting blood glucose levels and body mass index (BMI) in a selected male population.


A total of 428 men were analyzed. Anthropometry was taken from all, considering BMI as general obesity indicative variable. Fasting blood samples were drawn for determination of plasma glucose levels and serum levels of albumin, TT, and SHBG. The values of BT and FT were calculated from TT, SHBG, and albumin, by Vermeulen’s equation. Statistical significance was set at P ≤ 0.05.


Age was negatively correlated to BT (r = −0.301; P < 0.001) and FT (r = −0.273; P < 0.001), but not to TT levels (r = 0.002, P = 0.974). Age was positively correlated to SHBG (r = 0.376; P < 0.001). Age was independently associated with the occurrence of high SHBG levels (OR = 1.07, 95%CI = 1.05–1.10, P < 0.001) and of low BT (OR = 1.04, 95%CI = 1.02–1.07, P < 0.001) and FT levels (OR = 1.05, 95%CI = 1.03–1.08, P < 0.001), but not with low levels of TT (P = 0.08).


Age was significantly associated to high levels of SHBG and to low levels of BT and FT, without significant association to TT. This pattern was independent of BMI and glucose levels.


Aging Androgens Blood glucose Body mass index 


  1. 1.
    Lunenfeld B (2002) The ageing male: demographic and challenges. World J Urol 20:11–16PubMedCrossRefGoogle Scholar
  2. 2.
    Gooren LJ (2010) Androgens and male aging: current evidence of safety and efficacy. Asian J Androl 12:136–151PubMedCrossRefGoogle Scholar
  3. 3.
    Wang C, Nieschlag E, Swerdloff R et al (2009) Investigation, treatment, and monitoring of late-onset hypogonadism in males: ISA, ISSAM, EAU, EAA, and ASA recommendations. J Androl 30:1–9PubMedCrossRefGoogle Scholar
  4. 4.
    Svartberg J, Midtby M, Bonaa KH et al (2003) The associations of age, lifestyle factors and chronic disease with testosterone in men: the Tromso Study. Eur J Endocrinol 149:145–152PubMedCrossRefGoogle Scholar
  5. 5.
    Muller M, den Tonkelaar I, Thijssen JHH et al (2003) Endogenous sex hormones in men aged 40–80 years. Eur J Endocrinol 149:583–589PubMedCrossRefGoogle Scholar
  6. 6.
    Boyce MJ, Baisley KJ, Clark EV et al (2004) Are published normal ranges of serum testosterone too high? Results of a cross-sectional survey of serum testosterone and luteinizing hormone in healthy men. BJU Int 94:881–885PubMedCrossRefGoogle Scholar
  7. 7.
    Yeap BB, Almeida OP, Hyde Z et al (2007) In men older than 70 years, total testosterone remains stable while free testosterone declines with age. The health in men study. Eur J Endocrinol 156:585–594PubMedCrossRefGoogle Scholar
  8. 8.
    Wu FCW, Tajar A, Pye SR et al (2008) Hypothalamic-pituitary-testicular axis disruptions in older men are differentially linked to age and modifiable risk factors: the European male aging study. J Clin Endocrinol Metab 93:2737–2745PubMedCrossRefGoogle Scholar
  9. 9.
    Atlantis E, Martin SA, Haren MT et al (2009) Demographic, physical and lifestyle factors associated with androgen status: the Florey Adelaide Male Ageing Study (FAMAS). Clin Endocrinol 71:261–272CrossRefGoogle Scholar
  10. 10.
    Fukai S, Akishita M, Miyao M et al (2010) Age-related changes in plasma androgen levels and their association with cardiovascular risk factors in male Japanese office workers. Geriatr Gerontol Int 10:32–39PubMedCrossRefGoogle Scholar
  11. 11.
    Harman SM, Metter EJ, Tobin JD et al (2001) Longitudinal effects of aging on serum total and free testosterone levels in healthy men. J Clin Endocrinol Metab 86:724–730PubMedCrossRefGoogle Scholar
  12. 12.
    Feldman HA, Longcope C, Derby CA et al (2002) Age trends in the level of serum testosterone and other hormones in middle-aged men: longitudinal results from the Massachusetts male aging study. J Clin Endocrinol Metab 87:589–598PubMedCrossRefGoogle Scholar
  13. 13.
    Liu PY, Beilin J, Meier C et al (2007) Age-related changes in serum testosterone and sex hormone binding globulin in Australian men: longitudinal analyses of two geographically separate regional cohorts. J Clin Endocrinol Metab 92:3599–3603PubMedCrossRefGoogle Scholar
  14. 14.
    Travison TG, Araujo AB, O’Donnell AB et al (2007) A population-level decline in serum testosterone levels in American men. J Clin Endocrinol Metab 92:196–202PubMedCrossRefGoogle Scholar
  15. 15.
    Betancourt-Albrecht M, Cunningham GR (2003) Hypogonadism and diabetes. Int J Impot Res 15:S14–S20PubMedCrossRefGoogle Scholar
  16. 16.
    Kaplan SA, Meehan AG, Shah A (2006) The age related decrease in testosterone is significantly exacerbated in obese men with the metabolic syndrome. What are the implications for the relatively high incidence of erectile dysfunction observed in these men? J Urol 176:1524–1528PubMedCrossRefGoogle Scholar
  17. 17.
    Madersbacher S, Schatzl G, Bieglmayer C et al (2002) Impact of radical prostatectomy and turp on the hypothalamic-pituitary-gonadal hormone axis. Urology 60:869–874PubMedCrossRefGoogle Scholar
  18. 18.
    National Institutes of Health, Division of Nutrition and Physical Activity, National Center for Chronic Disease Prevention and Health Promotion’s: The practical guide: identification, evaluation, and treatment of overweight and obesity in adults. Available at: Accessed 22 Jan 2007
  19. 19.
    Rhoden EL, Ribeiro EP, Teloken C et al (2005) Diabetes mellitus is associated with subnormal serum levels of free testosterone in men. BJU 96:867–870CrossRefGoogle Scholar
  20. 20.
    Vermeulen A, Verdonck L, Kaufman JM (1999) A critical evaluation of simple methods for the estimation of free testosterone in serum. J Clin Endocrinol Metab 84:3666–3672PubMedCrossRefGoogle Scholar
  21. 21.
    Deslypere JP, Kaufman JM, Vermeulen T et al (1987) Influence of age on pulsatile luteinizing hormone release and responsiveness of the gonadotrophs to sex hormone feedback in men. J Clin Endocrinol Metab 64:68–73PubMedCrossRefGoogle Scholar
  22. 22.
    Lamberts SWJ, van den Beld AW, van der Lely AJ (1997) The endocrinology of aging. Science 278:419–424PubMedCrossRefGoogle Scholar
  23. 23.
    Vermeulen A, Kaufman JM, Giagulli VA (1996) Influence of some biological indexes on sex hormone-binding globulin and androgen levels in aging or obese males. J Clin Endocrinol Metab 81:1821–1826PubMedCrossRefGoogle Scholar
  24. 24.
    Lepage R (2006) Measurement of testosterone and its sub-fractions in Canada. Clin Biochem 39:97–108PubMedCrossRefGoogle Scholar
  25. 25.
    Goodman-Gruen D, Barrett-Connor E (2000) Sex differences in the association of endogenous sex hormone levels and glucose tolerance status in older men and women. Diabetes Care 23:912–918PubMedCrossRefGoogle Scholar
  26. 26.
    Dhindsa S, Prabhakar S, Sethi M et al (2004) Frequent occurrence of hypogonadotropic hypogonadism in type 2 diabetes. J Clin Endocrinol Metab 89:5462–5468PubMedCrossRefGoogle Scholar
  27. 27.
    Kapoor D, Aldred H, Clark S et al (2007) Clinical and Biochemical assessment of hypogonadism in men with type 2 diabetes. Diabetes Care 30:911–917PubMedCrossRefGoogle Scholar
  28. 28.
    Mah PM, Wittert GA (2010) Obesity and testicular function. Mol Cell Endocrinol 316:180–186PubMedCrossRefGoogle Scholar
  29. 29.
    Hofstra J, Loves S, van Wageningen B et al (2008) High prevalence of hypogonadotropic hypogonadism in men referred for obesity treatment. Neth J Med 66:103–109PubMedGoogle Scholar
  30. 30.
    Giton F, Fiet J, Guechot J et al (2006) Serum bioavailable testosterone: assayed or calculated? Clin Chem 52:474–481PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Graziele Halmenschlager
    • 1
  • Ernani Luis Rhoden
    • 2
    • 3
    • 4
  • Charles Edison Riedner
    • 5
  1. 1.Curso de Pós-Graduação em Ciências da SaúdeUniversidade Federal de Ciências da Saúde de Porto Alegre (UFCSPA)Porto AlegreBrazil
  2. 2.Universidade Federal de Ciências da Saúde de Porto Alegre (UFCSPA)Porto AlegreBrazil
  3. 3.CNPq-Conselho Nacional de Pesquisa, Researcher Level 2Porto AlegreBrazil
  4. 4.Médico Hospital Moinhos de VentoPorto AlegreBrazil
  5. 5.Urology Unit of Military Hospital of Porto AlegrePorto AlegreBrazil

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