Abstract
Purpose
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.
Methods
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.
Results
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).
Conclusions
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.
Similar content being viewed by others
References
Lunenfeld B (2002) The ageing male: demographic and challenges. World J Urol 20:11–16
Gooren LJ (2010) Androgens and male aging: current evidence of safety and efficacy. Asian J Androl 12:136–151
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 30:1–9
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 149:145–152
Muller M, den Tonkelaar I, Thijssen JHH et al (2003) Endogenous sex hormones in men aged 40–80 years. Eur J Endocrinol 149:583–589
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 94:881–885
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 156:585–594
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 93:2737–2745
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 71:261–272
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 10:32–39
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 86:724–730
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 87:589–598
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 92:3599–3603
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 92:196–202
Betancourt-Albrecht M, Cunningham GR (2003) Hypogonadism and diabetes. Int J Impot Res 15:S14–S20
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 176:1524–1528
Madersbacher S, Schatzl G, Bieglmayer C et al (2002) Impact of radical prostatectomy and turp on the hypothalamic-pituitary-gonadal hormone axis. Urology 60:869–874
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:http://www.nhlbi.nih.gov/guidelines/obesity/prctgd_c.pdf. Accessed 22 Jan 2007
Rhoden EL, Ribeiro EP, Teloken C et al (2005) Diabetes mellitus is associated with subnormal serum levels of free testosterone in men. BJU 96:867–870
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 84:3666–3672
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 64:68–73
Lamberts SWJ, van den Beld AW, van der Lely AJ (1997) The endocrinology of aging. Science 278:419–424
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 81:1821–1826
Lepage R (2006) Measurement of testosterone and its sub-fractions in Canada. Clin Biochem 39:97–108
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 23:912–918
Dhindsa S, Prabhakar S, Sethi M et al (2004) Frequent occurrence of hypogonadotropic hypogonadism in type 2 diabetes. J Clin Endocrinol Metab 89:5462–5468
Kapoor D, Aldred H, Clark S et al (2007) Clinical and Biochemical assessment of hypogonadism in men with type 2 diabetes. Diabetes Care 30:911–917
Mah PM, Wittert GA (2010) Obesity and testicular function. Mol Cell Endocrinol 316:180–186
Hofstra J, Loves S, van Wageningen B et al (2008) High prevalence of hypogonadotropic hypogonadism in men referred for obesity treatment. Neth J Med 66:103–109
Giton F, Fiet J, Guechot J et al (2006) Serum bioavailable testosterone: assayed or calculated? Clin Chem 52:474–481
Acknowledgments
Dr. Rhoden is a researcher of Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)–“National Counsel of Technological and Scientific Development”. M.Sc. Halmenschlager is supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—CAPES. We thank Federal University of Health Sciences of Porto Alegre (UFCSPA) for financial support.
Conflict of interest
None.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Halmenschlager, G., Rhoden, E.L. & Riedner, C.E. The influence of age on bioavailable and free testosterone is independent of body mass index and glucose levels. World J Urol 29, 541–546 (2011). https://doi.org/10.1007/s00345-011-0724-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00345-011-0724-x