Download PDF
Exp Clin Endocrinol Diabetes 2013; 121(07): 407-412
DOI: 10.1055/s-0033-1345164
Article
© Georg Thieme Verlag KG Stuttgart · New York

Total Testosterone and Sex Hormone-binding Globulin are Significantly Associated with Metabolic Syndrome in Middle-aged and Elderly Men

K.-Y. Chin
1   Pharmacology Department, Faculty of Medicine, Universiti Kebangsaan Malaysia
,
S. Ima-Nirwana
1   Pharmacology Department, Faculty of Medicine, Universiti Kebangsaan Malaysia
,
I. N. Mohamed
1   Pharmacology Department, Faculty of Medicine, Universiti Kebangsaan Malaysia
,
A. Aminuddin
2   Physiology Department, Faculty of Medicine, Universiti Kebangsaan Malaysia
,
W. Z. W. Ngah
3   Biochemistry Department, Faculty of Medicine, Universiti Kebangsaan Malaysia
› Author Affiliations
Further Information

Publication History

received 01 November 2012
first decision 27 December 2012

accepted 19 April 2013

Publication Date:
13 June 2013 (online)

Also available at
    Permissions and Reprints

Abstract

Testosterone and sex hormone-binding globulin (SHBG) have been shown to be associated with metabolic syndrome (MS) in men. This study aimed at validating these relationships in a group of middle-aged and elderly men and assessing their strength of association to MS. A cross-sectional study of 332 Malaysian men aged 40 years and above was conducted. The blood of subject was collected under fasting condition for determination of testosterone, SHBG, glucose and lipid levels. Their medical history, smoking and alcohol consumption status, waist circumference (WC), body mass index (BMI) and blood pressure (BP) were recorded. All testosterone and SHBG levels were significantly reduced in MS subjects compared to non-MS subjects (p<0.05). Testosterone and SHBG were correlated significantly with most of the MS indicators without adjustments. In multiple regression analysis, the triglyceride level was the only MS indicator that was significantly, inversely and independently associated with all testosterone measurements and SHBG (p<0.05). Waist circumference was significantly and negatively associated with SHBG level (p<0.05) though not independent of BMI. Total testosterone and SHBG were significantly and inversely associated with the presence of MS. Testosterone and SHBG are potential intervention targets for the prevention of MS in men.

Key words

testosterone - sex hormone-binding ­globulin - metabolic syndrome - men
 

  • References

  • 1 Svartberg J. Epidemiology: testosterone and the metabolic syndrome. Int J Impot Res 2007; 19: 124-128
    CrossrefPubMedGoogle Scholar
  • 2 Kassi E, Pervanidou P, Kaltsas G et al. Metabolic syndrome: definitions and controversies. BMC Medicine 2011; 9: 48
    CrossrefPubMedGoogle Scholar
  • 3 Alberti KGMM, Eckel RH, Grundy SM et al. Harmonizing the Metabolic Syndrome. Circulation 2009; 120: 1640-1645
    CrossrefPubMedGoogle Scholar
  • 4 Rossouw JE. Hormones, genetic factors, and gender differences in cardiovascular disease. Cardiovasc Res 2002; 53: 550-557
    CrossrefPubMedGoogle Scholar
  • 5 Morrison JA, Barton BA, Biro FM et al. Sex hormones and the changes in adolescent male lipids: Longitudinal studies in a biracial cohort. J Pediatr 2003; 142: 637-642
    CrossrefPubMedGoogle Scholar
  • 6 Morrison JA, Sprecher DL, Biro FM et al. Serum testosterone associates with lower high-density lipoprotein cholesterol in black and white males, 10 to 15 years of age, through lowered apolipoprotein AI and AII concentrations. Metabolism 2002; 51: 432-437
    CrossrefPubMedGoogle Scholar
  • 7 Bhasin S, Woodhouse L, Casaburi R et al. Testosterone dose-response relationships in healthy young men. Am J Physiol Endocrinol Metab 2001; 281: E1172-E1181
    CrossrefPubMedGoogle Scholar
  • 8 Hyde Z, Norman PE, Flicker L et al. Low Free Testosterone Predicts Mortality from Cardiovascular Disease But Not Other Causes: The Health in Men Study. J Clin Endocrinol Metab 2012; 97: 179-189
    CrossrefPubMedGoogle Scholar
  • 9 Khaw K-T, Dowsett M, Folkerd E et al. Endogenous Testosterone and Mortality Due to All Causes, Cardiovascular Disease, and Cancer in Men. Circulation 2007; 116: 2694-2701
    CrossrefPubMedGoogle Scholar
  • 10 Kaufman JM, Vermeulen A. The Decline of Androgen Levels in Elderly Men and Its Clinical and Therapeutic Implications. Endocr Rev 2005; 26: 833-876
    CrossrefPubMedGoogle Scholar
  • 11 Riggs BL, Khosla S, Melton 3rd LJ. Sex steroids and the construction and conservation of the adult skeleton. Endocr Rev 2002; 23: 279-302
    CrossrefPubMedGoogle Scholar
  • 12 Svartberg J, von Muhlen D, Sundsfjord J et al. Waist circumference and testosterone levels in community dwelling men. The Tromso study. Eur J Epidemiol 2004; 19: 657-663
    CrossrefPubMedGoogle Scholar
  • 13 Jiann BP, Hsieh JT, Liu SP et al. Associations of endogenous testosterone and lipid profiles in middle-aged to older Taiwanese men. Int J Impot Res 2011; 23: 62-69
    CrossrefPubMedGoogle Scholar
  • 14 Tsai EC, Matsumoto AM, Fujimoto WY et al. Association of Bioavailable, Free, and Total Testosterone With Insulin Resistance. Diabetes Care 2004; 27: 861-868
    CrossrefPubMedGoogle Scholar
  • 15 Kupelian V, Page ST, Araujo AB et al. Low sex hormone-binding globulin, total testosterone, and symptomatic androgen deficiency are associated with development of the metabolic syndrome in nonobese men. J Clin Endocrinol Metab 2006; 91: 843-850
    CrossrefPubMedGoogle Scholar
  • 16 Muller M, Grobbee DE, den Tonkelaar I et al. Endogenous sex hormones and metabolic syndrome in aging men. J Clin Endocrinol Metab 2005; 90: 2618-2623
    CrossrefPubMedGoogle Scholar
  • 17 Chen RY, Wittert GA, Andrews GR. Relative androgen deficiency in relation to obesity and metabolic status in older men. Diabetes Obes Metab 2006; 8: 429-435
    CrossrefPubMedGoogle Scholar
  • 18 Katabami T, Kato H, Asahina T et al. Serum free testosterone and metabolic syndrome in Japanese men. Endocr J 2010; 57: 533-539
    CrossrefPubMedGoogle Scholar
  • 19 Li C, Ford ES, Li B et al. Association of testosterone and sex hormone-binding globulin with metabolic syndrome and insulin resistance in men. Diabetes Care 2010; 33: 1618-1624
    CrossrefPubMedGoogle Scholar
  • 20 Chin KY, Soelaiman IN, Mohamed IN et al. Ethnicity, Smoking and Body Composition Influence Testosterone and Estradiol Levels in Healthy Young Adult Men in Malaysia: A Pilot Study. Int J Endocrinol Metab 2012; 10: 404-410
    CrossrefPubMedGoogle Scholar
  • 21 Chin K-Y, Soelaiman I-N, Mohamed IN et al. Serum testosterone, sex hormone-binding globulin and total calcium levels predict the calcaneal speed of sound in men. Clinics 2012; 67: 911-916
    CrossrefPubMedGoogle Scholar
  • 22 Sodergard R, Backstrom T, Shanbhag V et al. Calculation of free and bound fractions of testosterone and estradiol-17 beta to human plasma proteins at body temperature. J Steroid Biochem 1982; 16: 801-810
    CrossrefPubMedGoogle Scholar
  • 23 Friedewald WT, Levy RI, Fredrickson DS. Estimation of the Concentration of Low-Density Lipoprotein Cholesterol in Plasma, Without Use of the Preparative Ultracentrifuge. Clin Chem 1972; 18: 499-502
    CrossrefPubMedGoogle Scholar
  • 24 Alberti KGMM, Zimmet PZ. Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus. Provisional report of a WHO Consultation. Diabet Med 1998; 15: 539-553
    CrossrefPubMedGoogle Scholar
  • 25 Expert Panel on Detection Evaluation Treatment of High Blood Cholesterol in Adults . Executive summary of the third report of the national cholesterol education program (ncep) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (adult treatment panel iii). JAMA 2001; 285: 2486-2497
    CrossrefPubMedGoogle Scholar
  • 26 Grundy SM, Brewer HB, Cleeman JI et al. Definition of Metabolic Syndrome. Arterioscler Thromb Vasc Biol 2004; 24: e13-e18
    CrossrefPubMedGoogle Scholar
  • 27 Alberti KGMM, Zimmet P, Shaw J. The metabolic syndrome: a new worldwide definition. Lancet 2005; 366: 1059-1062
    CrossrefPubMedGoogle Scholar
  • 28 Laila Ruwaida MZ, Nur Firdaus I, Wan Manan WM et al. The Prevalence of Metabolic Syndrome According to Various Definitions and Hypertriglyceridemic-Waist in Malaysian Adults. Int J Prev Med 2011; 2: 229-237
    PubMedGoogle Scholar
  • 29 Langfort J, Jagsz S, Dobrzyn P et al. Testosterone affects hormone-sensitive lipase (HSL) activity and lipid metabolism in the left ventricle. Biochem Biophys Res Commun 2010; 399: 670-676
    CrossrefPubMedGoogle Scholar
  • 30 Agledahl I, Skjærpe P-A, Hansen J-B et al. Low serum testosterone in men is inversely associated with non-fasting serum triglycerides: The Tromsø study. Nutr Metab Cardiovasc Dis 2008; 18: 256-262
    CrossrefPubMedGoogle Scholar
  • 31 Van Pottelbergh I, Braeckman L, De Bacquer D et al. Differential contribution of testosterone and estradiol in the determination of cholesterol and lipoprotein profile in healthy middle-aged men. Atherosclerosis 2003; 166: 95-102
    CrossrefPubMedGoogle Scholar
  • 32 Maggio M, Lauretani F, Ceda GP et al. Association Between Hormones and Metabolic Syndrome in Older Italian Men. J Am Geriatr Soc 2006; 54: 1832-1838
    CrossrefPubMedGoogle Scholar
  • 33 Winters SJ, Brufsky A, Weissfeld J et al. Testosterone, sex hormone-binding globulin, and body composition in young adult African American and Caucasian men. Metabolism 2001; 50: 1242-1247
    CrossrefPubMedGoogle Scholar
  • 34 Paul Chubb SA, Hyde Z, Almeida OP et al. Lower sex hormone-binding globulin is more strongly associated with metabolic syndrome than lower total testosterone in older men: the Health in Men Study. Eur J Endocrinol 2008; 158: 785-792
    CrossrefPubMedGoogle Scholar
  • 35 Bhasin S, Jasjua GK, Pencina M et al. Sex Hormone-Binding Globulin, but Not Testosterone, Is Associated Prospectively and Independently With Incident Metabolic Syndrome in Men. Diabetes Care 2011; 34: 2464-2470
    CrossrefPubMedGoogle Scholar
  • 36 Laaksonen DE, Niskanen L, Punnonen K et al. Testosterone and Sex Hormone-Binding Globulin Predict the Metabolic Syndrome and Diabetes in Middle-Aged Men. Diabetes Care 2004; 27: 1036-1041
    CrossrefPubMedGoogle Scholar
  • 37 Bhattacharya R, Khera M, Blick G et al. Effect of 12 months of testosterone replacement therapy on metabolic syndrome components in hypogonadal men: data from the Testim Registry in the US (TRiUS). BMC Endocr Disord 2011; 11: 18
    CrossrefPubMedGoogle Scholar
  • 38 Kalinchenko SY, Tishova YA, Mskhalaya GJ et al. Effects of testosterone supplementation on markers of the metabolic syndrome and inflammation in hypogonadal men with the metabolic syndrome: the double-blinded placebo-controlled Moscow study. Clin Endocrinol 2010; 73: 602-612
    CrossrefPubMedGoogle Scholar
  • 39 Statistics Department of Malaysia . Population Distribution and Basic Demographic Characteristics. In: Putrajaya: Statistics Department of Malaysia; 2011
    Google Scholar
  • 40 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: 3666-3672
    CrossrefPubMedGoogle Scholar