Download PDF
Horm Metab Res 2018; 50(02): 138-144
DOI: 10.1055/s-0043-123348
Endocrine Care
© Georg Thieme Verlag KG Stuttgart · New York

Serum Sex Hormone Binding Globulin (SHBG) Relation with Different Components of Metabolic Syndrome in Men with Type 2 Diabetes

Khalid Siddiqui
1   Strategic Center for Diabetes Research, College of Medicine, King Saud University, Riyadh, Saudi Arabia
,
Khalid Al-Rubeaan
1   Strategic Center for Diabetes Research, College of Medicine, King Saud University, Riyadh, Saudi Arabia
2   University Diabetes Center, King Saud University, College of Medicine, Riyadh, Riyadh Province, Saudi Arabia
,
Shaik Sarfaraz Nawaz
1   Strategic Center for Diabetes Research, College of Medicine, King Saud University, Riyadh, Saudi Arabia
,
Khaled H. Aburisheh
2   University Diabetes Center, King Saud University, College of Medicine, Riyadh, Riyadh Province, Saudi Arabia
,
Anas M. Zein Alaabdin
2   University Diabetes Center, King Saud University, College of Medicine, Riyadh, Riyadh Province, Saudi Arabia
,
Ibrahim A. Tolba
2   University Diabetes Center, King Saud University, College of Medicine, Riyadh, Riyadh Province, Saudi Arabia
› Author Affiliations
Further Information

Publication History

received 01 June 2017

accepted 15 November 2017

Publication Date:
15 December 2017 (online)

Also available at
    Permissions and Reprints

Abstract

Sex hormone binding globulin (SHBG) is demonstrated to be decreased in subjects with metabolic syndrome (MetS). The aim of the present study was to investigate the association of SHBG in relation to MetS components among men with type 2 diabetes (T2D). This cross-sectional study was carried out among 429 Saudi T2D male patients aged >30 years. Metabolic syndrome was defined using International Diabetes Federation (IDF) criteria. Fasting blood glucose (FBG), HbA1c, albumin, and lipid parameter were measured. Gonadal hormones, namely total testosterone, luteinizing hormone (LH), follicle-stimulating hormone (FSH), and SHBG were determined using ELISA. The SHBG levels of the MetS group was significantly lower than non-MetS group 47.25±31.03 nmol/l vs. 56.55±37.84 nmol/l; p=0.013. As the MetS score increases, SHBG and HDL levels decrease while weight, BMI, waist circumference, SBP, DBP, FBG, HbA1c, TC, and TG levels increase. SHBG correlated with age, BMI, TG, HDL, TT, free testosterone, and bio-available testosterone. This is the first study that provides detailed analyses of SHBG with MetS components in male diabetic subjects. The mean serum SHBG levels gradually declined with the addition of MetS components in T2D men. TT, free testosterone, and bio-available testosterone remained independently associated with SHBG by multivariable regression analysis.

Key words

sex hormone binding globulin - type 2 diabetes - metabolic syndrome - total testosterone
 

  • References

  • 1 International Diabetes Federation. The IDF consensus worldwide definition of the Metabolic Syndrome 2006. Available at http://www.idf.org/webdata/docs/IDF_Meta_def_final.pdf Accessed on 18-03-2017
    PubMed
  • 2 Pugeat M, Nader N, Hogeveen K, Raverot G, Déchaud H, Grenot C. Sex hormone-binding globulin gene expression in the liver: Drugs and the metabolic syndrome. Mol Cell Endocrinol 2010; 316: 53-59
    CrossrefPubMedGoogle Scholar
  • 3 Hammond GL. Plasma steroid-binding proteins: Primary gatekeepers of steroid hormone action. J Endocrinol 2016; 230: R13-R25
    CrossrefPubMedGoogle Scholar
  • 4 Le TN, Nestler JE, Strauss JF, Wickham EP. Sex hormone-binding globulin and type 2 diabetes mellitus. Trends Endocrinol Metab 2012; 23: 32-40
    CrossrefPubMedGoogle Scholar
  • 5 Daka B, Rosen T, Jansson PA, Larsson CA, Rastam L, Lindblad U. Low sex hormone-binding globulin is associated with hypertension: A cross-sectional study in a Swedish population. BMC Cardiovasc Disord 2013; 13: 30
    CrossrefPubMedGoogle Scholar
  • 6 Ding EL, Song Y, Manson JE, Hunter DJ, Lee CC, Rifai N, Buring JE, Gaziano JM, Liu S. Sex hormone-binding globulin and risk of type 2 diabetes in women and men. N Engl J Med 2009; 361: 1152-1163
    CrossrefPubMedGoogle Scholar
  • 7 Li C, Ford ES, Li B, Giles WH, Liu S. Association of testosterone and sex hormone-binding globulin with metabolic syndrome and insulin resistance in men. Diabetes Care 2010; 33: 1618-1624
    CrossrefPubMedGoogle Scholar
  • 8 Laaksonen DE, Niskanen L, Punnonen K, Nyyssönen K, Tuomainen T-P, Valkonen V-P, Salonen R, Salonen JT. Testosterone and sex hormone-binding globulin predict the metabolic syndrome and diabetes in middle-aged men. Diabetes Care 2004; 27: 1036-1041
    CrossrefPubMedGoogle Scholar
  • 9 Al-Daghri NM, Khan N, Sabico S, Al-Attas OS, Alokail MS, Kumar S. Gender-specific associations of serum sex hormone-binding globulin with features of metabolic syndrome in children. Diabetol Metab Syndr 2016; 8: 22
    CrossrefPubMedGoogle Scholar
  • 10 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
  • 11 Hassan A, Aburisheh K, Sheikh TJ, Meo SA, Ahmed NA, Al Sharqawi AH. Prevalence of erectile dysfunction among Saudi type 2 diabetic patients. Eur Rev Med Pharmacol Sci 2014; 18: 1048-1057
    PubMedGoogle Scholar
  • 12 Kengne AP, Limen SN, Sobngwi E, Djouogo CF, Nouedoui C. Metabolic syndrome in type 2 diabetes: Comparative prevalence according to two sets of diagnostic criteria in sub-Saharan Africans. Diabetol Metab Syndr 2012; 4: 22
    CrossrefPubMedGoogle Scholar
  • 13 Pokharel DR, Khadka D, Sigdel M, Yadav NK, Acharya S, Kafle RC, Shukla PS. Prevalence of metabolic syndrome in Nepalese type 2 diabetic patients according to WHO, NCEP ATP III, IDF and Harmonized criteria. J Diabetes Metab Disord 2014; 13: 104
    CrossrefPubMedGoogle Scholar
  • 14 Pang X-N, Hu Y, Yuan Y, Shen J-P, Zha X-Y, Sun X. Lower levels sex hormone-binding globulin independently associated with metabolic syndrome in pre-elderly and elderly men in China. J Geriatr Cardiol 2013; 10: 28-33
    PubMedGoogle Scholar
  • 15 Xiao HY, Lu YH, Gong YP, Cheng XL, Tian H, Li CL. Correlation of serum sex hormone levels with metabolic syndrome in elderly men. Zhonghua Yi Xue Za Zhi 2016; 96: 702-706
    PubMedGoogle Scholar
  • 16 Yang Y-H, Zhao M-J, Zhou S-J, Lu W-H, Liang X-W, Xiong C-L, Wan C-C, Shang X-J, Gu Y-Q. Is serum sex hormone-binding globulin a dominant risk factor for metabolic syndrome?. Asian J Androl 2015; 17: 991-995
    CrossrefPubMedGoogle Scholar
  • 17 Chubb SAP, Hyde Z, Almeida OP, Flicker L, Norman PE, Jamrozik K, Hankey GJ, Yeap BB. 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
  • 18 Sá EQC, Sá FCF, Oliveira KC, Feres F, Verreschi ITN. Association between sex hormone-binding globulin (SHBG) and metabolic syndrome among men. Sao Paulo Med J 2014; 132: 111-115
    CrossrefPubMedGoogle Scholar
  • 19 Brand JS, Wareham NJ, Dowsett M, Folkerd E, van der Schouw YT, Luben RN, Khaw K-T. Associations of endogenous testosterone and SHBG with glycated haemoglobin in middle-aged and older men. Clin Endocrinol (Oxf) 2011; 74: 572-578
    CrossrefPubMedGoogle Scholar
  • 20 Vermeulen A, Kaufman JM, Deslypere JP, Thomas G. Attenuated luteinizing hormone (LH) pulse amplitude but normal LH pulse frequency, and its relation to plasma androgens in hypogonadism of obese men. J Clin Endocrinol Metab 1993; 76: 1140-1146
    PubMedGoogle Scholar
  • 21 Dandona P, Rosenberg MT. A practical guide to male hypogonadism in the primary care setting. Int J Clin Pract 2010; 64: 682-696
    CrossrefPubMedGoogle Scholar
  • 22 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: 460-464
    CrossrefPubMedGoogle Scholar
  • 23 Selva DM, Hogeveen KN, Innis SM, Hammond GL. Monosaccharide-induced lipogenesis regulates the human hepatic sex hormone-binding globulin gene. J Clin Invest 2007; 117: 3979-3987
    PubMedGoogle Scholar
  • 24 Simó R, Barbosa-Desongles A, Lecube A, Hernandez C, Selva DM. Potential role of tumor necrosis factor-α in downregulating sex hormone-binding globulin. Diabetes 2012; 61: 372-382
    CrossrefPubMedGoogle Scholar
  • 25 Simó R, Barbosa-Desongles A, Hernandez C, Selva DM. IL1β down-regulation of sex hormone-binding globulin production by decreasing HNF-4α via MEK-1/2 and JNK MAPK pathways. Mol Endocrinol 2012; 26: 1917-1927
    CrossrefPubMedGoogle Scholar
  • 26 Selva DM, Hammond GL. Peroxisome-proliferator receptor gamma represses hepatic sex hormone-binding globulin expression. Endocrinology 2009; 150: 2183-2189
    CrossrefPubMedGoogle Scholar
  • 27 Pang X-N, Yuan Y, Sun Y, Shen J-P, Zha X-Y, Hu Y. The relationship of sex hormone-binding globulin (SHBG) gene polymorphisms with serum SHBG level and metabolic syndrome in Chinese Han males. Aging Clin Exp Res 2014; 26: 583-589
    CrossrefPubMedGoogle Scholar