Can Low SHBG Serum Concentration Be A Good Early Marker Of Male Hypogonadism In Metabolic Syndrome?

References

• Basaria S , Muller DC , Carducci MA , Egan J , Dobs AS . Hyperglycemia and insulin resistance in men with prostate carcinoma who receive androgen-deprivation therapy. Cancer . 2006;106(3):581–588. doi:10.1002/cncr.21642 16388523
   PubMed Web of Science ®Google Scholar
• Hajamor S , Després J-P , Couillard C , et al. Relationship between sex hormone-binding globulin levels and features of the metabolic syndrome. Metabolism . 2003;52(6):724–730. doi:10.1016/s0026-0495(03)00066-0 12800098
   PubMed Web of Science ®Google Scholar
• 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(5):1036–1041. doi:10.2337/diacare.27.5.1036 15111517
   PubMed Web of Science ®Google Scholar
• Kupelian V , Page ST , Araujo AB , Travison TG , Bremner WJ , McKinlay JB . 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(3):843–850. doi:10.1210/jc.2005-1326 16394089
   PubMed Web of Science ®Google Scholar
• Hak AE , Witteman JCM , de Jong FH , Geerlings MI , Hofman A , Pols HAP . Low levels of endogenous androgens increase the risk of atherosclerosis in elderly men: the Rotterdam Study. J Clin Endocrinol Metab . 2002;87(8):3632–3639. doi:10.1210/jcem.87.8.8762 12161487
   PubMed Web of Science ®Google Scholar
• Alberti KGMM , Eckel RH , Grundy SM , et al. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation . 2009;120(16):1640–1645. doi:10.1161/CIRCULATIONAHA.109.192644 19805654
   PubMed Web of Science ®Google Scholar
• Feldman HA , Longcope C , Derby CA , et al. 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 . 2002;87(2):589–598. doi:10.1210/jcem.87.2.8201 11836290
   PubMed Web of Science ®Google Scholar
• Tannenbaum C , Barrett-Connor E , Laughlin GA , Platt RW . A longitudinal study of dehydroepiandrosterone sulphate (DHEAS) change in older men and women: the Rancho Bernardo Study. Eur J Endocrinol . 2004;151(6):717–725. doi:10.1530/eje.0.1510717 15588238
   PubMed Web of Science ®Google Scholar
• Vermeulen A , Rubens R , Verdonck L . Testosterone secretion and metabolism in male senescence. J Clin Endocrinol Metab . 1972;34(4):730–735. doi:10.1210/jcem-34-4-730 5012774
   PubMed Web of Science ®Google Scholar
• Morley JE , Kaiser FE , Perry HM , et al. Longitudinal changes in testosterone, luteinizing hormone, and follicle-stimulating hormone in healthy older men. Metabolism . 1997;46(4):410–413. doi:10.1016/s0026-0495(97)90057-3 9109845
   PubMed Web of Science ®Google Scholar
• Harman SM , Metter EJ , Tobin JD , Pearson J , Blackman MR ; Baltimore Longitudinal Study of Aging. Longitudinal effects of aging on serum total and free testosterone levels in healthy men. J Clin Endocrinol Metab . 2001;86(2):724–731. doi:10.1210/jcem.86.2.7219 11158037
   PubMed Web of Science ®Google Scholar
• Sparrow D , Bosse R , Rowe JW . The influence of age, alcohol consumption, and body build on gonadal function in men. J Clin Endocrinol Metab . 1980;51(3):508–512. doi:10.1210/jcem-51-3-508 6773977
   PubMed Web of Science ®Google Scholar
• van Den Beld AW , de Jong FH , Grobbee DE , Pols HA , Lamberts SW . Measures of bioavailable serum testosterone and estradiol and their relationships with muscle strength, bone density, and body composition in elderly men. J Clin Endocrinol Metab . 2000;85(9):3276–3282. doi:10.1210/jcem.85.9.6825 10999822
   PubMed Web of Science ®Google Scholar
• Harman SM , Tsitouras PD . Reproductive hormones in aging men. I. Measurement of sex steroids, basal luteinizing hormone, and Leydig cell response to human chorionic gonadotropin. J Clin Endocrinol Metab . 1980;51(1):35–40. doi:10.1210/jcem-51-1-35 7189758
   PubMed Web of Science ®Google Scholar
• 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. doi:10.2337/dc09-1788
   Web of Science ®Google Scholar
• de Sá EQC , de Sá FCF , Oliveira KC , Feres F , Verreschi ITN . Association between sex hormone-binding globulin (SHBG) and metabolic syndrome among men. Sao Paulo Med J Rev Paul Med . 2014;132(2):111–115.
   Web of Science ®Google Scholar
• Cooper LA , Page ST , Amory JK , Anawalt BD , Matsumoto AM . The association of obesity with sex hormone-binding globulin is stronger than the association with ageing–implications for the interpretation of total testosterone measurements. Clin Endocrinol (Oxf) . 2015;83(6):828–833. doi:10.1111/cen.12768 25777143
   PubMed Web of Science ®Google Scholar
• Seidell JC , Björntorp P , Sjöström L , Kvist H , Sannerstedt R . Visceral fat accumulation in men is positively associated with insulin, glucose, and C-peptide levels, but negatively with testosterone levels. Metabolism . 1990;39(9):897–901. doi:10.1016/0026-0495(90)90297-p 2202881
   PubMed Web of Science ®Google Scholar
• Tchernof A , Labrie F , Bélanger A , Després JP . Obesity and metabolic complications: contribution of dehydroepiandrosterone and other steroid hormones. J Endocrinol . 1996;150(Suppl):S155–164.8943799
   PubMed Web of Science ®Google Scholar
• Haring R , Völzke H , Felix SB , et al. Prediction of metabolic syndrome by low serum testosterone levels in men: results from the study of health in Pomerania. Diabetes . 2009;58(9):2027–2031. doi:10.2337/db09-0031 19581420
   PubMed Web of Science ®Google Scholar
• Mohammed M , AL-Habori M , Abdullateef A , Saif-Ali R . Impact of metabolic syndrome factors on testosterone and SHBG in type 2 diabetes mellitus and metabolic syndrome. J Diabetes Res . 2018. doi:10.1155/2018/4926789
   Web of Science ®Google Scholar
• Kroboth PD , Salek FS , Pittenger AL , Fabian TJ , Frye RF . DHEA and DHEA-S: a review. J Clin Pharmacol . 1999;39(4):327–348. doi:10.1177/00912709922007903 10197292
   PubMed Web of Science ®Google Scholar
• Blouin K , Després J-P , Couillard C , et al. Contribution of age and declining androgen levels to features of the metabolic syndrome in men. Metabolism . 2005;54(8):1034–1040. doi:10.1016/j.metabol.2005.03.006 16092053
   PubMed Web of Science ®Google Scholar
• Maggio M , Lauretani F , Ceda GP , et al. Association between hormones and metabolic syndrome in older Italian men. J Am Geriatr Soc . 2006;54(12):1832–1838. doi:10.1111/j.1532-5415.2006.00963.x 17198487
   PubMed Web of Science ®Google Scholar
• Rodriguez A , Muller DC , Metter EJ , et al. Aging, androgens, and the metabolic syndrome in a longitudinal study of aging. J Clin Endocrinol Metab . 2007;92(9):3568–3572. doi:10.1210/jc.2006-2764 17595254
   PubMed Web of Science ®Google Scholar
• Chen YC , Chang HH , Wen CJ , et al. Elevated serum dehydroepiandrosterone sulphate level correlates with increased risk for metabolic syndrome in the elderly men. Eur J Clin Invest . 2010;40(3):220–225. doi:10.1111/j.1365-2362.2009.02248.x 20050878
   PubMed Web of Science ®Google Scholar
• Hines GA , Smith ER , Azziz R . Influence of insulin and testosterone on adrenocortical steroidogenesis in vitro: preliminary studies. Fertil Steril . 2001;76(4):730–735. doi:10.1016/S0015-0282(01)02014-3 11591406
   PubMed Web of Science ®Google Scholar
• Vermeulen A , Kaufman JM , Giagulli VA . Influence of some biological indexes on sex hormone-binding globulin and androgen levels in aging or obese males. J Clin Endocrinol Metab . 1996;81(5):1821–1826. doi:10.1210/jcem.81.5.8626841 8626841
   PubMed Web of Science ®Google Scholar
• Pasquali R , Macor C , Vicennati V , et al. Effects of acute hyperinsulinemia on testosterone serum concentrations in adult obese and normal-weight men. Metabolism . 1997;46(5):526–529. doi:10.1016/s0026-0495(97)90189-x 9160819
   PubMed Web of Science ®Google Scholar
• Nestler JE , Beer NA , Jakubowicz DJ , Colombo C , Beer RM . Effects of insulin reduction with benfluorex on serum dehydroepiandrosterone (DHEA), DHEA sulfate, and blood pressure in hypertensive middle-aged and elderly men. J Clin Endocrinol Metab . 1995;80(2):700–706. doi:10.1210/jcem.80.2.7852539 7852539
   PubMed Web of Science ®Google Scholar
• Weiss EP , Villareal DT , Fontana L , Han D-H , Holloszy JO . Dehydroepiandrosterone (DHEA) replacement decreases insulin resistance and lowers inflammatory cytokines in aging humans. Aging . 2011;3(5):533–542. doi:10.18632/aging.100327 21566261
   PubMedGoogle Scholar
• Talaei A , Amini M , Siavash M , Zare M . The effect of dehydroepiandrosterone on insulin resistance in patients with impaired glucose tolerance. Horm Athens Greece . 2010;9(4):326–331.
   Web of Science ®Google Scholar
• Nestler JE , Kahwash Z . Sex-specific action of insulin to acutely increase the metabolic clearance rate of dehydroepiandrosterone in humans. J Clin Invest . 1994;94(4):1484–1489. doi:10.1172/JCI117487 7929824
   PubMed Web of Science ®Google Scholar
• Lavallée B , Provost PR , Kahwash Z , Nestler JE , Bélanger A . Effect of insulin on serum levels of dehydroepiandrosterone metabolites in men. Clin Endocrinol (Oxf) . 1997;46(1):93–100. doi:10.1046/j.1365-2265.1997.d01-1736.x 9059564
   PubMed Web of Science ®Google Scholar
• De Pergola G . The adipose tissue metabolism: role of testosterone and dehydroepiandrosterone. Int J Obes Relat Metab Disord J Int Assoc Study Obes . 2000;24 Suppl 2:S59–S63.
   Web of Science ®Google Scholar
• Hernández-Morante JJ , Pérez-de-Heredia F , Luján JA , Zamora S , Garaulet M . Role of DHEA-S on body fat distribution: gender- and depot-specific stimulation of adipose tissue lipolysis. Steroids . 2008;73(2):209–215. doi:10.1016/j.steroids.2007.10.005 18063002
   PubMed Web of Science ®Google Scholar
• Clark BJ , Prough RA , Klinge CM . Mechanisms of action of dehydroepiandrosterone. Vitam Horm . 2018;108:29–73. doi:10.1016/bs.vh.2018.02.003 30029731
   PubMed Web of Science ®Google Scholar
• Salzano A , D’Assante R , Heaney LM , et al. Klinefelter syndrome, insulin resistance, metabolic syndrome, and diabetes: review of literature and clinical perspectives. Endocrine . 2018;61(2):194–203. doi:10.1007/s12020-018-1584-6 29572708
   PubMed Web of Science ®Google Scholar
• Lieblich JM , Rogol AD , White BJ , Rosen SW . Syndrome of anosmia with hypogonadotropic hypogonadism (kallmann syndrome): clinical and laboratory studies in 23 cases. Am J Med . 1982;73(4):506–519. doi:10.1016/0002-9343(82)90329-1 6812419
   PubMed Web of Science ®Google Scholar
• 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(3):460–464. doi:10.1210/jcem-67-3-460 2842359
   PubMed Web of Science ®Google Scholar
• Pasquali R , Casimirri F , De Iasio R , et al. Insulin regulates testosterone and sex hormone-binding globulin concentrations in adult normal weight and obese men. J Clin Endocrinol Metab . 1995;80(2):654–658. doi:10.1210/jcem.80.2.7852532 7852532
   PubMed Web of Science ®Google Scholar
• Hautanen A . Synthesis and regulation of sex hormone-binding globulin in obesity. Int J Obes Relat Metab Disord J Int Assoc Study Obes . 2000;24 Suppl 2:S64–S70. doi:10.1038/sj.ijo.0801281
   Web of Science ®Google Scholar
• Sarkar M , VanWagner LB , Terry JG , et al. Sex hormone-binding globulin levels in young men are associated with nonalcoholic fatty liver disease in midlife. Am J Gastroenterol . 2019. doi:10.14309/ajg.0000000000000138
   Web of Science ®Google Scholar
• Moon H , Choi I , Kim S , et al. Cross-sectional association between testosterone, sex hormone-binding globulin and metabolic syndrome: the Healthy Twin Study. Clin Endocrinol (Oxf) . 2017;87(5):523–531. doi:10.1111/cen.13390 28581026
   PubMed Web of Science ®Google Scholar
• Heinlein CA , Chang C . The roles of androgen receptors and androgen-binding proteins in nongenomic androgen actions. Mol Endocrinol Baltim Md . 2002;16(10):2181–2187. doi:10.1210/me.2002-0070
   Google Scholar
• Kahn SM , Hryb DJ , Nakhla AM , Romas NA , Rosner W . Sex hormone-binding globulin is synthesized in target cells. J Endocrinol . 2002;175(1):113–120. doi:10.1677/joe.0.1750113 12379495
   PubMed Web of Science ®Google Scholar
• Kaukua J , Pekkarinen T , Sane T , Mustajoki P . Sex hormones and sexual function in obese men losing weight. Obes Res . 2003;11(6):689–694. doi:10.1038/oby.2003.98 12805389
   PubMedGoogle Scholar
• Hutchinson WL , Koenig W , Fröhlich M , Sund M , Lowe GDO , Pepys MB . Immunoradiometric assay of circulating C-reactive protein: age-related values in the adult general population. Clin Chem . 2000;46(7):934–938.10894836
   PubMed Web of Science ®Google Scholar
• Eckel RH , Grundy SM , Zimmet PZ . The metabolic syndrome. Lancet . 2005;365(9468):1415–1428. doi:10.1016/S0140-6736(05)66378-7 15836891
   PubMed Web of Science ®Google Scholar
• Maury E , Brichard SM . Adipokine dysregulation, adipose tissue inflammation and metabolic syndrome. Mol Cell Endocrinol . 2010;314(1):1–16. doi:10.1016/j.mce.2009.07.031 19682539
   PubMed Web of Science ®Google Scholar
• Esser N , Legrand-Poels S , Piette J , Scheen AJ , Paquot N . Inflammation as a link between obesity, metabolic syndrome and type 2 diabetes. Diabetes Res Clin Pract . 2014;105(2):141–150. doi:10.1016/j.diabres.2014.04.006 24798950
   PubMed Web of Science ®Google Scholar
• Ding Y , Li S , Ma R-L , et al. Association of homeostasis model assessment of insulin resistance, adiponectin, and low-grade inflammation with the course of the metabolic syndrome. Clin Biochem . 2015;48(7–8):503–507. doi:10.1016/j.clinbiochem.2015.02.005 25700597
   PubMed Web of Science ®Google Scholar
• Balogh A , Karpati E , Schneider AE , et al. Sex hormone-binding globulin provides a novel entry pathway for estradiol and influences subsequent signaling in lymphocytes via membrane receptor. Sci Rep . 2019;9(1):4. doi:10.1038/s41598-018-36882-3 30626909
   PubMed Web of Science ®Google Scholar
• Herman WA , Lącka K , Kaufman E , Wójcicka M , Kramer L , Losy J . The associations between iL-18 serum levels and the prevalence of metabolic syndrome in Polish men over the age of 40 according to other selected inflammatory indices and androgens: comparison of NCEP with IDF criteria. Exp Clin Endocrinol Diabetes Off J Ger Soc Endocrinol Ger Diabetes Assoc . 2011;119(7):423–430. doi:10.1055/s-0030-1270467
   Web of Science ®Google Scholar
• 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(2):372–382. doi:10.2337/db11-0727 22210320
   PubMed Web of Science ®Google Scholar
• Kiortsis DN , Mavridis AK , Vasakos S , Nikas SN , Drosos AA . Effects of infliximab treatment on insulin resistance in patients with rheumatoid arthritis and ankylosing spondylitis. Ann Rheum Dis . 2005;64(5):765–766. doi:10.1136/ard.2004.026534 15458960
   PubMed Web of Science ®Google Scholar
• 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(12):3979–3987. doi:10.1172/JCI32249 17992261
   PubMed Web of Science ®Google Scholar
• 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: the framingham heart study. Diabetes Care . 2011;34(11):2464–2470. doi:10.2337/dc11-0888 21926281
   PubMed Web of Science ®Google Scholar
• Ding EL , Song Y , Manson JE , et al. Sex hormone-binding globulin and risk of type 2 diabetes in women and men. N Engl J Med . 2009;361(12):1152–1163. doi:10.1056/NEJMoa0804381 19657112
   PubMed Web of Science ®Google Scholar
• Perry JRB , Weedon MN , Langenberg C , et al. Genetic evidence that raised sex hormone binding globulin (SHBG) levels reduce the risk of type 2 diabetes. Hum Mol Genet . 2010;19(3):535–544. doi:10.1093/hmg/ddp522 19933169
   PubMed Web of Science ®Google Scholar
• Svartberg J , Schirmer H , Wilsgaard T , et al. Single-nucleotide polymorphism, rs1799941 in the Sex Hormone-Binding Globulin (SHBG) gene, related to both serum testosterone and SHBG levels and the risk of myocardial infarction, type 2 diabetes, cancer and mortality in men: the Tromsø Study. Andrology . 2014;2(2):212–218. doi:10.1111/j.2047-2927.2013.00174.x 24327369
   PubMed Web of Science ®Google Scholar
• Brand JS , Rovers MM , Yeap BB , et al. Testosterone, sex hormone-binding globulin and the metabolic syndrome in men: an individual participant data meta-analysis of observational studies. PLoS One . 2014;9(7):e100409. doi:10.1371/journal.pone.0100409 25019163
   PubMed Web of Science ®Google Scholar