Testosterone levels and type 2 diabetes in men: current knowledge and clinical implications

References

• Danaei G Finucane MM Lu Y National, regional, and global trends in fasting plasma glucose and diabetes prevalence since 1980: systematic analysis of health examination surveys and epidemiological studies with 370 country-years and 2.7 million participants Lancet 2011 378 31 40 21705069
   PubMed Web of Science ®Google Scholar
• Ferrannini E Vichi S Beck-Nielson H Laakso M Paolisso G Smith U Insulin action and age Diabetes 1996 54 947 956 8666147
   PubMed Web of Science ®Google Scholar
• Haring R Baumeister SE Völzke H Prospective association of low total testosterone concentrations with an adverse lipid profile and increased incident dyslipidemia Eur J Cardiovasc Prev Rehabil 2011 18 86 96 20562628
   PubMedGoogle Scholar
• Haring R Völzke H Felix SB Prediction of metabolic syndrome by low serum testosterone levels in men: results from the study of health in Pomerania Diabetes 2009 58 2027 2031 19581420
   PubMed Web of Science ®Google Scholar
• Schipf S Haring R Friedrich N Low total testosterone is associated with increased risk of incident type 2 diabetes mellitus in men: results from the Study of Health in Pomerania (SHIP) Aging Male 2011 14 168 175 21039324
   PubMed Web of Science ®Google Scholar
• Svartberg J von Mühlen D Mathiesen E Joakimsen O Bønaa KH Stensland-Bugge E Low testosterone levels are associated with carotid atherosclerosis in men J Intern Med 2006 259 576 582 16704558
   PubMed Web of Science ®Google Scholar
• Araujo AB Kupelian V Page ST Handelsman DJ Bremner WJ McKinlay JB Sex steroids and all-cause and cause-specific mortality in men Arch Intern Med 2007 167 1252 1260 17592098
   PubMed Web of Science ®Google Scholar
• Ding EL Song Y Malik VS Liu S Sex differences of endogenous sex hormones and risk of type 2 diabetes: a systematic review and meta-analysis JAMA 2006 295 1288 1299 16537739
   PubMed Web of Science ®Google Scholar
• Corona G Monami M Rastrelli G Type 2 diabetes mellitus and testosterone: a meta-analysis study Int J Androl 2011 34 6 Pt 1 528 540 20969599
   PubMed Web of Science ®Google Scholar
• Selvin E Feinleib M Zhang L Androgens and diabetes in men: results from the Third National Health and Nutrition Examination Survey (NHANES III) Diabetes Care 2007 30 234 238 17259487
   PubMed Web of Science ®Google Scholar
• Brand JS Wareham NJ Dowsett M Associations of endogenous testosterone and SHBG with glycated haemoglobin in middle-aged and older men Clin Endocrinol (Oxf) 2011 74 572 578 21158891
   PubMed Web of Science ®Google Scholar
• Grossmann M Thomas MC Panagiotopoulos S Low testosterone levels are common and associated with insulin resistance in men with diabetes J Clin Endocrinol Metab 2008 93 1834 1840 18319314
   PubMed Web of Science ®Google Scholar
• Mulligan T Frick MF Zuraw QC Stemhagen A McWhirter C Prevalence of hypogonadism in males aged at least 45 years: the HIM study Int J Clin Pract 2006 60 762 769 16846397
   PubMed Web of Science ®Google Scholar
• Haffner SM Shaten J Stern MP Smith GD Kuller L Low levels of sex hormone-binding globulin and testosterone predict the development of non-insulin-dependent diabetes mellitus in men. MRFIT Research Group. Multiple Risk Factor Intervention Trial Am J Epidemiol 1996 143 889 897 8610702
   PubMed Web of Science ®Google Scholar
• Stellato RK Feldman HA Hamdy O Horton ES McKinlay JB Testosterone, sex hormone-binding globulin, and the development of type 2 diabetes in middle-aged men: prospective results from the Massachusetts Male Aging Study Diabetes Care 2000 23 490 494 10857940
   PubMed Web of Science ®Google Scholar
• Oh JY Barrett-Connor E Wedick NM Wingard DL Endogenous sex hormones and the development of type 2 diabetes in older men and women: the Rancho Bernardo Study Diabetes Care 2002 25 55 60 11772901
   PubMed Web of Science ®Google Scholar
• Laaksonen DE Niskanen L Punnonen K Testosterone and sex hormone-binding globulin predict the metabolic syndrome and diabetes in middle-aged men Diabetes Care 2004 27 1036 1041 15111517
   PubMed Web of Science ®Google Scholar
• Vikan T Schirmer H Njølstad I Svartberg J Low testosterone and sex hormone-binding globulin levels and high estradiol levels are independent predictors of type 2 diabetes in men Eur J Endocrinol 2010 162 747 754 20061333
   PubMed Web of Science ®Google Scholar
• Lakshman KM Bhasin S Araujo AB Sex hormone-binding globulin as an independent predictor of incident type 2 diabetes mellitus in men J Gerontol A Biol Sci Med Sci 2010 65 503 509 20106959
   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 91 843 850 16394089
   PubMed Web of Science ®Google Scholar
• Ding EL Song Y Manson JE Sex hormone-binding globulin and risk of type 2 diabetes in women and men N Engl J Med 2009 361 1152 1163 19657112
   PubMed Web of Science ®Google Scholar
• Perry JR Weedon MN Langenberg C Genetic evidence that raised sex hormone binding globulin (SHBG) levels reduce the risk of type 2 diabetes Hum Mol Genet 2010 19 535 544 19933169
   PubMed Web of Science ®Google Scholar
• Yeap BB Chubb SA Hyde Z Lower serum testosterone is independently associated with insulin resistance in non-diabetic older men: the Health in Men Study Eur J Endocrinol 2009 161 591 598 19661128
   PubMed Web of Science ®Google Scholar
• Pitteloud N Mootha VK Dwyer AA Relationship between testosterone levels, insulin sensitivity, and mitochondrial function in men Diabetes Care 2005 28 1636 1642 15983313
   PubMed Web of Science ®Google Scholar
• Tsai EC Matsumoto AM Fujimoto WY Boyko EJ Association of bioavailable, free, and total testosterone with insulin resistance: influence of sex hormone-binding globulin and body fat Diabetes Care 2004 27 861 868 15047639
   PubMed Web of Science ®Google Scholar
• Zumoff B Strain GW Miller LK Plasma free and non sex-hormone-binding-globulin bound testosterone are decreased in obese men in proportion to their degree of obesity J Clin Endocrinol Metab 1990 71 929 931 2401718
   PubMed Web of Science ®Google Scholar
• Haffner SM Valdez RA Stern MP Katz MS Obesity, body fat distribution and sex hormones in men Int J Obes 1993 17 643 649
   PubMed Web of Science ®Google Scholar
• Guzik TJ Mangalat D Korbut R Adipocytokines: novel link between inflammation and vascular function? J Physiol Pharmacol 2006 57 505 528 17229978
   PubMed Web of Science ®Google Scholar
• Grossmann M Gianatti EJ Zajac JD Testosterone and type 2 diabetes Curr Opin Endocrinol Diabetes Obes 2010 17 247 256 20418720
   PubMedGoogle Scholar
• Traish AM Saad F Guay A The dark side of testosterone deficiency. Type 2 diabetes and insulin resistance J Androl 2009 30 23 32 18772488
   PubMedGoogle Scholar
• Stanworth RD Jones TH Testosterone in obesity, metabolic syndrome and type 2 diabetes Front Horm Res 2009 37 74 90 19011290
   PubMed Web of Science ®Google Scholar
• Zitzmann M Testosterone deficiency, insulin resistance and the metabolic syndrome Nat Rev Endocrinol 2009 5 673 681 19859074
   PubMed Web of Science ®Google Scholar
• Cohen PG The hypogonadal-obesity cycle Med Hypotheses 1999 52 49 51 10342671
   PubMed Web of Science ®Google Scholar
• Finn PD Cunningham MJ Pau KY Spies HG Clifton DK Steiner RA The stimulatory effect of leptin on the neuroendocrine reproductive axis of the monkey Endocrinology 1998 139 4652 4662 9794477
   PubMed Web of Science ®Google Scholar
• Isidori AM Caprio M Stroll F Leptin and androgens in male obesity: evidence for leptin contribution to reduced androgen levels J Clin Endocrinol Metab 1999 84 3673 3680 10523013
   PubMed Web of Science ®Google Scholar
• Pitteloud N Hardin M Dwyer AA Increasing insulin resistance is associated with a decrease in Leydig cell testosterone secretion in men J Clin Endocrinol Metab 2005 90 2636 2641 15713702
   PubMed Web of Science ®Google Scholar
• Stanworth RD Kapoor D Channer KS Jones TH Androgen receptor CAG repeat polymorphism is associated with serum testosterone levels, obesity and serum leptin in men with type 2 diabetes Eur J Endocrinol 2008 159 739 746 18805913
   PubMed Web of Science ®Google Scholar
• Lin HY Xu Q Yeh S Wang RS Sparks JD Chang C Insulin and leptin resistance with hyperleptinemia in mice lacking androgen receptor Diabetes 2005 54 1717 1725 15919793
   PubMed Web of Science ®Google Scholar
• Unger RH Orci L Lipotoxic diseases of nonadipose tissues in obesity Int J Obes Relat Metab Disord 2000 24 Suppl 4 S28 S32 11126236
   PubMed Web of Science ®Google Scholar
• Kalinchenko SY Tishova YA Mskhalaya GJ Gooren LJ Giltay EJ Saad F 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 (Oxf) 2010 73 602 612 20718771
   PubMed Web of Science ®Google Scholar
• Kapoor D Goodwin E Channer KS Jones TH Testosterone replacement therapy improves insulin resistance, glycaemic control, visceral adiposity and hypercholesterolaemia in hypogonadal men with type 2 diabetes Eur J Endocrinol 2006 154 899 906 16728551
   PubMed Web of Science ®Google Scholar
• Heufelder AE Saad F Bunck MC Gooren L Fifty-two-week treatment with diet and exercise plus transdermal testosterone reverses the metabolic syndrome and improves glycemic control in men with newly diagnosed type 2 diabetes and subnormal plasma testosterone J Androl 2009 30 726 733 19578132
   PubMed Web of Science ®Google Scholar
• Jones TH Arver S Behre HM Testosterone replacement in hypogonadal men with type 2 diabetes and/or metabolic syndrome (the TIMES2 Study) Diabetes Care 2011 34 828 837 21386088
   PubMed Web of Science ®Google Scholar
• Muraleedharan V Marsh H Kapoor D Channer KS Jones TH Testosterone deficiency is associated with increased risk of mortality and testosterone replacement improves survival in men with type 2 diabetes Eur J Endocrinol 2013 169 725 733 23999642
   PubMed Web of Science ®Google Scholar
• Gopal RA Bothra N Acharya SV Treatment of hypogonadism with testosterone in patients with type 2 diabetes mellitus Endocr Pract 2010 16 570 576 20150021
   PubMed Web of Science ®Google Scholar
• Rebuffé-Scrive M Mårin P Björntorp P Effect of testosterone on abdominal adipose tissue in men Int J Obes 1991 15 791 795 1778664
   PubMed Web of Science ®Google Scholar
• Finkle WD Greenland S Ridgeway GK Increased risk of non-fatal myocardial infarction following testosterone therapy prescription in men PLoS One 2014 9 e85805 24489673
   PubMed Web of Science ®Google Scholar
• Vigen R O’Donnell CI Barón AE Association of testosterone therapy with mortality, myocardial infarction, and stroke in men with low testosterone levels JAMA 2013 310 1829 1836 24193080
   PubMed Web of Science ®Google Scholar
• Calof OM Singh AB Lee ML Adverse events associated with testosterone replacement in middle-aged and older men: a meta-analysis of randomized, placebo-controlled trials J Gerontol 2005 60 1451 1457
   Google Scholar
• Fernández-Balsells MM Murad MH Lane M Adverse effects of testosterone therapy in adult men: a systemic review and meta-analysis J Clin Endocrinol Metab 2010 95 2560 2575 20525906
   PubMed Web of Science ®Google Scholar
• Mathur A Malkin C Saeed B Muthusamy R Jones TH Channer K Long-term benefits of testosterone replacement therapy on angina threshold and atheroma in men Eur J Endocrinol 2009 161 443 449 19542238
   PubMed Web of Science ®Google Scholar
• Caminiti G Volterrani M Iellamo F Effect of long-acting testosterone treatment on functional exercise capacity, skeletal muscle performance, insulin resistance, and baroreflex sensitivity in elderly patients with chronic heart failure: a double-blind, placebo-controlled, randomized study J Am Coll Cardiol 2009 54 919 927 19712802
   PubMed Web of Science ®Google Scholar