Hypogonadism in men with type 2 diabetes

Practical Diabetes International

Volumn 24, Issue 5, 2007, Pages 269-277

  Jones, T Hugh ^a,b  

^a BARNSLEY HOSPITAL NHS FOUNDATION TRUST   (United Kingdom)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Atherosclerosis; Cardiovascular risk factors; Erectile dysfunction; Glycaemic control; Hypogonadism; Insulin resistance; Testosterone; Type 2 diabetes

Indexed keywords

ADIPONECTIN; C REACTIVE PROTEIN; GLUCOSE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; INSULIN; INTERLEUKIN 1; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; LEPTIN; LOW DENSITY LIPOPROTEIN CHOLESTEROL; PHOSPHODIESTERASE V INHIBITOR; PLACEBO; SEX HORMONE BINDING GLOBULIN; TESTOSTERONE; TESTOSTERONE UNDECANOATE; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR ALPHA;

ANDROGEN THERAPY; ANTIINFLAMMATORY ACTIVITY; AORTA ATHEROSCLEROSIS; BLOOD GLUCOSE MONITORING; CAROTID ARTERY DISEASE; CHOLESTEROL BLOOD LEVEL; CLINICAL TRIAL; CORONARY ARTERY ATHEROSCLEROSIS; DIABETES CONTROL; DIAGNOSTIC VALUE; DIET THERAPY; DRUG BLOOD LEVEL; DRUG DOSE REDUCTION; DRUG METABOLISM; DRUG RESPONSE; DRUG SAFETY; ERECTILE DYSFUNCTION; EVIDENCE BASED MEDICINE; EXERCISE; HUMAN; HYPERCOAGULABILITY; HYPERGONADOTROPIC HYPOGONADISM; HYPERTENSION; HYPOGONADISM; HYPOGONADOTROPIC HYPOGONADISM; INSULIN RESISTANCE; INSULIN SENSITIVITY; METABOLIC SYNDROME X; MORTALITY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PATHOGENESIS; PREVALENCE; QUALITY OF LIFE; REVIEW; RISK FACTOR; RISK REDUCTION; SKIN ALLERGY; TESTOSTERONE BLOOD LEVEL; WELLBEING;

EID: 34548301443     PISSN: 13578170     EISSN: 1528252X     Source Type: Journal    
DOI: 10.1002/pdi.1117     Document Type: Review

References (69)

1. Bojesen A, Juul S, Gravholt CH, et al. Prenatal and postnatal prevalence of Klinefelter's syndrome: a national registry study. J Clin Endocrinol Metab 2003; 88: 622-628.
2. Bojesen A, Kristensen K, Birkeback NH. The metabolic syndrome is frequent in men with Klinefelter's Syndrome. Diabetes Care 2006; 29: 1591-1598.
3. Nieschlag E, Swerdloff R, Behre HM, et al. Investigation, treatment and monitoring of late-onset hypogonadism in males: ISA, ISSAM and EAU recommendations. J Androl 2006; 27: 135-137.
4. Androgen Deficiency Syndromes in Men Guideline Task Force. Testosterone therapy in adult men with androgen deficiency syndromes: An Endocrine Society clinical practice guideline. J Clin Endocrinol Metab 2006; 91: 1995-2010.
5. Simon D, Preziosi P, Barrett-Connor E, et al. Interrelation between plasma testosterone and plasma insulin in healthy adult men: the Telecom Study. Diabetologia 1992; 35: 173-177.
6. Kapoor D, Aldred H, Clark S, et al. Clinical and biochemical assessment of hypogonadism in men with type 2 diabetes. Correlations with bioavailable testosterone and visceral adiposity. Diabetes Care 2007; 30: 911-917.
7. Stanworth RD, Kapoor D, Channer KS, et al. Use of atorvastatin, but not simvastatin in men with type 2 diabetes is associated with lower total testosterone levels with no effect on bioavailable or free testosterone. Endocrine Abstracts 2007; 14: OC7.7.
8. 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.
9. Morris PD, Malkin CJ, Channer KS, et al. A mathematical comparison of techniques to predict biologically available testosterone in a cohort of 1072 men. Eur J Endocrinol 2004; 151: 241-249.
10. Ando S, Rubens R. Rottiers R. Androgen plasma levels in mate diabetics. J Endocrinol Invest 1984; 7: 21-24.
11. Barrett-Connor E, Khaw KT, Yen SS. Endogenous sex hormones in older men with diabetes mellitus. Am J Epidemiol 1990; 132: 895-901.
12. Barrett-Connor E. Lower endogenous androgen levels and dyslipidemia in men with non-insulin-dependent diabetes mellitus. Ann Intern Med 1992; 117: 807-811.
13. Zietz B, Cuk A, Hugl S, et al. Association of increased C-peptide serum levels and testosterone in type 2 diabetes. Eur J Intern Med 2000; 11: 322-328.
14. Andersson B, Marin P, Lissner L, et al. Testosterone concentrations in women and men with NIDDM. Diabetes Care 1994; 17: 405-411.
15. Dhindsa S, Prabhakar S, Sethi M, et al. Frequent occurrence of hypogonadotrophic hypogonadism in type 2 diabetes. J Clin Endocrinol Metab 2004; 89: 5462-5468.
16. Stellato RK, Feldman HA, Hamdy O, et al. 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.
17. Haffner SM, Shaten J, Stern MP, et al. Low levels of sex hormone binding globulin and testosterone predict the development of non insulin dependent diabetes mellitus in men. Am J Epidemiol 1996; 143: 889-897.
18. Selvin E, Feinleib M, Zhang L, et al. Androgens and diabetes in men. Results from the Third National Health and Nutrition Examination Survey (NHANES III). Diabetes Care 2007; 30: 234-238.
19. Oh JY, Barrett-Connor E, Wedick NM, et al. 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.
20. 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.
21. 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 non-obese men. J Clin Endocrinol Metab 2006; 91: 843-850.
22. Keating NL, O'Malley J, Smith MR. Diabetes and cardiovascular disease during androgen deprivation therapy for prostate cancer. J Clin Oncol 2006; 24: 4448-4456.
23. Smith JC, Bennett S, Evans LM, et al. The effects of induced hypogonadism on arterial stiffness, body composition and metabolic parameters in males with prostate cancer. J Clin Endocrinol Metab 2001; 86: 4261-4267.
24. Basaria S, Muller DC, Carducci MA, et al. Hyperglycemia and insulin resistance in men with prostate carcinoma who receive androgen-deprivation therapy. Cancer 2006; 106: 581-588.
25. Marin P, Krotkiewski M, Bjorntorp P. Androgen treatment of middle-aged, obese men: effects on metabolism, muscle and adipose tissues. Eur J Med 1992; 1: 329-336.
26. Kapoor D, Malkin CJ, Channer KS, et al. Androgens, insulin resistance and vascular disease in men. Clin Endocrinol (Oxf) 2005; 63: 239-250.
27. Kapoor D, Goodwin E, Channer KS, et al. Testosterone replacement therapy improves insulin resistance, glycaemic control, visceral adiposity and hypercholes-terolemia in hypogonadal men with Type 2 diabetes. Eur J Endocrinol 2006; 154: 899-906.
28. Boyanov MA, Boneva Z, Christov VG. Testosterone supplementation in men with type 2 diabetes, visceral obesity and partial androgen deficiency. Aging Male 2003; 6: 1-7.
29. Yusuf S, Hawken S, Ounpuu S, et al. Effect of potentially modifiable risk factors associated with myocardial infarction in 52 countries (the INTERHEART study): case-control study. Lancet 2004; 364: 937-952.
30. Couillard C, Gagnon J, Bergeron J, et al. Contribution of body fatness and adipose tissue distribution to the age variation in plasma steroid hormone concentrations in men: the HERITAGE Family Study. J Clin Endocrinol Metab 2000; 85: 1026-1031.
31. Haffner SM, Valdez RA, Stern MP, et al. Obesity, body fat distribution and sex hormones in men. Int J Obesity 1993; 17: 643-649.
32. Strain GW, Zumoff B, Miller LK, et al. Effect of massive weight loss on hypothalamic-pituitary-gonadal function in obese men. J Clin Endocrinol Metab 1988; 66: 1019-1023.
33. Wang C, Swerdloff RS, Iranmanesh A, et al. Transdermal testosterone gel improves sexual function, mood, muscle strength, and body composition parameters in hypogonadal men. J Clin Endocrinol Metab 2000; 85: 2839-2853.
34. Cohen PG. The hypogonadal-obesity cycle. Med Hypotheses 1999; 52: 49-51.
35. Marin P, Oden B, Bjorntorp P. Assimilation and mobilization of triglycerides in subcutaneous abdominal and femoral adipose tissue in vivo in men: effects of androgens. J Clin Endocrinol Metab 1995; 80: 239-243.
36. Mantzoros CS. The role of leptin in human obesity and disease: a review of current evidence. Ann Intern Med 1999; 130: 671-680.
37. Isidori AM, Caprio M, Strollo F, et al. Leptin and androgens in male obesity: evidence for leptin contribution to reduced androgen levels. J Clin Endocrinol Metab 1999; 84: 3673-3680.
38. Jones RD, Nettleship JE, Kapoor D, et al. Testosterone and atherosclerosis in aging men. Purported association and clinical implication. Am J Cardiovasc Drugs 2005; 5: 141-154.
39. Whitsel EA, Boyko EJ, Matsumoto AM, et al. Intramuscular testosterone esters and plasma lipids in hypogonadal men: a meta-analysis. Am J Med 2001; 111: 261-269.
40. 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.
41. Stanworth RD, Kapoor D, Channer KS, et al. Testosterone levels correlate positively with HDL cholesterol levels in men with type 2 diabetes. Endocrine Abstracts 2007; 14: P628.
42. Malkin CJ, Pugh PJ, Kapoor D, et al. The effect of testosterone replacement on endogenous inflammatory cytokines and lipid profiles in hypogonadal men. J Clin Endocrinol Metab 2004; 89: 3313-3318.
43. Smith AM, English KM, Malkin CJ, et al. Testosterone does not adversely affect fibrinogen or tissue plasminogen activator (tPA) and plasminogen activator inhibitor-1 (PAI-1) levels in 46 men with chronic stable angina. Eur J Endocrinol 2005; 152: 285-291.
44. Corrales JJ, Almeida M, Burgo R, et al. Androgen-replacement therapy depresses the ex vivo production of inflammatory cytokines by circulating antigen-presenting cells in aging type-2 diabetic men with partial androgen deficiency. J Endocrinol 2006; 189: 595-604.
45. Kapoor D, Clarke S, Stanworth RD, et al. The effect of testosterone replacement therapy on adipocytokines and C-reactive protein in hypogonadal men with type 2 diabetes. Eur J Endocrinol 2007; 156: 595-602.
46. Fukui M, Kitagawa Y, Nakamura N, et al. Association between serum testosterone concentration and carotid atherosclerosis in men with Type 2 diabetes. Diabetes Care 2003; 26: 1869-1873.
47. Svartberg J, Von Muhlen D, Mathiesen E, et al. Low testosterone levels are associated with carotid atherosclerosis in men. J Intern Med 2006; 259: 576-582.
48. Hak AE, Witteman JCM, De Jong FH, et al. Low levels of endogenous androgens increase the risk of atherosclerosis in elderly men: the Rotterdam Study. J Clin Endocrinol Metab 2002; 87: 3632-3639.
49. De Pergola G, Pannacciulli N, Ciccone M, et al. Free testosterone plasma levels are negatively associated with the intima-media thickness of the common carotid artery in overweight and obese glucose-tolerant young adult men. Int J Obes Relat Metab Disord 2003; 27: 803-807.
50. Muller M, Van Den Beld AW, Bots ML, et al. Endogenous sex hormones and progression of carotid atherosclerosis in elderly men. Circulation 2004; 109: 2074-2079.
51. English KM, Mandour O, Steeds RP, et al. Men with coronary artery disease have lower levels of androgens than men with normal coronary angiograms. Eur Heart J 2000; 21: 890-894.
52. Edwards E, Hamilton J, Duntley S. Testosterone propionate as a therapeutic agent in patients with organic disease of peripheral vessels. N Engl J Med 1939; 220: 865-869.
53. Hamm L. Testosterone propionate in the treatment of angina. J Clin Endocrinol 1942; 2: 325-328.
54. English KM, Steeds RP, Jones TH, et al. Low dose transdermal testosterone therapy improves angina threshold in men with chronic stable angina. Circulation 2000; 102: 1906-1911.
55. Webb CM, McNeill JG, Hayward CS, et al. Effects of testosterone on coronary vasomotor regulation in men with coronary heart disease. Circulation 1999; 100: 1690-1696.
56. Webb CM, Adamson DL, de Zeigler D, et al. Effect of acute testosterone on myocardial ischaemia in men with coronary artery disease. Am J Cardiol 1999; 83: 437-439.
57. Jones RD, Pugh PJ, Jones TH, et al. The vasodilatory action of testosterone: a potassium channel opening or calcium antagonistic action? Br J Pharmarol 2003; 138: 733-744.
58. 2+ channels. Biochem Biophys Res Comm 2004; 318: 503-506.
59. 2+ channels in A7r5 cells by physiological levels of testosterone. Endocrinology 2006; 147: 2675-2680.
60. Pugh PJ, Jones TH, Channer KS. Acute haemodynamic effects of testosterone in men with chronic heart failure. Eur Heart J 2003; 24: 909-915.
61. Pugh PJ, Jones RD, West JN, et al. Testosterone treatment for men with chronic heart failure. Heart 2004; 90: 446-447.
62. Malkin CJ, Pugh PJ, West JN, et al. Testosterone therapy in men with moderate heart failure: a double-blind randomized placebo controlled trial. Eur Heart J 2006; 27: 57-64.
63. Kapoor D, Clarke S, Channer KS, et al. Erectile dysfunction is associated with low testosterone levels and visceral adiposity in men with type 2 diabetes. Int J Androl 2007; (OnlineEarly Articles). doi:10.1111/j.1365-2605.2007.00744.x
64. Kalinchenko SY, Kozlov GI, Gontcharov NP, et al. Oral testosterone undeconoate reverses erectile dysfunction associated with diabetes mellitus in patients failing with sildenafil citrate therapy alone. Aging Male 2003; 6: 94-99.
65. Shabsigh R, Kaufman J, Steidle J, et al. Randomized study of testosterone gel as adjunctive therapy to sildenafil in hypogonadal men with erectile dysfunction who do not respond to sildenafil alone. J Urol 2004; 172: 658-663.
66. Aversa A, Isidori AM, Spera G, et al. Androgens improve cavernous vasodilation and response to sildenafil in patients with erectile dysfunction. Clin Endocrinol (Oxf) 2003; 58: 632-638.
67. Marks LS, Mazer NA, Mostaghel E, et al. Effect of testosterone replacement therapy on prostate tissue in men with late-onset hypogonadism. A randomized controlled trial. JAMA 2006; 296: 2351-2361.
68. Rhoden EL, Morgentaler A. Risks of testosterone-replacement therapy and recommendations for monitoring. N Engl J Med 2004; 350: 482-492.
69. Shores MM, Matsumoto AM, Sloan KL, et al. Low serum testosterone and mortality in male veterans. Arch Intern Med 2006; 166: 1660-1665.