DOI: http://dx.doi.org/10.18203/2320-6012.ijrms20162298

Prevalence and predictors for low total testosterone levels among male type 2 diabetic patients: an Egyptian experience

Mohamed M. Aboelnaga, H. Elshahawy

Abstract


Background: Diabetes mellitus (DM) affects an estimated 285 million people worldwide. This number is expected to reach 438 million by the year 2030. The aim of this study was to determine the prevalence of male hypogonadism among Egyptian patients with type 2 diabetes and to identify the risk factors may be associated with low serum testosterone concentrations in men with type 2 diabetes.

Methods: 140 male patients with type 2 diabetes were recruited in this cross-sectional study.  This study WAS conducted from January 2012 to January 2016 in the endocrinology and metabolism unit, Mansoura University, Egypt.

Results: We found 48 (34.2%)  patients with hypogonadism  (defined as  TT ≤300 ng/dl) among 140 male patients with type 2 diabetes. 7 out of   48 (14.5%) patients with TT ≤300 ng/dl had high abnormal gondotrophins hormones levels while 41  patients out of   48 (85.5%) had normal gondotrophins hormones levels. We found BMI, WC, Hba1c,  UACR, retinopathy ratio, nephropathy ratio, smoker ratio and patient on insulin therapy ratio were increased in the low TT group with statistically significance, but non statistically significant difference in  age, diabetic duration, FSH, LH, Prolactin and  lipid profile. In this study by using Pearson correlation, we found a statistically significant correlation between TT levels with   BMI, WC, FSH, LH, Hba1c, and UACR (P value<0.05). Also by using stepwise multiple regression analysis, we found BMI, WC, LH, Hba1c, and UACR were statistically significant predictors of TT levels. In logistic regression analysis, we found Hba1c, UACR, and WC were statistically significant risk factors for MHG.  

Conclusions: Visceral obesity, higher Hba1c, and degree of albuminuria are independent risk factors for hypogonadism in Egyptian male patients with type 2 diabetes.

 


Keywords


Type 2 DM, Male hypogonadism, Total testosterone, Egyptian

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References


International Diabetes Federation. IDF Diabetes Atlas. Epidemiology and Morbidity. International Diabetes Federation. Available from: http://www.idf.org/. Accessed on 2016 March 1.

Basaria S. Male hypogonadism. The Lancet. 2014;383(9924):1250-63.

Dandona P, Rosenberg MT. A practical guide to male hypogonadism in the primary care setting. Int J Clin Pract. 2010;64:682-96.

Aydogan U, Aydogdu A, Akbulut H, Sonmez A, Yuksel S, Basaran Y, et al. Evaluation of the isokinetic muscle strength, balance and anaerobic performance in patients with young male hypogonadism. Endocrine Journal. 2012;59(4):321-7.

Aydogan U, Aydogdu A, Akbulut H, Sonmez A, Yuksel S, Basaran Y, et al. Increased frequency of anxiety, depression, quality of life and sexual life in young hypogonadotropic hypogonadal males and impacts of testosterone replacement therapy on these conditions.EndocrineJournal.2012;59(12):1099-105.

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;91:843-50.

Sorisky A. Late-onset hypogonadism in middle-aged and elderly men. The New England Journal of Medicine. 2010;363(19):1867-8.

Al Hayek AA, Khader YS, Jafal S, Khawaja N, Robert AA, Ajlouni K. Prevalence of low testosterone levels in men with type 2 diabetes mellitus: a cross-sectional study. J Family Community Med. 2013;20(3):179-86.

Grossmann M, Thomas MC, Panagiotopoulos S, Sharpe K, Macisaac RJ, Clarke S, et al. Low testosterone levels are common and associated with insulin resistance in men with diabetes. J Clin Endocrinol Metab. 2008;93:1834-40.

Kapoor D, Aldred H, Clark S, Channer KS, Jones TH. Clinical and biochemical assessment of hypogonadism in men with type 2 diabetes: Correlations with bioavailable testosterone and visceral adiposity. Diabetes Care. 2007;30:911-7.

Rhoden EL, Ribeiro EP, Teloken C, Souto CA. Diabetes mellitus is associated with subnormal serum levels of free testosterone in men. BJU Int. 2005;96:867-70.

Ghazi S, Zohdy W, Elkhiat Y, Shamloul R. Serum testosterone levels in diabetic men with and without erectile dysfunction. Andrologia. 2012;44:373-80.

Saboor Aftab SA, Kumar S, Barber TM. The role of obesity and type 2 diabetes mellitus in the development of male obesity-associated secondary hypogonadism. Clin Endocrinol (Oxf). 2013;78:330-7.

Basu AK, Singhania P, Bandyopadhyay R, Biswas K, Santra S, Singh S, et al. Late onset hypogonadism in type 2 diabetic and nondiabetic male: a comparative study. J Indian Med Assoc. 2012;110(8):573-5.

Costanzo PR, Suárez SM, Scaglia HE, Zylbersztein C, Litwak LE, Knoblovits P. “Evaluation of the hypothalamic-pituitary-gonadal axis in eugonadal men with type 2 diabetes mellitus,” Andrology. 2014; 2(1):117-24.

Langer C, Gansz B, Goepfert C, Engel T, Uehara Y, von Dehn G, et al. Testosterone up-regulates scavenger receptor BI and stimulates cholesterol efflux from macrophages. Biochemical and Biophysical Research Communications. 2002;296(5):1051-7.

Zheng R, Cao L, Cao W, Chu X, Hu Y, Zheng H, et al. C Risk Factors for Hypogonadism in Male Patients with Type 2 Diabetes J Diabetes Res. 2016;2016:5162167.

Boddi V, Barbaro V, McNieven P, Maggi M, Rotella CM. Present and future association between obesity and hypogonadism in Italian male. Archivio Italiano di Urologia e Andrologia. 2014;86(1):26-32.

Tripathy D, Dhindsa S, Garg R, Khaishagi A, Syed T, Dandona P. Hypogonadotropic hypogonadism in erectile dysfunction associated with type 2 diabetes mellitus: A common defect? Metab Syndr Relat Disord. 2003;1:75-80.

Pitteloud N, Dwyer AA, DeCruz S. The relative role of gonadal sex steroids and gonadotropin-releasing hormone pulse frequency in the regulation of follicle-stimulating hormone secretion in men. The Journal of Clinical Endocrinology & Metabolism. 2008;93(7):2686-92.

Kalyani RR. Androgen deficiency, diabetes, and the metabolic syndrome in men. Curr Opin Endocrinol Diabetes Obes. 2007;14:226-34.

Walker BR. Steroid metabolism in metabolic syndrome X. Best Pract Res Clin Endocrinol Metab. 2001;15:111-22.

Kapoor D, Aldred H, Clark S, Channer KS, Jones TH. Clinical and biochemical assessment of hypogonadism in men with type 2 diabetes: Correlations with bioavailable testosterone and visceral adiposity. Diabetes Care. 2007;30:911-7.

Grossmann M, Thomas MC, Panagiotopoulos S, Sharpe K, Macisaac RJ, Clarke S, et al. Low testosterone levels are common and associated with insulin resistance in men with diabetes. J Clin Endocrinol Metab. 2008;93:1834-40.

Dandona P, Dhindsa S, Chaudhuri A, Bhatia V, Topiwala S. Hypogonadotrophic hypogonadism in type 2 diabetes. Aging Male. 2008;11:107-17.

Fukui M, Tanaka M, Hasegawa G, Yoshikawa T, Nakamura N. Association between serum bioavailable testosterone concentration and the ratio of glycated albumin to glycated hemoglobin in men with type 2 diabetes. Diabetes Care. 2008;31:397-401.

Holt SK, Lopushnyan N, Hotaling J, Sarma AV, Dunn RL, Cleary PA, et al. Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications Research Group Prevalence of low testosterone and predisposing risk factors in men with type 1 diabetes mellitus: findings from the DCCT/EDIC J Clin Endocrinol Metab. 2014;99(9):E1655-60.

Chernyshova TE, Sitnikov VA, Martirosov IuK. The effect of diabetic nephropathy on the function of the hypophyseal-gonadal system in men Urol Nefrol (Mosk). 1991;(1):54-7.

Ganesh HK, Vijaya Sarathi HA, George J, Shivane VK, Bandgar T, Menon PS, et al. Prevalence of hypogonadism in patients with type 2 diabetes mellitus in an Asian Indian study group. Endocr Pract. 2009;15(6):513-20.

Hasan MJ, Muqueet A, Sharmeen A, Hoque MR. Prevalence of microalbuminuria in relation to glycemic control in type-2 diabetic patients in Mymensingh. Mymensingh Med J. 2015;24(1):18-24.

Seidman SN. The aging male: androgens, erectile dysfunction, and depression. J Clin Psychiatry. 2003;64 Suppl 10:31-7.

Ganesh HK, Vijaya Sarathi HA, George J, Shivane VK, Bandgar T, Menon PS, et al. Prevalence of hypogonadism in patients with type 2 diabetes mellitus in an Asian Indian study group. Endocr Pract.2009;15:513-20.

Ganesh HK, Vijaya Sarathi HA, George J, Shivane VK, Bandgar T, Menon PS, et al. Prevalence of hypogonadism in patients with type 2 diabetes mellitus in an Asian Indian study group. Endocr Pract. 2009;15:513-20.

Fukui M, Soh J, Tanaka M, Kitagawa Y, Hasegawa G, Yoshikawa T, et al. Low serum testosterone concentration in middle-aged men with type 2 diabetes. Endocr J. 2007;54:871-7.

Diaz-Arjonilla M, Schwarcz M, Swerdloff RS, Wang C. Obesity, low testosterone levels and erectile dysfunction. Int J Impot Res. 2009;21:89-98.

Corona G, Mannucci E, Petrone L, Balercia G, Paggi F, Fisher AD, et al. NCEP-ATPIII-defined metabolic syndrome, type 2 diabetes mellitus, and prevalence of hypogonadism in male patients with sexual dysfunction. J Sex Med. 2007;4:1038-45.

Field AE, Colditz GA, Willett WC, Longcope C, McKinlay JB. The relation of smoking, age, relative weight, and dietary intake to serum adrenal steroids, sex hormones, and sex hormone-binding globulin in middle-aged men. J Clin Endocrinol Metab 1994;79:1310-6.

Trummer H, Habermann H, Haas J, Pummer K. The impact of cigarette smoking on human semen parameters and hormones. Hum Reprod. 2002;17:1554-9.

Svartberg J, Midtby M, Bonaa KH, Sundsfjord J, Joakimsen RM, Jorde R. The associations of age, lifestyle factors and chronic disease with testosterone in men: the Tromso Study. Eur J Endocrinol. 2003;149:145-52.

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.

Sofikitis N, Miyagawa I, Dimitriadis D, Zavos P, Sikka S, Hellstrom W. Effects of smoking on testicular function, semen quality, and sperm .fertilizing capacity. J Urol. 1995;154:1030-4.

Zmuda JM, Cauley JA, Kriska A, Glynn NW, Gutai JP, Kuller LH Longitudinal relation between endogenous testosterone and cardiovascular disease risk factors in middle-aged men. A 13-year follow-up of former Multiple Risk Factor Intervention Trial participants. Am J Epidemiol. 1997;146:609-17.

Laaksonen DE, Niskanen L, Punnonen K, Nyyssonen K, Tuomainen TP, Valkonen VP, et al. The metabolic syndrome and smoking in relation to hypogonadism in middle-aged men: A prospective cohort study. J Clin Endocrinol Metab. 2005;90:712-9.

Barbieri RL, Gochberg J, Ryan KJ. Nicotine, cotinine, and anabasine inhibit aromatase in human trophoblast in vitro. J Clin Invest. 1986;7(7):1727-33.

Leder BZ, Rohrer JL, Rubin SD, Gallo J, Longcope C. Effects of aromatase inhibition in elderly men with low or borderline-low serum testosterone levels. J Clin Endocrinol Metab. 2004,89:1174-80.

Yeh J, Barbieri RL, Friedman AJ. Nicotine and cotinine inhibit rat testis androgen biosynthesis in vitro. J Steroid Biochem. 1989;33:627-30.

Ronnemaa T, Ronnemaa EM, Puukka P, Pyorala K, Laakso M. Smoking is independently associated with high plasma insulin levels in nondiabetic men. Diabetes Care. 1996;19:1229-32 .