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ABSTRACT
Introduction. Diabetes is a chronic metabolic disease that can lead to severe hormonal disorders such as hypogonadism. The objective of our study was to better define the biological risk factors of infertility related to hypogonadism in type 2 diabetics. Method. This was a retrospective descriptive and analytical cross-sectional study conducted at the Mali Hospital between January 2019 to August 2020. The markers being biologically monitored were: Testosteronemia, gonadotropins, prolactinemia, glycemia, Glycated hemoglobin A1c. Results. This study included 55 patients with type 2 diabetes. The age group between 51-70 years was the most represented with 92.73% of the population, the young subjects were little represented with 20%. We found overweight and grade 1 obesity respectively in 29.09 and 5.45% of the diabetic patients in our study. Hyperglycemia and glycated hyperhemoglobin A1c were found in 92.73% and 78.18% of diabetic patients with significant differences P= 0.02 and P = 0.001 respectively. Hypotestosteronemia of 58.18% was more marked in patients with decreased sexual desire with a significant difference P = 0.02. A prevalence of biological hypogonadism was found in 65.45% of type 2 diabetic patients but the statistical difference was not significant P = 0.46. Conclusion. A high prevalence of hypogonadism was found in diabetic patients. Diabetes through its deleterious action on the blood vessel wall through oxidative stress and insulin resistance could promote or accelerate the development of hypogonadism.
RÉSUMÉ
Introduction. Le diabète est une maladie métabolique chronique pouvant conduire à des troubles hormonaux sévères comme l’hypogonadisme. Objectif. Définir les facteurs de risque biologiques d'infertilité liés à l'hypogonadisme chez les diabétiques de type 2. Méthodes. C’était 'une étude rétrospective descriptive et analytique menée à l'hôpital du Mali entre janvier 2019 et août 2020. Les marqueurs suivis biologiquement étaient : La testostéronémie, les gonadotrophines, la prolactinémie, la glycémie, l'hémoglobine glyquée A1c. Résultats. Cette étude a inclus 55 patients diabétiques de type 2. La tranche d'âge entre 51-70 ans était la plus représentée avec 92,73% de la population, les sujets jeunes étaient peu représentés avec 20%. Nous avons retrouvé un surpoids chez 29,09 % des sujets et une obésité de grade 1 chez 5,45% des patients diabétiques. L'hyperglycémie et l’hyperhémoglobine glyquée A1c ont été retrouvées chez 92,73% et 78,18% des patients diabétiques avec des différences significatives P= 0,02 et P = 0,001 respectivement. Une hypotestostéronémie de 58,18% était plus marquée chez les patients présentant une diminution du désir sexuel avec une différence significative P = 0,02. Une prévalence d'hypogonadisme biologique a été retrouvée chez 65,45% des patients diabétiques de type 2 mais la différence statistique n'était pas significative P = 0,46. Conclusion. Une prévalence élevée d'hypogonadisme a été trouvée chez les patients diabétiques. Le diabète, par son action délétère sur la paroi des vaisseaux sanguins à travers le stress oxydatif et la résistance à l'insuline, pourrait favoriser ou accélérer le développement de l'hypogonadisme.
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References
- WHO, Organization WH. Preventing Chronic Diseases: A Vital Investment. World Health Organization; 2005. 199 p.
- Maire B, Lioret S, Gartner A, Delpeuch F. [Nutritional transition and non-communicable diet-related chronic diseases in developing countries]. Sante. 2002;12(1):45‑55.
- Update of mortality attributable to diabetes for the IDF Diabetes Atlas: Estimates for the year 2013. Diabetes Res Clin Pract. 2015 ;109(3):461-5.
- Sy S, Samake M, Sy D, Coulibaly M, Diallo D, Yattara H, et al. Prevalence des Micro et Macroalbuminuries chez les Diabetiques de Type 2 au Centre Hospitalier Universitaire du Point-G à Bamako. HEALTH SCIENCES AND DISEASE. 2020;21(3).
- Beran D, Yudkin JS, de Courten M. Access to Care for Patients With Insulin-Requiring Diabetes in Developing Countries. Diabetes Care. 1 sept 2005;28(9): 2136‑40.
- Bhasin S, Cunningham GR, Hayes FJ, Matsumoto AM, Snyder PJ, Swerdloff RS, et al. Testosterone Therapy in Men with Androgen Deficiency Syndromes: An Endocrine Society Clinical Practice Guideline. The Journal of Clinical Endocrinology & Metabolism. juin 2010;95(6):2536‑59.
- Boehm U, Bouloux PM, Dattani MT, de Roux N, Dodé C, Dunkel L, et al. European Consensus Statement on congenital hypogonadotropic hypogonadism—pathogenesis, diagnosis and treatment. Nat Rev Endocrinol. 2015;11(9):547‑64.
- Bouvattier C, Maione L, Bouligand J, Dodé C, Guiochon-Mantel A, Young J. Neonatal gonadotropin therapy in male congenital hypogonadotropic hypogonadism. Nat Rev Endocrinol. mars 2012;8(3):172‑82.
- Giton F, Trabado S, Maione L, Sarfati J, Le Bouc Y, Brailly-Tabard S, et al. Sex Steroids, Precursors, and Metabolite Deficiencies in Men With Isolated Hypogonadotropic Hypogonadism and Panhypopituitarism: A GCMS-Based Comparative Study. The Journal of Clinical Endocrinology & Metabolism. 1 févr 2015;100(2):E292‑6.
- Young J. Approach to the Male Patient with Congenital Hypogonadotropic Hypogonadism. The Journal of Clinical Endocrinology & Metabolism. 2012;97(3):707‑18.
- Dhindsa S, Prabhakar S, Sethi M, Bandyopadhyay A, Chaudhuri A, Dandona P. Frequent Occurrence of Hypogonadotropic Hypogonadism in Type 2 Diabetes. The Journal of Clinical Endocrinology & Metabolism. nov 2004;89(11):5462‑8.
- Kapoor D, Aldred H, Clark S, Channer KS, Jones TH. Clinical and Biochemical Assessment of Hypogonadism in Men With Type 2 Diabetes. Diabetes Care. 1 avr 2007;30(4):911‑7.
- Asare-Anane H, Ofori E, Agyemang Y, Oppong S, Tagoe E, Bani S, et al. Obesity and Testosterone Levels in Ghanaian Men With Type 2 Diabetes. Clinical Diabetes. 1 avr 2014;32(2):61‑5.
- 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. sept 2013;20(3):179‑86.
- Ugwu TE, Ikem RT, Kolawole BA, Ezeani IU. Clinicopathologic assessment of hypogonadism in men with type 2 diabetes mellitus. Indian J Endocrinol Metab. 2016;20(5):667‑73.
- Corona G, Mannucci E, Petrone L, Ricca V, Balercia G, Mansani R, et al. Association of hypogonadism and type II diabetes in men attending an outpatient erectile dysfunction clinic. Int J Impot Res. mars 2006;18(2):190‑7.
- Dandona P, Dhindsa S. Update: Hypogonadotropic Hypogonadism in Type 2 Diabetes and Obesity. The Journal of Clinical Endocrinology & Metabolism. 2011;96(9):2643‑51.
- Dhindsa S, Miller MG, McWhirter CL, Mager DE, Ghanim H, Chaudhuri A, et al. Testosterone Concentrations in Diabetic and Nondiabetic Obese Men. Diabetes Care. 1 juin 2010;33(6):1186‑92.
- Tomar R, Dhindsa S, Chaudhuri A, Mohanty P, Garg R, Dandona P. Contrasting Testosterone Concentrations in Type 1 and Type 2 Diabetes. Diabetes Care. 1 mai 2006;29(5):1120‑2.
- Zhang LY, He W, Wan JX, Yin QQ, Cheng Z, Chen GM, et al. [Hypogonadism and the quality of life in male patients with type-2 diabetes mellitus]. Zhonghua Nan Ke Xue. déc 2016;22(12):1088‑94.
- Tamler R, Deveney T. Hypogonadism, Erectile Dysfunction, and Type 2 Diabetes Mellitus: What the Clinician Needs to Know. Postgraduate Medicine. 1 nov 2010;122(6):165‑75.
- Feldman HA, Longcope C, Derby CA, Johannes CB, Araujo AB, Coviello AD, 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):589-98.
- Barrett-Connor E. Lower Endogenous Androgen Levels and Dyslipidemia in Men with Non-Insulin-Dependent Diabetes Mellitus. Ann Intern Med. 1992;117(10):807-11.
- Ding B, Li F fei, Zhai X fang, Ye L, Hu Y, Ma J hua. Men with Latent Autoimmune Diabetes and Type 2 Diabetes May Have Different Change Patterns in Free Testosterone. BioMed Research International. 24 juill 2020;2020:e6259437.
- 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. 1 mai 1996;143(9):889‑97.
- Hu TY, Chen YC, Lin P, Shih CK, Bai CH, Yuan KC, et al., Testosterone-Associated Dietary Pattern Predicts Low Testosterone Levels and Hypogonadism. Nutrients. 2018;10(11):1786.
- Allen NE, Key TJ. The effects of diet on circulating sex hormone levels in men. Nutr Res Rev. déc 2000;13(2):159‑84.
- Tajar A, Forti G, O’Neill TW, Lee DM, Silman AJ, Finn JD, et al. Characteristics of Secondary, Primary, and Compensated Hypogonadism in Aging Men: Evidence from the European Male Ageing Study. The Journal of Clinical Endocrinology & Metabolism. 1 avr 2010;95(4):1810‑8.
- Varlamov O. Western-style diet, sex steroids and metabolism.. Biochim Biophys Acta Mol Basis Dis. 2017 May;1863(5):1147-1155
- Russo V, Chen R, Armamento-Villareal R. Hypogonadism, Type-2 Diabetes Mellitus, and Bone Health: A Narrative Review. Front Endocrinol (Lausanne). 2021; 11:607240.
- Fernandez CJ, Chacko EC, Pappachan JM. Male Obesity-related Secondary Hypogonadism – Pathophysiology, Clinical Implications and Management. Eur Endocrinol. août 2019;15(2):83‑90.
- Oueslati I, Ounissi M, Talbi E, Azaiez S, Bacha MM, Abdallah TB. Prevalence and risk factors of hypogonadism in men with chronic renal failure. Tunis Med. 2020 Feb;98(2):138-143.
- Becquey E, Savy M, Danel P, Dabiré HB, Tapsoba S, Martin-Prével Y. Dietary patterns of adults living in Ouagadougou and their association with overweight. Nutrition Journal. 22 mars 2010;9(1):13.
- Rovira-Llopis S, Bañuls C, de Marañon AM, Diaz-Morales N, Jover A, Garzon S, et al. Low testosterone levels are related to oxidative stress, mitochondrial dysfunction and altered subclinical atherosclerotic markers in type 2 diabetic male patients. Free Radic Biol Med. juill 2017;108:155‑62.
- 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. mai 2008;93(5):1834‑40.
- Rao PM, Kelly DM, Jones TH. Testosterone and insulin resistance in the metabolic syndrome and T2DM in men. Nat Rev Endocrinol. août 2013;9(8):479‑93.
- Inzucchi SE, Bergenstal RM, Buse JB, Diamant M, Ferrannini E, Nauck M, et al. Management of Hyperglycemia in Type 2 Diabetes, 2015: A Patient-Centered Approach: Update to a Position Statement of the American Diabetes Association and the European Association for the Study of Diabetes. Diabetes Care. 13 déc 2014;38(1):140‑9.
References
WHO, Organization WH. Preventing Chronic Diseases: A Vital Investment. World Health Organization; 2005. 199 p.
Maire B, Lioret S, Gartner A, Delpeuch F. [Nutritional transition and non-communicable diet-related chronic diseases in developing countries]. Sante. 2002;12(1):45‑55.
Update of mortality attributable to diabetes for the IDF Diabetes Atlas: Estimates for the year 2013. Diabetes Res Clin Pract. 2015 ;109(3):461-5.
Sy S, Samake M, Sy D, Coulibaly M, Diallo D, Yattara H, et al. Prevalence des Micro et Macroalbuminuries chez les Diabetiques de Type 2 au Centre Hospitalier Universitaire du Point-G à Bamako. HEALTH SCIENCES AND DISEASE. 2020;21(3).
Beran D, Yudkin JS, de Courten M. Access to Care for Patients With Insulin-Requiring Diabetes in Developing Countries. Diabetes Care. 1 sept 2005;28(9): 2136‑40.
Bhasin S, Cunningham GR, Hayes FJ, Matsumoto AM, Snyder PJ, Swerdloff RS, et al. Testosterone Therapy in Men with Androgen Deficiency Syndromes: An Endocrine Society Clinical Practice Guideline. The Journal of Clinical Endocrinology & Metabolism. juin 2010;95(6):2536‑59.
Boehm U, Bouloux PM, Dattani MT, de Roux N, Dodé C, Dunkel L, et al. European Consensus Statement on congenital hypogonadotropic hypogonadism—pathogenesis, diagnosis and treatment. Nat Rev Endocrinol. 2015;11(9):547‑64.
Bouvattier C, Maione L, Bouligand J, Dodé C, Guiochon-Mantel A, Young J. Neonatal gonadotropin therapy in male congenital hypogonadotropic hypogonadism. Nat Rev Endocrinol. mars 2012;8(3):172‑82.
Giton F, Trabado S, Maione L, Sarfati J, Le Bouc Y, Brailly-Tabard S, et al. Sex Steroids, Precursors, and Metabolite Deficiencies in Men With Isolated Hypogonadotropic Hypogonadism and Panhypopituitarism: A GCMS-Based Comparative Study. The Journal of Clinical Endocrinology & Metabolism. 1 févr 2015;100(2):E292‑6.
Young J. Approach to the Male Patient with Congenital Hypogonadotropic Hypogonadism. The Journal of Clinical Endocrinology & Metabolism. 2012;97(3):707‑18.
Dhindsa S, Prabhakar S, Sethi M, Bandyopadhyay A, Chaudhuri A, Dandona P. Frequent Occurrence of Hypogonadotropic Hypogonadism in Type 2 Diabetes. The Journal of Clinical Endocrinology & Metabolism. nov 2004;89(11):5462‑8.
Kapoor D, Aldred H, Clark S, Channer KS, Jones TH. Clinical and Biochemical Assessment of Hypogonadism in Men With Type 2 Diabetes. Diabetes Care. 1 avr 2007;30(4):911‑7.
Asare-Anane H, Ofori E, Agyemang Y, Oppong S, Tagoe E, Bani S, et al. Obesity and Testosterone Levels in Ghanaian Men With Type 2 Diabetes. Clinical Diabetes. 1 avr 2014;32(2):61‑5.
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. sept 2013;20(3):179‑86.
Ugwu TE, Ikem RT, Kolawole BA, Ezeani IU. Clinicopathologic assessment of hypogonadism in men with type 2 diabetes mellitus. Indian J Endocrinol Metab. 2016;20(5):667‑73.
Corona G, Mannucci E, Petrone L, Ricca V, Balercia G, Mansani R, et al. Association of hypogonadism and type II diabetes in men attending an outpatient erectile dysfunction clinic. Int J Impot Res. mars 2006;18(2):190‑7.
Dandona P, Dhindsa S. Update: Hypogonadotropic Hypogonadism in Type 2 Diabetes and Obesity. The Journal of Clinical Endocrinology & Metabolism. 2011;96(9):2643‑51.
Dhindsa S, Miller MG, McWhirter CL, Mager DE, Ghanim H, Chaudhuri A, et al. Testosterone Concentrations in Diabetic and Nondiabetic Obese Men. Diabetes Care. 1 juin 2010;33(6):1186‑92.
Tomar R, Dhindsa S, Chaudhuri A, Mohanty P, Garg R, Dandona P. Contrasting Testosterone Concentrations in Type 1 and Type 2 Diabetes. Diabetes Care. 1 mai 2006;29(5):1120‑2.
Zhang LY, He W, Wan JX, Yin QQ, Cheng Z, Chen GM, et al. [Hypogonadism and the quality of life in male patients with type-2 diabetes mellitus]. Zhonghua Nan Ke Xue. déc 2016;22(12):1088‑94.
Tamler R, Deveney T. Hypogonadism, Erectile Dysfunction, and Type 2 Diabetes Mellitus: What the Clinician Needs to Know. Postgraduate Medicine. 1 nov 2010;122(6):165‑75.
Feldman HA, Longcope C, Derby CA, Johannes CB, Araujo AB, Coviello AD, 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):589-98.
Barrett-Connor E. Lower Endogenous Androgen Levels and Dyslipidemia in Men with Non-Insulin-Dependent Diabetes Mellitus. Ann Intern Med. 1992;117(10):807-11.
Ding B, Li F fei, Zhai X fang, Ye L, Hu Y, Ma J hua. Men with Latent Autoimmune Diabetes and Type 2 Diabetes May Have Different Change Patterns in Free Testosterone. BioMed Research International. 24 juill 2020;2020:e6259437.
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. 1 mai 1996;143(9):889‑97.
Hu TY, Chen YC, Lin P, Shih CK, Bai CH, Yuan KC, et al., Testosterone-Associated Dietary Pattern Predicts Low Testosterone Levels and Hypogonadism. Nutrients. 2018;10(11):1786.
Allen NE, Key TJ. The effects of diet on circulating sex hormone levels in men. Nutr Res Rev. déc 2000;13(2):159‑84.
Tajar A, Forti G, O’Neill TW, Lee DM, Silman AJ, Finn JD, et al. Characteristics of Secondary, Primary, and Compensated Hypogonadism in Aging Men: Evidence from the European Male Ageing Study. The Journal of Clinical Endocrinology & Metabolism. 1 avr 2010;95(4):1810‑8.
Varlamov O. Western-style diet, sex steroids and metabolism.. Biochim Biophys Acta Mol Basis Dis. 2017 May;1863(5):1147-1155
Russo V, Chen R, Armamento-Villareal R. Hypogonadism, Type-2 Diabetes Mellitus, and Bone Health: A Narrative Review. Front Endocrinol (Lausanne). 2021; 11:607240.
Fernandez CJ, Chacko EC, Pappachan JM. Male Obesity-related Secondary Hypogonadism – Pathophysiology, Clinical Implications and Management. Eur Endocrinol. août 2019;15(2):83‑90.
Oueslati I, Ounissi M, Talbi E, Azaiez S, Bacha MM, Abdallah TB. Prevalence and risk factors of hypogonadism in men with chronic renal failure. Tunis Med. 2020 Feb;98(2):138-143.
Becquey E, Savy M, Danel P, Dabiré HB, Tapsoba S, Martin-Prével Y. Dietary patterns of adults living in Ouagadougou and their association with overweight. Nutrition Journal. 22 mars 2010;9(1):13.
Rovira-Llopis S, Bañuls C, de Marañon AM, Diaz-Morales N, Jover A, Garzon S, et al. Low testosterone levels are related to oxidative stress, mitochondrial dysfunction and altered subclinical atherosclerotic markers in type 2 diabetic male patients. Free Radic Biol Med. juill 2017;108:155‑62.
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. mai 2008;93(5):1834‑40.
Rao PM, Kelly DM, Jones TH. Testosterone and insulin resistance in the metabolic syndrome and T2DM in men. Nat Rev Endocrinol. août 2013;9(8):479‑93.
Inzucchi SE, Bergenstal RM, Buse JB, Diamant M, Ferrannini E, Nauck M, et al. Management of Hyperglycemia in Type 2 Diabetes, 2015: A Patient-Centered Approach: Update to a Position Statement of the American Diabetes Association and the European Association for the Study of Diabetes. Diabetes Care. 13 déc 2014;38(1):140‑9.