Male hypogonadism is associated with obesity
https://doi.org/10.31146/1682-8658-ecg-228-8-65-75
Abstract
About the Authors
P. Ya. MerzlovaRussian Federation
S. V. Bulgakova
Russian Federation
D. P. Kurmaev
Russian Federation
L. A. Sharonova
Russian Federation
Yu. A. Dolgikh
Russian Federation
E. V. Treneva
Russian Federation
O. V. Kosareva
Russian Federation
References
1. Kurmaev D. P., Bulgakova S. V., Treneva E. V. Sarcopenic obesity - a current problem of modern geriatrics.Russian Journal of Geriatric Medicine. 2022;(4):228-235. (In Russ.) doi: 10.37586/2686-8636-4-2022-228-235.@@ Курмаев Д. П., Булгакова С. В., Тренева Е. В. Саркопеническое ожирение - актуальная проблема современной гериатрии. Российский журнал гериатрической медицины. 2022;(4):228-235. doi: 10.37586/2686-8636-4-2022-228-235.
2. Arroyo-Johnson C., Mincey K. D. Obesity Epidemiology Worldwide. Gastroenterol Clin North Am. 2016;45(4): 571-579. doi: 10.1016/j.gtc.2016.07.012.
3. Masood B., Moorthy M. Causes of obesity: a review. Clin Med (Lond). 2023;23(4):284-291. doi: 10.7861/clinmed.2023-0168.
4. NCD Risk Factor Collaboration (NCD-RisC). Worldwide trends in body-mass index, underweight, overweight, and obesity from 1975 to 2016: a pooled analysis of 2416 population-based measurement studies in 128·9 million children, adolescents, and adults. Lancet. 2017;390(10113):2627-2642. doi: 10.1016/S0140-6736(17)32129-3.
5. Alferova V. I., Mustafina S. V. The prevalence of obesity in the adult population of the Russian Federation (literature review). Obesity and metabolism. 2022;19(1):96-105. (In Russ.) doi: 10.14341/omet12809.@@ Алфёрова В. И., Мустафина С. В. Распространенность ожирения во взрослой популяции Российской Федерации (обзор литературы). Ожирение и метаболизм. 2022;19(1):96-105. doi: 10.14341/omet12809.
6. Who.int. Obesity and overweight. Available at: https://www.who.int/mediacentre/factsheets/fs311/en (Accessed: 05.05.2023)
7. Balanova Yu.A., Shal’nova S.A., Deev A. D. еt al. On behalf of the participants in the ESSE-RF study. Obesity in the Russian population - prevalence and associations with risk factors for chronic noncommunicable diseases.Russian journal of cardiology. 2018;23(6):123-130. (In Russ.) doi: 10.15829/1560-4071-2018-6-123-130.@@ Баланова Ю. А., Шальнова С. А., Деев А. Д. и др. Ожирение в российской популяции - распространенность и ассоциации с факторами риска хронических неинфекционных заболеваний. Российский кардиологический журнал. 2018;23(6):123-130. doi: 10.15829/1560-4071-2018-6-123-130.
8. Sharonova L. A., Bulgakova S. V., Dolgikh Yu.A. еt al. Obesity as a main component of metabolic syndrome and a risk factor for comorbidity. Experimental and Clinical Gastroenterology. 2024;(2):101-110. (In Russ.) doi: 10.31146/1682-8658-ecg-222-2-101-110.@@ Шаронова Л. А., Булгакова С. В., Долгих Ю. А., и др. Ожирение как основной компонент метаболического синдрома и фактор риска коморбидности. Экспериментальная и клиническая гастроэнтерология. 2024;(2):101-110. doi: 10.31146/1682-8658-ecg-222-2-101-110.
9. Bulgakova S. V., Sharonova L. A., Kurmaev D. P. еt al. Relationship between sarcopenic obesity and bone density in elderly patients. Farmateka. 2024;31(2):116-121. (In Russ.) doi: 10.18565/pharmateca.2024.2.116-121.@@ Булгакова С. В., Шаронова Л. А., Курмаев Д. П. и др. Взаимосвязь между саркопеническим ожирением и костной плотностью у пациентов пожилого возраста. Фарматека. 2024;31(2):116-121. doi: 10.18565/pharmateca.2024.2.116-121.
10. Berns S. A., Sheptulina A. F., Mamutova E. M. еt al. Sarcopenic obesity: epidemiology, pathogenesis and diagnostic criteria. Cardiovascular Therapy and Prevention. 2023;22(6):3576. (In Russ.) doi: 10.15829/1728-8800-2023-3576.@@ Бернс С. А., Шептулина А. Ф., Мамутова Э. М. и др. Саркопеническое ожирение: эпидемиология, патогенез и особенности диагностики. Кардиоваскулярная терапия и профилактика. 2023;22(6):3576. doi: 10.15829/1728-8800-2023-3576.
11. Tsygankov D. A., Krivoshapova K. E., Tsygankova D. P. Ultrasound potential in sarcopenic obesity diagnosis: a literature review.Russian Journal of Cardiology. 2023;28(3S):5345. (In Russ.) doi: 10.15829/1560-4071-2023-5345.@@ Цыганков Д. А., Кривошапова К. Е., Цыганкова Д. П. Ультразвуковые возможности диагностики саркопенического ожирения. Российский кардиологический журнал. 2023;28(3S):5345. doi: 10.15829/1560-4071-2023-5345.
12. Samoilova Yu.G., Matveeva M. V., Khoroshunova E. A. еt al. Cardiometabolic risk factors in patients with type 2 diabetes and sarcopenia. Cardiovascular Therapy and Prevention. 2024;23(1):3655. (In Russ.) doi: 10.15829/1728-8800-2024-3655.@@ Самойлова Ю. Г., Матвеева М. В., Хорошунова Е. А. и др. Кардиометаболические факторы риска у пациентов с сахарным диабетом 2 типа и саркопенией. Кардиоваскулярная терапия и профилактика. 2024;23(1):3655. doi: 10.15829/1728-8800-2024-3655.
13. Dedov II, Mokrysheva NG, Melnichenko GA, et al. Draft of Russian Clinical Practice Guidelines «Male hypogonadism». Obesity and metabolism. 2021;18(4):496-507. (In Russ.) doi: 10.14341/omet12817.@@ Дедов И. И., Мокрышева Н. Г., Мельниченко Г. А. и др. Проект клинических рекомендаций «Синдром гипогонадизма у мужчин». Ожирение и метаболизм. 2021;18(4):496-507. doi: 10.14341/omet12817.
14. 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(3):330-337. doi: 10.1111/cen.12092.
15. Molina-Vega M., Muñoz-Garach A., Damas-Fuentes M. et al. Secondary male hypogonadism: A prevalent but overlooked comorbidity of obesity. Asian J Androl. 2018;20(6):531-538. doi: 10.4103/aja.aja_44_18.
16. Gamidov S. I., Shatylko T. V., Gasanov N. G. Male health and obesity - diagnostic and therapeutic approach. Obesity and metabolism. 2019;16(3):29-36. (In Russ.) doi: 10.14341/omet10314.@@ Гамидов С. И., Шатылко Т. В., Гасанов Н. Г. Мужское здоровье и ожирение - диагностика и терапевтические подходы. Ожирение и метаболизм. 2019;16(3):29-36. doi: 10.14341/omet10314.
17. MacDonald A.A., Herbison G. P., Showell M., Farquhar C. M. The impact of body mass index on semen parameters and reproductive hormones in human males: a systematic review with meta-analysis. Hum Reprod Update. 2010;16(3):293-311. doi: 10.1093/humupd/dmp047.
18. Di Nisio A., Sabovic I., De Toni L. et al. Testosterone is sequestered in dysfunctional adipose tissue, modifying androgen-responsive genes.Int J Obes (Lond). 2020;44(7):1617-1625. doi: 10.1038/s41366-020-0568-9.
19. Cui H., López M., Rahmouni K. The cellular and molecular bases of leptin and ghrelin resistance in obesity. Nat Rev Endocrinol. 2017;13(6):338-351. doi: 10.1038/nrendo.2016.222.
20. Chou S. H., Mantzoros C. 20 years of leptin: role of leptin in human reproductive disorders. J Endocrinol. 2014;223(1): T49-T62. doi: 10.1530/JOE-14-0245.
21. Teerds K. J., de Rooij D. G., Keijer J. Functional relationship between obesity and male reproduction: from humans to animal models. Hum Reprod Update. 2011;17(5):667-683. doi: 10.1093/humupd/dmr017.
22. Moon H. S., Dalamaga M., Kim S. Y. et al. Leptin’s role in lipodystrophic and nonlipodystrophic insulin-resistant and diabetic individuals. Endocr Rev. 2013;34(3):377-412. doi: 10.1210/er.2012-1053.
23. Landry D. A., Sormany F., Haché J. et al. Steroidogenic genes expressions are repressed by high levels of leptin and the JAK/STAT signaling pathway in MA-10 Leydig cells. Mol Cell Biochem. 2017;433(1-2):79-95. doi: 10.1007/s11010-017-3017-x.
24. Isidori A. M., 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(10):3673-3680. doi: 10.1210/jcem.84.10.6082.
25. Cooper L. A., Page S. T., Amory J. K. et al. 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.
26. Simó R., Sáez-López C., Barbosa-Desongles A. et al. Novel insights in SHBG regulation and clinical implications. Trends Endocrinol Metab. 2015;26(7):376-383. doi: 10.1016/j.tem.2015.05.001.
27. Hammond G. L. Plasma steroid-binding proteins: primary gatekeepers of steroid hormone action. J Endocrinol. 2016;230(1): R13-R25. doi: 10.1530/JOE-16-0070.
28. Kawai T., Autieri M. V., Scalia R. Adipose tissue inflammation and metabolic dysfunction in obesity. Am J Physiol Cell Physiol. 2021;320(3): C375-C391. doi: 10.1152/ajpcell.00379.2020.
29. Russell S. H., Small C. J., Stanley S. A. et al. The in vitro role of tumour necrosis factor-alpha and interleukin-6 in the hypothalamic-pituitary gonadal axis. J Neuroendocrinol. 2001;13(3):296-301. doi: 10.1046/j.1365-2826.2001.00632.x.
30. Leisegang K., Henkel R. The in vitro modulation of steroidogenesis by inflammatory cytokines and insulin in TM3 Leydig cells. Reprod Biol Endocrinol. 2018;16(1):26. doi: 10.1186/s12958-018-0341-2.
31. Fan W., Xu Y., Liu Y. et al. Obesity or Overweight, a Chronic Inflammatory Status in Male Reproductive System, Leads to Mice and Human Subfertility. Front Physiol. 2018;8:1117. doi: 10.3389/fphys.2017.01117.
32. Ebrahimi F., Urwyler S. A., Straumann S. et al. IL-1 Antagonism in Men With Metabolic Syndrome and Low Testosterone: A Randomized Clinical Trial. J Clin Endocrinol Metab. 2018;103(9):3466-3476. doi: 10.1210/jc.2018-00739.
33. Giagulli V. A., Castellana M., Murro I. et al. The Role of Diet and Weight Loss in Improving Secondary Hypogonadism in Men with Obesity with or without Type 2 Diabetes Mellitus. Nutrients. 2019;11(12):2975. doi: 10.3390/nu11122975.
34. Corona G., Rastrelli G., Monami M. et al. Body weight loss reverts obesity-associated hypogonadotropic hypogonadism: a systematic review and meta-analysis. Eur J Endocrinol. 2013;168(6):829-843. doi: 10.1530/EJE-12-0955.
35. La J., Roberts N. H., Yafi F. A. Diet and Men’s Sexual Health. Sex Med Rev. 2018;6(1):54-68. doi: 10.1016/j.sxmr.2017.07.004.
36. Moran L. J., Brinkworth G. D., Martin S. et al. Long-Term Effects of a Randomised Controlled Trial Comparing High Protein or High Carbohydrate Weight Loss Diets on Testosterone, SHBG, Erectile and Urinary Function in Overweight and Obese Men. PLoS One. 2016;11(9): e0161297. doi: 10.1371/journal.pone.0161297.
37. Mongioì L. M., Cimino L., Condorelli R. A. et al. Effectiveness of a Very Low Calorie Ketogenic Diet on Testicular Function in Overweight/Obese Men. Nutrients. 2020;12(10):2967. doi: 10.3390/nu12102967.
38. Genchi V. A., Rossi E., Lauriola C. et al. Adipose Tissue Dysfunction and Obesity-Related Male Hypogonadism.Int J Mol Sci. 2022;23(15):8194. doi: 10.3390/ijms23158194.
39. Suleiman J. B., Nna V. U., Othman Z. A. et al. Orlistat attenuates obesity-induced decline in steroidogenesis and spermatogenesis by up-regulating steroidogenic genes. Andrology. 2020;8(5):1471-1485. doi: 10.1111/andr.12824.
40. Suleiman J. B., Nna V. U., Zakaria Z. et al. Orlistat reverses intratesticular lactate transport decline and infertility in male obese rats. Reproduction. 2020;160(6):863-872. doi: 10.1530/REP-20-0381.
41. Bellentani F. F., Fernandes G. S., Perobelli J. E. et al. Acceleration of sperm transit time and reduction of sperm reserves in the epididymis of rats exposed to sibutramine. J Androl. 2011;32(6):718-724. doi: 10.2164/jandrol.111.013466.
42. Borges C. S., Silva P. V., Lozano A. F.Q. et al. Impact of timing of the anorexigen sibutramine administration on reproductive end-points of male rats. Basic Clin Pharmacol Toxicol. 2020;127(6):525-532. doi: 10.1111/bcpt.13467.
43. Tak Y. J., Lee S. Y. Anti-Obesity Drugs: Long-Term Efficacy and Safety: An Updated Review. World J Mens Health. 2021;39(2):208-221. doi: 10.5534/wjmh.200010.
44. Cannarella R., Calogero A. E., Condorelli R. A. et al. Is there a role for glucagon-like peptide-1 receptor agonists in the treatment of male infertility?. Andrology. 2021;9(5):1499-1503. doi: 10.1111/andr.13015.
45. Giagulli V. A., Carbone M. D., Ramunni M. I. et al. Adding liraglutide to lifestyle changes, metformin and testosterone therapy boosts erectile function in diabetic obese men with overt hypogonadism. Andrology. 2015;3(6):1094-1103. doi: 10.1111/andr.12099.
46. Jensterle M., Podbregar A., Goricar K. et al. Effects of liraglutide on obesity-associated functional hypogonadism in men. Endocr Connect. 2019;8(3):195-202. doi: 10.1530/EC-18-0514.
47. Shao N., Yu X. Y., Yu Y. M. et al. Short-term combined treatment with exenatide and metformin is superior to glimepiride combined metformin in improvement of serum testosterone levels in type 2 diabetic patients with obesity. Andrologia. 2018;50(7): e13039. doi: 10.1111/and.13039.
48. Izzi-Engbeaya C., Jones S., Crustna Y. et al. Effects of Glucagon-like Peptide-1 on the Reproductive Axis in Healthy Men. J Clin Endocrinol Metab. 2020;105(4):1119-1125. doi: 10.1210/clinem/dgaa072.
49. Troshina E. A., Terekhov Р. A. Hypogonadism and visceral obesity in men are full-fledged components of the metabolic syndrome. Obesity and metabolism. 2023;20(1):84-91. (In Russ.) doi: 10.14341/omet12980.@@ Трошина Е. А., Терехов П. А. Гипогонадизм и висцеральное ожирение у мужчин - полноправные компоненты метаболического синдрома. Ожирение и метаболизм. 2023;20(1):84-91. doi: 10.14341/omet12980.
50. Klevanskaya A.A., Bulgakova S. V., Melikova A. V. A positive experience of using testosterone in combination with vitamin D3 and a complex of Omega-3 polyunsaturated fatty acids in a patient with late-onset hypogonadism and a history of radical prostatectomy for cancer. Vopr. urol. androl. (Urology and Andrology). 2020;8(4):16-20. (In Russ.)@@ Клеванская А. А., Булгакова С. В., Меликова А. В. Положительный опыт применения тестостерона в комбинации с витамином D3 и комплексом Омега-3 полиненасыщенных жирных кислот у пациента с поздним гипогонадизмом, перенесшего радикальную простатэктомию по поводу рака. Вопросы урологии и андрологии. 2020;8(4):16-20.
51. Corona G., Giagulli V. A., Maseroli E. et al. Therapy of endocrine disease: Testosterone supplementation and body composition: results from a meta-analysis study. Eur J Endocrinol. 2016;174(3): R99-116. doi: 10.1530/EJE-15-0262.
52. Ng Tang Fui M., Prendergast L. A., Dupuis P. et al. Effects of testosterone treatment on body fat and lean mass in obese men on a hypocaloric diet: a randomised controlled trial. BMC Med. 2016;14(1):153. doi: 10.1186/s12916-016-0700-9.
53. Caliber M., Hackett G. Important lessons about testosterone therapy- weight loss vs. testosterone therapy for symptom resolution, classical vs. functional hypogonadism, and shortterm vs. lifelong testosterone therapy. Aging Male. 2020;23(5):585-591. doi: 10.1080/13685538.2018.1549211.
54. Corona G., Vignozzi L., Sforza A. et al. Obesity and late-onset hypogonadism. Mol Cell Endocrinol. 2015;418 Pt 2:120-133. doi: 10.1016/j.mce.2015.06.031.
55. Pellitero S., Olaizola I., Alastrue A. et al. Hypogonadotropic hypogonadism in morbidly obese males is reversed after bariatric surgery. Obes Surg. 2012;22(12):1835-1842. doi: 10.1007/s11695-012-0734-9.
56. Pham N. H., Bena J., Bhatt D. L. et al. Increased Free Testosterone Levels in Men with Uncontrolled Type 2 Diabetes Five Years After Randomization to Bariatric Surgery. Obes Surg. 2018;28(1):277-280. doi: 10.1007/s11695-017-2881-5.
57. Calderón B., Galdón A., Calañas A. et al. Effects of bariatric surgery on male obesity-associated secondary hypogonadism: comparison of laparoscopic gastric bypass with restrictive procedures. Obes Surg. 2014;24(10):1686-1692. doi: 10.1007/s11695-014-1233-y.
58. Di Vincenzo A., Busetto L., Vettor R., Rossato M. Obesity, Male Reproductive Function and Bariatric Surgery. Front Endocrinol (Lausanne). 2018;9:769. doi: 10.3389/fendo.2018.00769.
59. Glina F. P.A., de Freitas Barboza J. W., Nunes V. M. et al. What Is the Impact of Bariatric Surgery on Erectile Function? A Systematic Review and Meta-Analysis. Sex Med Rev. 2017;5(3):393-402. doi: 10.1016/j.sxmr.2017.03.008.
60. Carette C., Levy R., Eustache F. et al. Changes in total sperm count after gastric bypass and sleeve gastrectomy: the BARIASPERM prospective study. Surg Obes Relat Dis. 2019;15(8):1271-1279. doi: 10.1016/j.soard.2019.04.019.
61. Lazaros L., Hatzi E., Markoula S. et al. Dramatic reduction in sperm parameters following bariatric surgery: report of two cases. Andrologia. 2012;44(6):428-432. doi: 10.1111/j.1439-0272.2012.01300.x.
Review
For citations:
Merzlova P.Ya., Bulgakova S.V., Kurmaev D.P., Sharonova L.A., Dolgikh Yu.A., Treneva E.V., Kosareva O.V. Male hypogonadism is associated with obesity. Experimental and Clinical Gastroenterology. 2024;(8):65-75. (In Russ.) https://doi.org/10.31146/1682-8658-ecg-228-8-65-75