ISSN 2412-4036 (print)
ISSN 2713-1823 (online)

Hypogonadism syndrome in men with systemic connective tissue diseases

Panevin T.S., Zotkin E.G., Glukhova S.I., Shumilova A.A., Desinova O.V., Khelkovskaya-Sergeeva A.N.

1) V.A. Nasonova Scientific and Research Institute of Rheumatology, Moscow; 2) Far Eastern State Medical University of the Ministry of Healthcare of Russia, Khabarovsk
Abstract. It is known that hypogonadism in men can influence the course and clinical presentation of immune-mediated inflammatory rheumatic diseases. Decreased testosterone levels are also associated with the development of various metabolic disorders.
The aim: to study factors associated with hypogonadism in men with systemic connective tissue diseases.
Material and methods. A cross-sectional study included 157 men, 59 of whom had systemic lupus erythematosus (SLE), 60 with systemic sclerosis (SSc), and 38 with idiopathic inflammatory myopathies. All patients underwent serum total testosterone measurements. Hypogonadism was defined as a testosterone level ≤ 12.0 nmol/L. A binary analysis was performed to identify factors associated with low testosterone levels.
Results. In a study of patients with SLE, it was found that taking prednisolone at a daily dose of ≥ 10 mg increased the odds of hypogonadism (OR 9.5; 95% CI: 1.60–56.46; p = 0.013), while current hydroxychloroquine use was associated with a reduced likelihood of this feature (OR 0.18; 95% CI: 0.03–0.93; p = 0.04). Among the patients with SSc, a risk factor for hypogonadism was positivity for antibodies to Scl70 (OR 16.2; 95% CI: 1.95–134.90; p = 0.01). Among patients with idiopathic inflammatory myopathies, the likelihood of hypogonadism was significantly higher in those with concomitant cardiovascular diseases (OR 5.6; 95% CI: 1.02–31.10; p = 0.048).
Conclusion. Decreased testosterone levels are associated with specific SLE treatment options, as well as with the presence of antibodies characteristic of the diffuse form of SSc.

Keywords

systemic lupus erythematosus
systemic sclerosis
myositis
hypogonadism
androgen deficiency

References

1. Насонов Е.Л., Александрова Е.Н., Новиков А.А. Аутоиммунные ревматические заболевания – проблемы иммунопатологии и персонифицированной терапии. Вестник Российской академии медицинских наук. 2015;70(2):169–82. (Nasonov EL, Aleksandrova EN, Novikov AA. Autoimmune rheumatic diseases – problems of immunopathology and personalized therapy. Vestnik Rossiyskoy akademii meditsinskikh nauk = Annals of the Russian Academy of Medical Sciences. 2015;70(2):169–82 (In Russ.)).

EDN: TVSSNP. https://doi.org/10.15690/vramn.v70i2.1310

2. Cutolo M, Straub RH. Sex steroids and autoimmune rheumatic diseases: State of the art. Nat Rev Rheumatol. 2020;16(11):628–44.

PMID: 33009519. https://doi.org/10.1038/s41584-020-0503-4

3. Motta F, Di Simone N, Selmi C. The impact of menopause on autoimmune and rheumatic diseases. Clin Rev Allergy Immunol. 2025;68(1):32.

PMID: 40117049. PMCID: PMC11928423. https://doi.org/10.1007/s12016-025-09031-8

4. Дедов И.И., Мокрышева Н.Г., Мельниченко Г.А., Роживанов Р.В., Камалов А.А., Мкртумян А.М. с соавт. Проект клинических рекомендаций «Синдром гипогонадизма у мужчин». Ожирение и метаболизм. 2021;18(4):496–507. (Dedov II, Mokrysheva NG, Melnichenko GA, et al. Draft of Russian clinical practice guidelines ”Male hypogonadism”. Ozhirenie i metabolizm = Obesity and Metabolism. 2021;18(4):496–507 (In Russ.)).

EDN: FUWRTV. https://doi.org/10.14341/omet12817

5. Паневин Т.С., Роживанов Р.В., Зоткин Е.Г., Диатроптов М.Е., Глухова С.И., Самаркина Е.Ю. Клинико-лабораторные особенности ревматоидного артрита у мужчин в зависимости от уровня тестостерона. Проблемы эндокринологии. 2024;70(3):98–104. (Panevin TS, Rozhivanov RV, Zotkin EG, Diatroptov ME, Glukhova SI, Samarkina EYu. Clinical and laboratory features of rheumatoid arthritis in men depending on testosterone levels. Problemy endokrinologii = Problems of Endocrinology. 2024;70(3):98–104 (In Russ.)).

EDN: AQHVSP. https://doi.org/10.14341/probl13373

6. Паневин Т.С., Коротаева Т.В., Эрдес Ш.Ф., Роживанов Р.В., Зоткин Е.Г., Глухова С.И., Черкасова М.В. Клиническая характеристика псориатического артрита у мужчин в зависимости от уровня тестостерона. Научно-практическая ревматология. 2024;62(6):627–32. (Panevin TS, Korotaeva TV, Erdes SF, Rozhivanov RV, Zotkin EG, Glukhova SI, Cherkasova MV. Clinical and instrumental characteristics of psoriatic arthritis in men depending on testosterone levels. Nauchno-prakticheskaya revmatologiya = Rheumatology Science and Practice. 2024;62(6):627–32 (In Russ.)).

EDN: BSJUSD. https://doi.org/10.47360/1995-4484-2024-627-632

7. Паневин Т.С., Эрдес Ш.Ф., Коротаева Т.В., Роживанов Р.В., Зоткин Е.Г., Глухова С.И. с соавт. Клинико-лабораторные особенности анкилозирующего спондилита у мужчин в зависимости от уровня тестостерона. Научно-практическая ревматология. 2025;63(5):483–489. (Panevin TS, Erdes SF, Korotaeva TV, Rozhivanov RV, Zotkin EG, Glukhova SI et al. Clinical and laboratory features of ankylosing spondylitis in men depending on testosterone levels. Nauchno-prakticheskaya revmatologiya = Rheumatology Science and Practice. 2025;63(5):483–489 (In Russ.)).

EDN: LIZSNW. https://doi.org/10.47360/1995-4484-2025-483-489

8. Паневин Т.С., Ананьева Л.П., Зоткин Е.Г., Глухова С.И., Диатроптова М.А., Самаркина Е.Ю. Частота гипогонадизма и клинические особенности системной склеродермии и идиопатических воспалительных миопатий у мужчин в зависимости от уровня тестостерона. Терапевтический архив. 2025;97(10):836–84. (Panevin TS, Ananyeva LP, Zotkin EG, Glukhova SI, Diatroptova MA, Samarkina EYu. Frequency of hypogonadism and clinical features of systemic sclerosis and idiopathic inflammatory myopathies in men depending on testosterone levels. Terapevticheskiy arkhiv = Terapeutic Archive. 2025;97(10):836–843 (In Russ.)).

EDN: PRUGKF. https://doi.org/10.26442/00403660.2025.10.203374

9. Паневин Т.С., Попкова Т.В., Зоткин Е.Г., Глухова С.И., Диатроптов М.Е. Клинические особенности системной красной волчанки у мужчин в зависимости от уровня тестостерона. Современная ревматология. 2025;19(2):63–69. (Panevin TS, Popkova TV, Zotkin EG, Glukhova SI, Diatroptov ME. Clinical features of systemic lupus erythematosus in men depending on testosterone levels. Sovremennaya revmatologiya = Modern Rheumatology Journal. 2025;19(2):63–69 (In Russ.)).

EDN: QELNCQ. https://doi.org/10.14412/1996-7012-2025-2-63-69

10. Mohamad NV, Wong SK, Wan Hasan WN, Jolly JJ, Nur-Farhana MF, Ima-Nirwana S, Chin KY. The relationship between circulating testosterone and inflammatory cytokines in men. Aging Male. 2019;22(2):129–40.

PMID: 29925283. https://doi.org/10.1080/13685538.2018.1482487

11. Cutolo M, Sulli A, Capellino S, Villaggio B, Montagna P, Pizzorni C et al. Anti-TNF and sex hormones. Ann N Y Acad Sci. 2006;1069:391–400.

PMID: 16855166. https://doi.org/10.1196/annals.1351.037

12. Wen P, Wang Y, Yang M, Qiao X, Yang P, Hu S et al. Sex hormone imbalance and rheumatoid arthritis in American men: A cross-sectional analysis from NHANES 2011–2016. Front Immunol. 2024;15:1501257.

PMID: 39759528. PMCID: PMC11695343. https://doi.org/10.3389/fimmu.2024.1501257

13. Baillargeon J, Al Snih S, Raji MA, Urban RJ, Sharma G, Sheffield-Moore M et al. Hypogonadism and the risk of rheumatic autoimmune disease. Clin Rheumatol. 2016;35(12):2983–87.

PMID: 27325124. PMCID: PMC5544431. https://doi.org/10.1007/s10067-016-3330-x

14. Yang DD, Krasnova A, Nead KT, Choueiri TK, Hu JC, Hoffman KE et al. Androgen deprivation therapy and risk of rheumatoid arthritis in patients with localized prostate cancer. Ann Oncol. 2018;29(2):386–91.

PMID: 29267861. https://doi.org/10.1093/annonc/mdx744

15. Arnaud L, Nordin A, Lundholm H, Svenungsson E, Hellbacher E, Wikner J et al. Effect of corticosteroids and cyclophosphamide on sex hormone profiles in male patients with systemic lupus erythematosus or systemic sclerosis. Arthritis Rheumatol. 2017;69(6):1272–79.

PMID: 28141919. https://doi.org/10.1002/art.40057

16. Mok CC, Lau CS. Profile of sex hormones in male patients with systemic lupus erythematosus. Lupus. 2000;9(4):252–57.

PMID: 1086609. https://doi.org/10.1191/096120300680198926

17. Thepwiwatjit S, Charoensri S, Sirithanaphol W, Mahakkanukrauh A, Suwannaroj S, Foocharoen C. Prevalence and clinical associations with primary hypogonadism in male systemic sclerosis. J Scleroderma Relat Disord. 2022;7(3):234–42.

PMID: 36211203. PMCID: PMC9537708. https://doi.org/10.1177/23971983221112021

About the Authors

Taras S. Panevin, MD, PhD (Medicine), researcher, endocrinologist at V.A. Nasonova Scientific and Research Institute of Rheumatology; associate professor of the Department of faculty and outpatient therapy with a course in endocrinology, Far Eastern State Medical University of the Ministry of Healthcare of Russia. Address: 115522, Moscow, 34A Kashirskoe Avenue.
E-mail: tarasel@list.ru
ORCID: https://orcid.org/0000-0002-5290-156X
Evgeny G. Zotkin, MD, Dr. Sci. (Medicine), first deputy director of V.A. Nasonova Scientific and Research Institute of Rheumatology. Address: 115522, Moscow, 34A Kashirskoe Avenue.
E-mail: ezotkin@mail.ru
ORCID: https://orcid.org/0000-0002-4579-2836
Svetlana I. Glukhova, MD, PhD (Physics and Mathematics), senior researcher at V.A. Nasonova Scientific and Research Institute of Rheumatology. Address: 115522, Moscow, 34A Kashirskoe Avenue.
E-mail: sveglukhova@yandex.ru
ORCID: https://orcid.org/0000-0002-4285-0869
Anastasia A. Shumilova, MD, junior researcher at V.A. Nasonova Scientific and Research Institute of Rheumatology. Address: 115522, Moscow, 34A Kashirskoe Avenue.
E-mail: dr.anashumilova@gmail.com
ORCID: https://orcid.org/0000-0003-1318-1894
Oksana V. Desinova, MD, PhD (Medicine), researcher at V.A. Nasonova Scientific and Research Institute of Rheumatology. Address: 115522, Moscow, 34A Kashirskoe Avenue.
ORCID: https://orcid.org/0000-0002-0283-9681
Anna N. Khelkovskaya-Sergeeva, MD, researcher at V.A. Nasonova Scientific and Research Institute of Rheumatology. Address: 115522, Moscow, 34A Kashirskoe Avenue.
E-mail: ankhill@yandex.ru
ORCID: https://orcid.org/0000-0002-9755-5760

Similar Articles