Characteristics of immunocompetent cells in the testicles of different age group patients with COVID-19

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Abstract

BACKGROUND: There is an opinion that the new coronavirus infection COVID-19 can initiate the development of a local inflammatory reaction in the testicles, which leads to damage to spermatogenic epithelial cells and a decrease in the fertility of patients in the long term.

AIM: Morphofunctional assessment of immunocompetent cells in the testicles of patients with COVID-19 depending on age.

MATERIAL AND METHODS: Based on anamnestic, clinical and morphological data, groups of patients were formed, each of which included subgroups according to the age periodization of the World Health Organization: the first group of patients who died as a result of COVID-19 (n=109; average age 58±2.8 years) — young subgroup (n=19, age 18–44 years), middle-aged subgroup (n=37, age 45–59 years), elderly subgroup (n=53, age 60–74 years); second group (n=30, average age 49±2.3 years; autopsy material from the testicles of patients who died from causes unrelated to COVID-19, obtained outside the pandemic) — a subgroup of young people (n=10, age 18–44 years), middle-aged subgroup (n=10, age 45–59 years), elderly subgroup (n=10, age 60–74 years). Histological and immunohistochemical studies were carried out using primary antibodies to CD3, CD4, CD68, CD163, CD138 and statistical methods: Kolmogorov–Smirnov test, Student's t-test, Mann–Whitney U test and Fisher test.

RESULTS: All testicular samples from patients with COVID-19 revealed signs of viral orchitis and a significant decrease in the spermatogenesis index (in young people — 5.9±0.2% with p=0.02; in middle age — 5.1±0.2% with p=0.008; in the elderly — 3.6±0.1% at p=0.006) compared to the control group (6.8±0.3%), and in immunohistochemical studies — an increase in the number of T-lymphocytes (CD3+, CD4+), macrophages (CD68+, CD163+) and plasma cells (CD138+) in interstitial tissue. In addition, a significant decrease in the spermatogenesis index (3.6±0.1% in the elderly versus 5.9±0.2% in the young, p=0.007) and a decrease in the number of T-lymphocytes (CD3+, CD4+) and macrophages (CD68+, CD163+) was found in older versus younger patients with COVID-19.

CONCLUSION: In patients with COVID-19, an increase in the number of immunocompetent cells (CD3+, CD4+, CD68+, CD138+, CD163+) in the interstitial tissue of the testicles was found, especially pronounced in the elderly group.

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About the authors

Grigory A. Demyashkin

First Moscow State Medical University named after I.M. Sechenov (Sechenov University); National Medical Research Center for Radiology

Author for correspondence.
Email: dr.dga@mail.ru
ORCID iD: 0000-0001-8447-2600
SPIN-code: 5157-0177

MD, Dr. Sci. (Med.), Head of the Laboratory, Laboratory of Histology and Immunohistochemistry, Institute of Translational Medicine and Biotechnology

Russian Federation, Moscow; Moscow

Dmitry V. Boldyrev

First Moscow State Medical University named after I.M. Sechenov (Sechenov University)

Email: Derfeelgood@yandex.ru
ORCID iD: 0000-0002-4548-5430
SPIN-code: 1893-4960

MD, Pathologist, Post-Graduate Student, Institute of Translational Medicine and Biotechnology

Russian Federation, Moscow

Matvey A. Vadyukhin

First Moscow State Medical University named after I.M. Sechenov (Sechenov University)

Email: vma20@mail.ru
ORCID iD: 0000-0002-6235-1020
SPIN-code: 9485-7722

Stud., N.V. Sklifosovsky Institute of Clinical Medicine

Russian Federation, Moscow

Lia N. Alieva

First Moscow State Medical University named after I.M. Sechenov (Sechenov University)

Email: pancake0401@gmail.com
ORCID iD: 0009-0002-9989-7868

Stud., N.V. Sklifosovsky Institute of Clinical Medicine

Russian Federation, Moscow

Elmar N. Shirinov

First Moscow State Medical University named after I.M. Sechenov (Sechenov University)

Email: ekaqaqa@mail.ru
ORCID iD: 0009-0000-9799-8601

Stud., Institute of Dentistry of the Sechenov University

Russian Federation, Moscow

References

  1. Mohamed S, Saad K, Elgohary G, Abd El Haffez A, El-Aziz NA. Is COVID-19 a systemic disease? Coronaviruses. 2020;2(5):4–8. doi: 10.2174/2666796701999201216101914
  2. Dong E, Du H, Gardner L. An interactive web-based dashboard to track COVID-19 in real time. Lancet Infect Dis. 2020;20(5):533–534. doi: 10.1016/S1473-3099(20)30120-1
  3. El-Kassas M, Alboraie M, Elbadry M. Non-pulmonary involvement in COVID-19: A systemic disease rather than a pure respiratory infection. World J Clin Cases. 2023;11(3):493–505. doi: 10.12998/wjcc.v11.i3.493
  4. Askari H, Rabiei F, Lohrasbi F, Ghadir S, Ghasemi-Kasman M. The latest cellular and molecular mechanisms of COVID-19 on non-lung organs. Brain Sci. 2023;13(3):415. doi: 10.3390/brainsci13030415
  5. Yang L, Liu S, Liu J, Zhang Z, Wan X, Huang B. COVID-19: Immunopathogenesis and immunotherapeutics. Signal Transduct Target Ther. 2020;5(1):1–8. doi: 10.1038/s41392-020-00243-2
  6. Sharma I, Kumari P, Sharma A, Saha SC. SARS-CoV-2 and the reproductive system: Known and the unknown. Middle East Fertil Soc J. 2021;26(1):1. doi: 10.1186/s43043-020-00046-z
  7. He Y, Wang J, Ren J, Zhao Y, Chen J, Chen X. Effect of COVID-19 on male reproductive system — a systematic review. Front Endocrinol. 2021;12:677701. doi: 10.3389/fendo.2021.677701
  8. Donders GGG, Bosmans E, Reumers J, Donders F, Jonckheere J, Salembier G. Sperm quality and absence of SARS-CoV-2 RNA in semen after COVID-19 infection: A prospective, observational study and validation of the SpermCOVID test. Fertil Steril. 2022;117(2):287–296. doi: 10.1016/j.fertnstert.2021.10.022
  9. Gong J, Zeng Q, Yu D, Duan YG. T lymphocytes and testicular immunity: A new insight into immune regulation in testes. Int J Mol Sci. 2020;22(1):57. doi: 10.3390/ijms220100576
  10. Baughn LB, Sharma N, Elhaik E, Sekulic A, Bryce AH, Fonseca R. Targeting TMPRSS2 in SARS-CoV-2 infection. Mayo Clin Proc. 2020;95(9):1989–1999. doi: 10.1016/j.mayocp.2020.06.018
  11. Lasiene K, Gasiliunas D, Juodziukyniene N, Dabuzinskiene A, Vitkus A, Zilaitiene B. Age-related morphological peculiarities of human testes. Folia Morphol. 2021;80(1):122–126. doi: 10.5603/FM.a2020.0033
  12. Duarte-Neto AN, Teixeira TA, Caldini EG. Testicular pathology in fatal COVID-19: A descriptive autopsy study. Andrology. 2022;10(1):13–23. doi: 10.1111/andr.13073
  13. Zhao S, Zhu W, Xue S, Han D. Testicular defense systems: Immune privilege and innate immunity. Cell Mol Immunol. 2014;11(5):428–437. doi: 10.1038/cmi.2014.38
  14. Kind S, Merenkow C, Büscheck F, Möller K, Dum D, Chirico V. Prevalence of syndecan-1 (CD138) expression in different kinds of human tumors and normal tissues. Dis Markers. 2019;2019:4928315. doi: 10.1155/2019/4928315
  15. Yang M, Chen S, Huang B, Zhong JM, Su H, Chen YJ. Pathological findings in the testes of COVID-19 patients: Clinical implications. Eur Urol Focus. 2020;6(5):1124–1129. doi: 10.1016/j.euf.2020.05.009
  16. Xie Y, Mirzaei M, Kahrizi MS, Shabestari AM, Riahi SM, Farsimadan M. SARS-CoV-2 effects on sperm parameters: A meta-analysis study. J Assist Reprod Genet. 2022;39(7):1555–1563. doi: 10.1007/s10815-022-02540-x
  17. Aksak T, Satar DA, Bağci R, Gültekin EO, Coşkun A, Demirdelen U. Investigation of the effect of COVID-19 on sperm count, motility, and morphology. J Med Virol. 2022;94(11):5201–5205. doi: 10.1002/jmv.27971
  18. Diagnostic testing for SARS-CoV-2: Interim guidance, 11 September 2020. World Health Organization. 2020. Available from: https://iris.who.int/handle/10665/334254 Accessed: Aug 02, 2023.
  19. Kloping YP, Hidayatullah F, Rahman ZA, Chung E, Hakim L. Male reproductive tract involvement and sperm parameters in SARS-CoV-2 patients: A systematic review and meta-analysis. World J Men’s Health. 2022;41:538–557. doi: 10.5534/wjmh.220019
  20. Malki MI. COVID-19 and male infertility: An overview of the disease. Medicine (Baltimore). 2022;101(27):e29401. doi: 10.1097/MD.0000000000029401
  21. Skytthe MK, Graversen JH, Moestrup SK. Targeting of CD163+ macrophages in inflammatory and malignant diseases. Int J Mol Sci. 2020;21(15):5497. doi: 10.3390/ijms21155497
  22. Strizova Z, Benesova I, Bartolini R. M1/M2 macrophages and their overlaps — myth or reality? Clin Sci (Lond). 2023;137(15):1067–1093. doi: 10.1042/CS20220531
  23. Shi X, Zhao H, Kang Y. The role of mononuclear phagocytes in the testes and epididymis. Int J Mol Sci. 2022;24(1):53. doi: 10.3390/ijms24010053
  24. Matzkin ME, Calandra RS, Rossi SP, Bartke A, Frungieri MB. Hallmarks of testicular aging: The challenge of anti-inflammatory and antioxidant therapies using natural and/or pharmacological compounds to improve the physiopathological status of the aged male gonad. Cells. 2021;10(11):3114. doi: 10.3390/cells10113114

Supplementary files

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1. JATS XML
2. Fig. 1. Morphological picture of the testicle of a patient with confirmed new coronavirus infection. Hematoxylin and eosin staining: a — magnification ×200; b — magnification ×400

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3. Fig. 2. Immunohistochemical study of the testicles of patients with COVID-19, staining with hematoxylin, magnification ×400

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