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Андрология и генитальная хирургия. 2022; 23: 30-36

Хемилюминесцентный анализ свободнорадикальных процессов в семенной плазме мужчин с патоспермией, перенесших инфекцию COVID-19

Курашова Н. А., Дашиев Б. Г., Гребенкина Л. А., Колесников С. И., Колесникова Л. И.

https://doi.org/10.17650/1726-9784-2022-23-1-30-36

Аннотация

Введение. В условиях пандемии COVID-19 актуальным представляется исследование клинических особенностей и влияния вируса SARS-CoV-2 на репродуктивную систему и фертильность мужчин.
Цель – оценить интенсивность окислительных процессов в семенной плазме мужчин с патозооспермией после перенесенной инфекции COVID-19.
Материалы и методы. Параметры спермограммы оценены в соответствии с критериями руководства Всемирной организации здравоохранения 2010 г. (5-е издание) по исследованию и обработке эякулята человека через 2–3 мес после получения пациентом отрицательного результата полимеразной цепной реакции назофарингеального мазка на ДНК вируса SARS-CoV-2. Методом хемилюминесценции, индуцированной ионами двухвалентного железа, исследована интенсивность свободнорадикальных процессов в семенной плазме.
Результаты. Установлено снижение подвижности сперматозоидов и повышение количества лейкоцитов у мужчин с патозооспермией, перенесших инфекцию COVID-19. Наблюдаются более низкие уровни таких показателей, как объем эякулята, общая концентрация сперматозоидов и количество морфологически нормальных форм сперматозоидов. Выявлена повышенная способность к генерации активных форм кислорода в семенной плазме при патозооспермии и COVID-19.
Выводы. Полученные результаты свидетельствуют о том, что SARS-CoV-2 влияет на мужскую половую систему прямым или косвенным образом и оказывает негативное воздействие на мужское репродуктивное здоровье, вызывая активацию процессов липопероксидации и сперматогенную недостаточность.

Список литературы

1. Курашова Н.А. Оценка репродуктивного потенциала мужского населения. Бюллетень Восточно-Сибирского научного центра Сибирского отделения Российской академии медицинских наук 2014;2(96):104–9. [Kurashova N.A. Assessment of reproduotive potential of men. Bjulletenʼ Vostochno-Sibirskogo nauchnogo centra Sibirskogo otdelenija Rossijskoj akademii medicinskih nauk = Bulletin of the East Siberian Scientific Center of the Siberian Branch of the Russian Academy of Medical Sciences 2014;2(96);104–9. (In Russ.)].

2. Velez D., Ohlander S., Niederberger C. Pyospermia: background and controversies. F S Rep 2021;2(1):2–6. DOI: 10.1016/j.xfre.2021.01.001.

3. Kolesnikova L.I., Kurashova N.A., Dolgikh M.I. et al. Parameters of proand antioxidant status in ejaculate of men of fertile age. Bull Exp Biol Med 2015;159(6):726–8. DOI: 10.1007/s10517-015-3059-6.

4. Kolesnikova L.I., Kurashova N.A., Bairova T.A. et al. Features of lipoperoxidation, antioxidant defense, and thiol/disulfide system in the pathogenesis of infertility in males, carriers of nonfunctional variants of GSTT1 and GSTM1 gene polymorphisms. Bull Exp Biol Med 2017;163(3):378–80. DOI: 10.1007/s10517-017-3808-9.

5. Seymen C.M. The other side of COVID-19 pandemic: Effects on male fertility. J Med Virol 2021;93(3):1396– 1402. DOI: 10.1002/jmv.26667.

6. Брагина Е.Е. Вирусное инфицирование сперматозоидов. Часть 2. Герпесвирусы человека, вирус иммунодефицита человека, вирус гепатита С, вирус Зика (обзор литературы). Андрология и генитальная хирургия 2020;21(4):20–30. [Bragina E.E.Viral infection of sperm. Part 2. Human herpes viruses, human immunodeficiency virus, hepatitis C virus, Zika virus (review). Andrologiya i genitalʼnaja khirurgija = Andrology and Genital Surgery 2020;21(4):20–30. (In Russ.)]. DOI: 10.17650/2070-9781-2020-21-4- 20-30.

7. Sheikhzadeh Hesari F., Hosseinzadeh S.S., Asl Monadi Sardroud M.A. Review of COVID-19 and male genital tract. Andrologia 2021;53(1):e13914. DOI: 10.1111/and.13914.

8. Сорокина Т.М., Брагина Е.Е., Сорокина Е.А. и др. Влияние перенесенной инфекции COVID-19 на спермиологические показатели мужчин с нарушением фертильности. Андрология и генитальная хирургия 2021;22(3): 25–33. [Sorokina T.M., Bragina E.E., Sorokina E.A. et al. Effect of COVID-19 infection on characteristics of sperm in men with impaired fertility. Andrologiya i genitalʼnaja khirurgija = Andrology and Genital Surgery 2021;22(3):25–33. (In Russ.)]. DOI 10.17650/1726-9784-2021-22-3-25-33.

9. Darbandi M., Darbandi S., Agarwal A. et al. Reactive oxygen species-induced alterations in H19-Igf2 methylation patterns, seminal plasma metabolites, and semen quality. J Assist Reprod Genet 2019;36(2):241–53. DOI: 10.1007/s10815-018-1350-y.

10. Darenskaya M., Kolesnikova L., Kolesnikov S. The association of respiratory viruses with oxidative stress and antioxidants. Implications for the COVID-19 pandemic. Curr Pharm Des 2021;27(13):1618–27. DOI: 10.2174/1381612827666210222113351.

11. Agarwal A., Durairajanayagam D., Halabi J. et al. Proteomics, oxidative stress and male infertility. Reprod Biomed Online 2014;29(1):32–58. DOI: 10.1016/j.rbmo.2014.02.013.

12. Владимиров Ю.А., Проскурнина Е.В., Измайлов Д.Ю. Кинетическая хемилюминесценция как метод изучения реакций свободных радикалов. Биофизика 2011;56(6):1081–90. [Vladimirov Yu.A., Proskurnina E.V., Izmaylov D.Yu. Kinetic chemiluminescence as a method for studying the reactions of free radicals. Biofizika = Biophysics 2011;56(6):1081–90. (In Russ.)].

13. Кривохижина Л.В., Ермолаева Е.Н., Сурина-Марышева Е.Ф. и др. Хемилюминесценция сыворотки при физических нагрузках различной интенсивности. Здоровье и образование в XXI веке 2016;18(2):542–7. [Krivohizhina L.V., Ermolaeva E.N., Surina-Marysheva E.F. et al. Serum chemiluminescence during physical activity of varying intensity. Zdorovʼe i obrazovanie v XXI veke = Health and education in the XXI century. 2016;18(2):542–7. (In Russ.)].

14. Piskarev I.M., Ivanova I.P. Assessment of oxidative and antioxidant capacity of biological substrates by chemiluminescence induced by fenton reaction. Sovremennye tehnologii v medicine 2016;8(3):16–26. DOI: 10.17691/stm2016.8.3.02.

15. Hamdi S., Bendayan M., Huyghe E. et al. COVID-19 and andrology: Recommendations of the Frenchspeaking society of andrology (Société d’Andrologie de langue Française SALF). Basic Clin Androl 2020;30:10. DOI: 10.1186/s12610-020-00106-4.

16. Liu X., Chen Y., Tang W. et al. Single-cell transcriptome analysis of the novel coronavirus (SARS-CoV-2) associated gene ACE2 expression in normal and non-obstructive azoospermia (NOA) human male testes. Sci China Life Sci 2020;63:1006–15. DOI: 10.1007/s11427-020-1705-0.

17. Sengupta P., Leisegang K., Agarwal A. The impact of COVID-19 on the male reproductive tract and fertility: A systematic review. Arab J Urol 2021;19(3):423–36. DOI: 10.1080/2090598X.2021.1955554.

18. Vessey W., Perez-Miranda A., Macfarquhar R. et al. Reactive oxygen species in human semen: validation and qualification of a chemiluminescence assay. Fertil Steril 2014;102(6):1576–83.e4. DOI: 10.1016/j.fertnstert.2014.09.009.

19. Azadi L., Tavalaee M., Deemeh M.R. et al. Effects of Tempol and Quercetin on Human Sperm Function after Cryopreservation. Cryo Letters 2017;38(1):29–36.

20. Agarwal A., Ahmad G., Sharma R. Reference values of reactive oxygen species in seminal ejaculates using chemiluminescence assay. J Assist Reprod Genet 2015;32(12):1721–9. DOI: 10.1007/s10815-015-0584-1.

21. Kulchenko N., Pashina N. Association of leukocyte activity and DNA fragmentation in men with nonobstructive azoospermia. Georgian Med News 2020;(299):26–9.

22. Sánchez V., Redmann K., Wistuba J. et al. Oxidative DNA damage in human sperm can be detected by Raman microspectroscopy. Fertil Steril 2012;98(5):1124-9.e1-3. DOI: 10.1016/j.fertnstert.2012.07.1059.

23. Massarotti C., Garolla A., Maccarini E. et al. SARS-CoV-2 in the semen: Where does it come from? Andrology 2021;9(1):39–41. DOI: 10.1111/andr.12839.

24. Li H., Xiao X., Zhang J. et al. Impaired spermatogenesis in COVID-19 patients. EClinicalMedicine 2020;28:100604. DOI: 10.1016/j.eclinm.2020.100604.

Andrology and Genital Surgery. 2022; 23: 30-36

Chemiluminescence analysis of free radical processes in seminal plasma of men with pathospermia who have undergone COVID-19 infection

Kurashova N. A., Dashiev B. G., Grebenkina L. A., Kolesnikov S. I., Kolesnikova L. I.

https://doi.org/10.17650/1726-9784-2022-23-1-30-36

Abstract

Introduction. In the context of the COVID-19 pandemic, it seems relevant to study the clinical features and the effect of the SARS-CoV-2 virus on the reproductive system and male fertility.
The study objective was to assess the intensity of oxidative processes in the seminal plasma of men with pathozoospermia after suffering a COVID-19 infection.
Materials and methods. Spermogram parameters were assessed in accordance with the criteria of the 2010 WHO Guidelines, 5th edition, for the study and processing of human ejaculate two to three months after the patient received a negative polymerase chain reaction result of a nasopharyngeal swab for SARS-CoV-2 DNA. The intensity of free radical processes in seminal plasma was investigated by the method of chemiluminescence induced by ions of bivalent iron.
Results. A decrease in sperm motility and an increase in the number of leukocytes were found in men with pathozoospermia who had undergone COVID-19 infection. There are lower levels of indicators such as ejaculate volume, total sperm concentration and the number of morphologically normal sperm forms. An increased ability to generate reactive oxygen species in seminal plasma was revealed in pathozoospermia and COVID-19.
Conclusions. The results obtained indicate that SARS-CoV-2 affects the male reproductive system directly or indirectly and has a negative effect on male reproductive health, causing the activation of lipid peroxidation processes and spermatogenic insufficiency.

References

1. Kurashova N.A. Otsenka reproduktivnogo potentsiala muzhskogo naseleniya. Byulleten' Vostochno-Sibirskogo nauchnogo tsentra Sibirskogo otdeleniya Rossiiskoi akademii meditsinskikh nauk 2014;2(96):104–9. [Kurashova N.A. Assessment of reproduotive potential of men. Bjulletenʼ Vostochno-Sibirskogo nauchnogo centra Sibirskogo otdelenija Rossijskoj akademii medicinskih nauk = Bulletin of the East Siberian Scientific Center of the Siberian Branch of the Russian Academy of Medical Sciences 2014;2(96);104–9. (In Russ.)].

2. Velez D., Ohlander S., Niederberger C. Pyospermia: background and controversies. F S Rep 2021;2(1):2–6. DOI: 10.1016/j.xfre.2021.01.001.

3. Kolesnikova L.I., Kurashova N.A., Dolgikh M.I. et al. Parameters of proand antioxidant status in ejaculate of men of fertile age. Bull Exp Biol Med 2015;159(6):726–8. DOI: 10.1007/s10517-015-3059-6.

4. Kolesnikova L.I., Kurashova N.A., Bairova T.A. et al. Features of lipoperoxidation, antioxidant defense, and thiol/disulfide system in the pathogenesis of infertility in males, carriers of nonfunctional variants of GSTT1 and GSTM1 gene polymorphisms. Bull Exp Biol Med 2017;163(3):378–80. DOI: 10.1007/s10517-017-3808-9.

5. Seymen C.M. The other side of COVID-19 pandemic: Effects on male fertility. J Med Virol 2021;93(3):1396– 1402. DOI: 10.1002/jmv.26667.

6. Bragina E.E. Virusnoe infitsirovanie spermatozoidov. Chast' 2. Gerpesvirusy cheloveka, virus immunodefitsita cheloveka, virus gepatita S, virus Zika (obzor literatury). Andrologiya i genital'naya khirurgiya 2020;21(4):20–30. [Bragina E.E.Viral infection of sperm. Part 2. Human herpes viruses, human immunodeficiency virus, hepatitis C virus, Zika virus (review). Andrologiya i genitalʼnaja khirurgija = Andrology and Genital Surgery 2020;21(4):20–30. (In Russ.)]. DOI: 10.17650/2070-9781-2020-21-4- 20-30.

7. Sheikhzadeh Hesari F., Hosseinzadeh S.S., Asl Monadi Sardroud M.A. Review of COVID-19 and male genital tract. Andrologia 2021;53(1):e13914. DOI: 10.1111/and.13914.

8. Sorokina T.M., Bragina E.E., Sorokina E.A. i dr. Vliyanie perenesennoi infektsii COVID-19 na spermiologicheskie pokazateli muzhchin s narusheniem fertil'nosti. Andrologiya i genital'naya khirurgiya 2021;22(3): 25–33. [Sorokina T.M., Bragina E.E., Sorokina E.A. et al. Effect of COVID-19 infection on characteristics of sperm in men with impaired fertility. Andrologiya i genitalʼnaja khirurgija = Andrology and Genital Surgery 2021;22(3):25–33. (In Russ.)]. DOI 10.17650/1726-9784-2021-22-3-25-33.

9. Darbandi M., Darbandi S., Agarwal A. et al. Reactive oxygen species-induced alterations in H19-Igf2 methylation patterns, seminal plasma metabolites, and semen quality. J Assist Reprod Genet 2019;36(2):241–53. DOI: 10.1007/s10815-018-1350-y.

10. Darenskaya M., Kolesnikova L., Kolesnikov S. The association of respiratory viruses with oxidative stress and antioxidants. Implications for the COVID-19 pandemic. Curr Pharm Des 2021;27(13):1618–27. DOI: 10.2174/1381612827666210222113351.

11. Agarwal A., Durairajanayagam D., Halabi J. et al. Proteomics, oxidative stress and male infertility. Reprod Biomed Online 2014;29(1):32–58. DOI: 10.1016/j.rbmo.2014.02.013.

12. Vladimirov Yu.A., Proskurnina E.V., Izmailov D.Yu. Kineticheskaya khemilyuminestsentsiya kak metod izucheniya reaktsii svobodnykh radikalov. Biofizika 2011;56(6):1081–90. [Vladimirov Yu.A., Proskurnina E.V., Izmaylov D.Yu. Kinetic chemiluminescence as a method for studying the reactions of free radicals. Biofizika = Biophysics 2011;56(6):1081–90. (In Russ.)].

13. Krivokhizhina L.V., Ermolaeva E.N., Surina-Marysheva E.F. i dr. Khemilyuminestsentsiya syvorotki pri fizicheskikh nagruzkakh razlichnoi intensivnosti. Zdorov'e i obrazovanie v XXI veke 2016;18(2):542–7. [Krivohizhina L.V., Ermolaeva E.N., Surina-Marysheva E.F. et al. Serum chemiluminescence during physical activity of varying intensity. Zdorovʼe i obrazovanie v XXI veke = Health and education in the XXI century. 2016;18(2):542–7. (In Russ.)].

14. Piskarev I.M., Ivanova I.P. Assessment of oxidative and antioxidant capacity of biological substrates by chemiluminescence induced by fenton reaction. Sovremennye tehnologii v medicine 2016;8(3):16–26. DOI: 10.17691/stm2016.8.3.02.

15. Hamdi S., Bendayan M., Huyghe E. et al. COVID-19 and andrology: Recommendations of the Frenchspeaking society of andrology (Société d’Andrologie de langue Française SALF). Basic Clin Androl 2020;30:10. DOI: 10.1186/s12610-020-00106-4.

16. Liu X., Chen Y., Tang W. et al. Single-cell transcriptome analysis of the novel coronavirus (SARS-CoV-2) associated gene ACE2 expression in normal and non-obstructive azoospermia (NOA) human male testes. Sci China Life Sci 2020;63:1006–15. DOI: 10.1007/s11427-020-1705-0.

17. Sengupta P., Leisegang K., Agarwal A. The impact of COVID-19 on the male reproductive tract and fertility: A systematic review. Arab J Urol 2021;19(3):423–36. DOI: 10.1080/2090598X.2021.1955554.

18. Vessey W., Perez-Miranda A., Macfarquhar R. et al. Reactive oxygen species in human semen: validation and qualification of a chemiluminescence assay. Fertil Steril 2014;102(6):1576–83.e4. DOI: 10.1016/j.fertnstert.2014.09.009.

19. Azadi L., Tavalaee M., Deemeh M.R. et al. Effects of Tempol and Quercetin on Human Sperm Function after Cryopreservation. Cryo Letters 2017;38(1):29–36.

20. Agarwal A., Ahmad G., Sharma R. Reference values of reactive oxygen species in seminal ejaculates using chemiluminescence assay. J Assist Reprod Genet 2015;32(12):1721–9. DOI: 10.1007/s10815-015-0584-1.

21. Kulchenko N., Pashina N. Association of leukocyte activity and DNA fragmentation in men with nonobstructive azoospermia. Georgian Med News 2020;(299):26–9.

22. Sánchez V., Redmann K., Wistuba J. et al. Oxidative DNA damage in human sperm can be detected by Raman microspectroscopy. Fertil Steril 2012;98(5):1124-9.e1-3. DOI: 10.1016/j.fertnstert.2012.07.1059.

23. Massarotti C., Garolla A., Maccarini E. et al. SARS-CoV-2 in the semen: Where does it come from? Andrology 2021;9(1):39–41. DOI: 10.1111/andr.12839.

24. Li H., Xiao X., Zhang J. et al. Impaired spermatogenesis in COVID-19 patients. EClinicalMedicine 2020;28:100604. DOI: 10.1016/j.eclinm.2020.100604.