Россия
Россия
УДК 591.16 Размножение. Развитие. Оплодотворение
УДК 612 Физиология. Сравнительная физиология
Факторы окружающей среды, в том числе радиационной природы, могут оказывать неблагоприятное воздействие на мужское репродуктивное здоровье, поэтому необходимо своевременно оценивать состояние мужских половых клеток. В настоящее время существует настоятельная необходимость в поиске адекватных показателей и методов для оценки качества мужских гамет. Одним из таких надежных показателей мужской фертильности и качества спермы, который отражает целостность генетического материала, является уровень фрагментации ДНК сперматозоидов. В статье с использованием данных литературы рассмотрены причины, последствия и возможные механизмы, приводящие к фрагментации ДНК сперматозоидов у млекопитающих, а также проанализированы основные методы их детекции. Показана диагностическая значимость определения нарушений структуры хроматина при анализе мужского бесплодия и приведены результаты, полученные авторами, которые свидетельствуют о высокой чувствительности SCD-теста (анализ дисперсии хроматина сперматозоидов) при изучении фрагментации ДНК сперматозоидов у полевок-экономок (Alexandromys oeconomus Pall.) в условиях хронического воздействия ионизирующего излучения (доза 40 сГр). Таким образом, данные литературы и полученные нами результаты показали, что уровень фрагментации ДНК сперматозоидов является надежным биомаркером мужской фертильности, а SCD-тест может быть рекомендован в качестве чувствительного метода для оценки состояние мужских половых клеток в радиобиологических исследованиях.
сперматозоиды, фрагментация ДНК, методы детекции, SCD-тест, полевки-экономки, ионизирующее излучение
1. Paternal influence of sperm DNA integrity on early embryonic development / L. Simon, K. Murphy, M. B. Shamsi [et al.] // Human Reproduction. – 2014. – Vol. 29, № 11. – Р. 2402–2412. – DOI:https://doi.org/10.1093/humrep/deu228
2. Investigation on the origin of sperm morphological defects: oxidative attacks, chromatin immaturity, and DNA fragmentation / A. Oumaima, A. Tesnim, H. Zohra [et al.] // Environmental Science and Pollution Research. – 2018. – Vol. 25. – Р. 13775–13786. – DOI:https://doi.org/10.1007/s11356-018-1417-4
3. ДНК фрагментация сперматозоидов при бесплодии. Обзор литературы / Л. К. Айткожина, Т. К. Кудайбергенов, Х. М. Бикташева [и др.] // Проблемы репродукции. – 2019. – Т. 1, № 38. – С. 25–29.
4. Javed, A. Evaluation of sperm DNA fragmentation using multiple methods: a comparison of their predictive power for male infertility / A. Javed, M. S. Talkad, M. K. Ramaiah // Clinical and Experimental Reproductive Medicine. – 2019. – Vol. 46, № 1. – P. 14–21. – DOI:https://doi.org/10.5653/cerm.2019.46.1.14
5. Структурные нарушения хроматина сперматозоидов. Патофизиологические аспекты. Клиническая значимость / М. Н. Коршунов, Е. С. Коршунова, П. С. Кызласов [и др.] // Вестник урологии. – 2021. – № 9. – С. 95–104. –DOI:https://doi.org/10.21886/2308-6424-2021-9-1-95-104
6. Sperm DNA fragmentation: unraveling its imperative impact on male infertility based on recent evidence / S. Stavros, A. Potiris, E. Molopodi [et al.] // International Journal of Molecular Sciences. – 2024. – Vol. 25. – Р. 1–13. – DOI:https://doi.org/10.3390/ijms251810167
7. Авадиева, Н. Э. Применение ДНК фрагментации спермы в андрологической практике / Н. Э. Авадиева // Вестник урологии. – 2019. – Т. 7, № 1. – С. 7–11. – DOI:https://doi.org/10.21886/2308-6424-2019-7-1-7-11
8. Sperm DNA fragmentation: a new guideline for clinicians / A. Agarwal, A. Majzoub, S. Baskaran [et al.] // World Journal in Mens Health. – 2020. – Vol. 38. – P. 412–471. – DOI:https://doi.org/10.5534/wjmh.200128
9. Oxidative stress and male reproductive health / R. J. Aitken, T. B. Smith, M. S. Jobling [et al.] //Asian Journal of Andrology. – 2014. – Vol. 16, № 1. – Р. 31–38. – DOI:https://doi.org/10.4103/1008-682X.122203
10. Measuring sperm DNA fragmentation and clinical outcomes of medically assisted reproduction: a systematic review and meta-analysis / M. Cissen, M. van Wely, I. Scholten [et al.] // PLoS One. – 2016. – Vol. 11, № 11. – Р. e0165125. – OI:https://doi.org/10.1371/journal.pone.0165125
11. WHO laboratory manual for the examination and processing of human semen // World Health Organization : [website]. – 2021. – 27 July. – URL: https://www.who.int/publications/i/item/9789240030787
12. Makhlouf, A. A. DNA integrity tests in clinical practice: it is not a simple matter of black and white (or red and green) / A. A. Makhlouf, C. Niederberger // Journal of Andrology. – 2006. – Vol. 27. – P. 316–323. – DOI:https://doi.org/10.2164/jandrol.05217
13. Фрагментация ДНК сперматозоидов: связь с параметрами сперматогенеза у молодых мужчин / Л. В. Осадчук, Д. А. Татару, Н. Н. Кузнецова [и др.] // Урология. – 2016. – № 6. – С. 118–123.
14. Cho, C. L. Role of sperm DNA fragmentation in male factor infertility: a systematic review / C. L. Cho, A. Agarwal // Arab Journal of Urology. – 2017. – Vol. 16, № 1. – Р. 21–34. – DOI:https://doi.org/10.1016/j.aju.2017.11.002
15. Comparison of chromatin assays for DNA fragmentation evaluation in human sperm / K. R. Chohan, J. T. Griffin, M. Lafromboise [et al.] // Journal of Andrology. – 2006. – Vol. 27. – Р. 53–59. – DOI:https://doi.org/10.2164/jandrol.05068
16. Comprehensive analysis of sperm DNA fragmentation by five different assays: TUNEL assay, SCSA, SCD test and alkaline and neutral Comet assay / J. Ribas-Maynou, A. García-Peiro, A. Fernandez-Encinas [et al.] // Andrology. – 2013. – Vol. 1, № 5. – P. 715–722. – DOI:https://doi.org/10.1111/j.2047-2927.2013.00111.x
17. Evenson, D. P. The Sperm Chromatin Structure Assay (SCSA®) and other sperm DNA fragmentation tests for evaluation of sperm nuclear DNA integrity as related to fertility / D. P. Evenson // Animal Reproduction Science. – 2016. – Vol. 169. – Р. 56–75. – Р. 1–20. – DOI:https://doi.org/10.1016/j.anireprosc
18. Sperm Chromatin Structure Assay (SCSA®) and flow cytometry-assisted TUNEL assay provide a concordant assessment of sperm DNA fragmentation as a function of age in a large cohort of approximately 10,000 patients / P. Behdarvandian, A. Nasr-Esfahani, M. Tavalaee [et al.] // Basic and Clinical Andrology. – 2023. – Vol. 33, № 33. – Р. 1–11. – DOI:https://doi.org/10.1186/s12610-023-00208-9
19. Нарушения структуры хроматина сперматозоидов: клиническое значение, причины, диагностика, лечение (обзор литературы) / В. А. Божедомов, И. В. Виноградов, Н. А. Липатова [и др.] // Проблемы репродукции. – 2012. – № 5. – С. 76–84.
20. Evenson, D. P. Evaluation of sperm chromatin structure and DNA strand breaks is an important part of clinical male fertility assessment / D. P. Evenson // Translational Andrology and Urology. – 2017. – Vol. 6, № 4. – Р. 495–500. –DOI:https://doi.org/10.21037/tau.2017.07.20
21. Мужское бесплодие и нарушение структурной организации хроматина сперматозоидов. Существует ли связь? / О. А. Воробьева, А. В. Воскресенская, А. А. Одинцов [и др.] // Проблемы репродукции. – 2005. – № 6. – С. 56–62.
22. Feijó, C. M. Diagnostic accuracy of sperm chromatin dispersion test to evaluate sperm deoxyribonucleic acid damage in men with unexplained infertility / C. M. Feijó, S. C. Esteves // Fertility and Sterility. –2014. – Vol. 101, № 1. – P. 58–63. – DOI:https://doi.org/10.1016/j.fertnstert.2013.09.002
23. Фрагментация ДНК сперматозоидов: клиническая значимость, причины, методы оценки и коррекции / С. Ю. Боровец, В. А. Егорова, А. М. Гзгзян [и др.] // Урологические ведомости. – 2020. – Т. 10, № 2. – С. 173–180. – DOI:https://doi.org/10.17816/uroved102173-180
24. Relationship between varicocele and sperm DNA damage and the effect of varicocele repair: a meta-analysis / Y. J. Wang, R. Q. Zhang, Y. J. Lin [et al.] // Reproductive BioMedicine Online. – 2012. – Vol. 25, №. 3. – Р. 307–314. – DOI:https://doi.org/10.1016/j.rbmo.2012.05.002
25. Application of the comet assay for the evaluation of DNA damage in mature sperm / G. Gajski, S. Ravlić, R. Godschalk [et al.] // Mutation Research. – 2021. – Vol. 788. – Р. 1–20. – DOI:https://doi.org/10.1016/j.mrrev.2021.108398
26. The spectrum of DNA damage in human sperms assessed by single cell gel electrophoresis (Comet assay) and its relationship to fertilization and embryo development / I. D. Morris, S. Ilott, L. Dixon [et al.] // Human Reproduction. – 2002. – № 17. – P. 990–998. – DOIhttps://doi.org/10.1093/humrep/17.4.990
27. Effects of cryopreservation on sperm quality, nuclear DNA integrity, in vitro fertilization, and in vitro embryo development in the mouse / C. Yildiz, P. Ottaviani, N. Law [et al.] // Reproduction. – 2007. – Vol. 133. – P. 585–595. – DOIhttps://doi.org/10.1530/REP-06-0256
28. Gosalvez, J. Sperm chromatin dispersion (SCD) test: technical aspects and clinical applications / J. Gosalvez, C. Lopez-Fernandez, J. L. Fernandez // In: A. Zini, A. Agarwal, editors. Sperm DNA damage: biological and clinical applications in male infertility and assisted reproduction. – New York : Springer US, 2011. – Р. 151–170.
29. Sperm DNA damage output parameters measured by the alkaline Comet assay and their importance /L. Simon, K. I. Aston, B. R. Emery [et al.] // Andrologia. –2016. – Vol. 49, № 2. – Р. 1–12. – DOI:https://doi.org/10.1111/and.12608
30. Hamilton, T. R. S. Sperm DNA fragmentation: causes and identification / T. R. S. Hamilton, M. E. O. D. Assumpçао // Zygote. – 2019. – Vol. 28, Iss. 1. – Р. 1–8. – DOI:https://doi.org/10.1017/S0967199419000595
31. Li, Ming-Wen. DNA fragmentation index (DFI) as a measure of sperm quality and fertility in mice / Ming-Wen Li, K. C. K. Lloyd // Scientific Reports. – 2020. – Vol. 10, № 3833. – P. 1–11. – DOI:https://doi.org/10.1038/s41598-020-60876-9
32. Pregnancy prediction by free sperm DNA and sperm DNA fragmentation in semen specimens of IVF/ICSI-ET patients / T. Bounartzi, K. Dafopoulos, G. Anifandis [et al.] // Human Fertility. – 2016. – Vol. 19, № 1. – P. 56–62. – DOI:https://doi.org/10.3109/14647273.2016.115762919
33. Коршунов, М. Н. Прогностическая ценность показателя ДНК-фрагментации сперматозоидов в успехе программ вспомогательных репродуктивных технологий / М. Н. Коршунов, Е. С. Коршунова, С. П. Даренков. – Экспериментальная и клиническая урология. – 2017. – № 3. – С. 70–76.
34. DNA fragmentation of normal spermatozoa negatively impacts embryo quality and intracytoplasmic sperm injection outcome / C. Avendanо, A. Franchi, H. Duran [et al.] // Fertility and Sterility. – 2010. – Vol. 94, № 2. – P. 549–557. – DOI:https://doi.org/10.1016/j.fertnstert.2009.02.050
35. Результаты преимплантационного генетического скрининга эмбрионов у супружеских пар с фрагментацией ДНК сперматозоидов / Ю. Ю. Киселева, М. М. Азова, Т. А. Кодылева [и др.] // Акушерство и гинекология. – 2017. – № 8. – С. 104–108. – DOI:https://doi.org/10.18565/aig.2017.8.104-8
36. Sperm DNA fragmentation: mechanisms of origin / M. Muratori, S. Marchiani, L. Tamburrino [et al.] // Genetic Damage in Human Spermatozoa. Advances in Experimental Medicine and Biology. – 2019. – Vol. 1166. – P. 78–85. – DOI:https://doi.org/10.1007/978-3-030-21664-1_5
37. Simon, L. Sperm DNA fragmentation: consequences for reproduction / L. Simon, B. Emery, D. T. Carrell // Advances in Experimental Medicine and Biology. – 2019. – Vol. 1166. – P. 87–105. – DOI:https://doi.org/10.1007/978-3-030-21664-1_6
38. Relationship between sperm morphology and sperm DNA dispersion / J. Jakubik-Uljasz, K. Gill, A. Rosiak-Gill [et al.] // Translational Andrology and Urology. – 2020. – Vol. 9, № 2. – P. 405–415. – DOI:https://doi.org/10.21037/tau.2020.01.31
39. Епанчинцева, Е. А. Индекс фрагментации ДНК сперматозоидов – необходимость для современной клинической практики / Е. А. Епанчинцева, В. Г. Селятицкая, В. А. Божедомов // Андрология и генитальная хирургия. – 2020. – Т. 21, № 1. – С. 14–21. – DOI: 10.17650 / 2070-9781-2020-21-1-14-21
40. Does sperm DNA fragmentation correlate with semen parameters? / M. T. Le, T. A. T. Nguyen, H. T. T. Nguyen [et al.] // Reproductive Medicine and Biology. – 2019. – Vol. 18. – Р. 390–396. – DOI:https://doi.org/10.1002/rmb2.12297
41. The relationship between isolated teratozoospermia, sperm DNA fragmentation and inflammatory biomarkers: findings from a cross-sectional study / L. Boeri, P. Capogrosso, W. Cazzaniga [et al.] // The Journal of Urology. – 2020. – Vol. 203. – P. e400-e401. – DOI:https://doi.org/10.1097/JU.0000000000000865.03
42. Das, S. K. Effect of sperm DNA fragmentation on blastocyst formation rate and subsequent IVF outcome / S. K. Das, K. Kalita // International Journal of Reproduction, Contraception, Obstetrics and Gynecology. – 2022. – Vol. 11, № 2. – P. 385–390. – DOI: https://doi.org/10.18203/2320-1770.ijrcog20220054
43. Значение индекса ДНК-фрагментации в диагностике мужской инфертильности / Л. В. Батуревич, И. Д. Шилейко, Л. И. Алехнович [и др.] // Лабораторная диагностика. Восточная Европа. – 2022. – Т. 11, № 1. – С. 30–37. – DOI:https://doi.org/10.34883/PI.2022.11.1.013
44. Relationship between spermatogenesis, DNA fragmentation index, and teratozoospermia index / J. M. Budiharto, R. Margiana, W. William [et al.] // International Journal of Health Sciences. – 2022. – Vol. 6, № 3. – Р. 1827–1837. – DOI:https://doi.org/10.53730/ijhs.v6nS3.5808
45. Saghaei, H. Sperm DNA damage in mice irradiated with various doses of X-rays alone or in combination with actinomycin D or bleomycin sulfate: an in vivo study / H. Saghaei, H. Mozdarani, A. Mahmoudzadeh // International Journal of Radiation Research. – 2019. – Vol. 17, № 2. – Р. 317–323. – DOI:https://doi.org/10.18869/acadpub.ijrr.17.2.317
46. Shamsi, M. B. Evaluation of nuclear DNA damage in human spermatozoa in men opting for assisted reproduction / M. B. Shamsi, R. Kumar, R. Dada // Indian Journal of Medical Research. – 2008. – Vol. 127, № 2. – Р. 115–123.
47. Zeng, F. Transcript profiling during preimplantation mouse development / F. Zeng, D. A. Baldwin, R. M. Schultz // Developmental Biology. – 2004. – Vol. – 272, № 2. – Р. 483–496. – DOI:https://doi.org/10.1016/j.ydbio.2004.05.018
48. Impact of radio frequency electromagnetic radiation on DNA integrity in the male germline / R. J. Aitken, L. E. Bennetts, D. Sawyer [et al.] // International Journal of Andrology. – 2005. – Vol. 28, № 3. – Р. 171–179. – DOI:https://doi.org/10.1111/j.1365-2605.2005.00531.x
49. Effect of ionizing radiation on the male reproductive system / A. Wdowiak, M. Skrzypek, M. Stec [et al.] // Annals of Agricultural and Environmental Medicine. – 2019. – Vol. 26, № 2. – Р. 210–216. – DOI:https://doi.org/10.26444/aaem/106085
50. Cho, C. L. Novel insights into the pathophysiology of varicocele and its association with reactive oxygen species and sperm DNA fragmentation / C. L. Cho, S. C. Esteves, A. Agarwal // Asian Journal of Andrology. – 2016. – Vol. 8. – P. 186–193. – DOI:https://doi.org/10.4103/1008-682X.170441
51. Oxidative stress status and sperm DNA fragmentation in fertile and infertile men / M. Dorostghoal, S. R. Kazeminejad, N. Shahbazian [et al.] // Andrologia. – 2017. – Vol. 49, № 10. – DOI:https://doi.org/10.1111/and.12762
52. Role of oxidative stress, infection and inflammation in male infertility / A. Agarwal, M. Rana, E. Qiu [et al.] // Andrologia. – 2018. – Vol. 50, № 11. – e13126. – DOI:https://doi.org/10.1111/and.13126
53. Barazani, Y. Functional sperm testing and the role of proteomics in the evaluation of male infertility / Y. Barazani, A. Agrawal, E. S. Jr. Sabanegh // Urology. – 2014. – Vol. 84, № 2. – Р. 255–261. – DOI:https://doi.org/10.1016/j.urology.2014.04.043
54. Agarwal, A. Role of sperm chromatin abnormalities and DNA damage in male infertility / A. Agarwal, T. M. Said // Human Reproduction Update – 2003. – Vol. 9. – P. 331–345. – DOI: /10.1093/humupd/dmg027
55. Aitken, R. J. On the possible origins of DNA damage in human spermatozoa / R. J. Aitken, G. N. De Iuliis // Molecular Human Reproduction. – 2010. – Vol. 16, № 1. – Р. 3–13. – DOI:https://doi.org/10.1093/molehr/gap059
56. Expression of Bcl-2 family proteins and spontaneous apoptosis in normal human testis / N. B. Oldereid, P. D. Angelis, R. Wiger [et al.] // Molecular Human Reproduction. – 2001. – Vol. 7, № 5. – Р. 403–408. – DOI:https://doi.org/10.1093/molehr/7.5.403
57. DNA damage and repair in human reproductive cells / A. García-Rodríguez, J. Gosálvez, A. Agarwal [et al.] // International Journal of Molecular Sciences. – 2018. – Vol. 20, № 1. – Р. 1–22. – DOI:https://doi.org/10.3390/ijms20010031
58. Society for translational medicine: clinical practice guidelines for sperm DNA fragmentation testing in male infertility / A. Agarwal, C. L. Cho, A. Majzoub [et al.] // Translational Andrology and Urology – 2017. – Vol. 6. – Р. 720–733. – DOI:https://doi.org/10.21037/tau.2017.08.06
59. Фрагментация ДНК в сперматозоидах и ее взаимосвязь с нарушением сперматогенеза / С. А. Руднева, Е. Е. Брагина, Е. А. Арифулин [и др.] // Андрология и генитальная хирургия. – 2014. – Т. 15, № 4. – С. 26–33. – DOI:https://doi.org/10.17650/2070-9781-2014-4
60. Direct and delayed X-ray-induced DNA damage in male mouse germ cells / E. Cordelli, P. Eleuteri, M. G. Grollino [et al.] // Environmental and Molecular Mutagenesis. – 2012. – Vol. 53, № 6. – Р. 429–439. – DOIhttps://doi.org/10.1002/em.21703
61. DNA and total protamine masses in individual sperm from fertile mammalian subjects / G. S. Bench, A. M. Friz, M. H. Corzett [et al.] // Cytometry. – 1996. – Vol. 23. – № 4. – Р. 263–271. – DOI:https://doi.org/10.1002/(SICI)1097-0320(19960401)23:4<263::AID-CYTO1>3.0.CO;2-I
62. Oliva, R. Proteomics and the genetics of sperm chromatin condensation / R. Oliva, J. Castillo // Asian Journal of Andrology. – 2011. – Vol. 13, № 1. – Р. 24–30. – DOI:https://doi.org/10.1038/aja.2010.65
63. Human sperm chromatin epigenetic potential: genomics, proteomics, and male infertility / J. Castillo, J. M. Estanyol, J. L. Ballescá [et al.] // Asian Journal of Andrology. – 2015. – Vol. 17, № 4. – Р. 601–609. – DOIhttps://doi.org/10.4103/1008-682X.153302
64. Boissonneault, G. Chromatin remodeling during spermiogenesis: a possible role for the transition proteins in DNA strand break repair / G. Boissonneault // FEBS Letters. – 2002. – Vol. 514, № 2–3. – Р. 111–114. – DOI:https://doi.org/10.1016/s0014-5793(02)02380-3
65. Gunes, S. Spermatogenesis, DNA damage and DNA repair mechanisms in male infertility / S. Gunes, M. Al-Sadaan, A. Agarwal // Reprod Biomed Online. – 2015. – Vol. 31, № 3. – Р. 309–319. – DOI:https://doi.org/10.1016/j.rbmo.2015.06.010
66. Santi, D. Sperm DNA fragmentation index as a promising predictive tool for male infertility diagnosis and treatment management – meta-analyses / D. Santi, G. Spaggiari, M. Simoni // Reproductive Biomedicine Online. – 2018. – Vol. 37, № 3. – Р. 315–326. – DOI:https://doi.org/10.1016/j.rbmo.2018.06.023
67. Leem, J. The capacity to repair sperm DNA damage in zygotes is enhanced by inhibiting WIP1 activity / J. Leem, G-Y. Bai, J. S. Oh // Frontiers in Cell and Developmental Biology. – 2022. – Vol. 10. – Р. 841327. – DOI:https://doi.org/10.3389/fcell.2022.841327
68. Setti, A. S. Oocyte ability to repair sperm DNA fragmentation: the impact of maternal age on intracytoplasmic sperm injection outcomes / A. S. Setti, D. P. de A. F. Braga [et al.] // Fertility and Sterility. – 2021. – Vol. 116, № 1. – P. 123–129. – DOI:https://doi.org/10.1016/j.fertnstert.2020.10.045
69. Perspective in the mechanisms for repairing sperm DNA damage / N. Li, H. Wang, S. Zou [et al.] // Reproductive Sciences. – 2025. – Vol. 32. – Р. 41–51. – DOI:https://doi.org/10.1007/s43032-024-01714-5
70. A systematic review and meta-analysis to determine the effect of sperm DNA damage on in vitro fertilization and intracytoplasmic sperm injection outcome / L. Simon, A. Zini, A. Dyachenko [et al.] // Asian Journal of Andrology. – 2017. – Vol. 19, № 1. – Р. 80–90. – DOI:https://doi.org/10.4103/1008-682X.182822
71. Ye, D. Effects of sperm DNA fragmentation on embryo morphokinetic parameters and laboratory outcomes in women of different ages during intracytoplasmic sperm treatment cycles / D. Ye, Z. Ye, H. Zhang // Archives of Gynecology and Obstetrics. – 2025. – Vol. 312, № 1. – Р. 191–196. – DOI:https://doi.org/10.1007/s00404-025-07949-0
72. Clinical relevance of sperm DNA damage in assisted reproduction / N. Tarozzi, D. Bizzaro, C. Flamigni [et al.] // Reproductive BioMedicine Online. – 2007. – Vol. 14, № 6. – Р. 746–757. – DOI:https://doi.org/10.1016/s1472-6483(10)60678-5
73. TUNEL assay and SCSA determine different aspects of sperm DNA damage / R. Henkel, C. F. Hoogendijk, P. J. Bouic [et al.] // Andrologia. – 2010. – Vol. 42, № 5. – P. 305–313. – DOI:https://doi.org/10.1111/j.1439-0272.2009.01002.x
74. Sperm DNA fragmentation: threshold value in male fertility / M. Sergerie, G. Laforest, L. Bujan [et al.] // Human Reproduction. – 2005. – Vol. 20, № 12. – Р. 3446–3451. – DOI:https://doi.org/10.1093/humrep/dei231
75. A simple technique for quantitation of low levels of DNA damage in individual cells / N. P. Singh, M. T. McCoy, R. R. Tice [et al.] // Experimental Cell Research. – 1988. – Vol. 175, № 1. – Р. 184–191. – DOI:https://doi.org/10.1016/0014-4827(88)90265-0
76. Ostling, O. Microelectrophoretic study of radiation-induced DNA damages in individual mammalian cells / O. Ostling, K. J. Johanson // Biochemical and Biophysical Research Communications. – 1984. – Vol. 123, № 1. – Р. 291–298. – DOI:https://doi.org/10.1016/0006-291X(84)90411-X
77. Simon, L. Sperm DNA damage measured by comet assay / L. Simon, D. T. Carrell // Spermatogenesis. Methods in Molecular Biology. – 2013. – Vol. 927. – P. 137–146. – DOI:https://doi.org/10.1007/978-1-62703-038-0_13
78. Analysis of DNA damage in individual cells / P. L. Olive, R. E. Durand, J. P. Banáth [et al.] // Methods in Cell Biology. – 2001. – Vol. 64. – Р. 235–249. – DOI:https://doi.org/10.1016/s0091-679x(01)64016-0
79. Lewis, S. E. Sperm DNA tests as useful adjuncts to semen analysis / S. E. Lewis, I. Agbaje, J. Alvarez // Systems Biology in Reproductive Medicine. – 2008. – Vol. 54, № 3. – Р. 111–125. – DOI:https://doi.org/10.1080/19396360801957739
80. Evenson, D. P. Sperm chromatin structure assay: its clinical use for detecting sperm DNA fragmentation in male infertility and comparisons with other techniques / D. P. Evenson, K. L. Larson, L. K. Jost // Journal of Andrology. – 2002. – Vol. 23. – Р. 25–43. – DOI:https://doi.org/10.1002/j.1939-4640.2002.tb02599.x
81. Evenson, D. Р. Sperm chromatin structure assay is useful for fertility assessment / D. Р. Evenson, L. Jost // Methods in Cell Science. – 2000. – Vol. 22, № 2–3. – Р. 169–189. – DOI:https://doi.org/10.1023/a:1009844109023
82. Schlegel, P. N. Yet another test of sperm chromatin structure / P. N. Schlegel, D. A. Paduch // Fertility and Sterility. – 2005. – Vol. 84, № 4. – Р. 854–859. – DOI:https://doi.org/10.1016/j.fertnstert.2005.04.050
83. Sperm DNA fragmentation decreases the pregnancy rate in an assisted reproductive technique / M. Benchaib, V. Braun, J. Lornage [et al.] // Human Reproduction. – 2003. – Vol. 18, № 5. – Р. 1023–1028. – DOI:https://doi.org/10.1093/humrep/deg228
84. Evenson, D. P. Sperm Chromatin Structure Assay (SCSAR) for fertility assessment / D. P. Evenson // Current Protocols. – 2022. – Vol. 2. – Р. 1–16. – DOI:https://doi.org/10.1002/cpz1.508
85. Sperm DNA damage is associated with an increased risk of pregnancy loss after IVF and ICSI: systematic review and meta-analysis / A. Zini, J. M. Boman, E. Belzile [et al.] // Human Reproduction. – 2008. – Vol. 23. – Р. 2663–2668. – DOI: /10.1093/ humrep/den321
86. The sperm chromatin structure assay as a diagnostic tool in the human fertility clinic / G. B. Boe-Hansen, J. Fedder, A. K. Ersbøll [et al.] // Human Reproduction. – 2006. – Vol. 21, № 6. – Р. 1576–1582. – DOI:https://doi.org/10.1093/humrep/del019
87. Fraser, L. Structural damage to nuclear DNA in mammalian spermatozoa: its evaluation techniques and relationship with male infertility / L. Fraser // Polish Journal of Veterinary Sciences. – 2004. – Vol. 7, № 4. – Р. 311–321.
88. Sperm chromatin status and DNA fragmentation in mouse species with divergent mating systems / C. Agudo-Rios, A. Sanchez-Rodriguez, II. D. Idrovo [et al.] // International Journal of Molecular Sciences. – 2023. – Vol. 24, № 21. – Р. 15954. – DOI:https://doi.org/10.3390/ijms242115954
89. The sperm chromatin dispersion test: a simple method for the determination of sperm DNA fragmentation / J. L. Fernández, L. Muriel, M. T. Rivero [et al.] // Journal of Andrology. – 2003. – Vol. 24, № 1. – Р. 59–66. – DOI:https://doi.org/10.1002/j.1939-4640.2003.tb02641.x
90. Simple determination of human sperm DNA fragmentation with an improved sperm chromatin dispersion test / J. L. Fernandez, L. Muriel, V. Goyanes [et al.] // Fertility and Sterility. – 2005. – Vol. 84. – P. 833–842. – DOI:https://doi.org/10.1016/j.fertnstert.2004.11.089
91. Single sperm selection and DNA fragmentation analysis: The case of MSOME/IMSI / J. Gosálvez, B. Migueles, С. López-Fernández [et al.] // Natural Science. – 2013. – Vol. 5, № 7A. – Р. 7–14. – DOI:https://doi.org/10.4236/ns.2013.57A002
92. Carretero, M. I. Evaluación de la calidad del ADN espermático en camélidos sudamericanos y otras especies domésticas / M. I. Carretero, M. S. Giuliano, D. M. Neild // Spermova. – 2017. – Vol. 1, № 7. – Р. 18–26. – DOIhttps://doi.org/10.18548/aspe/0005.04
93. Characterisation of a subpopulation of sperm with massive nuclear damage, as recognised with the sperm chromatin dispersion test / J. Gosálvez, M. Rodríguez-Predreira, A. Mosquera [et al.] // Andrologia. – 2014. – Vol. 46, № 6. – P. 602–609. – DOI:https://doi.org/10.1111/and.12118
94. Baumgartner, A. The comet assay in male reproductive toxicology / A. Baumgartner, E. Cemeli, D. Anderson // Cell Biology and Toxicology. – 2009. – Vol. 25, № 1. – Р. 81–98. – DOI:https://doi.org/10.1007/s10565-007-9041-y
95. Assessment of sperm deoxyribose nucleic acid fragmentation using sperm chromatin dispersion assay / H. Pratap, S. Y. Hottigoudar, K. S. Nichanahalli [et al.] // Journal of Pharmacol Pharmacother. – 2017. – Vol. 8, № 2. – Р. 45–49. – DOI:https://doi.org/10.4103/jpp.JPP_187_16
96. Sperm chromatin dispersion test in the assessment of DNA fragmentation and aneuploidy in human spermatozoa / A. Balasuriya, B. Speyera, P. Serhalb [et al.] // Reproductive BioMedicine Online. – 2011. – Vol. 22, № 5. – P. 428–436. – DOI:https://doi.org/10.1016/j.rbmo.2011.01.012
97. Esteves, S. C. An update on clinical and surgical interventions to reduce sperm DNA fragmentation in infertile men / S. C. Esteves, D. Santi, M. Simoni // Andrology. – 2020. – Vol. 8, № 1. – Р. 53–81. – DOI:https://doi.org/10.1111/andr.12724
98. Performing a sperm DNA fragmentation test in addition to semen examination based on the WHO criteria can be a more accurate diagnosis of IVF outcomes / T. Okubo, N. Onda, T. Hayashi [et al.] // BMC Urology. – 2023. – Vol. 23, № 78. – P. 1–7. – DOIhttps://doi.org/10.1186/s12894-023-01257-y
99. Evenson, D. P. Sperm Chromatin Structure Assay (SCSA®): evolution from origin to clinical utility / D. P. Evenson // A clinician’s guide to Sperm DNA and chromatin damage. – New York : Springer Science, 2018. – Р. 65–89. – DOI:https://doi.org/10.1007/978-3-319-71815-6_4
100. Sperm DNA fragmentation induced by DNAse I and hydrogen peroxide: an in vitro comparative study among different mammalian species / P. Villani, P. Eleuteri, M. G. Grollino [et al.] // Reproduction. – 2010. – Vol. 140. – Р. 445–452. – DOI:https://doi.org/10.1530/REP-10-0176
101. Dynamics of sperm DNA fragmentation in patients carrying structurally rearranged chromosomes / A. Garcia-Peiro, M. Oliver-Bonet, J. Navarro [et al.] // International Journal of Andrology. – 2011. – Vol. 34. – Р. 546–553. – DOI:https://doi.org/10.1111/j.1365-2605.2011.01153.x



