Main Article Content
Abstract
Highlights:
1. Spermatozoa can be affected by coronavirus disease 2019 (COVID-19) due to a disruption in spermatogenesis, leading to a decline in semen quality.
2. This study compared the semen quality of COVID-19 survivors and those who had not been infected with COVID-19, specifically on the first spermatogenesis cycle following the confirmation of COVID-19 infection.
3. This study is distinctive since no previous research in Indonesia has examined the semen quality parameters, such as the concentration, morphology, motility, and vitality of spermatozoa, in men who had a COVID-19 infection.
Abstract
Semen quality in COVID-19 patients shows inconsistencies and variations. This research was conducted considering that health is the main capital for humans in Indonesia's development, as outlined in Sustainable Development Goal 3. The purpose of this study was to compare the semen quality of COVID-19 survivors with non-COVID-19 men. This study was an analytical observational study with a cross-sectional design. Subjects were selected through consecutive sampling of up to 26 men of childbearing age who met the predetermined criteria. Semen quality assessment using the WHO Semen Analysis Guide 6th edition. Quantitative data were analyzed using SPSS. The data normality test was carried out using the Saphiro-Wilk test. Then, the data were tested by t-test from two unpaired samples and by the Mann-Whitney test. Data from semen analysis based on COVID-19 severity were tested using variant analysis (One-way ANOVA) and the Kruskal Wallis test. The normal morphology of spermatozoa in COVID-19 survivors was significantly lower (p=0.011) compared to uninfected men. Other semen quality parameters did not differ significantly, although they were lower in COVID-19 survivors. The results of the analysis also showed no significant difference in semen parameters related to COVID-19 severity (p=0.488 for progressive motility; p=0.372 for non-progressive motility; p=0.325 for total motility; p=0.707 for immotility; p=0.412 for vitality; p=0.324 for concentration; and p=0.334 for normal morphology). The study provides evidence that COVID-19 survivors have a lower normal spermatozoa morphology compared to uninfected men. However, the motility, vitality, and concentration of spermatozoa did not differ significantly between the two groups.
Keywords
Article Details
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References
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- Agustinus, I’tishom R, Pramesti MD (2018). Male reproductive biology. Airlangga University Press, Surabaya. Available at: https://repository.unair.ac. id/95965/3/Biologi Reproduksi Pria.pdf.
- Boitrelle F, Shah R, Saleh R, et al (2021). The sixth edition of the WHO manual for human semen analysis: A critical review and SWOT analysis. Life 11, 1368. doi: 10.3390/life11121368.
- Cheval S, Mihai Adamescu C, Georgiadis T, et al (2020). Observed and potential impacts of the covid-19 pandemic on the environment. International Journal of Environmental Research and Public Health 17, 4140. doi: 10.3390/ijerph17114140.
- Donders GGG, Bosmans E, Reumers J, et al (2022). 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. Fertility and Sterility 117, 287–296. doi: 10.1016/j.fertnstert.2021.10.022.
- Duarte‐Neto AN, Teixeira TA, Caldini EG, et al (2022). Testicular pathology in fatal COVID‐19: A descriptive autopsy study. Andrology 10, 13–23. doi: 10.1111/andr.13073.
- Falahieh FM, Zarabadipour M, Mirani M, et al (2021). Effects of moderate COVID-19 infection on semen oxidative status and parameters 14 and 120 days after diagnosis. Reproduction, Fertility and Development 33, 683–690. doi: 10.1071/RD21153.
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- Gonzalez DC, Nassau DE, Khodamoradi K, et al (2021). Sperm parameters before and after COVID-19 mRNA vaccination. JAMA 326, 273. doi: 10.1001/jama.2021.9976.
- Gunadi, Hakim MS, Wibawa H, et al (2021). Is the infection of the SARS-CoV-2 delta variant associated with the outcomes of COVID-19 patients? Frontiers in Medicine. doi: 10.3389/fmed.2021.780611.
- Hinting A, Agustinus, Pakpahan C (2020). A review of the impact of COVID-19 on male reproduction, and its implications on assisted reproductive technology services. Fertility & Reproduction 02, 109–114. doi: 10.1142/S2661318220300081.
- Holtmann N, Edimiris P, Andree M, et al (2020). Assessment of SARS-CoV-2 in human semen—a cohort study. Fertility and Sterility 114, 233–238. doi: 10.1016/j.fertnstert.2020.05.028.
- IBM Corp. 2019. IBM SPSS Statistics for Windows, Version 26.0. Armonk, NY: IBM Corp. Available at: https://www.ibm.com/support/pages/download ing-ibm-spss-statistics-26.
- Kishore K, Jaswal V (2022). Statistics corner: Comparing two unpaired groups. Journal of Postgraduate Medicine, Education and Research 56, 145–148. doi: 10.5005/jp-journals-10028-1594.
- Kleshchev M, Osadchuk A, Osadchuk L (2021). Impaired semen quality, an increase of sperm morphological defects and DNA fragmentation associated with environmental pollution in urban population of young men from Western Siberia, Russia ed. Yenugu S. PLoS One 16, e0258900. doi: 10.1371/journal.pone.0258900.
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- Li H, Xiao X, Zhang J, et al (2020). Impaired spermatogenesis in COVID-19 patients. EClinicalMedicine 28, 100604. doi: 10.1016/j.eclinm.2020.100604.
- Lwanga SK, Lemeshow S, World Health Organization (1991). Sample size determination in health studies : A practical manual. Biometrics 47, 347. doi: 10.2307/2532527.
- Ma L, Xie W, Li D, et al (2021a). Evaluation of sex‐related hormones and semen characteristics in reproductive‐aged male COVID‐19 patients. Journal of Medical Virology 93, 456–462. doi: 10.1002/jmv.26259.
- Ma X, Guan C, Chen R, et al (2021b). Pathological and molecular examinations of postmortem testis biopsies reveal SARS-CoV-2 infection in the testis and spermatogenesis damage in COVID-19 patients. Cellular & Molecular Immunology 18, 487–489. doi: 10.1038/s41423-020-00604-5.
- Ministry of Health of the Republic of Indonesia (2021). Clinical management of Corona virus disease 2019 (Covid-19) in health care facilities. Available at: https://bblabkesmasyogyakarta.go.id /uploads/regulasi/kmk-no-hk0107-menkes-5671-2021-ttg-manajemen-klinis-tata-laksana-covid-19-di-fasilitas-pelayanan-kesehatan-signed-1.pdf.
- Moghimi N, Eslami Farsani B, Ghadipasha M, et al (2021). COVID-19 disrupts spermatogenesis through the oxidative stress pathway following induction of apoptosis. Apoptosis 26, 415–430. doi: 10.1007/s10495-021-01680-2.
- Pullanna K, Reddy DN, Philip GH (2015). Effect of cigarette smoking on semen parameters of men. International Journal of Pharmaceutical Sciences and Research 4310–4315. doi: 10.13040/IJPSR.09 75-8232.6(10).4310-15.
- Rahman MKA, Moniem AA, Zarzour M, et al. (2021). The effect of COVID-19 on spermatogenesis. Virology: Current Research. Available at: https://www.hilarispublisher.com/ open-access/the-effect-of-covid19-on-spermatoge nesis.pdf.
- Reschini M, Pagliardini L, Boeri L, et al (2022). COVID-19 vaccination does not affect reproductive health parameters in men. Frontiers in Public Health. doi: 10.3389/fpubh.2022.83996 7.
- Ruan Y, Hu B, Liu Z, et al (2021). No detection of SARS‐CoV‐2 from urine, expressed prostatic secretions, and semen in 74 recovered COVID‐19 male patients: A perspective and urogenital evaluation. Andrology 9, 99–106. doi: 10.1111/an dr.12939.
- Rysz S, Al-Saadi J, Sjöström A, et al (2021). COVID-19 pathophysiology may be driven by an imbalance in the renin-angiotensin-aldosterone system. Nature Communications 12, 2417. doi: 10.1038/s41467-021-22713-z.
- Salas‐Huetos A, Maghsoumi‐Norouzabad L, James ER, et al (2021). Male adiposity, sperm parameters and reproductive hormones: An updated systematic review and collaborative meta‐analysis. Obesity Reviews. doi: 10.1111/obr.130 82.
- Temiz MZ, Dincer MM, Hacibey I, et al (2021). Investigation of SARS‐CoV‐2 in semen samples and the effects of COVID‐19 on male sexual health by using semen analysis and serum male hormone profile: A cross‐sectional, pilot study. Andrologia. doi: 10.1111/and.13912.
- Turner AJ (2015). ACE2 cell biology, regulation, and physiological functions. In The Protective Arm of the Renin Angiotensin System (RAS), pp. 185–9. Elsevier. Available at: https://linkinghub.el sevier.com/retrieve/pii/B9780128013649000250.
- World Health Organization (2021a). Weekly epidemiological update - 25 February 2021. WHO. Available at: https://www.who.int/publications/m/ item/covid-19-weekly-epidemiological-update.
- World Health Organization (2021b). WHO laboratory manual for the examination and processing of human semen. WHO. Available at: https://www.who.int/publications/i/item/9789240030787.
- Younis JS, Abassi Z, Skorecki K (2020). Is there an impact of the COVID-19 pandemic on male fertility? The ACE2 connection. American Journal of Physiology-Endocrinology and Metabolism 318, E878–880. doi: 10.1152/ajpendo.00183.20 20.
- Zafar MI, Yu J, Li H (2021). Implications of RNA viruses in the male reproductive tract: An outlook on SARS-CoV-2. Frontiers in Microbiology. doi: 10.3389/fmicb.2021.783963.
References
Absalan F, Ghannadi A, Zabihi A (2014). The effects of different doses of ketamine on quality of normal ejaculated sperm. International Journal of Fertility & Sterility 8, 207–214. Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC4107695.
Agustinus, I’tishom R, Pramesti MD (2018). Male reproductive biology. Airlangga University Press, Surabaya. Available at: https://repository.unair.ac. id/95965/3/Biologi Reproduksi Pria.pdf.
Boitrelle F, Shah R, Saleh R, et al (2021). The sixth edition of the WHO manual for human semen analysis: A critical review and SWOT analysis. Life 11, 1368. doi: 10.3390/life11121368.
Cheval S, Mihai Adamescu C, Georgiadis T, et al (2020). Observed and potential impacts of the covid-19 pandemic on the environment. International Journal of Environmental Research and Public Health 17, 4140. doi: 10.3390/ijerph17114140.
Donders GGG, Bosmans E, Reumers J, et al (2022). 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. Fertility and Sterility 117, 287–296. doi: 10.1016/j.fertnstert.2021.10.022.
Duarte‐Neto AN, Teixeira TA, Caldini EG, et al (2022). Testicular pathology in fatal COVID‐19: A descriptive autopsy study. Andrology 10, 13–23. doi: 10.1111/andr.13073.
Falahieh FM, Zarabadipour M, Mirani M, et al (2021). Effects of moderate COVID-19 infection on semen oxidative status and parameters 14 and 120 days after diagnosis. Reproduction, Fertility and Development 33, 683–690. doi: 10.1071/RD21153.
Gacci M, Coppi M, Baldi E, et al (2021). Semen impairment and occurrence of SARS-CoV-2 virus in semen after recovery from COVID-19. Human Reproduction 36, 1520–1529. doi: 10.1093/humre p/deab026.
Gonzalez DC, Nassau DE, Khodamoradi K, et al (2021). Sperm parameters before and after COVID-19 mRNA vaccination. JAMA 326, 273. doi: 10.1001/jama.2021.9976.
Gunadi, Hakim MS, Wibawa H, et al (2021). Is the infection of the SARS-CoV-2 delta variant associated with the outcomes of COVID-19 patients? Frontiers in Medicine. doi: 10.3389/fmed.2021.780611.
Hinting A, Agustinus, Pakpahan C (2020). A review of the impact of COVID-19 on male reproduction, and its implications on assisted reproductive technology services. Fertility & Reproduction 02, 109–114. doi: 10.1142/S2661318220300081.
Holtmann N, Edimiris P, Andree M, et al (2020). Assessment of SARS-CoV-2 in human semen—a cohort study. Fertility and Sterility 114, 233–238. doi: 10.1016/j.fertnstert.2020.05.028.
IBM Corp. 2019. IBM SPSS Statistics for Windows, Version 26.0. Armonk, NY: IBM Corp. Available at: https://www.ibm.com/support/pages/download ing-ibm-spss-statistics-26.
Kishore K, Jaswal V (2022). Statistics corner: Comparing two unpaired groups. Journal of Postgraduate Medicine, Education and Research 56, 145–148. doi: 10.5005/jp-journals-10028-1594.
Kleshchev M, Osadchuk A, Osadchuk L (2021). Impaired semen quality, an increase of sperm morphological defects and DNA fragmentation associated with environmental pollution in urban population of young men from Western Siberia, Russia ed. Yenugu S. PLoS One 16, e0258900. doi: 10.1371/journal.pone.0258900.
Kresch E, Achua J, Saltzman R, et al (2021). COVID-19 endothelial dysfunction can cause erectile dysfunction: Histopathological, immunohistochemical, and ultrastructural study of the human penis. The World Journal of Men's Health 39, 466. doi: 10.5534/wjmh.210055.
Li H, Xiao X, Zhang J, et al (2020). Impaired spermatogenesis in COVID-19 patients. EClinicalMedicine 28, 100604. doi: 10.1016/j.eclinm.2020.100604.
Lwanga SK, Lemeshow S, World Health Organization (1991). Sample size determination in health studies : A practical manual. Biometrics 47, 347. doi: 10.2307/2532527.
Ma L, Xie W, Li D, et al (2021a). Evaluation of sex‐related hormones and semen characteristics in reproductive‐aged male COVID‐19 patients. Journal of Medical Virology 93, 456–462. doi: 10.1002/jmv.26259.
Ma X, Guan C, Chen R, et al (2021b). Pathological and molecular examinations of postmortem testis biopsies reveal SARS-CoV-2 infection in the testis and spermatogenesis damage in COVID-19 patients. Cellular & Molecular Immunology 18, 487–489. doi: 10.1038/s41423-020-00604-5.
Ministry of Health of the Republic of Indonesia (2021). Clinical management of Corona virus disease 2019 (Covid-19) in health care facilities. Available at: https://bblabkesmasyogyakarta.go.id /uploads/regulasi/kmk-no-hk0107-menkes-5671-2021-ttg-manajemen-klinis-tata-laksana-covid-19-di-fasilitas-pelayanan-kesehatan-signed-1.pdf.
Moghimi N, Eslami Farsani B, Ghadipasha M, et al (2021). COVID-19 disrupts spermatogenesis through the oxidative stress pathway following induction of apoptosis. Apoptosis 26, 415–430. doi: 10.1007/s10495-021-01680-2.
Pullanna K, Reddy DN, Philip GH (2015). Effect of cigarette smoking on semen parameters of men. International Journal of Pharmaceutical Sciences and Research 4310–4315. doi: 10.13040/IJPSR.09 75-8232.6(10).4310-15.
Rahman MKA, Moniem AA, Zarzour M, et al. (2021). The effect of COVID-19 on spermatogenesis. Virology: Current Research. Available at: https://www.hilarispublisher.com/ open-access/the-effect-of-covid19-on-spermatoge nesis.pdf.
Reschini M, Pagliardini L, Boeri L, et al (2022). COVID-19 vaccination does not affect reproductive health parameters in men. Frontiers in Public Health. doi: 10.3389/fpubh.2022.83996 7.
Ruan Y, Hu B, Liu Z, et al (2021). No detection of SARS‐CoV‐2 from urine, expressed prostatic secretions, and semen in 74 recovered COVID‐19 male patients: A perspective and urogenital evaluation. Andrology 9, 99–106. doi: 10.1111/an dr.12939.
Rysz S, Al-Saadi J, Sjöström A, et al (2021). COVID-19 pathophysiology may be driven by an imbalance in the renin-angiotensin-aldosterone system. Nature Communications 12, 2417. doi: 10.1038/s41467-021-22713-z.
Salas‐Huetos A, Maghsoumi‐Norouzabad L, James ER, et al (2021). Male adiposity, sperm parameters and reproductive hormones: An updated systematic review and collaborative meta‐analysis. Obesity Reviews. doi: 10.1111/obr.130 82.
Temiz MZ, Dincer MM, Hacibey I, et al (2021). Investigation of SARS‐CoV‐2 in semen samples and the effects of COVID‐19 on male sexual health by using semen analysis and serum male hormone profile: A cross‐sectional, pilot study. Andrologia. doi: 10.1111/and.13912.
Turner AJ (2015). ACE2 cell biology, regulation, and physiological functions. In The Protective Arm of the Renin Angiotensin System (RAS), pp. 185–9. Elsevier. Available at: https://linkinghub.el sevier.com/retrieve/pii/B9780128013649000250.
World Health Organization (2021a). Weekly epidemiological update - 25 February 2021. WHO. Available at: https://www.who.int/publications/m/ item/covid-19-weekly-epidemiological-update.
World Health Organization (2021b). WHO laboratory manual for the examination and processing of human semen. WHO. Available at: https://www.who.int/publications/i/item/9789240030787.
Younis JS, Abassi Z, Skorecki K (2020). Is there an impact of the COVID-19 pandemic on male fertility? The ACE2 connection. American Journal of Physiology-Endocrinology and Metabolism 318, E878–880. doi: 10.1152/ajpendo.00183.20 20.
Zafar MI, Yu J, Li H (2021). Implications of RNA viruses in the male reproductive tract: An outlook on SARS-CoV-2. Frontiers in Microbiology. doi: 10.3389/fmicb.2021.783963.