Volume 21, Issue 1 (January 2023)                   IJRM 2023, 21(1): 1-16 | Back to browse issues page

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Samadian E, Aghcheli B, Gharaei R, Tabarraei A. A review on human reproductive systems encountering with the severe acute respiratory syndrome coronavirus 2 infection. IJRM 2023; 21 (1) :1-16
URL: http://ijrm.ir/article-1-2556-en.html
A review on human reproductive systems encountering with the severe acute respiratory syndrome coronavirus 2 infection
Esmaeil Samadian1 , Bahman Aghcheli2 , Roghaye Gharaei3 , Aligan Tabarraei * 4
1- Laboratory Sciences Research Center, Golestan University of Medical Sciences, Gorgan, Iran.
2- Infection Diseases Research Center, Golestan University of Medical Sciences, Gorgan, Iran.
3- Department of Obstetrics and Gynecology, School of Medicine, Golestan University of Medical Sciences, Gorgan, Iran.
4- Infection Diseases Research Center, Golestan University of Medical Sciences, Gorgan, Iran. , Tabarraei@yahoo.com
Abstract:   (996 Views)
The severe acute respiratory syndrome coronavirus 2 (SARS-CoV2) is the leading cause of the new deadly pneumonia named coronavirus disease 2019 (COVID-19) pandemic. This pathogen has different co-receptors on various tissues, resulting in vast pathophysiological circumstances. Here, we present a comprehensive narrative review focusing on the impact of SARS-CoV2 on human reproduction. Evidence-based literature revealed inconsistent results for this virus in the reproductive organs of patients with COVID-19, even in the critical phase. Conversely, numerous satisfactory data represented those different reproductive activities, from gametogenesis to pregnancy, can be targeted by SARS-CoV2. The severity of COVID-19 depends on the differential expression of the host cellular components required to enter SARS-CoV2. The cytokine storm and oxidative stress coming out during COVID-19 are associated with complications in reproductive endocrinopathies. Men are naturally more susceptible to COVID-19, especially accompanied by orchitis and varicocele. Synergistically the interaction of SARS-CoV2 and female reproductive failures (polycystic ovary syndrome and endometriosis) increases the susceptibility to COVID-19. Thus, pharmaceutical interventions that ameliorate the complications in individuals with reproductive disorders can be helpful to achieve good outcomes in assisted reproductive techniques. Soon, an increase in the infertility rate will likely be an overall impact of SARS-CoV2 in patients who recovered from COVID-19.
Keywords: SARS-CoV-2, Human, Reproductive system.
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Type of Study: Review Article | Subject: Reproductive Epidemiology
References
1. Chen WN, Yeong KY. Scopolamine, a toxin-induced experimental model, used for research in Alzheimer's disease. CNS Neurol Disord Drug Targets 2020; 19: 85-93. [DOI:10.2174/1871527319666200214104331] [PMID]
2. Kyrou I, Randeva HS, Spandidos DA, Karteris E. Not only ACE2-the quest for additional host cell mediators of SARS-CoV-2 infection: Neuropilin-1 (NRP1) as a novel SARS-CoV-2 host cell entry mediator implicated in COVID-19. Signal Transduct Target Ther 2021; 6: 21. [DOI:10.1038/s41392-020-00460-9] [PMID] [PMCID]
3. Cheng J, Zhou J, Fu Sh, Fu J, Zhou B, Chen H, et al. Prostate adenocarcinoma and COVID-19: The possible impacts of TMPRSS2 expressions in susceptibility to SARS-CoV-2. J Cell Mol Med 2021; 25: 4157-4165. [DOI:10.1111/jcmm.16385] [PMID] [PMCID]
4. Khare S, Azevedo M, Parajuli P, Gokulan K. Conformational changes of the receptor binding domain of SARS-CoV-2 spike protein and prediction of a B-cell antigenic epitope using structural data. Front Artif Intell 2021; 4: 630955. [DOI:10.3389/frai.2021.630955] [PMID] [PMCID]
5. Carneiro Gomes PR, Rodrigues da Rocha MD, da Rocha Coelho FA, Sousa Pinho de Lira JA, de Sousa Carmo RR, Silva Nascimento HM, et al. Alterations of the male and female reproductive systems induced by COVID-19. Wien Klin Wochenschr 2021; 133: 966-972. [DOI:10.1007/s00508-021-01875-2] [PMID] [PMCID]
6. Lin Y, Wu Y, Zhong P, Hou B, Liu J, Chen Y, et al. A clinical staging proposal of the disease course over time in non-severe patients with coronavirus disease 2019. Sci Rep 2021; 11: 10681. [DOI:10.1038/s41598-021-90111-y] [PMID] [PMCID]
7. 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. [DOI:10.1186/s43043-020-00046-z] [PMID] [PMCID]
8. Li H, Xiao X, Zhang J, Zafar MI, Wu C, Long Y, et al. Impaired spermatogenesis in COVID-19 patients. EClinicalMedicine 2020; 28: 100604. [DOI:10.1016/j.eclinm.2020.100604] [PMID] [PMCID]
9. Younis JS, Skorecki K, Abassi Z. The double edge sword of testosterone's role in the COVID-19 pandemic. Front Endocrinol 2021; 12: 607179. [DOI:10.3389/fendo.2021.607179] [PMID] [PMCID]
10. Jassim G, Jameel M, Brennan E, Yusuf M, Hasan N, Alwatani Y. Psychological impact of COVID-19, isolation, and quarantine: A cross-sectional study. Neuropsychiatr Dis Treat 2021; 17: 1413-1421. [DOI:10.2147/NDT.S311018] [PMID] [PMCID]
11. Foresta C, Rocca MS, Di Nisio A. Gender susceptibility to COVID-19: A review of the putative role of sex hormones and X chromosome. J Endocrinol Invest 2021; 44: 951-956. [DOI:10.1007/s40618-020-01383-6] [PMID] [PMCID]
12. Mannur S, Jabeen T, Khader MA, Rao LSS. Post-COVID-19-associated decline in long-term male fertility and embryo quality during assisted reproductive technology. QJM 2021; 114: 328-330. [DOI:10.1093/qjmed/hcab019] [PMID] [PMCID]
13. Dutta S, Sengupta P. SARS-CoV-2 and male infertility: Possible multifaceted pathology. Reprod Sci 2021; 28: 23-26. [DOI:10.1007/s43032-020-00261-z] [PMID] [PMCID]
14. Fan C, Lu W, Li K, Ding Y, Wang J. ACE2 expression in kidney and testis may cause kidney and testis infection in COVID-19 patients. Front Med 2021; 7: 563893. [DOI:10.3389/fmed.2020.563893] [PMID] [PMCID]
15. Shan D, Johnson JM, Fernandes SC, Suib H, Hwang S, Wuelfing D, et al. N-protein presents early in blood, dried blood and saliva during asymptomatic and symptomatic SARS-CoV-2 infection. Nat Commun 2021; 12: 1931. [DOI:10.1038/s41467-021-22072-9] [PMID] [PMCID]
16. Xu H, Wang Z, Feng C, Yu W, Chen Y, Zeng X, et al. Effects of SARS-CoV-2 infection on male sex-related hormones in recovering patients. Andrology 2021; 9: 107-114. [DOI:10.1111/andr.12942] [PMID]
17. Frara S, Allora A, Castellino L, di Filippo L, Loli P, Giustina A. COVID-19 and the pituitary. Pituitary 2021; 24: 465-481. [DOI:10.1007/s11102-021-01148-1] [PMID] [PMCID]
18. Solomon T. Neurological infection with SARS-CoV-2- the story so far. Nat Rev Neurol 2021; 17: 65-66. [DOI:10.1038/s41582-020-00453-w] [PMID] [PMCID]
19. Deng Q, Rasool Ru, Russell RM, Natesan R, Asangani IA. Targeting androgen regulation of TMPRSS2 and ACE2 as a therapeutic strategy to combat COVID-19. iScience 2021; 24: 102254. [DOI:10.1016/j.isci.2021.102254] [PMID] [PMCID]
20. Hashem NM, Abdelnour SA, Alhimaidi AR, Swelum AA. Potential impacts of COVID-19 on reproductive health: Scientific findings and social dimension. Saudi J Biol Sci 2021; 28: 1702-1712. [DOI:10.1016/j.sjbs.2020.12.012] [PMID] [PMCID]
21. Niemann PJ, Goldstein HV. Testosterone in COVID-19: Friend or Foe? Endocrine 2021; 71: 2281-2282. [DOI:10.1007/s12020-021-02623-2] [PMID] [PMCID]
22. Naous E, Nassani B-M, Yaghi C, Nasr F, Medlej R. Hemophagocytic lymphohistiocytosis, a new cause of death during 'post-acute COVID-19 syndrome?' A case report. J Hematop 2021; 14: 229-233. [DOI:10.1007/s12308-021-00452-w] [PMID] [PMCID]
23. Srivastava S, Garg I, Hembrom AA, Kumar B. Assessment of nitric oxide (NO) potential to mitigate COVID-19 severity. Virusdisease 2021; 32: 589-594. [DOI:10.1007/s13337-021-00702-6] [PMID] [PMCID]
24. Bertheloot D, Latz E, Franklin BS. Necroptosis, pyroptosis and apoptosis: An intricate game of cell death. Cell Mol Immunol 2021; 18: 1106-1121. [DOI:10.1038/s41423-020-00630-3] [PMID] [PMCID]
25. Darenskaya M, Kolesnikova L, Kolesnikov S. The association of respiratory viruses with oxidative stress and antioxidants: Implications for the COVID-19 pandemic. Curr Pharm Design 2021; 27: 1618-1627. https://doi.org/10.2174/18734286MTE0dNDIx5 [DOI:10.2174/1381612827666210222113351]
26. Barciszewska A-M. Elucidating of oxidative distress in COVID-19 and methods of its prevention. Chem Biol Interact 2021; 344: 109501. [DOI:10.1016/j.cbi.2021.109501] [PMID] [PMCID]
27. Dutta S, Sengupta P. The role of nitric oxide on male and female reproduction. Malays J Med Sci 2022; 29: 18-30.
28. Pike JFW, Polley EL, Pritchett DY, Lal A, Wynia BA, Roudebush WE, et al. Comparative analysis of viral infection outcomes in human seminal fluid from prior viral epidemics and Sars-CoV-2 may offer trends for viral sexual transmissibility and long-term reproductive health implications. Reprod Health 2021; 18: 123. [DOI:10.1186/s12978-021-01172-1] [PMID] [PMCID]
29. Gacci M, Coppi M, Baldi E, Sebastianelli A, Zaccaro C, Morselli S, et al. Semen impairment and occurrence of SARS-CoV-2 virus in semen after recovery from COVID-19. Hum Reprod 2021; 36: 1520-1529. [DOI:10.1093/humrep/deab026] [PMID] [PMCID]
30. Guo L, Zhao S, Li W, Wang Y, Li L, Jiang S, et al. Absence of SARS-CoV-2 in semen of a COVID-19 patient cohort. Andrology 2021; 9: 42-47. [DOI:10.1111/andr.12848] [PMID] [PMCID]
31. Paoli D, Pallotti F, Nigro G, Mazzuti L, Hirsch MN, Valli MB, et al. Molecular diagnosis of SARS-CoV-2 in seminal fluid. J Endocrinol Invest 2021; 44: 2675-2684. [DOI:10.1007/s40618-021-01580-x] [PMID] [PMCID]
32. Wang N, Qin L, Ma L, Yan H. Effect of severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) on reproductive system. Stem Cell Res 2021; 52: 102189. [DOI:10.1016/j.scr.2021.102189] [PMID] [PMCID]
33. Zhou L, Ayeh SK, Chidambaram V, Karakousis PC. Modes of transmission of SARS-CoV-2 and evidence for preventive behavioral interventions. BMC Infect Dis 2021; 21: 496. [DOI:10.1186/s12879-021-06222-4] [PMID] [PMCID]
34. Rastrelli G, Di Stasi V, Inglese F, Beccaria M, Garuti M, Di Costanzo D, et al. Low testosterone levels predict clinical adverse outcomes in SARS-CoV-2 pneumonia patients. Andrology 2021; 9: 88-98. [DOI:10.1111/andr.12821] [PMID] [PMCID]
35. Schroeder M, Tuku B, Jarczak D, Nierhaus A, Bai T, Jacobsen H, et al. The majority of male patients with COVID-19 present low testosterone levels on admission to intensive care in Hamburg, Germany: A retrospective cohort study. Emerg Microbes Infect 2021; 10: 1807-1818. [DOI:10.1080/22221751.2021.1969869] [PMID] [PMCID]
36. Achua JK, Chu KY, Ibrahim E, Khodamoradi K, Delma KS, Iakymenko OA, et al. Histopathology and ultrastructural findings of fatal COVID-19 infections on testis. World J Mens Health 2021; 39: 65-74. [DOI:10.5534/wjmh.200170] [PMID] [PMCID]
37. Hajizadeh Maleki B, Tartibian B. COVID-19 and male reproductive function: A prospective, longitudinal cohort study. Reproduction 2021; 161: 319-331. [DOI:10.1530/REP-20-0382] [PMID]
38. Moghimi N, Eslami Farsani B, Ghadipasha M, Mahmoudiasl GR, Piryaei A, Aliaghaei A, et al. COVID-19 disrupts spermatogenesis through the oxidative stress pathway following induction of apoptosis. Apoptosis 2021; 26: 415-430. [DOI:10.1007/s10495-021-01680-2] [PMID] [PMCID]
39. Salciccia S, Del Giudice F, Gentile V, Mastorianni CM, Pasculli P, Di Lascio G, et al. Interplay between male testosterone levels and the risk for subsequent invasive respiratory assistance among COVID-19 patients at hospital admission. Endocrine 2020; 70: 206-210. [DOI:10.1007/s12020-020-02515-x] [PMID] [PMCID]
40. Duarte-Neto AN, Monteiro RAA, da Silva LFF, Malheiros D, de Oliveira EP, Theodoro-Filho J, et al. Pulmonary and systemic involvement in COVID-19 patients assessed with ultrasound-guided minimally invasive autopsy. Histopathology 2020; 77: 186-197. [DOI:10.1111/his.14160] [PMID] [PMCID]
41. Temiz MZ, Dincer MM, Hacibey I, Yazar RO, Celik C, Kucuk SH, et al. 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 2021; 53: me13912. [DOI:10.1111/and.13912] [PMID] [PMCID]
42. Bian XW. Autopsy of COVID-19 patients in China. Nat Sci Rev 2020; 7: 1414-1418. [DOI:10.1093/nsr/nwaa123] [PMID] [PMCID]
43. Yang J, Yuan L, Wen Y, Zhou H, Jiang W, Xu D, et al. Protective effects of naringin in cerebral infarction and its molecular mechanism. Med Sci Monit 2020; 26: e918772. [DOI:10.12659/MSM.918772]
44. Li D, Jin M, Bao P, Zhao W, Zhang S. Clinical characteristics and results of semen tests among men with coronavirus disease 2019. JAMA Netw Open 2020; 3: e208292. [DOI:10.1001/jamanetworkopen.2020.8292] [PMID] [PMCID]
45. Pan F, Xiao X, Guo J, Song Y, Li H, Patel DP, et al. No evidence of severe acute respiratory syndrome-coronavirus 2 in semen of males recovering from coronavirus disease 2019. Fertil Steril 2020; 113: 1135-1139. [DOI:10.1016/j.fertnstert.2020.04.024] [PMID] [PMCID]
46. Ma L, Xie W, Li D, Shi L, Ye G, Mao Y, et al. Evaluation of sex-related hormones and semen characteristics in reproductive-aged male COVID-19 patients. J Med Virol 2021; 93: 456-462. [DOI:10.1002/jmv.26259] [PMID] [PMCID]
47. Holtmann N, Edimiris P, Andree M, Doehmen C, Baston-Buest D, Adams O, et al. Assessment of SARS-CoV-2 in human semen-a cohort study. Fertil Steril 2020; 114: 233-238. [DOI:10.1016/j.fertnstert.2020.05.028] [PMID] [PMCID]
48. Ning J, Li W, Ruan Y, Xia Y, Wu X, Hu K, et al. Effects of 2019 novel coronavirus on male reproductive system: A retrospective study. Pre Prints 2020; 2020040280. [DOI:10.20944/preprints202004.0280.v1]
49. Pavone C, Giammanco GM, Baiamonte D, Pinelli M, Bonura C, Montalbano M, et al. Italian males recovering from mild COVID-19 show no evidence of SARS-CoV-2 in semen despite prolonged nasopharyngeal swab positivity. Int J Impot Res 2020; 32: 560-562. [DOI:10.1038/s41443-020-00344-0] [PMID] [PMCID]
50. Gagliardi MC, Tieri P, Ortona E, Ruggieri A. ACE2 expression and sex disparity in COVID-19. Cell Death Discov 2020; 6: 37. [DOI:10.1038/s41420-020-0276-1] [PMID] [PMCID]
51. Beacon TH, Delcuve GP, Davie JR. Epigenetic regulation of ACE2, the receptor of the SARS-CoV-2 virus. Genome 2021; 64: 386-399. [DOI:10.1139/gen-2020-0124] [PMID]
52. Henarejos-Castillo I, Sebastian-Leon P, Devesa-Peiro A, Pellicer A, Diaz-Gimeno P. SARS-CoV-2 infection risk assessment in the endometrium: Viral infection-related gene expression across the menstrual cycle. Fertil Steril 2020; 114: 223-232. [DOI:10.1016/j.fertnstert.2020.06.026] [PMID] [PMCID]
53. Ma Y, Andrisse S, Chen Y, Childress S, Xue P, Wang Z, et al. Androgen receptor in the ovary theca cells plays a critical role in androgen-induced reproductive dysfunction. Endocrinology 2017; 158: 98-108. [DOI:10.1210/en.2016-1608] [PMID] [PMCID]
54. Barragan M, Guillén JJ, Martin-Palomino N, Rodriguez A, Vassena R. Undetectable viral RNA in oocytes from SARS-CoV-2 positive women. Hum Reprod 2021; 36: 390-394. [DOI:10.1093/humrep/deaa284] [PMID] [PMCID]
55. Aliee H, Massip F, Qi C, Stella de Biase M, van Nijnatten JL, Kersten ETG, et al. Determinants of SARS-CoV-2 receptor gene expression in upper and lower airways. medRxiv 2020: 2020.08.31.20169946. [DOI:10.1101/2020.08.31.20169946]
56. Al-kuraishy HM, Al-Gareeb AI, Faidah H, Al-Maiahy TJ, Cruz-Martins N, Batiha GE-S. The looming effects of estrogen in Covid-19: A rocky rollout. Front Nutr 2021; 8: 649728. [DOI:10.3389/fnut.2021.649128] [PMID] [PMCID]
57. Qiu L, Liu X, Xiao M, Xie J, Cao W, Liu Z, et al. SARS-CoV-2 is not detectable in the vaginal fluid of women with severe COVID-19 infection. Clin Infect Dis 2020; 71: 813-817. [DOI:10.1093/cid/ciaa375] [PMID] [PMCID]
58. Liao J, He X, Gong Q, Yang L, Zhou C, Li J. Analysis of vaginal delivery outcomes among pregnant women in Wuhan, China during the COVID-19 pandemic. Int J Gynaecol Obstet 2020; 150: 53-57. [DOI:10.1002/ijgo.13188] [PMID] [PMCID]
59. Futterman I, Toaff M, Navi L, Clare CA. COVID-19 and HELLP: Overlapping clinical pictures in two gravid patients. AJP Rep 2020; 10: e179-e182. [DOI:10.1055/s-0040-1712978] [PMID] [PMCID]
60. Cooke WR, Billett A, Gleeson S, Jacques A, Place K, Siddall J, et al. SARS-CoV-2 infection in very preterm pregnancy: Experiences from two cases. Eur J Obstet Gynecol Reprod Biol 2020; 250: 259-260. [DOI:10.1016/j.ejogrb.2020.05.025] [PMID] [PMCID]
61. González Romero D, Ocampo Pérez J, González Bautista L, Santana-Cabrera L. Pregnancy and perinatal outcome of a woman with COVID-19 infection. Rev Clin Esp 2020; 220: 533-534. [DOI:10.1016/j.rce.2020.04.006] [PMID] [PMCID]
62. Sentilhes L, De Marcillac F, Jouffrieau C, Kuhn P, Thuet V, Hansmann Y, et al. Coronavirus disease 2019 in pregnancy was associated with maternal morbidity and preterm birth. Am J Obstet Gynecol 2020; 223: 914. [DOI:10.1016/j.ajog.2020.06.022] [PMID] [PMCID]
63. Knight M, Bunch K, Vousden N, Morris E, Simpson N, Gale C, et al. Characteristics and outcomes of pregnant women admitted to hospital with confirmed SARS-CoV-2 infection in UK: National population based cohort study. BMJ 2020; 369: m2107. [DOI:10.1136/bmj.m2107] [PMID] [PMCID]
64. Li N, Han L, Peng M, Lv Y, Ouyang Y, Liu K, et al. Maternal and neonatal outcomes of pregnant women with COVID-19 pneumonia: A case-control study. Clin Infect Dis 2020; 17: 2035-2041. [DOI:10.1093/cid/ciaa352] [PMID] [PMCID]
65. Govind A, Essien S, Karthikeyan A, Fakokunde A, Janga D, Yoong W, et al. Re: Novel coronavirus COVID-19 in late pregnancy: Outcomes of first nine cases in an inner city London hospital. Eur J Obstet Gynecol Reprod Biol 2020; 251: 272-274. [DOI:10.1016/j.ejogrb.2020.05.004] [PMID] [PMCID]
66. Khan S, Jun L, Nawsherwan, Siddique R, Li Y, Han G, et al. Association of COVID-19 with pregnancy outcomes in health-care workers and general women. Clin Microbiol Infect 2020; 26: 788-790. [DOI:10.1016/j.cmi.2020.03.034] [PMID] [PMCID]
67. Subramanian A, Anand A, Adderley NJ, Okoth K, Toulis KA, Gokhale K, et al. Increased COVID-19 infections in women with polycystic ovary syndrome: A population-based study. Eur J Endocrinol 2021; 184: 637-645. [DOI:10.1530/EJE-20-1163] [PMID] [PMCID]
68. Wang W, Su X, Ding Y, Fan W, Zhou W, Su J, et al. Thyroid function abnormalities in COVID-19 patients. Front Endocrinol 2021; 11: 623792. [DOI:10.3389/fendo.2020.623792] [PMID] [PMCID]
69. Abdelmaksoud A, Goldust M, Vestita M. Comment on "Androgens and women: COVID-19 outcomes in women with acne vulgaris, polycystic ovarian syndrome, and hirsutism". Int J Dermatol 2021; 60: e337-e338. [DOI:10.1111/ijd.15617]
70. Mauvais-Jarvis F, Klein SL, Levin ER. Estradiol, progesterone, immunomodulation, and COVID-19 outcomes. Endocrinology 2020; 161: bqaa127. [DOI:10.1210/endocr/bqaa127] [PMID] [PMCID]
71. Moin ASM, Sathyapalan T, Butler AE, Atkin SL. Vitamin D association with macrophage-derived cytokines in polycystic ovary syndrome: An enhanced risk of COVID-19 infection? Front Endocrinol 2021; 12: 638621. [DOI:10.3389/fendo.2021.638621] [PMID] [PMCID]
72. Leonardi M, Horne AW, Armour M, Missmer SA, Roman H, Rombauts L, et al. Endometriosis and the Coronavirus (COVID-19) pandemic: Clinical advice and future considerations. Front Reprod Health 2020; 2: 5. [DOI:10.3389/frph.2020.00005] [PMID] [PMCID]
73. Ramos-Echevarría PM, Soto-Soto DM, Torres-Reverón A, Appleyard CB, Akkawi T, Barros-Cartagena BD, et al. Impact of the early COVID-19 era on endometriosis patients: Symptoms, stress, and access to care. J Endometriosis Pelvic Pain Disord 2021; 13: 111-121. [DOI:10.1177/22840265211009634]
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