The impact of COVID-19 on the male genital tract: A qualitative literature review of sexual transmission and fertility implications |
Verrienti, Pierangelo
(Department of Urology, Careggi Hospital, University of Florence)
Cito, Gianmartin (Department of Urology, Careggi Hospital, University of Florence) Maida, Fabrizio Di (Department of Urology, Careggi Hospital, University of Florence) Tellini, Riccardo (Department of Urology, Careggi Hospital, University of Florence) Cocci, Andrea (Department of Urology, Careggi Hospital, University of Florence) Minervini, Andrea (Department of Urology, Careggi Hospital, University of Florence) Natali, Alessandro (Department of Urology, Careggi Hospital, University of Florence) |
1 | Zou X, Chen K, Zou J, Han P, Hao J, Han Z. Single-cell RNA-seq data analysis on the receptor ACE2 expression reveals the potential risk of different human organs vulnerable to 2019-nCoV infection. Front Med 2020;14:185-92. DOI |
2 | Xu J, Xu Z, Jiang Y, Qian X, Huang Y. Cryptorchidism induces mouse testicular germ cell apoptosis and changes in bcl-2 and bax protein expression. J Environ Pathol Toxicol Oncol 2000;19:25-33. |
3 | Shang J, Wan Y, Luo C, Ye G, Geng Q, Auerbach A, et al. Cell entry mechanisms of SARS-CoV-2. Proc Natl Acad Sci U S A 2020;117:11727-34. DOI |
4 | Kohn FM, Muller C, Drescher D, Neukamm C, el Mulla KF, Henkel R, et al. Effect of angiotensin converting enzyme (ACE) and angiotensins on human sperm functions. Andrologia 1998;30:207-15. DOI |
5 | Zhang S, Wang X, Zhang H, Xu A, Fei G, Jiang X, et al. The absence of coronavirus in expressed prostatic secretion in COVID-19 patients in Wuhan city. Reprod Toxicol 2020;96:90-4. DOI |
6 | 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;93:456-62. DOI |
7 | 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;114:233-8. DOI |
8 | Flaifel A, Guzzetta M, Occidental M, Najari BB, Melamed J, Thomas KM, et al. Testicular changes associated with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Arch Pathol Lab Med 2021;145:8-9. DOI |
9 | Duggal NK, Ritter JM, Pestorius SE, Zaki SR, Davis BS, Chang GJ, et al. Frequent Zika virus sexual transmission and prolonged viral RNA shedding in an immunodeficient mouse model. Cell Rep 2017;18:1751-60. DOI |
10 | Alfaraj SH, Al-Tawfiq JA, Memish ZA. Middle east respiratory syndrome coronavirus (MERS-CoV) infection during pregnancy: report of two cases & review of the literature. J Microbiol Immunol Infect 2019;52:501-3. DOI |
11 | Pike JF, 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 |
12 | Mansuy JM, Suberbielle E, Chapuy-Regaud S, Mengelle C, Bujan L, Marchou B, et al. Zika virus in semen and spermatozoa. Lancet Infect Dis 2016;16:1106-7. DOI |
13 | Tur-Kaspa I, Tur-Kaspa T, Hildebrand G, Cohen D. COVID-19 may affect male fertility but is not sexually transmitted: a systematic review. F S Rev 2021;2:140-9. |
14 | Xu J, Qi L, Chi X, Yang J, Wei X, Gong E, et al. Orchitis: a complication of severe acute respiratory syndrome (SARS). Biol Reprod 2006;74:410-6. DOI |
15 | Verma S, Saksena S, Sadri-Ardekani H. ACE2 receptor expression in testes: implications in coronavirus disease 2019 pathogenesis. Biol Reprod 2020;103:449-51. DOI |
16 | Wang Z, Xu X. scRNA-seq profiling of human testes reveals the presence of the ACE2 receptor, a target for SARS-CoV-2 infection in spermatogonia, Leydig and Sertoli cells. Cells 2020;9:920. DOI |
17 | Aassve A, Cavalli N, Mencarini L, Plach S, Livi Bacci M. The COVID-19 pandemic and human fertility. Science 2020;369:370-1. DOI |
18 | 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;113:1135-9. DOI |
19 | Stanley KE, Thomas E, Leaver M, Wells D. Coronavirus disease-19 and fertility: viral host entry protein expression in male and female reproductive tissues. Fertil Steril 2020;114:33-43. DOI |
20 | Song H, Seddighzadeh B, Cooperberg MR, Huang FW. Expression of ACE2, the SARS-CoV-2 receptor, and TMPRSS2 in prostate epithelial cells. Eur Urol 2020;78:296-8. DOI |
21 | Ma L, Xie W, Li D, Shi L, Mao Y, Xiong Y, et al. Effect of SARS-CoV-2 infection upon male gonadal function: a single center-based study. medRxiv [Preprint]. 2020 [cited 2022 Jan 10]. Available from: http://medrxiv.org/content/early/2020/03/30/2020.03.21.20037267. |
22 | Dejucq N, Jegou B. Viruses in the mammalian male genital tract and their effects on the reproductive system. Microbiol Mol Biol Rev 2001;65:208-31. DOI |
23 | Li W, Moore MJ, Vasilieva N, Sui J, Wong SK, Berne MA, et al. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 2003;426:450-4. DOI |
24 | Cui P, Chen Z, Wang T, Dai J, Zhang J, Ding T, et al. Clinical features and sexual transmission potential of SARS-CoV-2 infected female patients: a descriptive study in Wuhan, China. medRxiv [Preprint]. 2020 [cited 2022 Jan 10]. Available from: https://doi.org/10.1101/2020.02.26.20028225. DOI |
25 | 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 |
26 | Song C, Wang Y, Li W, Hu B, Chen G, Xia P, et al. Detection of 2019 novel coronavirus in semen and testicular biopsy specimen of COVID-19 patients. medRxiv [Preprint]. 2020 [cited 2022 Jan 10]. Available from: https://doi.org/10.1101/2020.03.31.20042333. DOI |
27 | Shastri A, Wheat J, Agrawal S, Chaterjee N, Pradhan K, Goldfinger M, et al. Delayed clearance of SARS-CoV2 in male compared to female patients: high ACE2 expression in testes suggests possible existence of gender-specific viral reservoirs. medRxiv [Preprint]. 2020 [cited 2022 Jan 10]. Available from: https://doi.org/10.1101/2020.04.16.20060566. DOI |
28 | Vishvkarma R, Rajender S. Could SARS-CoV-2 affect male fertility? Andrologia 2020;52:e13712. |
29 | 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. Preprints [Preprint]. 2020 [cited 2022 Jan 10]. Available from: https://doi.org/10.20944/ preprints202004.0280.v1. DOI |
30 | Wong SF, Chow KM, Leung TN, Ng WF, Ng TK, Shek CC, et al. Pregnancy and perinatal outcomes of women with severe acute respiratory syndrome. Am J Obstet Gynecol 2004;191:292-7. DOI |
31 | Yang M, Chen S, Huang B, Zhong JM, Su H, Chen YJ, et al. Pathological findings in the testes of COVID-19 patients: clinical implications. Eur Urol Focus 2020;6:1124-9. DOI |
32 | Schroeder M, Schaumburg B, Mueller Z, Parplys A, Jarczak D, Roedl K, et al. High estradiol and low testosterone levels are associated with critical illness in male but not in female COVID-19 patients: a retrospective cohort study. Emerg Microbes Infect 2021;10:1807-18. DOI |
33 | 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 |
34 | Paoli D, Pallotti F, Colangelo S, Basilico F, Mazzuti L, Turriziani O, et al. Study of SARS-CoV-2 in semen and urine samples of a volunteer with positive naso-pharyngeal swab. J Endocrinol Invest 2020;43:1819-22. DOI |
35 | Al-Qahtani AA. Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2): emergence, history, basic and clinical aspects. Saudi J Biol Sci 2020;27:2531-8. DOI |
36 | Kayaaslan B, Korukluoglu G, Hasanoglu I, Kalem AK, Eser F, Akinci E, et al. Investigation of SARS-CoV-2 in semen of patients in the acute stage of COVID-19 infection. Urol Int 2020;104:678-83. DOI |
37 | Deen GF, Broutet N, Xu W, Knust B, Sesay FR, McDonald SL, et al. Ebola RNA persistence in semen of ebola virus disease survivors: final report. N Engl J Med 2017;377:1428-37. DOI |
38 | 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 |
39 | Liu W, Han R, Wu H, Han D. Viral threat to male fertility. Andrologia 2018;50:e13140. DOI |
40 | Wang D, Hu B, Hu C, Zhu F, Liu X, Zhang J, et al. Clinical characteristics of 138 hospitalized patients with 2019 novel coronavirus-infected pneumonia in Wuhan, China. JAMA 2020;323:1061-9. DOI |
41 | Aitken RJ. COVID-19 and human spermatozoa: potential risks for infertility and sexual transmission? Andrology 2021;9:48-52. DOI |
42 | Cocci A, Giunti D, Tonioni C, Cacciamani G, Tellini R, Polloni G, et al. Love at the time of the Covid-19 pandemic: preliminary results of an online survey conducted during the quarantine in Italy. Int J Impot Res 2020;32:556-7. DOI |
43 | Rawlings SA, Ignacio C, Porrachia M, Du P, Smith DM, Chaillon A. No evidence of SARS-CoV-2 seminal shedding despite SARSCoV-2 persistence in the upper respiratory tract. Open Forum Infect Dis 2020;7:ofaa325. DOI |