Pathogenesis of Viral Infections and Male Reproductive Health: An Evidence-Based Study.
Epidemic
Male reproductive system
Oxidative stress
Reproductive endocrinology
Sexual transmission
Viral infection
Journal
Advances in experimental medicine and biology
ISSN: 0065-2598
Titre abrégé: Adv Exp Med Biol
Pays: United States
ID NLM: 0121103
Informations de publication
Date de publication:
2022
2022
Historique:
entrez:
31
5
2022
pubmed:
1
6
2022
medline:
3
6
2022
Statut:
ppublish
Résumé
Viruses, being intracellular obligate parasites, can cause several congenital and sexually transmitted diseases. Depending on the site of infection, viruses can adopt various pathogenic mechanisms for their survival and to escape the host immune response. The male reproductive system is one of the attainable targets of many viruses including immunodeficiency virus (HIV), Zika virus (ZIKV), adenovirus, cytomegalovirus (CMV), and severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), and infection with such viruses may cause serious health issues. Leydig cells and seminiferous tubules are the prime sites of mammalian testis for viral infection. The azoospermic condition is a common symptom of viral infection, wherein the hypothalamic-pituitary-testicular (HPT) axis can be disrupted, leading to decreased levels of luteinizing hormone (LH). Furthermore, oxidative stress (OS) is a major contributing factor to viral infection-associated male infertility. The likelihood of direct and indirect infection, as well as sex-based variability in the vulnerability pattern to viral infections, has been observed. However, there appears to be a long-term impact of viral infection on male reproductive performance due to testicular tissue pathogenicity - a process that requires thorough investigation. The present study aimed to explore how the viruses affect the male reproductive system, including their distribution in tissues and body fluids, possible targets as well as the effects on the endocrine system. We used the major electronic databases such as MEDLINE and SCOPUS. Google Scholar was also consulted for additional literature search related to the topic. Obtained literatures were sorted based on the content. The articles that reported the pathogenesis of viruses on male reproductive health and were published in the English language were included in the present study.
Identifiants
pubmed: 35641876
doi: 10.1007/978-3-030-89340-8_14
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
325-343Informations de copyright
© 2022. The Author(s), under exclusive license to Springer Nature Switzerland AG.
Références
Roychoudhury S, Das A, Jha NK, Kesari KK, Roychoudhury S, Jha SK, Kosgi R, Choudhury AP, Lukac N, Madhu NR, Kumar D, Slama P. Viral pathogenesis of SARS-CoV-2 infection and male reproductive health. Open Biol. 2021;11(1):200347. https://doi.org/10.1098/rsob.200347 .
doi: 10.1098/rsob.200347
pubmed: 33465325
pmcid: 7881178
Roychoudhury S, Das A, Sengupta P, Dutta S, Roychoudhury S, Choudhury AP, Ahmed A, Bhattacharjee S, Slama P. Viral pandemics of the last four decades: pathophysiology, health impacts and perspectives. Int J Environ Res Public Health. 2020;17(24):9411. https://doi.org/10.3390/ijerph17249411 .
doi: 10.3390/ijerph17249411
pmcid: 7765415
Dutta S, Sengupta P. SARS-CoV-2 and male infertility: possible multifaceted pathology. Reprod Sci (Thousand Oaks, Calif.). 2021;28(1):23–6. https://doi.org/10.1007/s43032-020-00261-z .
doi: 10.1007/s43032-020-00261-z
Stanley KE, Thomas E, Leaver M, Wells D. Coronavirus disease (COVID-19) and fertility: viral ost entry protein expression in male and female reproductive tissues. Fertil Steril. 2020;114:33–43. https://doi.org/10.1016/j.fertnstert.2020.05.001 .
doi: 10.1016/j.fertnstert.2020.05.001
pubmed: 32622411
pmcid: 7205710
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(2):410–6.
doi: 10.1095/biolreprod.105.044776
Pan F, Xiao X, Guo J, Song Y, Li H, Patel DP, et al. No evidence of SARS-CoV-2 in semen of males recovering from COVID-19. Fertil Steril. 2020;113:1135–9. https://doi.org/10.1016/j.fertnstert .
doi: 10.1016/j.fertnstert
pubmed: 32482249
pmcid: 7164916
Nora H, Philippos E, Marcel A, Cornelius D, Dunja B-B, Ortwin A, et al. Assessment of SARS-CoV-2 in human semen-a cohort study. Fertil Steril. 2020; https://doi.org/10.1016/j.fertnstert.2020.05.028 .
Hoffmann M, Kleine-Weber H, Schroeder S, Krüger N, Herrler T, Erichsen S, et al. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell. 2020;181:271–80. https://doi.org/10.1016/j.cell.2020.02.052 .
doi: 10.1016/j.cell.2020.02.052
pubmed: 32142651
pmcid: 7102627
Cascella M, Rajnik M, Cuomo A, Dulebohn SC, Napoli RD. Features, evaluation and treatment coronavirus (COVID-19). In: Statpearls [Internet]. Treasure Island: StatPearls Publishing; 2020. p. 1–16.
Roychoudhury S, Das A, Sengupta P, Dutta S, Roychoudhury S, Kolesarova A, Hleba L, Massanyi P, Salma P. Viral pandemics of twenty-first century. J Microbiol Biotechnol Food Sci. 2021;11(1):711–6. https://doi.org/10.015414/jmbfs.2021.10.4
Bloom DE, Cadarette D. Infectious disease threats in the twenty-first century: strengthening the global response. Front Immunol. 2019;10:549.
doi: 10.3389/fimmu.2019.00549
Alex P, Salam PWH. The breadth of viruses in human semen. J Med Microbiol. 2000;49(10):937–40. https://doi.org/10.1099/0022-1317-49-10-937 .
doi: 10.1099/0022-1317-49-10-937
Corona G, et al. SARS-CoV-2 infection, male fertility and sperm cryopreservation: a position statement of the Italian Society of Andrology and Sexual Medicine (SIAMS). J Endocrinol Investig. 2020;43:1153–7. https://doi.org/10.1007/s40618-020-01290-w .
doi: 10.1007/s40618-020-01290-w
Dejucq N, Jégou B. Viruses in the mammalian male genital tract and their effects on the reproductive system. Microbiol Mol Biol Rev. 2001;65(2):208–31. https://doi.org/10.1128/mmbr.65.2.208-231.2001 .
doi: 10.1128/mmbr.65.2.208-231.2001
pubmed: 11381100
pmcid: 99025
La Vignera S, Vicari E, Condorelli RA, D’Agata R, Calogero AE. Male accessory gland infection and sperm parameters (review). Int J Androl. 2011;34(5PART 2) https://doi.org/10.1111/j.1365-2605.2011.01200.x .
Weidner W, Krause W, Ludwig M. Relevance of male accessory gland infection for subsequent fertility with special focus on prostatitis. Hum Reprod Update. 1999;5(5):421–32. https://doi.org/10.1093/humupd/5.5.421 .
doi: 10.1093/humupd/5.5.421
pubmed: 10582781
Bhushan S, Schuppe HC, Fijak M, Meinhardt A. Testicular infection: microorganisms, clinical implications and host-pathogen interaction. J Reprod Immunol. 2009;83(1–2):164–7. https://doi.org/10.1016/j.jri.2009.07.007 .
doi: 10.1016/j.jri.2009.07.007
pubmed: 19836838
Sarkar D. A Review on the Emerging Epidemic of Novel Coronavirus (nCoV- SARS CoV-2): Present Combating Strategies. Int J Pharm Sci. 2021;12(2):33–41. https://doi.org/10.22376/ijpbs.2021.12.2.b33-41 .
doi: 10.22376/ijpbs.2021.12.2.b33-41
Cardona-Maya W, Velilla PA, Montoya CJ, Cadavid Á, Rugeles MT. In vitro human immunodeficiency virus and sperm cell interaction mediated by the mannose receptor. J Reprod Immunol. 2011;92(1–2):1–7. https://doi.org/10.1016/j.jri.2011.09.002 .
doi: 10.1016/j.jri.2011.09.002
pubmed: 22015004
Dutta S, Thakare YR, Kshirsagar A, Sarkar D. A review on host genetic susceptibility to SARS CoV-2 related pneumonia. Int J Pharma Sci. 2021;12(2):b42–9. https://doi.org/10.22376/ijpbs.2021.12.2b42-49 .
doi: 10.22376/ijpbs.2021.12.2b42-49
Nickel JC. Prostatitis and related conditions, orchitis, and epididymitis. In: Wein AJ, editor. Campbell–Walsh urology. 10th ed. Philadelphia: Elsevier Saunders; 2011. [chapter 11] [Google Scholar].
Wald A, Matson P, Ryncarz A, Corey L. Detection of herpes simplex virus DNA in semen of men with genital HSV-2 infection. Sex Transm Dis. 1999;26:1–3. [PubMed] [Google Scholar]
doi: 10.1097/00007435-199901000-00001
Salam AP, Horby PW. The breadth of viruses in human semen. Emerg Infect Dis. 2017;23:1922–4.
doi: 10.3201/eid2311.171049
Dejucq-Rainsford N, Jegou B. Viruses in semen and male genital tissues—consequences for the reproductive system and therapeutic perspectives. Curr Pharm Des. 2004;10:557–75.
doi: 10.2174/1381612043453225
Murray K, Walker C, Herrington E, Lewis JA, McCormick J, Beasley DWC, Tesh RB, Fisher-Hoch S. Persistent infection with West Nile virus years after initial infection. J Infect Dis. 2010;201:2–4.
doi: 10.1086/648731
Bandeira AC, Campos GS, Rocha VF, Souza BS, Soares MB, Oliveira AA, Abreu YC, Menezes GS, Sardi S. Prolonged shedding of chikungunya virus in semen and urine: a new perspective for diagnosis and implications for transmission. IDCases. 2016;6:100–3.
doi: 10.1016/j.idcr.2016.10.007
Bornstein SR, Rutkowski H, Vrezas I. Cytokines and steroidogenesis. Mol Cell Endocrinol. 2004;215(1–2):135–41. https://doi.org/10.1016/j.mce.2003.11.022 .
doi: 10.1016/j.mce.2003.11.022
pubmed: 15026186
Wald A, Matson P, Ryncarz A, Corey L. Detection of herpes simplex virus DNA in semen of men with genital HSV-2 infection. Sex Transm Dis. 1999;26(1):1–3. https://doi.org/10.1097/00007435-199901000-00001 .
doi: 10.1097/00007435-199901000-00001
pubmed: 9918316
Dejucq N, Jégou B. Viruses in the mammalian male genital tract and their effects on the reproductive system. Microbiol Mol Biol Rev. 2001;65:208–31.
doi: 10.1128/MMBR.65.2.208-231.2001
Klimova RR, Chichev EV, Naumenko VA, et al. Herpes simplex virus and cytomegalovirus in male ejaculate: herpes simplex virus is more frequently encountered in idiopathic infertility and correlates with the reduction in sperm parameters. Vopr Virusol. 2010;55:27–31. [PubMed] [Google Scholar]
pubmed: 20364668
Mate SE, Kugelman JR, Nyenswah TG, Ladner JT, Wiley MR, Cordier-Lassalle T, Christie A, Schroth GP, Gross SM, Davies-Wayne GJ, et al. Molecular evidence of sexual transmission of Ebola virus. N Engl J Med. 2015;373:2448–54.
doi: 10.1056/NEJMoa1509773
Deen GF, Broutet N, Xu W, Knust B, Sesay FR, McDonald SLR, Ervin E, Marrinan JE, Gaillard P, Habib N, et al. Ebola RNA persistence in semen of Ebola virus disease survivors—preliminary report. N Engl J Med. 2017;377:1428–37.
doi: 10.1056/NEJMoa1511410
Dejucq N, Jégou B. Viruses in the mammalian male genital tract and their effects on the reproductive system. Microbiol Mol Biol Rev. 2001;65(2):208–31. https://doi.org/10.1128/MMBR.65.2.208-231.2001 .
doi: 10.1128/MMBR.65.2.208-231.2001
pubmed: 11381100
pmcid: 99025
Casella R, Leibundgut B, Lehmann K, Gasser TC. Mumps orchitis: report of a mini-epidemic. J Urol. 1997;158(6):2158–61. https://doi.org/10.1016/S0022-5347(01)68186-2 .
doi: 10.1016/S0022-5347(01)68186-2
pubmed: 9366335
Lafferty WE, Downey L, Celum C, Wald A. Herpes simplex virus type 1 as a cause of genital herpes: impact on surveillance and prevention. J Infect Dis. 2000;181:1454–7. [PubMed] [Google Scholar]
doi: 10.1086/315395
Mikuz G, Damjanov I. Inflammation of the testis, epididymis, peritesticular membranes, and scrotum. Pathol Annu. 1982;17:101–28. [PubMed] [Google Scholar]
pubmed: 6750533
Kapranos N, Petrakou E, Anastasiadou C, Kotronias D. Detection of herpes simplex virus, cytomegalovirus, and Epstein-Barr virus in the semen of men attending an infertility clinic. Fertil Steril. 2003;79(Suppl 3):1566–70. https://doi.org/10.1016/s0015-0282(03)00370-4 .
doi: 10.1016/s0015-0282(03)00370-4
pubmed: 12801561
Musso D, Roche C, Robin E, Nhan T, Teissier A, Cao-Lormeau VM. Potential sexual transmission of Zika virus. Emerg Infect Dis. 2015;21(2):359–61. https://doi.org/10.3201/eid2102.141363 .
doi: 10.3201/eid2102.141363
pubmed: 25625872
pmcid: 4313657
Schuppe HC, Pilatz A, Hossain H, Diemer T, Wagenlehner F, Weidner W. Urogenital infection as a risk factor for male infertility. Dtsch Arztebl Int. 2017;114(19):339–46. https://doi.org/10.3238/arztebl.2017.0339 .
doi: 10.3238/arztebl.2017.0339
pubmed: 28597829
pmcid: 5470348
Apari P, de Sousa JD, Muller V. Why sexually transmitted infections tend to cause infertility: an evolutionary hypothesis. PLoS Path. 2014;10(8):e1004111. https://doi.org/10.1371/journal.ppat.1004111Atkinson .
doi: 10.1371/journal.ppat.1004111Atkinson
Nguyen O, Sheppeard V, Douglas MW, Tu E, Rawlinson W. Acute hepatitis C infection with evidence of heterosexual transmission. J Clin Virol. 2010;49(1):65–8. https://doi.org/10.1016/j.jcv.2010.06.008 .
doi: 10.1016/j.jcv.2010.06.008
pubmed: 20667768
Sánchez-Montalvá A, Pou D, Sulleiro E, Salvador F, Bocanegra C, Treviño B, Rando A, Serre N, Pumarola T, Almirante B, et al. Zika virus dynamics in body fluids and risk of sexual transmission in a non-endemic area. Tropical Med Int Health. 2018;23:92–100.
doi: 10.1111/tmi.13019
Dejucq N, Jegou B. Viruses in the mammalian male genital tract and their effects on the reproductive system. Microbiol Mol Biol Rev. 2001;65(2):208–31. first and second pages, table of contents. https://doi.org/10.1128/MMBR.65.2.208-231.2001 .
doi: 10.1128/MMBR.65.2.208-231.2001
pubmed: 11381100
pmcid: 99025
Harrower J, Kiedrzynski T, Baker S, Upton A, Rahnama F, Sherwood J, Huang QS, Todd A, Pulford D. Sexual transmission of Zika virus and persistence in semen, New Zealand, 2016. Emerg Infect Dis. 2016;22:1855–7.
doi: 10.3201/eid2210.160951
Turmel JM, Abgueguen P, Hubert B, Vandamme YM, Maquart M, Le Guillou-Guillemette H, Leparc-Goffart I. Late sexual transmission of Zika virus related to persistence in the semen. Lancet. 2016;387:2501.
doi: 10.1016/S0140-6736(16)30775-9
Couto-Lima D, Madec Y, Bersot MI, Campos SS, Motta MA, Santos FBD, Vazeille M, Vasconcelos PFDC, Lourenço-de-Oliveira R, Failloux AB. Potential risk of re-emergence of urban transmission of yellow fever virus in Brazil facilitated by competent Aedes populations. Sci Rep. 2017;7:4848.
doi: 10.1038/s41598-017-05186-3
Barbosa CM, Di Paola N, Cunha MP, Rodrigues-Jesus MJ, Araujo DB, Silveira VB, Leal FB, Mesquita FS, Botosso VF, Zanotto PMA, et al. Yellow fever virus RNA in urine and semen of convalescent patient. Brazil Emerg Infect Dis. 2018;24:176–8.
doi: 10.3201/eid2401.171310
Venturi G, Zammarchi L, Fortuna C, Remoli ME, Benedetti E, Fiorentini C, Trotta M, Rizzo C, Mantella A, Rezza G, et al. An autochthonous case of Zika due to possible sexual transmission, Florence, Italy, 2014. Euro Surveill. 2016;21:30148.
pubmed: 26939607
Musso D, Roche C, Robin E, Nhan T, Teissier A, Cao-Lormeau VM. Potential sexual transmission of Zika virus. Emerg Infect Dis. 2015;21:2013–5.
doi: 10.3201/eid2110.151125
Mansuy JM, Dutertre M, Mengelle C, Fourcade C, Marchou B, Delobel P, Izopet J, Martin-Blondel G. Zika virus: high infectious viral load in semen, a new sexually transmitted pathogen? Lancet Infect Dis. 2016;16:405.
doi: 10.1016/S1473-3099(16)00138-9
Nguyen PV, Kafka JK, Ferreira VH, Roth K, Kaushic C. Innate and adaptive immune responses in male and female reproductive tracts in homeostasis and following HIV infection. Cell Mol Immunol. 2014;11:410–27.
doi: 10.1038/cmi.2014.41
Malolina EA, Kulibin AY, Naumenko VA, Gushchina EA, Zavalishina LE, Kushch AA. Herpes simplex virus inoculation in murine rete testis results in irreversible testicular damage. Int J Exp Pathol. 2014;95(2):120–30. Published online 2014 Feb 23. https://doi.org/10.1111/iep.12071 .
doi: 10.1111/iep.12071
pubmed: 24673915
pmcid: 3960039
Musso D, Richard V, Teissier A, Stone M, Lanteri MC, Latoni G, Alsina J, Reik R, Busch MP. Detection of Zika virus RNA in semen of asymptomatic blood donors. Clin Microbio Infect. 2017;23:1001.e1–3.
doi: 10.1016/j.cmi.2017.07.006
Foresta C, Pizzol D, Moretti A, Barzon L, Palu G, Garolla A. Clinical and prognostic significance of human papillomavirus DNA in the sperm or exfoliated cells of infertile patients and subjects with risk factors. Fertil Steril. 2010;94(5):1723–7.
doi: 10.1016/j.fertnstert.2009.11.012
Prisant N, Bujan L, Benichou H, Hayot P-H, Pavili L, Lurel S, Herrmann C, Janky E, Joguet G. Zika virus in the female genital tract. Lancet Infect Dis. 2016;16:1000–1.
doi: 10.1016/S1473-3099(16)30193-1
Davidson A, Slavinski S, Komoto K, Rakeman J, Weiss D. Suspected female-to-male sexual transmission of Zika virus—new York City, 2016. MMWR Morb Mortal Wkly Rep. 2016;65:716–7.
doi: 10.15585/mmwr.mm6528e2
Foresta C, Patassini C, Bertoldo A, Menegazzo M, Francavilla F, Barzon L, Ferlin A. Mechanism of human papillomavirus binding to human spermatozoa and fertilizing ability of infected spermatozoa. PLoS One. 2011;6(3):e15036. https://doi.org/10.1371/journal.pone.0015036 .
doi: 10.1371/journal.pone.0015036
pubmed: 21408100
pmcid: 3051064
Gimenes F, Souza RP, Bento JC, Teixeira JJ, Maria-Engler SS, Bonini MG, Consolaro ME. Male infertility: a public health issue caused by sexually transmitted pathogens. Nat Rev Urol. 2014;11(12):672–87. https://doi.org/10.1038/nrurol.2014.285 .
doi: 10.1038/nrurol.2014.285
pubmed: 25330794
Laprise C, Trottier H, Monnier P, Coutlee F, Mayrand MH. Prevalence of human papillomaviruses in semen: a systematic review and meta-analysis. Hum Reprod. 2014;29(4):640–51. https://doi.org/10.1093/humrep/det453 .
doi: 10.1093/humrep/det453
pubmed: 24365799
Croxson TS, Chapman WE, Miller LK, Levit CD, Senie R, Zumoff B. Changes in the hypothalamic-pituitary-gonadal axis in human immunodeficiency virus-infected homosexual men. J Clin Endocrinol Metab. 1989;68(2):317–21. https://doi.org/10.1210/jcem-68-2-317 .
doi: 10.1210/jcem-68-2-317
pubmed: 2493026
Poretsky L, Can S, Zumoff B. Testicular dysfunction in human immunodeficiency virus-infected men. Metabolism. 1995;44(7):946–53. https://doi.org/10.1016/0026-0495(95)90250-3 .
doi: 10.1016/0026-0495(95)90250-3
pubmed: 7616856
Matheron S, D’Ortenzio E, Leparc-Goffart I, Hubert B, de Lamballerie X, Yazdanpanah Y. Long-lasting persistence of Zika virus in semen. Clin Infect Dis. 2016;63:ciw509.
doi: 10.1093/cid/ciw509
Lai YM, Lee JF, Huang HY, Soong YK, Yang FP, Pao CC. The effect of human papillomavirus infection on sperm cell motility. Fertil Steril. 1997;67(6):1152–5. https://doi.org/10.1016/S0015-0282(97)81454-9 .
doi: 10.1016/S0015-0282(97)81454-9
pubmed: 9176459
Gimenes F, Souza RP, Bento JC, Teixeira JJ, Maria-Engler SS, Bonini MG, Consolaro ME. Male infertility: a public health issue caused by sexually transmitted pathogens. Nat Rev Urol. 2014;11(12):672–87. https://doi.org/10.1038/nrurol.2014.285 .
doi: 10.1038/nrurol.2014.285
pubmed: 25330794
Hills SL, Russell K, Hennessey M, Williams C, Oster AM, Fischer M, Mead P. Transmission of Zika virus through sexual contact with travelers to areas of ongoing transmission—continental United States, 2016. MMWR Morb Mortal Wkly Rep. 2016;65:215–6.
doi: 10.15585/mmwr.mm6508e2
Gimenes F, Souza RP, Bento JC, Teixeira JJ, Maria-Engler SS, Bonini MG, Consolaro ME. Male infertility: a public health issue caused by sexually transmitted pathogens. Nat Rev Urol. 2014;11(12):672–87. https://doi.org/10.1038/nrurol.2014.285 .
doi: 10.1038/nrurol.2014.285
pubmed: 25330794
Huang JM, Huang TH, Qiu HY, Fang XW, Zhuang TG, Qiu JW. Studies on the integration of hepatitis B virus DNA sequence in human sperm chromosomes. Asian J Androl. 2002;4(3):209–12.
pubmed: 12364978
Jenabian MA, Costiniuk CT, Mehraj V, Ghazawi FM, Fromentin R, Brousseau J, Brassard P, Bélanger M, Ancuta P, Bendayan R, et al. Immune tolerance properties of the testicular tissue as a viral sanctuary site in ART-treated HIV-infected adults. AIDS. 2016;30:2777–86.
doi: 10.1097/QAD.0000000000001282
La Vignera S, Condorelli RA, Vicari E, D'Agata R, Calogero AE. Sperm DNA damage in patients with chronic viral C hepatitis. Eur J Intern Med. 2012;23(1):e19–24. https://doi.org/10.1016/j.ejim.2011.08.011 .
doi: 10.1016/j.ejim.2011.08.011
pubmed: 22153543
Dutta S, Sengupta P. SARS-CoV-2 infection, oxidative stress and male reproductive hormones: can testicular-adrenal crosstalk be ruled-out? J Basic Clin Physiol. 2020;31:20200205. https://doi.org/10.1515/jbcpp-2020-0205 .
doi: 10.1515/jbcpp-2020-0205
Citil Dogan A, Wayne S, Bauer S, Ogunyemi D, Kulkharni SK, Maulik D, Carpenter CF, Bahado-Singh RO. The Zika virus and pregnancy: evidence, management, and prevention. J Matern Neonatal Med. 2017;30:386–96.
doi: 10.3109/14767058.2016.1174210
Yeniyol CO, Sorguc S, Minareci S, Ayder AR. Role of interferon-alpha-2B in prevention of testicular atrophy with unilateral mumps orchitis. Urology. 2000;55(6):931–3. https://doi.org/10.1016/S0090-4295(00)00491-X .
doi: 10.1016/S0090-4295(00)00491-X
pubmed: 10840112
Klein SL, Dhakal S, Ursin RL, Deshpande S, Sandberg K, Mauvais-Jarvis F. Biological sex impacts COVID-19 outcomes. PLoS Pathog. 2020;16:e1008570.
doi: 10.1371/journal.ppat.1008570
Theas MS, Rival C, Jarazo-Dietrich S, Jacobo P, Guazzone VA, Lustig L. Tumour necrosis factor-alpha released by testicular macrophages induces apoptosis of germ cells in autoimmune orchitis. Hum Reprod. 2008;23(8):1865–72.
doi: 10.1093/humrep/den240
Alahmar AT. Role of oxidative stress in male infertility: an updated review. J Hum Reprod Sci. 2019;12:4–18. https://doi.org/10.4103/jhrs.JHRS_150_18 .
doi: 10.4103/jhrs.JHRS_150_18
pubmed: 31007461
pmcid: 6472207
Li N, Wang T, Han D. Structural, cellular and molecular aspects of immune privilege in the testis. Front Immunol. 2012;3:152.
pubmed: 22701457
pmcid: 3371599
Loveland KL, Klein B, Pueschl D, Indumathy S, Bergmann M, Loveland BE, Hedger MP, Schuppe H-C. Cytokines in male fertility and reproductive pathologies: immunoregulation and beyond. Front Endocrinol (Lausanne). 2017;8:307.
doi: 10.3389/fendo.2017.00307
Mladinich MC, Schwedes J, Mackow ER. Zika virus persistently infects and is basolaterally released from primary human brain microvascular endothelial cells. mBio. 2017;8:e00952-17.
doi: 10.1128/mBio.00952-17
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: 10.3390/cells9040920