COVID-19 and its implications on male and female fertility: future impacts

Authors

DOI:

https://doi.org/10.33448/rsd-v11i16.38217

Keywords:

SARS-CoV-2; Infertility; Reproductive System.

Abstract

In recent years, the COVID-19 has been the focus of studies, widely explored by specialists from different areas, involving different research potentials due to the viral tropism for receptors in human body systems. Angiotensin-Converting Enzyme 2 (ACE2) is considered the main viral gateway, being located in different tissues and organs, allowing SARS-CoV-2 to affect various parts of the human body, including the reproductive system. The aim of this integrative review is to investigate the effects caused by the parhogenicity of the SARS- CoV-2 virus on reproductive system involving fertility. Thus, the question arises of the possibility that the virus promotes infertility due to the presence of ACE2 in the reproductive system, and the need to identify the possible effects that the virus can trigger. Studies indicate that in the female reproductive system, it was observed in post-infected patients: premature ovarian failure, involvement and damage of granulosa cells and ovarian tissues, alteration of the menstrual cycle, and hormonal alterations. About the male reproductive system, negative impacts were identified, such as the involvement of Sertoli cells and a decrease in Leydig cells, changes in hormone levels, reduction in the quantity and quality of sperm, leukocyte infiltrate in the testicular interstitial, orchitis, thickening basement membrane, destruction of germ cells and fragmentation of sperm DNA. Despite research indicating the possible damage caused by SARS-CoV-2 to the male and female reproductive system, there is a need for more theoretical and practical studies, which prove, through underlying mechanisms, the possible future impacts after viral infection on human fertility.

References

Abdelhamid, M.H.M., Fellah, A.A., Elmarghani, A., & Al Msellati, I.A. (2022). An Assessment of Men Semen Alterations in SARS-CoV-2: Is Fever the Principal Concern? Reproductive Sciences, 1–9.

Ahmadpour, D., & Ahmadpoor, P. (2020). How the COVID-19 Overcomes the Battle? An Approach to Virus Structure. Iran J Kidney Dis, 14(3), 167-172.

Bai, C., Zhong, Q., & Gao, G.F. (2021). Overview of SARS-CoV-2 genome-encoded proteins. Sci China Life Sci, 65(2), 280-294.

Bardin, L. (1977). L´analyse de contenu. Lisboa, Portugal: Edição 70.

Belouzard, S., Millet, J.K., Licitra, B.N., & Whittaker, G.R. (2012). Mechanisms of coronavirus cell entry mediated by the viral spike protein. Viruses, 4(6), 1011-1033.

Chen, H., Guo, J., Wang, C., Luo, F., Yu, X., Zhang, W., Li, J., Zhao, D., Xu, D., Gong, Q., Liao, J., Yang, H., Hou, W., & Zhang, Y. (2020). Clinical characteristics and intrauterine vertical transmission potential of COVID-19 infection in nine pregnant women: a retrospective review of medical records. Lancet, 395(10226), 809-815.

Cui, P., Chen, Z., Wang, T., Dai, J., Zhang, J., Ding, T., Jiang, J., Liu, J., Zhang, C., Shan, W., Wang, S., Rong, Y., Chang, J., Miao, X., Ma, X., & Wang, S. (2020). Severe acute respiratory syndrome coronavirus 2 detection in the female lower genital tract. Am J Obstet Gynecol, 223(1), 131-134.

Ding, T., Wang, T., Zhang, J., Cui, P., Chen, Z., Zhou, S., Yuan, S., Ma, W., Zhang, M., Rong, Y., Chang, J., Miao, X., Ma, X., & Wang, S. (2021). Analysis of Ovarian Injury Associated With COVID-19 Disease in Reproductive-Aged Women in Wuhan, China: An Observational Study. Front Med (Lausanne), 8, 1-11.

Ding, Y., He, L., Zhang, Q., Huang, Z., Che, X., Hou, J., Wang, H., Shen, H., Qiu, L., Li, Z., Geng, J., Cai, J., Han, H., Li, X., Kang, W., Weng, D., Liang, P., & Jiang, S. (2004). Organ distribution of severe acute respiratory syndrome (SARS) associated coronavirus (SARS-CoV) in SARS patients: implications for pathogenesis and virus transmission pathways. J Pathol, 203(2), 622-630.

Donders, G.G.G., Bosmans, E., Reumers, J., Donders, F., Jonckheere, J., Salembier, G., Stern, N., Jacquemyn, Y., Ombelet, W., & Depuydt, C.E. (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. Fertil Steril, 117(2), 287-296.

Evers, J.L. (2017). Towards prospective trial registration in Human Reproduction: step 3 of 3. Hum Reprod, 32(1), 1.

Fehr, A.R., & Perlman, S. (2015). Coronaviruses: an overview of their replication and pathogenesis. Methods Mol Biol, 1282, 1-23.

Gagliardi, M.C., Tieri, P., Ortona, E., & Ruggieri, A. (2020). ACE2 expression and sex disparity in COVID-19. Cell Death Discov, 6, 37.

Gheblawi, M., Wang, K., Viveiros, A., Nguyen, Q., Zhong, J.C., Turner, A.J., Raizada, M.K., Grant, M.B., & Oudit, G.Y. (2020). Angiotensin-Converting Enzyme 2: SARS-CoV-2 Receptor and Regulator of the Renin-Angiotensin System: Celebrating the 20th Anniversary of the Discovery of ACE2. Circ Res, 126(10), 1456-1474.

Gul, M. H., Htun, Z. M., & Inayat, A. (2020). Role of fever and ambient temperature in COVID-19. Expert Review of Respiratory Medicine, 15 (2), 171-173.

He, W., Liu, X., Feng, L., Xiong, S., Li, Y., Chen, L., Li, Y., Wang, G., Li, D., & Fu, B. (2020). Impact of SARS-CoV-2 on Male Reproductive Health: A Review of the Literature on Male Reproductive Involvement in COVID-19. Front Med (Lausanne), 7, 1-37.

Hoffmann, M., Kleine-Weber, H., Schroeder, S., Krüger, N., Herrler, T., Erichsen, S., Schiergens, T.S., Herrler, G., Wu, N.H., Nitsche, A., Müller, M.A., Drosten, C., & Pöhlmann, S. (2020). SARS-CoV-2 Cell Entry Depends on ACE2 and TMPRSS2 and Is Blocked by a Clinically Proven Protease Inhibitor. Cell, 181(2), 271-280.

Holtmann. N., Edimiris, P., Andree, M., Doehmen, C., Baston-Buest, D., Adams, O., Kruessel, J.S., & Bielfeld, A.P. (2020). Assessment of SARS-CoV-2 in human semen-a cohort study. Fertil Steril, 114(2), 233-238.

Hu, B., Guo, H., Zhou, P., & Shi, Z.L. (2021). Characteristics of SARS-CoV-2 and COVID-19. Nat Rev Microbiol, 19(3),141-154.

Jackson, C.B., Farzan, M., Chen, B., & Choe, H. (2022). Mechanisms of SARS-CoV-2 entry into cells. Nat Rev Mol Cell Biol, 23(1), 3-20.

Jing, Y., Run-Qian, L., Hao-Ran, W., Hao-Ran, C., Ya-Bin, L., Yang, G., & Fei, C. (2020). Potential influence of COVID-19/ACE2 on the female reproductive system. Mol Hum Reprod, 26(6), 367-373.

Ke, Z., Oton, J., Qu, K., Cortese, M., Zila, V., McKeane, L., Nakane, T., Zivanov, J., Neufeldt, C.J., Cerikan, B., Lu, J.M., Peukes, J., Xiong, X., Kräusslich, H.G., Scheres, S.H.W., Bartenschlager, R., & Briggs, J.A.G. (2020). Structures and distributions of SARS-CoV-2 spike proteins on intact virions. Nature, 588(7838), 498-502.

Keidar, S., Kaplan, M., & Gamliel-Lazarovich, A. (2007). ACE2 of the heart: From angiotensin I to angiotensin (1-7). Cardiovasc Res, 73(3), 463-469.

Khalili, M.A., Leisegang, K., Majzoub, A., Finelli, R., Panner Selvam, M.K., Henkel, R., Mojgan, M., & Agarwal, A. (2020). Male Fertility and the COVID-19 Pandemic: Systematic Review of the Literature. World J Mens Health, 38(4), 506-520.

Li, F., Lu, H., Zhang, Q., Li, X., Wang, T., Liu, Q., Yang, Q., & Qiang, L. (2021). Impact of COVID-19 on female fertility: a systematic review and meta-analysis protocol. BMJ Open, 11(2), 1-21.

Li, G., Tang, D., Song, B., Wang, C., Qunshan, S., Xu, C., Geng, H., Wu, H., He, X., & Cao, Y. (2020). Impact of the COVID-19 Pandemic on Partner Relationships and Sexual and Reproductive Health: Cross-Sectional, Online Survey Study. J Med Internet Res, 22(8), 1-15. Li, K., Chen, G., Hou, H., Liao, Q., Chen, J., Bai, H., Lee, S., Wang, C., Li, H., Cheng, L., & Ai, J. (2021). Analysis of sex hormones and menstruation in COVID-19 women of child-bearing age. Reprod Biomed Online, 42(1), 260-267.

Li, R., Yin, T., Fang, F., Li, Q., Chen, J., Wang, Y., Hao, Y., Wu, G., Duan, P., Wang, Y., Cheng, D., Zhou, Q., Zafar, M.I., Xiong, C., Li, H., Yang, J., & Qiao, J. (2020). Potential risks of SARS-CoV-2 infection on reproductive health. Reprod Biomed Online, 41(1), 89-95.

Li ,Y.C., Bai, W.Z., & Hashikawa, T. (2020). The neuroinvasive potential of SARS-CoV2 may play a role in the respiratory failure of COVID-19 patients. J Med Virol, 92(6), 552-555.

Liu, C., Mu, C., Zhang, Q., Yang, X., Yan, H., & Jiao, H. (2021). Effects of Infection with SARS-CoV-2 on the Male and Female Reproductive Systems: A Review. Medical Science Monitor, 27, 1-7.

Ma, X., Guan, C., Chen, R., Wang, Y., Feng, S., Wang, R., Qu, G., Zhao, S., Wang, F., Wang, X., Zhang D., Liu, L., Liao, A., & Yuan, S. (2021). 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.

Mahdian, S., Shahhoseini, M., & Moini, A. (2020). COVID-19 Mediated by Basigin Can Affect Male and Female Fertility. Int J Fertil Steril, 14(3), 262-263.

Mahmudpour, M., Roozbeh, J., Keshavarz, M., Farrokhi, S., & Nabipour, I. (2020). COVID-19 cytokine storm: The anger of inflammation. Cytokine, 133, 1-11.

Matsuyama, S., Nagata, N., Shirato, K., Kawase, M., Takeda, M., & Taguchi, F. (2010). Efficient activation of the severe acute respiratory syndrome coronavirus spike protein by the transmembrane protease TMPRSS2. J Virol, 84(24), 12658-12664.

Millet, J.K., & Whittaker, G.R. (2015). Host cell proteases: Critical determinants of coronavirus tropism and pathogenesis. Virus Research, 202, 120-134.

Millet, J.K., & Whittaker, G.R. (2017). Physiological and molecular triggers for SARS-CoV membrane fusion and entry into host cells. Virology, 517, 3-8.

Musa, S.S., Bello, U.M., Zhao, S., Abdullahi, Z.U., Lawan, M.A., & He, D. (2021). Vertical Transmission of SARS-CoV-2: A Systematic Review of Systematic Reviews. Viruses, 13(9), 1-20.

Omolaoye, T.S., Adeniji, A.A., Maya, W.D.C., & Plessis, S.S. (2021). SARS-COV-2 (Covid-19) and male fertility: Where are we? Reproductive Toxicology, 99, 65-70.

Ou, X., Liu, Y., Lei, X., Li, P., Mi, D., Ren, L., Guo, L., Guo, R., Chen, T., Hu, J., Xiang, Z., Um, Z., Chen, X., Chen, J., Hu, K., Jin, Q., Wang, J., & Qian, Z. (2020). Characterization of spike glycoprotein of SARS-CoV-2 on virus entry and its immune cross-reactivity with SARS-CoV. Nat Commun, 11(1), 1-12.

Oyola, M.G., & Handa, R.J. (2017). Hypothalamic-pituitary-adrenal and hypothalamic-pituitary-gonadal axes: sex differences in regulation of stress responsivity. Stress, 20(5), 476-494.

O'hara, L., & Smith, L. B. (2015). Androgen receptor roles in spermatogenesis and infertility. Best Pract Res Clin Endocrinol Metab, 29(4), 595-605.

Pan, F., Xiao, X., Guo, J., Song, Y., Li, H., Patel, D.P., Spivak, A.M., Alukal, J.P., Zhang, X., Xiong, C., Li, P.S., & Hotaling, J.M. (2020). No evidence of severe acute respiratory syndrome-coronavirus 2 in semen of males recovering from coronavirus disease 2019. Fertil Steril, 113(6), 1135-1139.

Plant, T.M. (2015). 60 YEARS OF NEUROENDOCRINOLOGY: The hypothalamo-pituitary-gonadal axis. J Endocrinol, 226(2), 41-54.

Puca, E., & Puca, E. (2022). Premature Ovarian Failure Related to SARS-CoV-2 infection. J Med Cases, 13(4), 155-158.

Qiu, L., Liu, X., Xiao, M., Xie, J., Cao, W., Liu, Z., Morse, A., Xie, Y., Li, T., & Zhu, L. (2020). SARS-CoV-2 Is Not Detectable in the Vaginal Fluid of Women With Severe COVID-19 Infection. Clin Infect Dis, 71(15), 813-817.

Racilan, A.M., Assis, W.A., Casalechi, M., Spagnolo-Souza, A., Pascoal-Xavier, M.A., Simões-E-Silva, A.C., Del Puerto, H.L., & Reis F.M. (2021). Angiotensin-converting enzyme 2, the SARS-CoV-2 cellular receptor, is widely expressed in human myometrium and uterine leiomyoma. J Endometr Pelvic Pain Disord, 13(1), 20-24.

Rahimi, A., Mirzazadeh, A., & Tavakolpour, S. (2021). Genetics and genomics of SARS-CoV-2: A review of the literature with the special focus on genetic diversity and SARS-CoV-2 genome detection. Genomics, 113, 1221-1232.

Rajak, P., Roy, S., Dutta, M., Podder, S., Sarkar, S., Ganguly, A., Mandi, M., & Khatun, S. (2021). Understanding the cross-talk between mediators of infertility and COVID-19. Reprod Biol, 21(4), 1-13.

Rastogi, M., Pandey, N., Shukla, A., & Singh, S.K. (2020). SARS coronavirus 2: from genome to infectome. Respir Res, 21, 1-15.

Rastrelli, G., Di Stasi, V., Inglese, F., Beccaria, M., Garuti, M., Di Costanzo, D., Spreafico, F., Greco, G.F., Cervi, G., Pecoriello, A., Magini, A., Todisco, T., Cipriani, S., Maseroli, E., Corona, G., Salonia, A., Lenzi, A., Maggi, M., De Donno, G., Vignozzi, L. (2021). Low testosterone levels predict clinical adverse outcomes in SARS-CoV-2 pneumonia patients. Andrology, 9, 88– 98.

Reis, F.M., Bouissou, D.R., Pereira, V.M., Camargos, AF., dos Reis, AM., & Santos, RA. (2011). Angiotensin-(1-7), its receptor Mas, and the angiotensin-converting enzyme type 2 are expressed in the human ovary. Fertil Steril, 95(1),176-181.

Salamanna, F., Maglio, M., Landini, M.P., & Fini, M. (2020). Body Localization of ACE-2: On the Trail of the Keyhole of SARS-CoV-2. Frontiers in Medicine, 7, 1-24.

Salam, A.P., & Horby, P.W. (2017). The Breadth of Viruses in Human Semen. Emerg Infect Dis, 23(11), 1922-1924.

Selvaraj, K., Ravichandran, S., Krishnan, S., Radhakrishnan R. K., Manickman N. & Kandasamy M. (2021). Testicular Atrophy and Hypothalamic Pathology in COVID-19: Possibility of the Incidence of Male Infertility and HPG Axis Abnormalities. Reproductive Sciences, 28, 2735-2742.

Sengupta, P., & Dutta, S. (2020). Does SARS-CoV-2 infection cause sperm DNA fragmentation? Possible link with oxidative stress. The European Journal of Contraception & Reproductive Health Care, 25(5), 405-406.

Song, C., Wang, Y., Li, W., Hu, B., Chen, G., Xia, P., Wang, W., Li, C., Diao, F., Hu, Z., Yang, X., Yao, B., & Liu, Y. (2020). Absence of 2019 novel coronavirus in semen and testes of COVID-19 patients†. Biol Reprod, 103(1), 4-6.

Souza, M.T., Silva, M.D., & Carvalho, R. (2010). Revisão integrativa: o que é e como fazer. Einstein, 8(1 Pt 1), 102-106.

Takahashi, T., Ellingson, M.K, Wong, P., Israelow, B., Lucas, C., Klein, J., Silva, J., Mao, T., Oh, J.E., Tokuyama, M., Lu, P., Venkataraman, A., Park, A., Liu, F., Meir, A., Sun, J., Wang, E.Y., Casanovas-Massana, A., Wyllie, A.L., Vogels, C.B.F., Earnest, R., Lapidus, S., Ott, I.M., Moore, A.J., Team, Y.I.R., Shaw, A., Fournier, J.B., Odio, C.D., Farhadian, S., Cruz, C.D., Grubaugh, N.D., Schulz, W.L., Ring, A.M., Ko, A.I., Omer, S.B., & Iwasaki, A. (2020). Sex differences in immune responses that underlie COVID-19 disease outcomes. Nature, 588, 315-320.

Tian, Y., & Zhou, L. (2021). Evaluating the impact of COVID-19 on male reproduction. Reproduction, 161(2), 37-44.

Troyano-Hernáez, P., Reinosa, R., & Holguín, Á. (2021). Evolution of SARS-CoV-2 Envelope, Membrane, Nucleocapsid, and Spike Structural Proteins from the Beginning of the Pandemic to September 2020: A Global and Regional Approach by Epidemiological Week. Viruses, 13(2), 243.

Tukiainen, T., Villani, A.C., Yen, A., Rivas, M.A., Marshall, J.L., Satija, R., Aguirre, M., Gauthier, L., Fleharty, M., Kirby, A., Cummings, B.B., Castel, S.E., Karczewski, K.J., Aguet, F., Byrnes, A., GTEx Consortium, Laboratory, Data Analysis & Coordinating Center (LDACC)—Analysis Working Group, Statistical Methods groups—Analysis Working Group, Enhancing GTEx (eGTEx) groups, NIH Common Fund, NIH/NCI, NIH/NHGRI, NIH/NIMH, NIH/NIDA, Biospecimen Collection Source Site—NDRI, Biospecimen Collection Source Site—RPCI, Biospecimen Core Resource—VARI, Brain Bank Repository—University of Miami Brain Endowment Bank, Leidos Biomedical—Project Management, ELSI Study, Genome Browser Data Integration &Visualization—EBI, Genome Browser Data Integration & Visualization—UCSC Genomics Institute, University of California Santa Cruz, Lappalainen, T., Regev, A., Ardlie, K.G., Hacohen, N., & MacArthur, D.G. (2017). Landscape of X chromosome inactivation across human tissues. Nature, 550(7675), 244-248.

Turato, E.R. (2005). Métodos qualitativos e quantitativos na área da saúde: definições, diferenças e seus objetos de pesquisa. Rev. Saúde Pública, 39 (3), 507-514.

Ulrich, H., & Pillat, M.M. (2020). CD147 as a Target for COVID-19 Treatment: Suggested Effects of Azithromycin and Stem Cell Engagement. Stem Cell Rev Rep, 16(3), 434-440.

Vaz-Silva, J., Carneiro, M.M., Ferreira, M.C., Pinheiro, S.V., Silva, D.A., Silva-Filho, A.L., Witz, C.A., Reis, A.M., Santos, R.A., & Reis, F.M. (2009) The vasoactive peptide angiotensin-(1-7), its receptor Mas and the angiotensin-converting enzyme type 2 are expressed in the human endometrium. Reprod Sci, 16(3), 247-256.

Vishvkarma, R., & Rajender S. (2020). Could SARS-CoV-2 affect male fertility? Andrologia, 52(9), 1-8.

V'kovski, P., Kratzel, A., Steiner, S., Stalder, H., & Thiel, V. (2021). Coronavirus biology and replication: implications for SARS-CoV-2. Nat Rev Microbiol, 19(3), 155-170.

Wang, K., Chen, W., Zhang, Z., Deng, Y., Lian, J.Q., Du, P., Wei, D., Zhang, Y., Sun, X.X., Gong, L., Yang, X., He, L., Zhang, L., Yang, Z., Geng, J.J., Chen, R., Zhang, H., Wang, B., Zhu, Y.M., Nan, G., Jiang, J.L., Li, L., Wu, J., Lin, P., Huang, W., Xie, L., Zheng, Z.H., Zhang, K., Miao, J.L., Cui, H.Y., Huang, M., Zhang, J., Fu, L., Yang, X.M., Zhao, Z., Sun, S., Gu, H., Wang, Z., Wang, C.F., Lu, Y., Liu, Y.Y., Wang, Q.Y., Bian, H., Zhu, P., & Chen, Z.N. (2020). CD147-spike protein is a novel route for SARS-CoV-2 infection to host cells. Signal Transduct Target Ther, 5(1), 1-10.

Wang, M.Y., Zhao, R., Gao, L.J., Gao, X.F., Wang, D.P., & Cao, J.M. (2020). SARS-CoV-2: Structure, Biology, and Structure-Based Therapeutics Development. Front Cell Infect Microbiol, 10, 1-17.

Wang, N., Qin, L., Ma, L., & Yan, H. (2021). Effect of severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) on reproductive system. Stem Cell Res, 52, 1-10.

Wang, Y., Pringle, K.G., Sykes, S.D., Marques, F.Z., Morris, B.J., Zakar, T., & Lumbers, E.R. (2012). Fetal sex affects expression of renin-angiotensin system components in term human decidua. Endocrinology, 153(1), 462-468.

Wang, Z., & Xu, X. (2020). 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, 9(4),1-9.

Weiss, S.R., & Navas-Martin, S. (2005). Coronavirus pathogenesis and the emerging pathogen severe acute respiratory syndrome coronavirus. Microbiol Mol Biol Ver, 69(4), 635-664.

Wilkins, J., & Al-Inizi, S. (2021). Premature ovarian insufficiency secondary to COVID-19 infection: An original case report. Int J Gynaecol Obstet, 154(1), 179-180.

Xia, X. (2021). Domains and Functions of Spike Protein in Sars-Cov-2 in the Context of Vaccine Design. Viruses, 13(1), 109.

Xu, J., Qi, L., Chi, X., Yang, J., Wei, X., Gong, E., Peh, S., & Gu, J. (2006). Orchitis: a complication of severe acute respiratory syndrome (SARS). Biol Reprod, 74(2), 410-416.

Yan, R., Zhang, Y., Li, Y., Xia, L., Guo, Y., & Zhou, Q. (2020). Structural basis for the recognition of SARS-CoV-2 by full-length human ACE2. Science, 367(6485), 1444-1448.

Yang, M., Chen, S., Huang, B., Zhong, J.M., Su, H., Chen, Y.J., Cao, Q., Ma, L., He, J., Li, X.F., Li, X., Zhou, J.J., Fan, J., Luo, D.J., Chang, X.N., Arkun, K., Zhou, M., & Nie, X. (2020). Pathological Findings in the Testes of COVID-19 Patients: Clinical Implications. Eur Urol Focus, 6(5), 1124-1129.

Younis, J.S., Abassi, Z., & Skorecki, K. (2020) Is there an impact of the COVID-19 pandemic on male fertility? The ACE2 connection. Am J Physiol Endocrinol Metab, 318(6), 878-880.

Zangeneh, F.Z. (2022). Interaction of SARS-CoV-2 With RAS / ACE2 in the Female Reproductive System. Journal of Family and Reproductive Health, 16(1), 1-8.

Zhang, H., Penninger, J.M., Li, Y., Zhong, N., & Slutsky, A.S. (2020). Angiotensin-converting enzyme 2 (ACE2) as a SARS-CoV-2 receptor: molecular mechanisms and potential therapeutic target. Intensive Care Med, 46(4), 586-590.

Zhao, J.M., Zhou, G.D., Sun, Y.L., Wang, S.S., Yang, J.F., Meng, E.H., Pan, D., Li, W.S., Zhou, X.S., Wang, Y.D., Lu, J.Y., Li, N., Wang, D.W., Zhou, B.C., & Zhang, T.H. (2003). [Clinical pathology and pathogenesis of severe acute respiratory syndrome]. Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi, 17(3), 217-221.

Zhou, P., Yang, X.L., Wang, X.G., Hu, B., Zhang, L., Zhang, W., Si, H.R., Zhu, Y., Li, B., Huang, C.L., Chen, H.D., Chen, J., Luo, Y., Guo, H., Jiang, R.D., Liu, M.Q., Chen, Y., Shen, X.R., Wang, X., Zheng, X.S., Zhao, K., Chen, Q.J., Deng, F., Liu, L.L., Yan, B., Zhan, F.X., Wang, Y.Y., Xiao, G.F., & Shi, Z.L. (2020). A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature, 579 (7798), 270–273.

Zirkin, Barry R. (1998). Spermatogenesis: its regulation by testosterone and FSH. Seminars in Cell & Developmental Biology, 9 (4), 417-421.

Published

11/12/2022

How to Cite

MOURA, J. A. D.; FELIX, E. M. de S.; PADILHA , D. de M. M. . COVID-19 and its implications on male and female fertility: future impacts. Research, Society and Development, [S. l.], v. 11, n. 16, p. e352111638217, 2022. DOI: 10.33448/rsd-v11i16.38217. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/38217. Acesso em: 19 apr. 2024.

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Review Article