سلول‌های میزبان متاثر در بافت‌های تولید مثلی مردانه و مسیرهای سیگنال‌دهی مرتبط با عفونت SARS-Cov-2

نوع مقاله : Review Article

نویسندگان

1 کارشناس ارشد ژنتیک،گروه ژنتیک پزشکی، دانشکده‌ی پزشکی، دانشگاه علوم پزشکی تهران، تهران، ایران

2 کارشناس زیست‌شناسی،کمیته‌ی تحقیقات دانشجویی، دانشگاه علوم پزشکی کرمانشاه، کرمانشاه، ایران

3 کارشناس ارشد ژنتیک،گروه ژنتیک پزشکی، دانشکده‌ی علوم پزشکی، دانشگاه علوم پزشکی هرمزگان، بندرعباس، ایران

4 استادیار، فلوشیپ آندرولوژی (ناباروری و اختلالات جنسی مردان)، گروه اورولوژی، دانشکده‌ی پزشکی، دانشگاه علوم پزشکی شیراز، شیراز، ایران

5 گروه زیست‌شناسی، دانشکده‌ی علوم پایه و فنی مهندسی، دانشگاه گنبدکاووس، گنبدکاووس، ایران

6 استاد، فلوشیپ نازایی و lVF، گروه زنان و زایمان، دانشکده‌ی پزشکی، دانشگاه علوم پزشکی شیراز، شیراز، ایران

7 استادیار، دکترای تخصصی بیوتکنولوژی پزشکی، مرکز تحقیقات پزشکی مولکولی، پژوهشکده‌ی سلامت هرمزگان، دانشگاه علوم پزشکی هرمزگان، بندرعباس، ایران

8 استاد، دکترای تخصصی ژنتیک مولکولی انسانی مرکز تحقیقات و بالینی ناباروری، دانشگاه علوم پزشکی شهید صدوقی، یزد، ایران

9 استادیار، دکترای تخصصی زیست‌شناسی سلولی و مولکولی، مرکز تحقیقات ناباروری، دانشگاه علوم پزشکی شیراز، شیراز، ایران

چکیده

مقاله مروری




مقدمه: COVID-19 که توسط ویروس  SARS-CoV-2ایجاد می‌شود، با آسیب به چندین سیستم ارگان مرتبط است. یکی از جنبه‌های قابل توجه این ویروس تأثیر آن بر باروری مردان و دستگاه تناسلی است. هدف ما جهت بررسی اجمالی مسیرهای مولکولی درگیر به منظور پیش‌بینی اثرات ویروس بر سیستم تناسلی مردان، اسپرم‌زایی و پارامترهای مایع منی می‌باشد.
روش‌ها: پایگاه‌های اطلاعاتی PubMed و Scopus (مقالات منتشر شده از سال 2020 تا 2023) برای مطالعاتی که تأثیر کووید-19 را بر مسیرهای مرتبط با سیستم تناسلی مردان در سطح سلولی گزارش می‌کنند، جستجو گردید و 98 مقاله بررسی شد.
یافته‌ها: اثرات کووید-19 ممکن است مستقیماً به دلیل حملات ویروس به دستگاه تناسلی مردان ایجاد شود و یا ممکن است به دلیل واکنش بیش از حد نامطلوب پاسخ ایمنی، مانند طوفان سیتوکین‌ها یا کاهش آن‌ها باشد. سیستم رنین-آنژیوتانسین و مسیر سیگنالینگ PI3K/AKT نیز درگیر هستند. تعداد و تحرک اسپرم کاهش می‌یابد، اگرچه تقریباً بهبودی در عرض چند ماه مشاهده شد. برخلاف داروهای مورد استفاده برای درمان کووید-19 که اثرات متناقضی نشان دادند به نظر می‌رسد واکسن‌ها هیچ اثر نامطلوب ملموسی بر باروری مردان ندارند.
نتیجه‌گیری: تأثیر SARS-CoV-2 بر باروری و سیستم تولید مثل مردان به دلیل وجود دو عامل میزبان اصلی شامل ACE2 و TMPRSS2 و درگیر شدن مسیرهای مرتبط قابل توجه است. می‌توان به درگیری بالقوه این اندام‌ها و اثرات بعدی آن بر نسل‌های آینده اشاره کرد. درک این فرایند ممکن است سرنخی برای مدیریت اثربخش ارائه دهد.

تازه های تحقیق

بهیه نام آور جهرمی: Google Scholar, PubMed

پگاه موسوی: Google Scholar, PubMed

سودابه ثابتیان: Google Scholar, PubMed

کلیدواژه‌ها

موضوعات

عنوان مقاله [English]

Affected Host Cells in Male Reproductive Tissue and Relevant Signaling Pathways Associated with SARS-Cov-2 Infection

نویسندگان [English]

  • Elham Karimi 1
  • Darya Salkhorde 2
  • Mahdis Hakkaki 3
  • Iman Shamohammadi 4
  • Negin Jahangiri 5
  • Fatemeh Baygan 3
  • Bahia Namavar Jahromi 6
  • Pegah Mousavi 7
  • Seyed Mehdi Kalantar 8
  • Soudabeh Sabetian 9
1 MSc, Department of Medical Genetics, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran
2 BSc, Student Research Committee, Kermanshah University of Medical Sciences, Kermanshah, Iran
3 MSc, Department of Medical Genetics, School of Medical Sciences, Hormozgan University of Medical Sciences, Bandar Abbas, Iran
4 MSc, Department of Medical Genetics, School of Medical Sciences, Hormozgan University of Medical Sciences, Bandar Abbas, Iran
5 Professor of Infertility & IVF, Department of Obstetrics and Gynecology, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran
6 Professor of Infertility & IVF, Department of Obstetrics and Gynecology, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran
7 Assistant Professor of Medical biotechnology, Molecular Medicine Research Center, Hormozgan Health Institute, Hormozgan University of Medical Sciences, Bandar Abbas, Iran
8 Professor of Molecular Cytogenetic, Research and Clinical Center for Infertility, Shahid Sadoughi University of Medical Sciences, Yazd, Iran
9 Assistant Professor of Cellular & Molecular Biology, Infertility Research Center, Shiraz University of Medical Sciences, Shiraz, Iran
چکیده [English]

Background: COVID-19, caused by the SARS-CoV-2 virus, has been associated with damage to multiple organ systems. One of the noteworthy aspects of the virus is its effect on male fertility and the reproductive system. We aimed to overview the involved molecular pathways to prospect the virus's effects on male reproductive tissue, spermatogenesis, and semen parameters.
Methods: PubMed and Scopus databases (papers published from 2020 to 2023) were searched for studies reporting the impact of COVID-19 on the related pathways associated with the male reproductive system at the level of cells, and 98 articles were reviewed.
Findings: The effects of COVID-19 may arise directly due to the virus's attacks on the male reproductive system or may be due to an undesirable overreaction of the immune response, such as cytokines storm or fewer. Renin-Angiotensin System and PI3K/AKT signaling pathway are also involved; counts and sperm motility were decreased, although approximately recovery was observed in survivals within months. Contrasting the drugs used for treating COVID-19 that had contradictory effects regarding vaccines, it seems there is no tangible adverse effect on male fertility.
Conclusion: The impact of SARS-CoV-2 on male fertility and the reproductive system is notable due to the presence of two major host factors, ACE2 and TMPRSS2, and involving the related pathways. It is possible that these organs could be involved, leading to effects on future generations. Understanding the process may provide a clue for managing the efficacies.

کلیدواژه‌ها [English]

  • SARS-CoV-2
  • COVID-19
  • Male infertility
  • Spermatogenesis
  • Sperm parameters

مراجع

  1. Ni W, Yang X, Yang D, Bao J, Li R, Xiao Y, et al. Role of angiotensin-converting enzyme 2 (ACE2) in COVID-19. Crit Care 2020; 24(1): 422.
  2. Li G, He X, Zhang L, Ran Q, Wang J, Xiong A, et al. Assessing ACE2 expression patterns in lung tissues in the pathogenesis of COVID-19. J Autoimmun 2020; 112: 102463.
  3. Saberiyan M, Safi A, Kamel A, Movahhed-Abbasabad P, Miralimalek M, Afkhami H, et al. An overview on the common laboratory parameter alterations and their related molecular pathways in screening for COVID-19 patients. Clin Lab 2020; 66(10).
  4. Bourgonje AR, Abdulle AE, Timens W, Hillebrands JL, Navis GJ, Gordijn SJ, et al. Angiotensin-converting enzyme 2 (ACE2), SARS-CoV-2 and the pathophysiology of coronavirus disease 2019 (COVID-19). J Pathol 2020; 251(3): 228-48.
  5. Hamming I, Timens W, Bulthuis ML, Lely AT, Navis G, van Goor H. Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis. J Pathol 2004; 203(2): 631-7.
  6. 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(2): 185-92.
  7. Zhang H, Li HB, Lyu JR, Lei XM, Li W, Wu G, et al. Specific ACE2 expression in small intestinal enterocytes may cause gastrointestinal symptoms and injury after 2019-nCoV infection. Int J Infect Dis 2020;96:19-24.
  8. Chan JF-W, Kok K-H, Zhu Z, Chu H, To KK-W, Yuan S, et al. Genomic characterization of the 2019 novel human-pathogenic coronavirus isolated from a patient with atypical pneumonia after visiting Wuhan. Emerg Microbes Infect 2020; 9(1): 221-36.
  9. Gonzalez-Villalobos RA, Shen XZ, Bernstein EA, Janjulia T, Taylor B, Giani JF, et al. Rediscovering ACE: novel insights into the many roles of the angiotensin-converting enzyme. J Mol Med (Berl) 2013; 91(10): 1143-54.
  10. ACE2 Cell Biology, Regulation, and Physiological Functions. Turner AJ. The Protective Arm of the Renin Angiotensin System (RAS) 2015:185-9.
  11. Li C, He Q, Qian H, Liu J. Overview of the pathogenesis of COVID‑19 (Review). Exp Ther Med 2021; 22(3): 1011.
  12. Evenson DP, Jost LK, Corzett M, Balhorn R. Characteristics of human sperm chromatin structure following an episode of influenza and high fever: a case study. J Androl 2000; 21(5): 739-46.
  13. Lugar DW, Ragland D, Stewart KRJJoSH, Production. Influenza outbreak causes reduction in semen quality of boars. J Swine Health Prod 2017; 25(6): 303-7.
  14. Akhigbe RE, Dutta S, Hamed MA, Ajayi AF, Sengupta P, Ahmad G. Viral infections and male infertility: a comprehensive review of the role of oxidative stress. Front Reprod Health 2022; 4: 782915.
  15. Xiong YQ, Chen YX, Cheng MJ, He WQ, Chen Q. The risk of human papillomavirus infection for male fertility abnormality: a meta-analysis. Asian J Androl 2018; 20(5): 493-7.
  16. 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.
  17. Seymen CM. The other side of COVID-19 pandemic: Effects on male fertility. J Med Virol 2021; 93(3): 1396-402.
  18. Omolaoye TS, Jalaleddine N, Cardona Maya WD, du Plessis SS. Mechanisms of SARS-CoV-2 and male infertility: could connexin and pannexin Play a Role? Front Physiol 2022; 13: 866675.
  19. Mir Mosavi SH, Esmaeili HJJoNEH. Zoning of Flood-prone Areas Using Geographic Information System (GIS) and Remote Sensing (RS),(Case Study: Darab City) [in Persian]. Journal of Natural Environmental Hazards 2021; 10(27): 21-46.
  20. Yang M, Chen S, Huang B, Zhong J-M, Su H, Chen Y-J, et al. Pathological findings in the testes of COVID-19 patients: clinical implications. Eur Urol Focus 2020; 6(5): 1124-9.
  21. Bendayan M, Boitrelle F. COVID-19 and impairment of spermatogenesis: What if fever was the only cause? 2020; 29: 100670.
  22. Yao XH, Luo T, Shi Y, He ZC, Tang R, Zhang PP, et al. A cohort autopsy study defines COVID-19 systemic pathogenesis. Cell Res 2021; 31(8): 836-46.
  23. Peirouvi T, Aliaghaei A, Eslami Farsani B, Ziaeipour S, Ebrahimi V, Forozesh M, et al. COVID-19 disrupts the blood–testis barrier through the induction of inflammatory cytokines and disruption of junctional proteins. Inflamm Res 2021; 70(10-12): 1165-75.
  24. Patel DP, Punjani N, Guo J, Alukal JP, Li PS, Hotaling JMJF, et al. The impact of SARS-CoV-2 and COVID-19 on male reproduction and men’s health. Fertil Steril 2021; 115(4): 813-23.
  25. Shamohammadi I, Kazemeyni S, Sadighi M, Hasanzadeh T, Dizavi AR. Efficacy of tadalafil on improvement of men with erectile dysfunction caused by COVID-19: A randomized placebo-controlled trial. Asian J Urol 2022; 11(1): 128-33.
  26. Li X, Geng M, Peng Y, Meng L, Lu SJJopa. Molecular immune pathogenesis and diagnosis of COVID-19. J Pharm Anal 2020; 10(2): 102-8.
  27. Azkur AK, Akdis M, Azkur D, Sokolowska M, van de Veen W, Brüggen MC, et al. Immune response to SARS‐CoV‐2 and mechanisms of immunopathological changes in COVID‐19. Allergy 2020; 75(7): 1564-81.
  28. Dai P, Qiao F, Chen Y, Chan DYL, Yim HCH, Fok KL, et al. SARS-CoV-2 and male infertility: from short- to long-term impacts. J Endocrinol Invest 2023; 1-17.
  29. 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. Cold Spring Harbor Laboratory
  30. Salonia A, Pontillo M, Capogrosso P, Gregori S, Carenzi C, Ferrara AM, et al. Testosterone in males with COVID‐19: A 7‐month cohort study. Andrology 2022; 10(1): 34-41.
  31. Barbagallo F, Calogero AE, Cannarella R, Condorelli RA, Mongioì LM, Aversa A, et al. The testis in patients with COVID-19: virus reservoir or immunization resource? Transl Androl Urol 2020; 9(5): 1897-900.
  32. Shen Q, Xiao X, Aierken A, Yue W, Wu X, Liao M, et al. The ACE2 expression in Sertoli cells and germ cells may cause male reproductive disorder after SARS‐CoV‐2 infection. J Cell Mol Med 2020; 24(16): 9472-7.
  33. Sabetian S, Castiglioni I, Jahromi BN, Mousavi P, Cava CJC. In silico identification of miRNA–lncRNA interactions in male reproductive disorder associated with COVID-19 infection. Cells 2021; 10(6): 1480.
  34. Li H, Xiao X, Zhang J, Zafar MI, Wu C, Long Y, et al. Impaired spermatogenesis in COVID-19 patients. EClinicalMedicine 2020; 28: 100604.
  35. Best JC, Kuchakulla M, Khodamoradi K, Lima TFN, Frech FS, Achua J, et al. Evaluation of SARS-CoV-2 in human semen and effect on total sperm number: a prospective observational study. World J Mens Health 2021; 39(3): 489-95.
  36. Wu F, Zhao S, Yu B, Chen Y-M, Wang W, Song Z-G, et al. A new coronavirus associated with human respiratory disease in China. Nature 2020; 579(7798): 265-9.
  37. Mruk DD, Cheng CYJEr. The mammalian blood-testis barrier: its biology and regulation. Endocr Rev 2015; 36(5): 564-91.
  38. Wang X, Li X, Wei X, Jiang H, Lan C, Yang S, et al. PD-L1 is a direct target of cancer-FOXP3 in pancreatic ductal adenocarcinoma (PDAC), and combined immunotherapy with antibodies against PD-L1 and CCL5 is effective in the treatment of PDAC. Sig Transduct Target Ther 2020; 5(1): 38.
  39. Chen Y-W, Lee M-S, Lucht A, Chou F-P, Huang W, Havighurst TC, et al. TMPRSS2, a serine protease expressed in the prostate on the apical surface of luminal epithelial cells and released into semen in prostasomes, is misregulated in prostate cancer cells. Am J Pathol 2010; 176(6): 2986-96.
  40. Sengupta P, Leisegang K, Agarwal A. The impact of COVID-19 on the male reproductive tract and fertility: A systematic review. Arab J Urol 2021; 19(3): 423-36.
  41. 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(2): 233-8.
  42. Costela-Ruiz VJ, Illescas-Montes R, Puerta-Puerta JM, Ruiz C, Melguizo-Rodríguez L. SARS-CoV-2 infection: The role of cytokines in COVID-19 disease. Cytokine Growth Factor Rev 2020; 54: 62-75.
  43. Dutta S, Sengupta P, Slama P, Rochoudhury S. Oxidative stress, testicular inflammatory pathways, and male reproduction. Int J Mol Sci 2021; 22(18): 10043.
  44. Aksak T, Satar DA, Bağci R, Gülteki̇n EO, Coşkun A, Demi̇rdelen U. Investigation of the effect of COVID‐19 on sperm count, motility, and morphology. J Med Virol 2022; 94(11): 5201-5.
  45. Masterson JM, Bui C, Hasan W, Zhang Y, Hyunh C, Jawanda H, et al. Case series–COVID-19 is unlikely to affect male fertility: Results of histopathological and reverse transcriptase polymerase chain reaction analysis. Can Urol Assoc J 2022; 16(11): E558-E562.
  46. Sabetian S, Namavar Jahromi B, Feiz F, Castiglioni I, Cava C, Vakili SJJoHS, et al. Clinical guidelines on the use of assisted reproductive technology during COVID-19 pandemic: A minireview of the current literature. 13 Assisted reproductive technology during COVID-19. J Health Sci Surveillance Sys 2022; 10(1): 13-8.
  47. Goebel H, Koeditz B, Huerta M, Kameri E, Nestler T, Kamphausen T, et al. COVID-19 infection induce mir-371a-3p upregulation resulting in influence on male fertility. Biomedicines 2022; 10(4): 858.
  48. Gharagozloo P, Cartagena S, Moazamian A, Drevet JR, Somkuti S, Aitken RJ. Rapid impact of COVID-19 infection on semen quality: a case report. Transl Androl Urol 2022; 11(1): 110-15.
  49. He Y, Wang J, Ren J, Zhao Y, Chen J, Chen X. Effect of COVID-19 on male reproductive system–a systematic review. Front Endocrinol (Lausanne). 2021; 12: 677701.
  50. Scroppo FI, Costantini E, Zucchi A, Illiano E, Trama F, Brancorsini S, et al. COVID-19 disease in clinical setting: impact on gonadal function, transmission risk, and sperm quality in young males. J Basic Clin Physiol Pharmacol 2021; 33(1): 97-102.
  51. Peirouvi T, Aliaghaei A, Eslami Farsani B, Ziaeipour S, Ebrahimi V, Forozesh M, et al. COVID-19 disrupts the blood–testis barrier through the induction of inflammatory cytokines and disruption of junctional proteins. Inflamm Res 2021; 70(10-12): 1165-75.
  52. Leanza C, Mongioì LM, Cannarella R, La Vignera S, Condorelli RA, Calogero AE. The possible role of SARS-CoV-2 in male fertility: a narrative review. Endocrines 2022; 3(3): 552-9.
  53. Edenfield RC, Easley IV CA. Implications of testicular ACE2 and the renin–angiotensin system for SARS-CoV-2 on testis function. Nat Rev Urol 2022; 19(2): 116-27.
  54. Ma X, Guan C, Chen R, Wang Y, Feng S, Wang R, et al. Pathological and molecular examinations of postmortem testis biopsies reveal SARS-CoV-2 infection in the testis and spermatogenesis damage in COVID-19 patients. Cell Mol Immunol 2021; 18(2): 487-9.
  55. 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(1): 456-62.
  56. Ruan Y, Hu B, Liu Z, Liu K, Jiang H, Li H, et al. 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 2021; 9(1): 99-106.
  57. Hajizadeh Maleki B, Tartibian B. COVID-19 and male reproductive function: a prospective, longitudinal cohort study. Reproduction 2021; 161(3): 319-31.
  58. Lifshitz D, Haas J, Lebovitz O, Raviv G, Orvieto R, Aizer A. Does mRNA SARS-CoV-2 vaccine detrimentally affect male fertility, as reflected by semen analysis? Reprod Biomed Online 2022; 44(1): 145-9.
  59. 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(1): 42-7.
  60. Rao M, Zhao X-L, Yang J, Hu S-F, Lei H, Xia W, et al. Effect of transient scrotal hyperthermia on sperm parameters, seminal plasma biochemical markers, and oxidative stress in men. Asian J Androl 2015; 17(4): 668-75.
  61. 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(2): e13912.
  62. Mokhtari T, Hassani F, Ghaffari N, Ebrahimi B, Yarahmadi A, Hassanzadeh G. COVID-19 and multiorgan failure: A narrative review on potential mechanisms. J Mol Histol 2020; 51(6): 613-28.
  63. Larasati T, Noda T, Fujihara Y, Shimada K, Tobita T, Yu Z, et al. Tmprss12 is required for sperm motility and uterotubal junction migration in mice†. Biol Reprod 2020; 103(2): 254-63.
  64. Karkin K, Gürlen G. Does COVID-19 cause testicular damage? A cross-sectional study comparing hormonal parameters. Eur Rev Med Pharmacol Sci 2022; 26(10): 3745-50.
  65. Unger T, Li J. The role of the renin-angiotensin-aldosterone system in heart failure. J Renin Angiotensin Aldosterone Syst 2004; 5(Suppl 1): S7-10.
  66. Bader M, Ganten D. Update on tissue renin-angiotensin systems. Journal of molecular medicine (Berlin, Germany) 2008; 86(6): 615-21.
  67. Colli LG, Belardin LB, Echem C, Akamine EH, Antoniassi MP, Andretta RR, et al. Systemic arterial hypertension leads to decreased semen quality and alterations in the testicular microcirculation in rats. Sci Rep 2019; 9(1): 11047.
  68. Khanum A, Dufau ML. Angiotensin II receptors and inhibitory actions in Leydig cells. J Biol Chem 1988; 263(11): 5070-4.
  69. Alenina N, Xu P, Rentzsch B, Patkin EL, Bader M. Genetically altered animal models for Mas and angiotensin-(1-7). Exp Physiol 2008; 93(5): 528-37.
  70. Costa APR, Fagundes-Moura CR, Pereira VM, Silva LF, Vieira MA, Santos RA, et al. Angiotensin-(1-7): a novel peptide in the ovary. Endocrinology 2003; 144(5): 1942-8.
  71. Jia HP, Look DC, Tan P, Shi L, Hickey M, Gakhar L, et al. Ectodomain shedding of angiotensin converting enzyme 2 in human airway epithelia. Am J Physiol Lung Cell Mol Physiol 2009; 297(1): L84-96.
  72. Stoddart CA, Geleziunas R, Ferrell S, Linquist-Stepps V, Moreno ME, Bare C, et al. Human immunodeficiency virus type 1 Nef-mediated downregulation of CD4 correlates with Nef enhancement of viral pathogenesis. J Virol 2003; 77(3): 2124-33.
  73. Nishimura H, L’Hernault SW. Spermatogenesis. Curr Biol 2017; 27(18): R988-R994.
  74. Wang Z, Ma Y, Chen Z, Yang R, Liu Q, Pan J, et al. COVID-19 inhibits spermatogenesis in the testes by inducing cellular senescence. Frontiers in Genetics 2022; 13: 981471.
  75. Haghpanah A, Masjedi F, Alborzi S, Hosseinpour A, Dehghani A, Malekmakan L, et al. Potential mechanisms of SARS‐CoV‐2 action on male gonadal function and fertility: Current status and future prospects. Andrologia 2021; 53(1): e13883.
  76. Nguyen T, Hulme J, Tran H, Vo T, Vo G. The potential impact of COVID-19 on male reproductive health. J Endocrinol Invest 2022; 45(8): 1483-95.
  77. Hu B, Liu K, Ruan Y, Wei X, Wu Y, Feng H, et al. Evaluation of mid-and long-term impact of COVID-19 on male fertility through evaluating semen parameters. Transl Androl Urol 2022; 11(2): 15967.
  78. Xu Y, Chen Y, Tang X. Guidelines for the diagnosis and treatment of coronavirus disease 2019 (COVID-19) in China. Glob Health Med 2020; 2(2): 66-72.
  79. Bermas BL. Paternal safety of anti-rheumatic medications. Best Pract Res Clin Obstet Gynaecol 2020; 64: 77-84.
  80. Pilkington V, Pepperrell T, Hill A. A review of the safety of favipiravir - a potential treatment in the COVID-19 pandemic? J Virus Erad 2020; 6(2): 45-51.
  81. Gul A, Zengin S, Dundar G, Ozturk M. Do SARS-CoV-2 infection (COVID-19) and the medications administered for its treatment impair testicular functions? Urol Int 2021; 105(11-12): 944-8.
  82. Lorusso F, Palmisano M, Chironna M, Vacca M, Masciandaro P, Bassi E, et al. Impact of chronic viral diseases on semen parameters. Andrologia 2010; 42(2): 121-6.
  83. Pazir Y, Eroglu T, Kose A, Bulut TB, Genc C, Kadihasanoglu M. Impaired semen parameters in patients with confirmed SARS-CoV-2 infection: A prospective cohort study. Andrologia 2021; 53(9): e14157.
  84. Drobnis EZ, Nangia AK. Antivirals and male reproduction. Adv Exp Med Biol 2017; 1034: 163-78.
  85. Rafiee B, Bagher Tabei SM. The effect of N-acetyl cysteine consumption on men with abnormal sperm parameters due to positive history of COVID-19 in the last three months. Arch Ital Urol Androl 2021; 93(4): 465-7.
  86. Ciftci H, Verit A, Savas M, Yeni E, Erel O. Effects of N-acetylcysteine on semen parameters and oxidative/antioxidant status. Urology 2009; 74(1): 73-6.
  87. Safarinejad MR, Safarinejad S. Efficacy of selenium and/or N-acetyl-cysteine for improving semen parameters in infertile men: a double-blind, placebo controlled, randomized study. J Urol 2009; 181(2): 741-51.
  88. Liu K, Tao W. Effects of coronavirus disease 2019 (COVID-19), including its prevention and treatment, on the male reproductive system. Chin Med J (Engl) 2021; 134(20): 2509-11.
  89. Malki MI. COVID-19 and male infertility: An overview of the disease. Medicine 2022; 101(27): e29401.
  90. Drobnis EZ, Nangia AK, Drobnis EZ, Nangia AK. Antivirals and male reproduction. Adv Exp Med Biol 2017: 163-78.
  91. Chi W-Y, Li Y-D, Huang H-C, Chan TEH, Chow S-Y, Su J-H, et al. COVID-19 vaccine update: vaccine effectiveness, SARS-CoV-2 variants, boosters, adverse effects, and immune correlates of protection. J Biomed Sci 2022; 29(1): 82.
  92. Navarra A, Albani E, Castellano S, Arruzzolo L, Levi-Setti PE. Coronavirus Disease-19 Infection: Implications on Male Fertility and Reproduction. Front Physiol 2020; 11: 574761.
  93. Barda S, Laskov I, Grisaru D, Lehavi O, Kleiman S, Wenkert A, et al. The impact of COVID-19 vaccine on sperm quality. Int J Gynaecol Obstet 2022; 158(1): 116-20.
  94. Mulligan MJ, Lyke KE, Kitchin N, Absalon J, Gurtman A, Lockhart S, et al. Phase I/II study of COVID-19 RNA vaccine BNT162b1 in adults. Nature 2020; 586(7830): 589-93.
  95. Polack FP, Thomas SJ, Kitchin N, Absalon J, Gurtman A, Lockhart S, et al. Safety and efficacy of the BNT162b2 mRNA COVID-19 vaccine. N Engl J Med 2020; 383(27): 2603-15.
  96. Gat I, Kedem A, Dviri M, Umanski A, Levi M, Hourvitz A, et al. COVID-19 vaccination BNT162b2 temporarily impairs semen concentration and total motile count among semen donors. Andrology 2022; 10(6): 1016-22.
  97. Abd ZH, Muter SA, Saeed RAM, Ammar O. Effects of COVID-19 vaccination on different semen parameters. Basic Clin Androl 2022; 32(1): 13.
  98. Safrai M, Herzberg S, Imbar T, Reubinoff B, Dior U, Ben-Meir A. The BNT162b2 mRNA COVID-19 vaccine does not impair sperm parameters. Reprod Biomed Online 2022; 44(4): 685-8.
  99. Gonzalez DC, Nassau DE, Khodamoradi K, Ibrahim E, Blachman-Braun R, Ory J, et al. Sperm parameters before and after COVID-19 mRNA vaccination. JAMA 2021; 326(3): 273-4.
  100. Dong Y, Li X, Li Z, Zhu Y, Wei Z, He J, et al. Effects of inactivated SARS-CoV-2 vaccination on male fertility: A retrospective cohort study. J Med Virol 2023; 95(1): e28329.
  101. Meitei H, Uppangala S, Lakshmi V, Kalthur G, Adiga S. Semen characteristics of individuals before and after CovishieldTM vaccination. Reprod Fertil 2022; RAF-22-0046.
مجله دانشکده پزشکی اصفهان
دوره 42، شماره 768
هفته 4، تیر
خرداد و تیر 1403
صفحه 418-430

فایل ها

سابقه مقاله

  • تاریخ دریافت: 18 فروردین 1403
  • تاریخ پذیرش: 01 مرداد 1403

هم رسانی

ارجاع به این مقاله

آمار