{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,9]],"date-time":"2026-07-09T22:19:16Z","timestamp":1783635556059,"version":"3.55.0"},"reference-count":42,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,10,6]],"date-time":"2023-10-06T00:00:00Z","timestamp":1696550400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004731","name":"Natural Science Foundation of Zhejiang Province","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100004731","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100013115","name":"Zhejiang Provincial Program for the Cultivation of High-Level Innovative Health Talents","doi-asserted-by":"publisher","award":["Year 2018"],"award-info":[{"award-number":["Year 2018"]}],"id":[{"id":"10.13039\/501100013115","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Endocrinol."],"abstract":"<jats:p>The influence of SARS-CoV-2 infection on clinical outcomes in patients undergoing <jats:italic>in vitro<\/jats:italic> fertilization has been uncertain. Therefore, this systematic review and meta-analysis aimed to evaluate the impact of past SARS-CoV-2 infection on IVF outcomes. A comprehensive search of PubMed, EMBASE, and Cochrane Library databases was conducted from December 2019 to January 2023. Included studies comparing IVF outcomes between patients with prior SARS-CoV-2 infection and controls without previous infection were analyzed. Study quality was assessed using the Newcastle-Ottawa Quality Assessment Scale. Sensitivity analysis, publication bias, and heterogeneity were also examined. The review protocol was registered with PROSPERO (CRD42023392007). A total of eight studies, involving 317 patients with past SARS-CoV-2 infection and 904 controls, met the inclusion criteria. The meta-analysis revealed no significant differences between the infection group and controls in terms of clinical pregnancy rate (OR 0.97, 95% CI 0.73-1.29; <jats:italic>P<\/jats:italic> = 0.82), implantation rate (OR 0.99, 95% CI 0.67-1.46; <jats:italic>P<\/jats:italic> = 0.96), or miscarriage rate (OR 0.64, 95% CI 0.15-2.65; <jats:italic>P<\/jats:italic> = 0.53). Subgroup analyses based on transfer type demonstrated comparable clinical pregnancy rates between the two groups in both fresh embryo transfer (OR 0.97, 95% CI 0.69-1.36; <jats:italic>P<\/jats:italic> = 0.86) and frozen embryo transfer (OR 0.96, 95% CI 0.38-2.44; <jats:italic>P<\/jats:italic> = 0.94). In conclusion, this meta-analysis suggests that previous SARS-CoV-2 infection does not have a detrimental impact on clinical outcomes in IVF patients. These findings provide valuable insights into assessing the influence of prior SARS-CoV-2 infection on successful pregnancy outcomes in IVF treatment. The systematic review was performed based on the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement. This review was prospectively registered with the International Prospective Register of Systematic Reviews (ID CRD42023392007) on January 16, 2023.<\/jats:p>","DOI":"10.3389\/fendo.2023.1233986","type":"journal-article","created":{"date-parts":[[2023,10,6]],"date-time":"2023-10-06T10:01:45Z","timestamp":1696586505000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":9,"title":["Impact of SARS-CoV-2 infection on clinical outcomes of in vitro fertilization treatments: a systematic review and meta-analysis"],"prefix":"10.3389","volume":"14","author":[{"given":"Yamei","family":"Xue","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuping","family":"Xiong","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaohong","family":"Cheng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kun","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2023,10,6]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","DOI":"10.1002\/path.5471","article-title":"Angiotensin-converting enzyme 2 (ACE2), SARS-CoV-2 and the pathophysiology of coronavirus disease 2019 (COVID-19)","volume":"251","author":"Bourgonje","year":"2020","journal-title":"J Pathol"},{"key":"B2","doi-asserted-by":"publisher","first-page":"271","DOI":"10.1016\/j.cell.2020.02.052","article-title":"SARS-coV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor","volume":"181","author":"Hoffmann","year":"2020","journal-title":"Cell"},{"key":"B3","doi-asserted-by":"publisher","first-page":"e105114","DOI":"10.15252\/embj.20105114","article-title":"SARS-CoV-2 receptor ACE2 and TMPRSS2 are primarily expressed in bronchial transient secretory cells","volume":"39","author":"Lukassen","year":"2020","journal-title":"EMBO J"},{"key":"B4","doi-asserted-by":"publisher","DOI":"10.1016\/j.celrep.2020.108175","article-title":"A single-cell RNA expression map of human coronavirus entry factors","volume":"32","author":"Singh","year":"2020","journal-title":"Cell Rep"},{"key":"B5","doi-asserted-by":"publisher","first-page":"920","DOI":"10.3390\/cells9040920","article-title":"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","volume":"9","author":"Wang","year":"2020","journal-title":"Cells"},{"key":"B6","doi-asserted-by":"publisher","first-page":"9","DOI":"10.5653\/cerm.2021.04511","article-title":"The impact of COVID-19 on the male genital tract: a qualitative literature review of sexual transmission and fertility implications","volume":"49","author":"Verrienti","year":"2022","journal-title":"Clin Exp Reprod Med"},{"key":"B7","doi-asserted-by":"publisher","first-page":"284","DOI":"10.3390\/ijerph18010284","article-title":"The scRNA-seq expression profiling of the receptor ACE2 and the cellular protease TMPRSS2 reveals human organs susceptible to SARS-coV-2 infection","volume":"18","author":"Qi","year":"2021","journal-title":"Int J Environ Res Public Health"},{"key":"B8","doi-asserted-by":"publisher","DOI":"10.1111\/andr.13019","article-title":"Short-term effects of COVID-19 on semen parameters: a multicenter study of 69 cases","volume":"9","author":"Erbay","year":"2021","journal-title":"Andrology"},{"key":"B9","doi-asserted-by":"publisher","DOI":"10.5489\/cuaj.7292","article-title":"Effect of SARS-CoV-2 infection on semen parameters","volume":"16","author":"Hamarat","year":"2022","journal-title":"Can Urol Assoc J"},{"key":"B10","doi-asserted-by":"publisher","DOI":"10.1016\/j.ygeno.2021.08.012","article-title":"Co-expression of the SARS-CoV-2 entry molecules ACE2 and TMPRSS2 in human ovaries: identification of cell types and trends with age","volume":"113","author":"Wu","year":"2021","journal-title":"Genomics"},{"key":"B11","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1016\/j.xfss.2020.12.005","article-title":"Human eggs, zygotes, and embryos express the receptor angiotensin 1-converting enzyme 2 and transmembrane serine protease 2 protein necessary for severe acute respiratory syndrome coronavirus 2 infection","volume":"2","author":"Rajput","year":"2021","journal-title":"F S Sci"},{"key":"B12","doi-asserted-by":"publisher","DOI":"10.1016\/j.fertnstert.2020.06.026","article-title":"SARS-CoV-2 infection risk assessment in the endometrium: viral infection-related gene expression across the menstrual cycle","volume":"114","author":"Henarejos-Castillo","year":"2020","journal-title":"Fertil Steril"},{"key":"B13","doi-asserted-by":"publisher","DOI":"10.1093\/humrep\/deab183","article-title":"Single-cell RNA sequencing of SARS-CoV-2 cell entry factors in the preconceptional human endometrium","volume":"36","author":"Vilella","year":"2021","journal-title":"Hum Reprod"},{"key":"B14","doi-asserted-by":"publisher","DOI":"10.1007\/s10815-020-01952-x","article-title":"SARS-CoV-2 host receptors ACE2 and CD147 (BSG) are present on human oocytes and blastocysts","volume":"37","author":"Essahib","year":"2020","journal-title":"J Assist Reprod Genet"},{"key":"B15","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1016\/j.fertnstert.2020.05.001","article-title":"Coronavirus disease-19 and fertility: viral host entry protein expression in male and female reproductive tissues","volume":"114","author":"Stanley","year":"2020","journal-title":"Fertil Steril"},{"key":"B16","doi-asserted-by":"publisher","DOI":"10.1016\/j.fertnstert.2010.06.060","article-title":"Angiotensin-(1-7), its receptor Mas, and the angiotensin-converting enzyme type 2 are expressed in the human ovary","volume":"95","author":"Reis","year":"2011","journal-title":"Fertil Steril"},{"key":"B17","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbadis.2021.166295","article-title":"SARS-CoV-2 infection negatively affects ovarian function in ART patients","volume":"1868","author":"Herrero","year":"2022","journal-title":"Biochim Biophys Acta Mol Basis Dis"},{"key":"B18","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2288-14-45","article-title":"Newcastle-Ottawa Scale: comparing reviewers' to authors' assessments","volume":"14","author":"Lo","year":"2014","journal-title":"BMC Med Res Methodol"},{"key":"B19","unstructured":"WellsGA\n            SheaB\n            O\u2019ConnellD\n            PetersonJ\n            WelchV\n            LososM\n          The newcastle-ottawa scale (NOS) for assessing the quality of nonrandomized studies in meta-analyses"},{"key":"B20","doi-asserted-by":"publisher","DOI":"10.1002\/9781119536604.ch10","article-title":"Analysing data and undertaking meta-analyses","author":"Deeks","year":"2019","journal-title":"Cochrane Handb Systematic Rev Interventions"},{"key":"B21","doi-asserted-by":"publisher","DOI":"10.1136\/bmj.327.7414.557","article-title":"Measuring inconsistency in meta-analyses","volume":"327","author":"Higgins","year":"2003","journal-title":"BMJ"},{"key":"B22","doi-asserted-by":"publisher","DOI":"10.1136\/bmj.315.7109.629","article-title":"Bias in meta-analysis detected by a simple, graphical test","volume":"315","author":"Egger","year":"1997","journal-title":"BMJ"},{"key":"B23","doi-asserted-by":"publisher","DOI":"10.1016\/j.eclinm.2021.101013","article-title":"Investigating the impact of asymptomatic or mild SARS-CoV-2 infection on female fertility and in vitro fertilization outcomes: a retrospective cohort study","volume":"38","author":"Wang","year":"2021","journal-title":"EClinicalMedicine"},{"key":"B24","doi-asserted-by":"publisher","first-page":"21702","DOI":"10.1038\/s41598-022-25757-3","article-title":"COVID-19 infection and vaccine have no impact on in-vitro fertilization (IVF) outcome","volume":"12","author":"Albeitawi","year":"2022","journal-title":"Sci Rep"},{"key":"B25","doi-asserted-by":"publisher","DOI":"10.1093\/humrep\/deac043","article-title":"IVF under COVID-19: treatment outcomes of fresh ART cycles","volume":"37","author":"Youngster","year":"2022","journal-title":"Hum Reprod"},{"key":"B26","doi-asserted-by":"publisher","first-page":"46","DOI":"10.1186\/s12958-022-00918-1","article-title":"Investigating the impact of SARS-CoV-2 infection on basic semen parameters and in vitro fertilization\/intracytoplasmic sperm injection outcomes: a retrospective cohort study","volume":"20","author":"Wang","year":"2022","journal-title":"Reprod Biol Endocrinol"},{"key":"B27","doi-asserted-by":"publisher","DOI":"10.1007\/s10815-022-02517-w","article-title":"The impact of past COVID-19 infection on pregnancy rates in frozen embryo transfer cycles","volume":"39","author":"Youngster","year":"2022","journal-title":"J Assist Reprod Genet"},{"key":"B28","doi-asserted-by":"publisher","DOI":"10.1016\/j.fertnstert.2022.01.009","article-title":"The effect of coronavirus disease 2019 immunity on frozen-thawed embryo transfer cycles outcome","volume":"117","author":"Aizer","year":"2022","journal-title":"Fertil Steril"},{"key":"B29","doi-asserted-by":"publisher","DOI":"10.1002\/mrd.23658","article-title":"Previous infection with SARS-CoV-2 impacts embryo morphokinetics but not clinical outcomes in a time-lapse imaging system","volume":"90","author":"Braga","year":"2023","journal-title":"Mol Reprod Dev"},{"key":"B30","doi-asserted-by":"publisher","DOI":"10.1089\/jwh.2022.0163","article-title":"Boosting dose of pfizer-bioNtech mRNA vaccine against SARS-coV-2 does not affect reproductive outcomes in in-vitro fertilization patients: A cohort study","volume":"32","author":"Adler Lazarovits","year":"2023","journal-title":"J Womens Health (Larchmt)"},{"key":"B31","doi-asserted-by":"publisher","first-page":"e40","DOI":"10.1097\/GRH.0000000000000040","article-title":"Assisted reproduction and COVID-19: a joint statement of ASRM, ESHRE, and IFFS","volume":"5","author":"Veiga","year":"2020","journal-title":"Glob Reprod Health"},{"key":"B32","doi-asserted-by":"publisher","DOI":"10.1093\/humrep\/deaa285","article-title":"The calm after the storm: re-starting ART treatments safely in the wake of the COVID-19 pandemic","volume":"36","author":"Group","year":"2021","journal-title":"Hum Reprod"},{"key":"B33","doi-asserted-by":"publisher","DOI":"10.1093\/humupd\/dmac037","article-title":"SARS-CoV-2, fertility and assisted reproduction","volume":"29","author":"Ata","year":"2023","journal-title":"Hum Reprod Update"},{"key":"B34","doi-asserted-by":"publisher","DOI":"10.1098\/rsob.200162","article-title":"Expression of SARS-CoV-2 receptor ACE2 and the protease TMPRSS2 suggests susceptibility of the human embryo in the first trimester","volume":"10","author":"Weatherbee","year":"2020","journal-title":"Open Biol"},{"key":"B35","doi-asserted-by":"publisher","first-page":"15451","DOI":"10.1038\/s41598-022-18906-1","article-title":"SARS-CoV-2 can infect human embryos","volume":"12","author":"Montano","year":"2022","journal-title":"Sci Rep"},{"key":"B36","doi-asserted-by":"publisher","DOI":"10.1093\/humrep\/deab182","article-title":"Ovarian follicular function is not altered by SARS-CoV-2 infection or BNT162b2 mRNA COVID-19 vaccination","volume":"36","author":"Bentov","year":"2021","journal-title":"Hum Reprod"},{"key":"B37","doi-asserted-by":"publisher","DOI":"10.1093\/humrep\/deaa284","article-title":"Undetectable viral RNA in oocytes from SARS-CoV-2 positive women","volume":"36","author":"Barragan","year":"2021","journal-title":"Hum Reprod"},{"key":"B38","doi-asserted-by":"publisher","DOI":"10.1007\/s43032-021-00502-9","article-title":"Failure to detect viral RNA in follicular fluid aspirates from a SARS-coV-2-positive woman","volume":"28","author":"Demirel","year":"2021","journal-title":"Reprod Sci"},{"key":"B39","doi-asserted-by":"publisher","DOI":"10.1016\/j.fertnstert.2021.12.032","article-title":"Undetectable viral RNA in follicular fluid, cumulus cells, and endometrial tissue samples in SARS-CoV-2-positive women","volume":"117","author":"Boudry","year":"2022","journal-title":"Fertil Steril"},{"key":"B40","doi-asserted-by":"publisher","DOI":"10.1093\/humrep\/deab255","article-title":"Risk of contamination of semen, vaginal secretions, follicular fluid and ovarian medulla with SARS-CoV-2 in patients undergoing ART","volume":"37","author":"Kteily","year":"2022","journal-title":"Hum Reprod"},{"key":"B41","doi-asserted-by":"publisher","DOI":"10.1016\/j.ajog.2020.04.038","article-title":"Severe acute respiratory syndrome coronavirus 2 detection in the female lower genital tract","volume":"223","author":"Cui","year":"2020","journal-title":"Am J Obstet Gynecol"},{"key":"B42","doi-asserted-by":"publisher","DOI":"10.1093\/cid\/ciaa375","article-title":"SARS-coV-2 is not detectable in the vaginal fluid of women with severe COVID-19 infection","volume":"71","author":"Qiu","year":"2020","journal-title":"Clin Infect Dis"}],"container-title":["Frontiers in Endocrinology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fendo.2023.1233986\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,10,6]],"date-time":"2023-10-06T10:01:48Z","timestamp":1696586508000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fendo.2023.1233986\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,10,6]]},"references-count":42,"alternative-id":["10.3389\/fendo.2023.1233986"],"URL":"https:\/\/doi.org\/10.3389\/fendo.2023.1233986","relation":{},"ISSN":["1664-2392"],"issn-type":[{"value":"1664-2392","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,10,6]]},"article-number":"1233986"}}