{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,29]],"date-time":"2026-07-29T04:39:59Z","timestamp":1785299999541,"version":"3.55.0"},"reference-count":52,"publisher":"Wiley","issue":"8","license":[{"start":{"date-parts":[[2024,3,12]],"date-time":"2024-03-12T00:00:00Z","timestamp":1710201600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Andrology"],"published-print":{"date-parts":[[2024,11]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:sec><jats:title>Background<\/jats:title><jats:p>Severe acute syndrome coronavirus 2 can invade a variety of tissues, including the testis. Even though this virus is scarcely found in human semen polymerase chain reaction tests, autopsy studies confirm the viral presence in all testicular cell types, including spermatozoa and spermatids.<\/jats:p><\/jats:sec><jats:sec><jats:title>Objective<\/jats:title><jats:p>To investigate whether the severe acute syndrome coronavirus 2 is present inside the spermatozoa of negative polymerase chain reaction\u2010infected men up to 3 months after hospital discharge.<\/jats:p><\/jats:sec><jats:sec><jats:title>Materials and methods<\/jats:title><jats:p>This cross\u2010sectional study included 13 confirmed moderate\u2010to\u2010severe COVID\u201019 patients enrolled 30\u201390 days after the diagnosis. Semen samples were obtained and examined with real\u2010time polymerase chain reaction for RNA detection and by transmission electron microscopy.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>In moderate\u2010to\u2010severe clinical scenarios, we identified the severe acute syndrome coronavirus 2 inside spermatozoa in nine of 13 patients up to 90 days after discharge from the hospital. Moreover, some DNA\u2010based extracellular traps were reported in all studied specimens.<\/jats:p><\/jats:sec><jats:sec><jats:title>Discussion and conclusion<\/jats:title><jats:p>Although severe acute syndrome coronavirus 2 was not present in the infected men's semen, it was intracellularly present in the spermatozoa till 3 months after hospital discharge. The Electron microscopy (EM) findings also suggest that spermatozoa produce nuclear DNA\u2010based extracellular traps, probably in a cell\u2010free DNA\u2010dependent manner, similar to those previously described in the systemic inflammatory response to COVID\u201019. In moderate\u2010to\u2010severe cases, the blood\u2013testes barrier grants little defence against different pathogenic viruses, including the severe acute syndrome coronavirus 2. The virus could also use the epididymis as a post\u2010testicular route to bind and fuse to the mature spermatozoon and possibly accomplish the reverse transcription of the single\u2010stranded viral RNA into proviral DNA. These mechanisms can elicit extracellular cell\u2010free DNA formation. The potential implications of our findings for assisted conception must be addressed, and the evolutionary history of DNA\u2010based extracellular traps as preserved ammunition in animals\u2019 innate defence might improve our understanding of the severe acute syndrome coronavirus 2 pathophysiology in the testis and spermatozoa.<\/jats:p><\/jats:sec>","DOI":"10.1111\/andr.13612","type":"journal-article","created":{"date-parts":[[2024,3,12]],"date-time":"2024-03-12T09:34:13Z","timestamp":1710236053000},"page":"1799-1807","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":18,"title":["Transmission electron microscopy reveals the presence of SARS\u2010CoV\u20102 in human spermatozoa associated with an ETosis\u2010like response"],"prefix":"10.1111","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6452-0502","authenticated-orcid":false,"given":"Jorge","family":"Hallak","sequence":"first","affiliation":[{"name":"Departamento de Cirurgia Disciplina de Urologia Faculdade de Medicina da Universidade de S\u00e3o Paulo  S\u00e3o Paulo Brazil"},{"name":"Androscience, Science &amp; Innovation Center in Andrology and High\u2010Complex Clinical and Research Andrology Laboratory. Androscience Institute  Sao Paulo Brasil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5322-3812","authenticated-orcid":false,"given":"Elia G.","family":"Caldini","sequence":"additional","affiliation":[{"name":"Departamento de Patologia Faculdade de Medicina da Universidade de S\u00e3o Paulo  S\u00e3o Paulo Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6598-2442","authenticated-orcid":false,"given":"Thiago A.","family":"Teixeira","sequence":"additional","affiliation":[{"name":"Androscience, Science &amp; Innovation Center in Andrology and High\u2010Complex Clinical and Research Andrology Laboratory. Androscience Institute  Sao Paulo Brasil"},{"name":"Departamento de Cirurgia Divis\u00e3o de Urologia Hospital Universit\u00e1rio da Universidade Federal do Amap\u00e1  Amap\u00e1 Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria Cassia Mendes","family":"Correa","sequence":"additional","affiliation":[{"name":"Instituto de Medicina Tropical Faculdade de Medicina da Universidade de S\u00e3o Paulo  S\u00e3o Paulo Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6659-7186","authenticated-orcid":false,"given":"Amaro N.","family":"Duarte\u2010Neto","sequence":"additional","affiliation":[{"name":"Departamento de Patologia Faculdade de Medicina da Universidade de S\u00e3o Paulo  S\u00e3o Paulo Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fabiola","family":"Zambrano","sequence":"additional","affiliation":[{"name":"Department of Preclinical Sciences Faculty of Medicine Universidad de La Frontera  Temuco Chile"},{"name":"Center of Translational Medicine\u2014Scientific and Technological Bioresource Nucleus (CEMT\u2014BIOREN) Faculty of Medicine Universidad de La Frontera  Temuco Chile"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anja","family":"Taubert","sequence":"additional","affiliation":[{"name":"Institute of Parasitology Justus Liebig University Giessen  Giessen Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4550-8492","authenticated-orcid":false,"given":"Carlos","family":"Hermosilla","sequence":"additional","affiliation":[{"name":"Institute of Parasitology Justus Liebig University Giessen  Giessen Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3077-6558","authenticated-orcid":false,"given":"Jo\u00ebl R.","family":"Drevet","sequence":"additional","affiliation":[{"name":"GReD Institute CNRS\u2010INSERM\u2010Universit\u00e9 Clermont Auvergne Faculty of Medicine  Clermont\u2010Ferrand France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9073-9989","authenticated-orcid":false,"given":"Marisa","family":"Dolhnikoff","sequence":"additional","affiliation":[{"name":"Departamento de Patologia Faculdade de Medicina da Universidade de S\u00e3o Paulo  S\u00e3o Paulo Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4853-4282","authenticated-orcid":false,"given":"Raul","family":"Sanchez","sequence":"additional","affiliation":[{"name":"Center of Translational Medicine\u2014Scientific and Technological Bioresource Nucleus (CEMT\u2014BIOREN) Faculty of Medicine Universidad de La Frontera  Temuco Chile"},{"name":"Institute of Parasitology Justus Liebig University Giessen  Giessen Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2005-8253","authenticated-orcid":false,"given":"Paulo H. N.","family":"Saldiva","sequence":"additional","affiliation":[{"name":"Departamento de Patologia Faculdade de Medicina da Universidade de S\u00e3o Paulo  S\u00e3o Paulo Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2024,3,12]]},"reference":[{"key":"e_1_2_9_2_1","doi-asserted-by":"publisher","DOI":"10.1177\/20503121221105583"},{"key":"e_1_2_9_3_1","doi-asserted-by":"publisher","DOI":"10.1002\/hsr2.745"},{"key":"e_1_2_9_4_1","doi-asserted-by":"publisher","DOI":"10.1007\/3\u2010540\u201026765\u20104_1"},{"key":"e_1_2_9_5_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.chom.2020.03.002"},{"key":"e_1_2_9_6_1","doi-asserted-by":"publisher","DOI":"10.1210\/en.2004\u20100443"},{"key":"e_1_2_9_7_1","doi-asserted-by":"publisher","DOI":"10.1002\/prca.200601013"},{"key":"e_1_2_9_8_1","doi-asserted-by":"publisher","DOI":"10.1093\/humupd\/dmy017"},{"key":"e_1_2_9_9_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.celrep.2020.108175"},{"key":"e_1_2_9_10_1","doi-asserted-by":"publisher","DOI":"10.1111\/andr.13073"},{"key":"e_1_2_9_11_1","doi-asserted-by":"publisher","DOI":"10.4103\/aja.aja_82_20"},{"key":"e_1_2_9_12_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00011\u2010021\u201001497\u20104"},{"key":"e_1_2_9_13_1","doi-asserted-by":"publisher","DOI":"10.3390\/cells11172631"},{"key":"e_1_2_9_14_1","doi-asserted-by":"publisher","DOI":"10.1093\/cid\/ciac142"},{"key":"e_1_2_9_15_1","doi-asserted-by":"publisher","DOI":"10.1111\/andr.12859"},{"key":"e_1_2_9_16_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00345\u2010003\u20100365\u20109"},{"key":"e_1_2_9_17_1","doi-asserted-by":"publisher","DOI":"10.3389\/fphys.2022.867444"},{"key":"e_1_2_9_18_1","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.200606027"},{"key":"e_1_2_9_19_1","doi-asserted-by":"publisher","DOI":"10.1007\/s13770\u2010020\u201000241\u2010z"},{"key":"e_1_2_9_20_1","doi-asserted-by":"publisher","DOI":"10.1038\/nri.2017.105"},{"key":"e_1_2_9_21_1","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2012.00362"},{"key":"e_1_2_9_22_1","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2022.838011"},{"key":"e_1_2_9_23_1","doi-asserted-by":"publisher","DOI":"10.1001\/jama.2013.281053"},{"key":"e_1_2_9_24_1","volume-title":"WHO Laboratory Manual for the Examination and Processing of Human Semen","author":"World Health Organization","year":"2021"},{"key":"e_1_2_9_25_1","doi-asserted-by":"publisher","DOI":"10.1111\/and.13973"},{"key":"e_1_2_9_26_1","first-page":"199","article-title":"SARS\u2010CoV\u20102 effects on the male genitourinary system","volume":"10","author":"Connelly ZM","year":"2022","journal-title":"Am J Clin Exp Urol"},{"key":"e_1_2_9_27_1","doi-asserted-by":"publisher","DOI":"10.1111\/andr.12896"},{"key":"e_1_2_9_28_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41422\u2010021\u201000523\u20108"},{"key":"e_1_2_9_29_1","doi-asserted-by":"publisher","DOI":"10.1002\/jum.15558"},{"key":"e_1_2_9_30_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41591\u2010022\u201001780\u20109"},{"key":"e_1_2_9_31_1","doi-asserted-by":"publisher","DOI":"10.1039\/d0an01988g"},{"key":"e_1_2_9_32_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ejrad.2020.108961"},{"key":"e_1_2_9_33_1","doi-asserted-by":"publisher","DOI":"10.1148\/radiol.2020200432"},{"key":"e_1_2_9_34_1","doi-asserted-by":"publisher","DOI":"10.2164\/jandrol.04104"},{"key":"e_1_2_9_35_1","doi-asserted-by":"publisher","DOI":"10.21037\/tau.2017.08.03"},{"key":"e_1_2_9_36_1","doi-asserted-by":"publisher","DOI":"10.1016\/0140\u20106736(92)92425\u2010f"},{"key":"e_1_2_9_37_1","doi-asserted-by":"publisher","DOI":"10.1111\/andr.12809"},{"key":"e_1_2_9_38_1","doi-asserted-by":"publisher","DOI":"10.1590\/S1677\u20105538.IBJU.2020.06.03"},{"key":"e_1_2_9_39_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.fertnstert.2019.02.002"},{"key":"e_1_2_9_40_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.fertnstert.2015.11.028"},{"key":"e_1_2_9_41_1","doi-asserted-by":"publisher","DOI":"10.1111\/and.13202"},{"key":"e_1_2_9_42_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1439\u20100272.1990.tb02005.x"},{"key":"e_1_2_9_43_1","doi-asserted-by":"publisher","DOI":"10.1093\/humupd\/dmac037"},{"key":"e_1_2_9_44_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.mrfmmm.2020.111722"},{"key":"e_1_2_9_45_1","doi-asserted-by":"publisher","DOI":"10.1084\/jem.20201129"},{"key":"e_1_2_9_46_1","doi-asserted-by":"publisher","DOI":"10.1590\/s1677\u20105538.ibju.2020.0872"},{"key":"e_1_2_9_47_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.1092385"},{"key":"e_1_2_9_48_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0032366"},{"key":"e_1_2_9_49_1","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.200806072"},{"key":"e_1_2_9_50_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.coi.2012.08.010"},{"key":"e_1_2_9_51_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.fertnstert.2016.06.005"},{"key":"e_1_2_9_52_1","doi-asserted-by":"publisher","DOI":"10.1530\/rep\u201020\u20100185"},{"key":"e_1_2_9_53_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.eclinm.2020.100604"}],"container-title":["Andrology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/andr.13612","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,11,7]],"date-time":"2024-11-07T12:15:23Z","timestamp":1730981723000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1111\/andr.13612"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,3,12]]},"references-count":52,"journal-issue":{"issue":"8","published-print":{"date-parts":[[2024,11]]}},"alternative-id":["10.1111\/andr.13612"],"URL":"https:\/\/doi.org\/10.1111\/andr.13612","archive":["Portico"],"relation":{},"ISSN":["2047-2919","2047-2927"],"issn-type":[{"value":"2047-2919","type":"print"},{"value":"2047-2927","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,3,12]]},"assertion":[{"value":"2023-09-04","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2024-01-23","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2024-03-12","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}