{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,13]],"date-time":"2026-05-13T01:21:17Z","timestamp":1778635277949,"version":"3.51.4"},"reference-count":23,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2022,3,3]],"date-time":"2022-03-03T00:00:00Z","timestamp":1646265600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JoF"],"abstract":"<jats:p>While COVID-19-associated pulmonary aspergillosis is now well described in developed countries, COVID-19-associated mucormycosis (CAM) has seemed to remain quite rare in Europe. A retrospective study was performed between March 2020 to September 2021 among COVID-19 adult patients in the intensive care unit (ICU) at Toulouse Hospital (Southern France). PCR screening on respiratory samples, which target Aspergillus or Mucorales DNA, were performed, and the number of fungal detections was evaluated monthly during the study period. During the 19 months of the study, 44 (20.3%) COVID-19 ICU patients had a positive PCR for Aspergillus, an overall rate in keeping with the incidence of ICU COVID-19 patients. Ten patients (7.1%) had a positive Mucorales PCR over the same period. Surprisingly, 9\/10 had a positive Mucor\/Rhizopus PCR in August-September 2021, during the fourth Delta SARS-CoV-2 variant wave. Epidemic investigations have identified a probable environmental cause linked to construction works in the vicinity of the ICU (high levels of airborne spores due to the mistaken interruption of preventive humidification and summer temperature). Even if CAM are apparently rare in Europe, a cluster can also develop in industrialised countries when environmental conditions (especially during construction work) are associated with a high number of COVID-19 patients in the ICU.<\/jats:p>","DOI":"10.3390\/jof8030258","type":"journal-article","created":{"date-parts":[[2022,3,3]],"date-time":"2022-03-03T09:24:53Z","timestamp":1646299493000},"page":"258","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["A Clustered Case Series of Mucorales Detection in Respiratory Samples from COVID-19 Patients in Intensive Care, France, August to September 2021"],"prefix":"10.3390","volume":"8","author":[{"given":"Emilie","family":"Guemas","sequence":"first","affiliation":[{"name":"Department of Parasitology and Mycology, Toulouse University Hospital, 31059 Toulouse, France"},{"name":"Institut Toulousain des Maladies Infectieuses et Inflammatoires (Infinity), Universit\u00e9 Toulouse, CNRS UMR5051, INSERM UMR1291, UPS, 31024 Toulouse, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0055-0136","authenticated-orcid":false,"given":"Sophie","family":"Cassaing","sequence":"additional","affiliation":[{"name":"Department of Parasitology and Mycology, Toulouse University Hospital, 31059 Toulouse, France"},{"name":"RESTORE (Geroscience and Rejuvenation Research Center), UMR 1301-Inserm 5070-CNRS EFS, Universit\u00e9 Paul Sabatier, 31100 Toulouse, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sandra","family":"Malavaud","sequence":"additional","affiliation":[{"name":"Healthcare Associated Risk Prevention Unit (UPRIAS), Toulouse University Hospital, 31059 Toulouse, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5277-189X","authenticated-orcid":false,"given":"Judith","family":"Fillaux","sequence":"additional","affiliation":[{"name":"Department of Parasitology and Mycology, Toulouse University Hospital, 31059 Toulouse, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Pamela","family":"Chauvin","sequence":"additional","affiliation":[{"name":"Department of Parasitology and Mycology, Toulouse University Hospital, 31059 Toulouse, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Lucie","family":"Leli\u00e8vre","sequence":"additional","affiliation":[{"name":"Department of Infectious and Tropical Diseases, Toulouse University Hospital, 31059 Toulouse, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"St\u00e9phanie","family":"Ruiz","sequence":"additional","affiliation":[{"name":"Department of Anesthesiology and Intensive Care, Toulouse University Hospital, 31059 Toulouse, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"B\u00e9atrice","family":"Riu","sequence":"additional","affiliation":[{"name":"Department of Anesthesiology and Intensive Care, Toulouse University Hospital, 31059 Toulouse, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Antoine","family":"Berry","sequence":"additional","affiliation":[{"name":"Department of Parasitology and Mycology, Toulouse University Hospital, 31059 Toulouse, France"},{"name":"Institut Toulousain des Maladies Infectieuses et Inflammatoires (Infinity), Universit\u00e9 Toulouse, CNRS UMR5051, INSERM UMR1291, UPS, 31024 Toulouse, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xavier","family":"Iriart","sequence":"additional","affiliation":[{"name":"Department of Parasitology and Mycology, Toulouse University Hospital, 31059 Toulouse, France"},{"name":"Institut Toulousain des Maladies Infectieuses et Inflammatoires (Infinity), Universit\u00e9 Toulouse, CNRS UMR5051, INSERM UMR1291, UPS, 31024 Toulouse, France"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,3,3]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"697","DOI":"10.1016\/S1473-3099(20)30200-0","article-title":"Clinical and virological data of the first cases of COVID-19 in Europe: A case series","volume":"20","author":"Lescure","year":"2020","journal-title":"Lancet Infect. Dis."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"e149","DOI":"10.1016\/S1473-3099(20)30847-1","article-title":"Defining and managing COVID-19-associated pulmonary aspergillosis: The 2020 ECMM\/ISHAM consensus criteria for research and clinical guidance","volume":"21","author":"Koehler","year":"2021","journal-title":"Lancet Infect. Dis."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"2349","DOI":"10.3201\/eid2709.210934","article-title":"Multicenter epidemiologic study of coronavirus disease-associated mucormycosis, India","volume":"27","author":"Patel","year":"2021","journal-title":"Emerg. Infect. Dis."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1028","DOI":"10.1111\/myc.13335","article-title":"ECMM\/ISHAM recommendations for clinical management of COVID-19 associated mucormycosis in low- and middle-income countries","volume":"64","author":"Rudramurthy","year":"2021","journal-title":"Mycoses"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1016\/S2213-2600(21)00442-2","article-title":"Fungal infections in mechanically ventilated patients with COVID-19 during the first wave: The French multicentre MYCOVID study","volume":"10","author":"Gangneux","year":"2021","journal-title":"Lancet Respir. Med."},{"key":"ref_6","unstructured":"de la Sant\u00e9 Publique, C. (2017). D\u00e9cret n\u00b0 2017-884 du 9 mai 2017 modifiant certaines dispositions r\u00e9glementaires relatives aux recherches impliquant la personne humaine. Article R., 1121-1-1."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"RECOVERY Collaborative Group, Horby, P., Lim, W.S., Emberson, J.R., Mafham, M., Bell, J.L., Linsell, L., Staplin, N., Brightling, C., and Ustianowski, A. (2021). Dexamethasone in hospitalized patients with COVID-19. N. Engl. J. Med., 384, 693\u2013704.","DOI":"10.1056\/NEJMoa2021436"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1637","DOI":"10.1016\/S0140-6736(21)00676-0","article-title":"Tocilizumab in patients admitted to hospital with COVID-19 (RECOVERY): A randomised, controlled, open-label, platform trial","volume":"397","author":"Abani","year":"2021","journal-title":"Lancet"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"2224","DOI":"10.1128\/JCM.40.6.2224-2227.2002","article-title":"Real-time PCR coupled with automated DNA extraction and detection of galactomannan antigen in serum by enzyme-linked immunosorbent assay for diagnosis of invasive aspergillosis","volume":"40","author":"Costa","year":"2002","journal-title":"J. Clin. Microbiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"e1","DOI":"10.1016\/j.cmi.2015.12.006","article-title":"Early diagnosis and monitoring of mucormycosis by detection of circulating DNA in serum: Retrospective analysis of 44 cases collected through the French Surveillance Network of Invasive Fungal Infections (RESSIF)","volume":"22","author":"Millon","year":"2016","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"2661","DOI":"10.1128\/JCM.00263-17","article-title":"Validation of a new web application for identification of fungi by use of Matrix-Assisted Laser Desorption Ionization\u2013Time of Flight Mass Spectrometry","volume":"55","author":"Normand","year":"2017","journal-title":"J. Clin. Microbiol. Am. Soc. Microbiol."},{"key":"ref_12","unstructured":"(2022, February 24). M\u00e9t\u00e9o Toulouse (Haute-Garonne), Ao\u00fbt 2021. Hist.-M\u00e9t\u00e9o. Available online: https:\/\/www.historique-meteo.net\/france\/midi-toulousain\/toulouse\/2021\/08\/."},{"key":"ref_13","first-page":"633","article-title":"Mixed mold infection with Aspergillus fumigatus and Rhizopus microsporus in a severe acute respiratory syndrome Coronavirus 2 (SARS-CoV-2) patient","volume":"51","author":"Bellanger","year":"2021","journal-title":"Infect. Dis. Now"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"2100510","DOI":"10.2807\/1560-7917.ES.2021.26.23.2100510","article-title":"Case series of four secondary mucormycosis infections in COVID-19 patients, the Netherlands, December 2020 to May 2021","volume":"26","author":"Buil","year":"2021","journal-title":"Eurosurveillance"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"ofab566","DOI":"10.1093\/ofid\/ofab566","article-title":"Coronavirus disease 2019-Associated Mucormycosis in France: A rare but deadly complication","volume":"9","author":"Danion","year":"2022","journal-title":"Open Forum Infect. Dis."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1351","DOI":"10.1016\/j.jiph.2021.09.004","article-title":"COVID19 associated mucormycosis: Is GRP78 a possible link?","volume":"14","author":"Gumashta","year":"2021","journal-title":"J. Infect. Public Health"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1086\/508832","article-title":"Filamentous fungi in a tertiary care hospital: Environmental surveillance and susceptibility to antifungal drugs","volume":"28","author":"Panagopoulou","year":"2007","journal-title":"Infect. Control. Hosp. Epidemiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"538","DOI":"10.1111\/j.1445-5994.2008.01727.x","article-title":"Preventing invasive fungal infection during hospital building works","volume":"38","author":"Chang","year":"2008","journal-title":"Intern. Med. J."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1093\/cid\/civ297","article-title":"Review of fungal outbreaks and infection prevention in healthcare settings during construction and renovation","volume":"61","author":"Kanamori","year":"2015","journal-title":"Clin. Infect. Dis."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1077","DOI":"10.3201\/eid2704.204895","article-title":"COVID-19-Associated Pulmonary Aspergillosis, March-August 2020","volume":"27","author":"Sprute","year":"2021","journal-title":"Emerg. Infect. Dis."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1186\/s13756-017-0282-0","article-title":"Seasonal clustering of sinopulmonary mucormycosis in patients with hematologic malignancies at a large comprehensive cancer center","volume":"6","author":"Sivagnanam","year":"2017","journal-title":"Antimicrob. Resist. Infect. Control."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1017\/S0950268805004930","article-title":"Mucormycosis in the Eastern Mediterranean: A seasonal disease","volume":"134","author":"Bizri","year":"2006","journal-title":"Epidemiol. Infect."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"503","DOI":"10.1086\/590004","article-title":"Delaying amphotericin B-based frontline therapy significantly increases mortality among patients with hematologic malignancy who have zygomycosis","volume":"47","author":"Chamilos","year":"2008","journal-title":"Clin. Infect. Dis."}],"container-title":["Journal of Fungi"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2309-608X\/8\/3\/258\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T22:31:15Z","timestamp":1760135475000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2309-608X\/8\/3\/258"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,3,3]]},"references-count":23,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2022,3]]}},"alternative-id":["jof8030258"],"URL":"https:\/\/doi.org\/10.3390\/jof8030258","relation":{},"ISSN":["2309-608X"],"issn-type":[{"value":"2309-608X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,3,3]]}}}