{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,8]],"date-time":"2026-10-08T13:11:15Z","timestamp":1791465075428,"version":"4.3.4"},"reference-count":43,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2022,12,14]],"date-time":"2022-12-14T00:00:00Z","timestamp":1670976000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>Background: The range of reported rates of bacterial and fungal superinfections in patients with a severe course of COVID-19 is wide, suggesting a lack of standardised reporting. Methods: The rates of bacterial and fungal superinfection were assessed using predefined criteria to differentiate between infection and contamination. Results: Overall, 117 patients admitted to the Intensive Care Unit due to severe COVID-19 were included. Overall, 55% of patients developed a superinfection and 13.6% developed a fungal superinfection (5.9% candidemia and 7.7% CAPA). The rate of ventilator-associated pneumonia was 65.2%. If superinfection was detected, the length of hospital stay was significantly longer and the mortality was especially increased if candidemia was detected. An increased risk of superinfection was observed in patients with pre-existing diabetes mellitus or chronic heart failure. The presence of immunomodulating therapy did not seem to have an impact on the frequency of superinfections. Conclusion: Increased awareness of high superinfection rates, fungal infections in particular, in patients suffering from severe COVID-19 is necessary.<\/jats:p>","DOI":"10.3390\/v14122785","type":"journal-article","created":{"date-parts":[[2022,12,14]],"date-time":"2022-12-14T03:21:52Z","timestamp":1670988112000},"page":"2785","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":12,"title":["The Role of Bacterial and Fungal Superinfection in Critical COVID-19"],"prefix":"10.3390","volume":"14","author":[{"given":"Tamara","family":"Seitz","sequence":"first","affiliation":[{"name":"Department of Infectious Diseases and Tropical Medicine, Klinik Favoriten, 1100 Vienna, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Johannes","family":"Holbik","sequence":"additional","affiliation":[{"name":"Department of Infectious Diseases and Tropical Medicine, Klinik Favoriten, 1100 Vienna, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9449-5144","authenticated-orcid":false,"given":"Alexander","family":"Grieb","sequence":"additional","affiliation":[{"name":"Department of Infectious Diseases and Tropical Medicine, Klinik Favoriten, 1100 Vienna, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mario","family":"Karolyi","sequence":"additional","affiliation":[{"name":"Department of Infectious Diseases and Tropical Medicine, Klinik Favoriten, 1100 Vienna, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4409-6855","authenticated-orcid":false,"given":"Julian","family":"Hind","sequence":"additional","affiliation":[{"name":"Department of Infectious Diseases and Tropical Medicine, Klinik Favoriten, 1100 Vienna, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Georg","family":"Gibas","sequence":"additional","affiliation":[{"name":"Department of Infectious Diseases and Tropical Medicine, Klinik Favoriten, 1100 Vienna, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stephanie","family":"Neuhold","sequence":"additional","affiliation":[{"name":"Department of Infectious Diseases and Tropical Medicine, Klinik Favoriten, 1100 Vienna, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alexander","family":"Zoufaly","sequence":"additional","affiliation":[{"name":"Department of Infectious Diseases and Tropical Medicine, Klinik Favoriten, 1100 Vienna, Austria"},{"name":"Faculty of Medicine, Sigmund Freud University, 1020 Vienna, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christoph","family":"Wenisch","sequence":"additional","affiliation":[{"name":"Department of Infectious Diseases and Tropical Medicine, Klinik Favoriten, 1100 Vienna, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,12,14]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1016\/j.cmi.2020.10.021","article-title":"Secondary infections in patients hospitalized with COVID-19: Incidence and predictive factors","volume":"27","author":"Ripa","year":"2021","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"8557","DOI":"10.21037\/apm-21-833","article-title":"Secondary infection in severe and critical COVID-19 patients in China: A multicenter retrospective study","volume":"10","author":"Sang","year":"2021","journal-title":"Ann. Palliat Med."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1016\/S0140-6736(20)30211-7","article-title":"Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: A descriptive study","volume":"395","author":"Chen","year":"2020","journal-title":"Lancet"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1054","DOI":"10.1016\/S0140-6736(20)30566-3","article-title":"Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: A retrospective cohort study","volume":"395","author":"Zhou","year":"2020","journal-title":"Lancet"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"921","DOI":"10.1164\/rccm.202106-1354OC","article-title":"Bacterial Superinfection Pneumonia in Patients Mechanically Ventilated for COVID-19 Pneumonia","volume":"204","author":"Pickens","year":"2021","journal-title":"Am. J. Respir. Crit. Care Med."},{"key":"ref_6","first-page":"1","article-title":"Inadequate use of antibiotics in the covid-19 era: Effectiveness of antibiotic therapy","volume":"21","author":"Agudo","year":"2021","journal-title":"BMC Infect. Dis."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1016\/j.jinf.2016.11.011","article-title":"Molecular diagnosis of bloodstream infections in onco-haematology patients with PCR\/ESI-MS technology","volume":"74","author":"Rivaya","year":"2017","journal-title":"J. Infect."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Roudbary, M., Kumar, S., Kumar, A., \u010cern\u00e1kov\u00e1, L., Nikoomanesh, F., and Rodrigues, C.F. (2021). Overview on the Prevalence of Fungal Infections, Immune Response, and Microbiome Role in COVID-19 Patients. J. Fungi, 7.","DOI":"10.3390\/jof7090720"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1111\/myc.13225","article-title":"Increased incidence of candidemia in a tertiary care hospital with the COVID-19 pandemic","volume":"64","author":"Nucci","year":"2021","journal-title":"Mycoses"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1016\/j.jmii.2020.09.004","article-title":"COVID-19 associated with pulmonary aspergillosis: A literature review","volume":"54","author":"Lai","year":"2021","journal-title":"J. Microbiol. Immunol. Infect."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/j.ijid.2021.10.001","article-title":"COVID-19 and antimicrobial stewardship: Lessons learned, best practices, and future implications","volume":"113","author":"Pierce","year":"2021","journal-title":"Int. J. Infect. Dis."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1007\/s10096-004-1103-y","article-title":"Epidemiology of candidaemia in Europe: Results of 28-month European Confederation of Medical Mycology (ECMM) hospital-based surveillance study","volume":"23","author":"Tortorano","year":"2004","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"475","DOI":"10.1016\/S2213-2600(20)30079-5","article-title":"Clinical course and outcomes of critically ill patients with SARS-CoV-2 pneumonia in Wuhan, China: A single-centered, retrospective, observational study","volume":"8","author":"Yang","year":"2020","journal-title":"Lancet Respir. Med."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"e0251170","DOI":"10.1371\/journal.pone.0251170","article-title":"Prevalence and outcomes of co-infection and superinfection with SARS-CoV-2 and other pathogens: A systematic review and meta-analysis","volume":"16","author":"Musuuza","year":"2021","journal-title":"PLoS ONE"},{"key":"ref_15","unstructured":"(2022, December 11). T2MR Technology|T2 Biosystems, n.d. Available online: https:\/\/www.t2biosystems.com\/products-technology\/t2mr-technology\/."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1086\/599376","article-title":"IDSA Guidelines for Intravascular Catheter-Related Infection Clinical Practice Guidelines for the Diagnosis and Management of Intravascular Catheter-Related Infection: 2009 Update by the Infectious Diseases Society of America","volume":"49","author":"Mermel","year":"2009","journal-title":"Clin. Infect. Dis."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"(2005). Guidelines for the management of adults with hospital-acquired, ventilator-associated, and healthcare-associated pneumonia. Am. J. Respir. Crit. Care Med., 171, 388\u2013416.","DOI":"10.1164\/rccm.200405-644ST"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"2002554","DOI":"10.1183\/13993003.02554-2020","article-title":"Confronting and mitigating the risk of COVID-19 associated pulmonary aspergillosis","volume":"56","author":"Youngs","year":"2020","journal-title":"Eur. Respir. J."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"454","DOI":"10.1016\/j.chest.2021.04.002","article-title":"Hospital-Acquired Infections in Critically Ill Patients With COVID-19","volume":"160","author":"Grasselli","year":"2021","journal-title":"Chest"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1078","DOI":"10.1093\/jac\/dkaa530","article-title":"Predictors of hospital-acquired bacterial and fungal superinfections in COVID-19: A prospective observational study","volume":"76","author":"Falcone","year":"2021","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1609","DOI":"10.3390\/covid2110116","article-title":"Inflammation in COVID-19: A Risk for Superinfections","volume":"2","author":"Boulos","year":"2022","journal-title":"COVID"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1083","DOI":"10.1111\/myc.13332","article-title":"Characteristics of candidemia in COVID-19 patients; increased incidence, earlier occurrence and higher mortality rates compared to non-COVID-19 patients","volume":"64","author":"Kayaaslan","year":"2021","journal-title":"Mycoses"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"802","DOI":"10.1093\/cid\/ciab562","article-title":"The Landscape of Candidemia During the Coronavirus Disease 2019 (COVID-19) Pandemic","volume":"74","author":"Seagle","year":"2022","journal-title":"Clin. Infect. Dis."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1262","DOI":"10.1093\/mmy\/myab056","article-title":"Clinical characteristics and risk factors for COVID-19-associated Candidemia","volume":"59","author":"Omrani","year":"2021","journal-title":"Med. Mycol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1284","DOI":"10.1093\/cid\/cit006","article-title":"Finding the \u201cmissing 50%\u201d of invasive candidiasis: How nonculture diagnostics will improve understanding of disease spectrum and transform patient care","volume":"56","author":"Clancy","year":"2013","journal-title":"Clin. Infect. Dis."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1007\/s11046-017-0238-1","article-title":"A Retrospective Assessment of Four Antigen Assays for the Detection of Invasive Candidiasis Among High-Risk Hospitalized Patients","volume":"183","author":"Hartl","year":"2018","journal-title":"Mycopathologia"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"e01756-17","DOI":"10.1128\/JCM.01756-17","article-title":"Efficacy of T2 Magnetic Resonance Assay in Monitoring Candidemia after Initiation of Antifungal Therapy: The Serial Therapeutic and Antifungal Monitoring Protocol (STAMP) Trial","volume":"56","author":"Mylonakis","year":"2018","journal-title":"J. Clin. Microbiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"e00140-22","DOI":"10.1128\/spectrum.00140-22","article-title":"Rapid Detection of Bacterial and Fungal Pathogens Using the T2MR versus Blood Culture in Patients with Severe COVID-19","volume":"10","author":"Seitz","year":"2022","journal-title":"Microbiol. Spectr."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"372","DOI":"10.3390\/idr14030041","article-title":"Bacterial and Fungal Co-Infections and Superinfections in a Cohort of COVID-19 Patients: Real-Life Data from an Italian Third Level Hospital","volume":"14","author":"Ceccarelli","year":"2022","journal-title":"Infect. Dis. Rep."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Russo, A., Olivadese, V., Trecarichi, E.M., and Torti, C. (2022). Bacterial Ventilator-Associated Pneumonia in COVID-19 Patients: Data from the Second and Third Waves of the Pandemic. J. Clin. Med., 11.","DOI":"10.3390\/jcm11092279"},{"key":"ref_31","first-page":"1","article-title":"Ventilator-associated pneumonia in critically ill patients with COVID-19","volume":"25","author":"Maes","year":"2021","journal-title":"Crit. Care"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"46","DOI":"10.4103\/0976-9668.198360","article-title":"Incidence, bacteriology, and clinical outcome of ventilator-associated pneumonia at tertiary care hospital","volume":"8","author":"Patil","year":"2017","journal-title":"J. Nat. Sci. Biol. Med."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"599","DOI":"10.1007\/s11046-020-00462-9","article-title":"Fungal Co-infections Associated with Global COVID-19 Pandemic: A Clinical and Diagnostic Perspective from China","volume":"185","author":"Song","year":"2020","journal-title":"Mycopathologia"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"e1","DOI":"10.1093\/cid\/ciw326","article-title":"Practice Guidelines for the Diagnosis and Management of Aspergillosis: 2016 Update by the Infectious Diseases Society of America","volume":"63","author":"Patterson","year":"2016","journal-title":"Clin. Infect. Dis."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"388","DOI":"10.1016\/j.jinf.2020.02.016","article-title":"Clinical characteristics and imaging manifestations of the 2019 novel coronavirus disease (COVID-19):A multi-center study in Wenzhou city, Zhejiang, China","volume":"80","author":"Yang","year":"2020","journal-title":"J. Infect."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"969","DOI":"10.1016\/j.cell.2020.04.042","article-title":"Trained Immunity: A Tool for Reducing Susceptibility to and the Severity of SARS-CoV-2 Infection","volume":"181","author":"Netea","year":"2020","journal-title":"Cell"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"484","DOI":"10.1016\/j.jinf.2019.04.002","article-title":"Development and internal validation of a model for predicting 60-day risk of invasive mould disease in patients with haematological malignancies","volume":"78","author":"Stanzani","year":"2019","journal-title":"J. Infect."},{"key":"ref_38","first-page":"1631","article-title":"Navigating the Uncertainties of COVID-19\u2013Associated Aspergillosis: A Comparison With Influenza-Associated Aspergillosis","volume":"224","author":"Lamoth","year":"2021","journal-title":"J. Infect. Dis."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"6670798","DOI":"10.1155\/2021\/6670798","article-title":"The Role of Bacterial and Fungal Human Respiratory Microbiota in COVID-19 Patients","volume":"2021","author":"Soltani","year":"2021","journal-title":"Biomed Res. Int."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"782","DOI":"10.1001\/jama.2020.12839","article-title":"Pathophysiology, Transmission, Diagnosis, and Treatment of Coronavirus Disease 2019 (COVID-19): A Review","volume":"324","author":"Wiersinga","year":"2020","journal-title":"JAMA"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1236","DOI":"10.1016\/j.numecd.2020.05.014","article-title":"Diabetes as a risk factor for greater COVID-19 severity and in-hospital death: A meta-analysis of observational studies","volume":"30","author":"Mantovani","year":"2020","journal-title":"Nutr. Metab. Cardiovasc. Dis."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/j.ijid.2020.03.017","article-title":"Prevalence of comorbidities and its effects in patients infected with SARS-CoV-2: A systematic review and meta-analysis","volume":"94","author":"Yang","year":"2020","journal-title":"Int. J. Infect. Dis."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"749","DOI":"10.1080\/00325481.2020.1786964","article-title":"COVID-19 and Comorbidities: A Systematic Review and Meta-Analysis","volume":"132","author":"Gold","year":"2020","journal-title":"Postgrad. Med."}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/14\/12\/2785\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:40:59Z","timestamp":1760146859000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/14\/12\/2785"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,12,14]]},"references-count":43,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2022,12]]}},"alternative-id":["v14122785"],"URL":"https:\/\/doi.org\/10.3390\/v14122785","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,12,14]]}}}