{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,16]],"date-time":"2026-06-16T13:15:21Z","timestamp":1781615721147,"version":"3.54.5"},"reference-count":43,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2023,9,15]],"date-time":"2023-09-15T00:00:00Z","timestamp":1694736000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"EU funding within the MUR PNRR Extended Partner-ship initiative on Emerging Infectious Diseases","award":["PE00000007"],"award-info":[{"award-number":["PE00000007"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>Background: The relationship between superinfection by multidrug-resistant Gram-negative bacteria and mortality among SARS-CoV-2 hospitalized patients is still unclear. Carbapenem-resistant Acinetobacter baumannii and carbapenemase-producing Enterobacterales are among the most frequently isolated species when it comes to hospital-acquired superinfections among SARS-CoV-2 patients. Methods: Herein, a retrospective study was carried out using data from adult patients hospitalized for COVID-19. The interaction between in-hospital mortality and rectal carriage and superinfection by carbapenemase-producing Enterobacterales and\/or carbapenem-resistant Acinetobacter baumannii was assessed. Results: The incidence of KPC-producing Klebsiella pneumoniae and\/or carbapenem-resistant Acinetobacter baumannii rectal carriage was 30%. Bloodstream infection and\/or pneumonia due to KPC-producing Klebsiella pneumoniae and\/or carbapenem-resistant Acinetobacter baumannii occurred in 20% of patients. A higher Charlson comorbidity index (OR 1.41, 95% CI 1.24\u20131.59), being submitted to invasive mechanical ventilation\/ECMO \u2265 96 h (OR 6.34, 95% CI 3.18\u201312.62), being treated with systemic corticosteroids (OR 4.67, 95% CI 2.43\u20139.05) and having lymphopenia at the time of admission (OR 0.54, 95% CI 0.40\u20130.72) were the features most strongly associated with in-hospital mortality. Conclusions: Although KPC-producing Klebsiella pneumoniae and\/or carbapenem-resistant Acinetobacter baumannii rectal carriage, and\/or bloodstream infection\/pneumonia were diagnosed in a remarkable percentage of COVID-19 patients, their impact on in-hospital mortality was not significant. Further studies are needed to assess the burden of antimicrobial resistance as a legacy of COVID-19 in order to identify future prevention opportunities.<\/jats:p>","DOI":"10.3390\/v15091934","type":"journal-article","created":{"date-parts":[[2023,9,17]],"date-time":"2023-09-17T06:36:45Z","timestamp":1694932605000},"page":"1934","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":22,"title":["Prevalence and Impact on Mortality of Colonization and Super-Infection by Carbapenem-Resistant Gram-Negative Organisms in COVID-19 Hospitalized Patients"],"prefix":"10.3390","volume":"15","author":[{"given":"Roberto","family":"Casale","sequence":"first","affiliation":[{"name":"Microbiology and Virology Unit, University Hospital Citt\u00e0 della Salute e della Scienza di Torino, 10126 Turin, Italy"},{"name":"Department of Public Health and Paediatrics, University of Torino, 10126 Turin, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8180-5075","authenticated-orcid":false,"given":"Gabriele","family":"Bianco","sequence":"additional","affiliation":[{"name":"Microbiology and Virology Unit, University Hospital Citt\u00e0 della Salute e della Scienza di Torino, 10126 Turin, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paulo","family":"Bastos","sequence":"additional","affiliation":[{"name":"Independent Researcher, 1169-056 Lisbon, Portugal"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sara","family":"Comini","sequence":"additional","affiliation":[{"name":"Microbiology and Virology Unit, University Hospital Citt\u00e0 della Salute e della Scienza di Torino, 10126 Turin, Italy"},{"name":"Department of Public Health and Paediatrics, University of Torino, 10126 Turin, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Silvia","family":"Corcione","sequence":"additional","affiliation":[{"name":"Department of Medical Sciences, Infectious Diseases, University of Turin, 10126 Turin, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6726-2716","authenticated-orcid":false,"given":"Matteo","family":"Boattini","sequence":"additional","affiliation":[{"name":"Microbiology and Virology Unit, University Hospital Citt\u00e0 della Salute e della Scienza di Torino, 10126 Turin, Italy"},{"name":"Department of Public Health and Paediatrics, University of Torino, 10126 Turin, Italy"},{"name":"Lisbon Academic Medical Centre, 1169-056 Lisbon, Portugal"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rossana","family":"Cavallo","sequence":"additional","affiliation":[{"name":"Microbiology and Virology Unit, University Hospital Citt\u00e0 della Salute e della Scienza di Torino, 10126 Turin, Italy"},{"name":"Department of Public Health and Paediatrics, University of Torino, 10126 Turin, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8338-0130","authenticated-orcid":false,"given":"Francesco Giuseppe De","family":"Rosa","sequence":"additional","affiliation":[{"name":"Department of Medical Sciences, Infectious Diseases, University of Turin, 10126 Turin, Italy"},{"name":"Unit of Infectious Diseases, Cardinal Massaia, 14100 Asti, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6549-4553","authenticated-orcid":false,"given":"Cristina","family":"Costa","sequence":"additional","affiliation":[{"name":"Microbiology and Virology Unit, University Hospital Citt\u00e0 della Salute e della Scienza di Torino, 10126 Turin, Italy"},{"name":"Department of Public Health and Paediatrics, University of Torino, 10126 Turin, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,9,15]]},"reference":[{"key":"ref_1","unstructured":"(2023, March 18). Weekly Epidemiological Update on COVID-19 22 February 2023 n.d. Available online: https:\/\/www.who.int\/publications\/m\/item\/weekly-epidemiological-update-on-covid-19---22-february-2023."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1007\/s12016-022-08921-5","article-title":"Risk and Protective Factors for COVID-19 Morbidity, Severity, and Mortality","volume":"64","author":"Zhang","year":"2023","journal-title":"Clin. Rev. Allergy Immunol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1202","DOI":"10.1513\/AnnalsATS.202008-1026OC","article-title":"COVID-19 versus Non-COVID-19 Acute Respiratory Distress Syndrome: Comparison of Demographics, Physiologic Parameters, Inflammatory Biomarkers, and Clinical Outcomes","volume":"18","author":"Bain","year":"2021","journal-title":"Ann. Am. Thorac. Soc."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"520","DOI":"10.1016\/j.cmi.2020.12.018","article-title":"Antibiotic prescribing in patients with COVID-19: Rapid review and meta-analysis","volume":"27","author":"Langford","year":"2021","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Musuuza, J.S., Watson, L., Parmasad, V., Putman-Buehler, N., Christensen, L., and Safdar, N. (2021). Prevalence and outcomes of co-infection and superinfection with SARS-CoV-2 and other pathogens: A systematic review and meta-analysis. PLoS ONE, 16.","DOI":"10.1371\/journal.pone.0251170"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"491","DOI":"10.1016\/j.cmi.2021.11.008","article-title":"Predictors and microbiology of respiratory and blood-stream bacterial infection in patients with COVID-19: Living rapid review update and meta-regression","volume":"28","author":"Langford","year":"2022","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"e179","DOI":"10.1016\/S2666-5247(22)00355-X","article-title":"Antimicrobial resistance in patients with COVID-19: A systematic review and meta-analysis","volume":"4","author":"Langford","year":"2023","journal-title":"Lancet Microbe"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1203","DOI":"10.1007\/s00134-018-5268-8","article-title":"Pathogen colonization of the gastro-intestinal microbiome at intensive care unit admission and risk for subsequent death or infection","volume":"44","author":"Freedberg","year":"2018","journal-title":"Intensive Care Med."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1016\/j.jhin.2016.05.018","article-title":"Carbapenem-resistant Enterobacteriaceae colonization and infection in critically ill patients: A retrospective matched cohort comparison with non-carriers","volume":"94","author":"Dickstein","year":"2016","journal-title":"J. Hosp. Infect."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Garc\u00eda-Garc\u00eda, J., Diez-Echave, P., Yuste, M.E., Chueca, N., Garc\u00eda, F., Cabeza-Barrera, J., Fern\u00e1ndez-Var\u00f3n, E., G\u00e1lvez, J., Colmenero, M., and Rodr\u00edguez-Cabezas, M.E. (2023). Gut Microbiota Composition Can Predict Colonization by Multidrug-Resistant Bacteria in SARS-CoV-2 Patients in Intensive Care Unit: A Pilot Study. Antibiotics, 12.","DOI":"10.3390\/antibiotics12030498"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Iacovelli, A., Oliva, A., Siccardi, G., Tramontano, A., Pellegrino, D., Mastroianni, C.M., Venditti, M., and Palange, P. (2023). Risk factors and effect on mortality of superinfections in a newly established COVID-19 respiratory sub-intensive care unit at University Hospital in Rome. BMC Pulm. Med., 23.","DOI":"10.1186\/s12890-023-02315-9"},{"key":"ref_12","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_13","doi-asserted-by":"crossref","unstructured":"Bedeni\u0107, B., Brati\u0107, V., Mihaljevi\u0107, S., Luki\u0107, A., Vidovi\u0107, K., Reiner, K., Sch\u00f6enthaler, S., Bari\u0161i\u0107, I., Zarfel, G., and Grisold, A. (2023). Multi-drug-Resistant Bacteria in a COVID-19 Hospital in Zagreb. Pathogens, 12.","DOI":"10.3390\/pathogens12010117"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1007\/s15010-021-01643-4","article-title":"Multidrug-resistant Acinetobacter bau-mannii infections in COVID-19 patients hospitalized in intensive care unit","volume":"50","author":"Russo","year":"2022","journal-title":"Infection"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1167","DOI":"10.1089\/mdr.2020.0489","article-title":"Multidrug-Resistant Infections and Outcome of Critically Ill Patients with Coronavirus Disease 2019: A Single Center Experience","volume":"27","author":"Karruli","year":"2021","journal-title":"Microb. Drug Resist."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1016\/j.jhin.2022.02.001","article-title":"Outbreak of ceftazidime-avibactam resistant KPC-producing Klebsiella pneumoniae in a COVID-19 Intensive Care Unit, Italy: Urgent need for updating diagnostic protocols of surveillance cultures","volume":"122","author":"Bianco","year":"2022","journal-title":"J. Hosp. Infect."},{"key":"ref_17","first-page":"537.e1","article-title":"Deciphering variable resistance to novel carbapenem-based \u03b2-lactamase inhibitor combinations in a multi-clonal outbreak caused by Klebsiella pneumoniae carbapenemase (KPC)-producing Klebsiella pneumoniae resistant to ceftazidime\/avibactam","volume":"29","author":"Principe","year":"2022","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"e0373322","DOI":"10.1128\/spectrum.03733-22","article-title":"Outbreak of Klebsiella pneumoniae ST11 Resistant To Ceftazidime-Avibactam Producing KPC-31 and the Novel Variant KPC-115 during COVID-19 Pan-demic in Argentina","volume":"10","author":"Nicola","year":"2022","journal-title":"Microbiol. Spectr."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"302","DOI":"10.1080\/1120009X.2022.2031471","article-title":"Activity of ceftolozane-tazobactam, ceftazidime-avibactam, meropenem-vaborbactam, cefiderocol and comparators against Gram-negative organisms causing bloodstream infections in Northern Italy (2019\u20132021): Emergence of complex resistance phenotypes","volume":"34","author":"Bianco","year":"2022","journal-title":"J. Chemother."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1016\/0021-9681(87)90171-8","article-title":"A new method of classifying prognostic comorbidity in longitudinal studies: Development and validation","volume":"40","author":"Charlson","year":"1987","journal-title":"J. Chronic Dis."},{"key":"ref_21","unstructured":"(2023, March 15). Available online: https:\/\/www.eucast.org\/fileadmin\/src\/media\/PDFs\/EUCAST_files\/Breakpoint_tables\/v_13.0_Breakpoint_Tables.pdf."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1875","DOI":"10.1002\/jmv.26050","article-title":"Predictors of mortality in hospitalized COVID-19 patients: A systematic review and meta-analysis","volume":"92","author":"Tian","year":"2020","journal-title":"J. Med. Virol."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Shbaklo, N., Corcione, S., Vicentini, C., Giordano, S., Fiorentino, D., Bianco, G., Cattel, F., Cavallo, R., Zotti, C.M., and De Rosa, F.G. (2022). An Observational Study of MDR Hospital-Acquired Infections and Antibiotic Use during COVID-19 Pandemic: A Call for Antimicrobial Stewardship Pro-grams. Antibiotics, 11.","DOI":"10.3390\/antibiotics11050695"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1772","DOI":"10.1016\/j.cmi.2021.06.001","article-title":"The interface between COVID-19 and bacterial healthcare-associated infections","volume":"27","year":"2021","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1186\/s13756-021-00919-6","article-title":"Risk factors for nosocomial rectal colonization with carbapenem-resistant Acinetobacter baumannii in hospital: A matched case-control study","volume":"10","author":"Meschiari","year":"2021","journal-title":"Antimicrob. Resist. Infect. Control"},{"key":"ref_26","first-page":"51","article-title":"Blood stream infections during the first wave of COVID-19. A short microbiological retrospective picture at Papa Giovanni XXIII Hospital, Bergamo, Italy","volume":"44","author":"Manisco","year":"2021","journal-title":"New Microbiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1017\/ice.2021.144","article-title":"Carbapenem-resistant bacteria in an intensive care unit during the coronavirus disease 2019 (COVID-19) pandemic: A multicenter before-and-after cross-sectional study","volume":"43","author":"Pascale","year":"2022","journal-title":"Infect. Control Hosp. Epidemiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"823626","DOI":"10.3389\/fcimb.2022.823626","article-title":"The Collateral Effects of COVID-19 Pandemic on the Status of Carbapenemase-Producing Pathogens","volume":"12","year":"2022","journal-title":"Front. Cell Infect. Microbiol."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Tiri, B., Sensi, E., Marsiliani, V., Cantarini, M., Priante, G., Vernelli, C., Martella, L.A., Costantini, M., Mariottini, A., and Andreani, P. (2020). Antimicrobial Stewardship Program, COVID-19, and Infection Control: Spread of Carbapenem-Resistant Klebsiella Pneumoniae Colonization in ICU COVID-19 Patients. What Did Not Work?. J. Clin. Med., 9.","DOI":"10.3390\/jcm9092744"},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Gaspar, G.G., Tamasco, G., Abichabki, N., Scaranello, A.F.T., Auxiliadora-Martins, M., Pocente, R., Andrade, L.N., Guazzaroni, M.-E., Silva-Rocha, R., and Bollela, V.R. (2022). Nosocomial Out-break of Extensively Drug-Resistant (Polymyxin B and Carbapenem) Klebsiella pneumoniae in a Collapsed University Hospital Due to COVID-19 Pandemic. Antibiotics, 11.","DOI":"10.3390\/antibiotics11060814"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Mendes, G., Ramalho, J.F., Duarte, A., Pedrosa, A., Silva, A.C., M\u00e9ndez, L., and Caneiras, C. (2022). First Outbreak of NDM-1-Producing Klebsiella pneumoniae ST11 in a Portuguese Hospital Centre during the COVID-19 Pandemic. Microorganisms, 10.","DOI":"10.3390\/microorganisms10020251"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"M\u0119drzycka-D\u0105browska, W., Lange, S., Zorena, K., D\u0105browski, S., Ozga, D., and Tomaszek, L. (2021). Carbapenem-Resistant Klebsiella pneumoniae Infections in ICU COVID-19 Patients-A Scoping Review. J. Clin. Med., 10.","DOI":"10.3390\/jcm10102067"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1016\/j.jhin.2021.09.015","article-title":"Evaluation of the Amplex eazyplex Super-Bug Acineto test for direct detection of multi-drug-resistant Acinetobacter baumannii bloodstream infections in high endemicity settings","volume":"117","author":"Comini","year":"2021","journal-title":"J. Hosp. Infect."},{"key":"ref_34","first-page":"e2020008","article-title":"Lymphopenia and neutrophilia at admission predicts severity and mortality in patients with COVID-19: A meta-analysis","volume":"91","author":"Henry","year":"2020","journal-title":"Acta Biomed."},{"key":"ref_35","first-page":"5057","article-title":"Alterations in lymphocyte subsets and monocytes in patients diagnosed with SARS-CoV-2 pneumonia: A mini review of the literature","volume":"25","author":"Lagadinou","year":"2021","journal-title":"Eur. Rev. Med. Pharmacol. Sci."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"200384","DOI":"10.1183\/16000617.0384-2020","article-title":"Current evidence for COVID-19 therapies: A systematic literature review","volume":"30","author":"Welte","year":"2021","journal-title":"Eur. Respir. Rev."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"673","DOI":"10.1177\/0885066621994057","article-title":"A comparison of methylprednisolone and dexamethasone in intensive care patients with COVID-19","volume":"36","author":"Ko","year":"2021","journal-title":"J. Intensive Care Med."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"4564","DOI":"10.1002\/jmv.27000","article-title":"Risk factors for bacterial infections in patients with moderate to severe COVID-19: A case-control study","volume":"93","author":"Nasir","year":"2021","journal-title":"J. Med. Virol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"307","DOI":"10.7883\/yoken.JJID.2020.884","article-title":"Increased Secondary Infection in COVID-19 Patients Treated with Steroids in New York City","volume":"74","author":"Obata","year":"2021","journal-title":"Jpn. J. Infect. Dis."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Pasero, D., Cossu, A.P., and Terragni, P. (2021). Multi-Drug Resistance Bacterial Infections in Critically Ill Patients Admitted with COVID-19. Microorganisms, 9.","DOI":"10.3390\/microorganisms9081773"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"e354","DOI":"10.1016\/S2666-5247(21)00090-2","article-title":"Co-infections, secondary infections, and antimicrobial use in patients hospitalised with COVID-19 during the first pandemic wave from the ISARIC WHO CCP-UK study: A multicentre, prospective cohort study","volume":"2","author":"Russell","year":"2021","journal-title":"Lancet Microbe"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1007\/s10096-023-04577-x","article-title":"Rapid diagnostics and ceftazidime\/avibactam for KPC-producing Klebsiella pneumoniae bloodstream infections: Impact on mortality and role of combination therapy","volume":"42","author":"Boattini","year":"2023","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Bianco, G., Comini, S., Boattini, M., Ricciardelli, G., Guarrasi, L., Cavallo, R., and Costa, C. (2022). MALDI-TOF MS-Based Approaches for Direct Identification of Gram-Negative Bacteria and BlaKPC-Carrying Plasmid Detection from Blood Cultures: A Three-Year Single-Centre Study and Proposal of a Diagnostic Algorithm. Microorganisms, 11.","DOI":"10.3390\/microorganisms11010091"}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/15\/9\/1934\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T20:51:50Z","timestamp":1760129510000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/15\/9\/1934"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,9,15]]},"references-count":43,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2023,9]]}},"alternative-id":["v15091934"],"URL":"https:\/\/doi.org\/10.3390\/v15091934","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,9,15]]}}}