{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,11,2]],"date-time":"2026-11-02T19:30:49Z","timestamp":1793647849639,"version":"4.5.1"},"reference-count":27,"publisher":"Oxford University Press (OUP)","issue":"3","license":[{"start":{"date-parts":[[2022,6,16]],"date-time":"2022-06-16T00:00:00Z","timestamp":1655337600000},"content-version":"vor","delay-in-days":44,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2022,5,3]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:sec>\n                  <jats:title>Objectives<\/jats:title>\n                  <jats:p>To describe clinical characteristics and outcomes of COVID-19 patients who developed secondary infections due to carbapenem-resistant Enterobacterales (CRE).<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Methods<\/jats:title>\n                  <jats:p>Retrospective observational study including COVID-19 patients admitted to 12 Italian hospitals from March to December 2020 who developed a superinfection by CRE. Superinfection was defined as the occurrence of documented bacterial infection &amp;gt;48\u2005h from admission. Patients with polymicrobial infections were excluded. Demographic, clinical characteristics and outcome were collected. Isolates were classified as KPC, metallo-\u03b2-lactamase (MBL) and OXA-48-producing CRE. A Cox regression analysis was performed to identify factors independently associated with 30\u2005day mortality.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Results<\/jats:title>\n                  <jats:p>Overall, 123 patients (median age 66\u2005years, IQR 59\u201375) were included. The majority of infections occurred in the ICU (81, 65.9%), while 42 (34.1%) in medical wards. The most common types of infection were bloodstream infections (BSI) (n\u200a=\u200a64, 52%), followed by urinary-tract infections (UTI) (n\u200a=\u200a28, 22.8%), hospital-acquired\/ventilator-associated pneumonia (HAP\/VAP) (n\u200a=\u200a28, 22.8%), intra-abdominal infections (n\u200a=\u200a2, 1.6%) and skin infections (n\u200a=\u200a1, 0.8%). Sixty-three (51.2%) infections were caused by KPC-, 54 (43.9%) by MBL-, and 6 (4.8%) by OXA-48-producing CRE. Thirty-day mortality was 33.3% (41\/123). On Cox regression analysis, HAP\/VAP compared with UTI (HR 7.23, 95% CI 2.09\u201324.97, P\u200a=\u200a0.004), BSI compared with UTI (HR 3.96, 95% CI, 1.33\u201311.77, P\u200a=\u200a0.004), lymphopenia on admission (HR 3, 95% CI 1.44\u20136.26, P\u200a=\u200a0.003) and age (HR 1.05, 95% CI 1.02\u20131.08, P\u200a=\u200a0.002) were predictors of 30\u2005day mortality.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Conclusions<\/jats:title>\n                  <jats:p>Superinfections by CRE were associated with high risk of 30\u2005day mortality in patients with COVID-19. HAP\/VAP was the strongest predictor of death in these patients.<\/jats:p>\n               <\/jats:sec>","DOI":"10.1093\/jacamr\/dlac064","type":"journal-article","created":{"date-parts":[[2022,6,16]],"date-time":"2022-06-16T05:00:06Z","timestamp":1655355606000},"source":"Crossref","is-referenced-by-count":17,"title":["Superinfections caused by carbapenem-resistant Enterobacterales in hospitalized patients with COVID-19: a multicentre observational study from Italy (CREVID Study)"],"prefix":"10.1093","volume":"4","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3813-8796","authenticated-orcid":false,"given":"Marco","family":"Falcone","sequence":"first","affiliation":[{"name":"Infectious Diseases Unit, Department of Clinical and Experimental Medicine, Azienda Ospedaliera Universitaria Pisana, University of Pisa , Pisa , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lorenzo Roberto","family":"Suardi","sequence":"additional","affiliation":[{"name":"Infectious Diseases Unit, Department of Clinical and Experimental Medicine, Azienda Ospedaliera Universitaria Pisana, University of Pisa , Pisa , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3884-4933","authenticated-orcid":false,"given":"Giusy","family":"Tiseo","sequence":"additional","affiliation":[{"name":"Infectious Diseases Unit, Department of Clinical and Experimental Medicine, Azienda Ospedaliera Universitaria Pisana, University of Pisa , Pisa , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Valentina","family":"Galfo","sequence":"additional","affiliation":[{"name":"Infectious Diseases Unit, Department of Clinical and Experimental Medicine, Azienda Ospedaliera Universitaria Pisana, University of Pisa , Pisa , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sara","family":"Occhineri","sequence":"additional","affiliation":[{"name":"Infectious Diseases Unit, Department of Clinical and Experimental Medicine, Azienda Ospedaliera Universitaria Pisana, University of Pisa , Pisa , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4287-7690","authenticated-orcid":false,"given":"Stefano","family":"Verdenelli","sequence":"additional","affiliation":[{"name":"Infectious Diseases Unit, Department of Clinical and Experimental Medicine, Azienda Ospedaliera Universitaria Pisana, University of Pisa , Pisa , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5921-3180","authenticated-orcid":false,"given":"Giancarlo","family":"Ceccarelli","sequence":"additional","affiliation":[{"name":"Department of Public Health and Infectious Diseases, Sapienza University of Rome , Rome , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Melita","family":"Poli","sequence":"additional","affiliation":[{"name":"Vittorio Emanuele II Hospital , Bisceglie , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5081-8669","authenticated-orcid":false,"given":"Marco","family":"Merli","sequence":"additional","affiliation":[{"name":"Divisione di Malattie Infettive, ASST Grande Ospedale Metropolitano Niguarda , Milan , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Davide","family":"Bavaro","sequence":"additional","affiliation":[{"name":"University of Bari, Clinic of Infectious Diseases , Bari , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anna","family":"Carretta","sequence":"additional","affiliation":[{"name":"Department of Infectious Diseases, University Hospital \u2018Ospedali Riuniti\u2019 of Foggia , Foggia , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Giuseppe","family":"Nunnari","sequence":"additional","affiliation":[{"name":"Unit of Infectious Diseases, Department of Clinical and Experimental Medicine, University of Messina , Messina , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emmanuele","family":"Venanzi Rullo","sequence":"additional","affiliation":[{"name":"Unit of Infectious Diseases, Department of Clinical and Experimental Medicine, University of Messina , Messina , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Enrico Maria","family":"Trecarichi","sequence":"additional","affiliation":[{"name":"Unit of Infectious and Tropical Diseases, Department of Medical and Surgical Sciences, \u2018Magna Graecia\u2019 University of Catanzaro-\u2018Mater Domini\u2019 Teaching Hospital , Catanzaro , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chiara","family":"Papalini","sequence":"additional","affiliation":[{"name":"Department of Medicine and Surgery, Clinic of Infectious Diseases, \u2018Santa Maria della Misericordia\u2019 Hospital, University of Perugia , Perugia , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Antonina","family":"Franco","sequence":"additional","affiliation":[{"name":"UOC Malattie Infettive, PO Umberto I , Siracusa , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rosa Fontana","family":"Del Vecchio","sequence":"additional","affiliation":[{"name":"UOC Malattie Infettive, PO Umberto I , Siracusa , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vincenzo","family":"Bianco","sequence":"additional","affiliation":[{"name":"Department of Infectious diseases, AORN Ospedali dei Colli, Cotugno Hospital , Naples , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rodolfo","family":"Punzi","sequence":"additional","affiliation":[{"name":"Department of Infectious diseases, AORN Ospedali dei Colli, Cotugno Hospital , Naples , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniela","family":"Francisci","sequence":"additional","affiliation":[{"name":"Department of Medicine and Surgery, Clinic of Infectious Diseases, \u2018Santa Maria della Misericordia\u2019 Hospital, University of Perugia , Perugia , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Raffaella","family":"Rubino","sequence":"additional","affiliation":[{"name":"Department of Health Promotion, Mother and Child Care, Internal Medicine and Medical Specialties, University of Palermo , Palermo , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carlo","family":"Torti","sequence":"additional","affiliation":[{"name":"Unit of Infectious and Tropical Diseases, Department of Medical and Surgical Sciences, \u2018Magna Graecia\u2019 University of Catanzaro-\u2018Mater Domini\u2019 Teaching Hospital , Catanzaro , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Massimo","family":"Puoti","sequence":"additional","affiliation":[{"name":"Divisione di Malattie Infettive, ASST Grande Ospedale Metropolitano Niguarda , Milan , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sergio","family":"Carbonara","sequence":"additional","affiliation":[{"name":"Vittorio Emanuele II Hospital , Bisceglie , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Antonio","family":"Cascio","sequence":"additional","affiliation":[{"name":"Department of Health Promotion, Mother and Child Care, Internal Medicine and Medical Specialties, University of Palermo , Palermo , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Annalisa","family":"Saracino","sequence":"additional","affiliation":[{"name":"University of Bari, Clinic of Infectious Diseases , Bari , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Teresa","family":"Santantonio","sequence":"additional","affiliation":[{"name":"Department of Infectious Diseases, University Hospital \u2018Ospedali Riuniti\u2019 of Foggia , Foggia , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mario","family":"Venditti","sequence":"additional","affiliation":[{"name":"Department of Public Health and Infectious Diseases, Sapienza University of Rome , Rome , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Francesco","family":"Menichetti","sequence":"additional","affiliation":[{"name":"Infectious Diseases Unit, Department of Clinical and Experimental Medicine, Azienda Ospedaliera Universitaria Pisana, University of Pisa , Pisa , Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2022,6,16]]},"reference":[{"key":"2022072609054028600_dlac064-B1","article-title":"WHO Coronavirus (COVID-19) Dashboard","author":"WHO"},{"key":"2022072609054028600_dlac064-B2","doi-asserted-by":"crossref","first-page":"2345","DOI":"10.2337\/dc20-1380","article-title":"Hyperglycemia at hospital admission is associated with severity of the prognosis in patients hospitalized for COVID-19: The Pisa COVID-19 Study","volume":"43","author":"Coppelli","year":"2020","journal-title":"Diabetes Care"},{"key":"2022072609054028600_dlac064-B3","doi-asserted-by":"crossref","DOI":"10.1093\/ofid\/ofaa563","article-title":"Role of low-molecular-weight heparin in hospitalized patients with severe acute respiratory syndrome coronavirus 2 pneumonia: a prospective observational study","volume":"7","author":"Falcone","year":"2020","journal-title":"Open Forum Infect Dis"},{"key":"2022072609054028600_dlac064-B4","doi-asserted-by":"crossref","first-page":"e0047321","DOI":"10.1128\/mBio.00473-21","article-title":"Tackling Antimicrobial Resistance in the Shadow of COVID-19","volume":"12","author":"Patel","year":"2021","journal-title":"mBio"},{"key":"2022072609054028600_dlac064-B5","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":"2022072609054028600_dlac064-B6","doi-asserted-by":"crossref","first-page":"1234","DOI":"10.3201\/eid2704.204036","article-title":"Rapid spread and control of multidrug-resistant Gram-negative bacteria in COVID-19 patient care units","volume":"27","author":"Patel","year":"2021","journal-title":"Emerg Infect Dis"},{"key":"2022072609054028600_dlac064-B7","doi-asserted-by":"crossref","first-page":"1140","DOI":"10.1093\/jac\/dkab495","article-title":"Spread of hypervirulent multidrug-resistant ST147 Klebsiella pneumoniae in patients with severe COVID-19: an observational study from Italy, 2020\u201321","volume":"77","author":"Falcone","year":"2022","journal-title":"J Antimicrob Chemother"},{"key":"2022072609054028600_dlac064-B8","doi-asserted-by":"crossref","first-page":"2021","DOI":"10.1093\/cid\/ciaa1410","article-title":"Cefiderocol as rescue therapy for Acinetobacter baumannii and other carbapenem-resistant gram-negative infections in intensive care unit patients","volume":"72","author":"Falcone","year":"2021","journal-title":"Clin Infect Dis"},{"key":"2022072609054028600_dlac064-B9","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1016\/S0140-6736(21)02724-0","article-title":"Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis","volume":"399","author":"Antimicrobial Resistance Collaborators","year":"2022","journal-title":"Lancet"},{"key":"2022072609054028600_dlac064-B10","article-title":"Carbapenem-resistant Enterobacteriaceae \u2013 second update","author":"Rapid risk assessment"},{"key":"2022072609054028600_dlac064-B11","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1080\/23744235.2021.1963471","article-title":"Carbapenemase-producing Enterobacterales infections in COVID-19 patients","volume":"54","author":"Pintado","year":"2022","journal-title":"Infect Dis (Lond)"},{"key":"2022072609054028600_dlac064-B12","doi-asserted-by":"crossref","first-page":"380","DOI":"10.1093\/jac\/dkaa466","article-title":"Carbapenemase-producing Enterobacterales causing secondary infections during the COVID-19 crisis at a New York City hospital","volume":"76","author":"Gomez-Simmonds","year":"2021","journal-title":"J Antimicrob Chemother"},{"key":"2022072609054028600_dlac064-B13","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1007\/s10096-020-04142-w","article-title":"Nosocomial infections associated to COVID-19 in the intensive care unit: clinical characteristics and outcome","volume":"40","author":"Bardi","year":"2021","journal-title":"Eur J Clin Microbiol Infect Dis"},{"key":"2022072609054028600_dlac064-B14","article-title":"CDC\/NHSN Surveillance Definitions for Specific Types of Infections","author":"CDC"},{"key":"2022072609054028600_dlac064-B15","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1016\/j.cmi.2020.12.011","article-title":"Therapeutic strategies for severe COVID-19: a position paper from the Italian Society of Infectious and Tropical Diseases (SIMIT)","volume":"27","author":"Mussini","year":"2021","journal-title":"Clin Microbiol Infect"},{"key":"2022072609054028600_dlac064-B16","doi-asserted-by":"crossref","first-page":"801","DOI":"10.1001\/jama.2016.0287","article-title":"The Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3)","volume":"315","author":"Singer","year":"2016","journal-title":"JAMA"},{"key":"2022072609054028600_dlac064-B17","doi-asserted-by":"crossref","first-page":"1826","DOI":"10.1093\/cid\/ciz528","article-title":"The Pitt bacteremia score predicts mortality in nonbacteremic infections","volume":"70","author":"Henderson","year":"2020","journal-title":"Clin Infect Dis"},{"key":"2022072609054028600_dlac064-B18","doi-asserted-by":"crossref","first-page":"707","DOI":"10.1007\/BF01709751","article-title":"The SOFA (Sepsis-related organ failure assessment) score to describe organ dysfunction\/failure","volume":"22","author":"Vincent","year":"1996","journal-title":"Intensive Care Med"},{"key":"2022072609054028600_dlac064-B19","doi-asserted-by":"crossref","first-page":"298.e1","DOI":"10.1016\/j.cmi.2021.06.031","article-title":"Bloodstream infections in patients with rectal colonization by Klebsiella pneumoniae producing different type of carbapenemases: a prospective, cohort study (CHIMERA study)","volume":"28","author":"Falcone","year":"2021","journal-title":"Clin Microbiol Infect"},{"key":"2022072609054028600_dlac064-B20","doi-asserted-by":"crossref","DOI":"10.1093\/ofid\/ofab065","article-title":"bacterial superinfections among persons with Coronavirus Disease 2019: a comprehensive review of data from postmortem studies","volume":"8","author":"Clancy","year":"2021","journal-title":"Open Forum Infect Dis"},{"key":"2022072609054028600_dlac064-B21","doi-asserted-by":"crossref","first-page":"100229","DOI":"10.1016\/j.xcrm.2021.100229","article-title":"Bacterial pulmonary superinfections are associated with longer duration of ventilation in critically ill COVID-19 patients","volume":"2","author":"Buehler","year":"2021","journal-title":"Cell Rep Med"},{"key":"2022072609054028600_dlac064-B22","doi-asserted-by":"crossref","first-page":"72","DOI":"10.1186\/s13054-021-03493-w","article-title":"Epidemiology and microbiology of ventilator-associated pneumonia in COVID-19 patients: a multicenter retrospective study in 188 patients in an un-inundated French region","volume":"25","author":"Blonz","year":"2021","journal-title":"Crit Care"},{"key":"2022072609054028600_dlac064-B23","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1186\/s13054-020-03013-2","article-title":"The challenge of ventilator-associated pneumonia diagnosis in COVID-19 patients","volume":"24","author":"Fran\u00e7ois","year":"2020","journal-title":"Crit Care"},{"key":"2022072609054028600_dlac064-B24","doi-asserted-by":"crossref","first-page":"555","DOI":"10.3390\/jcm10040555","article-title":"Incidence and prognosis of ventilator-associated pneumonia in critically ill patients with COVID-19: a multicenter study","volume":"10","author":"Giacobbe","year":"2021","journal-title":"J Clin Med"},{"key":"2022072609054028600_dlac064-B25","doi-asserted-by":"crossref","first-page":"2001886","DOI":"10.2807\/1560-7917.ES.2020.25.45.2001886","article-title":"Will coronavirus disease (COVID-19) have an impact on antimicrobial resistance?","volume":"25","author":"Monnet","year":"2020","journal-title":"Euro Surveill"},{"key":"2022072609054028600_dlac064-B26","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1186\/s13054-020-2742-9","article-title":"Time to appropriate antibiotic therapy is a predictor of outcome in patients with bloodstream infection caused by KPC-producing Klebsiella pneumoniae","volume":"24","author":"Falcone","year":"2020","journal-title":"Crit Care"},{"key":"2022072609054028600_dlac064-B27","doi-asserted-by":"crossref","first-page":"2479","DOI":"10.1007\/s40121-021-00525-4","article-title":"Efficacy of bamlanivimab\/etesevimab and casirivimab\/imdevimab in preventing progression to severe COVID-19 and role of variants of concern","volume":"10","author":"Falcone","year":"2021","journal-title":"Infect Dis Ther"}],"container-title":["JAC-Antimicrobial Resistance"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/jacamr\/article-pdf\/4\/3\/dlac064\/45065010\/dlac064.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jacamr\/article-pdf\/4\/3\/dlac064\/45065010\/dlac064.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,7,26]],"date-time":"2022-07-26T09:06:16Z","timestamp":1658826376000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jacamr\/article\/doi\/10.1093\/jacamr\/dlac064\/6608987"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,5,3]]},"references-count":27,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2022,5,3]]}},"URL":"https:\/\/doi.org\/10.1093\/jacamr\/dlac064","relation":{},"ISSN":["2632-1823"],"issn-type":[{"value":"2632-1823","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2022,6,1]]},"published":{"date-parts":[[2022,5,3]]},"article-number":"dlac064"}}