{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T02:52:26Z","timestamp":1791341546478,"version":"4.3.1"},"reference-count":34,"publisher":"Oxford University Press (OUP)","license":[{"start":{"date-parts":[[2026,9,28]],"date-time":"2026-09-28T00:00:00Z","timestamp":1790553600000},"content-version":"am","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/pages\/standard-publication-reuse-rights"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Background<\/jats:title>\n                    <jats:p>Kluyvera spp are increasingly recognized as significant pathogens in humans. Recent reports of carbapenemase-producing (CP) Kluyvera spp raise a concern that they may be disseminating carbapenemases to other species undetected. Research on CP-Kluyvera spp is scarce, and little is known about their characteristics.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>We aimed to investigate the epidemiology of CP-Kluyvera spp in Israel, characterize their antimicrobial resistance, and examine mechanisms of transmission of carbapenemase genes. We performed a retrospective epidemiological analysis of all cases of CP-Kluyvera spp reported to Israel's national surveillance system of carbapenem-resistant Enterobacterales from 2008 to 2023. Hospital-acquired cases were categorized as sporadic or part of an outbreak. Microbiological characterization of 22 available isolates included antimicrobial susceptibility testing and whole-genome sequencing.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>There were 146 cases of CP-Kluyvera spp in 2008\u20132023: 145 were detected in rectal screening samples, and 1 in a blood culture. The dominant reported species was Kluyvera ascorbata (60.3%), followed by Kluyvera cryocrescens (24%). The common carbapenemases were Klebsiella pneumoniae carbapenemase (67.1%) and New Delhi metallo-\u03b2-lactamase (26.7%); 41.1% of hospital-acquired cases were classified as part of an outbreak. All characterized isolates were multidrug resistant and produced at least 1 carbapenemase. Spread of carbapenemase genes in Kluyvera spp was plasmid-driven by IncC and by Rep-A\u2013type plasmids.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusions<\/jats:title>\n                    <jats:p>Cases of CP-Kluyvera spp increased annually. Spread of CP-Kluyvera was partially clonal, with both outbreaks and sporadic cases detected. We illustrated that Kluyvera spp produce a variety of plasmid-borne antimicrobial resistance genes, including those coding for carbapenemases, which could be horizontally transferred to additional bacterial species, revealing the increasing clinical significance of Kluyvera genus.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1093\/infdis\/jiag468","type":"journal-article","created":{"date-parts":[[2026,9,28]],"date-time":"2026-09-28T11:24:54Z","timestamp":1790594694000},"source":"Crossref","is-referenced-by-count":0,"title":["Carbapenemase-Producing\n                    <i>Kluyvera<\/i>\n                    Species: Epidemiology of an Evolving Species"],"prefix":"10.1093","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5403-4933","authenticated-orcid":false,"given":"Gabrielle D","family":"Levi","sequence":"first","affiliation":[{"name":"Ministry of Health, National Institute of Antibiotic Resistance and Infection Control , Tel Aviv ,","place":["Israel"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mor N","family":"Lurie-Weinberger","sequence":"additional","affiliation":[{"name":"Ministry of Health, National Institute of Antibiotic Resistance and Infection Control , Tel Aviv ,","place":["Israel"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David","family":"Schwartz","sequence":"additional","affiliation":[{"name":"Ministry of Health, National Institute of Antibiotic Resistance and Infection Control , Tel Aviv ,","place":["Israel"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4016-8628","authenticated-orcid":false,"given":"Meirav","family":"Mor","sequence":"additional","affiliation":[{"name":"Infection Control Unit, Schneider Children's Medical Center , Petach Tikva ,","place":["Israel"]},{"name":"Faculty of Medical and Health Sciences, Tel Aviv University , Tel Aviv ,","place":["Israel"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0006-5813-9701","authenticated-orcid":false,"given":"Shmuel","family":"Benenson","sequence":"additional","affiliation":[{"name":"Infection Prevention and Control Unit, Shaare Zedek Medical Center , Jerusalem ,","place":["Israel"]},{"name":"Faculty of Medicine, Hebrew University , Jerusalem ,","place":["Israel"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marc V","family":"Assous","sequence":"additional","affiliation":[{"name":"Infection Prevention and Control Unit, Shaare Zedek Medical Center , Jerusalem ,","place":["Israel"]},{"name":"Faculty of Medicine, Hebrew University , Jerusalem ,","place":["Israel"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Haim","family":"Ben-Zvi","sequence":"additional","affiliation":[{"name":"Faculty of Medical and Health Sciences, Tel Aviv University , Tel Aviv ,","place":["Israel"]},{"name":"Clinical Microbiology, Rabin Medical Center, Beilinson Hospital , Petach Tikva ,","place":["Israel"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Antoine","family":"Andremont","sequence":"additional","affiliation":[{"name":"Ministry of Health, National Institute of Antibiotic Resistance and Infection Control , Tel Aviv ,","place":["Israel"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0679-3967","authenticated-orcid":false,"given":"Alona","family":"Keren-Paz","sequence":"additional","affiliation":[{"name":"Ministry of Health, National Institute of Antibiotic Resistance and Infection Control , Tel Aviv ,","place":["Israel"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yehuda","family":"Carmeli","sequence":"additional","affiliation":[{"name":"Ministry of Health, National Institute of Antibiotic Resistance and Infection Control , Tel Aviv ,","place":["Israel"]},{"name":"Faculty of Medical and Health Sciences, Tel Aviv University , Tel Aviv ,","place":["Israel"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2026,9,28]]},"reference":[{"key":"2026100622213588000_jiag468-B1","doi-asserted-by":"crossref","first-page":"E69","DOI":"10.1086\/322686","article-title":"Infections caused by Kluyvera species in humans","volume":"33","author":"Sarria","year":"2001","journal-title":"Clin Infect Dis"},{"key":"2026100622213588000_jiag468-B2","doi-asserted-by":"crossref","first-page":"7498","DOI":"10.1128\/AAC.01165-16","article-title":"Kluyvera ascorbata strain from hospital sewage carrying the mcr-1 colistin resistance gene","volume":"60","author":"Zhao","year":"2016","journal-title":"Antimicrob Agents Chemother"},{"key":"2026100622213588000_jiag468-B3","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1309\/61XP4KTLJYWM5H35","article-title":"Clinically significant Kluyvera infections: a report of seven cases","volume":"123","author":"Carter","year":"2005","journal-title":"Am J Clin Pathol"},{"key":"2026100622213588000_jiag468-B4","doi-asserted-by":"crossref","first-page":"e01765","DOI":"10.1016\/j.idcr.2023.e01765","article-title":"Kluyvera intermedia bacteremia with septic shock: a case report","volume":"32","author":"Inoue","year":"2023","journal-title":"IDCases"},{"key":"2026100622213588000_jiag468-B5","doi-asserted-by":"crossref","first-page":"839","DOI":"10.1097\/INF.0b013e318170af5b","article-title":"Kluyvera infections in the pediatric population","volume":"27","author":"Carter","year":"2008","journal-title":"Pediatr Infect Dis J"},{"key":"2026100622213588000_jiag468-B6","doi-asserted-by":"crossref","first-page":"3595","DOI":"10.1128\/AAC.45.12.3595-3598.2001","article-title":"Characterization of a chromosomally encoded extended-spectrum class A \u03b2-lactamase from Kluyvera cryocrescens","volume":"45","author":"Decousser","year":"2001","journal-title":"Antimicrob Agents Chemother"},{"key":"2026100622213588000_jiag468-B7","doi-asserted-by":"crossref","first-page":"3045","DOI":"10.1128\/AAC.46.9.3045-3049.2002","article-title":"\u03b2-lactamases of Kluyvera ascorbata, probable progenitors of some plasmid-encoded CTX-M types","volume":"46","author":"Humeniuk","year":"2002","journal-title":"Antimicrob Agents Chemother"},{"issue":"Suppl 1","key":"2026100622213588000_jiag468-B8","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1111\/j.1469-0691.2007.01867.x","article-title":"The spread of CTX-M-type extended-spectrum \u03b2-lactamases","volume":"14","author":"Rossolini","year":"2008","journal-title":"Clin Microbiol Infect"},{"key":"2026100622213588000_jiag468-B9","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1016\/j.jgar.2023.07.008","article-title":"Emergence of NDM-1 and KPC-3 carbapenemases in Kluyvera cryocrescens: investigating genetic heterogeneity and acquisition routes of blaNDM-1 in Enterobacterales species in Portugal","volume":"34","author":"Loiodice","year":"2023","journal-title":"J Glob Antimicrob Resist"},{"key":"2026100622213588000_jiag468-B10","doi-asserted-by":"crossref","first-page":"719","DOI":"10.1093\/jac\/dks443","article-title":"Detection of the plasmid-mediated KPC-2 carbapenem-hydrolysing enzyme in three unusual species of the Enterobacteriaceae family in Israel","volume":"68","author":"Geffen","year":"2013","journal-title":"J Antimicrob Chemother"},{"key":"2026100622213588000_jiag468-B11","doi-asserted-by":"crossref","first-page":"e01238-18","DOI":"10.1128\/AAC.01238-18","article-title":"First report of an OXA-48- and CTX-M-213-producing Kluyvera species clone recovered from patients admitted in a university hospital in Madrid, Spain","volume":"62","author":"Hern\u00e1ndez-Garc\u00eda","year":"2018","journal-title":"Antimicrob Agents Chemother"},{"key":"2026100622213588000_jiag468-B12","first-page":"5745708","article-title":"A case of biliary tract infection caused by KPC-2-producing Kluyvera ascorbata","volume":"2018","author":"Wang","year":"2018","journal-title":"Case Rep Infect Dis"},{"key":"2026100622213588000_jiag468-B13","doi-asserted-by":"crossref","first-page":"2776","DOI":"10.1093\/jac\/dks294","article-title":"Detection of bla KPC-2 in a carbapenem-resistant Kluyvera georgiana","volume":"67","author":"Ribeiro","year":"2012","journal-title":"J Antimicrob Chemother"},{"key":"2026100622213588000_jiag468-B14","doi-asserted-by":"crossref","first-page":"149","DOI":"10.3390\/antibiotics8030149","article-title":"Characterization of a carbapenem-resistant Kluyvera cryocrescens isolate carrying Blandm-1 from hospital sewage","volume":"8","author":"Li","year":"2019","journal-title":"Antibiotics"},{"key":"2026100622213588000_jiag468-B15","doi-asserted-by":"crossref","first-page":"2096","DOI":"10.1128\/JCM.41.5.2096-2101.2003","article-title":"Evaluation of the Vitek 2 ID-GNB assay for identification of members of the family Enterobacteriaceae and other nonenteric gram-negative bacilli and comparison with the Vitek GNI+ card","volume":"41","author":"O\u2019Hara","year":"2003","journal-title":"J Clin Microbiol"},{"key":"2026100622213588000_jiag468-B16","doi-asserted-by":"crossref","first-page":"e0054224","DOI":"10.1128\/spectrum.00542-24","article-title":"Misidentification and misreporting of antibiotic resistance in Kluyvera bacteremia by blood culture molecular identification panels","volume":"12","author":"Vatterrodt","year":"2024","journal-title":"Microbiol Spectr"},{"key":"2026100622213588000_jiag468-B17","doi-asserted-by":"crossref","first-page":"e310","DOI":"10.1016\/S2666-5247(23)00390-7","article-title":"Emerging threats: global distribution and diversity of carbapenem resistance genes in Kluyvera intermedia","volume":"5","author":"Monte","year":"2024","journal-title":"Lancet Microbe"},{"key":"2026100622213588000_jiag468-B18","doi-asserted-by":"crossref","first-page":"697","DOI":"10.1093\/cid\/cit795","article-title":"An ongoing national intervention to contain the spread of carbapenem-resistant Enterobacteriaceae","volume":"58","author":"Schwaber","year":"2014","journal-title":"Clin Infect Dis"},{"key":"2026100622213588000_jiag468-B19","doi-asserted-by":"crossref","first-page":"848","DOI":"10.1093\/cid\/cir025","article-title":"Containment of a country-wide outbreak of carbapenem-resistant Klebsiella pneumoniae in Israeli hospitals via a nationally implemented intervention","volume":"52","author":"Schwaber","year":"2011","journal-title":"Clin Infect Dis"},{"key":"2026100622213588000_jiag468-B20","volume-title":"Managing multidrug-resistant pathogens of special epidemiological importance at medical institutions. Circular no: 15\/2022","author":"Israel Ministry of Health","year":"2022"},{"key":"2026100622213588000_jiag468-B21","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1093\/molbev\/msy242","article-title":"Beyond the SNP threshold: identifying outbreak clusters using inferred transmissions","volume":"36","author":"Stimson","year":"2019","journal-title":"Mol Biol Evol"},{"key":"2026100622213588000_jiag468-B22","doi-asserted-by":"crossref","first-page":"e349","DOI":"10.1016\/S2666-5247(22)00380-9","article-title":"Defining genomic epidemiology thresholds for common-source bacterial outbreaks: a modelling study","volume":"4","author":"Duval","year":"2023","journal-title":"Lancet Microbe"},{"key":"2026100622213588000_jiag468-B23","volume-title":"Performance standards for antimicrobial susceptibility testing","author":"Clinical and Laboratory Standard Institute","year":"2024","edition":". 34th ed"},{"key":"2026100622213588000_jiag468-B24","volume-title":"Breakpoint Committee consultation on colistin, 2021. Colistin breakpoints: guidance document","author":"European Committee on Antimicrobial Susceptibility Testing","year":"2021"},{"key":"2026100622213588000_jiag468-B25","volume-title":"CLSI Standard M07: methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically","author":"Clinical and Laboratory Standards Institute","year":"2024","edition":"12th ed"},{"key":"2026100622213588000_jiag468-B26","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1093\/cid\/ciae110","article-title":"The natural history of carbapenemase-producing Enterobacterales: progression from carriage of various carbapenemases to bloodstream infection","volume":"79","author":"Temkin","year":"2024","journal-title":"Clin Infect Dis"},{"key":"2026100622213588000_jiag468-B27","doi-asserted-by":"crossref","first-page":"1357","DOI":"10.1111\/1469-0691.12747","article-title":"Risk factors for carbapenem-resistant Klebsiella pneumoniae bloodstream infection among rectal carriers: a prospective observational multicentre study","volume":"20","author":"Giannella","year":"2014","journal-title":"Clin Microbiol Infect"},{"key":"2026100622213588000_jiag468-B28","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":"Murray","year":"2022","journal-title":"Lancet"},{"key":"2026100622213588000_jiag468-B29","doi-asserted-by":"crossref","first-page":"785","DOI":"10.1016\/S1473-3099(13)70190-7","article-title":"Clinical epidemiology of the global expansion of Klebsiella pneumoniae carbapenemases","volume":"13","author":"Munoz-Price","year":"2013","journal-title":"Lancet Infect Dis"},{"key":"2026100622213588000_jiag468-B30","doi-asserted-by":"crossref","first-page":"e0004","DOI":"10.5041\/RMMJ.10461","article-title":"The changing epidemiology of carbapenemase-producing Enterobacterales","volume":"13","author":"Hussein","year":"2022","journal-title":"Rambam Maimonides Med J"},{"key":"2026100622213588000_jiag468-B31","doi-asserted-by":"crossref","first-page":"1209","DOI":"10.3201\/eid1208.060291","article-title":"Carbapenem resistance in Klebsiella pneumoniae not detected by automated susceptibility testing","volume":"12","author":"Tenover","year":"2006","journal-title":"Emerg Infect Dis"},{"key":"2026100622213588000_jiag468-B32","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1186\/s13099-021-00458-w","article-title":"Comparative genomic characterization of multidrug-resistant Citrobacter spp. strains in fennec fox imported to China","volume":"13","author":"Qin","year":"2021","journal-title":"Gut Pathog"},{"key":"2026100622213588000_jiag468-B33","doi-asserted-by":"crossref","first-page":"9332","DOI":"10.1038\/s41598-020-66239-8","article-title":"Host dependent maintenance of a bla NDM-1-encoding plasmid in clinical Escherichia coli isolates","volume":"10","author":"Gama","year":"2020","journal-title":"Sci Rep"},{"key":"2026100622213588000_jiag468-B34","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1016\/j.plasmid.2017.10.001","article-title":"Evolution in situ of ARI-A in pB2-1, a type 1 IncC plasmid recovered from Klebsiella pneumoniae, and stability of Tn4352B","volume":"94","author":"Harmer","year":"2017","journal-title":"Plasmid"}],"container-title":["The Journal of Infectious Diseases"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/jid\/advance-article-pdf\/doi\/10.1093\/infdis\/jiag468\/71445490\/jiag468.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jid\/advance-article-pdf\/doi\/10.1093\/infdis\/jiag468\/71445490\/jiag468.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T02:21:45Z","timestamp":1791339705000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jid\/advance-article\/doi\/10.1093\/infdis\/jiag468\/8842567"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9,28]]},"references-count":34,"URL":"https:\/\/doi.org\/10.1093\/infdis\/jiag468","relation":{},"ISSN":["0022-1899","1537-6613"],"issn-type":[{"value":"0022-1899","type":"print"},{"value":"1537-6613","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9,28]]},"article-number":"jiag468"}}