Sentinel Surveillance reveals phylogenetic diversity and detection of linear plasmids harboring vanA and optrA among enterococci collected in the United States.
Alyssa G Kent, Lori M Spicer, Davina Campbell, Erin Breaker, Gillian A McAllister, Thomas O Ewing, Cynthia Longo, Rocio Balbuena, Mark Burroughs, Alex Burgin, Jasmine Padilla, J Kristie Johnson, Alison Laufer Halpin, Susannah L McKay, J Kamile Rasheed, Christopher A Elkins, Maria Karlsson, Joseph D Lutgring, Amy S Gargis
{"title":"Sentinel Surveillance reveals phylogenetic diversity and detection of linear plasmids harboring <i>vanA</i> and <i>optrA</i> among enterococci collected in the United States.","authors":"Alyssa G Kent, Lori M Spicer, Davina Campbell, Erin Breaker, Gillian A McAllister, Thomas O Ewing, Cynthia Longo, Rocio Balbuena, Mark Burroughs, Alex Burgin, Jasmine Padilla, J Kristie Johnson, Alison Laufer Halpin, Susannah L McKay, J Kamile Rasheed, Christopher A Elkins, Maria Karlsson, Joseph D Lutgring, Amy S Gargis","doi":"10.1128/aac.00591-24","DOIUrl":null,"url":null,"abstract":"<p><p><i>Enterococcus faecalis</i> and <i>Enterococcus faecium</i> are frequent causes of healthcare-associated infections. Antimicrobial-resistant enterococci pose a serious public health threat, particularly vancomycin-resistant enterococci (VRE), for which treatment options are limited. The Centers for Disease Control and Prevention's Division of Healthcare Quality Promotion Sentinel Surveillance system conducted surveillance from 2018 to 2019 to evaluate antimicrobial susceptibility profiles and molecular epidemiology of 205 <i>E. faecalis</i> and 180 <i>E. faecium</i> clinical isolates collected from nine geographically diverse sites in the United States. Whole genome sequencing revealed diverse genetic lineages, with no single sequence type accounting for more than 15% of <i>E. faecalis</i> or <i>E. faecium</i>. Phylogenetic analysis distinguished <i>E. faecium</i> from 19 <i>E. lactis</i> (previously known as <i>E. faecium</i> clade B). Resistance to vancomycin was 78.3% among <i>E. faecium</i>, 7.8% among <i>E. faecalis</i>, and did not occur among <i>E. lactis</i> isolates. Resistance to daptomycin and linezolid was rare: <i>E. faecium</i> (5.6%, 0.6%, respectively), <i>E. faecalis</i> (2%, 2%), and <i>E. lactis</i> (5.3%, 0%). All VRE harbored the <i>vanA</i> gene. Three of the seven isolates that were not susceptible to linezolid harbored <i>optrA</i>, one chromosomally located and two on linear plasmids that shared a conserved backbone with other multidrug-resistant conjugative linear plasmids. One of these isolates contained <i>optrA</i> and <i>vanA</i> co-localized on the linear plasmid. By screening all enterococci, 20% of <i>E. faecium</i> were predicted to harbor linear plasmids, whereas none were predicted among <i>E. faecalis</i> or <i>E. lactis</i>. Continued surveillance is needed to assess the future emergence and spread of antimicrobial resistance by linear plasmids and other mechanisms.IMPORTANCEThis work confirms prior reports of <i>E. faecium</i> showing higher levels of resistance to more antibiotics than <i>E. faecalis</i> and identifies that diverse sequence types are contributing to enterococcal infections in the United States. All VRE harbored the <i>vanA</i> gene. We present the first report of the linezolid resistance gene <i>optrA</i> on linear plasmids in the United States, one of which co-carried a <i>vanA</i> cassette. Additional studies integrating epidemiological, antimicrobial susceptibility, and genomic methods to characterize mechanisms of resistance, including the role of linear plasmids, will be critical to understanding the changing landscape of enterococci in the United States.</p>","PeriodicalId":8152,"journal":{"name":"Antimicrobial Agents and Chemotherapy","volume":" ","pages":"e0059124"},"PeriodicalIF":4.1000,"publicationDate":"2024-11-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11539240/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Antimicrobial Agents and Chemotherapy","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1128/aac.00591-24","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/10/15 0:00:00","PubModel":"Epub","JCR":"Q2","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Enterococcus faecalis and Enterococcus faecium are frequent causes of healthcare-associated infections. Antimicrobial-resistant enterococci pose a serious public health threat, particularly vancomycin-resistant enterococci (VRE), for which treatment options are limited. The Centers for Disease Control and Prevention's Division of Healthcare Quality Promotion Sentinel Surveillance system conducted surveillance from 2018 to 2019 to evaluate antimicrobial susceptibility profiles and molecular epidemiology of 205 E. faecalis and 180 E. faecium clinical isolates collected from nine geographically diverse sites in the United States. Whole genome sequencing revealed diverse genetic lineages, with no single sequence type accounting for more than 15% of E. faecalis or E. faecium. Phylogenetic analysis distinguished E. faecium from 19 E. lactis (previously known as E. faecium clade B). Resistance to vancomycin was 78.3% among E. faecium, 7.8% among E. faecalis, and did not occur among E. lactis isolates. Resistance to daptomycin and linezolid was rare: E. faecium (5.6%, 0.6%, respectively), E. faecalis (2%, 2%), and E. lactis (5.3%, 0%). All VRE harbored the vanA gene. Three of the seven isolates that were not susceptible to linezolid harbored optrA, one chromosomally located and two on linear plasmids that shared a conserved backbone with other multidrug-resistant conjugative linear plasmids. One of these isolates contained optrA and vanA co-localized on the linear plasmid. By screening all enterococci, 20% of E. faecium were predicted to harbor linear plasmids, whereas none were predicted among E. faecalis or E. lactis. Continued surveillance is needed to assess the future emergence and spread of antimicrobial resistance by linear plasmids and other mechanisms.IMPORTANCEThis work confirms prior reports of E. faecium showing higher levels of resistance to more antibiotics than E. faecalis and identifies that diverse sequence types are contributing to enterococcal infections in the United States. All VRE harbored the vanA gene. We present the first report of the linezolid resistance gene optrA on linear plasmids in the United States, one of which co-carried a vanA cassette. Additional studies integrating epidemiological, antimicrobial susceptibility, and genomic methods to characterize mechanisms of resistance, including the role of linear plasmids, will be critical to understanding the changing landscape of enterococci in the United States.
期刊介绍:
Antimicrobial Agents and Chemotherapy (AAC) features interdisciplinary studies that build our understanding of the underlying mechanisms and therapeutic applications of antimicrobial and antiparasitic agents and chemotherapy.