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":"哨点监测揭示了系统发育的多样性,并在美国收集的肠球菌中检测到携带 vanA 和 optrA 的线性质粒。","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":"{\"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}","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
摘要
粪肠球菌和粪肠球菌是医疗相关感染的常见病因。耐抗菌肠球菌对公共卫生构成严重威胁,尤其是耐万古霉素肠球菌(VRE),其治疗方案有限。美国疾病控制和预防中心的医疗质量促进部门哨点监测系统在 2018 年至 2019 年期间开展了监测,以评估从美国 9 个地理位置不同的地点收集的 205 株粪肠球菌和 180 株粪肠球菌临床分离物的抗菌药敏感性谱和分子流行病学。全基因组测序揭示了不同的遗传系,没有一种序列类型占粪肠球菌或粪肠球菌的 15%以上。系统发育分析将粪肠球菌与 19 种乳杆菌(以前称为粪肠球菌 B 支系)区分开来。粪肠球菌对万古霉素的耐药性为 78.3%,粪肠球菌为 7.8%,而乳杆菌分离株对万古霉素没有耐药性。对达托霉素和利奈唑胺的耐药性很少见:粪肠球菌(分别为 5.6%、0.6%)、粪肠杆菌(2%、2%)和乳酸杆菌(5.3%、0%)。所有 VRE 都携带 vanA 基因。对利奈唑胺不敏感的 7 个分离株中有 3 个携带 optrA,其中一个位于染色体上,另外两个位于线性质粒上,这些线性质粒与其他耐多药共轭线性质粒共享一个保守的骨架。其中一个分离物含有共定位在线性质粒上的 optrA 和 vanA。通过对所有肠球菌进行筛查,预测 20% 的粪肠球菌携带线性质粒,而在粪肠球菌或乳杆菌中没有预测到线性质粒。这项研究证实了之前关于粪肠球菌对更多抗生素的耐药性高于屎肠球菌的报道,并确定不同的序列类型是造成美国肠球菌感染的原因。所有 VRE 都携带 vanA 基因。我们首次报告了美国线性质粒上的利奈唑胺耐药基因 optrA,其中一个质粒同时携带 vanA 基因盒。整合流行病学、抗菌药敏感性和基因组学方法来描述耐药性机制(包括线性质粒的作用)的其他研究对于了解美国肠球菌不断变化的状况至关重要。
Sentinel Surveillance reveals phylogenetic diversity and detection of linear plasmids harboring vanA and optrA among enterococci collected in the United States.
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.