1887

Abstract

Between 2010 and 2015 the incidence of vancomycin-resistant (VRE) in Norway increased dramatically. Hence, we selected (1) a random subset of vancomycin-resistant enterococci (VRE) from the Norwegian Surveillance System for Communicable Diseases (2010–15; =239) and (2) Norwegian vancomycin-susceptible (VSE) bacteraemia isolates from the national surveillance system for antimicrobial resistance in microbes (2008 and 2014; =261) for further analysis. Whole-genome sequences were collected for population structure, gene cluster, mobile genetic element and virulome analysis, as well as antimicrobial susceptibility testing. Comparative genomic and phylogeographical analyses were performed with complete genomes of global strains from the National Center for Biotechnology Information (NCBI) (1946–2022; =272). All Norwegian VRE and most of the VSE clustered with global hospital-associated sequence types (STs) in the phylogenetic subclade A1. The subtype carried by chromosomal Tn integrative conjugative elements was the dominant type. The major Norwegian VRE cluster types (CTs) were in accordance with concurrent European CTs. The dominant -type VRE CTs, ST192-CT3/26 and ST117-CT24, were mostly linked to a single hospital in Norway where the clones spread after independent chromosomal acquisition of Tn. The less prevalent VRE were associated with more diverse CTs and carrying Inc18 or RepA_N plasmids with toxin–antitoxin systems. Only 5 % of the Norwegian VRE were all of which contained . The Norwegian VRE and VSE isolates harboured CT-specific virulence factor (VF) profiles supporting biofilm formation and colonization. The dominant VRE CTs in general hosted more virulence determinants than VSE. The phylogenetic clade B VSE isolates (=21) recently classified as , harboured fewer VFs than in general, and particularly subclade A1 isolates. In conclusion, the population structure of Norwegian isolates mirrors the globally prevalent clones and particularly concurrent European VRE/VSE CTs. Novel chromosomal acquisition of on Tn from the gut microbiota, however, formed a single major hospital VRE outbreak. Dominant VRE CTs contained more VFs than VSE.

Funding
This study was supported by the:
  • Helse Nord RHF (Award HNF1362-17)
    • Principle Award Recipient: KristinHegstad
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.001160
2023-12-19
2024-04-27
Loading full text...

Full text loading...

/deliver/fulltext/mgen/9/12/mgen001160.html?itemId=/content/journal/mgen/10.1099/mgen.0.001160&mimeType=html&fmt=ahah

References

  1. Fiore E, Van Tyne D, Gilmore MS. Pathogenicity of enterococci. Microbiol Spectr 2019; 7:4 [View Article] [PubMed]
    [Google Scholar]
  2. Ramos S, Silva V, Dapkevicius M de LE, Igrejas G, Poeta P. Enterococci, from harmless bacteria to a pathogen. Microorganisms 2020; 8:1118 [View Article] [PubMed]
    [Google Scholar]
  3. García-Solache M, Rice LB. The enterococcus: a model of adaptability to its environment. Clin Microbiol Rev 2019; 32:1–28 [View Article] [PubMed]
    [Google Scholar]
  4. van Hal SJ, Willems RJL, Gouliouris T, Ballard SA, Coque TM et al. The interplay between community and hospital Enterococcus faecium clones within health-care settings: a genomic analysis. Lancet Microbe 2022; 3:E133–E141 [View Article] [PubMed]
    [Google Scholar]
  5. Arredondo-Alonso S, Top J, McNally A, Puranen S, Pesonen M et al. Plasmids shaped the recent emergence of the major nosocomial pathogen Enterococcus faecium. mBio 2020; 11:e03284-19 [View Article] [PubMed]
    [Google Scholar]
  6. Lebreton F, van Schaik W, McGuire AM, Godfrey P, Griggs A et al. Emergence of epidemic multidrug-resistant Enterococcus faecium from animal and commensal strains. mBio 2013; 4:e00534-13 [View Article] [PubMed]
    [Google Scholar]
  7. Belloso Daza MV, Cortimiglia C, Bassi D, Cocconcelli PS. Genome-based studies indicate that the Enterococcus faecium Clade B strains belong to Enterococcus lactis species and lack of the hospital infection associated markers. Int J Syst Evol Microbiol 2021; 71:004948 [View Article] [PubMed]
    [Google Scholar]
  8. Sparo M, Delpech G, García Allende N. Impact on public health of the spread of high-level resistance to gentamicin and vancomycin in enterococci. Front Microbiol 2018; 9:3073 [View Article] [PubMed]
    [Google Scholar]
  9. Xavier BB, Coppens J, De Koster S, Rajakani SG, Van Goethem S et al. Novel vancomycin resistance gene cluster in Enterococcus faecium ST1486, Belgium, June 2021. Euro Surveill 2021; 26:2100767 [View Article] [PubMed]
    [Google Scholar]
  10. Moura TM de, Cassenego APV, Campos FS, Ribeiro AML, Franco AC et al. Detection of vanC1 gene transcription in vancomycin-susceptible Enterococcus faecalis. Mem Inst Oswaldo Cruz 2013; 108:453–456 [View Article] [PubMed]
    [Google Scholar]
  11. Sivertsen A, Pedersen T, Larssen KW, Bergh K, Rønning TG et al. A silenced vanA gene cluster on a transferable plasmid caused an outbreak of vancomycin-variable enterococci. Antimicrob Agents Chemother 2016; 60:4119–4127 [View Article] [PubMed]
    [Google Scholar]
  12. Arredondo-Alonso S, Top J, Corander J, Willems RJL, Schürch AC. Mode and dynamics of vanA-type vancomycin resistance dissemination in Dutch hospitals. Genome Med 2021; 13:1–18 [View Article] [PubMed]
    [Google Scholar]
  13. Hegstad K, Mikalsen T, Coque TM, Werner G, Sundsfjord A. Mobile genetic elements and their contribution to the emergence of antimicrobial resistant Enterococcus faecalis and Enterococcus faecium. Clin Microbiol Infect 2010; 16:541–554 [View Article] [PubMed]
    [Google Scholar]
  14. Zhou X, Chlebowicz MA, Bathoorn E, Rosema S, Couto N et al. Elucidating vancomycin-resistant Enterococcus faecium outbreaks: the role of clonal spread and movement of mobile genetic elements. J Antimicrob Chemother 2018; 73:3259–3267 [View Article] [PubMed]
    [Google Scholar]
  15. Weiss RA. Virulence and pathogenesis. Trends Microbiol 2002; 10:314–317 [View Article] [PubMed]
    [Google Scholar]
  16. Mundy LM, Sahm DF, Gilmore M. Relationships between enterococcal virulence and antimicrobial resistance. Clin Microbiol Rev 2000; 13:513–522 [View Article] [PubMed]
    [Google Scholar]
  17. Gao W, Howden BP, Stinear TP. Evolution of virulence in Enterococcus faecium, a hospital-adapted opportunistic pathogen. Curr Opin Microbiol 2018; 41:76–82 [View Article] [PubMed]
    [Google Scholar]
  18. NORM/NORM-VET 2020 Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. ISSN:1502-2307 (Print) / 1890-9965 (Electronic) Tromsø / Oslo: 2021
    [Google Scholar]
  19. NORM/NORM-VET 2008 Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. ISSN: 1502-2307 (Print) / 1890-9965 (Electronic) Tromsø / Oslo: 2009
    [Google Scholar]
  20. NORM/NORM-VET 2014 Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. ISSN: 1502-2307 (Print) / 1890-9965 (Electronic). ISSN:1502-2307 (Electronic) Tromsø / Oslo: 2015
    [Google Scholar]
  21. Rosvoll TCS, Lindstad BL, Lunde TM, Hegstad K, Aasnaes B et al. Increased high-level gentamicin resistance in invasive Enterococcus faecium is associated with aac(6´)Ie-aph(2″)Ia-encoding transferable megaplasmids hosted by major hospital-adapted lineages. FEMS Immunol Med Microbiol 2012; 66:166–176 [View Article] [PubMed]
    [Google Scholar]
  22. Grimes DA, Schulz KF. Compared to what? Finding controls for case-control studies. Lancet 2005; 365:1429–1433 [View Article] [PubMed]
    [Google Scholar]
  23. Dahl KH, Røkenes TP, Lundblad EW, Sundsfjord A. Nonconjugative transposition of the vanB-containing Tn5382-like element in Enterococcus faecium. Antimicrob Agents Chemother 2003; 47:786–789 [View Article] [PubMed]
    [Google Scholar]
  24. European Committee on Antimicrobial Susceptibility Testing – EUCAST Antimicrobial susceptibility testing: EUCAST disk diffusion method, version 7.0; 2019 https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Disk_test_documents/2019_manuals/Manual_v_7.0_EUCAST_Disk_Test_2019.pdf
  25. European Committee on Antimicrobial Susceptibility Testing Breakpoint tables for interpretation of MICs and zone diameters, version 9.0, 2019; 2019 https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_9.0_Breakpoint_Tables.pdf
  26. Swenson JM, Clark NC, Ferraro MJ, Sahm DF, Doern G et al. Development of a standardized screening method for detection of vancomycin-resistant enterococci. J Clin Microbiol 1994; 32:1700–1704 [View Article] [PubMed]
    [Google Scholar]
  27. AL Rubaye MTS, Janice J, Bjørnholt JV, Jakovljev A, Hultström ME et al. Novel genomic islands and a new vanD-subtype in the first sporadic VanD-type vancomycin resistant enterococci in Norway. PLoS One 2021; 16:1–15 [View Article] [PubMed]
    [Google Scholar]
  28. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
    [Google Scholar]
  29. Andrews S. Fastqc: a quality control tool for high throughput sequence data. Babraham Bioinform 2010
    [Google Scholar]
  30. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article] [PubMed]
    [Google Scholar]
  31. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [View Article] [PubMed]
    [Google Scholar]
  32. Koren S, Walenz BP, Berlin K, Miller JR, Bergman NH et al. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res 2017; 27:722–736 [View Article] [PubMed]
    [Google Scholar]
  33. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 2014; 9:e112963 [View Article] [PubMed]
    [Google Scholar]
  34. Hunt M, Silva ND, Otto TD, Parkhill J, Keane JA et al. Circlator: automated circularization of genome assemblies using long sequencing reads. Genome Biol 2015; 16:1–10 [View Article] [PubMed]
    [Google Scholar]
  35. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 2016; 44:6614–6624 [View Article] [PubMed]
    [Google Scholar]
  36. Seemann T. Snippy, Rapid haploid variant calling and core genome alignment; 2015 https://github.com/tseemann/snippy
  37. Jolley KA, Maiden MCJ. BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 2010; 11:595 [View Article] [PubMed]
    [Google Scholar]
  38. de Been M, Pinholt M, Top J, Bletz S, Mellmann A et al. Core genome multilocus sequence typing scheme for high-resolution typing of Enterococcus faecium. J Clin Microbiol 2015; 53:3788–3797 [View Article] [PubMed]
    [Google Scholar]
  39. Neumann B, Prior K, Bender JK, Harmsen D, Klare I et al. A core genome multilocus sequence typing scheme for Enterococcus faecalis. J Clin Microbiol 2019; 57:e01686-18 [View Article] [PubMed]
    [Google Scholar]
  40. Jolley KA, Bray JE, Maiden MCJ. Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res 2018; 3:124 [View Article] [PubMed]
    [Google Scholar]
  41. Treangen TJ, Ondov BD, Koren S, Phillippy AM. The Harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol 2014; 15:524 [View Article] [PubMed]
    [Google Scholar]
  42. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 2021; 49:W293–W296 [View Article] [PubMed]
    [Google Scholar]
  43. Seemann T. Abricate,Github. n.d https://github.com/tseemann/abricate
  44. Darling ACE, Mau B, Blattner FR, Perna NT. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 2004; 14:1394–1403 [View Article] [PubMed]
    [Google Scholar]
  45. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article] [PubMed]
    [Google Scholar]
  46. Carver TJ, Rutherford KM, Berriman M, Rajandream M-A, Barrell BG et al. ACT: the Artemis comparison tool. Bioinformatics 2005; 21:3422–3423 [View Article] [PubMed]
    [Google Scholar]
  47. Sullivan MJ, Petty NK, Beatson SA. Easyfig: a genome comparison visualizer. Bioinformatics 2011; 27:1009–1010 [View Article] [PubMed]
    [Google Scholar]
  48. Robertson J, Nash JHE. MOB-suite: software tools for clustering, reconstruction and typing of plasmids from draft assemblies. Microb Genom 2018; 4:e000206 [View Article] [PubMed]
    [Google Scholar]
  49. Li H. Aligning sequence reads, clone sequences and assembly Contigs with BWA-MEM. arXiv 2013; 1303:3997
    [Google Scholar]
  50. Danecek P, Bonfield JK, Liddle J, Marshall J, Ohan V et al. Twelve years of SAMtools and BCFtools. Gigascience 2021; 10:giab008 [View Article] [PubMed]
    [Google Scholar]
  51. Somarajan SR, La Rosa SL, Singh KV, Roh JH, Höök M et al. The fibronectin-binding protein Fnm contributes to adherence to extracellular matrix components and virulence of Enterococcus faecium. Infect Immun 2015; 83:4653–4661 [View Article] [PubMed]
    [Google Scholar]
  52. Choudhury T, Singh KV, Sillanpää J, Nallapareddy SR, Murray BE. Importance of two Enterococcus faecium loci encoding Gls-like proteins for in vitro bile salts stress response and virulence. J Infect Dis 2011; 203:1147–1154 [View Article] [PubMed]
    [Google Scholar]
  53. Xiong X, Tian S, Yang P, Lebreton F, Bao H et al. Emerging Enterococcus pore-forming toxins with MHC/HLA-I as receptors. Cell 2022; 185:1157–1171 [View Article] [PubMed]
    [Google Scholar]
  54. Paganelli FL, Willems RJL, Jansen P, Hendrickx A, Zhang X et al. Enterococcus faecium biofilm formation: identification of major autolysin AtlAEfm, associated Acm surface localization, and AtlAEfm-independent extracellular DNA Release. mBio 2013; 4:e00154-13 [View Article] [PubMed]
    [Google Scholar]
  55. Zhang S, Lebreton F, Mansfield MJ, Miyashita S-I, Zhang J et al. Identification of a botulinum neurotoxin-like toxin in a commensal strain of Enterococcus faecium. Cell Host Microbe 2018; 23:169–176 [View Article] [PubMed]
    [Google Scholar]
  56. Somarajan SR, Roh JH, Singh KV, Weinstock GM, Murray BE. CcpA is important for growth and virulence of Enterococcus faecium. Infect Immun 2014; 82:3580–3587 [View Article] [PubMed]
    [Google Scholar]
  57. Cacaci M, Giraud C, Leger L, Torelli R, Martini C et al. Expression profiling in a mammalian host reveals the strong induction of genes encoding LysM domain-containing proteins in Enterococcus faecium. Sci Rep 2018; 8:12412 [View Article] [PubMed]
    [Google Scholar]
  58. Ali L, Blum HE, Sakιnç T. Detection and characterization of bacterial polysaccharides in drug-resistant enterococci. Glycoconj J 2019; 36:429–438 [View Article] [PubMed]
    [Google Scholar]
  59. Zhang X, Top J, de Been M, Bierschenk D, Rogers M et al. Identification of a genetic determinant in clinical Enterococcus faecium strains that contributes to intestinal colonization during antibiotic treatment. J Infect Dis 2013; 207:1780–1786 [View Article] [PubMed]
    [Google Scholar]
  60. Wagner TM, Janice J, Paganelli FL, Willems RJ, Askarian F et al. Enterococcus faecium TIR-domain genes are part of a gene cluster which promotes bacterial survival in blood. Int J Microbiol 2018; 2018:1435820 [View Article] [PubMed]
    [Google Scholar]
  61. Palmer KL, Schaik W, Willems RJL, Gilmore MS. Enterococcal genomics. In Gilmore MS, Clewell DB, Ike Y. eds Enterococci: From Commensals to Leading Causes of Drug Resistant Infection Boston: Massachusetts Eye and Ear Infirmary; 2014
    [Google Scholar]
  62. NORM/NORM-VET 2019 Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. ISSN:1502-2307 (Print) / 1890-9965 (Electronic) Tromsø / Oslo: 2020
    [Google Scholar]
  63. Werner G, Neumann B, Weber RE, Kresken M, Wendt C et al. Thirty years of VRE in Germany - “expect the unexpected”: The view from the National Reference Centre for Staphylococci and Enterococci. Drug Resist Updat 2020; 53:100732 [View Article] [PubMed]
    [Google Scholar]
  64. Zhou W, Zhou H, Sun Y, Gao S, Zhang Y et al. Characterization of clinical enterococci isolates, focusing on the vancomycin-resistant enterococci in a tertiary hospital in China: based on the data from 2013 to 2018. BMC Infect Dis 2020; 20:356 [View Article] [PubMed]
    [Google Scholar]
  65. Sivertsen A, Billström H, Melefors Ö, Liljequist BO, Wisell KT et al. A multicentre hospital outbreak in Sweden caused by introduction of a vanB2 transposon into a stably maintained pRUM-plasmid in an Enterococcus faecium ST192 clone. PLoS One 2014; 9:e103274 [View Article] [PubMed]
    [Google Scholar]
  66. Weber A, Maechler F, Schwab F, Gastmeier P, Kola A. Increase of vancomycin-resistant Enterococcus faecium strain type ST117 CT71 at Charité - Universitätsmedizin Berlin, 2008 to 2018. Antimicrob Resist Infect Control 2020; 9:109 [View Article] [PubMed]
    [Google Scholar]
  67. Hammerum AM, Justesen US, Pinholt M, Roer L, Kaya H et al. Surveillance of vancomycin-resistant enterococci reveals shift in dominating clones and national spread of a vancomycin-variable vanA Enterococcus faecium ST1421-CT1134 clone, Denmark, 2015 to March 2019. Euro Surveill 2019; 24:1900503 [View Article] [PubMed]
    [Google Scholar]
  68. Bender JK, Kalmbach A, Fleige C, Klare I, Fuchs S et al. Population structure and acquisition of the vanB resistance determinant in German clinical isolates of Enterococcus faecium ST192. Sci Rep 2016; 6:21847 [View Article] [PubMed]
    [Google Scholar]
  69. Howden BP, Holt KE, Lam MMC, Seemann T, Ballard S et al. Genomic insights to control the emergence of vancomycin-resistant enterococci. mBio 2013; 4:e00412-13 [View Article] [PubMed]
    [Google Scholar]
  70. Quintiliani R, Courvalin P. Conjugal transfer of the vancomycin resistance determinant vanB between enterococci involves the movement of large genetic elements from chromosome to chromosome. FEMS Microbiol Lett 1994; 119:359–363 [View Article] [PubMed]
    [Google Scholar]
  71. Launay A, Ballard SA, Johnson PDR, Grayson ML, Lambert T. Transfer of vancomycin resistance transposon Tn1549 from Clostridium symbiosum to Enterococcus spp. in the gut of gnotobiotic mice. Antimicrob Agents Chemother 2006; 50:1054–1062 [View Article] [PubMed]
    [Google Scholar]
  72. Nygaard RM, Hegstad K, Kommedal Ø, Lindemann PC. High prevalence of vanB in non-enterococcal flora including a novel species contributes to persistent outbreaks of vancomycin resistant enterococci in a Norwegian hospital. In 12th International Meeting on Microbial Epidemiological Markers Dubrovnik, Croatia: 2019
    [Google Scholar]
  73. Tedim AP, Lanza VF, Rodríguez CM, Freitas AR, Novais C et al. Fitness cost of vancomycin-resistant Enterococcus faecium plasmids associated with hospital infection outbreaks. J Antimicrob Chemother 2021; 76:2757–2764 [View Article] [PubMed]
    [Google Scholar]
  74. Wagner TM, Janice J, Sivertsen A, Sjögren I, Sundsfjord A et al. Alternative vanHAX promoters and increased vanA-plasmid copy number resurrect silenced glycopeptide resistance in Enterococcus faecium. J Antimicrob Chemother 2021; 76:876–882 [View Article] [PubMed]
    [Google Scholar]
  75. Freitas AR, Tedim AP, Francia MV, Jensen LB, Novais C et al. Multilevel population genetic analysis of vanA and vanB Enterococcus faecium causing nosocomial outbreaks in 27 countries (1986-2012). J Antimicrob Chemother 2016; 71:3351–3366 [View Article] [PubMed]
    [Google Scholar]
  76. Grady R, Hayes F. Axe-Txe, a broad-spectrum proteic toxin-antitoxin system specified by a multidrug-resistant, clinical isolate of Enterococcus faecium. Mol Microbiol 2003; 47:1419–1432 [View Article] [PubMed]
    [Google Scholar]
  77. Rosvoll TCS, Pedersen T, Sletvold H, Johnsen PJ, Sollid JE et al. PCR-based plasmid typing in Enterococcus faecium strains reveals widely distributed pRE25-, pRUM-, pIP501- and pHTbeta-related replicons associated with glycopeptide resistance and stabilizing toxin-antitoxin systems. FEMS Immunol Med Microbiol 2010; 58:254–268 [View Article] [PubMed]
    [Google Scholar]
  78. Heikens E, Bonten MJM, Willems RJL. Enterococcal surface protein Esp is important for biofilm formation of Enterococcus faecium E1162. J Bacteriol 2007; 189:8233–8240 [View Article] [PubMed]
    [Google Scholar]
  79. Wagner T, Joshi B, Janice J, Askarian F, Škalko-Basnet N et al. Enterococcus faecium produces membrane vesicles containing virulence factors and antimicrobial resistance related proteins. J Proteomics 2018; 187:28–38 [View Article] [PubMed]
    [Google Scholar]
  80. Revtovich AV, Tjahjono E, Singh KV, Hanson BM, Murray BE et al. Development and characterization of high-throughput Caenorhabditis elegans - Enterococcus faecium infection model. Front Cell Infect Microbiol 2021; 11:667327 [View Article] [PubMed]
    [Google Scholar]
  81. Elstrøm P, Astrup E, Hegstad K, Samuelsen Ø, Enger H et al. The fight to keep resistance at bay, epidemiology of carbapenemase producing organisms (CPOs), vancomycin resistant enterococci (VRE) and methicillin resistant Staphylococcus aureus (MRSA) in Norway, 2006 - 2017. PLoS One 2019; 14:e0211741 [View Article]
    [Google Scholar]
  82. Pöntinen AK, Top J, Arredondo-Alonso S, Tonkin-Hill G, Freitas AR et al. Apparent nosocomial adaptation of Enterococcus faecalis predates the modern hospital era. Nat Commun 2021; 12:1523 [View Article] [PubMed]
    [Google Scholar]
  83. Paulsen IT, Banerjei L, Myers GSA, Nelson KE, Seshadri R et al. Role of mobile DNA in the evolution of vancomycin-resistant Enterococcus faecalis. Science 2003; 299:2071–2074 [View Article] [PubMed]
    [Google Scholar]
  84. Furlan S, Matos RC, Kennedy SP, Doublet B, Serror P et al. Fitness restoration of a genetically tractable Enterococcus faecalis V583 derivative to study decoration-related phenotypes of the enterococcal polysaccharide antigen. mSphere 2022; 4:e00310-19 [View Article] [PubMed]
    [Google Scholar]
  85. Ayobami O, Willrich N, Reuss A, Eckmanns T, Markwart R. The ongoing challenge of vancomycin-resistant Enterococcus faecium and Enterococcus faecalis in Europe: an epidemiological analysis of bloodstream infections. Emerg Microbes Infect 2020; 9:1180–1193 [View Article] [PubMed]
    [Google Scholar]
  86. Rios R, Reyes J, Carvajal LP, Rincon S, Panesso D et al. Genomic epidemiology of vancomycin-resistant Enterococcus faecium (VREfm) in Latin America: revisiting the global VRE population structure. Sci Rep 2020; 10:5636 [View Article] [PubMed]
    [Google Scholar]
  87. Lebreton F, Valentino MD, Schaufler K, Earl AM, Cattoir V et al. Transferable vancomycin resistance in clade B commensal-type Enterococcus faecium. J Antimicrob Chemother 2018; 73:1479–1486 [View Article] [PubMed]
    [Google Scholar]
  88. Roer L, Kaya H, Tedim AP, Novais C, Coque TM et al. In silico extended virulence profiling of Enterococcus faecium and Enterococcus lactis isolates by use of whole-genome sequencing data. In 33rd European Congress of Clinical Microbiology and Infectious Diseases Copenhagen: 2023 p 1861
    [Google Scholar]
  89. van Hal SJ, Willems RJL, Gouliouris T, Ballard SA, Coque TM et al. The global dissemination of hospital clones of Enterococcus faecium. Genome Med 2021; 13:52 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.001160
Loading
/content/journal/mgen/10.1099/mgen.0.001160
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error