1887

Abstract

Clinical isolates that produce extended-spectrum β-lactamases (ESBLs) have been increasingly reported at a global scale. However, comprehensive data on the molecular epidemiology of ESBL-producing strains are limited and few studies have been conducted in non-outbreak situations.

We used whole-genome sequencing to describe the population structure of 294 ESBL-producing and isolates that were recovered from a German community hospital throughout a 1 year sampling period in a non-outbreak situation.

We found a high proportion of isolates (61.5 %) belonged to the globally disseminated extraintestinal pathogenic ST131, whereas a wider diversity of STs was observed among isolates. The ST131 population in this study was shaped by multiple introductions of strains as demonstrated by contextual genomic analysis including ST131 strains from other geographical sources. While no recent common ancestor of the isolates of the current study and other international isolates was found, our clinical isolates clustered with those previously recovered in the region. Furthermore, we found that the isolation of ESBL-producing clinical strains in hospitalized patients could only rarely be associated with likely patient-to-patient transmission, indicating primarily a community and regional acquisition of strains.

Further genomic analyses of clinical, carriage and environmental isolates is needed to uncover hidden transmissions and thus discover the most common sources of ESBL-producing pathogen infections in our hospitals.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000901
2022-12-16
2024-11-07
Loading full text...

Full text loading...

/deliver/fulltext/mgen/8/12/mgen000901.html?itemId=/content/journal/mgen/10.1099/mgen.0.000901&mimeType=html&fmt=ahah

References

  1. Cantón R, Novais A, Valverde A, Machado E, Peixe L et al. Prevalence and spread of extended-spectrum beta-lactamase-producing Enterobacteriaceae in Europe. Clin Microbiol Infect 2008; 14 Suppl 1:144–153 [View Article]
    [Google Scholar]
  2. Coque TM, Novais A, Carattoli A, Poirel L, Pitout J et al. Dissemination of clonally related Escherichia coli strains expressing extended-spectrum beta-lactamase CTX-M-15. Emerg Infect Dis 2008; 14:195–200 [View Article] [PubMed]
    [Google Scholar]
  3. Mathers AJ, Peirano G, Pitout JDD. The role of epidemic resistance plasmids and international high-risk clones in the spread of multidrug-resistant Enterobacteriaceae. Clin Microbiol Rev 2015; 28:565–591 [View Article]
    [Google Scholar]
  4. Surveillance Atlas of Infectious Diseases. Internet 2021Aug 13 https://atlas.ecdc.europa.eu/public/index.aspx
    [Google Scholar]
  5. Mathers AJ, Peirano G, Pitout JDD. Escherichia coli ST131: the quintessential example of an international multiresistant high-risk clone. Adv Appl Microbiol 2015; 90:109–154 [View Article]
    [Google Scholar]
  6. Nicolas-Chanoine MH, Bertrand X, Madec JY. Escherichia coli ST131, an intriguing clonal group. Clin Microbiol Rev 2014; 27:543–574 [View Article]
    [Google Scholar]
  7. Petty NK, Ben Zakour NL, Stanton-Cook M, Skippington E, Totsika M et al. Global dissemination of a multidrug resistant Escherichia coli clone. Proc Natl Acad Sci 2014; 111:5694–5699 [View Article]
    [Google Scholar]
  8. Price LB, Johnson JR, Aziz M, Clabots C, Johnston B et al. The epidemic of extended-spectrum-β-lactamase-producing Escherichia coli ST131 is driven by a single highly pathogenic subclone, H30-Rx. mBio 2013; 4:e00377–13 [View Article]
    [Google Scholar]
  9. Birgy A, Bidet P, Levy C, Sobral E, Cohen R et al. CTX-M-27-producing Escherichia coli of sequence type 131 and clade C1-M27, France. Emerg Infect Dis 2017; 23:885 [View Article]
    [Google Scholar]
  10. Merino I, Hernández-García M, Turrientes M-C, Pérez-Viso B, López-Fresneña N et al. Emergence of ESBL-producing Escherichia coli ST131-C1-M27 clade colonizing patients in Europe. J Antimicrob Chemother 2018; 73:2973–2980 [View Article] [PubMed]
    [Google Scholar]
  11. Ghosh H, Doijad S, Falgenhauer L, Fritzenwanker M, Imirzalioglu C et al. blaCTX-M-27-encoding Escherichia coli sequence type 131 lineage C1-M27 clone in clinical isolates, Germany. Emerg Infect Dis 2017; 23:1754–1756 [View Article]
    [Google Scholar]
  12. Tchesnokova VL, Rechkina E, Larson L, Ferrier K, Weaver JL et al. Rapid and extensive expansion in the United States of a new multidrug-resistant Escherichia coli clonal group, sequence type 1193. Clin Infect Dis 2019; 68:334–337 [View Article]
    [Google Scholar]
  13. Valenza G, Werner M, Eisenberger D, Nickel S, Lehner-Reindl V et al. First report of the new emerging global clone ST1193 among clinical isolates of extended-spectrum β-lactamase (ESBL)-producing Escherichia coli from Germany. J Glob Antimicrob Resist 2019; 17:305–308 [View Article] [PubMed]
    [Google Scholar]
  14. Baym M, Kryazhimskiy S, Lieberman TD, Chung H, Desai MM et al. Inexpensive multiplexed library preparation for megabase-sized genomes. PLOS ONE 2015; 10:e0128036 [View Article]
    [Google Scholar]
  15. Steglich M, Hofmann JD, Helmecke J, Sikorski J, Spröer C et al. Convergent loss of ABC transporter genes from Clostridioides difficile genomes is associated with impaired tyrosine uptake and p-cresol production. Front Microbiol 2018; 9:901 [View Article]
    [Google Scholar]
  16. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article]
    [Google Scholar]
  17. Prjibelski A, Antipov D, Meleshko D, Lapidus A, Korobeynikov A. Using SPAdes de novo assembler. Curr Protoc Bioinformatics 2020; 70:e102 [View Article]
    [Google Scholar]
  18. Sambrook J, Fritsch EF, Maniatis T. Molecular cloning: a laboratory manual. In Molecular Cloning: A Laboratory Manual vol 2 1989
    [Google Scholar]
  19. 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]
    [Google Scholar]
  20. 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]
    [Google Scholar]
  21. McNally A, Oren Y, Kelly D, Pascoe B, Dunn S et al. Combined analysis of variation in core, accessory and regulatory genome regions provides a super-resolution view into the evolution of bacterial populations. PLoS Genet 2016; 12:e1006280 [View Article]
    [Google Scholar]
  22. Rasko DA, Rosovitz MJ, Myers GSA, Mongodin EF, Fricke WF et al. The pangenome structure of Escherichia coli: comparative genomic analysis of E. coli commensal and pathogenic isolates. J Bacteriol 2008; 190:6881–6893 [View Article]
    [Google Scholar]
  23. Croucher NJ, Harris SR, Grad YH, Hanage WP. Bacterial genomes in epidemiology--present and future. Philos Trans R Soc Lond B Biol Sci 2013; 368:20120202 [View Article]
    [Google Scholar]
  24. Seemann T. Snippy: fast bacterial variant calling from NGS reads; 2015
  25. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 2019; 47:W256–W259 [View Article] [PubMed]
    [Google Scholar]
  26. Zhou Z, Alikhan NF, Mohamed K, Fan Y, Achtman M. The enterobase user’s guide, with case studies on salmonella transmissions, yersinia pestis phylogeny, and escherichia core genomic diversity. Genome Research 2020; 30:138–152
    [Google Scholar]
  27. Pietsch M, Irrgang A, Roschanski N, Brenner Michael G, Hamprecht A et al. Whole genome analyses of CMY-2-producing Escherichia coli isolates from humans, animals and food in Germany. BMC Genomics 2018; 19:601 [View Article]
    [Google Scholar]
  28. Matsumura Y, Pitout JDD, Gomi R, Matsuda T, Noguchi T et al. Global Escherichia coli sequence type 131 clade with blaCTX-M-27 gene. Emerg Infect Dis 2016; 22:1900–1907 [View Article]
    [Google Scholar]
  29. Decano AG, Downing T. An Escherichia coli ST131 pangenome atlas reveals population structure and evolution across 4,071 isolates. Sci Rep 2019; 9:1–13 [View Article]
    [Google Scholar]
  30. Holt KE, Wertheim H, Zadoks RN, Baker S, Whitehouse CA et al. Genomic analysis of diversity, population structure, virulence, and antimicrobial resistance in Klebsiella pneumoniae, an urgent threat to public health. Proc Natl Acad Sci 2015; 112:E3574–81 [View Article]
    [Google Scholar]
  31. Hagel S, Makarewicz O, Hartung A, Weiß D, Stein C et al. ESBL colonization and acquisition in a hospital population: the molecular epidemiology and transmission of resistance genes. PLoS ONE 2019; 14:e0208505 [View Article]
    [Google Scholar]
  32. Tschudin-Sutter S, Frei R, Dangel M, Stranden A, Widmer AF. Rate of transmission of extended-spectrum beta-lactamase-producing Enterobacteriaceae without contact isolation. Clin Infect Dis 2012; 55:1505–1511 [View Article]
    [Google Scholar]
  33. Willemsen I, Elberts S, Verhulst C, Rijnsburger M, Filius M et al. Highly resistant gram-negative microorganisms: incidence density and occurrence of nosocomial transmission (TRIANGLe Study). Infect Control Hosp Epidemiol 2011; 32:333–341 [View Article]
    [Google Scholar]
  34. Xercavins M, Jiménez E, Padilla E, Riera M, Freixas N et al. High clonal diversity of ESBL-producing Klebsiella pneumoniae isolates from clinical samples in a non-outbreak situation. A cohort study. Antimicrob Resist Infect Control 2020; 9:1–9 [View Article]
    [Google Scholar]
  35. Schürch AC, Arredondo-Alonso S, Willems RJL, Goering RV. Whole genome sequencing options for bacterial strain typing and epidemiologic analysis based on single nucleotide polymorphism versus gene-by-gene-based approaches. Clin Microbiol Infect 2018; 24:350–354 [View Article]
    [Google Scholar]
  36. Besser JM, Carleton HA, Trees E, Stroika SG, Hise K et al. Interpretation of whole-genome sequencing for enteric disease surveillance and outbreak investigation. Foodborne Pathog Dis 2019; 16:504–512 [View Article]
    [Google Scholar]
  37. Stoesser N, Sheppard AE, Moore CE, Golubchik T, Parry CM et al. Extensive within-host diversity in fecally carried extended-spectrum-beta-lactamase-producing Escherichia coli isolates: implications for transmission analyses. J Clin Microbiol 2015; 53:2122–2131 [View Article]
    [Google Scholar]
  38. Thuy DB, Campbell J, Thuy CT, Hoang NVM, Voong Vinh P et al. Colonization with Staphylococcus aureus and Klebsiella pneumoniae causes infections in a Vietnamese intensive care unit. Microb Genom 2021; 7: [View Article]
    [Google Scholar]
  39. Erb S, Frei R, Dangel M, Widmer AF. Multidrug-resistant organisms detected more than 48 hours after hospital admission are not necessarily hospital-acquired. Infect Control Hosp Epidemiol 2017; 38:18–23 [View Article]
    [Google Scholar]
  40. Endimiani A, Depasquale JM, Forero S, Perez F, Hujer AM et al. Emergence of blaKPC-containing Klebsiella pneumoniae in a long-term acute care hospital: a new challenge to our healthcare system. J Antimicrob Chemother 2009; 64:1102–1110 [View Article]
    [Google Scholar]
  41. Rooney PJ, O’Leary MC, Loughrey AC, McCalmont M, Smyth B et al. Nursing homes as a reservoir of extended-spectrum beta-lactamase (ESBL)-producing ciprofloxacin-resistant Escherichia coli. J Antimicrob Chemother 2009; 64:635–641 [View Article] [PubMed]
    [Google Scholar]
/content/journal/mgen/10.1099/mgen.0.000901
Loading
/content/journal/mgen/10.1099/mgen.0.000901
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