1887

Abstract

Over the last decade, CTX-M enzymes have become the most prevalent extended-spectrum -lactamases (ESBLs) worldwide, mostly in , causing a major health problem. An epidemiological relationship has been established between a rare genotype of , the D genotype, and the presence of CTX-M genes. We investigated this striking association by exploring the genetic backgrounds of 18 D genotype CTX-M-producing strains and of the plasmids encoding CTX-M enzymes. The 18 strains had different genetic backgrounds, as assessed by multilocus sequence and O typing, and were associated with various plasmids bearing diverse CTX-M genes. The region encompassing the genetic marker of the D genotype (TSPE4.C2) was not correlated with the presence of CTX-M genes. CTX-M-producing D strains had far fewer virulence factors than a control group of 8 non-ESBL-producing D strains, and an inverse relationship was found between the number of co-resistances associated with the CTX-M gene and the number of virulence factors found in the strain. These findings provide evidence for multiple acquisitions of plasmids carrying CTX-M genes in different D genotype strains. They strongly suggest that convergent evolution has occurred, and indicate that there has been selection for the association of a specific genetic background of the strain and the CTX-M gene. This fine-tuning of the relationship between the D genotype and CTX-M genes presumably increases the fitness of the strain, indicating a role for the host cell in the acquisition and dissemination of CTX-M genes.

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2009-05-01
2020-09-19
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References

  1. Barlow M., Reik R. A., Jacobs S. D., Medina M., Meyer M. P., McGowan J. E. Jr, Tenover F. C.. 2008; High rate of mobilization for blaCTX-Ms. Emerg Infect Dis14:423–428
    [Google Scholar]
  2. Bettelheim K. A.. 1997a; Escherichia coli in the normal flora of humans and animals. In Escherichia coli: Mechanisms of Virulence pp85–109 Edited by Sussman M.. Cambridge, UK: Cambridge University Press;
  3. Bettelheim K. A.. 1997b; Escherichia coli and human disease. . In Escherichia coli: Mechanisms of Virulence pp3–48 Edited by Sussman M. Cambridge, UK: Cambridge University Press;
  4. Bingen-Bidois M., Clermont O., Bonacorsi S., Terki M., Brahimi N., Loukil C., Barraud D., Bingen E.. 2002; Phylogenetic analysis and prevalence of urosepsis strains of Escherichia coli bearing pathogenicity island-like domains. Infect Immun70:3216–3226
    [Google Scholar]
  5. Bonnet R.. 2004; Growing group of extended-spectrum beta-lactamases: the CTX-M enzymes. Antimicrob Agents Chemother48:1–14
    [Google Scholar]
  6. Boyd E. F., Hill C. W., Rich S. M., Hartl D. L.. 1996; Mosaic structure of plasmids from natural populations of Escherichia coli . Genetics143:1091–1100
    [Google Scholar]
  7. Branger C., Bruneau B., Lesimple A. L., Bouvet P. J., Berry P., Sevali-Garcia J., Lambert-Zechovsky N.. 1997; Epidemiological typing of extended-spectrum beta-lactamase-producing Klebsiella pneumoniae isolates responsible for five outbreaks in a university hospital. J Hosp Infect36:23–36
    [Google Scholar]
  8. Branger C., Zamfir O., Geoffroy S., Laurans G., Arlet G., Thien H. V., Gouriou S., Picard B., Denamur E.. 2005; Genetic background of Escherichia coli and extended-spectrum beta-lactamase type. Emerg Infect Dis11:54–61
    [Google Scholar]
  9. Canton R., Coque T. M.. 2006; The CTX-M beta-lactamase pandemic. Curr Opin Microbiol9:466–475
    [Google Scholar]
  10. Carattoli A., Bertini A., Villa L., Falbo V., Hopkins K. L., Threlfall E. J.. 2005a; Identification of plasmids by PCR-based replicon typing. J Microbiol Methods63:219–228
    [Google Scholar]
  11. Carattoli A., Lovari S., Franco A., Cordaro G., Di Matteo P., Battisti A.. 2005b; Extended-spectrum beta-lactamases in Escherichia coli isolated from dogs and cats in Rome, Italy, from 2001 to 2003. Antimicrob Agents Chemother49:833–835
    [Google Scholar]
  12. Clermont O., Bonacorsi S., Bingen E.. 2000; Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol66:4555–4558
    [Google Scholar]
  13. Clermont O., Johnson J. R., Menard M., Denamur E.. 2007; Determination of Escherichia coli O types by allele-specific polymerase chain reaction: application to the O types involved in human septicemia. Diagn Microbiol Infect Dis57:129–136
    [Google Scholar]
  14. Cooper T. F., Remold S. K., Lenski R. E., Schneider D.. 2008; Expression profiles reveal parallel evolution of epistatic interactions involving the CRP regulon in Escherichia coli . PLoS Genet4:e35
    [Google Scholar]
  15. Eckert C., Gautier V., Saladin-Allard M., Hidri N., Verdet C., Ould-Hocine Z., Barnaud G., Delisle F., Rossier A.. other authors 2004; Dissemination of CTX-M-type beta-lactamases among clinical isolates of Enterobacteriaceae in Paris, France. Antimicrob Agents Chemother48:1249–1255
    [Google Scholar]
  16. Eckert C., Gautier V., Arlet G.. 2006; DNA sequence analysis of the genetic environment of various blaCTX-M genes. J Antimicrob Chemother57:14–23
    [Google Scholar]
  17. Escobar-Paramo P., Clermont O., Blanc-Potard A. B., Bui H., Le Bouguenec C., Denamur E.. 2004a; A specific genetic background is required for acquisition and expression of virulence factors in Escherichia coli . Mol Biol Evol21:1085–1094
    [Google Scholar]
  18. Escobar-Paramo P., Grenet K., Le Menac'h A., Rode L., Salgado E., Amorin C., Gouriou S., Picard B., Rahimy M. C.. other authors 2004b; Large-scale population structure of human commensal Escherichia coli isolates. Appl Environ Microbiol70:5698–5700
    [Google Scholar]
  19. Eykyn S. J., Gransden W. R., Phillips I.. 1990; The causative organisms of septicaemia and their epidemiology. J Antimicrob Chemother25 : Suppl. C 41–58
    [Google Scholar]
  20. Gordon D. M., Clermont O., Tolley H., Denamur E.. 2008; Assigning Escherichia coli strains to phylogenetic groups: multi-locus sequence typing versus the PCR triplex method. Environ Microbiol10:2484–2496
    [Google Scholar]
  21. Guindon S., Gascuel O.. 2003; A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol52:696–704
    [Google Scholar]
  22. Johnson J. R., Goullet P., Picard B., Moseley S. L., Roberts P. L., Stamm W. E.. 1991; Association of carboxylesterase B electrophoretic pattern with presence and expression of urovirulence factor determinants and antimicrobial resistance among strains of Escherichia coli that cause urosepsis. Infect Immun59:2311–2315
    [Google Scholar]
  23. Johnson J. R., Delavari P., Kuskowski M., Stell A. L.. 2001; Phylogenetic distribution of extraintestinal virulence-associated traits in Escherichia coli . J Infect Dis183:78–88
    [Google Scholar]
  24. Johnson J. R., van der Schee C., Kuskowski M. A., Goessens W., van Belkum A.. 2002; Phylogenetic background and virulence profiles of fluoroquinolone-resistant clinical Escherichia coli isolates from the Netherlands. J Infect Dis186:1852–1856
    [Google Scholar]
  25. Johnson J. R., Johnston B., Kuskowski M. A., Colodner R., Raz R.. 2005; Spontaneous conversion to quinolone and fluoroquinolone resistance among wild-type Escherichia coli isolates in relation to phylogenetic background and virulence genotype. Antimicrob Agents Chemother49:4739–4744
    [Google Scholar]
  26. Johnson T. J., Wannemuehler Y. M., Johnson S. J., Logue C. M., White D. G., Doetkott C., Nolan L. K.. 2007; Plasmid replicon typing of commensal and pathogenic Escherichia coli isolates. Appl Environ Microbiol73:1976–1983
    [Google Scholar]
  27. Le Gall T., Clermont O., Gouriou S., Picard B., Nassif X., Denamur E., Tenaillon O.. 2007; Extraintestinal virulence is a coincidental by-product of commensalism in B2 phylogenetic group Escherichia coli strains. Mol Biol Evol24:2373–2384
    [Google Scholar]
  28. Livermore D. M., Canton R., Gniadkowski M., Nordmann P., Rossolini G. M., Arlet G., Ayala J., Coque T. M., Kern-Zdanowicz I.. other authors 2007; CTX-M: changing the face of ESBLs in Europe. J Antimicrob Chemother59:165–174
    [Google Scholar]
  29. Ochman H., Selander R. K.. 1984; Standard reference strains of Escherichia coli from natural populations. J Bacteriol157:690–693
    [Google Scholar]
  30. Oliver A., Coque T. M., Alonso D., Valverde A., Baquero F., Canton R.. 2005; CTX-M-10 linked to a phage-related element is widely disseminated among Enterobacteriaceae in a Spanish hospital. Antimicrob Agents Chemother49:1567–1571
    [Google Scholar]
  31. Osborn A. M., da Silva Tatley F. M., Steyn L. M., Pickup R. W., Saunders J. R.. 2000; Mosaic plasmids and mosaic replicons: evolutionary lessons from the analysis of genetic diversity in IncFII-related replicons. Microbiology146:2267–2275
    [Google Scholar]
  32. Paterson D. L., Bonomo R. A.. 2005; Extended-spectrum beta-lactamases: a clinical update. Clin Microbiol Rev18:657–686
    [Google Scholar]
  33. Picard B., Garcia J. S., Gouriou S., Duriez P., Brahimi N., Bingen E., Elion J., Denamur E.. 1999; The link between phylogeny and virulence in Escherichia coli extraintestinal infection. Infect Immun67:546–553
    [Google Scholar]
  34. Pitout J. D., Nordmann P., Laupland K. B., Poirel L.. 2005; Emergence of Enterobacteriaceae producing extended-spectrum beta-lactamases (ESBLs) in the community. J Antimicrob Chemother56:52–59
    [Google Scholar]
  35. Russo T. A., Johnson J. R.. 2000; Proposal for a new inclusive designation for extraintestinal pathogenic isolates of Escherichia coli : ExPEC. J Infect Dis181:1753–1754
    [Google Scholar]
  36. Sherley M., Gordon D. M., Collignon P. J.. 2004; Evolution of multi-resistance plasmids in Australian clinical isolates of Escherichia coli . Microbiology150:1539–1546
    [Google Scholar]
  37. Smet A., Martel A., Persoons D., Dewulf J., Heyndrickx M., Catry B., Herman L., Haesebrouck F., Butaye P.. 2008; Diversity of extended-spectrum beta-lactamases and class C beta-lactamases among cloacal Escherichia coli isolates in Belgian broiler farms. Antimicrob Agents Chemother52:1238–1243
    [Google Scholar]
  38. Soto S. M., Jimenez de Anta M. T., Vila J.. 2006; Quinolones induce partial or total loss of pathogenicity islands in uropathogenic Escherichia coli by SOS-dependent or -independent pathways, respectively. Antimicrob Agents Chemother50:649–653
    [Google Scholar]
  39. Southern E. M.. 1975; Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol98:503–517
    [Google Scholar]
  40. Toleman M. A., Bennett P. M., Walsh T. R.. 2006; ISCR elements: novel gene-capturing systems of the 21st century?. Microbiol Mol Biol Rev70:296–316
    [Google Scholar]
  41. Velasco M., Horcajada J. P., Mensa J., Moreno-Martinez A., Vila J., Martinez J. A., Ruiz J., Barranco M., Roig G., Soriano E.. 2001; Decreased invasive capacity of quinolone-resistant Escherichia coli in patients with urinary tract infections. Clin Infect Dis33:1682–1686
    [Google Scholar]
  42. Vila J., Simon K., Ruiz J., Horcajada J. P., Velasco M., Barranco M., Moreno A., Mensa J.. 2002; Are quinolone-resistant uropathogenic Escherichia coli less virulent?. J Infect Dis186:1039–1042
    [Google Scholar]
  43. Warren R. E., Ensor V. M., O'Neill P., Butler V., Taylor J., Nye K., Harvey M., Livermore D. M., Woodford N., Hawkey P. M.. 2008; Imported chicken meat as a potential source of quinolone-resistant Escherichia coli producing extended-spectrum beta-lactamases in the UK. J Antimicrob Chemother61:504–508
    [Google Scholar]
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