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Abstract

Enterohaemorrhagic (EHEC) is an important human pathogen worldwide. Although serotype O157 is currently the most dominant and important EHEC strain, serotypes O26, O111, O91, O103 and O121 are also recognized as serious pathogens that affect public health. EHEC outbreaks often occur in nurseries and elderly care facilities. In 2012, a nursery outbreak of EHEC O121 occurred during which the bacterium acquired a plasmid-borne extended-spectrum -lactamase (ESBL) gene. ESBL-producing O86 was concurrently isolated from one of the EHEC patients. Therefore, we investigated the isolates by whole-genome sequence (WGS) analysis to elucidate the transmission dynamics of the EHEC strains and the ESBL plasmid. According to WGS-based phylogeny, all 17 EHEC O121 isolates were clonal, while O86 was genetically distant from the EHEC O121 isolates. The complete sequence of an ESBL plasmid encoding the CTX-M-55 -lactamase was determined using S1-PFGE bands, and subsequent mapping of the WGS reads confirmed that the plasmid sequences from EHEC O121 and O86 were identical. Furthermore, conjugation experiments showed that the plasmid was capable of conjugative transfer. These results support the hypothesis that EHEC O121 acquired an ESBL-producing plasmid from O86 during the outbreak. This report demonstrates the importance of implementing preventive measures during EHEC outbreaks to control both secondary infection and the spread of antimicrobial resistance factors.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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2019-06-19
2024-03-28
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References

  1. Tarr PI, Gordon CA, Chandler WL. Shiga-toxin-producing Escherichia coli and haemolytic uraemic syndrome. Lancet 2005; 365:1073–1086 [View Article]
    [Google Scholar]
  2. Karmali MA. Infection by verocytotoxin-producing Escherichia coli . Clin Microbiol Rev 1989; 2:15–38 [View Article]
    [Google Scholar]
  3. Armstrong GL, Hollingsworth J, Morris JG. Emerging foodborne pathogens: Escherichia coli O157:H7 as a model of entry of a new pathogen into the food supply of the developed world. Epidemiol Rev 1996; 18:29–51 [View Article]
    [Google Scholar]
  4. Infectious Agents Surveillance Report Enterohemorrhagic Escherichia coli (EHEC) infection, as of March 2018, Japan; 2018 https://www.niid.go.jp/niid/en/iasr-vol39-e/865-iasr/8042-459te.html 2018/07/03
  5. Izumiya H, Pei YX, Terajima J, Ohnishi M, Hayashi T et al. New system for multilocus variable-number tandem-repeat analysis of the enterohemorrhagic Escherichia coli strains belonging to three major serogroups: O157, O26, and O111. Microbiol Immunol 2010; 54:569–577
    [Google Scholar]
  6. Scavia G, Gianviti A, Labriola V, Chiani P, Maugliani A et al. A case of haemolytic uraemic syndrome (HUS) revealed an outbreak of Shiga toxin-2-producing Escherichia coli O26:H11 infection in a nursery, with long-lasting shedders and person-to-person transmission, Italy 2015. J Med Microbiol 2018
    [Google Scholar]
  7. McFarland N, Bundle N, Jenkins C, Godbole G, Mikhail A et al. Recurrent seasonal outbreak of an emerging serotype of Shiga toxin-producing Escherichia coli (STEC O55:H7 Stx2a) in the south west of England, July 2014 to September 2015. Euro Surveill 2017; 22: [View Article]
    [Google Scholar]
  8. Moran-Gilad J, Rokney A, Danino D, Ferdous M, Alsana F et al. Real-time genomic investigation underlying the public health response to a Shiga toxin-producing Escherichia coli O26:H11 outbreak in a nursery. Epidemiol Infect 2017; 145:2998–3006 [View Article]
    [Google Scholar]
  9. Wahl E, Vold L, Lindstedt BA, Bruheim T, Afset JE. Investigation of an Escherichia coli O145 outbreak in a child day-care centre - extensive sampling and characterization of eae- and stx1-positive E. coli yields epidemiological and socioeconomic insight. BMC Infect Dis 2011; 11:238 [View Article]
    [Google Scholar]
  10. Muraoka R, Okazaki M, Fujimoto Y, Jo N, Yoshida R et al. An enterohemorrhagic Escherichia coli O103 outbreak at a nursery school in Miyazaki Prefecture, Japan. Jpn J Infect Dis 2007; 60:410–411
    [Google Scholar]
  11. Kishimoto M. [An outbreak of enterohemorrhagic Escherichia coli O111 infections at a nursery school in Hiroshima Prefecture]. Nihon Koshu Eisei Zasshi 2000; 47:440–444
    [Google Scholar]
  12. Kikuchi K, Ueno H, Tomari K, Kobori S, Kaetsu A et al. Identification of resistance and susceptibility to cefotaxime in EHEC O121 strains isolated from an outbreak at two nurseries. Kansenshogaku Zasshi 2014; 88:430–437 [View Article]
    [Google Scholar]
  13. Lee K, Morita-Ishihara T, Iyoda S, Ogura Y, Hayashi T et al. A geographically widespread outbreak investigation and development of a rapid screening method using whole genome sequences of enterohemorrhagic Escherichia coli O121. Front Microbiol 2017; 8: [View Article]
    [Google Scholar]
  14. Mellmann A, Harmsen D, Cummings CA, Zentz EB, Leopold SR et al. Prospective genomic characterization of the German enterohemorrhagic Escherichia coli O104:H4 outbreak by rapid next generation sequencing technology. PLoS One 2011; 6:e22751 [View Article]
    [Google Scholar]
  15. Pollard DR, Johnson WM, Lior H, Tyler SD, Rozee KR. Rapid and specific detection of Verotoxin genes in Escherichia coli by the polymerase chain reaction. J Clin Microbiol 1990; 28:540–545
    [Google Scholar]
  16. Paton JC, Paton AW. Pathogenesis and diagnosis of Shiga toxin-producing Escherichia coli infections. Clin Microbiol Rev 1998; 11:450–479 [View Article]
    [Google Scholar]
  17. Clinical Laboratory Standards Institute Performance standards for antimicrobial susceptibility testing, twenty-first Informational supplement. CLSI documents. M100-S21. 2011
    [Google Scholar]
  18. Shibata N, Kurokawa H, Doi Y, Yagi T, Yamane K et al. PCR classification of CTX-M-type beta-lactamase genes identified in clinically isolated Gram-negative bacilli in Japan. Antimicrob Agents Chemother 2006; 50:791–795 [View Article]
    [Google Scholar]
  19. Yagi T, Kurokawa H, Shibata N, Shibayama K, Arakawa Y. A preliminary survey of extended-spectrum β-lactamases (ESBLs) in clinical isolates of Klebsiella pneumoniae and Escherichia coli in Japan. FEMS Microbiol Lett 2000; 184:53–56 [View Article]
    [Google Scholar]
  20. Li H, Durbin R. Fast and accurate long-read alignment with Burrows–Wheeler transform. Bioinformatics 2010; 26:589–595 [View Article]
    [Google Scholar]
  21. Li H. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 2011; 27:2987–2993 [View Article]
    [Google Scholar]
  22. Koboldt DC, Zhang Q, Larson DE, Shen D, McLellan MD et al. VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Res 2012; 22:568–576 [View Article]
    [Google Scholar]
  23. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M et al. Versatile and open software for comparing large genomes. Genome Biol 2004; 5:R12 [View Article]
    [Google Scholar]
  24. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article]
    [Google Scholar]
  25. Zhou Z, Alikhan NF, Sergeant MJ, Luhmann N, Vaz C et al. GrapeTree: visualization of core genomic relationships among 100,000 bacterial pathogens. bioRxiv 2017
    [Google Scholar]
  26. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article]
    [Google Scholar]
  27. Clermont O, Christenson JK, Denamur E, Gordon DM. The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environ Microbiol Rep 2013; 5:58–65 [View Article]
    [Google Scholar]
  28. Barton BM, Harding GP, Zuccarelli AJ. A general method for detecting and sizing large plasmids. Anal Biochem 1995; 226:235–240 [View Article]
    [Google Scholar]
  29. Sekizuka T, Kawanishi M, Ohnishi M, Shima A, Kato K et al. Elucidation of quantitative structural diversity of remarkable rearrangement regions, shufflons, in IncI2 plasmids. Sci Rep 2017; 7:928 [View Article]
    [Google Scholar]
  30. Tanizawa Y, Fujisawa T, Nakamura Y. DFAST: a flexible prokaryotic genome annotation pipeline for faster genome publication. Bioinformatics 2018; 34:1037–1039 [View Article]
    [Google Scholar]
  31. Ishii Y, Ohno A, Taguchi H, Imajo S, Ishiguro M et al. Cloning and sequence of the gene encoding a cefotaxime-hydrolyzing class A β-lactamase isolated from Escherichia coli . Antimicrob Agents Chemother 1995; 39:2269–2275 [View Article]
    [Google Scholar]
  32. Yagi T, Kurokawa H, Senda K, Ichiyama S, Ito H et al. Nosocomial spread of cephem-resistant Escherichia coli strains carrying multiple Toho-1-like β-lactamase genes. Antimicrob Agents Chemother 1997; 41:2606–2611 [View Article]
    [Google Scholar]
  33. Kameyama M, Yabata J, Nomura Y, Tominaga K. Detection of CMY-2 AmpC β-lactamase-producing enterohemorrhagic Escherichia coli O157:H7 from outbreak strains in a nursery school in Japan. J Infect Chemother 2015; 21:544–546 [View Article]
    [Google Scholar]
  34. Valat C, Haenni M, Saras E, Auvray F, Forest K et al. CTX-M-15 extended-spectrum β-lactamase in a Shiga toxin-producing Escherichia coli isolate of serotype O111:H8. Appl Environ Microbiol 2012; 78:1308–1309 [View Article]
    [Google Scholar]
  35. Suzuki S, Shibata N, Yamane K, Wachino J, Ito K et al. Change in the prevalence of extended-spectrum-β-lactamase-producing Escherichia coli in Japan by clonal spread. J Antimicrob Chemother 2009; 63:72–79 [View Article]
    [Google Scholar]
  36. Kiratisin P, Apisarnthanarak A, Saifon P, Laesripa C, Kitphati R et al. The emergence of a novel ceftazidime-resistant CTX-M extended-spectrum β-lactamase, CTX-M-55, in both community-onset and hospital-acquired infections in Thailand. Diagn Microbiol Infect Dis 2007; 58:349–355 [View Article]
    [Google Scholar]
  37. Lee W, Chung HS, Lee H, Yum JH, Yong D et al. CTX-M-55-type extended-spectrum β-lactamase-producing Shigella sonnei isolated from a Korean patient who had travelled to China. Ann Lab Med 2013; 33:141–144 [View Article]
    [Google Scholar]
  38. Hu X, Gou J, Guo X, Cao Z, Li Y et al. Genetic contexts related to the diffusion of plasmid-mediated CTX-M-55 extended-spectrum β-lactamase isolated from Enterobacteriaceae in China. Ann Clin Microbiol Antimicrob 2018; 17:12 [View Article]
    [Google Scholar]
  39. Kameyama M, Chuma T, Yabata J, Tominaga K, Iwata H et al. Prevalence and epidemiological relationship of CMY-2 AmpC β-lactamase and CTX-M extended-spectrum β-lactamase-producing Escherichia coli isolates from broiler farms in Japan. J Vet Med Sci 2013; 75:1009–1015 [View Article]
    [Google Scholar]
  40. Shimizu T, Harada K, Tsuyuki Y, Kimura Y, Miyamoto T et al. In vitro efficacy of 16 antimicrobial drugs against a large collection of β-lactamase-producing isolates of extraintestinal pathogenic Escherichia coli from dogs and cats. J Med Microbiol 2017; 66:1085–1091 [View Article]
    [Google Scholar]
  41. Norizuki C, Kawamura K, Wachino J-I, Suzuki M, Nagano N et al. Detection of Escherichia coli producing CTX-M-1-Group extended-spectrum β-lactamases from pigs in Aichi Prefecture, Japan, between 2015 and 2016. Jpn J Infect Dis 2018; 71:33–38 [View Article]
    [Google Scholar]
  42. Nishino Y, Shimojima Y, Suzuki Y, Ida M, Fukui R et al. Detection of the mcr-1 gene in colistin-resistant Escherichia coli from retail meat in Japan. Microbiol Immunol 2017; 61:554–557 [View Article]
    [Google Scholar]
  43. Ohsaki Y, Hayashi W, Saito S, Osaka S, Taniguchi Y et al. First detection of an Escherichia coli strain harboring the mcr-1 gene in retail domestic chicken meat in Japan. Jpn J Infect Dis 2017; 70:590–592 [View Article]
    [Google Scholar]
  44. Imoto A, Ooi Y, Edogawa S, Ogura T, Masuda D et al. Liver abscess caused by CTX-M-55-type extended-spectrum β-lactamase (ESBL)-producing Salmonella enteritidis . Intern Med 2014; 53:1699–1703 [View Article]
    [Google Scholar]
  45. Wong CS, Jelacic S, Habeeb RL, Watkins SL, Tarr PI. The risk of the hemolytic-uremic syndrome after antibiotic treatment of Escherichia coli O157:H7 infections. N Engl J Med 2000; 342:1930–1936 [View Article]
    [Google Scholar]
  46. Tajiri H, Nishi J, Ushijima K, Shimizu T, Ishige T et al. A role for fosfomycin treatment in children for prevention of haemolytic–uraemic syndrome accompanying Shiga toxin-producing Escherichia coli infection. Int J Antimicrob Agents 2015; 46:586–589 [View Article]
    [Google Scholar]
  47. Mohsin M, Haque A, Ali A, Sarwar Y, Bashir S et al. Effects of ampicillin, gentamicin, and cefotaxime on the release of shiga toxins from Shiga toxin-producing Escherichia coli isolated during a diarrhea episode in Faisalabad, Pakistan. Foodborne Pathog Dis 2010; 7:85–90 [View Article]
    [Google Scholar]
  48. Nassar FJ, Rahal EA, Sabra A, Matar GM. Effects of subinhibitory concentrations of antimicrobial agents on Escherichia coli O157:H7 Shiga toxin release and role of the SOS response. Foodborne Pathog Dis 2013; 10:805–812 [View Article]
    [Google Scholar]
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