1887

Abstract

Purpose. Fluoroquinolone resistance (FQ-r) in extended-spectrum β-lactamase (ESBL) producers is an urgent health concern in countries where ESBL-producing K. pneumoniae (ESBL-Kpn) is prevalent. We investigated FQ-r in Japan where ESBL-Kpn is less prevalent.

Methodology. Clinical ESBL-Kpn isolates from 2011 to 2013 were collected in Nagasaki University Hospital. The ESBL genotypes included CTX-M-15, and the mechanisms of FQ-r through plasmid-mediated quinolone resistance (PMQR) and mutations in quinolone resistance-determining regions (QRDRs) were examined. Clonality was analysed by enterobacterial repetitive intergenic consensus (ERIC)-PCR and multi-locus sequence typing was performed on selected isolates.

Results/Key findings. Thirty ESBL-Kpn isolates, including seven levofloxacin-resistant isolates, were obtained from different patients. An increase in CTX-M-15-producing strains was observed during the study period (0/11 in 2011, 3/8 in 2012, and 5/11 in 2013). PMQR was detected in 53.3 % of the isolates and aac-(6′)-Ib-cr was the most common (36.7 %). ST15 was observed in 60.0 % of the isolates, and for the most predominant ERIC-PCR profiles, 62.5 % of the isolates possessed the CTX-M-15 genotype and 71.4 % were levofloxacin-resistant. Levofloxacin-resistance was significantly more common in CTX-M-15 isolates (62.5 %) compared to non-CTX-M-15 isolates (9.1 %). Three QRDR mutations and aac(6′)-Ib-cr, but not qnrB and qnrS, were significantly enriched in the CTX-M-15 isolates (100.0 %) compared to the non-CTX-M-15 isolates (13.6 %).

Conclusion. Cumulatively, these results indicate that the epidemic strain, the CTX-M-15-producing K. pneumoniae ST15, is covertly spreading even when ESBL producers are not prevalent. Monitoring these epidemic strains and ESBLs in general is important for quickly identifying health crises and minimizing future risks from FQ-r ESBL-Kpn.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.000577
2017-09-12
2019-10-16
Loading full text...

Full text loading...

/deliver/fulltext/jmm/66/10/1476.html?itemId=/content/journal/jmm/10.1099/jmm.0.000577&mimeType=html&fmt=ahah

References

  1. Paterson DL, Bonomo RA. Extended-spectrum β-lactamases: a clinical update. Clin Microbiol Rev 2005;18:657–686 [CrossRef][PubMed]
    [Google Scholar]
  2. Nicolas-Chanoine MH, Bertrand X, Madec JY. Escherichia coli ST131, an intriguing clonal group. Clin Microbiol Rev 2014;27:543–574 [CrossRef][PubMed]
    [Google Scholar]
  3. Damjanova I, Tóth A, Pászti J, Bauernfeind A, Füzi M. Nationwide spread of clonally related CTX-M-15-producing multidrug-resistant Klebsiella pneumoniae strains in Hungary. Eur J Clin Microbiol Infect Dis 2006;25:275–278 [CrossRef][PubMed]
    [Google Scholar]
  4. Oteo J, Cuevas O, López-Rodríguez I, Banderas-Florido A, Vindel A et al. Emergence of CTX-M-15-producing Klebsiella pneumoniae of multilocus sequence types 1, 11, 14, 17, 20, 35 and 36 as pathogens and colonizers in newborns and adults. J Antimicrob Chemother 2009;64:524–528 [CrossRef][PubMed]
    [Google Scholar]
  5. Robicsek A, Strahilevitz J, Jacoby GA, Macielag M, Abbanat D et al. Fluoroquinolone-modifying enzyme: a new adaptation of a common aminoglycoside acetyltransferase. Nat Med 2006;12:83–88 [CrossRef][PubMed]
    [Google Scholar]
  6. Briales A, Rodríguez-Martínez JM, Velasco C, de Alba PD, Rodríguez-Baño J et al. Prevalence of plasmid-mediated quinolone resistance determinants qnr and aac(6')-Ib-cr in Escherichia coli and Klebsiella pneumoniae producing extended-spectrum β-lactamases in Spain. Int J Antimicrob Agents 2012;39:431–434 [CrossRef][PubMed]
    [Google Scholar]
  7. Zurfluh K, Abgottspon H, Hächler H, Nüesch-Inderbinen M, Stephan R. Quinolone resistance mechanisms among extended-spectrum beta-lactamase (ESBL) producing Escherichia coli isolated from rivers and lakes in Switzerland. PLoS One 2014;9:e95864 [CrossRef][PubMed]
    [Google Scholar]
  8. Park KS, Kim MH, Park TS, Nam YS, Lee HJ et al. Prevalence of the plasmid-mediated quinolone resistance genes, aac(6')-Ib-cr, qepA, and oqxAB in clinical isolates of extended-spectrum β-lactamase (ESBL)-producing Escherichia coli and Klebsiella pneumoniae in Korea. Ann Clin Lab Sci 2012;42:191–197[PubMed]
    [Google Scholar]
  9. Center for Disease Dynamics EPC State of the World's Antibiotics, 2015 2015
    [Google Scholar]
  10. Chong Y, Shimoda S, Yakushiji H, Ito Y, Miyamoto T et al. Community spread of extended-spectrum β-lactamase-producing Escherichia coli, Klebsiella pneumoniae and Proteus mirabilis: a long-term study in Japan. J Med Microbiol 2013;62:1038–1043 [CrossRef][PubMed]
    [Google Scholar]
  11. Cantón R, Novais A, Valverde A, Machado E, Peixe L et al. Prevalence and spread of extended-spectrum β-lactamase-producing enterobacteriaceae in Europe. Clin Microbiol Infect 2008;14:144–153 [CrossRef][PubMed]
    [Google Scholar]
  12. Harada Y, Morinaga Y, Yamada K, Migiyama Y, Nagaoka K et al. Clinical and molecular epidemiology of extended-spectrum β-lactamase-producing Klebsiella pneumoniae and Escherichia coli in a Japanese Tertiary hospital. J Med Microb Diagn 2013;2:2161-0703.1000127
    [Google Scholar]
  13. Clinical and Laboratory Standards Institute Performance Standards for Antimicrobial Susceptibility Testing M100-S23 2013
    [Google Scholar]
  14. Doi Y, Adams-Haduch JM, Shivannavar CT, Paterson DL, Gaddad SM. Faecal carriage of CTX-M-15-producing Klebsiella pneumoniae in patients with acute gastroenteritis. Indian J Med Res 2009;129:599–602[PubMed]
    [Google Scholar]
  15. Muratani T, Kobayashi T, Matsumoto T. Emergence and prevalence of β-lactamase-producing Klebsiella pneumoniae resistant to cephems in Japan. Int J Antimicrob Agents 2006;27:491–499 [CrossRef][PubMed]
    [Google Scholar]
  16. Aoike N, Saga T, Sakata R, Yoshizumi A, Kimura S et al. Molecular characterization of extraintestinal Escherichia coli isolates in Japan: relationship between sequence types and mutation patterns of quinolone resistance-determining regions analyzed by pyrosequencing. J Clin Microbiol 2013;51:1692–1698 [CrossRef][PubMed]
    [Google Scholar]
  17. Guillard T, Duval V, Moret H, Brasme L, Vernet-Garnier V et al. Rapid detection of aac(6')-Ib-cr quinolone resistance gene by pyrosequencing. J Clin Microbiol 2010;48:286–289 [CrossRef][PubMed]
    [Google Scholar]
  18. Brisse S, Milatovic D, Fluit AC, Verhoef J, Martin N et al. Comparative in vitro activities of ciprofloxacin, clinafloxacin, gatifloxacin, levofloxacin, moxifloxacin, and trovafloxacin against Klebsiella pneumoniae, Klebsiella oxytoca, Enterobacter cloacae, and Enterobacter aerogenes clinical isolates with alterations in GyrA and ParC proteins. Antimicrob Agents Chemother 1999;43:2051–2055[PubMed]
    [Google Scholar]
  19. Versalovic J, Koeuth T, Lupski JR. Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res 1991;19:6823–6831 [CrossRef][PubMed]
    [Google Scholar]
  20. Diancourt L, Passet V, Verhoef J, Grimont PA, Brisse S. Multilocus sequence typing of Klebsiella pneumoniae nosocomial isolates. J Clin Microbiol 2005;43:4178–4182 [CrossRef][PubMed]
    [Google Scholar]
  21. Hawkey PM. Prevalence and clonality of extended-spectrum β-lactamases in Asia. Clin Microbiol Infect 2008;14:159–165 [CrossRef][PubMed]
    [Google Scholar]
  22. Bonnet R. Growing group of extended-spectrum β-lactamases: the CTX-M enzymes. Antimicrob Agents Chemother 2004;48:1–14 [CrossRef][PubMed]
    [Google Scholar]
  23. Lee MY, Ko KS, Kang CI, Chung DR, Peck KR et al. High prevalence of CTX-M-15-producing Klebsiella pneumoniae isolates in Asian countries: diverse clones and clonal dissemination. Int J Antimicrob Agents 2011;38:160–163 [CrossRef][PubMed]
    [Google Scholar]
  24. Okade H, Nakagawa S, Sakagami T, Hisada H, Nomura N et al. Characterization of plasmid-mediated quinolone resistance determinants in Klebsiella pneumoniae and Escherichia coli from Tokai, Japan. J Infect Chemother 2014;20:778–783 [CrossRef][PubMed]
    [Google Scholar]
  25. Yanagihara K, Kadota J, Aoki N, Matsumoto T, Yoshida M et al. Nationwide surveillance of bacterial respiratory pathogens conducted by the surveillance committee of Japanese Society of Chemotherapy, the Japanese Association for Infectious Diseases, and the Japanese Society for Clinical Microbiology in 2010: general view of the pathogens' antibacterial susceptibility. J Infect Chemother 2015;21:410–420 [CrossRef][PubMed]
    [Google Scholar]
  26. Vila J, Ruiz J, Marco F, Barcelo A, Goñi P et al. Association between double mutation in gyrA gene of ciprofloxacin-resistant clinical isolates of Escherichia coli and MICs. Antimicrob Agents Chemother 1994;38:2477–2479 [CrossRef][PubMed]
    [Google Scholar]
  27. Aathithan S, French GL. Prevalence and role of efflux pump activity in ciprofloxacin resistance in clinical isolates of Klebsiella pneumoniae. Eur J Clin Microbiol Infect Dis 2011;30:745–752 [CrossRef][PubMed]
    [Google Scholar]
  28. Damjanova I, Tóth A, Pászti J, Hajbel-Vékony G, Jakab M et al. Expansion and countrywide dissemination of ST11, ST15 and ST147 ciprofloxacin-resistant CTX-M-15-type β-lactamase-producing Klebsiella pneumoniae epidemic clones in Hungary in 2005-the new 'MRSAs'?. J Antimicrob Chemother 2008;62:978–985 [CrossRef][PubMed]
    [Google Scholar]
  29. Bratu S, Landman D, George A, Salvani J, Quale J. Correlation of the expression of acrB and the regulatory genes marA, soxS and ramA with antimicrobial resistance in clinical isolates of Klebsiella pneumoniae endemic to New York City. J Antimicrob Chemother 2009;64:278–283 [CrossRef][PubMed]
    [Google Scholar]
  30. Rodrigues C, Machado E, Ramos H, Peixe L, Novais Â. Expansion of ESBL-producing Klebsiella pneumoniae in hospitalized patients: a successful story of international clones (ST15, ST147, ST336) and epidemic plasmids (IncR, IncFIIK). Int J Med Microbiol 2014;304:1100–1108 [CrossRef][PubMed]
    [Google Scholar]
  31. Wang G, Huang T, Surendraiah PK, Wang K, Komal R et al. CTX-M β-lactamase-producing Klebsiella pneumoniae in suburban New York city, New York, USA. Emerg Infect Dis 2013;19:1803–1810 [CrossRef][PubMed]
    [Google Scholar]
  32. Cantón R, Morosini MI, Martín O, De La Maza OM, De La Pedrosa EG. IRT and CMT β-lactamases and inhibitor resistance. Clin Microbiol Infect 2008;14:53–62 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.000577
Loading
/content/journal/jmm/10.1099/jmm.0.000577
Loading

Data & Media loading...

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