1887

Abstract

Our aim was to identify long-term β-lactam resistance trends in local isolates, which are a common cause of sepsis in Western Australia. We studied three collections of isolates from Western Australia between 1977 and 2015 comprising contemporary blood culture ( = 98), multiresistant ( = 21) and historical ( = 50) isolates. Antimicrobial resistance was determined by Clinical and Laboratory Standards Institute agar dilution methods. PCR DNA sequencing identified β-lactamase variants and porin mutations contributing to β-lactam resistance. Isolates were genotyped by PFGE, multilocus sequence typing and a variable number tandem repeat method. From 1989 onwards, we detected the SHV-2a extended-spectrum β-lactamase (ESBL) in ceftriaxone-resistant isolates, and in ceftazidime- and aztreonam-resistant isolates from 1993. Ceftriaxone, ceftazidime and aztreonam resistance persisted, with types becoming the dominant ESBLs by 2010. CTX-M-15 was encountered in both multiresistant and blood culture isolates. Meropenem resistance was detected for the first time in 2011 in a locally isolated -positive . We found sequence types ST23 and ST86 that occurred in multiple isolates from invasive infections. ST86 was the most common and maintained a high degree (90 %) of similarity by PFGE since 1977. Ceftazidime-resistant sequence types have caused invasive infections in Western Australia since 1993. Invasive isolates producing CTX-M-14 and CTX-M-15 appeared in Western Australia during the last decade, before the appearance of carbapenemases. The diversity of β-lactam resistance and β-lactamase resistance mechanisms in Western Australian has increased since ESBLs were first described locally.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.000242
2016-05-01
2019-10-18
Loading full text...

Full text loading...

/deliver/fulltext/jmm/65/5/429.html?itemId=/content/journal/jmm/10.1099/jmm.0.000242&mimeType=html&fmt=ahah

References

  1. Arakawa Y. , Ohta M. , Kido N. , Mori M. , Ito H. , Komatsu T. , Fujii Y. , Kato N. . ( 1989;). Chromosomal beta-lactamase of Klebsiella oxytoca, a new class A enzyme that hydrolyzes broad-spectrum beta-lactam antibiotics. Antimicrob Agents Chemother 33: 63–70 [CrossRef] [PubMed].
    [Google Scholar]
  2. Bialek-Davenet S. , Criscuolo A. , Ailloud F. , Passet V. , Jones L. , Delannoy-Vieillard A.-S. , Garin B. , Le Hello S. , Arlet G. , other authors . ( 2014;). Genomic definition of hypervirulent and multidrug-resistant Klebsiella pneumoniae clonal groups. Emerg Infect Dis 20: 1812–1820 [CrossRef] [PubMed].
    [Google Scholar]
  3. Bochud P.-Y. , Bonten M. , Marchetti O. , Calandra T. . ( 2004;). Antimicrobial therapy for patients with severe sepsis and septic shock: an evidence-based review. Crit Care Med 32: (Suppl), S495–S512 [CrossRef] [PubMed].
    [Google Scholar]
  4. Cantón R. , González-Alba J. M. , Galán J.-C. . ( 2012;). CTX-M enzymes: origin and diffusion. Front Microbiol 3: 110 [PubMed].[CrossRef]
    [Google Scholar]
  5. Castanheira M. , Deshpande L. M. , Mathai D. , Bell J. M. , Jones R. N. , Mendes R. E. . ( 2011;). Early dissemination of NDM-1- and OXA-181-producing Enterobacteriaceae in Indian hospitals: report from the SENTRY Antimicrobial Surveillance Program, 2006–2007. Antimicrob Agents Chemother 55: 1274–1278 [CrossRef] [PubMed].
    [Google Scholar]
  6. Chang L. W. K. , Buising K. L. , Jeremiah C. J. , Cronin K. , Poy Lorenzo Y. S. , Howden B. P. , Kwong J. , Cocks J. , Blood A. , other authors . ( 2015;). Managing a nosocomial outbreak of carbapenem-resistant Klebsiella pneumoniae: an early Australian hospital experience. Intern Med J 45: 1037–1043 [CrossRef] [PubMed].
    [Google Scholar]
  7. Chung D. R. , Lee H. R. , Lee S. S. , Kim S. W. , Chang H.-H. , Jung S.-I. , Oh M.-D. , Ko K. S. , Kang C.-I. , other authors . ( 2008;). Evidence for clonal dissemination of the serotype K1 Klebsiella pneumoniae strain causing invasive liver abscesses in Korea. J Clin Microbiol 46: 4061–4063 [CrossRef] [PubMed].
    [Google Scholar]
  8. CLSI ( 2011;). Performance Standards for Antimicrobial Susceptibility Testing; 21st Informational Supplement Clinical and Laboratory Standards Institute;.
    [Google Scholar]
  9. Dallenne C. , Da Costa A. , Decré D. , Favier C. , Arlet G. . ( 2010;). Development of a set of multiplex PCR assays for the detection of genes encoding important beta-lactamases in Enterobacteriaceae. J Antimicrob Chemother 65: 490–495 [CrossRef] [PubMed].
    [Google Scholar]
  10. Decré D. , Verdet C. , Emirian A. , Le Gourrierec T. , Petit J.-C. , Offenstadt G. , Maury E. , Brisse S. , Arlet G. . ( 2011;). Emerging severe and fatal infections due to Klebsiella pneumoniae in two university hospitals in France. J Clin Microbiol 49: 3012–3014 [CrossRef] [PubMed].
    [Google Scholar]
  11. Diancourt L. , Passet V. , Verhoef J. , Grimont P. A. D. , Brisse S. . ( 2005;). Multilocus sequence typing of Klebsiella pneumoniae nosocomial isolates. J Clin Microbiol 43: 4178–4182 [CrossRef] [PubMed].
    [Google Scholar]
  12. Dulku G. , Tibballs J. . ( 2014;). Cryptogenic invasive Klebsiella pneumoniae liver abscess syndrome (CIKPLA) in Western Australia?. Australas Med J 7: 436–440 [CrossRef] [PubMed].
    [Google Scholar]
  13. Espedido B. A. , Steen J. A. , Ziochos H. , Grimmond S. M. , Cooper M. A. , Gosbell I. B. , van Hal S. J. , Jensen S. O. . ( 2013;). Whole genome sequencing analysis of the first Australian OXA-48-producing outbreak-associated Klebsiella pneumoniae isolates: the resistome and in vivo evolution. PLoS One 8: e59920 [CrossRef] [PubMed].
    [Google Scholar]
  14. Fang C.-T. , Chuang Y.-P. , Shun C.-T. , Chang S.-C. , Wang J.-T. . ( 2004;). A novel virulence gene in Klebsiella pneumoniae strains causing primary liver abscess and septic metastatic complications. J Exp Med 199: 697–705 [CrossRef] [PubMed].
    [Google Scholar]
  15. Fang H. , Ataker F. , Hedin G. , Dornbusch K. . ( 2008;). Molecular epidemiology of extended-spectrum beta-lactamases among Escherichia coli isolates collected in a Swedish hospital and its associated health care facilities from 2001 to 2006. J Clin Microbiol 46: 707–712 [CrossRef] [PubMed].
    [Google Scholar]
  16. Francisco A. P. , Bugalho M. , Ramirez M. , Carriço J. A. . ( 2009;). Global optimal eBURST analysis of multilocus typing data using a graphic matroid approach. BMC Bioinformatics 10: 152 [CrossRef] [PubMed].
    [Google Scholar]
  17. Gomez-Simmonds A. , Greenman M. , Sullivan S. B. , Tanner J. P. , Sowash M. G. , Whittier S. , Uhlemann A.-C. . ( 2015;). Population structure of Klebsiella pneumoniae causing bloodstream infections at a New York City tertiary care hospital: diversification of multidrug-resistant isolates. J Clin Microbiol 53: 2060–2067 [CrossRef] [PubMed].
    [Google Scholar]
  18. Holt K. E. , Wertheim H. , Zadoks R. N. , Baker S. , Whitehouse C. A. , Dance D. , Jenney A. , Connor T. R. , Hsu L. Y. , other authors . ( 2015;). Genomic analysis of diversity, population structure, virulence, and antimicrobial resistance in Klebsiella pneumoniae, an urgent threat to public health. Proc Natl Acad Sci U S A 112: E3574–E3581 [CrossRef] [PubMed].
    [Google Scholar]
  19. Inglis T. J. J. , Hodge M. , Ketharanathan S. . ( 2008;). A hospital-wide study of the impact of introducing a personal data assistant-augmented blood culture round. J Med Microbiol 57: 43–49 [CrossRef] [PubMed].
    [Google Scholar]
  20. Ko W.-C. , Paterson D. L. , Sagnimeni A. J. , Hansen D. S. , Von Gottberg A. , Mohapatra S. , Casellas J. M. , Goossens H. , Mulazimoglu L. , other authors . ( 2002;). Community-acquired Klebsiella pneumoniae bacteremia: global differences in clinical patterns. Emerg Infect Dis 8: 160–166 [CrossRef] [PubMed].
    [Google Scholar]
  21. Landman D. , Bratu S. , Quale J. . ( 2009;). Contribution of OmpK36 to carbapenem susceptibility in KPC-producing Klebsiella pneumoniae . J Med Microbiol 58: 1303–1308 [CrossRef] [PubMed].
    [Google Scholar]
  22. 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 Chemother 59: 165–174 [CrossRef] [PubMed].
    [Google Scholar]
  23. Maslow J. N. , Slutsky A. M. , Arbeit R. D. . ( 1993;). Application of pulsed-field gel electrophoresis to molecular epidemiology. . In Diagnostic Molecular Microbiology: Principles and Applications, pp. 563–572. Edited by Persing D. H. , Smith T. F. , Tenover F. C. , White T. J. . Washington, DC: American Society for Microbiology;.
    [Google Scholar]
  24. Mulgrave L. , Attwood P. V. . ( 1993;). Characterization of an SHV-5 related extended broad-spectrum beta-lactamase in Enterobacteriaceae from Western Australia. Pathology 25: 71–75 [CrossRef] [PubMed].
    [Google Scholar]
  25. Paterson D. L. , Ko W.-C. , Von Gottberg A. , Mohapatra S. , Casellas J. M. , Goossens H. , Mulazimoglu L. , Trenholme G. , Klugman K. P. , other authors . ( 2004;). Antibiotic therapy for Klebsiella pneumoniae bacteremia: implications of production of extended-spectrum beta-lactamases. Clin Infect Dis 39: 31–37 [CrossRef] [PubMed].
    [Google Scholar]
  26. Peirano G. , Laupland K. B. , Gregson D. B. , Pitout J. D. D. . ( 2011;). Colonization of returning travelers with CTX-M-producing Escherichia coli . J Travel Med 18: 299–303 [CrossRef] [PubMed].
    [Google Scholar]
  27. Pérez-Pérez F. J. , Hanson N. D. . ( 2002;). Detection of plasmid-mediated AmpC β-lactamase genes in clinical isolates by using multiplex PCR. J Clin Microbiol 40: 2153–2162 [CrossRef] [PubMed].
    [Google Scholar]
  28. Queenan A. M. , Bush K. . ( 2007;). Carbapenemases: the versatile β-lactamases. Clin Microbiol Rev 20: 440–458 [CrossRef] [PubMed].
    [Google Scholar]
  29. Rhomberg P. R. , Jones R. N. . ( 2009;). Summary trends for the Meropenem Yearly Susceptibility Test Information Collection Program: a 10-year experience in the United States (1999–2008). Diagn Microbiol Infect Dis 65: 414–426 [CrossRef] [PubMed].
    [Google Scholar]
  30. Rogers B. A. , Kennedy K. J. , Sidjabat H. E. , Jones M. , Collignon P. , Paterson D. L. . ( 2012;). Prolonged carriage of resistant E. coli by returned travellers: clonality, risk factors and bacterial characteristics. Eur J Clin Microbiol Infect Dis 31: 2413–2420 [CrossRef] [PubMed].
    [Google Scholar]
  31. Shin S. H. , Kim S. , Kim J. Y. , Lee S. , Um Y. , Oh M.-K. , Kim Y.-R. , Lee J. , Yang K.-S. . ( 2012;). Complete genome sequence of Klebsiella oxytoca KCTC 1686, used in production of 2,3-butanediol. J Bacteriol 194: 2371–2372 [CrossRef] [PubMed].
    [Google Scholar]
  32. Sidjabat H. E. , Townell N. , Nimmo G. R. , George N. M. , Robson J. , Vohra R. , Davis L. , Heney C. , Paterson D. L. . ( 2015;). Dominance of IMP-4-producing Enterobacter cloacae among carbapenemase-producing Enterobacteriaceae in Australia. Antimicrob Agents Chemother 59: 4059–4066 [CrossRef] [PubMed].
    [Google Scholar]
  33. Siu L. K. , Fung C.-P. , Chang F.-Y. , Lee N. , Yeh K.-M. , Koh T.-H. , Ip M. . ( 2011;). Molecular typing and virulence analysis of serotype K1 Klebsiella pneumoniae strains isolated from liver abscess patients and stool samples from noninfectious subjects in Hong Kong, Singapore, and Taiwan. J Clin Microbiol 49: 3761–3765 [CrossRef] [PubMed].
    [Google Scholar]
  34. Song W. , Lee H. , Lee K. , Jeong S. H. , Bae I. K. , Kim J. S. , Kwak H. S. . ( 2009;). CTX-M-14 and CTX-M-15 enzymes are the dominant type of extended-spectrum β-lactamase in clinical isolates of Escherichia coli from Korea. J Med Microbiol 58: 261–266 [CrossRef] [PubMed].
    [Google Scholar]
  35. Tai A. Y. C. , Stuart R. L. , Sidjabat H. E. , Lemoh C. N. , Rogers B. A. , Graham M. , Paterson D. L. , Korman T. M. . ( 2015;). Local acquisition and nosocomial transmission of Klebsiella pneumoniae harbouring the bla NDM-1 gene in Australia. Med J Aust 202: 270–271 [CrossRef] [PubMed].
    [Google Scholar]
  36. Tsai Y. K. , Fung C. P. , Lin J. C. , Chen J. H. , Chang F. Y. , Chen T. L. , Siu L. K. . ( 2011;). Klebsiella pneumoniae outer membrane porins OmpK35 and OmpK36 play roles in both antimicrobial resistance and virulence. Antimicrob Agents Chemother 55: 1485–1493 [CrossRef] [PubMed].
    [Google Scholar]
  37. Turnidge J. , Gottlieb T. , Bell J. . ( 2014a;). Enterobacteriaceae Sepsis Outcome Programme (EnSOP) 2013 Antimicrobial Susceptibility Report. http://www.agargroup.org/files/AGAR%20EnSOP13%20Web%20Report%20FINAL%202.pdf.
  38. Turnidge J. D. , Gottlieb T. , Mitchell D. H. , Coombs G. W. , Pearson J. C. , Bell J. M. , Australian Group on Antimicrobial Resistance . ( 2014b;). Hospital-onset Gram-negative Surveillance Program annual report, 2011. Commun Dis Intell Q Rep 38: E49–E53 [PubMed].
    [Google Scholar]
  39. Turton J. F. , Perry C. , Elgohari S. , Hampton C. V. . ( 2010;). PCR characterization and typing of Klebsiella pneumoniae using capsular type-specific, variable number tandem repeat and virulence gene targets. J Med Microbiol 59: 541–547 [CrossRef] [PubMed].
    [Google Scholar]
  40. Wiegand I. , Hilpert K. , Hancock R. E. W. . ( 2008;). Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat Protoc 3: 163–175 [CrossRef] [PubMed].
    [Google Scholar]
  41. Woodford N. , Tierno P.M., Jr , Young K. , Tysall L. , Palepou M.-F.I. , Ward E. , Painter R. E. , Suber D. F. , Shungu D. , other authors . ( 2004;). Outbreak of Klebsiella pneumoniae producing a new carbapenem-hydrolyzing class A beta-lactamase, KPC-3, in a New York Medical Center. Antimicrob Agents Chemother 48: 4793–4799 [CrossRef] [PubMed].
    [Google Scholar]
  42. Yu V. L. , Hansen D. S. , Ko W.-C. , Sagnimeni A. , Klugman K. P. , von Gottberg A. , Goossens H. , Wagener M. M. , Benedí V. J. , International Klebseilla Study Group . ( 2007;). Virulence characteristics of Klebsiella and clinical manifestations of K. pneumoniae bloodstream infections. Emerg Infect Dis 13: 986–993 [CrossRef] [PubMed].
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.000242
Loading
/content/journal/jmm/10.1099/jmm.0.000242
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