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Characterization of carbapenem-resistant Escherichia coli and Klebsiella pneumoniae from a healthcare region in Hong Kong

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Abstract

Carbapenem-resistant Enterobacteriaceae represents a major public health issue. This study investigated the clonality and resistance mechanisms of 92 carbapenem-resistant E. coli (n = 21) and K. pneumoniae (n = 71) isolates collected consecutively from clinical specimens and patients at high risk of carriage between 2010 and 2012 in a healthcare region in Hong Kong. Combined disk tests (CDTs) and the Carba NP test were used for phenotypic detection of carbapenemases. PCR assays were used to detect carbapenemase genes. All isolates were intermediate or resistant to at least one carbapenem. Nine (9.8 %) isolates were genotypic carbapenemase producers and included six K. pneumoniae (one ST1306/bla IMP-4, one ST889/bla IMP-4, two ST11/bla KPC-2, one ST258/bla KPC-2, one ST483/bla NDM-1) and three E. coli (one ST131/bla IMP-4, two ST744/ bla NDM-1) isolates. All nine isolates carrying carbapenemase genes could be detected by the CDTs and the Carba NP test. PCR identified bla CTX-M and bla AmpC alone or in combination in 77.8 % (7/9) and 96.4 % (80/83) of the carbapenemase-producers and non-producers, respectively. Porin loss was detected in 22.2 % (2/9) and 59.0 % (49/83) of the carbapenemase-producers and non-producers, respectively. Overall, the E. coli clones were diverse (14 different STs), but 36.6 % (26/71) of the K. pneumoniae isolates belonged to ST11. In conclusion, the prevalence of carbapenemases among carbapenem-nonsusceptible E. coli and K. pneumoniae remained low in Hong Kong. Porin loss combined with AmpC and/or CTX-M type ESBL was the major mechanism of carbapenem resistance in the study population.

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References

  1. Tzouvelekis LS, Markogiannakis A, Psichogiou M, Tassios PT, Daikos GL (2012) Carbapenemases in Klebsiella pneumoniae and other Enterobacteriaceae: an evolving crisis of global dimensions. Clin Microbiol Rev 25(4):682–707

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  2. Grundmann H, Livermore DM, Giske CG, Canton R, Rossolini GM, Campos J, Vatopoulos A, Gniadkowski M, Toth A, Pfeifer Y, Jarlier V, Carmeli Y (2010) Carbapenem-non-susceptible Enterobacteriaceae in Europe: conclusions from a meeting of national experts. Euro Surveill 15(46):1–13

    Google Scholar 

  3. Muscarella LF (2014) Risk of transmission of carbapenem-resistant Enterobacteriaceae and related "superbugs" during gastrointestinal endoscopy. World J Gastrointest Endosc 6(10):457–474

    Article  PubMed Central  PubMed  Google Scholar 

  4. Hrabak J, Chudackova E, Papagiannitsis CC (2014) Detection of carbapenemases in Enterobacteriaceae: a challenge for diagnostic microbiological laboratories. Clin Microbiol Infect 20(9):839–853

    Article  CAS  PubMed  Google Scholar 

  5. Ho PL, Li Z, Lo WU, Cheung YY, Lin CH, Sham PC, Chi-Chung C, V, Ng TK, Que TL, Chow KH (2012) Identification and characterization of a novel incompatibility group X3 plasmid carrying bla NDM-1 in Enterobacteriaceae isolates with epidemiological links to multiple geographical areas in China. Emerg Microbes Infect 1(11): e39

  6. Espedido BA, Partridge SR, Iredell JR (2008) bla IMP-4 in different genetic contexts in Enterobacteriaceae isolates from Australia. Antimicrob Agents Chemother 52(8):2984–2987

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  7. Ho PL, Lo WU, Chan J, Cheung YY, Chow KH, Yam WC, Lin CH, Que TL (2014) pIMP-PH114 carrying bla IMP-4 in a Klebsiella pneumoniae strain is closely related to other multidrug-resistant IncA/C2 plasmids. Curr Microbiol 68(2):227–232

    Article  CAS  PubMed  Google Scholar 

  8. Wang JT, Wu UI, Lauderdale TL, Chen MC, Li SY, Hsu LY, Chang SC (2015) Carbapenem-nonsusceptible Enterobacteriaceae in Taiwan. PLoS One 10(3):e0121668

    Article  PubMed Central  PubMed  Google Scholar 

  9. Cheng VC, Chan JF, Wong SC, Chen JH, Tai JW, Yan MK, Kwan GS, Tse H, To KK, Ho PL, Yuen KY (2013) Proactive infection control measures to prevent nosocomial transmission of carbapenem-resistant Enterobacteriaceae in a non-endemic area. Chin Med J (Engl ) 126(23):4504–4509

    Google Scholar 

  10. Ho PL, Cheung YY, Lo WU, Li Z, Chow KH, Lin CH, Chan JF, Cheng VC (2013) Molecular characterization of an atypical IncX3 plasmid pKPC-NY79 carrying bla KPC-2 in a Klebsiella pneumoniae. Curr Microbiol 67(4):493–498

    Article  CAS  PubMed  Google Scholar 

  11. CLSI (2015) Performance standards for antimicrobial susceptibility testing: twenty-fifth informational supplement M100-S25. CLSI, Wayne, PA, USA

  12. Ho PL, Lo WU, Yeung MK, Lin CH, Chow KH, Ang I, Tong AH, Bao JY, Lok S, Lo JY (2011) Complete sequencing of pNDM-HK encoding NDM-1 carbapenemase from a multidrug-resistant Escherichia coli strain isolated in Hong Kong. PLoS One 6(3):e17989

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  13. Maurer FP, Castelberg C, Quiblier C, Bloemberg GV, Hombach M (2015) Evaluation of carbapenemase screening and confirmation tests with Enterobacteriaceae and development of a practical diagnostic algorithm. J Clin Microbiol 53(1):95–104

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Perez-Perez FJ, Hanson ND (2002) Detection of plasmid-mediated AmpC beta-lactamase genes in clinical isolates by using multiplex PCR. J Clin Microbiol 40(6):2153–2162

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  15. Clermont O, Christenson JK, Denamur E, Gordon DM (2013) The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environ Microbiol Rep 5(1):58–65

    Article  CAS  PubMed  Google Scholar 

  16. Diancourt L, Passet V, Verhoef J, Grimont PA, Brisse S (2005) Multilocus sequence typing of Klebsiella pneumoniae nosocomial isolates. J Clin Microbiol 43(8):4178–4182

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Wirth T, Falush D, Lan R, Colles F, Mensa P, Wieler LH, Karch H, Reeves PR, Maiden MC, Ochman H, Achtman M (2006) Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 60(5):1136–1151

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  18. Spratt BG, Hanage WP, Li B, Aanensen DM, Feil EJ (2004) Displaying the relatedness among isolates of bacterial species -- the eBURST approach. FEMS Microbiol Lett 241(2):129–134

    Article  CAS  PubMed  Google Scholar 

  19. Hernandez-Alles S, Alberti S, Alvarez D, Domenech-Sanchez A, Martinez-Martinez L, Gil J, Tomas JM, Benedi VJ (1999) Porin expression in clinical isolates of Klebsiella pneumoniae. Microbiology 145(Pt 3):673–679

    Article  CAS  PubMed  Google Scholar 

  20. Cheng VC, Wong SC, Ho PL, Yuen KY (2015) Strategic measures for the control of surging antimicrobial resistance in Hong Kong and mainland of China. Emerg Microbes Infect 4(2):e8

    Article  PubMed Central  PubMed  Google Scholar 

  21. Ho PL, Chu YP, Lo WU, Chow KH, Law PY, Tse CW, Ng TK, Cheng VC, Que TL (2015) High prevalence of Escherichia coli sequence type 131 among antimicrobial-resistant E. coli isolates from geriatric patients. J Med Microbiol 64(Pt 3):243–247

    Article  CAS  PubMed  Google Scholar 

  22. Mathers AJ, Peirano G, Pitout JD (2015) The role of epidemic resistance plasmids and international high-risk clones in the spread of multidrug-resistant Enterobacteriaceae. Clin Microbiol Rev 28(3):565–591

    Article  PubMed  Google Scholar 

  23. Pfeifer Y, Cullik A, Witte W (2010) Resistance to cephalosporins and carbapenems in Gram-negative bacterial pathogens. Int J Med Microbiol 300(6):371–379

    Article  CAS  PubMed  Google Scholar 

  24. Gallagher LC, Roundtree SS, Lancaster DP, Rudin SD, Bard JD, Roberts AL, Marshall SH, Bonomo RA, Sullivan KV (2015) Performance of the CLSI Carba NP and the Rosco Carb Screen Assays Using North American Carbapenemase-Producing Enterobacteriaceae and Pseudomonas aeruginosa Isolates. J Clin Microbiol 53(10):3370–3373

    Article  PubMed  Google Scholar 

  25. Dortet L, Brechard L, Cuzon G, Poirel L, Nordmann P (2014) Strategy for rapid detection of carbapenemase-producing Enterobacteriaceae. Antimicrob Agents Chemother 58(4):2441–2445

    Article  PubMed Central  PubMed  Google Scholar 

  26. Osei SJ, Govinden U, Essack SY (2015) Review of established and innovative detection methods for carbapenemase-producing Gram-negative bacteria. J Appl Microbiol 119(5):1219–1233

    Article  Google Scholar 

  27. Chong PM, McCorrister SJ, Unger MS, Boyd DA, Mulvey MR, Westmacott GR (2015) MALDI-TOF MS detection of carbapenemase activity in clinical isolates of Enterobacteriaceae spp., Pseudomonas aeruginosa, and Acinetobacter baumannii compared against the Carba-NP assay. J Microbiol Methods 111:21–23

    Article  CAS  PubMed  Google Scholar 

  28. Tijet N, Boyd D, Patel SN, Mulvey MR, Melano RG (2013) Evaluation of the Carba NP test for rapid detection of carbapenemase-producing Enterobacteriaceae and Pseudomonas aeruginosa. Antimicrob Agents Chemother 57(9):4578–4580

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  29. Osterblad M, Hakanen AJ, Jalava J (2014) Evaluation of the Carba NP test for carbapenemase detection. Antimicrob Agents Chemother 58(12):7553–7556

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  30. Papagiannitsis CC, Studentova V, Izdebski R, Oikonomou O, Pfeifer Y, Petinaki E, Hrabak J (2015) Matrix-assisted laser desorption ionization-time of flight mass spectrometry meropenem hydrolysis assay with NH4HCO3, a reliable tool for direct detection of carbapenemase activity. J Clin Microbiol 53(5):1731–1735

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  31. Garcia-Sureda L, Juan C, Domenech-Sanchez A, Alberti S (2011) Role of Klebsiella pneumoniae LamB Porin in antimicrobial resistance. Antimicrob Agents Chemother 55(4):1803–1805

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  32. Kaczmarek FM, Dib-Hajj F, Shang W, Gootz TD (2006) High-level carbapenem resistance in a Klebsiella pneumoniae clinical isolate is due to the combination of bla ACT-1 beta-lactamase production, porin OmpK35/36 insertional inactivation, and down-regulation of the phosphate transport porin phoe. Antimicrob Agents Chemother 50(10):3396–3406

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the Health and Medical Research Fund of the Food and Health Bureau of the Government of the HKSAR and the RGC Collaborative Research Fund Project on Syndromic Surveillance and Modelling for Infectious Diseases (CityU8/CRF/12G).

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Authors and Affiliations

  1. Department of Microbiology, Queen Mary Hospital, University of Hong Kong, Pokfulam Road, Pokfulam, Hong Kong, SAR, People’s Republic of China

    P. L. Ho, Y. Y. Cheung, Y. Wang, W. U. Lo, E. L. Y. Lai, K. H. Chow & V. C. C. Cheng

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  1. P. L. Ho
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  2. Y. Y. Cheung
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  3. Y. Wang
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  4. W. U. Lo
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  6. K. H. Chow
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  7. V. C. C. Cheng
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Correspondence to P. L. Ho.

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Ho, P.L., Cheung, Y.Y., Wang, Y. et al. Characterization of carbapenem-resistant Escherichia coli and Klebsiella pneumoniae from a healthcare region in Hong Kong. Eur J Clin Microbiol Infect Dis 35, 379–385 (2016). https://doi.org/10.1007/s10096-015-2550-3

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  • DOI: https://doi.org/10.1007/s10096-015-2550-3

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