1887

Abstract

Carbapenem-resistant (CRE) are a serious public health threat because of their rapid dissemination. To determine the epidemiological and genetic characteristics of CRE infections in Thailand, we performed whole-genome sequencing of 577 carbapenem-resistant isolates and 170 carbapenem-resistant isolates from hospitals across the nation. The four most prevalent carbapenemase genes harboured by these bacteria were , , and . The gene was identified in diverse sequence types. The gene was identified almost exclusively in . The genes , , and co-carriage of and were found in specific sequence types from certain provinces. Replicon typing revealed the diverse backbones of - and -harbouring plasmids and successful expansion of -harbouring IncN2-type plasmids. Core-genome single-nucleotide polymorphism analysis suggested that -, -, -, and co-carriage of and -associated sub-clonal lineages have recently predominated in the provinces from where these isolates were isolated. Thus, we demonstrate genotype-dependent dissemination of CRE in Thailand, which is helpful for establishing infection-control strategies in CRE-endemic areas.

Funding
This study was supported by the:
  • Japan Agency for Medical Research and Development (Award 20wm0125010h0001)
    • Principle Award Recipient: HamadaShigeyuki
  • Japan Agency for Medical Research and Development (Award 21wm0225013h0502)
    • Principle Award Recipient: HamadaShigeyuki
  • Japan Agency for Medical Research and Development (Award 20wm0225013h0001)
    • Principle Award Recipient: HamadaShigeyuki
  • J-GRID (Award JP18fm0108003)
    • Principle Award Recipient: HamadaShigeyuki
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000797
2022-04-19
2024-05-13
Loading full text...

Full text loading...

/deliver/fulltext/mgen/8/4/mgen000797.html?itemId=/content/journal/mgen/10.1099/mgen.0.000797&mimeType=html&fmt=ahah

References

  1. Takeuchi D, Kerdsin A, Akeda Y, Sugawara Y, Sakamoto N et al. Nationwide surveillance in Thailand revealed genotype-dependent dissemination of carbapenem-resistant Enterobacterales. Figshare 2022 [View Article]
    [Google Scholar]
  2. Papp-Wallace KM, Endimiani A, Taracila MA, Bonomo RA. Carbapenems: past, present, and future. Antimicrob Agents Chemother 2011; 55:4943–4960 [View Article] [PubMed]
    [Google Scholar]
  3. Temkin E, Adler A, Lerner A, Carmeli Y. Carbapenem-resistant Enterobacteriaceae: biology, epidemiology, and management. Ann N Y Acad Sci 2014; 1323:22–42 [View Article] [PubMed]
    [Google Scholar]
  4. Nordmann P, Poirel L. Epidemiology and diagnostics of carbapenem resistance in gram-negative bacteria. Clin Infect Dis 2019; 69:S521–S528 [View Article] [PubMed]
    [Google Scholar]
  5. Sidjabat HE, Silveira FP, Potoski BA, Abu-Elmagd KM, Adams-Haduch JM et al. Interspecies spread of Klebsiella pneumoniae carbapenemase gene in a single patient. Clin Infect Dis 2009; 49:1736–1738 [View Article] [PubMed]
    [Google Scholar]
  6. Mathers AJ, Cox HL, Kitchel B, Bonatti H, Brassinga AKC et al. Molecular dissection of an outbreak of carbapenem-resistant enterobacteriaceae reveals Intergenus KPC carbapenemase transmission through a promiscuous plasmid. mBio 2011; 2:e00204–11 [View Article] [PubMed]
    [Google Scholar]
  7. Conlan S, Thomas PJ, Deming C, Park M, Lau AF et al. Single-molecule sequencing to track plasmid diversity of hospital-associated carbapenemase-producing Enterobacteriaceae. Sci Transl Med 2014; 6:254 [View Article] [PubMed]
    [Google Scholar]
  8. Pitout JDD, Nordmann P, Poirel L. Carbapenemase-Producing Klebsiella pneumoniae, a key pathogen set for global nosocomial dominance. Antimicrob Agents Chemother 2015; 59:5873–5884 [View Article] [PubMed]
    [Google Scholar]
  9. van Duin D, Doi Y. The global epidemiology of carbapenemase-producing Enterobacteriaceae. Virulence 2017; 8:460–469 [View Article] [PubMed]
    [Google Scholar]
  10. Hsu L-Y, Apisarnthanarak A, Khan E, Suwantarat N, Ghafur A et al. Carbapenem-resistant Acinetobacter baumannii and Enterobacteriaceae in South and Southeast Asia. Clin Microbiol Rev 2017; 30:1–22 [View Article] [PubMed]
    [Google Scholar]
  11. Tran DM, Larsson M, Olson L, Hoang NTB, Le NK et al. High prevalence of colonisation with carbapenem-resistant Enterobacteriaceae among patients admitted to Vietnamese hospitals: Risk factors and burden of disease. J Infect 2019; 79:115–122 [View Article] [PubMed]
    [Google Scholar]
  12. Wyres KL, Nguyen TNT, Lam MMC, Judd LM, van Vinh Chau N et al. Genomic surveillance for hypervirulence and multi-drug resistance in invasive Klebsiella pneumoniae from South and Southeast Asia. Genome Med 2020; 12:11 [View Article] [PubMed]
    [Google Scholar]
  13. Sugawara Y, Akeda Y, Sakamoto N, Takeuchi D, Motooka D et al. Genetic characterization of blaNDM-harboring plasmids in carbapenem-resistant Escherichia coli from Myanmar. PLoS One 2017; 12:e0184720 [View Article] [PubMed]
    [Google Scholar]
  14. Laolerd W, Akeda Y, Preeyanon L, Ratthawongjirakul P, Santanirand P. Carbapenemase-Producing Carbapenem-Resistant Enterobacteriaceae from Bangkok, Thailand, and their detection by the carba NP and modified carbapenem inactivation method tests. Microb Drug Resist 2018; 24:1006–1011 [View Article] [PubMed]
    [Google Scholar]
  15. Sugawara Y, Akeda Y, Hagiya H, Sakamoto N, Takeuchi D et al. Spreading Patterns of NDM-Producing Enterobacteriaceae in clinical and environmental settings in Yangon, Myanmar. Antimicrob Agents Chemother 2019; 63:e01924–e01918 [View Article] [PubMed]
    [Google Scholar]
  16. Paveenkittiporn W, Lyman M, Biedron C, Chea N, Bunthi C et al. Molecular epidemiology of carbapenem-resistant Enterobacterales in Thailand, 2016-2018. Antimicrob Resist Infect Control 2021; 10:88 [View Article] [PubMed]
    [Google Scholar]
  17. Clinical and Laboratory Standards Institute Performance Standard for Antimicrobial Susceptibility Testing; M100-S22 Wayne, PA: 2012
    [Google Scholar]
  18. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article] [PubMed]
    [Google Scholar]
  19. Larsen MV, Cosentino S, Rasmussen S, Friis C, Hasman H et al. Multilocus sequence typing of total-genome-sequenced bacteria. J Clin Microbiol 2012; 50:1355–1361 [View Article] [PubMed]
    [Google Scholar]
  20. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S et al. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 2012; 67:2640–2644 [View Article] [PubMed]
    [Google Scholar]
  21. Carattoli A, Zankari E, García-Fernández A, Voldby Larsen M, Lund O et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother 2014; 58:3895–3903 [View Article] [PubMed]
    [Google Scholar]
  22. Simpson EH. Measurement of Diversity. Nature 1949; 163:688 [View Article]
    [Google Scholar]
  23. Hunter PR, Gaston MA. Numerical index of the discriminatory ability of typing systems: an application of Simpson’s index of diversity. J Clin Microbiol 1988; 26:2465–2466 [View Article] [PubMed]
    [Google Scholar]
  24. Robertson J, Nash JHE. MOB-suite: software tools for clustering, reconstruction and typing of plasmids from draft assemblies. Microb Genom 2018; 4: [View Article] [PubMed]
    [Google Scholar]
  25. Cerqueira GC, Earl AM, Ernst CM, Grad YH, Dekker JP et al. Multi-institute analysis of carbapenem resistance reveals remarkable diversity, unexplained mechanisms, and limited clonal outbreaks. Proc Natl Acad Sci U S A 2017; 114:1135–1140 [View Article] [PubMed]
    [Google Scholar]
  26. Darling AE, Mau B, Perna NT. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 2010; 5:e11147 [View Article] [PubMed]
    [Google Scholar]
  27. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res 2015; 43:e15 [View Article] [PubMed]
    [Google Scholar]
  28. Page AJ, Taylor B, Delaney AJ, Soares J, Seemann T et al. SNP-sites: rapid efficient extraction of SNPs from multi-FASTA alignments. Microb Genom 2016; 2:e000056 [View Article] [PubMed]
    [Google Scholar]
  29. Price MN, Dehal PS, Arkin AP. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 2009; 26:1641–1650 [View Article] [PubMed]
    [Google Scholar]
  30. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 2019; 47:W256–W259 [View Article] [PubMed]
    [Google Scholar]
  31. David S, Reuter S, Harris SR, Glasner C, Feltwell T et al. Epidemic of carbapenem-resistant Klebsiella pneumoniae in Europe is driven by nosocomial spread. Nat Microbiol 2019; 4:1919–1929 [View Article] [PubMed]
    [Google Scholar]
  32. Ferrari C, Corbella M, Gaiarsa S, Comandatore F, Scaltriti E et al. Multiple Klebsiella pneumoniae KPC Clones Contribute to an Extended Hospital Outbreak. Front Microbiol 2019; 10:2767 [View Article] [PubMed]
    [Google Scholar]
  33. Roer L, Overballe-Petersen S, Hansen F, Schønning K, Wang M et al. Escherichia coli Sequence Type 410 Is Causing New International High-Risk Clones. mSphere 2018; 3:e00337–e00318 [View Article] [PubMed]
    [Google Scholar]
  34. Lee C-R, Lee JH, Park KS, Kim YB, Jeong BC et al. Global dissemination of carbapenemase-producing Klebsiella pneumoniae: epidemiology, genetic context, treatment options, and detection methods. Front Microbiol 2016; 7:895 [View Article] [PubMed]
    [Google Scholar]
  35. Sidjabat HE, Paterson DL. Multidrug-resistant Escherichia coli in Asia: epidemiology and management. Expert Rev Anti Infect Ther 2015; 13:575–591 [View Article] [PubMed]
    [Google Scholar]
  36. Giske CG, Fröding I, Hasan CM, Turlej-Rogacka A, Toleman M et al. Diverse sequence types of Klebsiella pneumoniae contribute to the dissemination of blaNDM-1 in India, Sweden, and the United Kingdom. Antimicrob Agents Chemother 2012; 56:2735–2738 [View Article] [PubMed]
    [Google Scholar]
  37. Netikul T, Kiratisin P. Genetic characterization of carbapenem-resistant Enterobacteriaceae and the spread of carbapenem-resistant Klebsiella pneumonia ST340 at a University Hospital in Thailand. PLoS One 2015; 10:e0139116 [View Article] [PubMed]
    [Google Scholar]
  38. Poirel L, Bonnin RA, Nordmann P. Analysis of the resistome of a multidrug-resistant NDM-1-producing Escherichia coli strain by high-throughput genome sequencing. Antimicrob Agents Chemother 2011; 55:4224–4229 [View Article] [PubMed]
    [Google Scholar]
  39. Rozwandowicz M, Brouwer MSM, Fischer J, Wagenaar JA, Gonzalez-Zorn B et al. Plasmids carrying antimicrobial resistance genes in Enterobacteriaceae. J Antimicrob Chemother 2018; 73:1121–1137 [View Article] [PubMed]
    [Google Scholar]
  40. Netikul T, Sidjabat HE, Paterson DL, Kamolvit W, Tantisiriwat W et al. Characterization of an IncN2-type blaNDM-₁-carrying plasmid in Escherichia coli ST131 and Klebsiella pneumoniae ST11 and ST15 isolates in Thailand. J Antimicrob Chemother 2014; 69:3161–3163 [View Article] [PubMed]
    [Google Scholar]
  41. Hao Y, Shao C, Geng X, Bai Y, Jin Y et al. Genotypic and phenotypic characterization of clinical Escherichia coli sequence type 405 carrying IncN2 plasmid harboring blaNDM-1. Front Microbiol 2019; 10:788 [View Article]
    [Google Scholar]
  42. Espinal P, Nucleo E, Caltagirone M, Mattioni Marchetti V, Fernandes MR et al. Genomics of Klebsiella pneumoniae ST16 producing NDM-1, CTX-M-15, and OXA-232. Clin Microbiol Infect 2019; 25:385 [View Article] [PubMed]
    [Google Scholar]
  43. Srijan A, Margulieux KR, Ruekit S, Snesrud E, Maybank R et al. Genomic characterization of nonclonal mcr-1-positive multidrug-resistant Klebsiella pneumoniae from clinical samples in Thailand. Microb Drug Resist 2018; 24:403–410 [View Article] [PubMed]
    [Google Scholar]
  44. Kwon T, Yang JW, Lee S, Yun M-R, Yoo WG et al. Complete genome sequence of Klebsiella pneumoniae subsp. pneumoniae KP617, coproducing OXA-232 and NDM-1 carbapenemases, isolated in South Korea. Genome Announc 2016; 4:e01550–e01555 [View Article] [PubMed]
    [Google Scholar]
  45. Doi Y, Hazen TH, Boitano M, Tsai Y-C, Clark TA et al. Whole-genome assembly of Klebsiella pneumoniae coproducing NDM-1 and OXA-232 carbapenemases using single-molecule, real-time sequencing. Antimicrob Agents Chemother 2014; 58:5947–5953 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000797
Loading
/content/journal/mgen/10.1099/mgen.0.000797
Loading

Data & Media loading...

Supplements

Loading data from figshare Loading data from figshare
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