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Volume 6, Issue 4

Comparison of core-genome MLST, coreSNP and PFGE methods for cluster analysis Open Access

Abstract

In this work we compared the most frequently used typing methods: PFGE, cgMLST and coreSNP. We evaluated the discriminatory power of the three methods to confirm or exclude nosocomial transmission on strains isolated from January to December 2017, in the framework of the routine surveillance for multidrug-resistant organisms at the San Raffaele Hospital, in Milan. We compared the results of the different methods to the results of epidemiological investigation. Our results showed that cgMLST and coreSNP are more discriminant than PFGE, and that both approaches are suitable for transmission analyses. cgMLST appeared to be inferior to coreSNP in the CG258 phylogenetic reconstruction. Indeed, we found that the phylogenetic reconstruction based on cgMLST genes wrongly clustered ST258 clade1 and clade2 strains, conversely properly assigned by coreSNP approach. In conclusion, this study provides evidences supporting the reliability of both cgMLST and coreSNP for hospital surveillance programs and highlights the limits of cgMLST scheme genes for phylogenetic reconstructions.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): CG258 , cgMLST , cluster and K. pneumoniae
© 2020 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2020-03-09
2024-04-19
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References

  1. Tumbarello M, Trecarichi EM, De Rosa FG, Giannella M, Giacobbe DR et al. Infections caused by KPC-producing Klebsiella pneumoniae: differences in therapy and mortality in a multicentre study. J Antimicrob Chemother 2015; 70:2133–2143 [View Article]
     [Google Scholar]
  2. Qureshi ZA, Paterson DL, Potoski BA, Kilayko MC, Sandovsky G et al. Treatment outcome of bacteremia due to KPC-producing Klebsiella pneumoniae: superiority of combination antimicrobial regimens. Antimicrob Agents Chemother 2012; 56:2108–2113 [View Article]
     [Google Scholar]
  3. Bialek-Davenet S, Criscuolo A, Ailloud F, Passet V, Jones L et al. Genomic definition of hypervirulent and multidrug-resistant Klebsiella pneumoniae clonal groups. Emerg Infect Dis 2014; 20:1812–1820 [View Article]
     [Google Scholar]
  4. Logan LK, Weinstein RA. The epidemiology of carbapenem-resistant Enterobacteriaceae: the impact and evolution of a global menace. J Infect Dis 2017; 215:S28–S36 [View Article]
     [Google Scholar]
  5. Giani T, Antonelli A, Caltagirone M, Mauri C, Nicchi J et al. Evolving beta-lactamase epidemiology in Enterobacteriaceae from Italian nationwide surveillance, October 2013: KPC-carbapenemase spreading among outpatients. Euro Surveill 2017; 22:pii: 30583 [View Article]
     [Google Scholar]
  6. Chen L, Mathema B, Chavda KD, DeLeo FR, Bonomo RA et al. Carbapenemase-producing Klebsiella pneumoniae: molecular and genetic decoding. Trends Microbiol 2014; 22:686–696 [View Article]
     [Google Scholar]
  7. Munoz-Price LS, Poirel L, Bonomo RA, Schwaber MJ, Daikos GL et al. Clinical epidemiology of the global expansion of Klebsiella pneumoniae carbapenemases. Lancet Infect Dis 2013; 13:785–796 [View Article]
     [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]
     [Google Scholar]
  9. Giani T, D'Andrea MM, Pecile P, Borgianni L, Nicoletti P et al. Emergence in Italy of Klebsiella pneumoniae sequence type 258 producing KPC-3 Carbapenemase. J Clin Microbiol 2009; 47:3793–3794 [View Article]
     [Google Scholar]
  10. Navon-Venezia S, Kondratyeva K, Carattoli A. Klebsiella pneumoniae: a major worldwide source and shuttle for antibiotic resistance. FEMS Microbiol Rev 2017; 41:252–275 [View Article]
     [Google Scholar]
  11. Bowers JR, Kitchel B, Driebe EM, MacCannell DR, Roe C et al. Genomic Analysis of the Emergence and Rapid Global Dissemination of the Clonal Group 258 Klebsiella pneumoniae Pandemic. PLoS One 2015; 10:e0133727 [View Article]
     [Google Scholar]
  12. Wyres KL, Wick RR, Judd LM, Froumine R, Tokolyi A et al. Distinct evolutionary dynamics of horizontal gene transfer in drug resistant and virulent clones of Klebsiella pneumoniae . PLoS Genet 2019; 15:e1008114 [View Article]
     [Google Scholar]
  13. Bowers JR, Lemmer D, Sahl JW, Pearson T, Driebe EM et al. KlebSeq, a diagnostic tool for surveillance, detection, and monitoring of Klebsiella pneumoniae . J Clin Microbiol 2016; 54:2582–2596 [View Article]
     [Google Scholar]
  14. Tang P, Croxen MA, Hasan MR, Hsiao WWL, Hoang LM. Infection control in the new age of genomic epidemiology. Am J Infect Control 2017; 45:170–179 [View Article]
     [Google Scholar]
  15. Struelens MJ. Molecular epidemiologic typing systems of bacterial pathogens: current issues and perspectives. Mem Inst Oswaldo Cruz 1998; 93:581–586 [View Article]
     [Google Scholar]
  16. Nutman A, Marchaim D. How to: molecular investigation of a hospital outbreak. Clin Microbiol Infect 2019; 25:688-695 [View Article]
     [Google Scholar]
  17. Holt KE, Wertheim H, Zadoks RN, Baker S, Whitehouse CA et al. 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 2015; 112:E3574–E3581 [View Article]
     [Google Scholar]
  18. Struve C, Roe CC, Stegger M, Stahlhut SG, Hansen DS et al. Mapping the evolution of hypervirulent Klebsiella pneumoniae . mBio 2015; 6:1–12 [View Article]
     [Google Scholar]
  19. Maiden MCJ, Jansen van Rensburg MJ, Bray JE, Earle SG, Ford SA et al. Mlst revisited: the gene-by-gene approach to bacterial genomics. Nat Rev Microbiol 2013; 11:728–736 [View Article]
     [Google Scholar]
  20. Diancourt L, Passet V, Verhoef J, Grimont PAD, Brisse S et al. Multilocus sequence typing of Klebsiella pneumoniae nosocomial isolates. J Clin Microbiol 2005; 43:4178–4182 [View Article]
     [Google Scholar]
  21. Onori R, Gaiarsa S, Comandatore F, Pongolini S, Brisse S et al. Tracking nosocomial Klebsiella pneumoniae infections and outbreaks by whole-genome analysis: small-scale italian scenario within a single hospital. J Clin Microbiol 2015; 53:2861–2868 [View Article]
     [Google Scholar]
  22. Dekker JP, Frank KM. Next-Generation epidemiology: using real-time core genome multilocus sequence typing to support infection control policy. J Clin Microbiol 2016; 54:2850–2853 [View Article]
     [Google Scholar]
  23. Cunningham SA, Chia N, Jeraldo PR, Quest DJ, Johnson JA et al. Comparison of whole-genome sequencing methods for analysis of three methicillin-resistant Staphylococcus aureus outbreaks. J Clin Microbiol 2017; 55:1946–1953 [View Article]
     [Google Scholar]
  24. Daehre K, Projahn M, Friese A, Semmler T, Guenther S et al. ESBL-Producing Klebsiella pneumoniae in the Broiler Production Chain and the First Description of ST3128. Front Microbiol 2018; 9:2302 [View Article]
     [Google Scholar]
  25. Henri C, Leekitcharoenphon P, Carleton HA, Radomski N, Kaas RS et al. An Assessment of Different Genomic Approaches for Inferring Phylogeny of Listeria monocytogenes . Front Microbiol 2017; 8:2351 [View Article]
     [Google Scholar]
  26. Kohl TA, Diel R, Harmsen D, Rothgänger J, Walter KM et al. Whole-genome-based Mycobacterium tuberculosis surveillance: a standardized, portable, and expandable approach. J Clin Microbiol 2014; 52:2479–2486 [View Article]
     [Google Scholar]
  27. de Been M, Pinholt M, Top J, Bletz S, Mellmann A et al. Core genome multilocus sequence typing scheme for high- resolution typing of Enterococcus faecium . J Clin Microbiol 2015; 53:3788–3797 [View Article]
     [Google Scholar]
  28. Wattam AR, Davis JJ, Assaf R, Boisvert S, Brettin T et al. Improvements to PATRIC, the all-bacterial bioinformatics database and analysis resource center. Nucleic Acids Res 2017; 45:D535–D542 [View Article]
     [Google Scholar]
  29. Mezzatesta ML, Gona F, Caio C, Adembri C, Dell'utri P et al. Emergence of an extensively drug-resistant ArmA- and KPC-2-producing ST101 Klebsiella pneumoniae clone in Italy. J Antimicrob Chemother 2013; 68:1932–1934 [View Article]
     [Google Scholar]
  30. Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE et al. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 1995; 33:2233e92239 [View Article]
     [Google Scholar]
  31. Gona F, Bongiorno D, Aprile A, Corazza E, Pasqua B et al. Emergence of two novel sequence types (3366 and 3367) NDM-1- and OXA-48-co-producing K. pneumoniae in Italy. Eur J Clin Microbiol Infect Dis 2019; 38:1687–1691 [View Article]
     [Google Scholar]
  32. Nurk S, Bankevich A, Antipov D, Gurevich AA, Korobeynikov A et al. Assembling single-cell genomes and mini-metagenomes from chimeric MDA products. J Comput Biol 2013; 20:714–737 [View Article]
     [Google Scholar]
  33. Ondov BD, Treangen TJ, Melsted P, Mallonee AB, Bergman NH et al. Mash: fast genome and metagenome distance estimation using MinHash. Genome Biol 2016; 17:132 [View Article]
     [Google Scholar]
  34. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [View Article]
     [Google Scholar]
  35. Tafaj S, Gona F, Kapisyzi P, Cani A, Hatibi A et al. Isolation of the first New Delhi metallo-ß-lactamase-1 (NDM-1)-producing and colistin-resistant Klebsiella pneumoniae sequence type ST15 from a digestive carrier in Albania, May 2018. J Glob Antimicrob Resist 2019; 17:142–144 [View Article]
     [Google Scholar]
  36. Lepuschitz S, Schill S, Stoeger A, Pekard-Amenitsch S, Huhulescu S et al. Whole genome sequencing reveals resemblance between ESBL-producing and carbapenem resistant Klebsiella pneumoniae isolates from Austrian rivers and clinical isolates from hospitals. Sci Total Environ 2019; 662:227–235 [View Article]
     [Google Scholar]
  37. Edgar RC. Muscle: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 2004; 5:113 [View Article]
     [Google Scholar]
  38. Darling AE, Mau B, Perna NT. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 2010; 5:e11147 [View Article]
     [Google Scholar]
  39. Gaiarsa S, Comandatore F, Gaibani P, Corbella M, Dalla Valle C et al. Genomic epidemiology of Klebsiella pneumoniae in Italy and novel insights into the origin and global evolution of its resistance to carbapenem antibiotics. Antimicrob Agents Chemother 2015; 59:389–396 [View Article]
     [Google Scholar]
  40. 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]
  41. Akhter S, Aziz RK, Edwards RA. PhiSpy: a novel algorithm for finding prophages in bacterial genomes that combines similarity- and composition-based strategies. Nucleic Acids Res 2012; 40:e126 [View Article]
     [Google Scholar]
  42. Scaltriti E, Sassera D, Comandatore F, Morganti M, Mandalari C et al. Differential single nucleotide polymorphism-based analysis of an outbreak caused by Salmonella enterica serovar Manhattan reveals epidemiological details missed by standard pulsed-field gel electrophoresis. J Clin Microbiol 2015; 53:1227–1238 [View Article]
     [Google Scholar]
  43. 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]
     [Google Scholar]
  44. Paradis E, Schliep K. Ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 2019; 35:526–528 [View Article]
     [Google Scholar]
  45. Darriba D, Posada D, Kozlov AM, Stamatakis A, Morel B et al. Model Test-NG: a new and scalable tool for the selection of DNA and protein evolutionary models. BioRxiv 2019612903
     [Google Scholar]
  46. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of. large phylogenies 2014; 30:1312–1313 [View Article]
     [Google Scholar]
  47. Mellmann A, Bletz S, Böking T, Kipp F, Becker K et al. Real-Time genome sequencing of resistant bacteria provides precision infection control in an institutional setting. J Clin Microbiol 2016; 54:2874e812881 [View Article]
     [Google Scholar]
  48. Adler A, Lifshitz Z, Gordon M, Ben-David D, Khabra E et al. Evolution and dissemination of the Klebsiella pneumoniae clonal group 258 throughout Israeli post-acute care hospitals, 2008-13. J Antimicrob Chemother 2017; 72:2219–2224 [View Article]
     [Google Scholar]
  49. Jiang Y, Wei Z, Wang Y, Hua X, Feng Y et al. Tracking a hospital outbreak of KPC-producing ST11 Klebsiella pneumoniae with whole genome sequencing. Clin Microbiol Infect 2015; 21:1001–1007 [View Article]
     [Google Scholar]
  50. Nadon C, Van Walle I, Gerner-Smidt P, Campos J, Chinen I et al. Pulsenet International: vision for the implementation of whole genome sequencing (WGS) for global food-borne disease surveillance. Euro Surveill 2017; 22:pii: 30544 [View Article]
     [Google Scholar]
  51. Deleo FR, Chen L, Porcella SF, Martens CA, Kobayashi SD et al. Molecular dissection of the evolution of carbapenem-resistant multilocus sequence type 258 Klebsiella pneumoniae . Proc Natl Acad Sci U S A 2014; 111:4988–4993 [View Article]
     [Google Scholar]
  52. Comandatore F, Sassera D, Bayliss SC, Scaltriti E, Gaiarsa S et al. Gene composition as a potential barrier to large recombinations in the bacterial pathogen Klebsiella pneumoniae. Genome Biol Evol 2019; 11:3240–3251
     [Google Scholar]
  53. Chen L, Mathema B, Pitout JDD, DeLeo FR, Kreiswirth BN. Epidemic Klebsiella pneumoniae ST258 is a hybrid strain. mBio 2014; 5:e01355–14 [View Article]
     [Google Scholar]
  54. Wright MS, Perez F, Brinkac L, Jacobs MR, Kaye K et al. Population structure of KPC-producing Klebsiella pneumoniae isolates from midwestern U.S. hospitals. Antimicrob Agents Chemother 2014; 58:4961–4965 [View Article]
     [Google Scholar]
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Comparison of core-genome MLST, coreSNP and PFGE methods for Klebsiella pneumoniae cluster analysis
M Gen 6, e000347 (2020); https://doi.org/10.1099/mgen.0.000347
/content/journal/mgen/10.1099/mgen.0.000347
/content/journal/mgen/10.1099/mgen.0.000347
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