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Abstract

The population structure of a set of OXA-48-producing isolates belonging to sequence type 11 (ST11 Kp-OXA) and obtained from two hospitals in Madrid in the period from 2012 to 2015 was studied by genome sequencing. Overall, 97 ST11 Kp-OXA isolates were sequenced and their population structure and demography were studied by Bayesian phylodynamic analysis using core-genome SNVs. In total, 92 isolates were from Hospital La Paz, 57 of them from two selected units. The remaining five isolates were from different units of Hospital Doce de Octubre. Altogether, 96 out of the 97 ST11 Kp-OXA isolates could be ascribed to a single lineage that evolved into three sublineages. Demographic inference showed an expansion of the ST11 Kp-OXA in the first half of 2013 in agreement with the registered incidences. Dated phylogeny showed transmission clusters within hospital wards, between wards and between hospitals. The ST11 Kp-OXA outbreak in Hospital La Paz was largely due to the expansion of a single clone that was transmitted between different units and to Hospital Doce de Octubre. This clone diverged into three sub-lineages and spread out following a mixed mode of neutral core-genome evolution with some features of antibiotic selection, frequent large deletions and plasmid loss and gain events.

Funding
This study was supported by the:
  • Instituto de Salud Carlos III (Award PI19/01356)
    • Principle Award Recipient: JesúsMingorance
  • Instituto de Salud Carlos III (Award PI16/01209)
    • Principle Award Recipient: JesúsMingorance
  • Instituto de Salud Carlos III (Award PI13/01218)
    • Principle Award Recipient: JesúsMingorance
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2022-04-08
2024-04-26
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References

  1. Lázaro-Perona F, Dahdouh E, Sotillo A, Pérez-Blanco V, Villa J et al. Dissemination of a single ST11 clone of OXA-48-producing Klebsiella pneumoniae within a large polyclonal hospital outbreak determined by genomic sequencing. Figshare 2022 [View Article]
    [Google Scholar]
  2. Castanheira M, Doyle TB, Collingsworth TD, Sader HS, Mendes RE. Increasing frequency of OXA-48-producing Enterobacterales worldwide and activity of ceftazidime/avibactam, meropenem/vaborbactam and comparators against these isolates. J Antimicrob Chemother 2021; 76:3125–3134 [View Article] [PubMed]
    [Google Scholar]
  3. Paño-Pardo JR, Ruiz-Carrascoso G, Navarro-San Francisco C, Gómez-Gil R, Mora-Rillo M et al. Infections caused by OXA-48-producing Klebsiella pneumoniae in a tertiary hospital in Spain in the setting of a prolonged, hospital-wide outbreak. J Antimicrob Chemother 2013; 68:89–96 [View Article] [PubMed]
    [Google Scholar]
  4. Paño-Pardo JR, López Quintana B, Lázaro Perona F, Ruiz Carrascoso G, Romero-Gómez MP et al. Community-onset bloodstream and other infections, caused by carbapenemase-producing enterobacteriaceae: epidemiological, microbiological, and clinical features. Open Forum Infect Dis 2016; 3:ofw136 [View Article] [PubMed]
    [Google Scholar]
  5. Zhao J, Liu C, Liu Y, Zhang Y, Xiong Z et al. Genomic characteristics of clinically important ST11 Klebsiella pneumoniae strains worldwide. J Glob Antimicrob Resist 2020; 22:519–526 [View Article] [PubMed]
    [Google Scholar]
  6. Liao W, Liu Y, Zhang W. Virulence evolution, molecular mechanisms of resistance and prevalence of ST11 carbapenem-resistant Klebsiella pneumoniae in China: A review over the last 10 years. J Glob Antimicrob Resist 2020; 23:174–180 [View Article] [PubMed]
    [Google Scholar]
  7. 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]
  8. Chen L, Mathema B, Pitout JDD, DeLeo FR, Kreiswirth BN et al. Epidemic Klebsiella pneumoniae ST258 is a hybrid strain. mBio 2014; 5:1–8 [View Article] [PubMed]
    [Google Scholar]
  9. Dong N, Zhang R, Liu L, Li R, Lin D et al. Genome analysis of clinical multilocus sequence Type 11 Klebsiella Pneumoniae from China. Microb Genom 2018; 4:1–12 [View Article]
    [Google Scholar]
  10. Hernández-García M, Pérez-Viso B, Carmen Turrientes M, Díaz-Agero C, López-Fresneña N et al. Characterization of carbapenemase-producing Enterobacteriaceae from colonized patients in a university hospital in Madrid, Spain, during the R-GNOSIS project depicts increased clonal diversity over time with maintenance of high-risk clones. J Antimicrob Chemother 2018; 73:3039–3043 [View Article]
    [Google Scholar]
  11. Gijón D, Tedim AP, Valverde A, Rodríguez I, Morosini M-I et al. Early OXA-48-producing enterobacterales isolates recovered in a spanish hospital reveal a complex introduction dominated by sequence type 11 (ST11) and ST405 Klebsiella pneumoniae clones. mSphere 2020; 5:e00080-20 [View Article]
    [Google Scholar]
  12. Piedra-Carrasco N, Fàbrega A, Calero-Cáceres W, Cornejo-Sánchez T, Brown-Jaque M et al. Carbapenemase-producing enterobacteriaceae recovered from a Spanish river ecosystem. PLoS One 2017; 12:1–11 [View Article] [PubMed]
    [Google Scholar]
  13. Darwich L, Vidal A, Seminati C, Albamonte A, Casado A et al. High prevalence and diversity of extended-spectrum β-lactamase and emergence of OXA-48 producing Enterobacterales in wildlife in Catalonia. PLoS One 2019; 14:e0210686 [View Article] [PubMed]
    [Google Scholar]
  14. López-Camacho E, Rentero Z, Ruiz-Carrascoso G, Wesselink J-J, Pérez-Vázquez M et al. Design of clone-specific probes from genome sequences for rapid PCR-typing of outbreak pathogens. Clin Microbiol Infect 2014; 20:891–893 [View Article] [PubMed]
    [Google Scholar]
  15. Diancourt L, Passet V, Verhoef J, Grimont PAD, Brisse S. Multilocus sequence typing of Klebsiella pneumoniae nosocomial isolates. J Clin Microbiol 2005; 43:4178–4182 [View Article] [PubMed]
    [Google Scholar]
  16. 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]
  17. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 2016; 44:6614–6624 [View Article] [PubMed]
    [Google Scholar]
  18. Seemann T, Goncalves da Silva A, Bulach DM, Schultz MB, Kwong JC. n.d Nullarbor Github.
  19. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article] [PubMed]
    [Google Scholar]
  20. 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]
  21. Clausen P, Aarestrup FM, Lund O. Rapid and precise alignment of raw reads against redundant databases with KMA. BMC Bioinformatics 2018; 19:307 [View Article] [PubMed]
    [Google Scholar]
  22. Wyres KL, Wick RR, Gorrie C, Jenney A, Follador R et al. Identification of Klebsiella capsule synthesis loci from whole genome data. Microb Genom 2016; 2:e000102 [View Article] [PubMed]
    [Google Scholar]
  23. Bouckaert R, Vaughan TG, Barido-Sottani J, Duchêne S, Fourment M et al. BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Comput Biol 2019; 15:1–28 [View Article] [PubMed]
    [Google Scholar]
  24. Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA. Posterior Summarization in Bayesian Phylogenetics Using Tracer 1.7. Syst Biol 2018; 67:901–904 [View Article] [PubMed]
    [Google Scholar]
  25. Rambaut A. FigTree 1.4.4 Github 2018 https://github.com/rambaut/figtree/releases
    [Google Scholar]
  26. Poirel L, Bonnin RA, Nordmann P. Genetic features of the widespread plasmid coding for the carbapenemase OXA-48. Antimicrob Agents Chemother 2012; 56:559–562 [View Article] [PubMed]
    [Google Scholar]
  27. León-Sampedro R, DelaFuente J, Díaz-Agero C, Crellen T, Musicha P et al. Pervasive transmission of a carbapenem resistance plasmid in the gut microbiota of hospitalized patients. Nat Microbiol 2021; 6:606–616 [View Article] [PubMed]
    [Google Scholar]
  28. Loo SL, Ong A, Kyaw W, Thibaut LM, Lan R et al. Nonsynonymous polymorphism counts in bacterial genomes: a comparative examination. Appl Environ Microbiol 2020; 87:1–16 [View Article] [PubMed]
    [Google Scholar]
  29. Villa J, Viedma E, Brañas P, Mingorance J, Chaves F. Draft whole-genome sequence of OXA-48-producing multidrug-resistant Klebsiella pneumoniae KP_ST11_OXA-48. Genome Announc 2014; 2:e00737-14 [View Article] [PubMed]
    [Google Scholar]
  30. Pérez-Blanco V, Redondo-Bravo L, Ruíz-Carrascoso G, Paño-Pardo JR, Gómez-Gil R et al. Epidemiology and control measures of an OXA-48-producing Enterobacteriaceae hospital-wide oligoclonal outbreak. Epidemiol Infect 2018; 146:656–662 [View Article] [PubMed]
    [Google Scholar]
  31. Lee AHY, Porto WF, de Faria C, Dias SC, Alencar SA et al. Genomic insights into the diversity, virulence and resistance of klebsiella pneumoniae extensively drug resistant clinical isolates. Microb Genom 2021; 7: [View Article] [PubMed]
    [Google Scholar]
  32. Spencer MD, Winglee K, Passaretti C, Earl AM, Manson AL et al. Whole genome sequencing detects inter-facility transmission of carbapenem-resistant Klebsiella pneumoniae . J Infect 2019; 78:187–199 [View Article] [PubMed]
    [Google Scholar]
  33. 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]
  34. 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] [PubMed]
    [Google Scholar]
  35. Poirel L, Bonnin RA, Nordmann P. Genetic features of the widespread plasmid coding for the carbapenemase OXA-48. Antimicrob Agents Chemother 2012; 56:559–562 [View Article] [PubMed]
    [Google Scholar]
  36. Lázaro-Perona F, Ramos JC, Sotillo A, Mingorance J, García-Rodríguez J et al. Intestinal persistence of a plasmid harbouring the OXA-48 carbapenemase gene after hospital discharge. J Hosp Infect 2019; 101:175–178 [View Article] [PubMed]
    [Google Scholar]
  37. Potel C, Ortega A, Martínez-Lamas L, Bautista V, Regueiro B et al. Interspecies transmission of the blaOXA-48 gene from a klebsiella pneumoniae high-risk clone of sequence type 147 to different Escherichia coli clones in the gut microbiota. Antimicrob Agents Chemother 2018; 62:15–17 [View Article] [PubMed]
    [Google Scholar]
  38. Brañas P, Villa J, Viedma E, Mingorance J, Orellana MA et al. Molecular epidemiology of carbapenemase-producing Klebsiella pneumoniae in a hospital in Madrid: Successful establishment of an OXA-48 ST11 clone. Int J Antimicrob Agents 2015; 46:111–116 [View Article] [PubMed]
    [Google Scholar]
  39. López-Camacho E, Paño-Pardo JR, Ruiz-Carrascoso G, Wesselink J-J, Lusa-Bernal S et al. Population structure of OXA-48-producing Klebsiella pneumoniae ST405 isolates during a hospital outbreak characterised by genomic typing. J Glob Antimicrob Resist 2018; 15:48–54 [View Article] [PubMed]
    [Google Scholar]
  40. Lázaro-Perona F, Rodríguez-Tejedor M, Ruiz-Carrascoso G, Díaz-Pollán B, Loeches B et al. Intestinal loads of OXA-48-producing Klebsiella pneumoniae in colonized patients determined from surveillance rectal swabs. Clin Microbiol Infect 2021; 27:1169 [View Article] [PubMed]
    [Google Scholar]
  41. Feldman N, Adler A, Molshatzki N, Navon-Venezia S, Khabra E et al. Gastrointestinal colonization by KPC-producing Klebsiella pneumoniae following hospital discharge: Duration of carriage and risk factors for persistent carriage. Clin Microbiol Infect 2013; 19:E190–6 [View Article] [PubMed]
    [Google Scholar]
  42. Lerner A, Adler A, Abu-Hanna J, Cohen Percia S, Kazma Matalon M et al. Spread of KPC-producing carbapenem-resistant Enterobacteriaceae: The importance of super-spreaders and rectal KPC concentration. Clin Microbiol Infect 2015; 21:470 [View Article]
    [Google Scholar]
  43. Robustillo-Rodela A, Pérez-Blanco V, Espinel Ruiz MA, Ruiz Carrascoso G, Figueira Iglesias JC et al. Successful control of 2 simultaneous outbreaks of OXA-48 carbapenemase-producing Enterobacteriaceae and multidrug-resistant Acinetobacter baumannii in an intensive care unit. Am J Infect Control 2017; 45:1356–1362 [View Article]
    [Google Scholar]
  44. Viehweger A, Blumenscheit C, Lippmann N, Wyres KL, Brandt C et al. Context-aware genomic surveillance reveals hidden transmission of a carbapenemase-producing Klebsiella pneumoniae . Microb Genom 2021; 7:bioRxiv [View Article] [PubMed]
    [Google Scholar]
  45. Pecora ND, Li N, Allard M, Li C, Albano E et al. Genomically informed surveillance for carbapenem-resistant enterobacteriaceae in a health care system. mBio 2015; 6:1–11 [View Article] [PubMed]
    [Google Scholar]
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