1887
Research Open Access
Like 0

Abstract

Background

ST131, a global, high-risk clone, comprises fluoroquinolone resistance (FQ-R) mutations and CTX-M extended-spectrum beta-lactamases associated with the 30-encoding clades, C1 and C2. Further carbapenem resistance development in ST131 is a public health concern.

Aim

This observational study aimed to probe the diversity of carbapenemase-producing (CP ) ST131 across England.

Methods

ST131 isolates were identified using whole-genome sequencing (WGS) data generated for all non-duplicate CP from human samples submitted to the national reference laboratory from January 2014 to June 2016. Antimicrobial resistance (AMR) gene content and single nucleotide polymorphism (SNP) data were compared against a published ST131 phylogeny and analysed alongside patient metadata.

Results

Thirty-nine genetically diverse ST131 CP , from eight of nine regions, represented 10% of CP isolates sequenced. Ten and eight isolates were from the FQ-susceptible (FQ-S) clades A and B, while eight and 15 isolates belonged to the FQ-R clades C1 or C2, respectively. Seven distinct carbapenemases were identified: KPC-2 (21 isolates, 6 regions) frequently occurred among clade C2 isolates (n = 10). OXA-48-producers (10 isolates, 3 regions) were often from clade A (n = 5). NDM-1 (n = 4), NDM-5 (n = 1), VIM-1 (n = 1), VIM-4 (n = 1) and OXA-181 (n = 1) were also identified. Clade C2 isolates encoded more AMR genes than those from clades A (p = 0.02), B (p = 9.6 x 10−3) or C1 (p = 0.03).

Conclusion

When compared with its global predominance among ESBL- ST131 represented a fraction of the CP received, belonging to diverse clades and encoding diverse carbapenemases. The greater accumulation of resistance genes in clade C2 isolates highlights the need for ongoing monitoring of this high-risk lineage.

Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2019.24.37.1800627
2019-09-12
2024-11-22
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2019.24.37.1800627
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/24/37/eurosurv-24-37-3.html?itemId=/content/10.2807/1560-7917.ES.2019.24.37.1800627&mimeType=html&fmt=ahah

References

  1. Ben Zakour NL, Alsheikh-Hussain AS, Ashcroft MM, Khanh Nhu NT, Roberts LW, Stanton-Cook M, et al. Sequential Acquisition of Virulence and Fluoroquinolone Resistance Has Shaped the Evolution of Escherichia coli ST131. MBio. 2016;7(2):e00347-16.  https://doi.org/10.1128/mBio.00347-16  PMID: 27118589 
  2. Stoesser N, Sheppard AE, Pankhurst L, De Maio N, Moore CE, Sebra R, et al. Evolutionary History of the Global Emergence of the Escherichia coli Epidemic Clone ST131. MBio. 2016;7(2):e02162.  https://doi.org/10.1128/mBio.02162-15  PMID: 27006459 
  3. Johnson JR, Tchesnokova V, Johnston B, Clabots C, Roberts PL, Billig M, et al. Abrupt emergence of a single dominant multidrug-resistant strain of Escherichia coli. J Infect Dis. 2013;207(6):919-28.  https://doi.org/10.1093/infdis/jis933  PMID: 23288927 
  4. Wu XR, Sun TT, Medina JJ. In vitro binding of type 1-fimbriated Escherichia coli to uroplakins Ia and Ib: relation to urinary tract infections. Proc Natl Acad Sci USA. 1996;93(18):9630-5.  https://doi.org/10.1073/pnas.93.18.9630  PMID: 8790381 
  5. Martinez JJ, Mulvey MA, Schilling JD, Pinkner JS, Hultgren SJ. Type 1 pilus-mediated bacterial invasion of bladder epithelial cells. EMBO J. 2000;19(12):2803-12.  https://doi.org/10.1093/emboj/19.12.2803  PMID: 10856226 
  6. Cantón R, Coque TM. The CTX-M beta-lactamase pandemic. Curr Opin Microbiol. 2006;9(5):466-75.  https://doi.org/10.1016/j.mib.2006.08.011  PMID: 16942899 
  7. Pitout JDD, DeVinney R. Escherichia coli ST131: a multidrug-resistant clone primed for global domination. F1000 Res. 2017;6:195.  https://doi.org/10.12688/f1000research.10609.1  PMID: 28344773 
  8. Matsumura Y, Pitout JD, Gomi R, Matsuda T, Noguchi T, Yamamoto M, et al. Global Escherichia coli sequence type 131 clade with blaCTX-M-27 gene. Emerg Infect Dis. 2016;22(11):1900-7.  https://doi.org/10.3201/eid2211.160519  PMID: 27767006 
  9. McNulty CAM, Lecky DM, Xu-McCrae L, Nakiboneka-Ssenabulya D, Chung KT, Nichols T, et al. CTX-M ESBL-producing Enterobacteriaceae: estimated prevalence in adults in England in 2014. J Antimicrob Chemother. 2018;73(5):1368-88.  https://doi.org/10.1093/jac/dky007  PMID: 29514211 
  10. Birgy A, Bidet P, Levy C, Sobral E, Cohen R, Bonacorsi S. CTX-M-27–producing escherichia coli of sequence type 131 and clade C1-M27, France. Emerg Infect Dis. 2017;23(5):885.  https://doi.org/10.3201/eid2305.161865  PMID: 28418829 
  11. Peirano G, Schreckenberger PC, Pitout JDD. Characteristics of NDM-1-producing Escherichia coli isolates that belong to the successful and virulent clone ST131. Antimicrob Agents Chemother. 2011;55(6):2986-8.  https://doi.org/10.1128/AAC.01763-10  PMID: 21444703 
  12. Isozumi R, Yoshimatsu K, Yamashiro T, Hasebe F, Nguyen BM, Ngo TC, et al. bla(NDM-1)-positive Klebsiella pneumoniae from environment, Vietnam. Emerg Infect Dis. 2012;18(8):1383-5.  https://doi.org/10.3201/eid1808.111816  PMID: 22840532 
  13. Stoesser N, Sheppard AE, Peirano G, Anson LW, Pankhurst L, Sebra R, et al. Genomic epidemiology of global Klebsiella pneumoniae carbapenemase (KPC)-producing Escherichia coli. Sci Rep. 2017;7(1):5917.  https://doi.org/10.1038/s41598-017-06256-2  PMID: 28725045 
  14. Morris D, McGarry E, Cotter M, Passet V, Lynch M, Ludden C, et al. Detection of OXA-48 carbapenemase in the pandemic clone Escherichia coli O25b:H4-ST131 in the course of investigation of an outbreak of OXA-48-producing Klebsiella pneumoniae. Antimicrob Agents Chemother. 2012;56(7):4030-1.  https://doi.org/10.1128/AAC.00638-12  PMID: 22564840 
  15. Peirano G, Bradford PA, Kazmierczak KM, Badal RE, Hackel M, Hoban DJ, et al. Global incidence of carbapenemase-producing Escherichia coli ST131. Emerg Infect Dis. 2014;20(11):1928-31.  https://doi.org/10.3201/eid2011.141388  PMID: 25340464 
  16. Piedra-Carrasco N, Fàbrega A, Calero-Cáceres W, Cornejo-Sánchez T, Brown-Jaque M, Mir-Cros A, et al. Carbapenemase-producing enterobacteriaceae recovered from a Spanish river ecosystem. PLoS One. 2017;12(4):e0175246.  https://doi.org/10.1371/journal.pone.0175246  PMID: 28380016 
  17. Giufrè M, Accogli M, Ricchizzi E, Barbanti F, Farina C, Fazii P, et al. Multidrug-resistant infections in long-term care facilities: extended-spectrum β-lactamase-producing Enterobacteriaceae and hypervirulent antibiotic resistant Clostridium difficile. Diagn Microbiol Infect Dis. 2018;91(3):275-81.  https://doi.org/10.1016/j.diagmicrobio.2018.02.018  PMID: 29571838 
  18. Woodford N, Ward ME, Kaufmann ME, Turton J, Fagan EJ, James D, et al. Community and hospital spread of Escherichia coli producing CTX-M extended-spectrum beta-lactamases in the UK. J Antimicrob Chemother. 2004;54(4):735-43.  https://doi.org/10.1093/jac/dkh424  PMID: 15347638 
  19. GitHub. phe-bioinformatics/kmerid. San Francisco: GitHub. [Accessed 1 Sep 2019]. Available from: https://github.com/phe-bioinformatics/kmerid
  20. Tewolde R, Dallman T, Schaefer U, Sheppard CL, Ashton P, Pichon B, et al. MOST: a modified MLST typing tool based on short read sequencing. PeerJ. 2016;4:e2308.  https://doi.org/10.7717/peerj.2308  PMID: 27602279 
  21. Doumith M, Godbole G, Ashton P, Larkin L, Dallman T, Day M, et al. Detection of the plasmid-mediated mcr-1 gene conferring colistin resistance in human and food isolates of Salmonella enterica and Escherichia coli in England and Wales. J Antimicrob Chemother. 2016;71(8):2300-5.  https://doi.org/10.1093/jac/dkw093  PMID: 27090630 
  22. SAMtools. HTSlib. Cambridge: Genome Research Limited. [Accessed 1 Sep 2019]. Available from: www.htslib.org/download/
  23. Schmieder R, Edwards R. Quality control and preprocessing of metagenomic datasets. Bioinformatics. 2011;27(6):863-4.  https://doi.org/10.1093/bioinformatics/btr026  PMID: 21278185 
  24. GitHub. phe-bioinformatics/PHEnix. San Francisco: GitHub. [Accessed 1 Sep 2019]. Available from: https://github.com/phe-bioinformatics/PHEnix
  25. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA, Bentley SD, et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res. 2015;43(3):e15.  https://doi.org/10.1093/nar/gku1196  PMID: 25414349 
  26. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30(9):1312-3.  https://doi.org/10.1093/bioinformatics/btu033  PMID: 24451623 
  27. Yu G, Smith DK, Zhu H, Guan Y, Lam TTY. Ggtree: an R Package for Visualization and Annotation of Phylogenetic Trees With Their Covariates and Other Associated Data. Methods Ecol Evol. 2017;8(1):28-36.  https://doi.org/10.1111/2041-210X.12628 
  28. Rambaut A, Lam TT, Max Carvalho L, Pybus OG. Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol. 2016;2(1):vew007.  https://doi.org/10.1093/ve/vew007  PMID: 27774300 
  29. Drummond AJ, Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol. 2007;7(1):214.  https://doi.org/10.1186/1471-2148-7-214  PMID: 17996036 
  30. R Core Team. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2018. Available from: http://www.R-project.org/
  31. Martin J, Phan HTT, Findlay J, Stoesser N, Pankhurst L, Navickaite I, et al. Covert dissemination of carbapenemase-producing Klebsiella pneumoniae (KPC) in a successfully controlled outbreak: long- and short-read whole-genome sequencing demonstrate multiple genetic modes of transmission. J Antimicrob Chemother. 2017;72(11):3025-34.  https://doi.org/10.1093/jac/dkx264  PMID: 28961793 
  32. Poirel L, Bonnin RA, Nordmann P. Genetic features of the widespread plasmid coding for the carbapenemase OXA-48. Antimicrob Agents Chemother. 2012;56(1):559-62.  https://doi.org/10.1128/AAC.05289-11  PMID: 22083465 
  33. Oteo J, Hernández JM, Espasa M, Fleites A, Sáez D, Bautista V, et al. Emergence of OXA-48-producing Klebsiella pneumoniae and the novel carbapenemases OXA-244 and OXA-245 in Spain. J Antimicrob Chemother. 2013;68(2):317-21.  https://doi.org/10.1093/jac/dks383  PMID: 23034714 
  34. Dimou V, Dhanji H, Pike R, Livermore DM, Woodford N. Characterization of Enterobacteriaceae producing OXA-48-like carbapenemases in the UK. J Antimicrob Chemother. 2012;67(7):1660-5.  https://doi.org/10.1093/jac/dks124  PMID: 22532467 
  35. Pitart C, Solé M, Roca I, Fàbrega A, Vila J, Marco F. First outbreak of a plasmid-mediated carbapenem-hydrolyzing OXA-48 beta-lactamase in Klebsiella pneumoniae in Spain. Antimicrob Agents Chemother. 2011;55(9):4398-401.  https://doi.org/10.1128/AAC.00329-11  PMID: 21746954 
  36. Poirel L, Potron A, Nordmann P. OXA-48-like carbapenemases: the phantom menace. J Antimicrob Chemother. 2012;67(7):1597-606.  https://doi.org/10.1093/jac/dks121  PMID: 22499996 
  37. Munoz-Price LS, Poirel L, Bonomo RA, Schwaber MJ, Daikos GL, Cormican M, et al. Clinical epidemiology of the global expansion of Klebsiella pneumoniae carbapenemases. Lancet Infect Dis. 2013;13(9):785-96.  https://doi.org/10.1016/S1473-3099(13)70190-7  PMID: 23969216 
/content/10.2807/1560-7917.ES.2019.24.37.1800627
Loading

Data & Media loading...

Supplementary data

Submit comment
Close
Comment moderation successfully completed
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