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Abstract

Background

Carbapenemase-producing Enterobacterales (CPE) are rapidly increasing worldwide, also in Europe. Although prevalence of CPE in Germany is comparatively low, the National Reference Centre for Multidrug-resistant Gram-negative Bacteria noted annually increasing numbers of NDM-5-producing isolates.

Aim

As part of our ongoing surveillance programme, we characterised NDM-5-producing isolates received between 2013 and 2019 using whole genome sequencing (WGS).

Methods

From 329 identified NDM-5-producing , 224 isolates from known geographical locations were subjected to Illumina WGS. Analyses of 222 sequenced isolates included multilocus sequence typing (MLST), core genome (cg)MLST and single-nucleotide polymorphism (SNP)-based analyses.

Results

Results of cgMLST revealed genetically distinct clusters for many of the 43 detected sequence types (ST), of which ST167, ST410, ST405 and ST361 predominated. The SNP-based phylogenetic analyses combined with geographical information identified sporadic cases of nosocomial transmission on a small spatial scale. However, we identified large clusters corresponding to clonal dissemination of ST167, ST410, ST405 and ST361 strains in consecutive years in different regions in Germany.

Conclusion

Occurrence of NDM-5-producing rose in Germany, which was to a large extent due to the increased prevalence of isolates belonging to the international high-risk clones ST167, ST410, ST405 and ST361. Of particular concern is the supra-regional dissemination of these epidemic clones. Available information suggest community spread of NDM-5-producing in Germany, highlighting the importance of epidemiological investigation and an integrated surveillance system in the One Health framework.

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/content/10.2807/1560-7917.ES.2023.28.10.2200509
2023-03-09
2024-06-19
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2023.28.10.2200509
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References

  1. Brolund A, Lagerqvist N, Byfors S, Struelens MJ, Monnet DL, Albiger B, et al. Worsening epidemiological situation of carbapenemase-producing Enterobacteriaceae in Europe, assessment by national experts from 37 countries, July 2018. Euro Surveill. 2019;24(9):1900123.  https://doi.org/10.2807/1560-7917.ES.2019.24.9.1900123  PMID: 30862330 
  2. Pfennigwerth N. Bericht des Nationalen Referenzzentrums für gramnegative Krankenhauserreger, 2018. [Report of the national reference centre for Gram-negative hospital pathogens]. Epid Bull. 2019;31:289-94. German. Available from: https://www.rki.de/DE/Content/Infekt/EpidBull/Archiv/2019/Ausgaben/31_19.pdf
  3. Kremer K, Kramer R, Neumann B, Haller S, Pfennigwerth N, Werner G, et al. Rapid spread of OXA-244-producing Escherichia coli ST38 in Germany: insights from an integrated molecular surveillance approach; 2017 to January 2020. Euro Surveill. 2020;25(25):2000923.  https://doi.org/10.2807/1560-7917.ES.2020.25.25.2000923  PMID: 32613940 
  4. Hornsey M, Phee L, Wareham DW. A novel variant, NDM-5, of the New Delhi metallo-β-lactamase in a multidrug-resistant Escherichia coli ST648 isolate recovered from a patient in the United Kingdom. Antimicrob Agents Chemother. 2011;55(12):5952-4.  https://doi.org/10.1128/AAC.05108-11  PMID: 21930874 
  5. Wu W, Feng Y, Tang G, Qiao F, McNally A, Zong Z. NDM metallo-β-Lactamases and their bacterial producers in health care settings. Clin Microbiol Rev. 2019;32(2):e00115.  https://doi.org/10.1128/CMR.00115-18  PMID: 30700432 
  6. Bi R, Kong Z, Qian H, Jiang F, Kang H, Gu B, et al. High prevalence of blaNDM variants among carbapenem-resistant Escherichia coli in Northern Jiangsu Province, China. Front Microbiol. 2018;9:2704.  https://doi.org/10.3389/fmicb.2018.02704  PMID: 30483231 
  7. Baraniak A, Izdebski R, Fiett J, Gawryszewska I, Bojarska K, Herda M, et al. NDM-producing Enterobacteriaceae in Poland, 2012-14: inter-regional outbreak of Klebsiella pneumoniae ST11 and sporadic cases. J Antimicrob Chemother. 2016;71(1):85-91.  https://doi.org/10.1093/jac/dkv282  PMID: 26386745 
  8. Bitar I, Piazza A, Gaiarsa S, Villa L, Pedroni P, Oliva E, et al. ST405 NDM-5 producing Escherichia coli in Northern Italy: the first two clinical cases. Clin Microbiol Infect. 2017;23(7):489-90.  https://doi.org/10.1016/j.cmi.2017.01.020  PMID: 28159670 
  9. Barrado L, Pérez-Vázquez M, Del Pozo JL, Martín-Salas C, Leiva J, Mazón A, et al. Clonal transmission of NDM-5-producing Escherichia coli belonging to high-risk sequence type ST405. Int J Antimicrob Agents. 2018;52(1):123-4.  https://doi.org/10.1016/j.ijantimicag.2018.05.018  PMID: 29864499 
  10. Bathoorn E, Rossen JW, Lokate M, Friedrich AW, Hammerum AM. Isolation of an NDM-5-producing ST16 Klebsiella pneumoniae from a Dutch patient without travel history abroad, August 2015. Euro Surveill. 2015;20(41):30040.  https://doi.org/10.2807/1560-7917.ES.2015.20.41.30040  PMID: 26537842 
  11. Hammerum AM, Hansen F, Olesen B, Struve C, Holzknecht BJ, Andersen PS, et al. Investigation of a possible outbreak of NDM-5-producing ST16 Klebsiella pneumoniae among patients in Denmark with no history of recent travel using whole-genome sequencing. J Glob Antimicrob Resist. 2015;3(3):219-21.  https://doi.org/10.1016/j.jgar.2015.05.003  PMID: 27873714 
  12. Pitart C, Solé M, Roca I, Román A, Moreno A, Vila J, et al. Molecular characterization of blaNDM-5 carried on an IncFII plasmid in an Escherichia coli isolate from a nontraveler patient in Spain. Antimicrob Agents Chemother. 2015;59(1):659-62.  https://doi.org/10.1128/AAC.04040-14  PMID: 25313215 
  13. Sadek M, Poirel L, Nordmann P, Nariya H, Shimamoto T, Shimamoto T. Genetic characterisation of NDM-1 and NDM-5-producing Enterobacterales from retail chicken meat in Egypt. J Glob Antimicrob Resist. 2020;23:70-1.  https://doi.org/10.1016/j.jgar.2020.07.031  PMID: 32889140 
  14. Ma Z, Zeng Z, Liu J, Liu C, Pan Y, Zhang Y, et al. Emergence of IncHI2 plasmid-harboring blaNDM-5 from porcine Escherichia coli isolates in Guangdong, China. Pathogens. 2021;10(8):954.  https://doi.org/10.3390/pathogens10080954  PMID: 34451418 
  15. Grönthal T, Österblad M, Eklund M, Jalava J, Nykäsenoja S, Pekkanen K, et al. Sharing more than friendship - transmission of NDM-5 ST167 and CTX-M-9 ST69 Escherichia coli between dogs and humans in a family, Finland, 2015. Euro Surveill. 2018;23(27):1700497.  https://doi.org/10.2807/1560-7917.ES.2018.23.27.1700497  PMID: 29991384 
  16. Ahlstrom CA, Woksepp H, Sandegren L, Mohsin M, Hasan B, Muzyka D, et al. Genomically diverse carbapenem resistant Enterobacteriaceae from wild birds provide insight into global patterns of spatiotemporal dissemination. Sci Total Environ. 2022;824:153632.  https://doi.org/10.1016/j.scitotenv.2022.153632  PMID: 35124031 
  17. Almakki A, Maure A, Pantel A, Romano-Bertrand S, Masnou A, Marchandin H, et al. NDM-5-producing Escherichia coli in an urban river in Montpellier, France. Int J Antimicrob Agents. 2017;50(1):123-4.  https://doi.org/10.1016/j.ijantimicag.2017.04.003  PMID: 28435018 
  18. Bleichenbacher S, Stevens MJA, Zurfluh K, Perreten V, Endimiani A, Stephan R, et al. Environmental dissemination of carbapenemase-producing Enterobacteriaceae in rivers in Switzerland. Environ Pollut. 2020;265(Pt B):115081.  https://doi.org/10.1016/j.envpol.2020.115081  PMID: 32806462 
  19. Peirano G, Chen L, Nobrega D, Finn TJ, Kreiswirth BN, DeVinney R, et al. Genomic epidemiology of global carbapenemase-producing Escherichia coli, 2015-2017. Emerg Infect Dis. 2022;28(5):924-31.  https://doi.org/10.3201/eid2805.212535  PMID: 35451367 
  20. Bibbolino G, Di Lella FM, Oliva A, Lichtner M, Del Borgo C, Raponi G, et al. Molecular epidemiology of NDM-5-producing Escherichia coli high-risk clones identified in two Italian hospitals in 2017-2019. Diagn Microbiol Infect Dis. 2021;100(4):115399.  https://doi.org/10.1016/j.diagmicrobio.2021.115399  PMID: 34030105 
  21. Chakraborty T, Sadek M, Yao Y, Imirzalioglu C, Stephan R, Poirel L, et al. Cross-border emergence of Escherichia coli producing the carbapenemase NDM-5 in Switzerland and Germany. J Clin Microbiol. 2021;59(3):e02238-20.  https://doi.org/10.1128/JCM.02238-20  PMID: 33361340 
  22. Findlay J, Poirel L, Kessler J, Kronenberg A, Nordmann P. New Delhi metallo-β-lactamase-producing Enterobacterales bacteria, Switzerland, 2019-2020. Emerg Infect Dis. 2021;27(10):2628-37.  https://doi.org/10.3201/eid2710.211265  PMID: 34545787 
  23. European Committee on Antimicrobial Susceptibility Testing (EUCAST). Breakpoint tables for interpretation of MICs and zone diameters, Version 12.0. Växjö: EUCAST; 2022. Available from: https://www. eucast.org/clinical_breakpoints
  24. Pfennigwerth N, Gatermann SG, Körber-Irrgang B, Hönings R. Phenotypic detection and differentiation of carbapenemase classes including OXA-48-like enzymes in Enterobacterales and Pseudomonas aeruginosa by a highly specialized MICRONAUT-S microdilution assay. J Clin Microbiol. 2020;58(11):e00171-20.  https://doi.org/10.1128/JCM.00171-20  PMID: 32878951 
  25. Andrews S. FastQC: a quality control tool for high throughput sequence data. Cambridge: Babraham Institute. [Accessed: 28 Jan 2021]. Available from: https://www.bioinformatics.babraham.ac.uk/projects/fastqc
  26. Ondov BD, Treangen TJ, Melsted P, Mallonee AB, Bergman NH, Koren S, et al. Mash: fast genome and metagenome distance estimation using MinHash. Genome Biol. 2016;17(1):132.  https://doi.org/10.1186/s13059-016-0997-x  PMID: 27323842 
  27. Ondov BD, Starrett GJ, Sappington A, Kostic A, Koren S, Buck CB, et al. Mash Screen: high-throughput sequence containment estimation for genome discovery. Genome Biol. 2019;20(1):232.  https://doi.org/10.1186/s13059-019-1841-x  PMID: 31690338 
  28. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19(5):455-77.  https://doi.org/10.1089/cmb.2012.0021  PMID: 22506599 
  29. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics. 2013;29(8):1072-5.  https://doi.org/10.1093/bioinformatics/btt086  PMID: 23422339 
  30. Seemann T. ABRicate: Mass screening of contigs for antimicrobial resistance or virulence genee GitHub. [Accessed: 18 Sep 2021]. Available from: https://github.com/tseemann/abricate
  31. Feldgarden M, Brover V, Haft DH, Prasad AB, Slotta DJ, Tolstoy I, et al. Validating the AMRFinder tool and resistance gene database by using antimicrobial resistance genotype-phenotype correlations in a collection of isolates. Antimicrob Agents Chemother. 2019;63(11):e00483-19.  https://doi.org/10.1128/AAC.00483-19  PMID: 31427293 
  32. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 2021;49(W1):W293-6.  https://doi.org/10.1093/nar/gkab301  PMID: 33885785 
  33. Emeraud C, Girlich D, Bonnin RA, Jousset AB, Naas T, Dortet L. Emergence and polyclonal dissemination of OXA-244-producing Escherichia coli, France. Emerg Infect Dis. 2021;27(4):1206-10.  https://doi.org/10.3201/eid2704.204459  PMID: 33755001 
  34. Dortet L, Cuzon G, Ponties V, Nordmann P. Trends in carbapenemase-producing Enterobacteriaceae, France, 2012 to 2014. Euro Surveill. 2017;22(6):30461.  https://doi.org/10.2807/1560-7917.ES.2017.22.6.30461  PMID: 28205502 
  35. Ramette A, Gasser M, Nordmann P, Zbinden R, Schrenzel J, Perisa D, et al. Temporal and regional incidence of carbapenemase-producing Enterobacterales, Switzerland, 2013 to 2018. Euro Surveill. 2021;26(15):1900760.  https://doi.org/10.2807/1560-7917.ES.2021.26.15.1900760  PMID: 33860749 
  36. Giufrè M, Errico G, Accogli M, Monaco M, Villa L, Distasi MA, et al. Emergence of NDM-5-producing Escherichia coli sequence type 167 clone in Italy. Int J Antimicrob Agents. 2018;52(1):76-81.  https://doi.org/10.1016/j.ijantimicag.2018.02.020  PMID: 29501819 
  37. Garcia-Fernandez A, Villa L, Bibbolino G, Bressan A, Trancassini M, Pietropaolo V, et al. Novel insights and features of the NDM-5-producing Escherichia coli sequence type 167 high-risk clone. MSphere. 2020;5(2):e00269-20.  https://doi.org/10.1128/mSphere.00269-20  PMID: 32350092 
  38. Bitar I, Piazza A, Gaiarsa S, Villa L, Pedroni P, Oliva E, et al. ST405 NDM-5 producing Escherichia coli in Northern Italy: the first two clinical cases. Clin Microbiol Infect. 2017;23(7):489-90.  https://doi.org/10.1016/j.cmi.2017.01.020  PMID: 28159670 
  39. Corbellini S, Scaltriti E, Piccinelli G, Gurrieri F, Mascherpa M, Boroni G, et al. Genomic characterisation of Escherichia coli isolates co-producing NDM-5 and OXA-1 from hospitalised patients with invasive infections. J Glob Antimicrob Resist. 2022;28:136-9.  https://doi.org/10.1016/j.jgar.2021.12.018  PMID: 34965471 
  40. Peterhans S, Stevens MJA, Nüesch-Inderbinen M, Schmitt S, Stephan R, Zurfluh K. First report of a blaNDM-5-harbouring Escherichia coli ST167 isolated from a wound infection in a dog in Switzerland. J Glob Antimicrob Resist. 2018;15:226-7.  https://doi.org/10.1016/j.jgar.2018.10.013  PMID: 30339894 
  41. Reynolds ME, Phan HTT, George S, Hubbard ATM, Stoesser N, Maciuca IE, et al. Occurrence and characterization of Escherichia coli ST410 co-harbouring blaNDM-5, blaCMY-42 and blaTEM-190 in a dog from the UK. J Antimicrob Chemother. 2019;74(5):1207-11.  https://doi.org/10.1093/jac/dkz017  PMID: 30753576 
  42. Alba P, Taddei R, Cordaro G, Fontana MC, Toschi E, Gaibani P, et al. Carbapenemase IncF-borne blaNDM-5 gene in the E. coli ST167 high-risk clone from canine clinical infection, Italy. Vet Microbiol. 2021;256:109045.  https://doi.org/10.1016/j.vetmic.2021.109045  PMID: 33887564 
  43. Falgenhauer L, Imirzalioglu C, Ghosh H, Gwozdzinski K, Schmiedel J, Gentil K, et al. Circulation of clonal populations of fluoroquinolone-resistant CTX-M-15-producing Escherichia coli ST410 in humans and animals in Germany. Int J Antimicrob Agents. 2016;47(6):457-65.  https://doi.org/10.1016/j.ijantimicag.2016.03.019  PMID: 27208899 
  44. Irrgang A, Falgenhauer L, Fischer J, Ghosh H, Guiral E, Guerra B, et al. CTX-M-15-producing E. coli isolates from food products in Germany are mainly associated with an IncF-type plasmid and belong to two predominant clonal E. coli lineages. Front Microbiol. 2017;8:2318.  https://doi.org/10.3389/fmicb.2017.02318  PMID: 29209306 
  45. Roer L, Overballe-Petersen S, Hansen F, Schønning K, Wang M, Røder BL, et al. Escherichia coli sequence type 410 is causing new international high-risk clones. MSphere. 2018;3(4):e00337-18.  https://doi.org/10.1128/mSphere.00337-18  PMID: 30021879 
  46. Tsilipounidaki K, Athanasakopoulou Z, Billinis C, Miriagou V, Petinaki E. Letter to the Editor: Importation of the First Bovine ST361 New Delhi Metallo-5 Positive Escherichia coli in Greece. Microb Drug Resist. 2022;28(3):386-7. https://doi.org/10.1128/mSphere.00337-18  PMID: 34935518 
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