1887
  1. Home
  2. Eurosurveillance
  3. Volume 28, Issue 42, 19/Oct/2023
  4. Article
Research Open Access
Like 0
Download

Abstract

Background

Since 2021, an emergence of New Delhi metallo-β-lactamase (NDM)-14-producing has been identified in France. This variant with increased carbapenemase activity was not previously detected in Enterobacterales.

Aim

We investigated the rapid dissemination of NDM-14 producers among patients in hospitals in France.

Methods

All NDM-14-producing non-duplicate clinical isolates identified in France until June 2022 (n = 37) were analysed by whole genome sequencing. The phylogeny of NDM-14-producers among all sequence type (ST) 147 reported in France since 2014 (n = 431) was performed. Antimicrobial susceptibility testing, conjugation experiments, clonal relationship and molecular clock analysis were performed.

Results

The 37 NDM-14 producers recovered in France until 2022 belonged to ST147. The dissemination of NDM-14-producing was linked to a single clone, likely imported from Morocco and responsible for several outbreaks in France. The gene was harboured on a 54 kilobase non-conjugative IncFIB plasmid that shared high homology with a known -carrying plasmid. Using Bayesian analysis, we estimated that the NDM-14-producing ST147 clone appeared in 2020. The evolutionary rate of this clone was estimated to 5.61 single nucleotide polymorphisms per genome per year. The NDM-14 producers were highly resistant to all antimicrobials tested except to colistin, cefiderocol (minimum inhibitory concentration 2 mg/L) and the combination of aztreonam/avibactam.

Conclusion

Highly resistant NDM-14 producing can rapidly spread in healthcare settings. Surveillance and thorough investigations of hospital outbreaks are critical to evaluate and limit the dissemination of this clone.

© Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2023.28.42.2300095
2023-10-19
2024-04-27
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2023.28.42.2300095
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/28/42/eurosurv-28-42-3.html?itemId=/content/10.2807/1560-7917.ES.2023.28.42.2300095&mimeType=html&fmt=ahah

References

  1. Naas T, Dortet L, Iorga BI. Structural and functional aspects of class A carbapenemases. Curr Drug Targets. 2016;17(9):1006-28.  https://doi.org/10.2174/1389450117666160310144501  PMID: 26960341 
  2. Mojica MF, Bonomo RA, Fast W. B1-metallo-β-lactamases: where do we stand? Curr Drug Targets. 2016;17(9):1029-50.  https://doi.org/10.2174/1389450116666151001105622  PMID: 26424398 
  3. 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 
  4. 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 
  5. Dortet L, Poirel L, Nordmann P. Worldwide dissemination of the NDM-type carbapenemases in Gram-negative bacteria. BioMed Res Int. 2014;2014:249856.  https://doi.org/10.1155/2014/249856  PMID: 24790993 
  6. 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):e00115-8.  https://doi.org/10.1128/CMR.00115-18  PMID: 30700432 
  7. Yong D, Toleman MA, Giske CG, Cho HS, Sundman K, Lee K, et al. Characterization of a new metallo-beta-lactamase gene, bla(NDM-1), and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae sequence type 14 from India. Antimicrob Agents Chemother. 2009;53(12):5046-54.  https://doi.org/10.1128/AAC.00774-09  PMID: 19770275 
  8. Naas T, Oueslati S, Bonnin RA, Dabos ML, Zavala A, Dortet L, et al. Beta-lactamase database (BLDB) - structure and function. J Enzyme Inhib Med Chem. 2017;32(1):917-9.  https://doi.org/10.1080/14756366.2017.1344235  PMID: 28719998 
  9. Zou D, Huang Y, Zhao X, Liu W, Dong D, Li H, et al. A novel New Delhi metallo-β-lactamase variant, NDM-14, isolated in a Chinese Hospital possesses increased enzymatic activity against carbapenems. Antimicrob Agents Chemother. 2015;59(4):2450-3.  https://doi.org/10.1128/AAC.05168-14  PMID: 25645836 
  10. Logan LK, Weinstein RA. The epidemiology of carbapenem-resistant Enterobacteriaceae: the impact and evolution of a global menace. J Infect Dis. 2017;215(suppl_1):S28-36.  https://doi.org/10.1093/infdis/jiw282  PMID: 28375512 
  11. Patiño-Navarrete R, Rosinski-Chupin I, Cabanel N, Zongo PD, Héry M, Oueslati S, et al. Specificities and commonalities of carbapenemase-producing Escherichia coli isolated in France from 2012 to 2015. mSystems. 2022;7(1):e0116921.  https://doi.org/10.1128/msystems.01169-21  PMID: 35014866 
  12. Peirano G, Chen L, Kreiswirth BN, Pitout JDD. Emerging Antimicrobial-resistant high-risk Klebsiella pneumoniae clones ST307 and ST147. Antimicrob Agents Chemother. 2020;64(10):e01148-20.  https://doi.org/10.1128/AAC.01148-20  PMID: 32747358 
  13. Melegh S, Schneider G, Horváth M, Jakab F, Emődy L, Tigyi Z. Identification and characterization of CTX-M-15 producing Klebsiella pneumoniae clone ST101 in a Hungarian university teaching hospital. Acta Microbiol Immunol Hung. 2015;62(3):233-45.  https://doi.org/10.1556/030.62.2015.3.2  PMID: 26551567 
  14. Bonnin RA, Jousset AB, Chiarelli A, Emeraud C, Glaser P, Naas T, et al. Emergence of new non–clonal group 258 high-risk clones among Klebsiella pneumoniae carbapenemase–producing K. pneumoniae isolates, France. Emerg Infect Dis. 2020;26(6):1212-20.  https://doi.org/10.3201/eid2606.191517  PMID: 32441629 
  15. Mendes G, Ramalho JF, Bruschy-Fonseca A, Lito L, Duarte A, Melo-Cristino J, et al. Whole-genome sequencing enables molecular characterization of non-clonal group 258 high-risk clones (ST13, ST17, ST147 and ST307) among carbapenem-resistant Klebsiella pneumoniae from a tertiary university hospital centre in Portugal. Microorganisms. 2022;10(2):416.  https://doi.org/10.3390/microorganisms10020416  PMID: 35208876 
  16. Samuelsen Ø, Toleman MA, Hasseltvedt V, Fuursted K, Leegaard TM, Walsh TR, et al. Molecular characterization of VIM-producing Klebsiella pneumoniae from Scandinavia reveals genetic relatedness with international clonal complexes encoding transferable multidrug resistance. Clin Microbiol Infect. 2011;17(12):1811-6.  https://doi.org/10.1111/j.1469-0691.2011.03532.x  PMID: 21595797 
  17. Grami R, Mansour W, Ben Haj Khalifa A, Dahmen S, Chatre P, Haenni M, et al. Emergence of ST147 Klebsiella pneumoniae producing OXA-204 carbapenemase in a university hospital, Tunisia. Microb Drug Resist. 2016;22(2):137-40.  https://doi.org/10.1089/mdr.2014.0278  PMID: 26447939 
  18. Liapis E, Pantel A, Robert J, Nicolas-Chanoine MH, Cavalié L, van der Mee-Marquet N, et al. Molecular epidemiology of OXA-48-producing Klebsiella pneumoniae in France. Clin Microbiol Infect. 2014;20(12):O1121-3.  https://doi.org/10.1111/1469-0691.12727  PMID: 24942039 
  19. Nahid F, Zahra R, Sandegren L. A blaOXA-181-harbouring multi-resistant ST147 Klebsiella pneumoniae isolate from Pakistan that represent an intermediate stage towards pan-drug resistance. PLoS One. 2017;12(12):e0189438.  https://doi.org/10.1371/journal.pone.0189438  PMID: 29220374 
  20. Peirano G, Pillai DR, Pitondo-Silva A, Richardson D, Pitout JDD. The characteristics of NDM-producing Klebsiella pneumoniae from Canada. Diagn Microbiol Infect Dis. 2011;71(2):106-9.  https://doi.org/10.1016/j.diagmicrobio.2011.06.013  PMID: 21924993 
  21. Biedrzycka M, Urbanowicz P, Guzek A, Brisse S, Gniadkowski M, Izdebski R. Dissemination of Klebsiella pneumoniae ST147 NDM-1 in Poland, 2015-19. J Antimicrob Chemother. 2021;76(10):2538-45.  https://doi.org/10.1093/jac/dkab207  PMID: 34164678 
  22. Di Pilato V, Henrici De Angelis L, Aiezza N, Baccani I, Niccolai C, Parisio EM, et al. Resistome and virulome accretion in an NDM-1-producing ST147 sublineage of Klebsiella pneumoniae associated with an outbreak in Tuscany, Italy: a genotypic and phenotypic characterisation. Lancet Microbe. 2022;3(3):e224-34.  https://doi.org/10.1016/S2666-5247(21)00268-8  PMID: 35544076 
  23. Takei S, Lu YJ, Tohya M, Watanabe S, Misawa S, Tabe Y, et al. Spread of carbapenem-resistant Klebsiella pneumoniae clinical isolates producing NDM-type metallo-β-lactamase in Myanmar. Microbiol Spectr. 2022;10(4):e0067322.  https://doi.org/10.1128/spectrum.00673-22  PMID: 35762817 
  24. Muraya A, Kyany’a C, Kiyaga S, Smith HJ, Kibet C, Martin MJ, et al. Antimicrobial resistance and virulence characteristics of Klebsiella pneumoniae isolates in Kenya by whole-genome sequencing. Pathogens. 2022;11(5):545.  https://doi.org/10.3390/pathogens11050545  PMID: 35631066 
  25. Wang C, Yang D, Wang Y, Ni W. Cefiderocol for the Treatment of multidrug-resistant Gram-negative bacteria: A systematic review of currently available evidence. Front Pharmacol. 2022;13:896971.  https://doi.org/10.3389/fphar.2022.896971  PMID: 35496290 
  26. Bonnin RA, Emeraud C, Jousset AB, Naas T, Dortet L. Comparison of disk diffusion, MIC test strip and broth microdilution methods for cefiderocol susceptibility testing on carbapenem-resistant enterobacterales. Clin Microbiol Infect. 2022;28(8):1156.e1-5.  https://doi.org/10.1016/j.cmi.2022.04.013  PMID: 35533970 
  27. Emeraud C, Escaut L, Boucly A, Fortineau N, Bonnin RA, Naas T, et al. Aztreonam plus clavulanate, tazobactam, or avibactam for treatment of infections caused by metallo-β-lactamase-producing Gram-negative bacteria. Antimicrob Agents Chemother. 2019;63(5):e00010-9.  https://doi.org/10.1128/AAC.00010-19  PMID: 30858212 
  28. Emeraud C, Gonzalez C, Dortet L. Comparison of ComASP® and UMIC® methods with the reference method for cefiderocol susceptibility testing on carbapenem-resistant Enterobacterales. J Antimicrob Chemother. 2023;78(7):1800-1.  https://doi.org/10.1093/jac/dkad134  PMID: 37141286 
  29. Dortet L, Niccolai C, Pfennigwerth N, Frisch S, Gonzalez C, Antonelli A, et al. Performance evaluation of the UMIC® Cefiderocol to determine MIC in Gram-negative bacteria. J Antimicrob Chemother. 2023;78(7):1672-6.  https://doi.org/10.1093/jac/dkad149  PMID: 37209112 
  30. Lartigue M-F, Poirel L, Aubert D, Nordmann P. In vitro analysis of ISEcp1B-mediated mobilization of naturally occurring beta-lactamase gene blaCTX-M of Kluyvera ascorbata. Antimicrob Agents Chemother. 2006;50(4):1282-6.  https://doi.org/10.1128/AAC.50.4.1282-1286.2006  PMID: 16569841 
  31. Girlich D, Bonnin RA, Proust A, Naas T, Dortet L. Undetectable production of the VIM-1 carbapenemase in an Atlantibacter hermannii clinical isolate. Front Microbiol. 2021;12:741972.  https://doi.org/10.3389/fmicb.2021.741972  PMID: 34987484 
  32. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32(1):268-74.  https://doi.org/10.1093/molbev/msu300  PMID: 25371430 
  33. 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 
  34. Dellicour S, Gill MS, Faria NR, Rambaut A, Pybus OG, Suchard MA, et al. Relax, keep walking — a practical guide to continuous phylogeographic inference with BEAST. Mol Biol Evol. 2021;38(8):3486-93.  https://doi.org/10.1093/molbev/msab031  PMID: 33528560 
  35. Rodrigues C, Desai S, Passet V, Gajjar D, Brisse S. Genomic evolution of the globally disseminated multidrug-resistant Klebsiella pneumoniae clonal group 147. Microb Genom. 2022;8(1):000737.  https://doi.org/10.1099/mgen.0.000737  PMID: 35019836 
  36. 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(9):4224-9.  https://doi.org/10.1128/AAC.00165-11  PMID: 21746951 
  37. Tang B, Wang C, Sun D, Lin H, Ma J, Guo H, et al. In silico characterization of blaNDM-harboring conjugative plasmids in Acinetobacter species. Microbiol Spectr. 2022;10(6):e0210222.  https://doi.org/10.1128/spectrum.02102-22  PMID: 36301090 
  38. Poirel L, Bonnin RA, Boulanger A, Schrenzel J, Kaase M, Nordmann P. Tn125-related acquisition of blaNDM-like genes in Acinetobacter baumannii. Antimicrob Agents Chemother. 2012;56(2):1087-9.  https://doi.org/10.1128/AAC.05620-11  PMID: 22143526 
  39. Leavitt A, Carmeli Y, Chmelnitsky I, Goren MG, Ofek I, Navon-Venezia S. Molecular epidemiology, sequence types, and plasmid analyses of KPC-producing Klebsiella pneumoniae strains in Israel. Antimicrob Agents Chemother. 2010;54(7):3002-6.  https://doi.org/10.1128/AAC.01818-09  PMID: 20350950 
  40. David S, Reuter S, Harris SR, Glasner C, Feltwell T, Argimon S, et al. Epidemic of carbapenem-resistant Klebsiella pneumoniae in Europe is driven by nosocomial spread. Nat Microbiol. 2019;4(11):1919-29.  https://doi.org/10.1038/s41564-019-0492-8  PMID: 31358985 
  41. Bowers JR, Kitchel B, Driebe EM, MacCannell DR, Roe C, Lemmer D, et al. Genomic analysis of the emergence and rapid global dissemination of the clonal group 258 Klebsiella pneumoniae pandemic. PLoS One. 2015;10(7):e0133727.  https://doi.org/10.1371/journal.pone.0133727  PMID: 26196384 
  42. Wyres KL, Hawkey J, Hetland MAK, Fostervold A, Wick RR, Judd LM, et al. Emergence and rapid global dissemination of CTX-M-15-associated Klebsiella pneumoniae strain ST307. J Antimicrob Chemother. 2019;74(3):577-81.  https://doi.org/10.1093/jac/dky492  PMID: 30517666 
  43. Roe CC, Vazquez AJ, Esposito EP, Zarrilli R, Sahl JW. Diversity, virulence, and antimicrobial resistance in isolates from the newly emerging Klebsiella pneumoniae ST101 lineage. Front Microbiol. 2019;10:542.  https://doi.org/10.3389/fmicb.2019.00542  PMID: 31001209 
Emergence and rapid dissemination of highly resistant NDM-14-producing Klebsiella pneumoniae ST147, France, 2022
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=C%C3%A9cile+Emeraud&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Emeraud Cécile</a>, <a href="/search?value1=Aba+Mahamat&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Mahamat Aba</a>, <a href="/search?value1=Agn%C3%A8s+B.+Jousset&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Jousset Agnès B.</a>, <a href="/search?value1=Sandrine+Bernabeu&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Bernabeu Sandrine</a>, <a href="/search?value1=Tania+Goncalves&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Goncalves Tania</a>, <a href="/search?value1=Camille+Pommier&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Pommier Camille</a>, <a href="/search?value1=Delphine+Girlich&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Girlich Delphine</a>, <a href="/search?value1=Aur%C3%A9lien+Birer&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Birer Aurélien</a>, <a href="/search?value1=Christophe+Rodriguez&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Rodriguez Christophe</a>, <a href="/search?value1=Jean-Michel+Pawlotsky&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Pawlotsky Jean-Michel</a>, <a href="/search?value1=Thierry+Naas&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Naas Thierry</a>, <a href="/search?value1=R%C3%A9my+A.+Bonnin&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Bonnin Rémy A.</a>, <a href="/search?value1=Laurent+Dortet&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Dortet Laurent</a></span>. Emergence and rapid dissemination of highly resistant NDM-14-producing Klebsiella pneumoniae ST147, France, 2022. <a href="/content/ecdc">Euro Surveill.</a> 2023;28(42):pii=2300095. <a href="https://doi.org/10.2807/1560-7917.ES.2023.28.42.2300095" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2023.28.42.2300095</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 06 Feb 2023;&nbsp;&nbsp; <span class="generated">Accepted</span>: 26 Jun 2023 </span> </p>
/content/10.2807/1560-7917.ES.2023.28.42.2300095
/content/10.2807/1560-7917.ES.2023.28.42.2300095
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