1887
  1. Home
  2. Eurosurveillance
  3. Volume 29, Issue 11, 14/Mar/2024
  4. Article
Research Open Access
Like 0
Download

SDG 3: Antimicrobial resistance

Abstract

Background

From 2019 to 2022, the French National Reference Centre for Antibiotic Resistance (NRC) received a total of 25 isolates of subsp. sequence type (ST)1740. All produced metallo-β-lactamase(s) and were from the Lyon area.

Aim

To understand these strains’ spread and evolution, more extended microbiological and molecular analyses were conducted.

Methods

Patients’ demographics and specimen type related to isolates were retrieved. All strains underwent short-read whole genome sequencing, and for 15, long-read sequencing to understand carbapenemase-gene acquisition. Clonal relationships were inferred from core-genome single nt polymorphisms (SNPs). Plasmids and the close genetic environment of each carbapenemase-encoding gene were analysed.

Results

Patients (10 female/15 male) were on average 56.6 years old. Seven isolates were recovered from infections and 18 through screening. With ≤ 27 SNPs difference between each other’s genome sequences, the 25 strains represented a clone dissemination. All possessed a chromosome-encoded gene inside a composite transposon flanked by two IS. While spreading, the clone independently acquired a -carrying plasmid of IncHI2 type (n = 12 isolates), or a -carrying plasmid of IncP-1 type (n = 1 isolate). Of the 12 isolates co-producing NDM-1 and VIM-4, seven harboured the colistin resistance gene ; the remaining five likely lost this gene through excision.

Conclusion

This long-term outbreak was caused by a chromosome-encoded NDM-1-producing ST1740 subsp. clone, which, during its dissemination, acquired plasmids encoding VIM-4 or IMP-13 metallo-β-lactamases. To our knowledge, IMP-13 has not prior been reported in Enterobacterales in France. Epidemiological and environmental investigations should be considered alongside microbiological and molecular ones.

© 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.2024.29.11.2300521
2024-03-14
2024-04-27
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2024.29.11.2300521
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/29/11/eurosurv-29-11_2.html?itemId=/content/10.2807/1560-7917.ES.2024.29.11.2300521&mimeType=html&fmt=ahah

References

  1. Nordmann P, Dortet L, Poirel L. Carbapenem resistance in Enterobacteriaceae: here is the storm! Trends Mol Med. 2012;18(5):263-72.  https://doi.org/10.1016/j.molmed.2012.03.003  PMID: 22480775 
  2. Bonomo RA, Burd EM, Conly J, Limbago BM, Poirel L, Segre JA, et al. Carbapenemase-producing organisms: a global scourge. Clin Infect Dis. 2018;66(8):1290-7.  https://doi.org/10.1093/cid/cix893  PMID: 29165604 
  3. Mojica MF, Bonomo RA, Fast W. B1-Metallo-beta-lactamases: where do we stand? Curr Drug Targets. 2016;17(9):1029-50.  https://doi.org/10.2174/1389450116666151001105622  PMID: 26424398 
  4. Santé Publique France. Caractéristiques et évolution des souches d’entérobactéries productrices de carbapénémases (EPC) isolées en France, 2012-2020. https://www.santepubliquefrance.fr/import/caracteristiques-et-evolution-des-souches-d-enterobacteries-productrices-de-carbapenemases-epc-isolees-en-france-2012-2020; 2021. [accessed January 24th, 2024]
  5. Davin-Regli A, Pagès JM. Enterobacter aerogenes and Enterobacter cloacae; versatile bacterial pathogens confronting antibiotic treatment. Front Microbiol. 2015;6:392.  https://doi.org/10.3389/fmicb.2015.00392  PMID: 26042091 
  6. Dong X, Zhu M, Li Y, Huang D, Wang L, Yan C, et al. Whole-genome sequencing-based species classification, multilocus sequence typing, and antimicrobial resistance mechanism analysis of the Enterobacter cloacae complex in Southern China. Microbiol Spectr. 2022;10(6):e0216022.  https://doi.org/10.1128/spectrum.02160-22  PMID: 36350178 
  7. Chavda KD, Chen L, Fouts DE, Sutton G, Brinkac L, Jenkins SG, et al. Comprehensive genome analysis of carbapenemase-producing Enterobacter spp.: new insights into phylogeny, population structure, and resistance mechanisms. MBio. 2016;7(6):e02093-16.  https://doi.org/10.1128/mBio.02093-16  PMID: 27965456 
  8. Emeraud C, Petit C, Gauthier L, Bonnin RA, Naas T, Dortet L. Emergence of VIM-producing Enterobacter cloacae complex in France between 2015 and 2018. J Antimicrob Chemother. 2022;77(4):944-51.  https://doi.org/10.1093/jac/dkab471  PMID: 35045171 
  9. Santella G, Pollini S, Docquier JD, Mereuta AI, Gutkind G, Rossolini GM, et al. Intercontinental dissemination of IMP-13-producing Pseudomonas aeruginosa belonging in sequence type 621. J Clin Microbiol. 2010;48(11):4342-3.  https://doi.org/10.1128/JCM.00614-10  PMID: 20844220 
  10. Bernabeu S, Bonnin RA, Dortet L. Comment on: Comparison of three lateral flow immunochromatographic assays for the rapid detection of KPC, NDM, IMP, VIM and OXA-48 carbapenemases in Enterobacterales. J Antimicrob Chemother. 2023;78(1):314-7.  https://doi.org/10.1093/jac/dkac381  PMID: 36376016 
  11. Dortet L, Bréchard L, Poirel L, Nordmann P. Impact of the isolation medium for detection of carbapenemase-producing Enterobacteriaceae using an updated version of the Carba NP test. J Med Microbiol. 2014;63(5):772-6.  https://doi.org/10.1099/jmm.0.071340-0  PMID: 24591705 
  12. European Committee on Antimicrobial Susceptibility Testing (EUCAST). EUCAST guidelines for detection of resistance mechanisms and specific resistances of clinical and/or epidemiological importance – Version 13.0. Växjö: EUCAST; 2023. Available from: v_13.0_Breakpoint_Tables.xlsx (live.com)
  13. 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 
  14. Moura A, Soares M, Pereira C, Leitão N, Henriques I, Correia A. INTEGRALL: a database and search engine for integrons, integrases and gene cassettes. Bioinformatics. 2009;25(8):1096-8.  https://doi.org/10.1093/bioinformatics/btp105  PMID: 19228805 
  15. Potron A, Poirel L, Nordmann P. Plasmid-mediated transfer of the bla(NDM-1) gene in Gram-negative rods. FEMS Microbiol Lett. 2011;324(2):111-6.  https://doi.org/10.1111/j.1574-6968.2011.02392.x  PMID: 22092811 
  16. Pfeifer Y, Witte W, Holfelder M, Busch J, Nordmann P, Poirel L. NDM-1-producing Escherichia coli in Germany. Antimicrob Agents Chemother. 2011;55(3):1318-9.  https://doi.org/10.1128/AAC.01585-10  PMID: 21189341 
  17. Girlich D, Dortet L, Poirel L, Nordmann P. Integration of the blaNDM-1 carbapenemase gene into Proteus genomic island 1 (PGI1-PmPEL) in a Proteus mirabilis clinical isolate. J Antimicrob Chemother. 2015;70(1):98-102.  https://doi.org/10.1093/jac/dku371  PMID: 25239462 
  18. Sakamoto N, Akeda Y, Sugawara Y, Takeuchi D, Motooka D, Yamamoto N, et al. Genomic characterization of carbapenemase-producing Klebsiella pneumoniae with chromosomally carried blaNDM-1. Antimicrob Agents Chemother. 2018;62(12):e01520-18.  https://doi.org/10.1128/AAC.01520-18  PMID: 30323033 
  19. Kong LH, Xiang R, Wang YL, Wu SK, Lei CW, Kang ZZ, et al. Integration of the blaNDM-1 carbapenemase gene into a novel SXT/R391 integrative and conjugative element in Proteus vulgaris. J Antimicrob Chemother. 2020;75(6):1439-42.  https://doi.org/10.1093/jac/dkaa068  PMID: 32155266 
  20. Bonnin RA, Poirel L, Naas T, Pirs M, Seme K, Schrenzel J, et al. Dissemination of New Delhi metallo-β-lactamase-1-producing Acinetobacter baumannii in Europe. Clin Microbiol Infect. 2012;18(9):E362-5.  https://doi.org/10.1111/j.1469-0691.2012.03928.x  PMID: 22738206 
  21. Luo X, Yin Z, Zeng L, Hu L, Jiang X, Jing Y, et al. Chromosomal Integration of huge and complex blaNDM-carrying genetic elements in Enterobacteriaceae. Front Cell Infect Microbiol. 2021;11:690799.  https://doi.org/10.3389/fcimb.2021.690799  PMID: 34211858 
  22. Acman M, Wang R, van Dorp L, Shaw LP, Wang Q, Luhmann N, et al. Role of mobile genetic elements in the global dissemination of the carbapenem resistance gene blaNDM. Nat Commun. 2022;13(1):1131.  https://doi.org/10.1038/s41467-022-28819-2  PMID: 35241674 
  23. Campos JC, da Silva MJ, dos Santos PR, Barros EM, Pereira MO, Seco BM, et al. Characterization of Tn3000, a transposon responsible for blaNDM-1 dissemination among Enterobacteriaceae in Brazil, Nepal, Morocco, and India. Antimicrob Agents Chemother. 2015;59(12):7387-95.  https://doi.org/10.1128/AAC.01458-15  PMID: 26392506 
  24. Toleman MA, Biedenbach D, Bennett D, Jones RN, Walsh TR. Genetic characterization of a novel metallo-beta-lactamase gene, blaIMP-13, harboured by a novel Tn5051-type transposon disseminating carbapenemase genes in Europe: report from the SENTRY worldwide antimicrobial surveillance programme. J Antimicrob Chemother. 2003;52(4):583-90.  https://doi.org/10.1093/jac/dkg410  PMID: 12951335 
  25. Jolivet S, Couturier J, Vuillemin X, Gouot C, Nesa D, Adam M, et al. Outbreak of OXA-48-producing Enterobacterales in a haematological ward associated with an uncommon environmental reservoir, France, 2016 to 2019. Euro Surveill. 2021;26(21):2000118.  https://doi.org/10.2807/1560-7917.ES.2021.26.21.2000118  PMID: 34047273 
Regional dissemination of NDM-1 producing Enterobacter hormaechei ST1740, with a subset of strains co-producing VIM-4 or IMP-13, France, 2019 to 2022
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=In%C3%A8s+Rezzoug&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Rezzoug Inès</a>, <a href="/search?value1=C%C3%A9cile+Emeraud&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Emeraud Cécile</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=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>. Regional dissemination of NDM-1 producing Enterobacter hormaechei ST1740, with a subset of strains co-producing VIM-4 or IMP-13, France, 2019 to 2022. <a href="/content/ecdc">Euro Surveill.</a> 2024;29(11):pii=2300521. <a href="https://doi.org/10.2807/1560-7917.ES.2024.29.11.2300521" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2024.29.11.2300521</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 28 Sept 2023;&nbsp;&nbsp; <span class="generated">Accepted</span>: 02 Feb 2024 </span> </p>
/content/10.2807/1560-7917.ES.2024.29.11.2300521
/content/10.2807/1560-7917.ES.2024.29.11.2300521
Loading

Data & Media loading...

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