Genomic Characterization of an Extensively Drug-Resistant Extra-Intestinal Pathogenic (ExPEC) Escherichia coli Clinical Isolate Co-Producing Two Carbapenemases and a 16S rRNA Methylase
Abstract
:1. Introduction
2. Material and Methods
3. Results and Discussion
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Marin, J.; Clermont, O.; Royer, G.; Mercier-Darty, M.; Decousser, J.W.; Tenaillon, O.; Denamur, E.; Blanquart, F. The population genomics of increased virulence and antibiotic resistance in human commensal Escherichia coli over 30 Years in France. Appl. Environ. Microbiol. 2022, 88, e0066422. [Google Scholar] [CrossRef] [PubMed]
- Poirel, L.; Madec, J.Y.; Lupo, A.; Schink, A.K.; Kieffer, N.; Nordmann, P.; Schwarz, S. Antimicrobial resistance in Escherichia coli. Microbiol. Spectr. 2018, 6, 4. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Doi, Y. Treatment options for carbapenem-resistant Gram-negative bacterial infections. Clin. Infect. Dis. 2019, 69 (Suppl. 7), S565–S575. [Google Scholar] [CrossRef] [Green Version]
- Lee, Y.L.; Chen, H.M.; Hii, I.M.; Hsueh, P.R. Carbapenemase-producing Enterobacterales infections: Recent advances in diagnosis and treatment. Int. J. Antimicrob. Agents. 2022, 59, 106528. [Google Scholar] [CrossRef] [PubMed]
- Fu, L.; Wang, S.; Zhang, Z.; Hu, X.; Zhang, L.; Zhu, B.; Wang, G.; Long, H.; Zhou, Y. Whole genome sequence of blaNDM and blaKPC co-producing Klebsiella pneumoniae isolate KSH203 with capsular serotype K25 belonging to ST11 from China. J. Glob. Antimicrob. Resist. 2020, 20, 272–274. [Google Scholar] [CrossRef]
- Wu, W.; Feng, Y.; Carattoli, A.; Zong, Z. Characterization of an Enterobacter cloacae strain producing both KPC and NDM carbapenemases by whole-genome sequencing. Antimicrob. Agents Chemother. 2015, 59, 6625–6628. [Google Scholar] [CrossRef] [Green Version]
- Feng, J.; Qiu, Y.; Yin, Z.; Chen, W.; Yang, H.; Yang, W.; Wang, J.; Gao, Y.; Zhou, D. Coexistence of a novel KPC-2-encoding MDR plasmid and an NDM-1-encoding pNDM-HN380-like plasmid in a clinical isolate of Citrobacter freundii. J. Antimicrob. Chemother. 2015, 70, 2987–2991. [Google Scholar] [CrossRef] [Green Version]
- Paul, D.; Dhar Chanda, D.; Maurya, A.P.; Mishra, S.; Chakravarty, A.; Sharma, G.D.; Bhattacharjee, A. Co-carriage of blaKPC-2 and blaNDM-1 in clinical isolates of Pseudomonas aeruginosa associated with hospital infections from India. PLoS ONE 2015, 10, e0145823. [Google Scholar] [CrossRef] [Green Version]
- Kumarasamy, K.; Kalyanasundaram, A. Emergence of Klebsiella pneumoniae isolate co-producing NDM-1 with KPC-2 from India. J. Antimicrob. Chemother. 2012, 67, 243–244. [Google Scholar] [CrossRef] [Green Version]
- Pereira, P.S.; Borghi, M.; Albano, R.M.; Lopes, J.C.O.; Silveira, M.C.; Marques, E.A.; Oliveira, J.C.R.; Asensi, M.D.; Carvalho-Assef, A.P.D. Coproduction of NDM-1 and KPC-2 in Enterobacter hormaechei from Brazil. Microb. Drug Resist. 2015, 21, 234–236. [Google Scholar] [CrossRef]
- Sadek, M.; Ruppé, E.; Habib, A.; Zahra, R.; Poirel, L.; Nordmann, P. International circulation of aztreonam/avibactam-resistant NDM-5-producing Escherichia coli isolates: Successful epidemic clones. J. Glob. Antimicrob. Resist. 2021, 27, 326–328. [Google Scholar] [CrossRef] [PubMed]
- Sadek, M.; Juhas, M.; Poirel, L.; Nordmann, P. Genetic features leading to reduced susceptibility to aztreonam-avibactam among metallo-β-lactamase-producing Escherichia coli isolates. Antimicrob. Agents Chemother. 2020, 64, e01659-20. [Google Scholar] [CrossRef] [PubMed]
- Kohira, N.; West, J.; Ito, A.; Ito-Horiyama, T.; Nakamura, R.; Sato, T.; Rittenhouse, S.; Tsuji, M.; Yamano, Y. In vitro antimicrobial activity of a siderophore cephalosporin, S-649266, against Enterobacteriaceae Clinical isolates, including carbapenem-resistant strains. Antimicrob. Agents Chemother. 2015, 60, 729–734. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hackel, M.A.; Tsuji, M.; Yamano, Y.; Echols, R.; Karlowsky, J.A.; Sahm, D.F. In vitro activity of the siderophore cephalosporin, cefiderocol, against carbapenem non-susceptible and multidrug-resistant isolates of Gram-negative bacilli collected worldwide in 2014 to 2016. Antimicrob. Agents Chemother. 2018, 62, e01968-17. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hackel, M.A.; Tsuji, M.; Yamano, Y.; Echols, R.; Karlowsky, J.A.; Sahm, D.F. Reproducibility of broth microdilution MICs for the novel siderophore cephalosporin, cefiderocol, determined using iron-depleted cation-adjusted Mueller-Hinton broth. Diagn. Microbiol. Infect. Dis. 2019, 94, 321–325. [Google Scholar] [CrossRef]
- EUCAST. The European Committee on Antimicrobial Susceptibility Testing. Breakpoint Tables for Interpretation of MICs and Zone Diameters. Version 12.0. 2022. Available online: https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_12.0_Breakpoint_Tables.pdf (accessed on 14 February 2022).
- Nordmann, P.; Poirel, L.; Dortet, L. Rapid detection of carbapenemase producing Enterobacteriaceae. Emerg. Infect. Dis. 2012, 18, 1503–1507. [Google Scholar] [CrossRef] [Green Version]
- Nordmann, P.; Sadek, M.; Demord, A.; Poirel, L. NitroSpeed-Carba NP test for rapid detection and differentiation between different classes of carbapenemases in Enterobacterales. J. Clin. Microbiol. 2020, 58, e00932-20. [Google Scholar] [CrossRef]
- Nordmann, P.; Jayol, A.; Poirel, L. Rapid detection of polymyxin resistance in Enterobacteriaceae. Emerg. Infect. Dis. 2016, 22, 1038–1043. [Google Scholar] [CrossRef] [Green Version]
- Nordmann, P.; Poirel, L.; Mueller, L. Rapid detection of fosfomycin resistance in Escherichia coli. J. Clin. Microbiol. 2019, 57, e01531-18. [Google Scholar] [CrossRef] [Green Version]
- Sadek, M.; de la Rosa, J.M.O.; Ramadan, M.; Nordmann, P.; Poirel, L. Molecular characterization of extended-spectrum ß-lactamase producers, carbapenemase producers, polymyxin-resistant, and fosfomycin-resistant Enterobacterales among pigs from Egypt. J. Glob. Antimicrob. Resist. 2022, 30, 81–87. [Google Scholar] [CrossRef]
- Ali, T.; Rahman, S.U.; Zhang, L.; Shahid, M.; Han, D.; Gao, J.; Zhang, S.; Ruegg, P.L.; Saddique, U.; Han, B. Characteristics and genetic diversity of multi-drug resistant extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli isolated from bovine mastitis. Oncotarget 2017, 8, 90144–90163. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zogg, A.L.; Simmen, S.; Zurfluh, K.; Stephan, R.; Schmitt, S.N.; Nüesch-Inderbinen, M. High prevalence of extended-spectrum β-lactamase producing Enterobacteriaceae among clinical isolates from cats and dogs admitted to a veterinary hospital in Switzerland. Front. Vet. Sci. 2018, 5, 62. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Qin, S.; Fu, Y.; Zhang, Q.; Qi, H.; Wen, J.G.; Xu, H.; Xu, L.; Zeng, L.; Tian, H.; Rong, L.; et al. High incidence and endemic spread of NDM-1-positive Enterobacteriaceae in Henan Province, China. Antimicrob. Agents Chemother. 2014, 58, 4275–4282. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ingti, B.; Saikia, P.; Paul, D.; Maurya, A.P.; Chanda, D.D.; Chakravarty, A.; Deshamukhya, C.; Bhattacharjee, A. Occurrence of blaCMY-42 on an IncI1 plasmid in multidrug-resistant Escherichia coli from a tertiary referral hospital in India. J. Glob. Antimicrob. Resist. 2018, 14, 78–82. [Google Scholar] [CrossRef] [PubMed]
- Tavoschi, L.; Forni, S.; Porretta, A.; Righi, L.; Pieralli, F.; Menichetti, F.; Falcone, M.; Gemignani, G.; Sani, S.; Vivani, P.; et al. Prolonged outbreak of New Delhi metallo-β-lactamase–producing carbapenem-resistant Enterobacterales (NDM-CRE), Tuscany, Italy, 2018 to 2019. Eurosurveillance 2020, 25, 2000085. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chakraborty, T.; Sadek, M.; Yao, Y.; Imirzalioglu, C.; Stephan, R.; Poirel, L.; Nordmann, P. Cross-border emergence of Escherichia coli producing the carbapenemase NDM-5 in Switzerland and Germany. J. Clin. Microbiol. 2021, 59, e02238-20. [Google Scholar] [CrossRef] [PubMed]
- Tsilipounidaki, K.; Athanasakopoulou, Z.; Billinis, C.; Miriagou, V.; Petinaki, E. Importation of the first bovine ST361 New Delhi Metallo-5 positive Escherichia coli in Greece. Microb. Drug Resist. 2022, 28, 386–387. [Google Scholar] [CrossRef]
- Yang, P.; Xie, Y.; Feng, P.; Zong, Z. blaNDM-5 carried by an IncX3 plasmid in Escherichia coli sequence type 167. Antimicrob. Agents Chemother. 2014, 58, 7548–7552. [Google Scholar] [CrossRef] [Green Version]
- Zhu, Y.Q.; Zhao, J.Y.; Xu, C.; Zhao, H.; Jia, N.; Li, Y.N. Identification of an NDM-5-producing Escherichia coli Sequence Type 167 in a Neonatal Patient in China. Sci. Rep. 2016, 6, 29934. [Google Scholar] [CrossRef] [Green Version]
- Sadek, M.; Poirel, L.; Nordmann, P.; Nariya, H.; Shimamoto, T.; Shimamoto, T. Genetic characterization of NDM-1 and NDM-5-producing Enterobacterales from retail chicken meat in Egypt. J. Glob. Antimicrob. Resist. 2020, 23, 70–71. [Google Scholar] [CrossRef]
- Sadek, M.; Poirel, L.; Nordmann, P. Occurrence of aztreonam-avibactam-resistant NDM-5-producing Escherichia coli in the food chain. Antimicrob. Agents Chemother. 2021, 65, e00882-21. [Google Scholar] [CrossRef] [PubMed]
- Farzana, R.; Jones, L.S.; Rahman, A.; Sands, K.; van Tonder, A.J.; Portal, E.; Criollo, J.M.; Parkhill, J.; Guest, M.F.; Watkins, W.J.; et al. Genomic insights into the mechanism of carbapenem resistance dissemination in Enterobacterales from a tertiary public heath setting in South Asia. Clin. Infect. Dis. 2022, ciac287. [Google Scholar] [CrossRef]
- Venditti, C.; Fortini, D.; Villa, L.; Vulcano, A.; D’Arezzo, S.; Capone, A.; Petrosillo, N.; Nisii, C.; Carattoli, A.; Di Caro, A. Circulation of blaKPC-3-carrying IncX3 plasmids among Citrobacter freundii isolates in an Italian hospital. Antimicrob. Agents Chemother. 2017, 61, e00505-17. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bitar, I.; Caltagirone, M.; Villa, L.; Mattioni Marchetti, V.; Nucleo, E.; Sarti, M.; Migliavacca, R.; Carattoli, A. Interplay among IncA and blaKPC-carrying plasmids in Citrobacter freundii. Antimicrob. Agents Chemother. 2019, 63, e02609-18. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fortini, D.; Villa, L.; Feudi, C.; Pires, J.; Bonura, C.; Mammina, C.; Endimiani, A.; Carattoli, A. Double Copies of bla(KPC-3)::Tn4401a on an IncX3 plasmid in Klebsiella pneumoniae successful clone ST512 from Italy. Antimicrob. Agents Chemother. 2015, 60, 646–649. [Google Scholar] [CrossRef] [Green Version]
- Sato, T.; Ito, A.; Ishioka, Y.; Matsumoto, S.; Rokushima, M.; Kazmierczak, K.M.; Hackel, M.; Sahm, D.F.; Yamano, Y. Escherichia coli strains possessing a four amino acid YRIN insertion in PBP3 identified as part of the SIDERO-WT-2014 surveillance study. JAC-Antimicrob. Resist. 2020, 2, dlaa081. [Google Scholar] [CrossRef]
- Ito, A.; Sato, T.; Ota, M.; Takemura, M.; Nishikawa, T.; Toba, S.; Kohira, N.; Miyagawa, S.; Ishibashi, N.; Matsumoto, S.; et al. In vitro antibacterial properties of cefiderocol, a novel siderophore cephalosporin, against Gram-Negative Bacteria. Antimicrob. Agents Chemother. 2017, 62, e01454-17. [Google Scholar] [CrossRef] [Green Version]
- Nordmann, P.; Shields, R.K.; Doi, Y.; Takemura, M.; Echols, R.; Matsunaga, Y.; Yamano, Y. Mechanisms of reduced susceptibility to cefiderocol among isolates from the CREDIBLE-CR and APEKS-NP clinical trials. Microb. Drug Resist. 2022, 28, 398–407. [Google Scholar] [CrossRef]
- Moynié, L.; Luscher, A.; Rolo, D.; Pletzer, D.; Tortajada, A.; Weingart, H.; Braun, Y.; Page, M.G.P.; Naismith, J.H.; Köhler, T. Structure and function of the PiuA and PirA siderophore-drug receptors from Pseudomonas aeruginosa and Acinetobacter baumannii. Antimicrob. Agents Chemother. 2017, 61, e02531-16. [Google Scholar] [CrossRef] [Green Version]
- Simner, P.J.; Beisken, S.; Bergman, Y.; Ante, M.; Posch, A.E.; Tamma, P.D. Defining baseline mechanisms of cefiderocol resistance in the Enterobacterales. Microb. Drug Resist. 2022, 28, 161–170. [Google Scholar] [CrossRef]
- Poirel, L.; Sadek, M.; Nordmann, P. Contribution of PER-type and NDM-Type β-lactamases to cefiderocol resistance in Acinetobacter baumannii. Antimicrob. Agents Chemother. 2021, 65, e0087721. [Google Scholar] [CrossRef] [PubMed]
- Poirel, L.; Sadek, M.; Kusaksizoglu, A.; Nordmann, P. Co-resistance to ceftazidime-avibactam and cefiderocol in clinical isolates producing KPC variants. Eur. J. Clin. Microbiol. Infect. Dis. 2022, 41, 677–680. [Google Scholar] [CrossRef] [PubMed]
- Poirel, L.; de la Rosa, J.M.O.; Sadek, M.; Nordmann, P. Impact of acquired broad-spectrum β-lactamases on susceptibility to cefiderocol and newly developed β-lactam/β-lactamase inhibitor combinations in Escherichia coli and Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 2022, 66, e0003922. [Google Scholar] [CrossRef] [PubMed]
- Fröhlich, C.; Sørum, V.; Tokuriki, N.; Johnsen, P.J.; Samuelsen, Ø. Evolution of β-lactamase-mediated cefiderocol resistance. J. Antimicrob. Chemother. 2022, dkac221. [Google Scholar] [CrossRef]
- Chudejova, K.; Kraftova, L.; Mattioni Marchetti, V.; Hrabak, J.; Papagiannitsis, C.C.; Bitar, I. Genetic plurality of OXA/NDM-encoding features characterized from Enterobacterales recovered from Czech Hospitals. Front. Microbiol. 2021, 12, 641415. [Google Scholar] [CrossRef]
- Bibbolino, G.; Di Lella, F.M.; Oliva, A.; Lichtner, M.; Del Borgo, C.; Raponi, G.; Trancassini, M.; Mengoni, F.; Arcari, G.; Antonelli, 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, 115399. [Google Scholar] [CrossRef]
- Cen, D.J.; Sun, R.Y.; Mai, J.L.; Jiang, Y.W.; Wang, D.; Guo, W.Y.; Jiang, Q.; Zhang, H.; Zhang, J.-F.; Zhang, R.-M.; et al. Occurrence and transmission of bla(NDM)-carrying Enterobacteriaceae from geese and the surrounding environment on a commercial goose farm. Appl. Environ. Microbiol. 2021, 87, e00087-21. [Google Scholar] [CrossRef]
- Nordmann, P.; Sadek, M.; Poirel, L.; Chakraborty, T. Fosfomycin as a salvage therapy for treating urinary tract infections due to multidrug-resistant Escherichia coli. Eur. J. Clin. Microbiol. Infect. Dis. 2022, 41, 689–690. [Google Scholar] [CrossRef]
Strain | MICs (mg/L) | |||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
N1606 | CTX | CZD | CZA | FEP | C/T | IMI | IMI/REL | ETP | MEM | MEM/ VAB | ATM | ATM/ AVI | FDC | CST | FOS | TGC |
>32 | >256 | >256 | >256 | >256 | >32 | >32 | >32 | >32 | >32 | >256 | 16 | 64 | ≤0.125 | 0.5 | 0.38 |
Genetic Elements | Size (bp) | MLST a | pMLSTs (ABC Formula) | Plasmid Group | Antibiotic Resistance Gene(s) | PBP3 | Virulence Factors | GenBank Accession no. |
---|---|---|---|---|---|---|---|---|
Chr1606 | 5,036,231 | ST-361 | - | - | mdf(A), qepA, aadA1, catA1, blaOXA-1 | YRIN, Q227H, E353K, I532L | SitA, gad, hra, terC | CP083701 |
p1606A | 120,731 | - | [F36:A4:B-] | IncFII-FIA | blaNDM-5, rmtB, aadA5, dfrA17, tet(A), blaTEM-1B, sul1, qacE | - | traT | CP083702 |
p1606B | 53,292 | - | Unknown | IncX3 | blaKPC-3, blaSHV-11 | - | CP083703 | |
p1606C | 58,698 | - | Unknown | IncIγ | blaCMY-145 | - | CP083704 | |
p1606D | 146,558 | - | [F2:A-:B-] | IncFII | blaCTX-M-15, sul1, dfrA17, aadA5, erm(B), mph(A), qnrS1, qacE | - | traT | CP083705 |
p1606E | 89,634 | - | IncY | - | - | CP083706 | ||
p1606F | 107,032 | - | Unknown | IncI1-I(Alpha) | - | - | cia | CP083707 |
p1606G | 2634 | - | Col(BS512) | - | - | CP083708 |
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Sadek, M.; Saad, A.M.; Nordmann, P.; Poirel, L. Genomic Characterization of an Extensively Drug-Resistant Extra-Intestinal Pathogenic (ExPEC) Escherichia coli Clinical Isolate Co-Producing Two Carbapenemases and a 16S rRNA Methylase. Antibiotics 2022, 11, 1479. https://doi.org/10.3390/antibiotics11111479
Sadek M, Saad AM, Nordmann P, Poirel L. Genomic Characterization of an Extensively Drug-Resistant Extra-Intestinal Pathogenic (ExPEC) Escherichia coli Clinical Isolate Co-Producing Two Carbapenemases and a 16S rRNA Methylase. Antibiotics. 2022; 11(11):1479. https://doi.org/10.3390/antibiotics11111479
Chicago/Turabian StyleSadek, Mustafa, Alaaeldin Mohamed Saad, Patrice Nordmann, and Laurent Poirel. 2022. "Genomic Characterization of an Extensively Drug-Resistant Extra-Intestinal Pathogenic (ExPEC) Escherichia coli Clinical Isolate Co-Producing Two Carbapenemases and a 16S rRNA Methylase" Antibiotics 11, no. 11: 1479. https://doi.org/10.3390/antibiotics11111479