Plasmid-mediated colistin resistance among human clinical Enterobacterales isolates: national surveillance in the Czech Republic
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
37180238
PubMed Central
PMC10174314
DOI
10.3389/fmicb.2023.1147846
Knihovny.cz E-zdroje
- Klíčová slova
- Enterobacterales, antibiotic resistance, human, mcr, plasmids,
- Publikační typ
- časopisecké články MeSH
The occurrence of colistin resistance has increased rapidly among Enterobacterales around the world. We performed a national survey of plasmid-mediated colistin resistance in human clinical isolates through a retrospective analysis of samples from 2009 to 2017 and a prospective sampling in 2018-2020. The aim of this study was to identify and characterize isolates with mcr genes from various regions of the Czech Republic using whole genome sequencing (WGS). Of all 1932 colistin-resistant isolates analyzed, 73 (3.8%) were positive for mcr genes. Most isolates carried mcr-1 (48/73) and were identified as Escherichia coli (n = 44) and Klebsiella pneumoniae (n = 4) of various sequence types (ST). Twenty-five isolates, including Enterobacter spp. (n = 24) and Citrobacter freundii (n = 1) carrying the mcr-9 gene were detected; three of them (Enterobacter kobei ST54) co-harbored the mcr-4 and mcr-9 genes. Multi-drug resistance phenotype was a common feature of mcr isolates and 14% (10/73) isolates also co-harbored clinically important beta-lactamases, including two isolates with carbapenemases KPC-2 and OXA-48. Phylogenetic analysis of E. coli ST744, the dominant genotype in this study, with the global collection showed Czech isolates belonged to two major clades, one containing isolates from Europe, while the second composed of isolates from diverse geographical areas. The mcr-1 gene was carried by IncX4 (34/73, 47%), IncHI2/ST4 (6/73, 8%) and IncI2 (8/73, 11%) plasmid groups. Small plasmids belonging to the ColE10 group were associated with mcr-4 in three isolates, while mcr-9 was carried by IncHI2/ST1 plasmids (4/73, 5%) or the chromosome (18/73, 25%). We showed an overall low level of occurrence of mcr genes in colistin-resistant bacteria from human clinical samples in the Czech Republic.
CEITEC VETUNI University of Veterinary Sciences Brno Brno Czechia
Department of Chemistry Faculty of Science University of Hradec Králové Hradec Králové Czechia
Department of Microbiology University Hospital of Larissa Larissa Greece
Zobrazit více v PubMed
Aghapour Z., Gholizadeh P., Ganbarov K., bialvaei A. Z., Mahmood S. S., Tanomand A., et al. . (2019). Molecular mechanisms related to colistin resistance in Enterobacteriaceae. Infect. Drug Resist. 12, 965–975. doi: 10.2147/IDR.S199844, PMID: PubMed DOI PMC
Alikhan N. F., Petty N. K., Ben Zakour N. L., Beatson S. A. (2011). BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 12, 1–10. doi: 10.1186/1471-2164-12-402, PMID: PubMed DOI PMC
Arndt D., Grant J. R., Marcu A., Sajed T., Pon A., Liang Y., et al. . (2016). PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res. 44, W16–W21. doi: 10.1093/nar/gkw387, PMID: PubMed DOI PMC
Bankevich A., Nurk S., Antipov D., Gurevich A. A., Dvorkin M., Kulikov A. S., et al. . (2012). SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477. doi: 10.1089/cmb.2012.0021, PMID: PubMed DOI PMC
Bauer A. P., Dieckmann S. M., Ludwig W., Schleifer K.-H. (2007). Rapid identification of Escherichia coli safety and laboratory strain lineages based on multiplex-PCR. FEMS Microbiol. Lett. 269, 36–40. doi: 10.1111/j.1574-6968.2006.00594.x, PMID: PubMed DOI
Bitar I., Medvecky M., Gelbicova T., Jakubu V., Hrabak J., Zemlickova H., et al. . (2019). Complete Nucleotide Sequences of mcr-4.3 -Carrying Plasmids in Acinetobacter baumannii Sequence Type 345 of Human and Food Origin from the Czech Republic, the First Case in Europe. Antimicrobial. Agents Chemother. 63. doi: 10.1128/aac.01166-19 PubMed DOI PMC
Bitar I., Papagiannitsis C. C., Kraftova L., Chudejova K., Mattioni Marchetti V., Hrabak J. (2020). Detection of five mcr-9 -carrying Enterobacterales isolates in four czech hospitals. mSphere 5:e01008-20. doi: 10.1128/mSphere.01008-20, PMID: PubMed DOI PMC
Bolger A. M., Lohse M., Usadel B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120. doi: 10.1093/bioinformatics/btu170, PMID: PubMed DOI PMC
Borowiak M., Hammerl J. A., Deneke C., Fischer J., Szabo I., Malorny B. (2019). Characterization of mcr-5-harboring Salmonella enterica subsp. enterica serovar typhimurium isolates from animal and food origin in germany. Antimicrob. Agents Chemother. 63:e00063-19. doi: 10.1128/aac.00063-19, PMID: PubMed DOI PMC
Carattoli A., Bertini A., Villa L., Falbo V., Hopkins K. L., Threlfall E. J. (2005). Identification of plasmids by PCR-based replicon typing. J. Microbiol. Methods 63, 219–228. doi: 10.1016/j.mimet.2005.03.018, PMID: PubMed DOI
Carattoli A., Villa L., Feudi C., Curcio L., Orsini S., Luppi A., et al. . (2017). Novel plasmid-mediated colistin resistance mcr-4 gene in Salmonella and Escherichia coli, Italy 2013, Spain and Belgium, 2015 to 2016. Eur. Secur. 22:30589. doi: 10.2807/1560-7917.ES.2017.22.31.30589, PMID: PubMed DOI PMC
Carattoli A., Zankari E., García-Fernández A., Voldby Larsen M., Lund O., Villa L., et al. . (2014). In silicodetection and typing of plasmids using plasmidfinder and plasmid multilocus sequence typing. Antimicrob. Agents Chemother. 58, 3895–3903. doi: 10.1128/AAC.02412-14, PMID: PubMed DOI PMC
Centers for Disease Control and Prevention (2004). Standardized molecular subtyping of foodborne bacterial pathogens by pulse-field gel electrophoresis. Centers for Disease Control and Prevention, Atlanta, GA.
Dalmolin V. T., de Lima-Morales D., Barth L. A. (2018). Plasmid-mediated colistin resistance: what do we know? J. Infect. 1, 16–22. doi: 10.29245/2689-9981/2018/2.1109, PMID: PubMed DOI
Darling A. E., Mau B., Perna N. T. (2010). progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 5:e11147. doi: 10.1371/journal.pone.0011147, PMID: PubMed DOI PMC
Del Bianco F., Morotti M., Pedna M. F., Farabegoli P., Sambri V. (2018). Microbiological surveillance of plasmid mediated colistin resistance in human Enterobacteriaceae isolates in Romagna (Northern Italy): August 2016–July 2017. Int. J. Infect. Dis. 69, 96–98. doi: 10.1016/j.ijid.2018.02.006, PMID: PubMed DOI
Doumith M., Godbole G., Ashton P., Larkin L., Dallman T., Day M., et al. . (2016). 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. 71, 2300–2305. doi: 10.1093/jac/dkw093, PMID: PubMed DOI
ECDC, European Centre for Disease Prevention and Control (2019). ECDC Technical Report, Expert consensus protocol on colistin resistance detection and characterisation for the survey of carbapenem- and/or colistin-resistant Enterobacteriaceae. Available at: https://www.ecdc.europa.eu/sites/default/files/documents/expert-consensus-protocol-colistin-resistance.pdf
El Garch F., de Jong A., Bertrand X., Hocquet D., Sauget M. (2018). mcr-1-like detection in commensal Escherichia coli and Salmonella spp. from food-producing animals at slaughter in Europe. Vet. Microbiol. 213, 42–46. doi: 10.1016/j.vetmic.2017.11.014, PMID: PubMed DOI
El-Sayed Ahmed M. A. E.-G., Zhong L.-L., Shen C., Yang Y., Doi Y., Tian G.-B. (2020). Colistin and its role in the Era of antibiotic resistance: an extended review (2000–2019). Emerg. Microbes Infect. 9, 868–885. doi: 10.1080/22221751.2020.1754133, PMID: PubMed DOI PMC
European Committee on Antimicrobial Susceptibility Testing . (2017). Breakpoint tabled for interpretation of MICs and zone diameters. Version 2.0. Available at: http://www.eucast.org.
Forde T. L., Dennis T. P. W., Aminu O. R., Harvey W. T., Hassim A., Kiwelu I., et al. . (2022). Population genomics of Bacillus anthracis from an anthrax hyperendemic area reveals transmission processes across spatial scales and unexpected within-host diversity. Microb. Genomics 8:759. doi: 10.1099/mgen.0.000759, PMID: PubMed DOI PMC
Giani T., Sennati S., Antonelli A., Di Pilato V., di Maggio T., Mantella A., et al. . (2018). High prevalence of carriage of mcr-1-positive enteric bacteria among healthy children from rural communities in the Chaco region, Bolivia, September to October 2016. Eur. Secur. 23:1800115. doi: 10.2807/1560-7917.ES.2018.23.45.1800115, PMID: PubMed DOI PMC
Gilchrist C. L., Chooi Y. H. (2021). Clinker & clustermap. js: Automatic generation of gene cluster comparison figures. Bioinformatics 37, 2473–2475. doi: 10.1093/bioinformatics/btab007, PMID: PubMed DOI
Gröndahl-Yli-Hannuksela K., Lönnqvist E., Kallonen T., Lindholm L., Jalava J., Rantakokko-Jalava K., et al. . (2018). The first human report of mobile colistin resistance gene, mcr-1, in Finland. APMIS 126, 413–417. doi: 10.1111/apm.12834, PMID: PubMed DOI
Hamel M., Rolain J.-M., Baron S. A. (2021). The history of colistin resistance mechanisms in bacteria: progress and challenges. Microorganisms 9:442. doi: 10.3390/microorganisms9020442 PubMed DOI PMC
Javed H., Saleem S., Zafar A., Ghafoor A., Shahzad A. B., Ejaz H., et al. . (2020). Emergence of plasmid-mediated mcr genes from Gram-negative bacteria at the human-animal interface. Gut Pathogens 12:54. doi: 10.1186/s13099-020-00392-3, PMID: PubMed DOI PMC
Katip W., Yoodee J., Uitrakul S., Oberdorfer P. (2021). Efficacy of loading dose colistin versus carbapenems for treatment of extended spectrum beta lactamase producing Enterobacteriaceae. Sci. Rep. 11:18. doi: 10.1038/s41598-020-78098-4, PMID: PubMed DOI PMC
Katoh K., Standley D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780. doi: 10.1093/molbev/mst010 PubMed DOI PMC
Kieffer N., Royer G., Decousser J.-W., Bourrel A.-S., Palmieri M., Ortiz De La Rosa J.-M., et al. . (2019). mcr-9, an inducible gene encoding an acquired phosphoethanolamine transferase in Escherichia coli, and its origin. Antimicrob. Agents Chemother. 63:e00965-19. doi: 10.1128/AAC.00965-19, PMID: PubMed DOI PMC
Koboldt D. C., Zhang Q., Larson D. E., Shen D., McLellan M. D., Lin L., et al. . (2012). VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Res. 22, 568–576. doi: 10.1101/gr.129684.111, PMID: PubMed DOI PMC
Krutova M., Kalova A., Nycova E., Gelbicova T., Karpiskova R., Smelikova E., et al. . (2021). The colonisation of Czech travellers and expatriates living in the Czech Republic by colistin-resistant Enterobacteriaceae and whole genome characterisation of E. coli isolates harbouring the mcr-1 genes on a plasmid or chromosome: A cross-sectional study. Travel Med. Infect. Dis. 39:101914. doi: 10.1016/j.tmaid.2020.101914, PMID: PubMed DOI
Langmead B., Salzberg S. L. (2012). Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359. doi: 10.1038/nmeth.1923, PMID: PubMed DOI PMC
Larsen M. V., Cosentino S., Rasmussen S., Friis C., Hasman H., Marvig R. L., et al. . (2012). Multilocus sequence typing of total-genome-sequenced bacteria. J. Clin. Microbiol. 50, 1355–1361. doi: 10.1128/jcm.06094-11 PubMed DOI PMC
Letunic I., Bork P. (2021). Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 49, W293–W296. doi: 10.1093/nar/gkab301, PMID: PubMed DOI PMC
Li Y., Dai X., Zeng J., Gao Y., Zhang Z., Zhang L. (2020). Characterization of the global distribution and diversified plasmid reservoirs of the colistin resistance gene mcr-9. Sci. Rep. 10:8113. doi: 10.1038/s41598-020-65106-w, PMID: PubMed DOI PMC
Liao W., Cui Y., Quan J., Zhao D., Han X., Shi Q., et al. . (2022). High prevalence of colistin resistance and mcr-9/10 genes in Enterobacter spp. in a tertiary hospital over a decade. Int. J. Antimicrob. Agents 59:106573. doi: 10.1016/j.ijantimicag.2022.106573, PMID: PubMed DOI
Lin Y., Yuan J., Kolmogorov M., Shen M. W., Chaisson M., Pevzner P. A. (2016). Assembly of long error-prone reads using de Bruijn graphs. Proc. Natl. Acad. Sci. 113, E8396–E8405. doi: 10.1073/pnas.1604560113, PMID: PubMed DOI PMC
Marchetti V. M., Bitar I., Sarti M., Fogato E., Scaltriti E., Bracchi C., et al. . (2021). Genomic characterization of VIM and MCR co-producers: the first two clinical cases, in Italy. Diagnostics 11:79. doi: 10.3390/diagnostics11010079, PMID: PubMed DOI PMC
Meier-Kolthoff J. P., Auch A. F., Klenk H.-P., Göker M. (2013). Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformat. 14:60. doi: 10.1186/1471-2105-14-60 PubMed DOI PMC
Page A. J., Cummins C. A., Hunt M., Wong V. K., Reuter S., Holden M. T. G., et al. . (2015). Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 31, 3691–3693. doi: 10.1093/bioinformatics/btv421 PubMed DOI PMC
Papagiannitsis C. C., Študentová V., Izdebski R., Oikonomou O., Pfeifer Y., Petinaki E., et al. . (2015). Matrix-assisted laser desorption ionization–time of flight mass spectrometry meropenem hydrolysis assay with NH 4 HCO 3, a reliable tool for direct detection of carbapenemase activity. J. Clin. Microbiol. 53, 1731–1735. doi: 10.1128/JCM.03094-14, PMID: PubMed DOI PMC
Price M. N., Dehal P. S., Arkin A. P. (2010). FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS One 5:e9490. doi: 10.1371/journal.pone.0009490, PMID: PubMed DOI PMC
Prim N., Turbau M., Rivera A., Rodríguez-Navarro J., Coll P., Mirelis B. (2017). Prevalence of colistin resistance in clinical isolates of Enterobacteriaceae: A four-year cross-sectional study. J. Infect. 75, 493–498. doi: 10.1016/j.jinf.2017.09.008, PMID: PubMed DOI
Quiroga C., Nastro M., Di Conza J. (2019). Current scenario of plasmid-mediated colistin resistance in Latin America. Rev. Argent. Microbiol. 51, 93–100. doi: 10.1016/j.ram.2018.05.001, PMID: PubMed DOI
Rebelo A. R., Bortolaia V., Kjeldgaard J. S., Pedersen S. K., Leekitcharoenphon P., Hansen I. M., et al. . (2018). Multiplex PCR for detection of plasmid-mediated colistin resistance determinants, mcr-1, mcr-2, mcr-3, mcr-4 and mcr-5 for surveillance purposes. Euro Surveill. 23, 17–00672. doi: 10.2807/1560-7917.ES.2018.23.6.17-00672 PubMed DOI PMC
Ruan Z., Sun Q., Jia H., Huang C., Zhou W., Xie X., et al. . (2019). Emergence of a ST2570 Klebsiella pneumoniae isolate carrying mcr-1 and blaCTX-M-14 recovered from a bloodstream infection in China. Clin. Microbiol. Infect. 25, 916–918. doi: 10.1016/j.cmi.2019.02.005 PubMed DOI
Stamatakis A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313. doi: 10.1093/bioinformatics/btu033 PubMed DOI PMC
Tkadlec J., Kalova A., Brajerova M., Gelbicova T., Karpiskova R., Smelikova E., et al. . (2021). The intestinal carriage of plasmid-mediated colistin-resistant Enterobacteriaceae in tertiary care settings. Antibiotics 10:258. doi: 10.3390/antibiotics10030258, PMID: PubMed DOI PMC
Tyson G. H., Li C., Hsu C.-H., Ayers S., Borenstein S., Mukherjee S., et al. . (2020). The mcr-9 gene of Salmonella and Escherichia coli is not associated with colistin resistance in the United States. Antimicrob. Agents Chemother. 64:e00573-20. doi: 10.1128/AAC.00573-20, PMID: PubMed DOI PMC
Viñes J., Cuscó A., Napp S., Alvarez J., Saez-Llorente J. L., Rosàs-Rodoreda M., et al. . (2021). Transmission of similar mcr-1 carrying plasmids among different Escherichia coli lineages isolated from livestock and the farmer. Antibiotics 10:313. doi: 10.3390/antibiotics10030313, PMID: PubMed DOI PMC
Walker B. J., Abeel T., Shea T., Priest M., Abouelliel A., Sakthikumar S., et al. . (2014). Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 9:e112963. doi: 10.1371/journal.pone.0112963, PMID: PubMed DOI PMC
Wang C., Feng Y., Liu L., Wei L., Kang M., Zong Z. (2020). Identification of novel mobile colistin resistance gene mcr-10. Emerg. Microbes Infect. 9, 508–516. doi: 10.1080/22221751.2020.1732231 PubMed DOI PMC
Wang X., Wang Y., Zhou Y., Li J., Yin W., Wang S., et al. . (2018). Emergence of a novel mobile colistin resistance gene, mcr-8, in NDM-producing Klebsiella pneumoniae. Emerg. Microbes Infect. 7, 1–9. doi: 10.1038/s41426-018-0124-z PubMed DOI PMC
Wang Y., Xu C., Zhang R., Chen Y., Shen Y., Hu F., et al. . (2020). Changes in colistin resistance and mcr-1 abundance in Escherichia coli of animal and human origins following the ban of colistin-positive additives in China: an epidemiological comparative study. Lancet Infect. Dis. 20, 1161–1171. doi: 10.1016/s1473-3099(20)30149-3 PubMed DOI
Wick R. R., Judd L. M., Gorrie C. L., Holt K. E. (2017). Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput. Biol. 13:e1005595. doi: 10.1371/journal.pcbi.1005595, PMID: PubMed DOI PMC
Xavier B. B., Lammens C., Butaye P., Goossens H., Malhotra-Kumar S. (2016). Complete sequence of an IncFII plasmid harbouring the colistin resistance gene mcr-1 isolated from Belgian pig farms. J. Antimicrob. Chemother. 71, 2342–2344. doi: 10.1093/jac/dkw191 PubMed DOI
Yilmaz G. R., Dizbay M., Guven T., Pullukcu H., Tasbakan M., Guzel O. T., et al. . (2016). Risk factors for infection with colistin-resistant gram-negative microorganisms: a multicenter study. Ann. Saudi Med. 36, 216–222. doi: 10.5144/0256-4947.2016.216 PubMed DOI PMC
Yoon S. H., Ha S. M., Kwon S., Lim J., Kim Y., Seo H., et al. . (2017). Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int. J. Syst. Evol. Microbiol. 67:1613. doi: 10.1099/ijsem.0.001755, PMID: PubMed DOI PMC
Zankari E., Allesøe R., Joensen K. G., Cavaco L. M., Lund O., Aarestrup F. M. (2017). PointFinder: a novel web tool for WGS-based detection of antimicrobial resistance associated with chromosomal point mutations in bacterial pathogens. J. Antimicrob. Chemother. 72, 2764–2768. doi: 10.1093/jac/dkx217, PMID: PubMed DOI PMC
Zankari E., Hasman H., Cosentino S., Vestergaard M., Rasmussen S., Lund O., et al. . (2012). Identification of acquired antimicrobial resistance genes. J. Antimicrob. Chemother. 67, 2640–2644. doi: 10.1093/jac/dks261, PMID: PubMed DOI PMC
Zelendova M., Papagiannitsis C. C., Valcek A., Medvecky M., Bitar I., Hrabak J., et al. . (2021). Characterization of the complete nucleotide sequences of mcr-1-encoding plasmids from Enterobacterales isolates in retailed raw meat products from the Czech Republic. Front. Microbiol. 11:604067. doi: 10.3389/fmicb.2020.604067 PubMed DOI PMC
Zhang Z., Tian X., Shi C. (2022). Global Spread of MCR-Producing Salmonella enterica Isolates. Antibiotics 11:998. doi: 10.3390/antibiotics11080998 PubMed DOI PMC
Zhu W., Lawsin A., Lindsey R. L., Batra D., Knipe K., Yoo B. B., et al. . (2019). Conjugal transfer, whole-genome sequencing, and plasmid analysis of four mcr-1 -bearing isolates from U.S. patients. Antimicrob. Agents Chemotherapy 63:e02417-18. doi: 10.1128/AAC.02417-18, PMID: PubMed DOI PMC
Zurfluh K., Nüesch-Inderbinen M., Klumpp J., Poirel L., Nordmann P., Stephan R. (2017). Key features of mcr-1-bearing plasmids from Escherichia coli isolated from humans and food. Antimicrob. Resistan. Infect. Control 6:91. doi: 10.1186/s13756-017-0250-8, PMID: PubMed DOI PMC
VIM-1-producing Enterobacter asburiae with mobile colistin resistance genes from wastewaters