The Intestinal Carriage of Plasmid-Mediated Colistin-Resistant Enterobacteriaceae in Tertiary Care Settings
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
NV18-09-00254
Ministerstvo Zdravotnictví Ceské Republiky
PubMed
33806455
PubMed Central
PMC8002115
DOI
10.3390/antibiotics10030258
PII: antibiotics10030258
Knihovny.cz E-zdroje
- Klíčová slova
- Czech Republic, E. coli, IncX4, colistin, mcr, silent carriage,
- Publikační typ
- časopisecké články MeSH
Background: In order to estimate the prevalence of plasmid borne colistin resistance and to characterize in detail the mcr-positive isolates, we carried out a sentinel testing survey on the intestinal carriage of plasmid-mediated colistin-resistant Enterobacteriaceae in hospitalized patients. Methods: Between June 2018 and September 2019, 1922 faecal samples from hospitalised patients were analysed by selective culture in presence of colistin (3.5 mg/L), and in parallel by direct detection of the mcr-1 to mcr-8 genes by qPCR. The mcr-positive isolates were characterised by whole-genome sequencing. Results: The prevalence of the mcr-1 gene was 0.21% (n = 4/1922); the mcr-2 to 8 genes were not detected. The mcr-1 gene was found to be localised in the IncX4 (n = 3) and IncHI2 (n = 1) plasmid type. One Escherichia coli isolate was susceptible to colistin due to the inactivation of the mcr-1 gene through the insertion of the IS2 element; however, the colistin resistance was inducible by culture in low concentrations of colistin. One human mcr-1 positive E. coli isolate was related genetically to the mcr-1 E. coli isolate derived from turkey meat of Czech origin. Conclusions:mcr-mediated colistin resistance currently poses little threat to patients hospitalised in Czech healthcare settings. The presence of the mcr-1 gene in the human population has a possible link to domestically produced, retail meat.
Department of Experimental Biology Faculty of Science Masaryk University 611 37 Brno Czech Republic
Department of Medical Microbiology Motol University Hospital 150 06 Prague Czech Republic
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Poirel L., Jayol A., Nordmann P. Polymyxins: Antibacterial activity, susceptibility testing, and resistance mechanisms encoded by plasmids or chromosomes. Clin. Microbiol. Rev. 2017;30:557–596. doi: 10.1128/CMR.00064-16. PubMed DOI PMC
Skov R.L., Monnet D.L. Plasmid-mediated colistin resistance (mcr-1 gene): Three months later, the story unfolds. Eurosurveillance. 2016;21:30155. doi: 10.2807/1560-7917.ES.2016.21.9.30155. PubMed DOI
Liu Y.Y., Wang Y., Walsh T.R., Yi L.X., Zhang R., Spencer J., Doi Y., Tian G., Dong B., Huang X., et al. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: A microbiological and molecular biological study. Lancet Infect. Dis. 2016;16:161–168. doi: 10.1016/S1473-3099(15)00424-7. PubMed DOI
El-Sayed Ahmed M.A.E.G., Zhong L.L., Shen C., Yang Y., Doi Y., Tian G.B. Colistin and its role in the Era of antibiotic resistance: An extended review (2000–2019) Emerg. Microbes Infect. 2020;9:868–885. doi: 10.1080/22221751.2020.1754133. PubMed DOI PMC
Wang C., Feng Y., Liu L., Wei L., Kang M., Zong Z. Identification of novel mobile colistin resistance gene mcr-10. Emerg. Microbes Infect. 2020;9:508–516. doi: 10.1080/22221751.2020.1732231. PubMed DOI PMC
Nang S.C., Li J., Velkov T. The rise and spread of mcr plasmid-mediated polymyxin resistance. Crit. Rev. Microbiol. 2019;45:131–161. doi: 10.1080/1040841X.2018.1492902. PubMed DOI PMC
Shen Y., Zhou H., Xu J., Wang Y., Zhang Q., Walsh T.R., Shao B., Wu C., Hu Y., Yang L., et al. Anthropogenic and environmental factors associated with high incidence of mcr-1 carriage in humans across China. Nat. Microbiol. 2018;3:1054–1062. doi: 10.1038/s41564-018-0205-8. PubMed DOI PMC
European Medicines Agency . Sales of Veterinary Antimicrobial Agents in 31 European Countries in 2018: Trends from 2010 to 2018. European Medicines Agency; Amsterdam, The Netherlands: 2020. Tenth European Surveillance of Veterinary Antimicrobial Consumption (ESVAC) Report.
Shen C., Zhong L.-L., Yang Y., Doi Y., Paterson D.L., Stoesser N., Ma F., El-Sayed Ahmed M.A.E.-G., Feng S., Huang S., et al. Dynamics of mcr-1 prevalence and mcr-1-positive Escherichia coli after the cessation of colistin use as a feed additive for animals in China: A prospective cross-sectional and whole genome sequencing-based molecular epidemiological study. Lancet Microbe. 2020;1:e34–e43. doi: 10.1016/S2666-5247(20)30005-7. PubMed DOI
Giani T., Sennati S., Antonelli A., Di Pilato V., Di Maggio T., Mantella A., Niccolai C., Spinicci M., Monasterio J., Castellanos P., et al. 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. Eurosurveillance. 2018;23 doi: 10.2807/1560-7917.ES.2018.23.45.1800115. PubMed DOI PMC
Trung N.V., Matamoros S., Carrique-Mas J.J., Nghia N.H., Nhung N.T., Chieu T.T.B., Mai H.H., Van Rooijen W., Campbell J., Wagenaar J.A., et al. Zoonotic transmission of mcr-1 colistin resistance gene from small-scale poultry farms, Vietnam. Emerg. Infect. Dis. 2017;23:529–532. doi: 10.3201/eid2303.161553. PubMed DOI PMC
Yamamoto Y., Kawahara R., Fujiya Y., Sasaki T., Hirai I., Khong D.T., Nguyen T.N., Nguyen B.X. Wide dissemination of colistin-resistant Escherichia coli with the mobile resistance gene mcr in healthy residents in Vietnam. J. Antimicrob. Chemother. 2019;74:523–524. doi: 10.1093/jac/dky435. PubMed DOI
Germ J., Cerar Kišek T., Kokošar Ulčar B., Lejko Zupanc T., Mrvič T., Kerin Povšič M., Seme K., Pirs M. Surveillance cultures for detection of rectal and lower respiratory tract carriage of colistin-resistant Gram-negative bacilli in intensive care unit patients: Comparison of direct plating and pre-enrichment step. J. Med. Microbiol. 2019;68:1269–1278. doi: 10.1099/jmm.0.001029. PubMed DOI
Saly M., Jayol A., Poirel L., Megraud F., Nordmann P., Dubois V. Prevalence of faecal carriage of colistin-resistant gram-negative rods in a university hospital in Western France, 2016. J. Med. Microbiol. 2017;66:842–843. doi: 10.1099/jmm.0.000497. PubMed DOI
Fernández-Verdugo A., Forcelledo L., Rodríguez-Lozano J., Rodríguez-Lucas C., Barreiro-Hurlé L., Canut A., de la Iglesia P., Escudero D., Calvo J., Boga J.A., et al. Prospective multicentre study of rectal carriage of multidrug-resistant Enterobacteriaceae among health-care workers in Spain. Clin. Microbiol. Infect. 2020;26:649.e1–649.e4. doi: 10.1016/j.cmi.2020.01.015. PubMed DOI
Bourrel A.S., Poirel L., Royer G., Darty M., Vuillemin X., Kieffer N., Clermont O., Denamur E., Nordmann P., Decousser J.W. Colistin resistance in Parisian inpatient faecal Escherichia coli as the result of two distinct evolutionary pathways. J. Antimicrob. Chemother. 2019;74:1521–1530. doi: 10.1093/jac/dkz090. PubMed DOI
Terveer E.M., Nijhuis R.H.T., Crobach M.J.T., Knetsch C.W., Veldkamp K.E., Gooskens J., Kuijper E.J., Claas E.C.J. Prevalence of colistin resistance gene (mcr-1) containing Enterobacteriaceae in feces of patients attending a tertiary care hospital and detection of a mcr-1 containing, colistin susceptible E. coli. PLoS ONE. 2017;12:e0178598. doi: 10.1371/journal.pone.0178598. PubMed DOI PMC
von Wintersdorff C.J.H., Wolffs P.F.G., van Niekerk J.M., Beuken E., van Alphen L.B., Stobberingh E.E., Lashof A.M.L.O., Hoebe C.J.P.A., Savelkoul P.H.M., Penders J. Detection of the plasmid-mediated colistin-resistance gene mcr-1 in faecal metagenomes of Dutch travellers. J. Antimicrob. Chemother. 2016;71:3416–3419. doi: 10.1093/jac/dkw328. PubMed DOI
Schaumburg F., Sertic S.M., Correa-Martinez C., Mellmann A., Köck R., Becker K. Acquisition and colonization dynamics of antimicrobial-resistant bacteria during international travel: A prospective cohort study. Clin. Microbiol. Infect. 2019;25:1287.e1–1287.e7. doi: 10.1016/j.cmi.2019.03.002. PubMed DOI
Gelbicova T., Kolackova I., Krutova M., Karpiskova R. The emergence of mcr-1-mediated colistin-resistant Escherichia coli and Klebsiella pneumoniae in domestic and imported turkey meat in the Czech Republic 2017–2018. Folia Microbiol. 2020;65:211–216. doi: 10.1007/s12223-019-00709-z. PubMed DOI
Nordmann P., Jayol A., Poirel L. A universal culture medium for screening polymyxin-resistant gram-negative isolates. J. Clin. Microbiol. 2016;54:1395–1399. doi: 10.1128/JCM.00446-16. PubMed DOI PMC
Wick R.R., Judd L.M., Gorrie C.L., Holt K.E. Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput. Biol. 2017;13:e1005595. doi: 10.1371/journal.pcbi.1005595. PubMed DOI PMC
Beyrouthy R., Robin F., Lessene A., Lacombat I., Dortet L., Naas T., Ponties V., Bonnet R. MCR-1 and OXA-48 in vivo acquisition in KPC-producing Escherichia coli after colistin treatment. Antimicrob. Agents Chemother. 2017;61:8–11. doi: 10.1128/AAC.02540-16. PubMed DOI PMC
Poirel L., Kieffer N., Brink A., Coetze J., Jayol A., Nordmann P. Genetic features of MCR-1-producing colistin-resistant Escherichia coli isolates in South Africa. Antimicrob. Agents Chemother. 2016;60:4394–4397. doi: 10.1128/AAC.00444-16. PubMed DOI PMC
Gelbicova T., Barakova A., Florianova M., Jamborova I., Zelendova M., Pospisilova L., Kolackova I., Karpiskova R. Dissemination and comparison of genetic determinants of mcr-mediated colistin resistance in Enterobacteriaceae via retailed raw meat products. Front. Microbiol. 2019;10 doi: 10.3389/fmicb.2019.02824. PubMed DOI PMC
Wang Y., Xu C., Zhang R., Chen Y., Shen Y., Hu F., Liu D., Lu J., Guo Y., Xia X., et al. 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. 2020;20:1161–1171. doi: 10.1016/S1473-3099(20)30149-3. PubMed DOI
Zurfluh K., Stephan R., Widmer A., Poirel L., Nordmann P., Nüesch H.J., Hächler H., Nüesch-Inderbinen M. Screening for fecal carriage of MCR-producing Enterobacteriaceae in healthy humans and primary care patients. Antimicrob. Resist. Infect. Control. 2017;6:7–10. doi: 10.1186/s13756-017-0186-z. PubMed DOI PMC
Kusumoto M., Nishiya Y., Kawamura Y. Reactivation of insertionally inactivated Shiga toxin 2 genes of Escherichia coli O157:H7 caused by nonreplicative transposition of the insertion sequence. Appl. Environ. Microbiol. 2000;66:1133–1138. doi: 10.1128/AEM.66.3.1133-1138.2000. PubMed DOI PMC
Kieffer N., Royer G., Decousser J.W., Bourrel A.S., Palmieri M., De La Rosa J.M.O., Jacquier H., Denamur E., Nordmann P., Poirel L. mcr-9, an inducible gene encoding an acquired phosphoethanolamine transferase in Escherichia coli, and its origin. Antimicrob. Agents Chemother. 2019;63 doi: 10.1128/AAC.00965-19. PubMed DOI PMC
Pham Thanh D., Thanh Tuyen H., Nguyen Thi Nguyen T., Chung The H., Wick R.R., Thwaites G.E., Baker S., Holt K.E. Inducible colistin resistance via a disrupted plasmid-borne mcr-1 gene in a 2008 Vietnamese Shigella sonnei isolate. J. Antimicrob. Chemother. 2016;71:2314–2317. doi: 10.1093/jac/dkw173. PubMed DOI PMC
Zhou K., Luo Q., Wang Q., Huang C., Lu H., Rossen J.W.A., Xiao Y., Li L. Silent transmission of an IS1294b-deactivated mcr-1 gene with inducible colistin resistance. Int. J. Antimicrob. Agents. 2018;51:822–828. doi: 10.1016/j.ijantimicag.2018.01.004. PubMed DOI
Liassine N., Assouvie L., Descombes M.C., Tendon V.D., Kieffer N., Poirel L., Nordmann P. Very low prevalence of MCR-1/MCR-2 plasmid-mediated colistin resistance in urinary tract Enterobacteriaceae in Switzerland. Int. J. Infect. Dis. 2016;51:4–5. doi: 10.1016/j.ijid.2016.08.008. PubMed DOI
Pomorska K., Jakubu V., Zelendova M., Dolejska M., Zemlickova H. Detection of plasmid-determined colistin resistance mediated by mcr genes in the Czech Republic. Zpravy Cent. Epidemiol. A Mikrobiol. 2018;27:219–222.
Krutova M., Kalova A., Nycova E., Gelbicova T., Karpiskova R., Smelikova E., Nyc O., Drevinek P., Tkadlec J. The colonisation of Czech travellers and expatriates living in the Czech Republic by colistin-resistant Enterobacteriaceae and whole genome characterisation of E. coli isolates harbouing the mcr-1 genes on plasmid or chromosome: A cross-sectional study. Travel Med. Infect. Dis. 2021;39:101914. doi: 10.1016/j.tmaid.2020.101914. PubMed DOI
Xavier B.B., Lammens C., Ruhal R., Kumar-Singh S., Butaye P., Goossens H., Malhotra-Kumar S. Identification of a novel plasmid-mediated colistin- resistance gene, mcr-2, in Escherichia coli, Belgium, June 2016. Eurosurveillance. 2016;21:6–11. doi: 10.2807/1560-7917.ES.2016.21.27.30280. PubMed DOI
Yin W., Li H., Shen Y., Liu Z., Wang S., Shen Z., Zhang R., Walsh T.R., Shen J., Wang Y. Novel plasmid-mediated colistin resistance gene mcr-3 in Escherichia coli. MBio. 2017;8:4–9. doi: 10.1128/mBio.00543-17. PubMed DOI PMC
Carattoli A., Villa L., Feudi C., Curcio L., Orsini S., Luppi A., Pezzotti G., Magistrali C.F. Novel plasmid-mediated colistin resistance mcr-4 gene in Salmonella and Escherichia coli, Italy 2013, Spain and Belgium, 2015 to 2016. Eurosurveillance. 2017;22:30589. doi: 10.2807/1560-7917.ES.2017.22.31.30589. PubMed DOI PMC
Borowiak M., Fischer J., Hammerl J.A., Hendriksen R.S., Szabo I., Malorny B. Identification of a novel transposon-associated phosphoethanolamine transferase gene, mcr-5, conferring colistin resistance in d-tartrate fermenting Salmonella enterica subsp. enterica serovar Paratyphi B. J. Antimicrob. Chemother. 2017;72:3317–3324. doi: 10.1093/jac/dkx327. PubMed DOI
AbuOun M., Stubberfield E.J., Duggett N.A., Kirchner M., Dormer L., Nunez-Garcia J., Randall L.P., Lemma F., Crook D.W., Teale C., et al. mcr-1 and mcr-2 variant genes identified in Moraxella species isolated from pigs in Great Britain from 2014 to 2015. J. Antimicrob. Chemother. 2017;72:2745–2749. doi: 10.1093/jac/dkx286. PubMed DOI PMC
Yang Y.Q., Li Y.X., Lei C.W., Zhang A.Y., Wang H.N. Novel plasmid-mediated colistin resistance gene mcr-7.1 in Klebsiella pneumoniae. J. Antimicrob. Chemother. 2018;73:1791–1795. doi: 10.1093/jac/dky111. PubMed DOI
Wang X., Wang Y., Zhou Y., Li J., Yin W., Wang S., Zhang S., Shen J., Shen Z., Wang Y. Emergence of a novel mobile colistin resistance gene, mcr-8, in NDM-producing Klebsiella pneumoniae. Emerg. Microbes Infect. 2018;7:122. doi: 10.1038/s41426-018-0124-z. PubMed DOI PMC
European Committee on Antimicrobial Susceptibility Testing Testing Breakpoint Tables for Interpretation of MICs and Zone Diameters. [(accessed on 10 November 2020)];2020 Available online: https://eucast.org/clinical_breakpoints/
Larsen M.V., Cosentino S., Rasmussen S., Friis C., Hasman H., Marvig R.L., Jelsbak L., Sicheritz-Ponten T., Ussery D.W., Aarestrup F.M., et al. Multilocus sequence typing of total-genome-sequenced bacteria. J. Clin. Microbiol. 2012;50:1355–1361. doi: 10.1128/JCM.06094-11. PubMed DOI PMC
Joensen K.G., Tetzschner A.M.M., Iguchi A., Aarestrup F.M., Scheutz F. Rapid and easy in silico serotyping of Escherichia coli isolates by use of whole-genome sequencing data. J. Clin. Microbiol. 2015;53:2410–2426. doi: 10.1128/JCM.00008-15. PubMed DOI PMC
Zankari E., Hasman H., Cosentino S., Vestergaard M., Rasmussen S., Lund O., Aarestrup F.M., Larsen M.V. Identification of acquired antimicrobial resistance genes. J. Antimicrob. Chemother. 2012;67:2640–2644. doi: 10.1093/jac/dks261. PubMed DOI PMC
Carattoli A., Zankari E., Garciá-Fernández A., Larsen M.V., Lund O., Villa L., Aarestrup F.M., Hasman H. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob. Agents Chemother. 2014;58:3895–3903. doi: 10.1128/AAC.02412-14. PubMed DOI PMC
Beghain J., Bridier-Nahmias A., Le Nagard H., Denamur E., Clermont O. ClermonTyping: An easy-to-use and accurate in silico method for Escherichia genus strain phylotyping. Microb. Genom. 2018;4:e000192. doi: 10.1099/mgen.0.000192. PubMed DOI PMC
Siguier P., Perochon J., Lestrade L., Mahillon J., Chandler M. ISfinder: The reference centre for bacterial insertion sequences. Nucleic Acids Res. 2006;34:D32–D36. doi: 10.1093/nar/gkj014. PubMed DOI PMC
Clinical and Laboratory Standards Institute (CLSI) Performance Standards for Antimicrobial Susceptibility Testing. 27th ed. CLSI; Wayne, PA, USA: 2017. Informational Supplement CLSI Document M100-S27.
Feng Y., Zou S., Chen H., Yu Y., Ruan Z. BacWGSTdb 2.0: A one-stop repository for bacterial whole-genome sequence typing and source tracking. Nucleic Acids Res. 2021;49:D644–D650. doi: 10.1093/nar/gkaa821. PubMed DOI PMC