Multi-Drug Resistant Plasmids with ESBL/AmpC and mcr-5.1 in Paraguayan Poultry Farms: The Linkage of Antibiotic Resistance and Hatcheries

. 2021 Apr 17 ; 9 (4) : . [epub] 20210417

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid33920558

Grantová podpora
CEITEC/Literak/ITA2021 2021ITA31 Internal Grant Agency of University of Veterinary and Pharmaceutical Sciences Brno

Odkazy

PubMed 33920558
PubMed Central PMC8072826
DOI 10.3390/microorganisms9040866
PII: microorganisms9040866
Knihovny.cz E-zdroje

Poultry represents a common source of bacteria with resistance to antibiotics including the critically important ones. Selective cultivation using colistin, cefotaxime and meropenem was performed for 66 chicken samples coming from 12 farms in Paraguay while two breeding companies supplied the farms. A total of 62 Escherichia coli and 22 Klebsiella pneumoniae isolates were obtained and representative isolates were subjected to whole-genome sequencing. Relatively high prevalence of phylogenetic group D and F was observed in E. coli isolates and several zoonotic sequence types (STs) including ST457 (14 isolates), ST38 (5), ST10 (2), ST117 (2) or ST93 (4) were detected. Isolates from three farms, which purchased chicken from a Paraguayan hatchery showed higher prevalence of mcr-5.1 and blaCTX-M-8 compared to the other nine farms, which purchased chickens from a Brazilian hatchery. Moreover, none of the K. pneumoniae isolates were linked to the Paraguayan hatchery. ESBL/AmpC and mcr-5-carrying multi-drug resistant (MDR) plasmids were characterized, and complete sequences were obtained for eight plasmids. The study shed light on Paraguayan poultry farms as a reservoir of antibiotic resistance commonly conferred via MDR plasmids and showed linkage between resistance and origin of the chickens at the hatcheries level.

Zobrazit více v PubMed

Ventola C.L. The Antibiotic Resistance Crisis. Pharm. Ther. 2015;40:278–283. doi: 10.5796/electrochemistry.82.749. DOI

Aarestrup F.M. Veterinary drug usage and antimicrobial resistance in bacteria of animal origin. Basic Clin. Pharmacol. Toxicol. 2005;96:271–281. doi: 10.1111/j.1742-7843.2005.pto960401.x. PubMed DOI

Carattoli A. Animal reservoirs for extended spectrum β-lactamase producers. Clin. Microbiol. Infect. 2008;14:117–123. doi: 10.1111/j.1469-0691.2007.01851.x. PubMed DOI

Leverstein-van Hall M.A., Dierikx C.M., Cohen Stuart J., Voets G.M., van den Munckhof M.P., van Essen-Zandbergen A., Platteel T., Fluit A.C., van de Sande-Bruinsma N., Scharinga J., et al. Dutch patients, retail chicken meat and poultry share the same ESBL genes, plasmids and strains. Clin. Microbiol. Infect. 2011;17:873–880. doi: 10.1111/j.1469-0691.2011.03497.x. PubMed DOI

Norizuki C., Wachino J.I., Suzuki M., Kawamura K., Nagano N., Kimura K., Arakawa Y. Specific blaCTX-M-8/IncI1 Plasmid Transfer among Genetically Diverse Escherichia coli Isolates between Humans and Chickens. Antimicrob. Agent. Chemother. 2017;61:e00663-17. doi: 10.1128/AAC.00663-17. PubMed DOI PMC

Apostolakos I., Feudi C., Eichhorn I., Palmieri N., Fasolato L., Schwarz S., Piccirillo A. High‑resolution characterisation of ESBL/pAmpC—producing Escherichia coli isolated from the broiler production pyramid. Sci. Rep. 2020;10:11123. doi: 10.1038/s41598-020-68036-9. PubMed DOI PMC

Ferreira J.C., Penha Filho R.A.C., Neves Andrade L., Berchieri A., Jr., Costa Darini A.N. Evaluation and characterization of plasmids carrying CTX-M genes in a non-clonal population of multidrug-resistant Enterobacteriaceae isolated from poultry in Brazil. Diagn. Microbiol. Infect. Dis. 2016;85:444–448. doi: 10.1016/j.diagmicrobio.2016.05.011. PubMed DOI

Wang C., Feng Y., Liu L., Wei L., Kang M., Zong Z. Identification of novel mobile colistin resistance gene mcr-10. Emerg. Microbe. Infect. 2020;9:508–516. doi: 10.1080/22221751.2020.1732231. PubMed DOI PMC

Quiroga C., Nastro M., di Conza J. Current scenario of plasmid-mediated colistin resistance in Latin America. Rev. Argent. Microbiol. 2019;51:93–100. doi: 10.1016/j.ram.2018.05.001. PubMed DOI

Fernandes M.R., Moura Q., Sartori L., Silva K.C., Cunha M.P., Esposito F., Lopes R., Otutumi L.K., Gonçalves D.D., Dropa M., et al. Silent dissemination of colistin-resistant Escherichia coli in South America could contribute to the global spread of the mcr-1 gene. Euro. Surveill. 2016;21:30214. doi: 10.2807/1560-7917.ES.2016.21.17.30214. PubMed DOI

Dropa M., Balsalobre L.C., Lincopan N., Matté G.R., Matté M.H. Complex class 1 integrons harboring CTX-M-2-encoding genes in clinical Enterobacteriaceae from a hospital in Brazil. J. Infect. Dev. Ctries. 2015;9:890–897. doi: 10.3855/jidc.6241. PubMed DOI

Nesporova K., Jamborova I., Valcek A., Medvecky M., Literak I., Dolejska M. Various conjugative plasmids carrying the mcr-5 gene in Escherichia coli isolates from healthy chickens in Paraguay. J. Antimicrob. Chemother. 2019;74:3394–3397. doi: 10.1093/jac/dkz317. PubMed DOI

Nesporova K., Wyrsch E.R., Valcek A., Bitar I., Chaw K., Harris P., Hrabak J., Literak I., Djordjevic S.P., Dolejska M. Escherichia coli sequence type 457 is an emerging extended-spectrum-β-lactam-resistant lineage with reservoirs in wildlife and food-producing animals. Antimicrob. Agent. Chemother. 2021;65:e01118-20. doi: 10.1128/AAC.01118-20. PubMed DOI PMC

Dobiasova H., Dolejska M., Jamborova I., Brhelova E., Blazkova L., Papousek I., Kozlova M., Klimes J., Cizek A., Literak I. Extended spectrum beta-lactamase and fluoroquinolone resistance genes and plasmids among Escherichia coli isolates from zoo animals, Czech Republic. FEMS Microbiol. Ecol. 2013;85:604–611. doi: 10.1111/1574-6941.12149. PubMed DOI

Perez-Perez F.J., Hanson N.D. Detection of Plasmid-Mediated AmpC Beta-Lactamase Genes in Clinical Isolates by Using Multiplex PCR. JCM. 2002;157:5336. doi: 10.1128/JCM.40.6.2153. PubMed DOI PMC

Rebelo A.R., Bortolaia V., Kjeldgaard J.S., Pedersen S.K., Leekitcharoenphon P., Hansen I.M., Guerra B., Malorny B., Borowiak M., Hammerl J.A., et al. Multiplex PCR for detection of plasmid-mediated mcr-4 and mcr-5 for surveillance purposes. Euro. Surveill. 2018;23:17-00672. doi: 10.2807/1560-7917.ES.2018.23.6.17-00672. PubMed DOI PMC

Bolger A.M., Lohse M., Usadel B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics. 2018;30:2114–2120. doi: 10.1093/bioinformatics/btu170. PubMed DOI PMC

Bankevich A., Nurk S., Antipov D., Gurevich A.A., Dvorkin M., Kulikov A.S., Lesin V.M., Nikolenko S.I., Pham S., Prjibelski A.D., et al. SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 2012;5:455–477. doi: 10.1089/cmb.2012.0021. 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

Larsen M.V., Cosentino S., Rasmussen S., Friis C., Hasman H., Lykke Marvig R., Jelsbak L., Sicheritz-Pontén 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

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. Agent. 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

Kaas R.S., Leekitcharoenphon P., Aarestrup F.M., Lund O. Solving the problem of comparing whole bacterial genomes across different sequencing platforms. PLoS ONE. 2014;9:e104984. doi: 10.1371/journal.pone.0104984. PubMed DOI PMC

Seemann T. Prokka: Rapid prokaryotic genome annotation. Bioinformatics. 2014;30:2068–2069. doi: 10.1093/bioinformatics/btu153. PubMed DOI

Page A.J., Cummins C.A., Hunt M., Wong V.K., Reuter S., Holden M.T.G., Fookes M., Falush D., Keane J.A. Parkhill, Roary: Rapid large-scale prokaryote pan genome analysis. Bioinformatics. 2015;31:3691–3693. doi: 10.1093/bioinformatics/btv421. PubMed DOI PMC

Stamatakis A. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–1313. doi: 10.1093/bioinformatics/btu033. PubMed DOI PMC

Letunic I., Bork P. Interactive Tree of Life (iTOL) v4: Recent updates and new developments. Nucleic Acids Res. 2019;47:256–259. doi: 10.1093/nar/gkz239. PubMed DOI PMC

Darling A.E., Mau B., Perna N.T. Progressive Mauve: Multiple Genome Alignment with Gene Gain, Loss and Rearrangement. PLoS ONE. 2010;5:e11147. doi: 10.1371/journal.pone.0011147. PubMed DOI PMC

Carattoli A., Bertini A., Villa L., Falbo V., Hopkins K.L., Threlfall E.J. Identification of plasmids by PCR-based replicon typing. J. Microbiol. Method. 2005;63:219–228. doi: 10.1016/j.mimet.2005.03.018. PubMed DOI

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

Alikhan N., Petty N.K., Ben Zakour N.L., Beatson S.A. BLAST Ring Image Generator (BRIG): Simple prokaryote genome comparisons. BMC Genom. 2011;12:402. doi: 10.1186/1471-2164-12-402. PubMed DOI PMC

Braykov N.P., Eisenberg J.N.S., Grossman M., Zhang L., Vasco K., Cevallos W., Muñoz D., Acevedo A., Moser K.A., Marrs C.F., et al. Antibiotic resistance in animal and environmental samples associated with small-scale poultry farming in northwestern Ecuador. mSphere. 2016;1:e00021-15. doi: 10.1128/mSphere.00021-15. PubMed DOI PMC

Chauvin C., Devendec L., Jouy E., Cornec L., Francart S., Marois-Créhan C., Kempf I. National Prevalence of Resistance to Third-Generation Cephalosporins in Escherichia coli Isolates from Layer Flocks in France. Antimicrob. Agent. Chemother. 2013;57:6351–6353. doi: 10.1128/AAC.01460-13. PubMed DOI PMC

Dame-Korevaar A., Fischer E.A.J., van der Goot J., Stegeman A., Mevius D. Transmission routes of ESBL/pAmpC producing bacteria in the broiler production pyramid, a literature review. Prev. Vet. Med. 2019;162:136–150. doi: 10.1016/j.prevetmed.2018.12.002. PubMed DOI

Guo S., Wakeham D., Brouwers H.J., Cobbold R.N., Abraham S., Mollinger J.L., Johnson J.R., Chapman T.A., Gordon D.M., Barrs V.R., et al. Human-associated fluoroquinolone-resistant Escherichia coli clonal lineages, including ST354, isolated from canine feces and extraintestinal infections in Australia. Microb. Infect. 2015;17:266–274. doi: 10.1016/j.micinf.2014.12.016. PubMed DOI

Zhuge X., Zhou Z., Jiang M., Wang Z., Sun Y., Tang F., Xue F., Ren J., Dai J. Chicken-source Escherichia coli within phylogroup F shares virulence genotypes and is closely related to extraintestinal pathogenic E. coli causing human infections. Transbound. Emerg. Dis. 2020:1–16. doi: 10.1111/tbed.13755. PubMed DOI

Hung W.T., Cheng M.F., Tseng F.C., Chen Y.S., Lee S.S.J., Chang T.H., Lin H.H., Hung C.H., Wang J.L. Bloodstream infection with extended-spectrum beta-lactamase-producing Escherichia coli: The role of virulence genes. J. Microbiol. Immunol. Infect. 2019;52:947–955. doi: 10.1016/j.jmii.2019.03.005. PubMed DOI

Maluta R.P., Logue C.M., Casas M.R.T., Meng T., Lopes Guastalli E.A., Galvão Rojas T.C., Montelli A.C., Sadatsune T., de Carvalho Ramos M., Nolan K.L., et al. Overlapped sequence types (STs) and serogroups of avian pathogenic (APEC) and human extra-intestinal pathogenic (ExPEC) Escherichia coli isolated in Brazil. PLoS ONE. 2014;9:e105016. doi: 10.1371/journal.pone.0105016. PubMed DOI PMC

De Carvalho M.P.N., Fernandes M.R., Sellera F.P., Lopes R., Monte D.F., Hippólito A.G., Milanelo L., Raso T.F., Lincopan N. International clones of extended-spectrum β -lactamase (CTX- M)-producing Escherichia coli in peri-urban wild animals, Brazil. Transbound. Emerg. Dis. 2020;67:1804–1815. doi: 10.1111/tbed.13558. PubMed DOI PMC

Hayer S.S., Lim S., Hong S., Elnekave E., Johnson T.J., Rovira A., Vannucci F. Genetic Determinants of Resistance to Extended-Spectrum Cephalosporin and Fluoroquinolone in Escherichia coli Isolated from Diseased Pigs in the United States. mSphere. 2020;5:e00990-20. doi: 10.1128/mSphere.00990-20. PubMed DOI PMC

Turton J.F., Doumith M., Hopkins K.L., Perry C., Meunier D., Woodford N. Clonal expansion of Escherichia coli ST38 carrying a chromosomally integrated OXA-48 carbapenemase gene. J. Med. Microbiol. 2016;65:538–546. doi: 10.1099/jmm.0.000248. PubMed DOI

Guenther S., Semmler T., Stubbe A., Stubbe M., Wieler L.H., Schaufler K. Chromosomally encoded ESBL genes in Escherichia coli of ST38 from Mongolian wild birds. J. Antimicrob. Chemother. 2017;72:310–1313. doi: 10.1093/jac/dkx006. PubMed DOI

Fu L., Huang M., Zhang X., Yang X., Liu Y., Zhang L. Microbial Pathogenesis Frequency of virulence factors in high biofilm formation blaKPC-2 producing Klebsiella pneumoniae strains from hospitals. Microb. Pathog. 2018;116:168–172. doi: 10.1016/j.micpath.2018.01.030. PubMed DOI

Markovska R., Stoeva T., Boyanova L., Stankova P., Pencheva D., Keuleyan E., Murjeva M., Sredkova M., Ivanova D., Lazarova G., et al. Dissemination of successful international clone ST15 and clonal complex 17 among Bulgarian CTX-M-15 producing K. pneumoniae isolates. Diagn. Microbiol. Infect. Dis. 2017;89:310–313. doi: 10.1016/j.diagmicrobio.2017.08.012. PubMed DOI

Ewers C., Stamm I., Pfeifer Y., Wieler L.H., Kopp P.A., Schønning K., Prenger-Berninghoff E., Scheufen S., Stolle I., Günther S., et al. Clonal spread of highly successful ST15-CTX-M-15 Klebsiella pneumoniae in companion animals and horses. J. Antimicrob. Chemother. 2014;69:2676–2680. doi: 10.1093/jac/dku217. PubMed DOI

Lam M.M.C., Wyres K.L., Wick R.R., Judd L.M., Fostervold A., Holt K.E., Löhr I.H. Convergence of virulence and MDR in a single plasmid vector in MDR Klebsiella pneumoniae ST15. J. Antimicrob. Chemother. 2019;74:1218–1222. doi: 10.1093/jac/dkz028. PubMed DOI PMC

Palmeira J.D., Haenni M., Metayer V., Madec J.Y., Ferreira M.H.N. Epidemic spread of IncI1/pST113 plasmid carrying the Extended-Spectrum Beta-Lactamase (ESBL) blaCTX-M-8 gene in Escherichia coli of Brazilian cattle. Vet. Microbiol. 2020;243:108629. doi: 10.1016/j.vetmic.2020.108629. PubMed DOI

Melo L.C., Oresco C., Leigue L., Netto H.M., Melville P.A., Benites N.R., Saras E., Haenni M., Lincopan N., Madec J.Y. Prevalence and molecular features of ESBL/pAmpC-producing Enterobacteriaceae in healthy and diseased companion animals in Brazil. Vet. Microbiol. 2018;22:59–66. doi: 10.1016/j.vetmic.2018.05.017. PubMed DOI

Eller C., Leistner R., Guerra B., Fischer J., Wendt C., Rabsch W., Werner G., Pfeifer Y. Emergence of extended-spectrum β-lactamase (ESBL) CTX-M-8 in Germany. J. Antimicrob. Chemother. 2014;69:562–564. doi: 10.1093/jac/dkt387. PubMed DOI

Palmeira J.D., Ferreira H., Madec J.Y., Haenni M. Pandemic Escherichia coli ST648 isolate harbouring fosA3 and blaCTX-M-8 on an IncI1/ST113 plasmid: A new successful combination for the spread of fosfomycin resistance? J. Glob. Antimicrob. Resist. 2018;15:254–255. doi: 10.1016/j.jgar.2018.10.025. PubMed DOI

Roer L., Overballe-Petersen S., Hansen F., Johannesen T.B., Stegger M., Bortolaia V., Leekitcharoenphon P., Korsgaard H.B., Seyfarth A.M., Mossong J., et al. ST131 fimH22 Escherichia coli isolate with a blaCMY-2/IncI1/ST12 plasmid obtained from a patient with bloodstream infection: Highly similar to E. coli isolates of broiler origin. J. Antimicrob. Chemother. 2019;74:557–560. doi: 10.1093/jac/dky484. PubMed DOI

Rozwandowicz M., Brouwer M.S.M., Fischer J., Wagenaar J.A., Guerra B., Mevius D.J. Plasmids carrying antimicrobial resistance genes in Enterobacteriaceae. J. Antimicrob. Chemother. 2018;73:1121–1137. doi: 10.1093/jac/dkx488. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...