{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,20]],"date-time":"2026-10-20T15:46:45Z","timestamp":1792511205715,"version":"4.5.0"},"reference-count":82,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,4,6]],"date-time":"2023-04-06T00:00:00Z","timestamp":1680739200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:sec><jats:title>Background<\/jats:title><jats:p>The increasing number of infections caused by <jats:italic>Escherichia coli<\/jats:italic> resistant to clinically important antibiotics is a global concern for human and animal health. High overall levels of extended-spectrum beta-lactamase (ESBL)-producing and ciprofloxacin-resistant (ciproR) <jats:italic>Escherichia coli<\/jats:italic> in livestock are reported in Belgium. This cross-sectional study aimed to genotypically characterize and trace ESBL-and ciproR-<jats:italic>E. coli<\/jats:italic> of Belgian food-producing animals.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>A total of 798 fecal samples were collected in a stratified-random sampling design from Belgian broilers and sows. Consequently, 77 ESBL-<jats:italic>E. coli<\/jats:italic> and 84 ciproR-<jats:italic>E. coli<\/jats:italic> were sequenced using Illumina MiSeq. Minimum inhibitory concentration (MIC) for fluoroquinolones and cephalosporins were determined. Molecular <jats:italic>in silico<\/jats:italic> typing, resistance and virulence gene determination, and plasmid identification was performed. Scaffolds harboring ESBL or plasmid-mediated quinolone resistance (PMQR) genes were analyzed to detect mobile genetic elements (MGEs) and plasmid origins. Core genome allelic distances were used to determine genetic relationships among isolates.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>A variety of <jats:italic>E. coli<\/jats:italic> sequence types (ST) (<jats:italic>n<\/jats:italic>\u2009=\u200963), resistance genes and virulence profiles was detected. ST10 was the most frequently encountered ST (8.1%, <jats:italic>n<\/jats:italic>\u2009=\u200913). The pandemic multidrug-resistant clone ST131 was not detected. Most farms harbored more than one ESBL type, with <jats:italic>bla<\/jats:italic><jats:sub>CTX-M-1<\/jats:sub> (41.6% of ESBL-<jats:italic>E. coli<\/jats:italic>) being the most prevalent and <jats:italic>bla<\/jats:italic><jats:sub>CTX M-15<\/jats:sub> (<jats:italic>n<\/jats:italic>\u2009=\u20093) being the least prevalent. PMQR genes (15.5%, <jats:italic>n<\/jats:italic>\u2009=\u200913) played a limited role in the occurrence of ciproR-<jats:italic>E. coli<\/jats:italic>. More importantly, sequential acquisition of mutations in quinolone resistance-determining regions (QRDR) of <jats:italic>gyrA<\/jats:italic> and <jats:italic>parC<\/jats:italic> led to increasing MICs for fluoroquinolones. GyrA S83L, D87N and ParC S80I mutations were strongly associated with high-level fluoroquinolone resistance. Genetically related isolates identified within the farms or among different farms highlight transmission of resistant <jats:italic>E. coli<\/jats:italic> or the presence of a common reservoir. IncI1-I(alpha) replicon type plasmids carried different ESBL genes (<jats:italic>bla<\/jats:italic><jats:sub>CTX-M-1<\/jats:sub>, <jats:italic>bla<\/jats:italic><jats:sub>CTX-M-32<\/jats:sub> and <jats:italic>bla<\/jats:italic><jats:sub>TEM-52C<\/jats:sub>). In addition, the detection of plasmid replicons with associated insertion sequence (IS) elements and ESBL\/PMQR genes in different farms and among several STs (e.g., IncI1-I(alpha)\/IncX3) underline that plasmid transmission could be another important contributor to transmission of resistance in these farms.<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusion<\/jats:title><jats:p>Our findings reveal a multifaceted narrative of transmission pathways. These findings could be relevant in understanding and battling the problem of antibiotic resistance in farms.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fmicb.2023.1150470","type":"journal-article","created":{"date-parts":[[2023,4,6]],"date-time":"2023-04-06T12:43:38Z","timestamp":1680785018000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":30,"title":["Genetic characterization of ESBL-producing and ciprofloxacin-resistant Escherichia coli from Belgian broilers and pigs"],"prefix":"10.3389","volume":"14","author":[{"given":"Sien","family":"De Koster","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Moniek","family":"Ringenier","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Basil Britto","family":"Xavier","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christine","family":"Lammens","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dieter","family":"De Coninck","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katrien","family":"De Bruyne","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Klaas","family":"Mensaert","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marjolein","family":"Kluytmans-van den Bergh","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jan","family":"Kluytmans","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jeroen","family":"Dewulf","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Herman","family":"Goossens","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"name":"on behalf of the i-4-1-Health Study Group","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2023,4,6]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1371\/journal.pone.0178623","article-title":"The genetic diversity of commensal Escherichia coli strains isolated from nonantimicrobial treated pigs varies according to age group","volume":"12","author":"Ahmed","year":"2017","journal-title":"PLoS One"},{"key":"ref2","doi-asserted-by":"publisher","first-page":"4479","DOI":"10.1093\/nar\/19.16.4479","article-title":"Molecular characterization of the soxRS genes of Escherichia coli: two genes control a superoxide stress regulon","volume":"19","author":"Am\u00e1bile-cuevas","year":"1991","journal-title":"Nucleic Acids Res."},{"key":"ref3","doi-asserted-by":"publisher","first-page":"455","DOI":"10.1089\/cmb.2012.0021","article-title":"SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing","volume":"19","author":"Bankevich","year":"2012","journal-title":"J. Comput. Biol."},{"key":"ref4","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1099\/mgen.0.000192","article-title":"ClermonTyping: an easy-to-use and accurate in silico method for Escherichia genus strain phylotyping","volume":"4","author":"Beghain","year":"2018","journal-title":"Microb Genom"},{"key":"ref5","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3390\/microorganisms9081676","article-title":"The pheno- and genotypic characterization of porcine Escherichia coli isolates","volume":"9","author":"Bernreiter-Hofer","year":"2021","journal-title":"Microorganisms"},{"key":"ref6","doi-asserted-by":"publisher","first-page":"e0135402","DOI":"10.1371\/journal.pone.0135402","article-title":"Distribution, numbers, and diversity of ESBL-Producing E. coli in the poultry farm environment","volume":"10","author":"Blaak","year":"2015","journal-title":"PLoS One"},{"key":"ref7","doi-asserted-by":"publisher","first-page":"3511","DOI":"10.1073\/pnas.1419939112","article-title":"AcrB drug-binding pocket substitution confers clinically relevant resistance and altered substrate specificity","volume":"112","author":"Blair","year":"2015","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"ref8","doi-asserted-by":"publisher","first-page":"2","DOI":"10.1186\/s13567-021-01017-6","article-title":"Recurring outbreaks by the same Escherichia coli ST10 clone in a broiler unit during 18 months","volume":"53","author":"Bojesen","year":"2022","journal-title":"Vet. Res."},{"key":"ref9","doi-asserted-by":"publisher","first-page":"3491","DOI":"10.1093\/jac\/dkaa345","article-title":"ResFinder 4.0 for predictions of phenotypes from genotypes","volume":"75","author":"Bortolaia","year":"2020","journal-title":"J. Antimicrob. Chemother."},{"key":"ref10","doi-asserted-by":"publisher","first-page":"558455","DOI":"10.3389\/fvets.2020.558455","article-title":"Comparing farm biosecurity and antimicrobial use in high-antimicrobial-consuming broiler and pig farms in the Belgian-Dutch border region","volume":"7","author":"Caekebeke","year":"2020","journal-title":"Front Vet Sci"},{"key":"ref11","doi-asserted-by":"publisher","first-page":"3895","DOI":"10.1007\/978-1-4939-9877-7_20","article-title":"PlasmidFinder and in silico pMLST: identification and typing of plasmid replicons in whole-genome sequencing (WGS)","volume":"2075","author":"Carattoli","year":"2020","journal-title":"Methods Mol. Biol."},{"key":"ref12","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fmicb.2019.00076","article-title":"Diversity of plasmids and genes encoding resistance to extended spectrum cephalosporins in commensal Escherichia coli from Dutch livestock in 2007-2017","volume":"10","author":"Ceccarelli","year":"2019","journal-title":"Front. Microbiol."},{"key":"ref13","doi-asserted-by":"publisher","first-page":"D694","DOI":"10.1093\/nar\/gkv1239","article-title":"VFDB 2016: hierarchical and refined dataset for big data analysis - 10 years on","volume":"44","author":"Chen","year":"2016","journal-title":"Nucleic Acids Res."},{"key":"ref14","doi-asserted-by":"publisher","first-page":"e1004776","DOI":"10.1371\/journal.pgen.1004776","article-title":"Dissemination of cephalosporin resistance genes between Escherichia coli strains from farm animals and humans by specific plasmid lineages","volume":"10","author":"de Been","year":"2014","journal-title":"PLoS Genet."},{"key":"ref15","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3390\/antibiotics10080945","article-title":"ESBL-producing, carbapenem-and ciprofloxacin-resistant Escherichia coli in Belgian and Dutch broiler and pig farms: a cross-sectional and cross-border study","volume":"10","author":"De Koster","year":"2021","journal-title":"Antibiotics"},{"key":"ref16","doi-asserted-by":"publisher","first-page":"e79005","DOI":"10.1371\/journal.pone.0079005","article-title":"Presence of ESBL\/AmpC -producing Escherichia coli in the broiler production pyramid: a descriptive study","volume":"8","author":"Dierikx","year":"2013","journal-title":"PLoS One"},{"key":"ref17","doi-asserted-by":"publisher","first-page":"2118","DOI":"10.1093\/jac\/dkw144","article-title":"Prevalence and diversity of IncX plasmids carrying fluoroquinolone and \u03b2-lactam resistance genes in Escherichia coli originating from diverse sources and geographical areas","volume":"71","author":"Dobiasova","year":"2016","journal-title":"J. Antimicrob. Chemother."},{"key":"ref18","doi-asserted-by":"publisher","first-page":"19880","DOI":"10.1038\/s41598-020-76877-7","article-title":"The importance of using whole genome sequencing and extended spectrum beta-lactamase selective media when monitoring antimicrobial resistance","volume":"10","author":"Duggett","year":"2020","journal-title":"Sci. Rep."},{"key":"ref19","doi-asserted-by":"publisher","first-page":"140","DOI":"10.1016\/j.chom.2019.10.022","article-title":"A Bioinformatic analysis of integrative Mobile genetic elements highlights their role in bacterial adaptation","volume":"27","author":"Durrant","year":"2020","journal-title":"Cell Host Microbe"},{"key":"ref20","doi-asserted-by":"publisher","first-page":"e06490","DOI":"10.2903\/j.efsa.2021.6490","article-title":"The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2018\/2019","volume":"19","year":"2021","journal-title":"EFSA J."},{"key":"ref21","unstructured":"2021"},{"key":"ref22","unstructured":"2021"},{"key":"ref23","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1111\/nyas.12830.Mechanisms","article-title":"Mechanisms of drug resistance: quinolone resistance","volume":"176","author":"Gordon","year":"2015","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref24","doi-asserted-by":"publisher","first-page":"1072","DOI":"10.1093\/bioinformatics\/btt086","article-title":"QUAST: quality assessment tool for genome assemblies","volume":"29","author":"Gurevich","year":"2013","journal-title":"Bioinformatics"},{"key":"ref25","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1093\/jac\/dkm167","article-title":"Substrate specificity of the OqxAB multidrug resistance pump in Escherichia coli and selected enteric bacteria","volume":"60","author":"Hansen","year":"2007","journal-title":"J. Antimicrob. Chemother."},{"key":"ref26","doi-asserted-by":"publisher","first-page":"3070","DOI":"10.1128\/JCM.01096-13","article-title":"Susceptibility breakpoint for enrofloxacin against swine salmonella spp","volume":"51","author":"Hao","year":"2013","journal-title":"J. Clin. Microbiol."},{"key":"ref27","doi-asserted-by":"publisher","first-page":"e00990","DOI":"10.1128\/mSphere.00990-20","article-title":"Genetic determinants of resistance to extended-Spectrum cephalosporin and fluoroquinolone in Escherichia coli isolated from diseased pigs in the United States","author":"Hayer","year":"2020"},{"key":"ref28","doi-asserted-by":"publisher","first-page":"2","DOI":"10.1128\/microbiolspec.PLAS-0006-2013.Plasmid-mediated","article-title":"Plasmid-mediated quinolone resistance","author":"Jacoby","year":"2015"},{"key":"ref29","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3390\/antibiotics10020099","article-title":"Genomic analysis of antimicrobial resistance and resistance plasmids in salmonella serovars from poultry in Nigeria","volume":"10","author":"Jibril","year":"2021","journal-title":"Antibiotics"},{"key":"ref30","doi-asserted-by":"publisher","first-page":"2410","DOI":"10.1128\/JCM.00008-15","article-title":"Rapid and easy in silico serotyping of Escherichia coli isolates by use of whole-genome sequencing data","volume":"53","author":"Joensen","year":"2015","journal-title":"J. Clin. Microbiol."},{"key":"ref31","doi-asserted-by":"publisher","first-page":"261","DOI":"10.1086\/315217","article-title":"Extended virulence genotypes of Escherichia coli strains from patients with Urosepsis in relation to phylogeny and host compromise","volume":"181","author":"Johnson","year":"2000","journal-title":"J. Infect. Dis."},{"key":"ref32","doi-asserted-by":"publisher","first-page":"124","DOI":"10.12688\/wellcomeopenres.14826.1","article-title":"Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications","volume":"3","author":"Jolley","year":"2018","journal-title":"Wellcome Open Res"},{"key":"ref33","doi-asserted-by":"publisher","first-page":"1236","DOI":"10.3390\/antibiotics10101236","article-title":"Dissection of highly prevalent qnrS1-carrying IncX plasmid types in commensal Escherichia coli from German food and livestock","volume":"10","author":"Juraschek","year":"2021","journal-title":"Antibiotics"},{"key":"ref34","doi-asserted-by":"publisher","first-page":"7113","DOI":"10.1128\/AEM.00600-11","article-title":"Mechanisms of fluoroquinolone resistance in Escherichia coli isolates from food-producing animals","volume":"77","author":"Karczmarczyk","year":"2011","journal-title":"Appl. Environ. Microbiol."},{"key":"ref35","doi-asserted-by":"publisher","first-page":"e02769","DOI":"10.1128\/AEM.02769-19","article-title":"Dissemination of quinolone-resistant Escherichia coli in the Norwegian broiler and pig production chains and possible persistence in the broiler production environment","volume":"86","author":"Kaspersen","year":"2020","journal-title":"Appl. Environ. Microbiol."},{"key":"ref36","author":"Kluytmans-van den Bergh","year":"2019"},{"key":"ref37","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fmicb.2021.592291","article-title":"Plasmid-borne and chromosomal ESBL\/AmpC genes in Escherichia coli and Klebsiella pneumoniae in global food products","volume":"12","author":"Kurittu","year":"2021","journal-title":"Front. Microbiol."},{"key":"ref38","doi-asserted-by":"publisher","first-page":"15108","DOI":"10.1038\/s41598-021-93970-7","article-title":"Genomic evolution of antimicrobial resistance in Escherichia coli","volume":"11","author":"Leekitcharoenphon","year":"2021","journal-title":"Sci. Rep."},{"key":"ref39","doi-asserted-by":"publisher","first-page":"W293","DOI":"10.1093\/nar\/gkab301","article-title":"Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation","volume":"49","author":"Letunic","year":"2021","journal-title":"Nucleic Acids Res."},{"key":"ref40","doi-asserted-by":"publisher","first-page":"873","DOI":"10.1111\/j.1469-0691.2011.03497.x","article-title":"Dutch patients, retail chicken meat and poultry share the same ESBL genes, plasmids and strains","volume":"17","author":"Leverstein-van Hall","year":"2011","journal-title":"Clin. Microbiol. Infect."},{"key":"ref41","doi-asserted-by":"publisher","first-page":"3222","DOI":"10.1128\/AAC.47.10.3222-3232.2003","article-title":"Mutation rate and evolution of fluoroquinolone resistance in Escherichia coli isolates from patients with urinary tract infections","volume":"47","author":"Lindgren","year":"2003","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref42","doi-asserted-by":"publisher","first-page":"268","DOI":"10.1111\/j.1469-0691.2011.03570.x","article-title":"Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance","volume":"18","author":"Magiorakos","year":"2012","journal-title":"Clin. Microbiol. Infect."},{"key":"ref43","doi-asserted-by":"publisher","first-page":"302","DOI":"10.1089\/fpd.2014.1860","article-title":"Multilocus sequence typing and virulence gene profiles associated with Escherichia coli from human and animal sources","volume":"12","author":"Manges","year":"2015","journal-title":"Foodborne Pathog. Dis."},{"key":"ref44","doi-asserted-by":"publisher","first-page":"UTI-0006-2012","DOI":"10.1128\/microbiolspec.uti-0006-2012","article-title":"Reservoirs of Extraintestinal pathogenic Escherichia coli","volume":"3","author":"Manges","year":"2015","journal-title":"Microbiol Spectr"},{"key":"ref45","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3390\/antibiotics9110782","article-title":"Snapshot study of whole genome sequences of Escherichia coli from healthy companion animals, livestock, wildlife, humans and food in Italy","volume":"9","author":"Massella","year":"2020","journal-title":"Antibiotics"},{"key":"ref46","doi-asserted-by":"publisher","first-page":"3348","DOI":"10.1128\/AAC.00419-13","article-title":"The comprehensive antibiotic resistance database","volume":"57","author":"McArthur","year":"2013","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref47","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1371\/journal.pone.0154019","article-title":"Plasmid and host strain characteristics of Escherichia coli resistant to extended-spectrum cephalosporins in the norwegian broiler production","volume":"11","author":"Mo","year":"2016","journal-title":"PLoS One"},{"key":"ref48","doi-asserted-by":"publisher","first-page":"106382","DOI":"10.1016\/j.ijantimicag.2021.106382","article-title":"Dynamics of extended-spectrum cephalosporin-resistant Escherichia coli in pig farms: a longitudinal study","volume":"58","author":"Moor","year":"2021","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref49","doi-asserted-by":"publisher","first-page":"629","DOI":"10.1016\/s0140-6736(21)02724-0","article-title":"Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis","volume":"399","author":"Murray","year":"2022","journal-title":"Lancet"},{"key":"ref50","doi-asserted-by":"publisher","first-page":"3812","DOI":"10.1093\/nar\/gkg509","article-title":"SIFT: predicting amino acid changes that affect protein function","volume":"31","author":"Ng","year":"2003","journal-title":"Nucleic Acids Res."},{"key":"ref51","doi-asserted-by":"publisher","first-page":"2089","DOI":"10.1128\/aac.42.8.2089","article-title":"Overexpression of the marA or soxS regulatory gene in clinical topoisomerase mutants of Escherichia coli","volume":"42","author":"Oethinger","year":"1998","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref52","doi-asserted-by":"publisher","first-page":"173","DOI":"10.1016\/j.ijantimicag.2009.03.006","article-title":"Extended-spectrum \u03b2-lactamase-producing Escherichia coli in Spain belong to a large variety of multilocus sequence typing types, including ST10 complex\/a, ST23 complex\/a and ST131\/B2","volume":"34","author":"Oteo","year":"2009","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref53","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1128\/CMR.00088-17","article-title":"Mobile genetic elements associated with antimicrobial resistance","volume":"31","author":"Partridge","year":"2018","journal-title":"Clin. Microbiol. Rev."},{"key":"ref54","doi-asserted-by":"publisher","first-page":"75","DOI":"10.1093\/jac\/dkw364","article-title":"Ciprofloxacin selects for RNA polymerase mutations with pleiotropic antibiotic resistance effects","volume":"72","author":"Pietsch","year":"2017","journal-title":"J. Antimicrob. Chemother."},{"key":"ref55","doi-asserted-by":"publisher","first-page":"2938","DOI":"10.1128\/AAC.47.9.2938-2945.2003","article-title":"Insertion sequence ISEcp1B is involved in expression and mobilization of a blaCTX-M \u03b2-lactamase gene","volume":"47","author":"Poirel","year":"2003","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref56","doi-asserted-by":"publisher","first-page":"1017","DOI":"10.1111\/1751-7915.13040","article-title":"Environmental adaptation and vertical dissemination of ESBL-\/pAmpC-producing Escherichia coli in an integrated broiler production chain in the absence of an antibiotic treatment","volume":"11","author":"Projahn","year":"2018","journal-title":"Microb. Biotechnol."},{"key":"ref57","unstructured":"2020"},{"key":"ref58","doi-asserted-by":"publisher","first-page":"e000143","DOI":"10.1099\/mgen.0.000143","article-title":"Porcine commensal Escherichia coli: a reservoir for class 1 integrons associated with IS26","volume":"3","author":"Reid","year":"2017","journal-title":"Microb Genom"},{"key":"ref59","doi-asserted-by":"publisher","first-page":"380","DOI":"10.1111\/1469-0691.12646","article-title":"Pandemic lineages of extraintestinal pathogenic Escherichia coli","volume":"20","author":"Riley","year":"2014","journal-title":"Clin. Microbiol. Infect."},{"key":"ref60","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1038\/nm1347","article-title":"Fluoroquinolone-modifying enzyme: a new adaptation of a common aminoglycoside acetyltransferase","volume":"12","author":"Robicsek","year":"2006","journal-title":"Nat. Med."},{"key":"ref61","doi-asserted-by":"publisher","first-page":"2538","DOI":"10.1128\/JCM.00737-17","article-title":"Development of a web tool for Escherichia coli subtyping based on fimH alleles","volume":"55","author":"Roer","year":"2017","journal-title":"J. Clin. Microbiol."},{"key":"ref62","doi-asserted-by":"publisher","first-page":"1121","DOI":"10.1093\/jac\/dkx488","article-title":"Plasmids carrying antimicrobial resistance genes in Enterobacteriaceae","volume":"73","author":"Rozwandowicz","year":"2018","journal-title":"J. Antimicrob. Chemother."},{"key":"ref63","doi-asserted-by":"publisher","first-page":"350","DOI":"10.1016\/j.cmi.2017.12.016","article-title":"Whole genome sequencing options for bacterial strain typing and epidemiologic analysis based on single nucleotide polymorphism versus gene-by-gene\u2013based approaches","volume":"24","author":"Sch\u00fcrch","year":"2018","journal-title":"Clin. Microbiol. Infect."},{"key":"ref64","doi-asserted-by":"publisher","first-page":"2068","DOI":"10.1093\/bioinformatics\/btu153","article-title":"Prokka: rapid prokaryotic genome annotation","volume":"30","author":"Seemann","year":"2014","journal-title":"Bioinformatics"},{"key":"ref65","doi-asserted-by":"publisher","first-page":"D32","DOI":"10.1093\/nar\/gkj014","article-title":"ISfinder: the reference Centre for bacterial insertion sequences","volume":"34","author":"Siguier","year":"2006","journal-title":"Nucleic Acids Res."},{"key":"ref66","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1099\/mgen.0.000166","article-title":"chewBBACA: a complete suite for gene-by-gene schema creation and strain identification","volume":"4","author":"Silva","year":"2018","journal-title":"Microb. Genom."},{"key":"ref67","doi-asserted-by":"publisher","first-page":"1238","DOI":"10.1128\/AAC.01285-07","article-title":"Diversity of extended-Spectrum -lactamases and class C -lactamases among cloacal Escherichia coli isolates in Belgian broiler farms","volume":"52","author":"Smet","year":"2008","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref68","doi-asserted-by":"publisher","first-page":"1900136","DOI":"10.2807\/1560-7917.ES.2019.24.50.1900136","article-title":"Use of whole genome sequencing of commensal Escherichia coli in pigs for antimicrobial resistance surveillance, United Kingdom, 2018","volume":"24","author":"Stubberfield","year":"2019","journal-title":"Eur. Secur."},{"key":"ref69","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1128\/JCM.01269-20","article-title":"In silico genotyping of Escherichia coli isolates for sequencing data","volume":"58","author":"Tetzschner","year":"2020","journal-title":"J. Clin. Microbiol."},{"key":"ref70","unstructured":"2022"},{"key":"ref71","doi-asserted-by":"publisher","first-page":"407","DOI":"10.1128\/JCM.02069-13","article-title":"Characterization of Escherichia coli isolates from hospital inpatients or outpatients with urinary tract infection","volume":"52","author":"Toval","year":"2014","journal-title":"J. Clin. Microbiol."},{"key":"ref72","doi-asserted-by":"publisher","first-page":"3050","DOI":"10.1128\/AAC.49.7.3050-3052.2005","article-title":"Interaction of the plasmid-encoded quinolone resistance protein QnrA with Escherichia coli topoisomerase IV","volume":"49","author":"Tran","year":"2005","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref73","doi-asserted-by":"publisher","first-page":"190","DOI":"10.1016\/j.vetmic.2017.08.009","article-title":"High abundance and diversity of extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli in faeces and tonsils of pigs at slaughter","volume":"208","author":"van Damme","year":"2017","journal-title":"Vet. Microbiol."},{"key":"ref74","doi-asserted-by":"publisher","first-page":"543","DOI":"10.1093\/jac\/dkz507","article-title":"Transmission of ESBL-producing Escherichia coli between broilers and humans on broiler farms","volume":"75","author":"Van Hoek","year":"2020","journal-title":"J. Antimicrob. Chemother."},{"key":"ref75","doi-asserted-by":"publisher","first-page":"6122","DOI":"10.1128\/jb.179.19.6122-6126.1997","article-title":"Role of the acrAB locus in organic solvent tolerance mediated by expression of marA, soxS, or robA in Escherichia coli","volume":"179","author":"White","year":"1997","journal-title":"J. Bacteriol."},{"key":"ref76","unstructured":"2018"},{"key":"ref77","unstructured":"2018"},{"key":"ref78","doi-asserted-by":"publisher","first-page":"100769","DOI":"10.1016\/j.isci.2019.100769","article-title":"BacPipe: a rapid, user-friendly whole-genome sequencing pipeline for clinical diagnostic bacteriology","volume":"23","author":"Xavier","year":"2020","journal-title":"iScience"},{"key":"ref79","doi-asserted-by":"publisher","first-page":"3354","DOI":"10.1128\/AAC.00339-07","article-title":"New plasmid-mediated fluoroquinolone efflux pump, QepA, found in an Escherichia coli clinical isolate","volume":"51","author":"Yamane","year":"2007","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref80","doi-asserted-by":"publisher","first-page":"4765","DOI":"10.1038\/s41467-021-25096-3","article-title":"An omics-based framework for assessing the health risk of antimicrobial resistance genes","volume":"12","author":"Zhang","year":"2021","journal-title":"Nat. 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