{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T23:55:58Z","timestamp":1790207758920,"version":"4.1.0"},"reference-count":79,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2022,6,7]],"date-time":"2022-06-07T00:00:00Z","timestamp":1654560000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Comprehensive Development for Implementing Smart Specialization Strategies","award":["EFOP-3.6.1.-16-2016-00004"],"award-info":[{"award-number":["EFOP-3.6.1.-16-2016-00004"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Antibiotics"],"abstract":"<jats:p>Antimicrobials in wastewater promote the emergence of antibiotic resistance, facilitated by selective pressure and transfer of resistant genes. Enteric bacteria belonging to Escherichia coli, Klebsiella pneumoniae, Klebsiella oxytoca, Enterobacter cloacae, and Citrobacter species (n = 126) from hospital effluents and proximate wastewater treatment plant were assayed for susceptibility to four antimicrobial classes. The \u03b2-lactamase encoding genes harbored in plasmids were genotyped and the plasmids were sequenced. A multidrug resistance phenotype was found in 72% (n = 58) of E. coli isolates, 70% (n = 43) of Klebsiella species isolates, and 40% (n = 25) of Enterobacter and Citrobacter species. Moreover, 86% (n = 50) of E. coli, 77% (n = 33) of Klebsiella species, and 25% (n = 4) of Citrobacter species isolates phenotypically expressed extended spectrum \u03b2-lactamase. Regarding ESBL genes, blaCTX-M-27 and blaTEM-1 were found in E. coli, while Klebsiella species harbored blaCTX-M-15, blaCTX-M-30, or blaSHV-12. Genes coding for aminoglycoside modifying enzymes, adenylyltransferases (aadA1, aadA5), phosphotransferases (aph(6)-1d, aph(3\u2033)-Ib), acetyltransferases (aac(3)-IIa), (aac(6)-Ib), sulfonamide\/trimethoprim resistant dihydropteroate synthase (sul), dihydrofolate reductase (dfrA), and quinolone resistance protein (qnrB1) were also identified. Monitoring wastewater from human sources for acquired resistance in clinically important bacteria may provide a cheaper alternative in regions facing challenges that limit clinical surveillance.<\/jats:p>","DOI":"10.3390\/antibiotics11060776","type":"journal-article","created":{"date-parts":[[2022,6,9]],"date-time":"2022-06-09T10:49:14Z","timestamp":1654771754000},"page":"776","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":21,"title":["Characterization of \u03b2-Lactamases and Multidrug Resistance Mechanisms in Enterobacterales from Hospital Effluents and Wastewater Treatment Plant"],"prefix":"10.3390","volume":"11","author":[{"given":"Christopher","family":"Mutuku","sequence":"first","affiliation":[{"name":"Department of General and Environmental Microbiology, Faculty of Sciences, University of P\u00e9cs, 7622 P\u00e9cs, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1016-6066","authenticated-orcid":false,"given":"Szilvia","family":"Melegh","sequence":"additional","affiliation":[{"name":"Department of Medical Microbiology and Immunology, Medical School, University of P\u00e9cs, 7622 P\u00e9cs, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Krisztina","family":"Kovacs","sequence":"additional","affiliation":[{"name":"Department of Medical Microbiology and Immunology, Medical School, University of P\u00e9cs, 7622 P\u00e9cs, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4043-3428","authenticated-orcid":false,"given":"Peter","family":"Urban","sequence":"additional","affiliation":[{"name":"Bioinformatics Research Group, Szent\u00e1gothai Research Centre, 7624 P\u00e9cs, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1566-0143","authenticated-orcid":false,"given":"Eszter","family":"Vir\u00e1g","sequence":"additional","affiliation":[{"name":"Educomat Ltd., Iskola utca 12\/A, 8360 Keszthely, Hungary"},{"name":"Department of Molecular Biotechnology and Microbiology, Institute of Biotechnology, Faculty of Science and Technology, University of Debrecen, Egyetem Square 1, 4032 Debrecen, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Reka","family":"Heninger","sequence":"additional","affiliation":[{"name":"Department of General and Environmental Microbiology, Faculty of Sciences, University of P\u00e9cs, 7622 P\u00e9cs, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Robert","family":"Herczeg","sequence":"additional","affiliation":[{"name":"Bioinformatics Research Group, Szent\u00e1gothai Research Centre, 7624 P\u00e9cs, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7065-1736","authenticated-orcid":false,"given":"\u00c1gnes","family":"Sonnevend","sequence":"additional","affiliation":[{"name":"Department of Medical Microbiology and Immunology, Medical School, University of P\u00e9cs, 7622 P\u00e9cs, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Attila","family":"Gyenesei","sequence":"additional","affiliation":[{"name":"Bioinformatics Research Group, Szent\u00e1gothai Research Centre, 7624 P\u00e9cs, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Csaba","family":"Fekete","sequence":"additional","affiliation":[{"name":"Department of General and Environmental Microbiology, Faculty of Sciences, University of P\u00e9cs, 7622 P\u00e9cs, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8531-4070","authenticated-orcid":false,"given":"Zoltan","family":"Gazdag","sequence":"additional","affiliation":[{"name":"Department of General and Environmental Microbiology, Faculty of Sciences, University of P\u00e9cs, 7622 P\u00e9cs, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,6,7]]},"reference":[{"key":"ref_1","first-page":"108","article-title":"Study of awareness of pharmacy employees in Ukraine with the problem of antibiotics resistance","volume":"6","author":"Iakovlieva","year":"2020","journal-title":"Health Sci."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1016\/S1473-3099(18)30605-4","article-title":"Attributable deaths and disability-adjusted life-years caused by infections with antibiotic-resistant bacteria in the EU and the European Economic Area in 2015: A population-level modelling analysis","volume":"19","author":"Cassini","year":"2019","journal-title":"Lancet Infect. Dis."},{"key":"ref_3","unstructured":"(2019). No Time to Wait\u2014Securing the Future from Drug-Resistant Infections. Report to the Secretary General of the Nations, UN."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"120","DOI":"10.3329\/jbcps.v29i3.9431","article-title":"Antimicrobial resistance: A man made crisis","volume":"29","author":"Islam","year":"2011","journal-title":"J. Bangladesh Coll. Physicians Surg."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"310","DOI":"10.1038\/nrmicro3439","article-title":"Tackling antibiotic resistance: The environmental framework","volume":"13","author":"Berendonk","year":"2015","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"eaau9124","DOI":"10.1126\/sciadv.aau9124","article-title":"Antibiotic resistance in European wastewater treatment plants mirrors the pattern of clinical antibiotic resistance prevalence","volume":"5","author":"Kneis","year":"2019","journal-title":"J. Sci. Adv."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"O132","DOI":"10.1111\/1469-0691.12336","article-title":"KPC-2 and OXA-48 carbapenemase-harbouring Enterobacteriaceae detected in an Austrian wastewater treatment plant","volume":"20","author":"Galler","year":"2014","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"957","DOI":"10.1016\/j.watres.2012.11.027","article-title":"Urban wastewater treatment plants as hotspots for the release of antibiotics in the environment: A review","volume":"47","author":"Michael","year":"2013","journal-title":"Water Res."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"978","DOI":"10.1016\/j.fct.2008.06.012","article-title":"Gene transfer events and their occurrence in selected environments","volume":"47","author":"Kelly","year":"2009","journal-title":"J. Food Chem. Toxicol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"276","DOI":"10.1097\/PAT.0000000000000237","article-title":"Resistance mechanisms in Enterobacteriaceae","volume":"47","author":"Partridge","year":"2015","journal-title":"Pathology"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1016\/S1473-3099(08)70041-0","article-title":"Extended-spectrum \u03b2-lactamase-producing Enterobacteriaceae: An emerging public-health concern","volume":"8","author":"Pitout","year":"2008","journal-title":"Lancet Infect. Dis."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"3909","DOI":"10.1128\/AAC.00622-08","article-title":"Prevalence and mechanisms of broad-spectrum beta-lactam resistance in Enterobacteriaceae: A children\u2019s hospital experience","volume":"52","author":"Qin","year":"2008","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1177\/14690446050060060701","article-title":"Extended-spectrum beta lactamases: An overview","volume":"6","year":"2005","journal-title":"Br. J. Infect. Control"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1016\/j.jhin.2016.01.010","article-title":"What happens in hospitals does not stay in hospitals: Antibiotic-resistant bacteria in hospital wastewater systems","volume":"93","author":"Hocquet","year":"2016","journal-title":"J. Hosp. Infect."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1119","DOI":"10.1016\/j.scitotenv.2017.09.217","article-title":"Occurrence and characteristics of extended-spectrum \u03b2-lactamase-and carbapenemase-producing bacteria from hospital effluents in Singapore","volume":"615","author":"Haller","year":"2018","journal-title":"Sci. Total Environ."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"13906","DOI":"10.1021\/acs.est.7b03380","article-title":"Hospital Wastewater Releases of Carbapenem-Resistance Pathogens and Genes in Urban India","volume":"51","author":"Lamba","year":"2017","journal-title":"Environ. Sci. Technol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"2306","DOI":"10.1099\/mic.0.028233-0","article-title":"Detection of 140 clinically relevant antibiotic-resistance genes in the plasmid metagenome of wastewater treatment plant bacteria showing reduced susceptibility to selected antibiotics","volume":"155","author":"Szczepanowski","year":"2009","journal-title":"Microbiology"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1128\/CMR.18.4.657-686.2005","article-title":"Extended-spectrum beta-lactamases: A clinical update","volume":"18","author":"Paterson","year":"2005","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"969","DOI":"10.1128\/AAC.01009-09","article-title":"Updated functional classification of beta-lactamases","volume":"54","author":"Bush","year":"2010","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"S4","DOI":"10.1186\/cc6820","article-title":"Gram-negative antibiotic resistance: There is a price to pay","volume":"12","author":"Slama","year":"2008","journal-title":"Crit. Care"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1238","DOI":"10.1128\/AAC.01285-07","article-title":"Diversity of extended-spectrum \u03b2-lactamases and class C \u03b2-lactamases among cloacal Escherichia coli isolates in Belgian broiler farms","volume":"52","author":"Smet","year":"2008","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"19044","DOI":"10.2807\/ese.13.47.19044-en","article-title":"Increasing prevalence of ESBL-producing Enterobacteriaceae in Europe","volume":"13","author":"Coque","year":"2008","journal-title":"Eurosurveillance"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Codjoe, F.S., and Donkor, E.S. (2018). Carbapenem resistance: A review. Med. Sci., 6.","DOI":"10.3390\/medsci6010001"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1093\/jac\/dkt392","article-title":"Carbapenemase-producing Enterobacteriaceae and non-Enterobacteriaceae from animals and the environment: An emerging public health risk of our own making?","volume":"69","author":"Woodford","year":"2014","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"204","DOI":"10.1016\/j.diagmicrobio.2012.02.007","article-title":"Enterobacteriaceae producing the KPC-2 carbapenemase from hospital sewage","volume":"73","author":"Zhang","year":"2012","journal-title":"Diagn. Microbiol. Infect. Dis."},{"key":"ref_26","unstructured":"ECDC (2020). Annual Report of the European Antimicrobial Resistance Surveillance Network Antimicrobial Resistance Surveillance in Europe 2020."},{"key":"ref_27","first-page":"887","article-title":"Monitoring and comparison of antibiotic resistant bacteria and their resistance genes in municipal and hospital wastewaters","volume":"5","author":"Aali","year":"2014","journal-title":"Int. J. Prev. Med."},{"key":"ref_28","unstructured":"Chartier, Y. (2014). Safe Management of Wastes from Health-Care Activities."},{"key":"ref_29","unstructured":"Morris, D., Harris, S., Morris, C., Commins, E., and Cormican, M. (2008). Hospital Effluent: Impact on the Microbial Environment and Risk to Human Health."},{"key":"ref_30","first-page":"164","article-title":"Multiple antibiotic resistance (MAR) indices of Pseudomonas and Klebsiella species isolates in Lagos University Teaching Hospital","volume":"14","author":"Osundiya","year":"2013","journal-title":"Afr. J. Clin. Exp. Microbiol."},{"key":"ref_31","first-page":"1","article-title":"Epidemiology and resistance levels of Enterobacteriaceae isolates from urinary tract infections expressed as Multiple Antibiotic Resistance (MAR) indices","volume":"29","year":"2019","journal-title":"J. Pharm. Res. Int."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1016\/j.jhin.2016.03.007","article-title":"Carbapenemase-producing Enterobacteriaceae in hospital wastewater: A reservoir that may be unrelated to clinical isolates","volume":"93","author":"White","year":"2016","journal-title":"J. Hosp. Infect."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"4772","DOI":"10.1128\/AEM.02898-09","article-title":"Enumeration and characterization of antimicrobial-resistant Escherichia coli bacteria in effluent from municipal, hospital, and secondary treatment facility sources","volume":"76","author":"Galvin","year":"2010","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"2","DOI":"10.2807\/1560-7917.ES.2019.24.46.1900656","article-title":"Decreasing and stabilising trends of antimicrobial consumption and resistance in Escherichia coli and Klebsiella pneumoniae in segmented regression analysis, European Union\/European Economic Area, 2001 to 2018","volume":"24","author":"Penalva","year":"2019","journal-title":"Eurosurveillance"},{"key":"ref_35","unstructured":"Connor, R., Renata, A., Ortigara, C., Koncag\u00fcl, E., Uhlenbrook, S., Lamizana-Diallo, B.M., Zadeh, S.M., Qadir, M., Kjell\u00e9n, M., and Sj\u00f6din, J. (2017). The United Nations World Water Development Report 2017. Wastewater: The Untapped Resource, UN."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/j.watres.2014.02.041","article-title":"High dissemination of extended-spectrum beta-lactamase-producing Enterobacteriaceae in effluents from wastewater treatment plants","volume":"56","author":"Gonzalez","year":"2014","journal-title":"Water. Res."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"785411","DOI":"10.3389\/fmicb.2021.785411","article-title":"Comparison of Extended-Spectrum Beta-Lactamase-Producing Escherichia coli Isolates from Rooks (Corvus frugilegus) and Contemporary Human-Derived Strains: A One Health Perspective","volume":"12","author":"Nagy","year":"2021","journal-title":"Front. Microbiol."},{"key":"ref_38","first-page":"3","article-title":"Population snapshot of the extended-spectrum \u03b2-lactamase-producing Escherichia coli invasive strains isolated from a Hungarian hospital","volume":"21","author":"Kamotsay","year":"2022","journal-title":"Ann. Clin. Microbiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"135550","DOI":"10.1016\/j.scitotenv.2019.135550","article-title":"Antibiotic resistant Klebsiella spp. from a hospital, hospital effluents and wastewater treatment plants in the uMgungundlovu District, KwaZulu-Natal, South Africa","volume":"712","author":"King","year":"2020","journal-title":"Sci. Total Environ."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1016\/j.jgar.2019.01.002","article-title":"Extended-spectrum beta-lactamase-producing Enterobacteriaceae from animal origin and wastewater in Tunisia: First detection of O25b-B23-CTX-M-27-ST131 Escherichia coli and CTX-M-15\/OXA-204-producing Citrobacter freundii from wastewater","volume":"17","author":"Sghaier","year":"2019","journal-title":"J. Glob. Antimicrob. Resist."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1173","DOI":"10.1128\/AAC.01076-09","article-title":"Network for Antimicrobial Resistance Surveillance (Singapore) Surveillance and correlation of antibiotic prescription and resistance of Gram-negative bacteria in Singaporean hospitals","volume":"54","author":"Hsu","year":"2010","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1383","DOI":"10.3201\/eid1808.111816","article-title":"blaNDM-1\u2013positive Klebsiella pneumoniae from Environment, Vietnam","volume":"18","author":"Isozumi","year":"2012","journal-title":"Emerg. Infect. Dis."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1524","DOI":"10.3201\/eid1809.111727","article-title":"blaOXA-181\u2013positive Klebsiella pneumoniae, Singapore","volume":"18","author":"Koh","year":"2012","journal-title":"Emerg. Infect. Dis."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"531","DOI":"10.1016\/j.ijantimicag.2013.08.020","article-title":"Early (2008\u20132010) hospital outbreak of Klebsiella pneumoniae producing OXA-48 carbapenemase in the UK","volume":"42","author":"Thomas","year":"2013","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"O27","DOI":"10.1111\/1469-0691.12293","article-title":"Emergence of VIM-4 metallo-\u03b2-lactamase-producing Klebsiella pneumoniae ST15 clone in the Clinical Centre University of P\u00e9cs, Hungary","volume":"20","author":"Melegh","year":"2014","journal-title":"Clin. Microbiol. Infect. Control"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"788","DOI":"10.1099\/jmm.0.000498","article-title":"Spectrum and antibiotic resistance of uropathogens between 2004 and 2015 in a tertiary care hospital in Hungary","volume":"66","author":"Magyar","year":"2017","journal-title":"J. Med. Microbiol."},{"key":"ref_47","first-page":"1735","article-title":"Antimicrobial resistance in Enterococcus spp.","volume":"40","author":"Bernardo","year":"2006","journal-title":"isolated in inflow, effluent and sludge from municipal sewage water treatment plants. Water Res."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1017","DOI":"10.1111\/j.1365-2672.2008.03828.x","article-title":"Species distribution and antimicrobial resistance of enterococci isolated from surface and ocean water","volume":"105","author":"Moore","year":"2008","journal-title":"J. Appl. Microbiol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1016\/j.ecoenv.2016.10.031","article-title":"Characterization of CTX-M enzymes, quinolone resistance determinants, and antimicrobial residues from hospital sewage, wastewater treatment plant, and river water","volume":"136","author":"Conte","year":"2017","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"2261","DOI":"10.3389\/fmicb.2017.02261","article-title":"Double-serine fluoroquinolone resistance mutations advance major international clones and lineages of various multi-drug resistant bacteria","volume":"8","author":"Fuzi","year":"2017","journal-title":"Front. Microbiol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"312","DOI":"10.1086\/502687","article-title":"A nosocomial outbreak of Escherichia coli producing CTX-M-15 and OXA-30 beta-lactamase","volume":"27","author":"Pai","year":"2006","journal-title":"Infect. Control Hosp. Epidemiol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1016\/j.plasmid.2015.03.005","article-title":"Plasmids in antibiotic susceptible and antibiotic resistant commensal Escherichia coli from healthy Australian adults","volume":"80","author":"Moran","year":"2015","journal-title":"Plasmid"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"e00709-20","DOI":"10.1128\/mSphere.00709-20","article-title":"F Plasmids Are the Major Carriers of Antibiotic Resistance Genes in Human-Associated Commensal Escherichia coli","volume":"5","author":"Stephens","year":"2020","journal-title":"mSphere"},{"key":"ref_54","doi-asserted-by":"crossref","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":"ref_55","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1016\/j.jgar.2017.04.009","article-title":"Detection of multidrug resistant (MDR) bacteria in untreated waste water disposals of hospitals in Dhaka City, Bangladesh","volume":"10","author":"Rabbani","year":"2017","journal-title":"J. Glob. Antimicrob. Resist."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"1306","DOI":"10.3201\/eid1108.050192","article-title":"Drug-resistant diarrheogenic Escherichia coli, Mexico","volume":"11","author":"Cerna","year":"2005","journal-title":"Emerg. Infect. Dis."},{"key":"ref_57","first-page":"17","article-title":"Role of untreated liquid hospital waste to the development of antibiotic resistant bacteria","volume":"2","author":"Islam","year":"2008","journal-title":"J. Innov. Dev. Strategy"},{"key":"ref_58","first-page":"1859","article-title":"Evidence for a complex relationship between antibiotics and antibiotic-resistant Escherichia coli: From medical center patients to a receiving environment","volume":"46","author":"Capdeville","year":"2012","journal-title":"J. Environ. Sci."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1038\/nrmicro2298","article-title":"The population genetics of commensal Escherichia coli","volume":"8","author":"Tenaillon","year":"2010","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_60","unstructured":"Morris, D., Harris, S., Morris, C., Commins, E., and Cormican, M. (2016). Hospital Effluent: Impact on the Microbial Environment and Risk to Human Health, Report no. 162."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"1157","DOI":"10.1007\/s00253-010-2583-6","article-title":"Factors influencing antibiotic resistance burden in municipal wastewater treatment plants","volume":"87","author":"Novo","year":"2010","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_62","unstructured":"Cheesbrough, M. (1990). Medical Laboratory Manual for Tropical Countries, Tropical Health Technology."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1016\/j.patbio.2009.07.020","article-title":"MALDI-TOF mass spectrometry to identify clinical bacterial isolates: Evaluation in a teaching hospital in Lille","volume":"58","author":"Blondiaux","year":"2010","journal-title":"Pathol. Biol."},{"key":"ref_64","unstructured":"EUCAST (2018). Breakpoint Tables for Interpretation of MICs and Zone Diameters, European Committee on Antimicrobial Susceptibility Testing. Version 8.1."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1186\/s12941-016-0144-2","article-title":"Genetic characterization of TEM-type ESBL-associated antibacterial resistance in Enterobacteriaceae in a tertiary hospital in Ghana","volume":"15","author":"Bonney","year":"2016","journal-title":"Ann. Clin. Microbiol. Antimicrob."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"3724","DOI":"10.1128\/AAC.47.12.3724-3732.2003","article-title":"Prevalence and molecular epidemiology of CTX-M extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae in Russian hospitals","volume":"47","author":"Edelstein","year":"2003","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"1167","DOI":"10.1128\/JCM.01988-06","article-title":"Detection of extended-spectrum beta-lactamases among Enterobacteriaceae by use of semiautomated microbiology systems and manual detection procedures","volume":"45","author":"Wiegand","year":"2007","journal-title":"Clin. Microbiol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1089\/mdr.2004.10.334","article-title":"Prevalence of \u03b2-lactamases among ampicillin-resistant Escherichia coli and Salmonella isolated from food animals in Denmark","volume":"10","author":"Olesen","year":"2004","journal-title":"Microb. Drug Resist."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1016\/j.diagmicrobio.2010.12.002","article-title":"Multiplex PCR for detection of acquired carbapenemase genes","volume":"70","author":"Poirel","year":"2011","journal-title":"Diagn. Microbiol. Infect. Dis."},{"key":"ref_70","unstructured":"Andrews, S., Krueger, F., Segonds-Pichon, A., Biggins, L., Krueger, C., Wingett, S., and FastQC (2022, May 04). A Quality Control Tool for High Throughput Sequence Data. Babraham Bioinformatics. Available online: http:\/\/www.bioinformatics.babraham.ac.uk\/projects\/fastqc."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"2114","DOI":"10.1093\/bioinformatics\/btu170","article-title":"Trimmomatic: A flexible trimmer for Illumina sequence data","volume":"30","author":"Bolger","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1016\/S0022-2836(05)80360-2","article-title":"Basic local alignment search tool","volume":"215","author":"Altschul","year":"1990","journal-title":"J. Mol. Biol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"4636","DOI":"10.1093\/nar\/27.23.4636","article-title":"Improved microbial gene identification with GLIMMER","volume":"27","author":"Delcher","year":"1999","journal-title":"Nucleic Acids Res."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"3420","DOI":"10.1093\/nar\/gkn176","article-title":"High-throughput functional annotation and data mining with the Blast2GO suite","volume":"36","author":"Terol","year":"2008","journal-title":"Nucleic Acids Res."},{"key":"ref_75","doi-asserted-by":"crossref","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":"ref_76","doi-asserted-by":"crossref","first-page":"3895","DOI":"10.1128\/AAC.02412-14","article-title":"In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing","volume":"58","author":"Carattoli","year":"2014","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_77","first-page":"e1005944","article-title":"MUMmer4: A fast and versatile genome alignment system","volume":"14","author":"Delcher","year":"2018","journal-title":"Comput. Biol."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1128\/JB.01202-08","article-title":"A genomic distance based on MUM indicates discontinuity between most bacterial species and genera","volume":"191","author":"Deloger","year":"2009","journal-title":"J. Bacteriol."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"254","DOI":"10.1093\/molbev\/msj030","article-title":"Application of phylogenetic networks in evolutionary studies","volume":"23","author":"Huson","year":"2006","journal-title":"Mol. Biol. 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