{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,18]],"date-time":"2026-09-18T20:32:58Z","timestamp":1789763578001,"version":"4.0.1"},"reference-count":89,"publisher":"Public Library of Science (PLoS)","issue":"11","license":[{"start":{"date-parts":[[2020,11,16]],"date-time":"2020-11-16T00:00:00Z","timestamp":1605484800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/publicdomain\/zero\/1.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:p>Though carbapenems are not licensed for use in food animals in the U.S., carbapenem resistance among Enterobacteriaceae has been identified in farm animals and their environments. The objective of our study was to determine the extent to which older-generation \u03b2-lactam antibiotics approved for use in food animals in the U.S. might differentially select for resistance to antibiotics of critical importance to human health, such as carbapenems.<jats:italic>Escherichia coli (E<\/jats:italic>.<jats:italic>coli)<\/jats:italic>strains from humans, food animals, or the environment bearing a single \u03b2-lactamase gene (n = 20 each) for<jats:italic>bla<\/jats:italic><jats:sub>TEM-1<\/jats:sub>,<jats:italic>bla<\/jats:italic><jats:sub>CMY-2<\/jats:sub>, and<jats:italic>bla<\/jats:italic><jats:sub>CTX-M-*<\/jats:sub>or else<jats:italic>bla<\/jats:italic><jats:sub><jats:italic>KPC\/IMP\/NDM<\/jats:italic><\/jats:sub>(due to limited availability, often in combination with other<jats:italic>bla<\/jats:italic>genes), were identified, along with 20<jats:italic>E<\/jats:italic>.<jats:italic>coli<\/jats:italic>strains lacking any known beta-lactamase genes. Baseline estimates of intrinsic bacterial fitness were derived from the population growth curves. Effects of ampicillin (32 \u03bcg\/mL), ceftriaxone (4 \u03bcg\/mL) and meropenem (4 \u03bcg\/mL) on each strain and resistance-group also were assessed. Further,<jats:italic>in vitro<\/jats:italic>batch cultures were prepared by mixing equal concentrations of 10 representative<jats:italic>E<\/jats:italic>.<jats:italic>coli<\/jats:italic>strains (two from each resistance gene group), and each mixture was incubated at 37\u00b0C for 24 hours in non-antibiotic cation-adjusted Mueller-Hinton II (CAMH-2) broth, ampicillin + CAMH-2 broth (at 2, 4, 8, 16, and 32 \u03bcg\/mL) and ceftiofur + CAMH-2 broth (at 0.5, 1, 2, 4, and 8\u03bcg\/mL). Relative and absolute abundance of resistance-groups were estimated phenotypically. Line plots of the raw data were generated, and non-linear Gompertz models and multilevel mixed-effect linear regression models were fitted to the data. The observed strain growth rate distributions were significantly different across the groups. AmpC strains (i.e.,<jats:italic>bla<\/jats:italic><jats:sub>CMY-2<\/jats:sub>) had distinctly less robust (p &lt; 0.05) growth in ceftriaxone (4 \u03bcg\/mL) compared to extended-spectrum beta-lactamase (ESBL) producers harboring<jats:italic>bla<\/jats:italic><jats:sub>CTX-M-*<\/jats:sub>variants. With increasing beta-lactam antibiotic concentrations, relative proportions of ESBLs and CREs were over-represented in the mixed bacterial communities; importantly, this was more pronounced with ceftiofur than with ampicillin. These results indicate that aminopenicillins and extended-spectrum cephalosporins would be expected to propagate carbapenemase-producing Enterobacteriaceae in food animals if and when Enterobacteriaceae from human health care settings enter the food animal environment.<\/jats:p>","DOI":"10.1371\/journal.pone.0242195","type":"journal-article","created":{"date-parts":[[2020,11,16]],"date-time":"2020-11-16T18:30:52Z","timestamp":1605551452000},"page":"e0242195","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":24,"title":["Can the use of older-generation beta-lactam antibiotics in livestock production over-select for beta-lactamases of greatest consequence for human medicine? An in vitro experimental model"],"prefix":"10.1371","volume":"15","author":[{"given":"Olanrewaju J.","family":"Ogunrinu","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Keri N.","family":"Norman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Javier","family":"Vinasco","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9207-9999","authenticated-orcid":true,"given":"Gizem","family":"Levent","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sara D.","family":"Lawhon","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Virginia R.","family":"Fajt","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Victoria V.","family":"Volkova","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tara","family":"Gaire","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Toni L.","family":"Poole","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kenneth J.","family":"Genovese","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9216-1308","authenticated-orcid":true,"given":"Thomas E.","family":"Wittum","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0538-5961","authenticated-orcid":true,"given":"H. Morgan","family":"Scott","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2020,11,16]]},"reference":[{"issue":"suppl_1","key":"pone.0242195.ref001","doi-asserted-by":"crossref","first-page":"S28","DOI":"10.1093\/infdis\/jiw282","article-title":"The Epidemiology of Carbapenem-Resistant Enterobacteriaceae: The Impact and Evolution of a Global Menace","volume":"215","author":"LK Logan","year":"2017","journal-title":"J Infect Dis"},{"key":"pone.0242195.ref002","unstructured":"WHO | Global action plan on antimicrobial resistance [Internet]. WHO. [cited 2019 Aug 18]. Available from: http:\/\/www.who.int\/antimicrobial-resistance\/publications\/global-action-plan\/en\/."},{"key":"pone.0242195.ref003","unstructured":"Centres for Disease Control and Prevention. Antibiotic resistance threats in the United States, 2013. Centres for Disease Control and Prevention, US Department of Health and \u2026; 2013."},{"key":"pone.0242195.ref004","article-title":"Review on antimicrobial resistance, tackling drug-resistant infections globally: final report and recommendations.","author":"J O\u2019Neill","year":"2016","journal-title":"Lond Wellcome Trust UK Gov"},{"issue":"5","key":"pone.0242195.ref005","doi-asserted-by":"crossref","first-page":"525","DOI":"10.1016\/j.mib.2005.08.016","article-title":"\u03b2-Lactam antibiotic resistance: a current structural perspective","volume":"8","author":"MS Wilke","year":"2005","journal-title":"Curr Opin Microbiol"},{"issue":"8","key":"pone.0242195.ref006","doi-asserted-by":"crossref","first-page":"a025247","DOI":"10.1101\/cshperspect.a025247","article-title":"\u03b2-Lactams and \u03b2-Lactamase Inhibitors: An Overview.","volume":"6","author":"K Bush","year":"2016","journal-title":"Cold Spring Harb Perspect Med."},{"issue":"1","key":"pone.0242195.ref007","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.jpba.2007.06.002","article-title":"Analysis of cephalosporin antibiotics","volume":"45","author":"SR El-Shaboury","year":"2007","journal-title":"J Pharm Biomed Anal"},{"issue":"12","key":"pone.0242195.ref008","doi-asserted-by":"crossref","first-page":"1899","DOI":"10.1002\/jps.2600641202","article-title":"Pharmacokinetics and clinical use of cephalosporin antibiotics","volume":"64","author":"CH Nightingale","year":"1975","journal-title":"J Pharm Sci"},{"key":"pone.0242195.ref009","unstructured":"Peechakara BV, Basit H, Gupta M. Ampicillin. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2020 [cited 2020 Apr 30]. Available from: http:\/\/www.ncbi.nlm.nih.gov\/books\/NBK519569\/."},{"key":"pone.0242195.ref010","unstructured":"U.S. Food and Drug Administration. Roche rocephin ceftriaxone sodium for injection [Internet]. [cited 2020 Apr 30]. Available from: https:\/\/www.accessdata.fda.gov\/drugsatfda_docs\/label\/2009\/0550585s063lbl.pdf."},{"key":"pone.0242195.ref011","unstructured":"Medicine C for V. Extralabel Use and Antimicrobials. FDA [Internet]. 2019 Jul 30 [cited 2019 Aug 18]; Available from: http:\/\/www.fda.gov\/animal-veterinary\/antimicrobial-resistance\/extralabel-use-and-antimicrobials."},{"issue":"9","key":"pone.0242195.ref012","doi-asserted-by":"crossref","first-page":"517","DOI":"10.1016\/j.tree.2006.06.013","article-title":"Assembly of the human intestinal microbiota","volume":"21","author":"L Dethlefsen","year":"2006","journal-title":"Trends Ecol Evol"},{"issue":"18","key":"pone.0242195.ref013","doi-asserted-by":"crossref","first-page":"10452","DOI":"10.1073\/pnas.1734063100","article-title":"Honor thy symbionts","volume":"100","author":"J Xu","year":"2003","journal-title":"Proc Natl Acad Sci"},{"issue":"7","key":"pone.0242195.ref014","doi-asserted-by":"crossref","first-page":"e0220068","DOI":"10.1371\/journal.pone.0220068","article-title":"Effects of two-dose ceftiofur treatment for metritis on the temporal dynamics of antimicrobial resistance among fecal Escherichia coli in Holstein-Friesian dairy cows.","volume":"14","author":"EA Taylor","year":"2019","journal-title":"PloS One."},{"key":"pone.0242195.ref015","unstructured":"World Health Organization. Integrated surveillance of antimicrobial resistance in foodborne bacteria: application of a one health approach: guidance from the WHO Advisory Group on Integrated Surveillanec of Antimicrobial Resistance (AGISAR). 2017."},{"key":"pone.0242195.ref016","unstructured":"Centers for Disease Control and Prevention. Tracking CRE in the United States [Internet]. [cited 2020 Mar 29]. Available from: https:\/\/www.cdc.gov\/hai\/organisms\/cre\/trackingcre.html."},{"issue":"3\u20134","key":"pone.0242195.ref017","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1016\/j.vetmic.2005.12.004","article-title":"Klebsiella to Salmonella gene transfer within rumen protozoa: implications for antibiotic resistance and rumen defaunation","volume":"114","author":"ZP McCuddin","year":"2006","journal-title":"Vet Microbiol"},{"key":"pone.0242195.ref018","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1128\/CMR.8.4.557","article-title":"\u2424-Lactamases in Laboratory and Clinical Resistance.","volume":"8","author":"DM Livermore","year":"1995","journal-title":"CLIN MICROBIOL REV"},{"issue":"3713","key":"pone.0242195.ref019","doi-asserted-by":"crossref","first-page":"837","DOI":"10.1038\/146837a0","article-title":"An enzyme from bacteria able to destroy penicillin","volume":"146","author":"EP Abraham","year":"1940","journal-title":"Nature"},{"issue":"6","key":"pone.0242195.ref020","doi-asserted-by":"crossref","first-page":"1050","DOI":"10.1093\/jac\/dki130","article-title":"Revised Ambler classification of \u03b2-lactamases","volume":"55","author":"BG Hall","year":"2005","journal-title":"J Antimicrob Chemother"},{"issue":"1036","key":"pone.0242195.ref021","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1098\/rstb.1980.0049","article-title":"The structure of \u03b2-lactamases","volume":"289","author":"RP Ambler","year":"1980","journal-title":"Philos Trans R Soc Lond B Biol Sci"},{"key":"pone.0242195.ref022","first-page":"23","volume":"39","author":"K Bush","year":"1995","journal-title":"A Functional Classification Scheme for \u2424-Lactamases and Its Correlation with Molecular Structure"},{"issue":"3","key":"pone.0242195.ref023","doi-asserted-by":"crossref","first-page":"969","DOI":"10.1128\/AAC.01009-09","article-title":"Updated Functional Classification of -Lactamases","volume":"54","author":"K Bush","year":"2010","journal-title":"Antimicrob Agents Chemother"},{"key":"pone.0242195.ref024","volume-title":"The chemistry of \u03b2-lactams.","author":"MI Page","year":"2012"},{"issue":"5","key":"pone.0242195.ref025","doi-asserted-by":"crossref","first-page":"824","DOI":"10.1093\/clind\/15.5.824","article-title":"\u03b2-Lactam resistance in gram-negative bacteria: global trends and clinical impact","volume":"15","author":"CC Sanders","year":"1992","journal-title":"Clin Infect Dis"},{"issue":"1","key":"pone.0242195.ref026","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1128\/CMR.00036-08","article-title":"AmpC -Lactamases.","volume":"22","author":"GA Jacoby","year":"2009","journal-title":"Clin Microbiol Rev"},{"issue":"4","key":"pone.0242195.ref027","doi-asserted-by":"crossref","first-page":"228","DOI":"10.1016\/S1473-3099(09)70054-4","article-title":"The real threat of Klebsiella pneumoniae carbapenemase-producing bacteria","volume":"9","author":"P Nordmann","year":"2009","journal-title":"Lancet Infect Dis"},{"issue":"1","key":"pone.0242195.ref028","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1128\/AAC.48.1.15-22.2004","article-title":"Emergence of oxacillinase-mediated resistance to imipenem in Klebsiella pneumoniae","volume":"48","author":"L Poirel","year":"2004","journal-title":"Antimicrob Agents Chemother"},{"issue":"3","key":"pone.0242195.ref029","doi-asserted-by":"crossref","first-page":"1274","DOI":"10.1128\/AAC.01497-10","article-title":"Early dissemination of NDM-1-and OXA-181-producing Enterobacteriaceae in Indian hospitals: report from the SENTRY Antimicrobial Surveillance Program, 2006\u20132007","volume":"55","author":"M Castanheira","year":"2011","journal-title":"Antimicrob Agents Chemother"},{"key":"pone.0242195.ref030","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1146\/annurev-micro-090110-102911","article-title":"Epidemiological expansion, structural studies, and clinical challenges of new \u03b2-lactamases from gram-negative bacteria","volume":"65","author":"K Bush","year":"2011","journal-title":"Annu Rev Microbiol"},{"key":"pone.0242195.ref031","doi-asserted-by":"crossref","first-page":"48","DOI":"10.3389\/fmicb.2013.00048","article-title":"\u201cStormy waters ahead\u201d: global emergence of carbapenemases.","volume":"4","author":"G Patel","year":"2013","journal-title":"Front Microbiol"},{"issue":"Supplement_3","key":"pone.0242195.ref032","doi-asserted-by":"crossref","first-page":"S93","DOI":"10.1086\/340246","article-title":"Antimicrobial use and resistance in animals","volume":"34","author":"SA McEwen","year":"2002","journal-title":"Clin Infect Dis"},{"issue":"7404","key":"pone.0242195.ref033","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1038\/486465a","article-title":"Get pigs off antibiotics: Frank Aarestrup explains how he helped Denmark to cut the use of antibiotics in its livestock by 60%, and calls on the rest of the world to follow suit","volume":"486","author":"F Aarestrup","year":"2012","journal-title":"Nature"},{"issue":"1","key":"pone.0242195.ref034","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1086\/504921","article-title":"Similarity between human and chicken Escherichia coli isolates in relation to ciprofloxacin resistance status","volume":"194","author":"JR Johnson","year":"2006","journal-title":"J Infect Dis"},{"issue":"14","key":"pone.0242195.ref035","doi-asserted-by":"crossref","first-page":"2058","DOI":"10.1001\/jama.1985.03350380074024","article-title":"An outbreak of multiple-drug-resistant Salmonella enteritis from raw milk","volume":"253","author":"CO Tacket","year":"1985","journal-title":"Jama"},{"issue":"1","key":"pone.0242195.ref036","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1016\/j.ijfoodmicro.2009.11.008","article-title":"Farm-to-fork characterization of Escherichia coli associated with feedlot cattle with a known history of antimicrobial use","volume":"137","author":"TW Alexander","year":"2010","journal-title":"Int J Food Microbiol"},{"issue":"16","key":"pone.0242195.ref037","doi-asserted-by":"crossref","first-page":"1161","DOI":"10.1056\/NEJMoa010692","article-title":"Transient intestinal carriage after ingestion of antibiotic-resistant Enterococcus faecium from chicken and pork","volume":"345","author":"TL S\u00f8rensen","year":"2001","journal-title":"N Engl J Med"},{"issue":"12","key":"pone.0242195.ref038","doi-asserted-by":"crossref","first-page":"1738","DOI":"10.1289\/ehp.10191","article-title":"Elevated risk of carrying gentamicin-resistant Escherichia coli among US poultry workers","volume":"115","author":"LB Price","year":"2007","journal-title":"Environ Health Perspect"},{"issue":"5546","key":"pone.0242195.ref039","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1038\/260040a0","article-title":"Spread of antibiotic-resistant plasmids from chicken to chicken and from chicken to man","volume":"260","author":"SB Levy","year":"1976","journal-title":"Nature"},{"key":"pone.0242195.ref040","unstructured":"OIE. OIE list of antimicrobials of veterinary importance. 2007 May;9."},{"issue":"7","key":"pone.0242195.ref041","doi-asserted-by":"crossref","first-page":"1793","DOI":"10.1093\/jac\/dks108","article-title":"Escherichia coli producing VIM-1 carbapenemase isolated on a pig farm","volume":"67","author":"J Fischer","year":"2012","journal-title":"J Antimicrob Chemother"},{"issue":"2","key":"pone.0242195.ref042","doi-asserted-by":"crossref","first-page":"478","DOI":"10.1093\/jac\/dks393","article-title":"Salmonella enterica subsp. enterica producing VIM-1 carbapenemase isolated from livestock farms","volume":"68","author":"J Fischer","year":"2012","journal-title":"J Antimicrob Chemother"},{"key":"pone.0242195.ref043","unstructured":"Fischer J, Schmoger S, Baumann B, Laube H, von Salviati C, Friese A, et al. Carbapenemases are present in enterobacteria from non-domestic animals\u2026 more frequently than we thought. In: Twenty-third European Congress of Clinical Microbiology and Infectious Diseases Berlin, Germany. 2013."},{"issue":"5","key":"pone.0242195.ref044","doi-asserted-by":"crossref","first-page":"e37152","DOI":"10.1371\/journal.pone.0037152","article-title":"Identification of New Delhi metallo-\u03b2-lactamase 1 in Acinetobacter lwoffii of food animal origin.","volume":"7","author":"Y Wang","year":"2012","journal-title":"PloS One."},{"issue":"7","key":"pone.0242195.ref045","doi-asserted-by":"crossref","first-page":"1681","DOI":"10.1093\/jac\/dkt066","article-title":"Complete sequence of the bla NDM-1-carrying plasmid pNDM-AB from Acinetobacter baumannii of food animal origin","volume":"68","author":"W-J Zhang","year":"2013","journal-title":"J Antimicrob Chemother"},{"issue":"3","key":"pone.0242195.ref046","doi-asserted-by":"crossref","first-page":"950","DOI":"10.1093\/jac\/dku469","article-title":"Emergence of carbapenemase-producing Pseudomonas aeruginosa and Acinetobacter baumannii in livestock animals in Lebanon","volume":"70","author":"C Al Bayssari","year":"2014","journal-title":"J Antimicrob Chemother"},{"issue":"1","key":"pone.0242195.ref047","doi-asserted-by":"crossref","first-page":"e0147363","DOI":"10.1371\/journal.pone.0147363","article-title":"Carbapenem-Resistant Bacteria Recovered from Faeces of Dairy Cattle in the High Plains Region of the USA","volume":"11","author":"HE Webb","year":"2016","journal-title":"PLOS ONE"},{"key":"pone.0242195.ref048","article-title":"Carbapenemase-producing Enterobacteriaceae recovered from the environment of a swine farrow-to-finish operation in the United States","author":"DF Mollenkopf","year":"2016","journal-title":"Antimicrob Agents Chemother"},{"issue":"6","key":"pone.0242195.ref049","doi-asserted-by":"crossref","first-page":"372","DOI":"10.1089\/fpd.2017.2355","article-title":"Maintenance of Carbapenemase-Producing Enterobacteriaceae in a Farrow-to-Finish Swine Production System.","volume":"15","author":"DF Mollenkopf","year":"2018","journal-title":"Foodborne Pathog Dis."},{"issue":"3","key":"pone.0242195.ref050","doi-asserted-by":"crossref","first-page":"523","DOI":"10.3201\/eid1803.111330","article-title":"Carbapenemase-producing Acinetobacter spp. in cattle, France","volume":"18","author":"L Poirel","year":"2012","journal-title":"Emerg Infect Dis"},{"issue":"2","key":"pone.0242195.ref051","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":"N Woodford","year":"2014","journal-title":"J Antimicrob Chemother"},{"key":"pone.0242195.ref052","unstructured":"CDC-FDA Antimicrobial Resistance Isolate Bank. Atlanta (GA): CDC. 2019. https:\/\/wwwn.cdc.gov\/ARIsolateBank\/. Enterobacteriaceae Carbapenem Breakpoint Panel, Gram Negative Carbapenemase Detection (Active) Panel, Gram Negative Carbapenemase Detection Panel, Enterobacteriaceae Carbapenemase DiversityPanel, Ceftazidime\/avibactam Panel, Ceftazidime\/avibactam (Active) Panel, Cefepime\/ zidebactam (Active) Panel, Meropenem\/vaborbactam Verification (Active) Panel. [Internet]. [cited 2019 Dec 10]. Available from: https:\/\/wwwn.cdc.gov\/ARIsolateBank\/"},{"issue":"10","key":"pone.0242195.ref053","doi-asserted-by":"crossref","first-page":"504","DOI":"10.3390\/genes9100504","article-title":"Distribution of the pco Gene Cluster and Associated Genetic Determinants among Swine Escherichia coli from a Controlled Feeding Trial","volume":"9","author":"G Chalmers","year":"2018","journal-title":"Genes"},{"key":"pone.0242195.ref054","unstructured":"National Antimicrobial Resistance Monitoring System. Interagency Laboratory Manual Third Edition [Internet]. U.S Food and Drug Administration; 2016. Available from: https:\/\/www.fda.gov\/media\/101423\/download."},{"key":"pone.0242195.ref055","unstructured":"Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing. 27th ed. CLSI supplement M100. Wayne, PA: Clinical and Laboratory Standards Institute; 2017 [Internet]. 27th ed. 2017. Available from: https:\/\/clsi.org\/media\/1469\/m100s27_sample.pdf."},{"key":"pone.0242195.ref056","article-title":"Using the Velvet de novo assembler for short-read sequencing technologies.","author":"DR Zerbino","year":"2010","journal-title":"Curr Protoc Bioinforma Ed Board Andreas Baxevanis Al."},{"issue":"5","key":"pone.0242195.ref057","doi-asserted-by":"crossref","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":"A Bankevich","year":"2012","journal-title":"J Comput Biol"},{"issue":"4","key":"pone.0242195.ref058","doi-asserted-by":"crossref","first-page":"771","DOI":"10.1093\/jac\/dks496","article-title":"Genotyping using whole-genome sequencing is a realistic alternative to surveillance based on phenotypic antimicrobial susceptibility testing","volume":"68","author":"E Zankari","year":"2013","journal-title":"J Antimicrob Chemother"},{"issue":"31","key":"pone.0242195.ref059","doi-asserted-by":"crossref","DOI":"10.2807\/1560-7917.ES.2017.22.31.30589","article-title":"Novel plasmid-mediated colistin resistance mcr-4 gene in Salmonella and Escherichia coli, Italy 2013, Spain and Belgium, 2015 to 2016.","volume":"22","author":"A Carattoli","year":"2017","journal-title":"Eurosurveillance"},{"key":"pone.0242195.ref060","unstructured":"National Center for Biotechnology Information (NCBI). The Sequence Read Archive [Internet]. [cited 2020 May 12]. Available from: https:\/\/www.ncbi.nlm.nih.gov\/sra."},{"issue":"11","key":"pone.0242195.ref061","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1186\/s13073-014-0090-6","article-title":"SRST2: rapid genomic surveillance for public health and hospital microbiology labs","volume":"6","author":"M Inouye","year":"2014","journal-title":"Genome Med"},{"issue":"4","key":"pone.0242195.ref062","doi-asserted-by":"crossref","first-page":"1355","DOI":"10.1128\/JCM.06094-11","article-title":"Multilocus sequence typing of total-genome-sequenced bacteria","volume":"50","author":"MV Larsen","year":"2012","journal-title":"J Clin Microbiol"},{"key":"pone.0242195.ref063","unstructured":"Seemann T. ABRicate [Internet]. [cited 2020 May 12]. Available from: https:\/\/github.com\/tseemann\/abricate."},{"issue":"7","key":"pone.0242195.ref064","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":"A Carattoli","year":"2014","journal-title":"Antimicrob Agents Chemother"},{"issue":"2","key":"pone.0242195.ref065","doi-asserted-by":"crossref","first-page":"673","DOI":"10.1128\/AEM.68.2.673-690.2002","article-title":"Culture-independent analysis of gut bacteria: the pig gastrointestinal tract microbiota revisited","volume":"68","author":"TD Leser","year":"2002","journal-title":"Appl Environ Microbiol"},{"issue":"1","key":"pone.0242195.ref066","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1146\/annurev.nu.07.070187.002045","article-title":"The pig as a model for human nutrition","volume":"7","author":"ER Miller","year":"1987","journal-title":"Annu Rev Nutr"},{"key":"pone.0242195.ref067","article-title":"Limit distributions for sums of independent.","volume":"105","author":"BV Gnedenko","year":"1954","journal-title":"Am J Math."},{"key":"pone.0242195.ref068","author":"DF Morrison","year":"1976","journal-title":"Multivariate statistical methods: McGraw-Hill series in probability and statistics"},{"issue":"6","key":"pone.0242195.ref069","doi-asserted-by":"crossref","first-page":"e0178691","DOI":"10.1371\/journal.pone.0178691","article-title":"The use of Gompertz models in growth analyses, and new Gompertz-model approach: An addition to the Unified-Richards family","volume":"12","author":"KMC Tj\u00f8rve","year":"2017","journal-title":"PLOS ONE."},{"issue":"5","key":"pone.0242195.ref070","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1016\/j.fm.2004.01.007","article-title":"A new logistic model for Escherichia coli growth at constant and dynamic temperatures.","volume":"21","author":"H Fujikawa","year":"2004","journal-title":"Food Microbiol."},{"issue":"3","key":"pone.0242195.ref071","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1016\/j.ijfoodmicro.2003.07.002","article-title":"Estimating the bacterial lag time: which model, which precision?","volume":"91","author":"F Baty","year":"2004","journal-title":"Int J Food Microbiol"},{"issue":"1","key":"pone.0242195.ref072","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1111\/j.1574-6968.1988.tb02909.x","article-title":"Diauxic growth of Clostridium thermosaccharolyticum on glucose and xylose","volume":"50","author":"J Aduse-Opoku","year":"1988","journal-title":"FEMS Microbiol Lett"},{"issue":"2","key":"pone.0242195.ref073","doi-asserted-by":"crossref","first-page":"866","DOI":"10.1128\/JB.164.2.866-871.1985","article-title":"Diauxic growth in Azotobacter vinelandii","volume":"164","author":"SE George","year":"1985","journal-title":"J Bacteriol"},{"issue":"5","key":"pone.0242195.ref074","doi-asserted-by":"crossref","first-page":"831","DOI":"10.1128\/AEM.28.5.831-835.1974","article-title":"Diauxic growth of Propionibacterium shermanii.","volume":"28","author":"IH Lee","year":"1974","journal-title":"Appl Env Microbiol"},{"key":"pone.0242195.ref075","doi-asserted-by":"crossref","DOI":"10.1007\/978-1-60327-279-7","volume-title":"Antibiotic resistance protocols.","author":"SH Gillespie","year":"2010"},{"issue":"5","key":"pone.0242195.ref076","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1016\/S1369-5274(99)00005-3","article-title":"The biological cost of antibiotic resistance","volume":"2","author":"DI Andersson","year":"1999","journal-title":"Curr Opin Microbiol"},{"issue":"1","key":"pone.0242195.ref077","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1128\/AAC.38.1.122","article-title":"In vitro selective antibiotic concentrations of beta-lactams for penicillin-resistant Streptococcus pneumoniae populations","volume":"38","author":"MC Negri","year":"1994","journal-title":"Antimicrob Agents Chemother"},{"issue":"856","key":"pone.0242195.ref078","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1086\/281957","article-title":"The meanings of competition","volume":"91","author":"LC Birch","year":"1957","journal-title":"Am Nat"},{"issue":"8","key":"pone.0242195.ref079","doi-asserted-by":"crossref","first-page":"3073","DOI":"10.1073\/pnas.71.8.3073","article-title":"Interference competition and niche theory","volume":"71","author":"TJ Case","year":"1974","journal-title":"Proc Natl Acad Sci"},{"issue":"2","key":"pone.0242195.ref080","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1099\/00222615-35-2-111","article-title":"Selected faecal bacteria and nutrients essential for antagonism of Salmonella typhimurium in anaerobic continuous flow cultures","volume":"35","author":"T Ushijima","year":"1991","journal-title":"J Med Microbiol"},{"issue":"4","key":"pone.0242195.ref081","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1038\/nrmicro2977","article-title":"Competition sensing: the social side of bacterial stress responses","volume":"11","author":"DM Cornforth","year":"2013","journal-title":"Nat Rev Microbiol"},{"issue":"3","key":"pone.0242195.ref082","doi-asserted-by":"crossref","first-page":"985","DOI":"10.1093\/genetics\/154.3.985","article-title":"Compensatory mutations, antibiotic resistance and the population genetics of adaptive evolution in bacteria","volume":"154","author":"BR Levin","year":"2000","journal-title":"Genetics"},{"issue":"1","key":"pone.0242195.ref083","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1093\/jac\/dkh505","article-title":"Reduction of the fitness burden of quinolone resistance in Pseudomonas aeruginosa","volume":"55","author":"E Kugelberg","year":"2005","journal-title":"J Antimicrob Chemother"},{"issue":"3","key":"pone.0242195.ref084","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1139\/w03-111","article-title":"Cefotaximases (CTX-M-ases), an expanding family of extended-spectrum \u03b2-lactamases.","volume":"50","author":"J Walther-Rasmussen","year":"2004","journal-title":"Can J Microbiol"},{"issue":"6\u20137","key":"pone.0242195.ref085","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1016\/j.ijmm.2013.02.009","article-title":"Intrinsic antibiotic resistance: mechanisms, origins, challenges and solutions","volume":"303","author":"G Cox","year":"2013","journal-title":"Int J Med Microbiol"},{"issue":"2","key":"pone.0242195.ref086","doi-asserted-by":"crossref","first-page":"224","DOI":"10.1093\/cid\/cis387","article-title":"Features of Infections Due to Klebsiella pneumoniae Carbapenemase\u2013Producing Escherichia coli: Emergence of Sequence Type 131","volume":"55","author":"YA Kim","year":"2012","journal-title":"Clin Infect Dis"},{"issue":"10","key":"pone.0242195.ref087","doi-asserted-by":"crossref","first-page":"4933","DOI":"10.1128\/AAC.00719-11","article-title":"When carbapenem-hydrolyzing \u03b2-lactamase KPC meets Escherichia coli ST131 in France","volume":"55","author":"T Naas","year":"2011","journal-title":"Antimicrob Agents Chemother"},{"issue":"1","key":"pone.0242195.ref088","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1111\/nyas.12537","article-title":"Carbapenem-resistant Enterobacteriaceae: biology, epidemiology, and management","volume":"1323","author":"E Temkin","year":"2014","journal-title":"Ann N Y Acad Sci"},{"issue":"6","key":"pone.0242195.ref089","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0218650","article-title":"Carbapenemase-producing Enterobacteriaceae and Aeromonas spp. present in wastewater treatment plant effluent and nearby surface waters in the US.","volume":"14","author":"DA Mathys","year":"2019","journal-title":"PloS One."}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0242195","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,11,28]],"date-time":"2022-11-28T09:02:59Z","timestamp":1669626179000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0242195"}},"subtitle":[],"editor":[{"given":"Iddya","family":"Karunasagar","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2020,11,16]]},"references-count":89,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2020,11,16]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0242195","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,11,16]]}}}