{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,20]],"date-time":"2026-07-20T18:09:09Z","timestamp":1784570949353,"version":"3.55.0"},"reference-count":57,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2021,4,16]],"date-time":"2021-04-16T00:00:00Z","timestamp":1618531200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100010712","name":"Agricultural and Horticultural Development Board","doi-asserted-by":"publisher","award":["61110063"],"award-info":[{"award-number":["61110063"]}],"id":[{"id":"10.13039\/100010712","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Antibiotics"],"abstract":"<jats:p>Little data exist on the levels of antimicrobial resistance from bacteria isolated from British sheep and beef cattle. The aim of this study was to investigate antimicrobial resistance patterns on sheep and beef farms in England and Wales using multiple interpretation methods. Fecal samples (n = 350) from sheep and beef cattle were collected from 35 farms. Disk diffusion antimicrobial susceptibility testing against ten antimicrobials was carried out for 1115 (699 sheep, 416 beef) \u03b2-glucuronidase-positive Escherichia coli isolates. Susceptibility was interpreted using clinical breakpoints, which determine clinically resistant bacteria, and epidemiological and livestock-specific cut-off values, which determine microbiological-resistant bacteria (non-wild type). Using livestock-specific cut-off values, a high frequency of wild type for all ten antimicrobials was observed in isolates from sheep (90%) and beef cattle (85%). Cluster analysis was performed to identify patterns in antimicrobial resistance. Interpretation of susceptibility using livestock-specific cut-off values showed a cluster of isolates that were non-wild type to cefotaxime and amoxicillin\/clavulanic acid, whereas clinical breakpoints did not. A multilevel logistic regression model determined that tetracycline use on the farm and soil copper concentration were significantly associated with tetracycline non-wild type isolates. The results suggest that using human clinical breakpoints could lead to both the under-reporting and over-reporting of antimicrobial resistance in sheep and beef cattle.<\/jats:p>","DOI":"10.3390\/antibiotics10040453","type":"journal-article","created":{"date-parts":[[2021,4,16]],"date-time":"2021-04-16T10:20:11Z","timestamp":1618568411000},"page":"453","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Antimicrobial Resistance Patterns of Escherichia coli Isolated from Sheep and Beef Farms in England and Wales: A Comparison of Disk Diffusion Interpretation Methods"],"prefix":"10.3390","volume":"10","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-1344-7808","authenticated-orcid":false,"given":"Charlotte","family":"Doidge","sequence":"first","affiliation":[{"name":"School of Veterinary Medicine and Science, University of Nottingham, Sutton Bonington LE12 5RD, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Helen","family":"West","sequence":"additional","affiliation":[{"name":"School of Biosciences, University of Nottingham, Sutton Bonington LE12 5RD, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3332-7064","authenticated-orcid":false,"given":"Jasmeet","family":"Kaler","sequence":"additional","affiliation":[{"name":"School of Veterinary Medicine and Science, University of Nottingham, Sutton Bonington LE12 5RD, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,4,16]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"718","DOI":"10.1128\/CMR.00002-11","article-title":"Food Animals and Antimicrobials: Impacts on Human Health","volume":"24","author":"Marshall","year":"2011","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1136\/vr.104501","article-title":"Quantitative analysis of antibiotic usage in British sheep flocks","volume":"181","author":"Davies","year":"2017","journal-title":"Vet. Rec."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"e119","DOI":"10.1136\/vr.105878","article-title":"Antimicrobial use practices and opinions of beef farmers in England and Wales","volume":"187","author":"Doidge","year":"2020","journal-title":"Vet. Rec."},{"key":"ref_4","unstructured":"DEFRA (2020, November 04). Farming Statistics Final Land Use, Livestock Populations and Agricultural Workforce at 1 June 2018\u2014England, Available online: https:\/\/assets.publishing.service.gov.uk\/government\/uploads\/system\/uploads\/attachment_data\/file\/869064\/structure-jun2018final-eng-28feb20.pdf."},{"key":"ref_5","unstructured":"Welsh Government (2020, December 12). Farming Facts and Figure, Wales, Available online: https:\/\/gov.wales\/sites\/default\/files\/statistics-and-research\/2019-07\/farming-facts-and-figures-2019-492.pdf."},{"key":"ref_6","unstructured":"VMD (2020, November 19). UK Veterinary Antibiotic Resistance and Sales Surveillance Report, Available online: https:\/\/assets.publishing.service.gov.uk\/government\/uploads\/system\/uploads\/attachment_data\/file\/936107\/UK-VARSS_2019_Report__2020_.pdf."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"105174","DOI":"10.1016\/j.prevetmed.2020.105174","article-title":"Antimicrobial & antiparasitic use and resistance in British sheep and cattle: A systematic review","volume":"185","author":"Hennessey","year":"2020","journal-title":"Prev. Vet. Med."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1093\/jac\/dkl491","article-title":"Antibiotic resistance and molecular epidemiology of Escherichia coli O26, O103 and O145 shed by two cohorts of Scottish beef cattle","volume":"59","author":"Vali","year":"2007","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1111\/j.1574-6968.2007.00991.x","article-title":"A high prevalence of antimicrobial resistant Escherichia coli isolated from pigs and a low prevalence of antimicrobial resistant E. coli from cattle and sheep in Great Britain at slaughter","volume":"278","author":"Enne","year":"2008","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Silva, N., Phythian, C.J., Currie, C., Tassi, R., Ballingall, K.T., Magro, G., McNeilly, T.N., and Zadoks, R.N. (2020). Antimicrobial resistance in ovine bacteria: A sheep in wolf\u2019s clothing?. PLoS ONE, 15.","DOI":"10.1371\/journal.pone.0238708"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"656","DOI":"10.1136\/vr.100037","article-title":"Investigation of the presence of ESBL-producing Escherichia coli in the North Wales and West Midlands areas of the UK in 2007 to 2008 using scanning surveillance","volume":"169","author":"Snow","year":"2011","journal-title":"Vet. Rec."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1081","DOI":"10.1111\/jam.14211","article-title":"Detection of extended-spectrum \u03b2-lactam, AmpC and carbapenem resistance in Enterobacteriaceae in beef cattle in Great Britain in 2015","volume":"126","author":"Velasova","year":"2019","journal-title":"J. Appl. Microbiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1016\/j.prevetmed.2008.10.002","article-title":"Associations between reported on-farm antimicrobial use practices and observed antimicrobial resistance in generic fecal Escherichia coli isolated from Alberta finishing swine farms","volume":"88","author":"Varga","year":"2009","journal-title":"Prev. Vet. Med."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1893","DOI":"10.1017\/S0950268813002665","article-title":"Antimicrobial resistance in commensal Escherichia coli in veal calves is associated with antimicrobial drug use","volume":"142","author":"Bosman","year":"2014","journal-title":"Epidemiol. Infect."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1111\/zph.12225","article-title":"Antimicrobial Resistance of Faecal Escherichia coli Isolates from Pig Farms with Different Durations of In-feed Antimicrobial Use","volume":"63","author":"Gibbons","year":"2016","journal-title":"Zoonoses Public Health"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1338","DOI":"10.2460\/javma.236.12.1338","article-title":"Geographic, farm, and animal factors associated with multiple antimicrobial resistance in fecal Escherichia coli isolates from cattle in the western United States","volume":"236","author":"Berge","year":"2010","journal-title":"J. Am. Vet. Med. Assoc."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"srep12439","DOI":"10.1038\/srep12439","article-title":"Prevalence and patterns of antimicrobial resistance among Escherichia coli isolated from Zambian dairy cattle across different production systems","volume":"5","author":"Mainda","year":"2015","journal-title":"Sci. Rep."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Mir, R.A., Weppelmann, T.A., Johnson, J.A., Archer, D., Morris, J.G., and Jeong, K.C. (2016). Identification and Characterization of Cefotaxime Resistant Bacteria in Beef Cattle. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0163279"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"500","DOI":"10.3389\/fmicb.2018.00500","article-title":"Colonization Dynamics of Cefotaxime Resistant Bacteria in Beef Cattle Raised Without Cephalosporin Antibiotics","volume":"9","author":"Mir","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"176","DOI":"10.3389\/fmicb.2019.00176","article-title":"High Prevalence of Cefotaxime Resistant Bacteria in Grazing Beef Cattle: A Cross Sectional Study","volume":"10","author":"Markland","year":"2019","journal-title":"Front. Microbiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1080\/1040841X.2020.1715339","article-title":"Prevalence of extended-spectrum \u03b2-lactamases in the local farm environment and livestock: Challenges to mitigate antimicrobial resistance","volume":"46","author":"Lee","year":"2020","journal-title":"Crit. Rev. Microbiol."},{"key":"ref_22","unstructured":"EUCAST (2020, November 24). EUCAST Disk Diffusion Method for Antimicrobial Susceptibility Testing. Available online: https:\/\/www.eucast.org\/fileadmin\/src\/media\/PDFs\/EUCAST_files\/Disk_test_documents\/2020_manuals\/Manual_v_8.0_EUCAST_Disk_Test_2020.pdf."},{"key":"ref_23","unstructured":"CLSI (2020). Performance Standards for Antimicrobial Susceptibility Testing, Clinical and Laboratory Standards Institute. [30th ed.]."},{"key":"ref_24","unstructured":"EUCAST (2018). Breakpoint Tables for Interpretation of MICs and Zone Diameters, EUCAST. Available online: http:\/\/www.eucast.org."},{"key":"ref_25","unstructured":"EUCAST (2020, November 24). EUCAST Definitions of Clinical Breakpoints and Epidemiological Cutoff Values. Available online: https:\/\/www.eucast.org\/fileadmin\/src\/media\/PDFs\/EUCAST_files\/EUCAST_SOPs\/EUCAST_definitions_of_clinical_breakpoints_and_ECOFFs.pdf."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"78","DOI":"10.3109\/03009734.2014.901446","article-title":"Defining antibiotic resistance-towards international harmonization","volume":"119","author":"Kahlmeter","year":"2014","journal-title":"Upsala J. Med Sci."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"584","DOI":"10.1016\/j.resmic.2015.03.006","article-title":"Assessment of antibiotic resistance of Escherichia coli isolates and screening of Salmonella spp. in wild ungulates from Portugal","volume":"166","author":"Dias","year":"2015","journal-title":"Res. Microbiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1023","DOI":"10.1111\/apm.12624","article-title":"Normalized resistance interpretation, the NRI method","volume":"124","author":"Kronvall","year":"2016","journal-title":"APMIS"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"7644","DOI":"10.3168\/jds.2014-8521","article-title":"Effect of on-farm use of antimicrobial drugs on resistance in fecal Escherichia coli of preweaned dairy calves","volume":"97","author":"Pereira","year":"2014","journal-title":"J. Dairy Sci."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1153","DOI":"10.1007\/s10499-016-9977-0","article-title":"Epidemiological cut-off values for disc diffusion data generated by standard test protocols from Edwardsiella tarda and Vibrio harveyi","volume":"24","author":"Lim","year":"2016","journal-title":"Aquac. Int."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1016\/j.aquaculture.2011.11.011","article-title":"Use of normalised resistance analyses to set interpretive criteria for antibiotic disc diffusion data produce by Aeromonas spp.","volume":"326\u2013329","author":"Smith","year":"2012","journal-title":"Aquaculture"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1016\/j.vetmic.2007.01.015","article-title":"\u03b2-Lactam resistance and \u03b2-lactamases in bacteria of animal origin","volume":"121","author":"Li","year":"2007","journal-title":"Vet. Microbiol."},{"key":"ref_33","unstructured":"EUCAST (2020, November 24). Subcommittee for Detection of Resistance Mechanisms and Specific Resistances of Clinical and\/or Epidemiological Importance. EUCAST Guidelines for Detection of Resistance Mechanisms and Specific Resistances of Clinical and\/or Epidemiological Importance, Version 2.0. Available online: http:\/\/www.eucast.org\/fileadmin\/src\/media\/PDFs\/EUCAST_files\/Resistance_mechanisms\/EUCAST_detection_of_resistance_mechanisms_170711.pdf."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"2653","DOI":"10.1017\/S0950268814003963","article-title":"Cross-sectional survey of antibiotic resistance in Escherichia coli isolated from diseased farm livestock in England and Wales","volume":"143","author":"Cheney","year":"2015","journal-title":"Epidemiol. Infect."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"e01468-20","DOI":"10.1128\/AEM.01468-20","article-title":"Reduced Antibacterial Drug Resistance and blaCTX-M \u03b2-Lactamase Gene Carriage in Cattle-Associated Escherichia coli at Low Temperatures, at Sites Dominated by Older Animals, and on Pastureland: Implications for Surveillance","volume":"87","author":"Schubert","year":"2021","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"524","DOI":"10.3389\/fvets.2020.00524","article-title":"Farmers\u2019 Perceptions of Preventing Antibiotic Resistance on Sheep and Beef Farms: Risk, Responsibility, and Action","volume":"7","author":"Doidge","year":"2020","journal-title":"Front. Vet. Sci."},{"key":"ref_37","unstructured":"RUMA (2020, November 30). Targets Task Force Report. Available online: https:\/\/www.ruma.org.uk\/wp-content\/uploads\/2020\/11\/Targets-Task-Force-Report-2020-FINAL-181120-download.pdf."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"180682","DOI":"10.1155\/2010\/180682","article-title":"Role of antimicrobial selective pressure and secondary factors on antimicrobial resistance prevalence in Escherichia coli from food-producing animals in Japan","volume":"2010","author":"Harada","year":"2010","journal-title":"J. Biomed. Biotechnol."},{"key":"ref_39","unstructured":"EMA (2020, November 30). Categorisation of Antibiotics in the European Union. Available online: https:\/\/www.ema.europa.eu\/en\/documents\/report\/categorisation-antibiotics-european-union-answer-request-european-commission-updating-scientific_en.pdf."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Knapp, C.W., McCluskey, S.M., Singh, B.K., Campbell, C.D., Hudson, G., and Graham, D.W. (2011). Antibiotic Resistance Gene Abundances Correlate with Metal and Geochemical Conditions in Archived Scottish Soils. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0027300"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"2484","DOI":"10.1007\/s11356-016-7997-y","article-title":"Relationship between antibiotic resistance genes and metals in residential soil samples from Western Australia","volume":"24","author":"Knapp","year":"2017","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"3040","DOI":"10.1021\/acs.est.6b05342","article-title":"Comparison of Metals and Tetracycline as Selective Agents for Development of Tetracycline Resistant Bacterial Communities in Agricultural Soil","volume":"51","author":"Song","year":"2017","journal-title":"Environ. Sci. Technol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"116602","DOI":"10.1016\/j.envpol.2021.116602","article-title":"Towards a general model for predicting minimal metal concentrations co-selecting for antibiotic resistance plasmids","volume":"275","author":"Arya","year":"2021","journal-title":"Environ. Pollut."},{"key":"ref_44","first-page":"119","article-title":"Antimicrobial resistance in generic fecal Escherichia coli from 29 beef farms in Ontario","volume":"72","author":"Carson","year":"2008","journal-title":"Can. J. Vet. Res."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"3027","DOI":"10.1128\/AEM.00204-13","article-title":"Prevalence of Extended-Spectrum \u03b2-Lactamase-Producing Escherichia coli on Bavarian Dairy and Beef Cattle Farms","volume":"79","author":"Schmid","year":"2013","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_46","unstructured":"APHA (2021, February 02). Livestock Demographic Data Group: Cattle Population Report, Available online: http:\/\/apha.defra.gov.uk\/documents\/surveillance\/diseases\/lddg-pop-report-cattle-1118.pdf."},{"key":"ref_47","unstructured":"APHA (2021, February 02). Livestock Demographic Data Group: Sheep Population Report, Available online: http:\/\/apha.defra.gov.uk\/documents\/surveillance\/diseases\/lddg-pop-report-sheep-1118.pdf."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Benedict, K.M., Gow, S.P., Checkley, S., Booker, C.W., McAllister, T.A., and Morley, P.S. (2013). Methodological comparisons for antimicrobial resistance surveillance in feedlot cattle. BMC Vet. Res., 9.","DOI":"10.1186\/1746-6148-9-216"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1016\/j.prevetmed.2017.08.007","article-title":"Comparison of antimicrobial resistance in E. coli isolated from rectal and floor samples in pens with diarrhoeic nursery pigs in Denmark","volume":"147","author":"Rosager","year":"2017","journal-title":"Prev. Vet. Med."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/j.aquaculture.2018.02.020","article-title":"Influence of incubation temperature and time on the precision of MIC and disc diffusion antimicrobial susceptibility test data","volume":"490","author":"Smith","year":"2018","journal-title":"Aquaculture"},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Fleiss, J.L., Levin, B., and Paik, M.C. (2003). Statistical Methods for Rates and Proportions, John Wiley & Sons. [3rd ed.].","DOI":"10.1002\/0471445428"},{"key":"ref_52","unstructured":"Romesburg, C. (2004). Cluster Analysis for Researchers, Lulu Press."},{"key":"ref_53","unstructured":"Met Office (2020, November 24). Historic Station Data, Available online: https:\/\/www.metoffice.gov.uk\/research\/climate\/maps-and-data\/historic-station-data."},{"key":"ref_54","unstructured":"UK Soil Observatory (2020, December 05). Advanced Soil Geochemical Atlas of England and Wales. Available online: http:\/\/ukso.org\/static-maps\/advanced-soil-geochemical-atlas-of-england-and-wales.html."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1209","DOI":"10.3168\/jds.2011-4527","article-title":"Antimicrobial use on Canadian dairy farms","volume":"95","author":"Saini","year":"2012","journal-title":"J. Dairy Sci."},{"key":"ref_56","unstructured":"Charlton, C., Rabash, J., Browne, W., Healy, M., and Cameron, B. (2017). MLwiN, Centre for Multilevel Modelling, University of Bristol. 3.02."},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Leyland, A.H., and Groenewegen, P.P. (2020). Apportioning Variation in Multilevel Models. Multilevel Modelling for Public Health and Health Services Research, Springer.","DOI":"10.1007\/978-3-030-34801-4"}],"container-title":["Antibiotics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-6382\/10\/4\/453\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T05:48:55Z","timestamp":1760161735000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-6382\/10\/4\/453"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,4,16]]},"references-count":57,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2021,4]]}},"alternative-id":["antibiotics10040453"],"URL":"https:\/\/doi.org\/10.3390\/antibiotics10040453","relation":{},"ISSN":["2079-6382"],"issn-type":[{"value":"2079-6382","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,4,16]]}}}