{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,28]],"date-time":"2026-09-28T20:33:06Z","timestamp":1790627586909,"version":"4.1.0"},"reference-count":44,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2018,9,13]],"date-time":"2018-09-13T00:00:00Z","timestamp":1536796800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100005908","name":"Bundesministerium f\u00fcr Ern\u00e4hrung und Landwirtschaft","doi-asserted-by":"publisher","award":["2817701814"],"award-info":[{"award-number":["2817701814"]}],"id":[{"id":"10.13039\/501100005908","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJERPH"],"abstract":"<jats:p>Gaining knowledge about the spread of resistance against antibacterial agents is a primary challenge in livestock farming. The purpose of this study was to test the effect of double antibiotic treatment (at days 10\u201314 and days 26\u201330) with enrofloxacin or solely environmental exposition (identical times, directly into the litter) on resistance against antibacterial agents in commensal Escherichia coli in comparison with the control (without treatment), depending on different flooring. A total of 720 Big 6 turkeys participated in three trials. Four different flooring designs were examined: An entire floor pen covered with litter, a floor pen with heating, a partially slatted flooring including 50% littered area, and a fully slatted flooring with a sand bath. A total of 864 Escherichia coli isolates were obtained from cloacal swabs and poultry manure samples at days 2, 9, 15, 21, and 35. The broth microdilution method (MIC) was used to determine the resistance of isolates to enrofloxacin and ampicillin. A double antibiotic treatment with enrofloxacin reduced the proportion of susceptible Escherichia coli isolates significantly in all flooring designs. Simulation of water losses had no significant effect, nor did the flooring design. Ampicillin-resistant isolates were observed, despite not using ampicillin.<\/jats:p>","DOI":"10.3390\/ijerph15091993","type":"journal-article","created":{"date-parts":[[2018,9,13]],"date-time":"2018-09-13T11:46:04Z","timestamp":1536839164000},"page":"1993","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":19,"title":["Resistance of Escherichia coli in Turkeys after Therapeutic or Environmental Exposition with Enrofloxacin Depending on Flooring"],"prefix":"10.3390","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-2144-4930","authenticated-orcid":false,"given":"Bussarakam","family":"Chuppava","sequence":"first","affiliation":[{"name":"Institute for Animal Nutrition, University of Veterinary Medicine Hannover, Foundation, Bischofsholer Damm 15, D-30173 Hanover, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Birgit","family":"Keller","sequence":"additional","affiliation":[{"name":"Institute for Animal Nutrition, University of Veterinary Medicine Hannover, Foundation, Bischofsholer Damm 15, D-30173 Hanover, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amr Abd","family":"El-Wahab","sequence":"additional","affiliation":[{"name":"Department of Nutrition and Nutritional Deficiency Diseases, Faculty of Veterinary Medicine, Mansoura University, Mansoura 35516, Egypt"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7263-848X","authenticated-orcid":false,"given":"Jessica","family":"Mei\u00dfner","sequence":"additional","affiliation":[{"name":"Institute for Pharmacology, Toxicology, and Pharmacy, University of Veterinary Medicine Hannover, Foundation, B\u00fcnteweg 17, D-30559 Hannover, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Manfred","family":"Kietzmann","sequence":"additional","affiliation":[{"name":"Institute for Pharmacology, Toxicology, and Pharmacy, University of Veterinary Medicine Hannover, Foundation, B\u00fcnteweg 17, D-30559 Hannover, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christian","family":"Visscher","sequence":"additional","affiliation":[{"name":"Institute for Animal Nutrition, University of Veterinary Medicine Hannover, Foundation, Bischofsholer Damm 15, D-30173 Hanover, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2018,9,13]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"158","DOI":"10.1111\/j.1863-2378.2011.01451.x","article-title":"Emerging antimicrobial resistance in commensal Escherichia coli with public health relevance","volume":"59","author":"Kaesbohrer","year":"2012","journal-title":"Zoonoses Public Health"},{"key":"ref_2","unstructured":"Schroeter, A., and Kaesbohrer, A. (2010). German Antimicrobial Resistance Situation in the Food Chain\u2013DARlink, Bundesinstitut fur Risikobewertung (BfR)."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"ECDC, EFSA, and EMA (2017). Second joint report on the integrated analysis of the consumption of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from humans and food-producing animals\u2014joint interagency antimicrobial consumption and resistance analysis (JIACRA) report. EFSA J., 15, 4872.","DOI":"10.2903\/j.efsa.2017.4872"},{"key":"ref_4","unstructured":"WHO (2018, March 29). Antimicrobial Resistance: Global Report on Surveillance. Available online: http:\/\/apps.who.int\/iris\/bitstream\/10665\/112642\/1\/9789241564748_eng.pdf."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0065-2113(05)87001-4","article-title":"Antibiotic use in agriculture and its impact on the terrestrial environment","volume":"87","author":"Kumar","year":"2005","journal-title":"Adv. Agron."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"792","DOI":"10.1016\/j.etap.2014.09.011","article-title":"Determination of fluoroquinolones in chicken feces\u2014A new liquid\u2013liquid extraction method combined with LC\u2013MS\/MS","volume":"38","author":"Janusch","year":"2014","journal-title":"Environ. Toxicol. Pharmacol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"704","DOI":"10.1016\/j.chemosphere.2017.10.092","article-title":"Fluoroquinolones (FQs) in the environment: A review on their abundance, sorption and toxicity in soil","volume":"191","author":"Riaz","year":"2018","journal-title":"Chemosphere"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"E99","DOI":"10.1016\/S1473-3099(17)30485-1","article-title":"Surveillance for control of antimicrobial resistance","volume":"18","author":"Tacconelli","year":"2017","journal-title":"Lancet Infect. Dis."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1","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":"ref_10","first-page":"181","article-title":"Comparison of antimicrobial resistance in generic Escherichia coli and Salmonella spp. Cultured from identical fecal samples in finishing swine","volume":"72","author":"Varga","year":"2008","journal-title":"Can. J. Vet. Res."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"EFSA (2015). The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2013. EFSA J., 13, 4036.","DOI":"10.2903\/j.efsa.2015.4036"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"ECDC, EFSA, and EMA (2015). First joint report on the integrated analysis of the consumption of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from humans and food-producing animals. EFSA J., 13, 4006.","DOI":"10.2903\/j.efsa.2015.4006"},{"key":"ref_13","unstructured":"European Surveillance of Veterinary Antimicrobial Consumption (ESVAC) (2018, March 29). Sales of Veterinary Antimicrobial Agents in 30 European Countries in 2015. Available online: https:\/\/publications.europa.eu\/en\/publication-detail\/-\/publication\/7656bd79-d970-11e7-a506-01aa75ed71a1\/language-en."},{"key":"ref_14","unstructured":"GERMAP (2016). Report on the Consumption of Antimicrobials and the Spread of Antimicrobial Resistance in Human and Veterinary Medicine in Germany, Antiinfectives Intelligence."},{"key":"ref_15","unstructured":"Kreienbrock, L. (2013). Ergebnisse aus VetCAb, Antibiotikaresistenz in der Lebensmittelkette, Bundesinstitut f\u00fcr Risikobewertung (BfR)."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"282","DOI":"10.3389\/fmicb.2014.00282","article-title":"Antibiotics in Canadian poultry productions and anticipated alternatives","volume":"5","author":"Diarra","year":"2014","journal-title":"Front. Microbiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"180","DOI":"10.3382\/ps.2009-00198","article-title":"Veterinary pharmaceuticals and antibiotic resistance of Escherichia coli isolates in poultry litter from commercial farms and controlled feeding trials","volume":"89","author":"Furtula","year":"2010","journal-title":"Poult. Sci."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"550","DOI":"10.3389\/fmicb.2018.00550","article-title":"Prevalence and characterization of multi-drug-resistant gram-negative bacilli isolated from Lebanese poultry: A nationwide study","volume":"9","author":"Dandachi","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"827","DOI":"10.1093\/jac\/dkt443","article-title":"Correlation between veterinary antimicrobial use and antimicrobial resistance in food-producing animals: A report on seven countries","volume":"69","author":"Chantziaras","year":"2013","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_20","unstructured":"Werckenthin, C. (2016). Escherichia coli Strains from Northwestern Lower Saxony Obtained as Part of the Zoonosis Monitoring (General Administrative Regulation on Zoonoses in the Food Chain). GERMAP 2015\u2014Report on the Consumption of Antimicrobials and the Spread of Antimicrobial Resistance in Human and Veterinary Medicine in Germany, Antiinfectives Intelligence."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1016\/j.enconman.2011.08.017","article-title":"Characterisation, kinetics and modelling of gasification of poultry manure and litter: An overview","volume":"53","year":"2012","journal-title":"Energy Convers. Manag."},{"key":"ref_22","first-page":"147","article-title":"Influences of feeding and housing on foot pad health in hens and turkeys","volume":"39","author":"Kamphues","year":"2011","journal-title":"\u00dcbers. Tierern\u00e4hrg"},{"key":"ref_23","unstructured":"Bhushan, C., Khurana, A., Sinha, R., and Nagaraju, M. (2017). Antibiotic Resistance in Poultry Environment: Spread of Resistance from Poultry Farm to Agricultural Field, CSE."},{"key":"ref_24","first-page":"1069","article-title":"Study on the excretion of enrofloxacin in chicken and its degradation in chicken feces","volume":"36","author":"Wu","year":"2005","journal-title":"Acta Vet. Zootech. Sin."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1016\/j.vetmic.2018.02.018","article-title":"Effects of different types of flooring design on the development of antimicrobial resistance in commensal Escherichia coli in fattening turkeys","volume":"217","author":"Chuppava","year":"2018","journal-title":"Vet. Microbiol."},{"key":"ref_26","unstructured":"(2018, March 29). Annex I of Council Regulation. European Commission (EC) No. 1099\/2009 on the Protection of Animals at the Time of Killing. Available online: https:\/\/eur-lex.europa.eu\/eli\/reg\/2009\/1099\/oj."},{"key":"ref_27","unstructured":"Scherz, G. (2013). Carryover of Subtherapeutic Antimicrobial Dosages of Enrofloxacin and the Influence on the Development of Antibiotic Resistance of Commensal Escherichia Coli in the Intestine of Poultry. [Ph.D. Thesis, University of Veterinary Medicine]."},{"key":"ref_28","unstructured":"CLSI (2013). Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals, Clinical and Laboratory Standards Institute. Approved Standard-Fourth Edition; CLSI document Vet01-A4."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"996","DOI":"10.1126\/science.279.5353.996","article-title":"Medical consequences of antibiotic use in agriculture","volume":"279","author":"Witte","year":"1998","journal-title":"Science"},{"key":"ref_30","first-page":"204","article-title":"Oral medication via feed and water pharmacological aspects","volume":"116","author":"Kietzmann","year":"2009","journal-title":"Dtsch. Tierarztl. Wochenschr."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"284","DOI":"10.1016\/j.vetmic.2009.06.006","article-title":"Field trial evaluating changes in prevalence and patterns of antimicrobial resistance among Escherichia coli and Enterococcus spp. isolated from growing broilers medicated with enrofloxacin, apramycin and amoxicillin","volume":"139","author":"Belo","year":"2009","journal-title":"Vet. Microbiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1020","DOI":"10.3390\/ijerph10031020","article-title":"Antimicrobial resistance in Enterococcus spp. isolated from environmental samples in an area of intensive poultry production","volume":"10","author":"Furtula","year":"2013","journal-title":"Int. J. Environ. Res. Public Health"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1643","DOI":"10.3382\/ps.2007-00485","article-title":"Evolution of resistance in poultry intestinal Escherichia coli during three commonly used antimicrobial therapeutic treatments in poultry","volume":"87","author":"Miranda","year":"2008","journal-title":"Poult. Sci."},{"key":"ref_34","first-page":"195","article-title":"Resistance to non-quinolone antimicrobials in commensal Escherichia coli isolates from chickens treated orally with enrofloxacin","volume":"63","author":"Jurado","year":"2015","journal-title":"Jpn. J. Vet. Res."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1051\/vetres:2001120","article-title":"Use of antimicrobials in veterinary medicine and mechanisms of resistance","volume":"32","author":"Schwarz","year":"2001","journal-title":"Vet. Res."},{"key":"ref_36","first-page":"321","article-title":"Application of antibiotics in poultry","volume":"37","author":"Richter","year":"2009","journal-title":"Tier\u00e4rztl. Praxis Gro\u00dftiere"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1079\/WPS20040017","article-title":"Characteristics of the gastrointestinal microbial communities, with special reference to the chicken","volume":"60","author":"Apajalahti","year":"2004","journal-title":"Worlds Poult. Sci. J."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"836","DOI":"10.1046\/j.1365-2672.2000.01023.x","article-title":"Effects of heat stress on the antimicrobial drug resistance of Escherichia coli of the intestinal flora of swine","volume":"88","author":"Moro","year":"2000","journal-title":"J. Appl. Microbiol."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Oloso, N.O., Fagbo, S., Garbati, M., Olonitola, S.O., Awosanya, E.J., Aworh, M.K., Adamu, H., Odetokun, I.A., and Fasina, F.O. (2018). Antimicrobial Resistance in Food Animals and the Environment in Nigeria: A Review. Int. J. Environ. Res. Public Health, 15.","DOI":"10.3390\/ijerph15061284"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1016\/j.vetmic.2010.12.020","article-title":"Antimicrobial resistance in fecal Escherichia coli isolated from growing chickens on commercial broiler farms","volume":"150","author":"Ozaki","year":"2011","journal-title":"Vet. Microbiol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1080\/03079457.2016.1168515","article-title":"Antimicrobial resistance of Escherichia coli isolated in newly-hatched chickens and effect of amoxicillin treatment during their growth","volume":"45","author":"Fenollar","year":"2016","journal-title":"Avian Pathol."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Dierikx, C.M., van der Goot, J.A., Smith, H.E., Kant, A., and Mevius, D.J. (2013). Presence of ESBL\/AmpC-producing Escherichia coli in the broiler production pyramid: A descriptive study. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0079005"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"765","DOI":"10.1017\/S0950268810001524","article-title":"Risk factors for ceftiofur resistance in Escherichia coli from belgian broilers","volume":"139","author":"Persoons","year":"2011","journal-title":"Epidemiol. Infect."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1016\/j.ijantimicag.2005.02.006","article-title":"Mechanisms of quinolone resistance in Escherichia coli and Salmonella: Recent developments","volume":"25","author":"Hopkins","year":"2005","journal-title":"Int. J. Antimicrob. Agents"}],"container-title":["International Journal of Environmental Research and Public Health"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1660-4601\/15\/9\/1993\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T15:20:16Z","timestamp":1760196016000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1660-4601\/15\/9\/1993"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,9,13]]},"references-count":44,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2018,9]]}},"alternative-id":["ijerph15091993"],"URL":"https:\/\/doi.org\/10.3390\/ijerph15091993","relation":{},"ISSN":["1660-4601"],"issn-type":[{"value":"1660-4601","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,9,13]]}}}