E. coli; ESBL; MDR; colistin; meat lamb; sheep; Animal Science and Zoology; Veterinary (all)
Abstract :
[en] Major efforts have been made to reduce the use of colistin in livestock since the discovery of the plasmid-borne mobile colistin resistance (mcr) gene in E. coli a decade ago, to curb the burden of its potential transmission to other bacterial species, spread between animals, humans and the environment. This study explored the longitudinal prevalence and characteristics of colistin-resistant and extended-spectrum beta-lactamase-producing (ESBL) E. coli via in vivo fecal and ex vivo carcass swabs from two batches of conventional indoor and organic outdoor Wallon meat sheep from birth to slaughter in 2020 and 2021. Antimicrobial susceptibility testing via broth microdilution revealed that n = 16/109 (15%) E. coli isolates from conventional meat lamb fecal samples had a reduced colistin sensitivity (MIC = 0.5 μg/mL) and thereof, n = 9/109 (8%) were multi-drug-resistant E. coli, while no resistant isolates were recovered from their carcasses. Sequencing revealed causative pmrB genes, indicating that the reduced sensitivity to colistin was not plasmid-borne. While the sample size was small (n = 32), no colistin-resistant and ESBL-producing E. coli were isolated from the organic meat sheep and their carcasses, potentially due to the different husbandry conditions. Prudent and judicious antimicrobial use and strict slaughter hygiene remain imperative for effective risk management to protect consumers in a sustainable One Health approach.
Research Center/Unit :
FARAH. Santé publique vétérinaire - ULiège
Disciplines :
Food science
Author, co-author :
Dragon, Delphine ✱; Integrated Veterinary Research Unit, Faculty of Science, Université de Namur, Rue de Bruxelles 61, 5000 Namur, Belgium ; Department of Food Sciences, Microbiology, Fundamental and Applied Research for Animal & Health (FARAH), Faculty of Veterinary Medicine, Université de Liège, Avenue de Cureghem 10, 4000 Liège, Belgium
Jansen, Wiebke ✱; Integrated Veterinary Research Unit, Faculty of Science, Université de Namur, Rue de Bruxelles 61, 5000 Namur, Belgium ; Federation of Veterinarians of Europe (FVE), Rue Victor Oudart 7, 1030 Brussels, Belgium
Dumont, Helene; Integrated Veterinary Research Unit, Faculty of Science, Université de Namur, Rue de Bruxelles 61, 5000 Namur, Belgium
Wiggers, Laetitia; Integrated Veterinary Research Unit, Faculty of Science, Université de Namur, Rue de Bruxelles 61, 5000 Namur, Belgium
Coupeau, Damien ; Integrated Veterinary Research Unit, Faculty of Science, Université de Namur, Rue de Bruxelles 61, 5000 Namur, Belgium
Saulmont, Marc; Regional Animal Health and Identification Association (ARSIA), 5590 Ciney, Belgium
Taminiau, Bernard ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Santé publique vétérinaire
Muylkens, Benoit ✱; Integrated Veterinary Research Unit, Faculty of Science, Université de Namur, Rue de Bruxelles 61, 5000 Namur, Belgium
Daube, Georges ✱; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires
✱ These authors have contributed equally to this work.
Language :
English
Title :
Conventionally Reared Wallon Meat Lambs Carry Transiently Multi-Drug-Resistant Escherichia coli with Reduced Sensitivity to Colistin Before Slaughter.
NARILIS - Namur Research Institute for Life Sciences
Funding text :
This research was funded by the NARILIS research institute, grant number 2018-COLREC. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.
Murray C.J.L. Ikuta K.S. Sharara F. Swetschinski L. Robles Aguilar G. Gray A. Han C. Bisignano C. Rao P. Wool E. et al. Global Burden of Bacterial Antimicrobial Resistance in 2019: A Systematic Analysis Lancet 2022 399 629 655 10.1016/S0140-6736(21)02724-0 35065702
Serna C. Gonzalez-Zorn B. Antimicrobial Resistance and One Health Rev. Esp. Quimioter. 2022 35 37 40 10.37201/req/s03.09.2022 36285856
El-Sayed Ahmed M.A.E.-G. Zhong L.-L. Shen C. Yang Y. Doi Y. Tian G.-B. Colistin and Its Role in the Era of Antibiotic Resistance: An Extended Review (2000–2019) Emerg. Microbes Infect. 2020 9 868 885 10.1080/22221751.2020.1754133 32284036
Binsker U. Käsbohrer A. Hammerl J.A. Global Colistin Use: A Review of the Emergence of Resistant Enterobacterales and the Impact on Their Genetic Basis FEMS Microbiol. Rev. 2022 46 fuab049 10.1093/femsre/fuab049
Jansen W. Van Hout J. Wiegel J. Iatridou D. Chantziaras I. De Briyne N. Colistin Use in European Livestock: Veterinary Field Data on Trends and Perspectives for Further Reduction Vet. Sci. 2022 9 650 10.3390/vetsci9110650
Liu Y.-Y. Wang Y. Walsh T.R. Yi L.-X. Zhang R. Spencer J. Doi Y. Tian G. Dong B. Huang X. Emergence of Plasmid-Mediated Colistin Resistance Mechanism MCR-1 in Animals and Human Beings in China: A Microbiological and Molecular Biological Study Lancet 2016 16 161 168 10.1016/S1473-3099(15)00424-7
Hussein N.H. AL-Kadmy I.M.S. Taha B.M. Hussein J.D. Mobilized Colistin Resistance (mcr) Genes from 1 to 10: A Comprehensive Review Mol. Biol. Rep. 2021 48 2897 2907 10.1007/s11033-021-06307-y
European Commission 2013/652/EU: Commission Implementing Decision of 12 November 2013 on the Monitoring and Reporting of Antimicrobial Resistance in Zoonotic and Commensal Bacteria (Notified under Document C(2013) 7145) Text with EEA Relevance 2013 39 Available online: https://eur-lex.europa.eu/eli/dec_impl/2013/652/oj (accessed on 25 August 2024)
ECDC EFSA EMA Third Joint Inter-agency Report on Integrated Analysis of Consumption of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Bacteria from Humans and Food-producing Animals in the EU/EEA: JIACRA III 2016–2018 EFSA J. 2021 19 e06712 10.2903/j.efsa.2021.6712
EEFSA (European Food Safety Authority) Brocca D. Salvatore S. Report for 2020 on the Results from the Monitoring of Veterinary Medicinal Product Residues and Other Substances in Live Animals and Animal Products EFSA Supporting Publications Parma, Italy 2022 Volume 19 91p 10.2903/sp.efsa.2022.EN-7143
Cargnel M. Dispas M. Antimicrobial Resistance in Commensal Escherichia Coli from Livestock in Belgium: Trend Analysis 2011–2018. Sciensano Report 2018 Available online: https://www.amcra.be/swfiles/files/20190605-Rapport_AMR_2011-2018_trend_AMR_Ecoli.pdf (accessed on 24 August 2024)
AMCRA (AntiMicrobial Consumption and Resistance in Animals) Activités et realizations—Utilisation et la résistance d’antibiotiques chez les animaux en Belgique 2021. Report 2022 Available online: https://www.amcra.be/swfiles/files/Publiek-rapport-2023_finaal_FR.pdf (accessed on 25 August 2024)
BELMAP One Health Report on Antibiotic Use and Resistance in Belgium 2022. Report Available online: https://www.health.belgium.be/sites/default/files/uploads/fields/fpshealth_theme_file/rapport_annuel_amr_2021.pdf (accessed on 25 August 2024)
European Commission Commission Regulation (EC) No 2073/2005 of 15 November 2005 on Microbiological Criteria for Foodstuffs 2005 Available online: https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX%3A02005R2073-20200308 (accessed on 25 August 2024)
Société Française de Microbiologie CA-SFM, (Comité de l’antibiogramme de la Société Française de Microbiologie) Recommandations Vétérinaires 2021. Report 2021 Available online: https://www.sfm-microbiologie.org/wp-content/uploads/2021/12/CASFM_VET2021.pdf (accessed on 25 August 2024)
The European Committee on Antimicrobial Susceptibility Testing. Breakpoint Tables for Interpretation of MICs and Zone Diameters Version 14.0 2024 Available online: http://www.eucast.org (accessed on 25 August 2024)
Société Française de; Microbiologie CA-SFM, (Comité de l’antibiogramme de la Société Française de Microbiologie) Recommandations Vétérinaires 2013; Société Française de Microbiologie 2013 Available online: https://www.sfm-microbiologie.org/wp-content/uploads/2020/07/CASFM_2013.pdf (accessed on 25 August 2024)
Gennart I. Petit A. Wiggers L. Pejaković S. Dauchot N. Laurent S. Coupeau D. Muylkens B. Epigenetic Silencing of MicroRNA-126 Promotes Cell Growth in Marek’s Disease Microorganisms 2021 9 1339 10.3390/microorganisms9061339
Chen S. Zhou Y. Chen Y. Gu J. Fastp: An Ultra-Fast All-in-One FASTQ Preprocessor Bioinformatics 2018 34 i884 i890 10.1093/bioinformatics/bty560
Wick R.R. Judd L.M. Gorrie C.L. Holt K.E. Unicycler: Resolving Bacterial Genome Assemblies from Short and Long Sequencing Reads PLOS Computat Biol. 2017 13 e1005595 10.1371/journal.pcbi.1005595 28594827
Zhou Z. Alikhan N.-F. Mohamed K. Fan Y. The Agama Study Group Achtman M. The EnteroBase User’s Guide, with Case Studies on Salmonella Transmissions, Yersinia pestis Phylogeny, and Escherichia Core Genomic Diversity Genome Res. 2020 30 138 152 10.1101/gr.251678.119 31809257
Feldgarden M. Brover V. Gonzalez-Escalona N. Frye J.G. Haendiges J. Haft D.H. Hoffmann M. Pettengill J.B. Prasad A.B. Tillman G.E. et al. AMRFinderPlus and the Reference Gene Catalog Facilitate Examination of the Genomic Links among Antimicrobial Resistance, Stress Response, and Virulence Sci. Rep. 2021 11 12728 10.1038/s41598-021-91456-0 34135355
Magiorakos A.-P. Srinivasan A. Carey R.B. Carmeli Y. Falagas M.E. Giske C.G. Harbarth S. Hindler J.F. Kahlmeter G. Olsson-Liljequist B. et al. Multidrug-Resistant, Extensively Drug-Resistant and Pandrug-Resistant Bacteria: An International Expert Proposal for Interim Standard Definitions for Acquired Resistance Clin. Microbiol. Infect. 2012 18 268 281 10.1111/j.1469-0691.2011.03570.x
Seni J. Falgenhauer L. Simeo N. Mirambo M.M. Imirzalioglu C. Matee M. Rweyemamu M. Chakraborty T. Mshana S.E. Multiple ESBL-Producing Escherichia Coli Sequence Types Carrying Quinolone and Aminoglycoside Resistance Genes Circulating in Companion and Domestic Farm Animals in Mwanza, Tanzania, Harbor Commonly Occurring Plasmids Front. Microbiol. 2016 7 142 10.3389/fmicb.2016.00142
Dantas Palmeira J. Haenni M. Madec J.-Y. Ferreira H.M. First Global Report of Plasmid-Mediated mcr-1 and Extended-Spectrum Beta-Lactamase-Producing Escherichia Coli from Sheep in Portugal Antibiotics 2021 10 1403 10.3390/antibiotics10111403
Geser N. Stephan R. Hächler H. Occurrence and Characteristics of Extended-Spectrum β-Lactamase (ESBL) Producing Enterobacteriaceae in Food Producing Animals, Minced Meat and Raw Milk BMC Vet. Res. 2012 8 21 10.1186/1746-6148-8-21
Snow L.C. Wearing H. Stephenson B. Teale C.J. Coldham N.G. 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 Vet. Rec. 2011 169 656 10.1136/vr.100037
Benavides J.A. Salgado-Caxito M. Opazo-Capurro A. Gonzalez Munoz P. Piñeiro A. Otto Medina M. Rivas L. Munita J. Millán J. ESBL-Producing Escherichia Coli Carrying CTX-m Genes Circulating among Livestock, Dogs, and Wild Mammals in Small-Scale Farms of Central Chile Antibiotics 2021 10 510 10.3390/antibiotics10050510
Pehlivanoglu F. Turutoglu H. Ozturk D. Yardimci H. Molecular Characterization of ESBL-Producing Escherichia Coli Isolated from Healthy Cattle and Sheep Acta Vet. 2016 66 520 533 10.1515/acve-2016-0045
İlknur A. La Ragione Roberto M. Woodward Martin J. Colonization, Persistence, and Tissue Tropism of Escherichia coli O26 in Conventionally Reared Weaned Lambs Appl. Environ. Microbiol. 2007 73 691 698 10.1128/AEM.01879-06
Brown C.A. Harmon B.G. Zhao T. Doyle M.P. Experimental Escherichia coli O157:H7 Carriage in Calves Appl. Environ. Microbiol. 1997 63 27 32 10.1128/aem.63.1.27-32.1997 8979335
Hu X. Chen Y. Xu H. Qiao J. Ge H. Liu R. Zheng B. Genomic Epidemiology and Transmission Characteristics of mcr1-oositive Colistin-Resistant Escherichia coli Strains Circulating at Natural Environment Sci. Total Environ. 2023 882 163600 10.1016/j.scitotenv.2023.163600 37086987
Hamame A. Davoust B. Hasnaoui B. Mwenebitu D.L. Rolain J.-M. Diene S.M. Screening of Colistin-Resistant Bacteria in Livestock Animals from France Vet. Res. 2022 53 96 10.1186/s13567-022-01113-1
Rhouma M. Madec J.-Y. Laxminarayan R. Colistin: From the Shadows to a One Health Approach for Addressing Antimicrobial Resistance Int. J. Antimicrob. Agents 2023 61 106713 10.1016/j.ijantimicag.2023.106713
Chen H.D. Groisman E.A. The Biology of the PmrA/PmrB Two-Component System: The Major Regulator of Lipopolysaccharide Modifications Annu. Rev. Microbiol. 2013 67 83 112 10.1146/annurev-micro-092412-155751
Quesada A. Porrero M.C. Téllez S. Palomo G. García M. Domínguez L. Polymorphism of Genes Encoding PmrAB in Colistin-Resistant Strains of Escherichia coli and Salmonella enterica Isolated from Poultry and Swine J. Antimicro Chemothera 2015 70 71 74 10.1093/jac/dku320
Wong T.L. Nicol C. Cook R. Macdiarmid S. Salmonella in Uncooked Retail Meats in New Zealand J. Food Prot. 2007 70 1360 1365 10.4315/0362-028X-70.6.1360
Chinnam B.K. Nelapati S. Tumati S.R. Bobbadi S. Chaitanya Peddada V. Bodempudi B. Detection of β-Lactamase–Producing Proteus mirabilis Strains of Animal Origin in Andhra Pradesh, India and Their Genetic Diversity J. Food Prot. 2021 84 1374 1379 10.4315/JFP-20-399
Kalchayanand N. Arthur T.M. Bosilevac J.M. Brichta-Harhay D.M. Guerini M.N. Shackelford S.D. Wheeler T.L. Koohmaraie M. Microbiological Characterization of Lamb Carcasses at Commercial Processing Plants in the United States J. Food Prot. 2007 70 1811 1819 10.4315/0362-028X-70.8.1811
Nobili G. La Bella G. Basanisi M.G. Damato A.M. Coppola R. Migliorelli R. Rondinone V. Leekitcharoenphon P. Bortolaia V. La Salandra G. Occurrence and Characterisation of Colistin-Resistant Escherichia coli in Raw Meat in Southern Italy in 2018–2020 Microorganisms 2022 10 1805 10.3390/microorganisms10091805 36144407
Ghafur A. Shankar C. GnanaSoundari P. Venkatesan M. Mani D. Thirunarayanan M.A. Veeraraghavan B. Detection of Chromosomal and Plasmid-Mediated Mechanisms of Colistin Resistance in Escherichia coli and Klebsiella pneumoniae from Indian Food Samples J. Glob. Antimicrob. Resist. 2019 16 48 52 10.1016/j.jgar.2018.09.005 30244040
Schimmer B. Nygard K. Eriksen H.-M. Lassen J. Lindstedt B.-A. Brandal L.T. Kapperud G. Aavitsland P. Outbreak of Haemolytic Uraemic Syndrome in Norway Caused by Stx2-Positive Escherichia coli O103:H25 Traced to Cured Mutton Sausages BMC Infect. Dis. 2008 8 41 10.1186/1471-2334-8-41 18387178
Obaidat M.M. Tarazi Y.H. AlSmadi W.M. Sheep and Goats Are Reservoirs of Colistin Resistant Escherichia coli That Co-resist Critically Important Antimicrobials: First Study from Jordan J. Food Saf. 2023 43 e13023 10.1111/jfs.13023
Hammad A.M. Hoffmann M. Gonzalez-Escalona N. Abbas N.H. Yao K. Koenig S. Allué-Guardia A. Eppinger M. Genomic Features of Colistin Resistant Escherichia coli ST69 Strain Harboring mcr-1 on IncHI2 Plasmid from Raw Milk Cheese in Egypt Infect. Genet. Evol. 2019 73 126 131 10.1016/j.meegid.2019.04.021
Imre K. Ban-Cucerzan A. Herman V. Sallam K.I. Cristina R.T. Abd-Elghany S.M. Morar D. Popa S.A. Imre M. Morar A. Occurrence, Pathogenic Potential and Antimicrobial Resistance of Escherichia coli Isolated from Raw Milk Cheese Commercialized in Banat Region, Romania Antibiotics 2022 11 721 10.3390/antibiotics11060721
Rodrigues da Costa M. Diana A. A Systematic Review on the Link between Animal Welfare and Antimicrobial Use in Captive Animals Animals 2022 12 1025 10.3390/ani12081025
Österberg J. Wingstrand A. Nygaard Jensen A. Kerouanton A. Cibin V. Barco L. Denis M. Aabo S. Bengtsson B. Antibiotic Resistance in Escherichia coli from Pigs in Organic and Conventional Farming in Four European Countries PLoS ONE 2016 11 e0157049 10.1371/journal.pone.0157049
Kempf I. Kerouanton A. Bougeard S. Nagard B. Rose V. Mourand G. Osterberg J. Denis M. Bengtsson B.O. Campylobacter coli in Organic and Conventional Pig Production in France and Sweden: Prevalence and Antimicrobial Resistance Front. Microbiol. 2017 8 955 10.3389/fmicb.2017.00955
Tenhagen B.-A. Flor M. Alt K. Knüver M.-T. Buhler C. Käsbohrer A. Stingl K. Association of Antimicrobial Resistance in Campylobacter spp. in Broilers and Turkeys with Antimicrobial Use Antibiotics 2021 10 673 10.3390/antibiotics10060673
Von Borell E. Sørensen J.T. Organic Livestock Production in Europe: Aims, Rules and Trends with Special Emphasis on Animal Health and Welfare Livest. Prod. Sci. 2004 90 3 9 10.1016/j.livprodsci.2004.07.003
Xiao H. Yan H. Tian P. Ji S. Zhao W. Lu C. Zhang Y. Liu Y. The Effect of Early Colonized Gut Microbiota on the Growth Performance of Suckling Lambs Front. Microbiol. 2023 14 1273444 10.3389/fmicb.2023.1273444 37954254
Prache S. Schreurs N. Guillier L. Review: Factors Affecting Sheep Carcass and Meat Quality Attributes Animal 2022 16 100330 10.1016/j.animal.2021.100330 34400114
García-Fernández S. García-Castillo M. Ruiz-Garbajosa P. Morosini M.-I. Bala Y. Zambardi G. Cantón R. Performance of CHROMID® Colistin R Agar, a New Chromogenic Medium for Screening of Colistin-Resistant Enterobacterales Diagn. Microbiol. Infect. Dis. 2019 93 1 4 10.1016/j.diagmicrobio.2018.07.008 30097296
Leshaba T.M.S. Mbelle N.M. Osei Sekyere J. Current and Emerging Polymyxin Resistance Diagnostics: A Systematic Review of Established and Novel Detection Methods J. Appl. Microbiol. 2022 132 8 30 10.1111/jam.15184
Thiry D. Berrah A. Evrard J. Duprez J.-N. Mainil J.G. Saulmont M. Assessment of Two Selective Agar Media to Isolate Colistin-Resistant Bovine Escherichia coli: Correlation with Minimal Inhibitory Concentration and Presence of mcr Genes J. Microbiol. Meth 2019 159 174 178 10.1016/j.mimet.2019.03.004
Bastidas-Caldes C. de Waard J.H. Salgado M.S. Villacís M.J. Coral-Almeida M. Yamamoto Y. Calvopiña M. Worldwide Prevalence of mcr-Mediated Colistin-Resistance Escherichia coli in Isolates of Clinical Samples, Healthy Humans, and Livestock—A Systematic Review and Meta-Analysis Pathogens 2022 11 659 10.3390/pathogens11060659
Matuschek E. Åhman J. Webster C. Kahlmeter G. Antimicrobial Susceptibility Testing of Colistin—Evaluation of Seven Commercial MIC Products against Standard Broth Microdilution for Escherichia coli, Klebsiella pneumoniae, Pseudomonas aeruginosa, and Acinetobacter spp. Clin. Microbiol. Infect. 2018 24 865 870 10.1016/j.cmi.2017.11.020
Feldgarden M. Vyacheslav B. Haft Daniel H. Prasad Arjun B. Slotta Douglas J. Igor T. Tyson Gregory H. Zhao S. Hsu C.-H. McDermott Patrick F. et al. Validating the AMRFinder Tool and Resistance Gene Database by Using Antimicrobial Resistance Genotype-Phenotype Correlations in a Collection of Isolates Antimicrob. Agents Chemother. 2019 63 e00483-19 10.1128/AAC.00483-19
Tyson G.H. Li C. Ayers S. McDermott P.F. Zhao S. Using Whole-Genome Sequencing to Determine Appropriate Streptomycin Epidemiological Cutoffs for Salmonella and Escherichia coli FEMS Microbiol. Lett. 2016 363 fnw009 10.1093/femsle/fnw009
Tyson G.H. Zhao S. Li C. Ayers S. Sabo J.L. Lam C. Miller R.A. McDermott P.F. Establishing Genotypic Cutoff Values to Measure Antimicrobial Resistance in Salmonella Antimicrob. Agents Chemother. 2017 61 10 1128 10.1128/AAC.02140-16