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Uncovering the effects of copper feed supplementation on the selection of copper-tolerant and antibiotic-resistant Enterococcus in poultry production for sustainable environmental practices

2023-11-20Journal article Embargoed access
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dc.contributor.authorRebelo, Andreia
dc.contributor.authorDuarte, Bárbara
dc.contributor.authorFreitas, Ana R.
dc.contributor.authorAlmeida, Agostinho
dc.contributor.authorAzevedo, Rui
dc.contributor.authorPinto, Edgar
dc.contributor.authorPeixe, Luísa
dc.contributor.authorAntunes, Patrícia
dc.contributor.authorNovais, Carla
dc.date.accessioned2024-04-08T14:15:03Z
dc.date.embargo2026-01-02
dc.date.issued2023-11-20
dc.description.abstractThe use of antibiotics in animal production is linked to the emergence and spread of antibiotic-resistant bacteria, a threat to animal, environmental and human health. Copper (Cu) is an essential element in poultry diets and an alternative to antibiotics, supplementing inorganic or organic trace mineral feeds (ITMF/OTMF). However, its contribution to select multidrug-resistant (MDR) and Cu tolerant Enterococcus, a bacteria with a human-animal-environment-food interface, remains uncertain. We evaluated whether feeding chickens with Cu-ITMF or Cu-OTMF contributes to the selection of Cu tolerant and MDR Enterococcus from rearing to slaughter. Animal faeces [2–3-days-old (n = 18); pre-slaughter (n = 16)] and their meat (n = 18), drinking-water (n = 14) and feed (n = 18) from seven intensive farms with ITMF and OTMF flocks (10.000–64.000 animals each; 2019–2020; Portugal) were sampled. Enterococcus were studied by cultural, molecular and whole-genome sequencing methods and Cu concentrations by ICP-MS. Enterococcus (n = 477; 60 % MDR) were identified in 80 % of the samples, with >50 % carrying isolates resistant to tetracycline, quinupristin-dalfopristin, erythromycin, streptomycin, ampicillin or ciprofloxacin. Enterococcus with Cu tolerance genes, especially tcrB ± cueO, were mainly found in faeces (85 %; E. faecium/E. lactis) of ITMF/OTMF flocks. Similar occurrence and load of tcrB ± cueO Enterococcus in the faeces was detected throughout the chickens' lifespan in the ITMF/OTMF flocks, decreasing in meat. Most of the polyclonal MDR Enterococcus population carrying tcrB ± cueO or only cueO (67 %) showed a wild-type phenotype (MICCuSO4 ≤ 12 mM) linked to absence of tcrYAZB or truncated variants, also detected in 85 % of Enterococcus public genomes from poultry. Finally, < 65 μg/g Cu was found in all faecal and meat samples. In conclusion, Cu present in ITMF/OTMF is not selecting Cu tolerant and MDR Enterococcus during chickens' lifespan. However, more studies are needed to assess the minimum concentration of Cu required for MDR bacterial selection and horizontal transfer of antibiotic resistance genes, which would support sustainable practices mitigating antibiotic resistance spread in animal production and the environment beyond.pt_PT
dc.description.versioninfo:eu-repo/semantics/publishedVersionpt_PT
dc.identifier.citationRebelo, A., Duarte, B., Freitas, A. R., Almeida, A., Azevedo, R., Pinto, E., Peixe, L., Antunes, P., & Novais, C. (2023). Uncovering the effects of copper feed supplementation on the selection of copper-tolerant and antibiotic-resistant Enterococcus in poultry production for sustainable environmental practices. Science of The Total Environment, 900, 165769. https://doi.org/10.1016/j.scitotenv.2023.165769pt_PT
dc.identifier.doi10.1016/j.scitotenv.2023.165769pt_PT
dc.identifier.eissn1879-1026
dc.identifier.issn0048-9697
dc.identifier.urihttp://hdl.handle.net/10400.22/25309
dc.language.isoengpt_PT
dc.peerreviewedyespt_PT
dc.publisherElsevierpt_PT
dc.relationThis work was supported by the Applied Molecular Biosciences Unit - UCIBIO which is financed by national funds from FCT - Fundação para a Ciência e a Tecnologia (projects UIDP/04378/2020 and UIDB/04378/2020), by the Associate Laboratory Institute for Health and Bioeconomy-i4HB (project LA/P/0140/2020), by the AgriFood XXI I&D&I project (NORTE-01-0145-FEDER-000041) co-financed by the European Regional Development Fund (ERDF) through NORTE 2020 (Programa Operacional Regional do Norte 2014/2020) and by the University of Porto and SOJA DE PORTUGAL (Grant No. IJUP-Empresas-2019-17). Andreia Rebelo was supported by a PhD fellowship from FCT (SFRH/BD/137100/2018) co-financed by the European Social Fund through NORTE 2020 and ARF acknowledges the Junior Research Position (CEECIND/02268/2017) granted by FCT. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
dc.relation.publisherversionhttps://www.sciencedirect.com/science/article/pii/S0048969723043929?via%3Dihubpt_PT
dc.rights.urihttp://creativecommons.org/licenses/by-nc/4.0/pt_PT
dc.subjectBacillotapt_PT
dc.subjectTrace-mineralspt_PT
dc.subjectChicken-productionpt_PT
dc.subjectAntimicrobial resistancept_PT
dc.subjectMetalspt_PT
dc.subjectFood-safetypt_PT
dc.titleUncovering the effects of copper feed supplementation on the selection of copper-tolerant and antibiotic-resistant Enterococcus in poultry production for sustainable environmental practicespt_PT
dc.typejournal article
dspace.entity.typePublication
oaire.citation.endPage12pt_PT
oaire.citation.startPage1pt_PT
oaire.citation.titleScience of The Total Environmentpt_PT
oaire.citation.volume900pt_PT
person.familyNameRebelo
person.familyNamePinto
person.givenNameAndreia
person.givenNameEdgar
person.identifier.ciencia-idA81C-7A59-ECAD
person.identifier.ciencia-id271F-B7DF-8FAB
person.identifier.orcid0000-0003-2218-6005
person.identifier.orcid0000-0002-8021-4783
person.identifier.ridT-9024-2017
rcaap.rightsembargoedAccesspt_PT
rcaap.typearticlept_PT
relation.isAuthorOfPublication913dc5cd-9e92-456d-88f5-419571a87f85
relation.isAuthorOfPublicationeaf9fc86-1a1c-437f-adee-d28040aa7f2f
relation.isAuthorOfPublication.latestForDiscovery913dc5cd-9e92-456d-88f5-419571a87f85

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