Cargando…

Competitive Exclusion Prevents Colonization and Compartmentalization Reduces Transmission of ESBL-Producing Escherichia coli in Broilers

Extended spectrum beta-lactamase (ESBL)-producing bacteria are resistant to extended-spectrum cephalosporins and are common in broilers. Interventions are needed to reduce the prevalence of ESBL-producing bacteria in the broiler production pyramid. This study investigated two different interventions...

Descripción completa

Detalles Bibliográficos
Autores principales: Dame-Korevaar, Anita, Kers, Jannigje G., van der Goot, Jeanet, Velkers, Francisca C., Ceccarelli, Daniela, Mevius, Dik J., Stegeman, Arjan, Fischer, Egil A. J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7693455/
https://www.ncbi.nlm.nih.gov/pubmed/33304325
http://dx.doi.org/10.3389/fmicb.2020.566619
_version_ 1783614748281012224
author Dame-Korevaar, Anita
Kers, Jannigje G.
van der Goot, Jeanet
Velkers, Francisca C.
Ceccarelli, Daniela
Mevius, Dik J.
Stegeman, Arjan
Fischer, Egil A. J.
author_facet Dame-Korevaar, Anita
Kers, Jannigje G.
van der Goot, Jeanet
Velkers, Francisca C.
Ceccarelli, Daniela
Mevius, Dik J.
Stegeman, Arjan
Fischer, Egil A. J.
author_sort Dame-Korevaar, Anita
collection PubMed
description Extended spectrum beta-lactamase (ESBL)-producing bacteria are resistant to extended-spectrum cephalosporins and are common in broilers. Interventions are needed to reduce the prevalence of ESBL-producing bacteria in the broiler production pyramid. This study investigated two different interventions. The effect of a prolonged supply of competitive exclusion (CE) product and compartmentalization on colonization and transmission, after challenge with a low dose of ESBL-producing Escherichia coli, in broilers kept under semi-field conditions, were examined. One-day-old broilers (Ross 308) (n = 400) were housed in four experimental rooms, subdivided in one seeder (S/C1)-pen and eight contact (C2)-pens. In two rooms, CE product was supplied from day 0 to 7. At day 5, seeder-broilers were inoculated with E. coli strain carrying bla(CTX–M–)(1) on plasmid IncI1 (CTX-M-1-E. coli). Presence of CTX-M-1-E. coli was determined using cloacal swabs (day 5–21 daily) and cecal samples (day 21). Time until colonization and cecal excretion (log(10) CFU/g) were analyzed using survival analysis and linear regression. Transmission coefficients within and between pens were estimated using maximum likelihood. The microbiota composition was assessed by 16S ribosomal RNA gene amplicon sequencing in cecal content of broilers on days 5 and 21. None of the CE broilers was CTX-M-1-E. coli positive. In contrast, in the untreated rooms 187/200 of the broilers were CTX-M-1-E. coli positive at day 21. Broilers in C2-pens were colonized later than seeder-broilers (Time to event Ratio 3.53, 95% CI 3.14 to 3.93). The transmission coefficient between pens was lower than within pens (3.28 × 10(–4) day(–2), 95% CI 2.41 × 10(–4) to 4.32 × 10(–4) vs. 6.12 × 10(–2) day(–2), 95% CI 4.78 × 10(–2) to 7.64 × 10(–2)). The alpha diversity of the cecal microbiota content was higher in CE broilers than in control broilers at days 5 and 21. The supply of a CE product from day 0 to 7 prevented colonization of CTX-M-1-E. coli after challenge at day 5, likely as a result of CE induced effects on the microbiota composition. Furthermore, compartmentalization reduced transmission rate between broilers. Therefore, a combination of compartmentalization and supply of a CE product may be a useful intervention to reduce transmission and prevent colonization of ESBL/pAmpC-producing bacteria in the broiler production pyramid.
format Online
Article
Text
id pubmed-7693455
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-76934552020-12-09 Competitive Exclusion Prevents Colonization and Compartmentalization Reduces Transmission of ESBL-Producing Escherichia coli in Broilers Dame-Korevaar, Anita Kers, Jannigje G. van der Goot, Jeanet Velkers, Francisca C. Ceccarelli, Daniela Mevius, Dik J. Stegeman, Arjan Fischer, Egil A. J. Front Microbiol Microbiology Extended spectrum beta-lactamase (ESBL)-producing bacteria are resistant to extended-spectrum cephalosporins and are common in broilers. Interventions are needed to reduce the prevalence of ESBL-producing bacteria in the broiler production pyramid. This study investigated two different interventions. The effect of a prolonged supply of competitive exclusion (CE) product and compartmentalization on colonization and transmission, after challenge with a low dose of ESBL-producing Escherichia coli, in broilers kept under semi-field conditions, were examined. One-day-old broilers (Ross 308) (n = 400) were housed in four experimental rooms, subdivided in one seeder (S/C1)-pen and eight contact (C2)-pens. In two rooms, CE product was supplied from day 0 to 7. At day 5, seeder-broilers were inoculated with E. coli strain carrying bla(CTX–M–)(1) on plasmid IncI1 (CTX-M-1-E. coli). Presence of CTX-M-1-E. coli was determined using cloacal swabs (day 5–21 daily) and cecal samples (day 21). Time until colonization and cecal excretion (log(10) CFU/g) were analyzed using survival analysis and linear regression. Transmission coefficients within and between pens were estimated using maximum likelihood. The microbiota composition was assessed by 16S ribosomal RNA gene amplicon sequencing in cecal content of broilers on days 5 and 21. None of the CE broilers was CTX-M-1-E. coli positive. In contrast, in the untreated rooms 187/200 of the broilers were CTX-M-1-E. coli positive at day 21. Broilers in C2-pens were colonized later than seeder-broilers (Time to event Ratio 3.53, 95% CI 3.14 to 3.93). The transmission coefficient between pens was lower than within pens (3.28 × 10(–4) day(–2), 95% CI 2.41 × 10(–4) to 4.32 × 10(–4) vs. 6.12 × 10(–2) day(–2), 95% CI 4.78 × 10(–2) to 7.64 × 10(–2)). The alpha diversity of the cecal microbiota content was higher in CE broilers than in control broilers at days 5 and 21. The supply of a CE product from day 0 to 7 prevented colonization of CTX-M-1-E. coli after challenge at day 5, likely as a result of CE induced effects on the microbiota composition. Furthermore, compartmentalization reduced transmission rate between broilers. Therefore, a combination of compartmentalization and supply of a CE product may be a useful intervention to reduce transmission and prevent colonization of ESBL/pAmpC-producing bacteria in the broiler production pyramid. Frontiers Media S.A. 2020-11-10 /pmc/articles/PMC7693455/ /pubmed/33304325 http://dx.doi.org/10.3389/fmicb.2020.566619 Text en Copyright © 2020 Dame-Korevaar, Kers, van der Goot, Velkers, Ceccarelli, Mevius, Stegeman and Fischer. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Dame-Korevaar, Anita
Kers, Jannigje G.
van der Goot, Jeanet
Velkers, Francisca C.
Ceccarelli, Daniela
Mevius, Dik J.
Stegeman, Arjan
Fischer, Egil A. J.
Competitive Exclusion Prevents Colonization and Compartmentalization Reduces Transmission of ESBL-Producing Escherichia coli in Broilers
title Competitive Exclusion Prevents Colonization and Compartmentalization Reduces Transmission of ESBL-Producing Escherichia coli in Broilers
title_full Competitive Exclusion Prevents Colonization and Compartmentalization Reduces Transmission of ESBL-Producing Escherichia coli in Broilers
title_fullStr Competitive Exclusion Prevents Colonization and Compartmentalization Reduces Transmission of ESBL-Producing Escherichia coli in Broilers
title_full_unstemmed Competitive Exclusion Prevents Colonization and Compartmentalization Reduces Transmission of ESBL-Producing Escherichia coli in Broilers
title_short Competitive Exclusion Prevents Colonization and Compartmentalization Reduces Transmission of ESBL-Producing Escherichia coli in Broilers
title_sort competitive exclusion prevents colonization and compartmentalization reduces transmission of esbl-producing escherichia coli in broilers
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7693455/
https://www.ncbi.nlm.nih.gov/pubmed/33304325
http://dx.doi.org/10.3389/fmicb.2020.566619
work_keys_str_mv AT damekorevaaranita competitiveexclusionpreventscolonizationandcompartmentalizationreducestransmissionofesblproducingescherichiacoliinbroilers
AT kersjannigjeg competitiveexclusionpreventscolonizationandcompartmentalizationreducestransmissionofesblproducingescherichiacoliinbroilers
AT vandergootjeanet competitiveexclusionpreventscolonizationandcompartmentalizationreducestransmissionofesblproducingescherichiacoliinbroilers
AT velkersfranciscac competitiveexclusionpreventscolonizationandcompartmentalizationreducestransmissionofesblproducingescherichiacoliinbroilers
AT ceccarellidaniela competitiveexclusionpreventscolonizationandcompartmentalizationreducestransmissionofesblproducingescherichiacoliinbroilers
AT meviusdikj competitiveexclusionpreventscolonizationandcompartmentalizationreducestransmissionofesblproducingescherichiacoliinbroilers
AT stegemanarjan competitiveexclusionpreventscolonizationandcompartmentalizationreducestransmissionofesblproducingescherichiacoliinbroilers
AT fischeregilaj competitiveexclusionpreventscolonizationandcompartmentalizationreducestransmissionofesblproducingescherichiacoliinbroilers