Drivers of ESBL-producing Escherichia coli dynamics in calf fattening farms: A modelling study

The contribution of bacteria in livestock to the global burden of antimicrobial resistance raises concerns worldwide. However, the dynamics of selection and diffusion of antimicrobial resistance in farm animals are not fully understood. Here, we used veal calf fattening farms as a model system, as t...

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Main Authors: Jonathan Bastard, Marisa Haenni, Emilie Gay, Philippe Glaser, Jean-Yves Madec, Laura Temime, Lulla Opatowski
Format: Article
Language:English
Published: Elsevier 2021-06-01
Series:One Health
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2352771421000288
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spelling doaj-6783c516de4e4bc79d131931f8bb241f2021-04-26T05:57:14ZengElsevierOne Health2352-77142021-06-0112100238Drivers of ESBL-producing Escherichia coli dynamics in calf fattening farms: A modelling studyJonathan Bastard0Marisa Haenni1Emilie Gay2Philippe Glaser3Jean-Yves Madec4Laura Temime5Lulla Opatowski6Université Paris-Saclay, UVSQ, Univ. Paris-Sud, Inserm, CESP, Anti-infective evasion and pharmacoepidemiology team, F-78180 Montigny-le-Bretonneux, France; Institut Pasteur, Epidemiology and Modelling of Antibiotic Evasion unit, F-75015 Paris, France; MESuRS laboratory, Conservatoire national des arts et métiers, 292 rue Saint-Martin, 75003 Paris, France; PACRI unit, Institut Pasteur, Conservatoire national des arts et métiers, Paris, France; Université Paris Diderot, Sorbonne Paris Cité, Paris, France; Corresponding author at: Institut Pasteur, EMEA unit, 25 rue du Docteur Roux, 75015 Paris, France.Université de Lyon - Anses, Laboratoire de Lyon, Unité Antibiorésistance et Virulence Bactériennes, Lyon, FranceUniversité de Lyon - Anses, Laboratoire de Lyon, Unité EAS, Lyon, FranceEcology and Evolution of Antibiotics Resistance (EERA) unit, CNRS UMR 3525, Institut Pasteur, AP-HP, Université Paris-Sud, Paris, FranceUniversité de Lyon - Anses, Laboratoire de Lyon, Unité Antibiorésistance et Virulence Bactériennes, Lyon, FranceMESuRS laboratory, Conservatoire national des arts et métiers, 292 rue Saint-Martin, 75003 Paris, France; PACRI unit, Institut Pasteur, Conservatoire national des arts et métiers, Paris, FranceUniversité Paris-Saclay, UVSQ, Univ. Paris-Sud, Inserm, CESP, Anti-infective evasion and pharmacoepidemiology team, F-78180 Montigny-le-Bretonneux, France; Institut Pasteur, Epidemiology and Modelling of Antibiotic Evasion unit, F-75015 Paris, FranceThe contribution of bacteria in livestock to the global burden of antimicrobial resistance raises concerns worldwide. However, the dynamics of selection and diffusion of antimicrobial resistance in farm animals are not fully understood. Here, we used veal calf fattening farms as a model system, as they are a known reservoir of Extended Spectrum β-Lactamase-producing Escherichia coli (ESBL-EC). Longitudinal data of ESBL-EC carriage and antimicrobial use (AMU) were collected from three veal calf farms during the entire fattening process. We developed 18 agent-based mechanistic models to assess different hypotheses regarding the main drivers of ESBL-EC dynamics in calves. The models were independently fitted to the longitudinal data using Markov Chain Monte Carlo and the best model was selected. Within-farm transmission between individuals and sporadic events of contamination were found to drive ESBL-EC dynamics on farms. In the absence of AMU, the median carriage duration of ESBL-EC was estimated to be 19.6 days (95% credible interval: [12.7; 33.3]). In the best model, AMU was found to influence ESBL-EC dynamics, by affecting ESBL-EC clearance rather than acquisition. This effect of AMU was estimated to decrease gradually after the end of exposure and to disappear after 62.5 days [50.0; 76.9]. Moreover, using a simulation study, we quantified the efficacy of ESBL-EC mitigation strategies. Decreasing ESBL-EC prevalence by 50% on arrival at the fattening farm reduced prevalence at slaughter age by 33.3%. Completely eliminating the use of selective antibiotics on arrival had a strong effect on average ESBL-EC prevalence (relative reduction of 77.0%), but the effect was mild if this use was only decreased by 50% compared to baseline (relative reduction of 3.3%).http://www.sciencedirect.com/science/article/pii/S2352771421000288Antimicrobial resistanceESBLLivestockCalvesEscherichia coliMathematical modelling
collection DOAJ
language English
format Article
sources DOAJ
author Jonathan Bastard
Marisa Haenni
Emilie Gay
Philippe Glaser
Jean-Yves Madec
Laura Temime
Lulla Opatowski
spellingShingle Jonathan Bastard
Marisa Haenni
Emilie Gay
Philippe Glaser
Jean-Yves Madec
Laura Temime
Lulla Opatowski
Drivers of ESBL-producing Escherichia coli dynamics in calf fattening farms: A modelling study
One Health
Antimicrobial resistance
ESBL
Livestock
Calves
Escherichia coli
Mathematical modelling
author_facet Jonathan Bastard
Marisa Haenni
Emilie Gay
Philippe Glaser
Jean-Yves Madec
Laura Temime
Lulla Opatowski
author_sort Jonathan Bastard
title Drivers of ESBL-producing Escherichia coli dynamics in calf fattening farms: A modelling study
title_short Drivers of ESBL-producing Escherichia coli dynamics in calf fattening farms: A modelling study
title_full Drivers of ESBL-producing Escherichia coli dynamics in calf fattening farms: A modelling study
title_fullStr Drivers of ESBL-producing Escherichia coli dynamics in calf fattening farms: A modelling study
title_full_unstemmed Drivers of ESBL-producing Escherichia coli dynamics in calf fattening farms: A modelling study
title_sort drivers of esbl-producing escherichia coli dynamics in calf fattening farms: a modelling study
publisher Elsevier
series One Health
issn 2352-7714
publishDate 2021-06-01
description The contribution of bacteria in livestock to the global burden of antimicrobial resistance raises concerns worldwide. However, the dynamics of selection and diffusion of antimicrobial resistance in farm animals are not fully understood. Here, we used veal calf fattening farms as a model system, as they are a known reservoir of Extended Spectrum β-Lactamase-producing Escherichia coli (ESBL-EC). Longitudinal data of ESBL-EC carriage and antimicrobial use (AMU) were collected from three veal calf farms during the entire fattening process. We developed 18 agent-based mechanistic models to assess different hypotheses regarding the main drivers of ESBL-EC dynamics in calves. The models were independently fitted to the longitudinal data using Markov Chain Monte Carlo and the best model was selected. Within-farm transmission between individuals and sporadic events of contamination were found to drive ESBL-EC dynamics on farms. In the absence of AMU, the median carriage duration of ESBL-EC was estimated to be 19.6 days (95% credible interval: [12.7; 33.3]). In the best model, AMU was found to influence ESBL-EC dynamics, by affecting ESBL-EC clearance rather than acquisition. This effect of AMU was estimated to decrease gradually after the end of exposure and to disappear after 62.5 days [50.0; 76.9]. Moreover, using a simulation study, we quantified the efficacy of ESBL-EC mitigation strategies. Decreasing ESBL-EC prevalence by 50% on arrival at the fattening farm reduced prevalence at slaughter age by 33.3%. Completely eliminating the use of selective antibiotics on arrival had a strong effect on average ESBL-EC prevalence (relative reduction of 77.0%), but the effect was mild if this use was only decreased by 50% compared to baseline (relative reduction of 3.3%).
topic Antimicrobial resistance
ESBL
Livestock
Calves
Escherichia coli
Mathematical modelling
url http://www.sciencedirect.com/science/article/pii/S2352771421000288
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