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Modelling the effectiveness of surveillance based on metagenomics in detecting, monitoring, and forecasting antimicrobial resistance in livestock production under economic constraints

Current surveillance of antimicrobial resistance (AMR) is mostly based on testing indicator bacteria using minimum inhibitory concentration (MIC) panels. Metagenomics has the potential to identify all known antimicrobial resistant genes (ARGs) in complex samples and thereby detect changes in the occ...

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Autores principales: Apenteng, Ofosuhene O., Aarestrup, Frank M., Vigre, Håkan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10663573/
https://www.ncbi.nlm.nih.gov/pubmed/37990114
http://dx.doi.org/10.1038/s41598-023-47754-w
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author Apenteng, Ofosuhene O.
Aarestrup, Frank M.
Vigre, Håkan
author_facet Apenteng, Ofosuhene O.
Aarestrup, Frank M.
Vigre, Håkan
author_sort Apenteng, Ofosuhene O.
collection PubMed
description Current surveillance of antimicrobial resistance (AMR) is mostly based on testing indicator bacteria using minimum inhibitory concentration (MIC) panels. Metagenomics has the potential to identify all known antimicrobial resistant genes (ARGs) in complex samples and thereby detect changes in the occurrence earlier. Here, we simulate the results of an AMR surveillance program based on metagenomics in the Danish pig population. We modelled both an increase in the occurrence of ARGs and an introduction of a new ARG in a few farms and the subsequent spread to the entire population. To make the simulation realistic, the total cost of the surveillance was constrained, and the sampling schedule was set at one pool per month with 5, 20, 50, or 100 samples. Our simulations demonstrate that a pool of 20–50 samples and a sequencing depth of 250 million fragments resulted in the shortest time to detection in both scenarios, with a time delay to detection of change of [Formula: see text] 15 months in all scenarios. Compared with culture-based surveillance, our simulation indicates that there are neither significant reductions nor increases in time to detect a change using metagenomics. The benefit of metagenomics is that it is possible to monitor all known resistance in one sampling and laboratory procedure in contrast to the current monitoring that is based on the phenotypic characterisation of selected indicator bacterial species. Therefore, overall changes in AMR in a population will be detected earlier using metagenomics due to the fact that the resistance gene does not have to be transferred to and expressed by an indicator bacteria before it is possible to detect.
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spelling pubmed-106635732023-11-21 Modelling the effectiveness of surveillance based on metagenomics in detecting, monitoring, and forecasting antimicrobial resistance in livestock production under economic constraints Apenteng, Ofosuhene O. Aarestrup, Frank M. Vigre, Håkan Sci Rep Article Current surveillance of antimicrobial resistance (AMR) is mostly based on testing indicator bacteria using minimum inhibitory concentration (MIC) panels. Metagenomics has the potential to identify all known antimicrobial resistant genes (ARGs) in complex samples and thereby detect changes in the occurrence earlier. Here, we simulate the results of an AMR surveillance program based on metagenomics in the Danish pig population. We modelled both an increase in the occurrence of ARGs and an introduction of a new ARG in a few farms and the subsequent spread to the entire population. To make the simulation realistic, the total cost of the surveillance was constrained, and the sampling schedule was set at one pool per month with 5, 20, 50, or 100 samples. Our simulations demonstrate that a pool of 20–50 samples and a sequencing depth of 250 million fragments resulted in the shortest time to detection in both scenarios, with a time delay to detection of change of [Formula: see text] 15 months in all scenarios. Compared with culture-based surveillance, our simulation indicates that there are neither significant reductions nor increases in time to detect a change using metagenomics. The benefit of metagenomics is that it is possible to monitor all known resistance in one sampling and laboratory procedure in contrast to the current monitoring that is based on the phenotypic characterisation of selected indicator bacterial species. Therefore, overall changes in AMR in a population will be detected earlier using metagenomics due to the fact that the resistance gene does not have to be transferred to and expressed by an indicator bacteria before it is possible to detect. Nature Publishing Group UK 2023-11-21 /pmc/articles/PMC10663573/ /pubmed/37990114 http://dx.doi.org/10.1038/s41598-023-47754-w Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Apenteng, Ofosuhene O.
Aarestrup, Frank M.
Vigre, Håkan
Modelling the effectiveness of surveillance based on metagenomics in detecting, monitoring, and forecasting antimicrobial resistance in livestock production under economic constraints
title Modelling the effectiveness of surveillance based on metagenomics in detecting, monitoring, and forecasting antimicrobial resistance in livestock production under economic constraints
title_full Modelling the effectiveness of surveillance based on metagenomics in detecting, monitoring, and forecasting antimicrobial resistance in livestock production under economic constraints
title_fullStr Modelling the effectiveness of surveillance based on metagenomics in detecting, monitoring, and forecasting antimicrobial resistance in livestock production under economic constraints
title_full_unstemmed Modelling the effectiveness of surveillance based on metagenomics in detecting, monitoring, and forecasting antimicrobial resistance in livestock production under economic constraints
title_short Modelling the effectiveness of surveillance based on metagenomics in detecting, monitoring, and forecasting antimicrobial resistance in livestock production under economic constraints
title_sort modelling the effectiveness of surveillance based on metagenomics in detecting, monitoring, and forecasting antimicrobial resistance in livestock production under economic constraints
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10663573/
https://www.ncbi.nlm.nih.gov/pubmed/37990114
http://dx.doi.org/10.1038/s41598-023-47754-w
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