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Microbial diversity and antimicrobial resistance in faecal samples from acute medical patients assessed through metagenomic sequencing

Antimicrobial resistance (AMR) is a threat to global public health. However, unsatisfactory approaches to directly measuring the AMR burden carried by individuals has hampered efforts to assess interventions aimed at reducing selection for AMR. Metagenomics can provide accurate detection and quantif...

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Autores principales: Yokoyama, Maho, Peto, Leon, Budgell, Eric P., Jones, Nicola, Sheridan, Elizabeth, Liu, Jane, Walker, A. Sarah, Stoesser, Nicole, Gweon, Hyun S., Llewelyn, Martin J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10019653/
https://www.ncbi.nlm.nih.gov/pubmed/36928667
http://dx.doi.org/10.1371/journal.pone.0282584
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author Yokoyama, Maho
Peto, Leon
Budgell, Eric P.
Jones, Nicola
Sheridan, Elizabeth
Liu, Jane
Walker, A. Sarah
Stoesser, Nicole
Gweon, Hyun S.
Llewelyn, Martin J.
author_facet Yokoyama, Maho
Peto, Leon
Budgell, Eric P.
Jones, Nicola
Sheridan, Elizabeth
Liu, Jane
Walker, A. Sarah
Stoesser, Nicole
Gweon, Hyun S.
Llewelyn, Martin J.
author_sort Yokoyama, Maho
collection PubMed
description Antimicrobial resistance (AMR) is a threat to global public health. However, unsatisfactory approaches to directly measuring the AMR burden carried by individuals has hampered efforts to assess interventions aimed at reducing selection for AMR. Metagenomics can provide accurate detection and quantification of AMR genes within an individual person’s faecal flora (their gut “resistome”). Using this approach, we aimed to test the hypothesis that differences in antimicrobial use across different hospitals in the United Kingdom will result in observable differences in the resistome of individual patients. Three National Health Service acute Hospital Trusts with markedly different antibiotic use and Clostridioides difficile infection rates collected faecal samples from anonymous patients which were discarded after C. difficile testing over a period of 9 to 15 months. Metagenomic DNA was extracted from these samples and sequenced using an Illumina NovaSeq 6000 platform. The resulting sequencing reads were analysed for taxonomic composition and for the presence of AMR genes. Among 683 faecal metagenomes we found huge variation between individuals in terms of taxonomic diversity (Shannon Index range 0.10–3.99) and carriage of AMR genes (Median 1.50 genes/cell/sample overall). We found no statistically significant differences in diversity (median Shannon index 2.16 (IQR 1.71–2.56), 2.15 (IQR 1.62–2.50) and 2.26 (IQR 1.55–2.51)) or carriage of AMR genes (median 1.37 genes/cell/sample (IQR 0.70–3.24), 1.70 (IQR 0.70–4.52) and 1.43 (IQR 0.55–3.71)) at the three trusts respectively. This was also the case across the sample collection period within the trusts. While we have not demonstrated differences over place or time using metagenomic sequencing of faecal discards, other sampling frameworks may be more suitable to determine whether organisational level differences in antibiotic use are associated with individual-level differences in burden of AMR carriage.
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spelling pubmed-100196532023-03-17 Microbial diversity and antimicrobial resistance in faecal samples from acute medical patients assessed through metagenomic sequencing Yokoyama, Maho Peto, Leon Budgell, Eric P. Jones, Nicola Sheridan, Elizabeth Liu, Jane Walker, A. Sarah Stoesser, Nicole Gweon, Hyun S. Llewelyn, Martin J. PLoS One Research Article Antimicrobial resistance (AMR) is a threat to global public health. However, unsatisfactory approaches to directly measuring the AMR burden carried by individuals has hampered efforts to assess interventions aimed at reducing selection for AMR. Metagenomics can provide accurate detection and quantification of AMR genes within an individual person’s faecal flora (their gut “resistome”). Using this approach, we aimed to test the hypothesis that differences in antimicrobial use across different hospitals in the United Kingdom will result in observable differences in the resistome of individual patients. Three National Health Service acute Hospital Trusts with markedly different antibiotic use and Clostridioides difficile infection rates collected faecal samples from anonymous patients which were discarded after C. difficile testing over a period of 9 to 15 months. Metagenomic DNA was extracted from these samples and sequenced using an Illumina NovaSeq 6000 platform. The resulting sequencing reads were analysed for taxonomic composition and for the presence of AMR genes. Among 683 faecal metagenomes we found huge variation between individuals in terms of taxonomic diversity (Shannon Index range 0.10–3.99) and carriage of AMR genes (Median 1.50 genes/cell/sample overall). We found no statistically significant differences in diversity (median Shannon index 2.16 (IQR 1.71–2.56), 2.15 (IQR 1.62–2.50) and 2.26 (IQR 1.55–2.51)) or carriage of AMR genes (median 1.37 genes/cell/sample (IQR 0.70–3.24), 1.70 (IQR 0.70–4.52) and 1.43 (IQR 0.55–3.71)) at the three trusts respectively. This was also the case across the sample collection period within the trusts. While we have not demonstrated differences over place or time using metagenomic sequencing of faecal discards, other sampling frameworks may be more suitable to determine whether organisational level differences in antibiotic use are associated with individual-level differences in burden of AMR carriage. Public Library of Science 2023-03-16 /pmc/articles/PMC10019653/ /pubmed/36928667 http://dx.doi.org/10.1371/journal.pone.0282584 Text en © 2023 Yokoyama et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Yokoyama, Maho
Peto, Leon
Budgell, Eric P.
Jones, Nicola
Sheridan, Elizabeth
Liu, Jane
Walker, A. Sarah
Stoesser, Nicole
Gweon, Hyun S.
Llewelyn, Martin J.
Microbial diversity and antimicrobial resistance in faecal samples from acute medical patients assessed through metagenomic sequencing
title Microbial diversity and antimicrobial resistance in faecal samples from acute medical patients assessed through metagenomic sequencing
title_full Microbial diversity and antimicrobial resistance in faecal samples from acute medical patients assessed through metagenomic sequencing
title_fullStr Microbial diversity and antimicrobial resistance in faecal samples from acute medical patients assessed through metagenomic sequencing
title_full_unstemmed Microbial diversity and antimicrobial resistance in faecal samples from acute medical patients assessed through metagenomic sequencing
title_short Microbial diversity and antimicrobial resistance in faecal samples from acute medical patients assessed through metagenomic sequencing
title_sort microbial diversity and antimicrobial resistance in faecal samples from acute medical patients assessed through metagenomic sequencing
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10019653/
https://www.ncbi.nlm.nih.gov/pubmed/36928667
http://dx.doi.org/10.1371/journal.pone.0282584
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