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Effect of antimicrobial administration on fecal microbiota of critically ill dogs: dynamics of antimicrobial resistance over time

BACKGROUND: Multidrug resistance in companion animals poses significant risks to animal and human health. Prolonged antimicrobial drug (AMD) treatment in animals is a potential source of selection pressure for antimicrobial resistance (AMR) including in the gastrointestinal microbiota. We performed...

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Autores principales: Menard, Julie, Goggs, Robert, Mitchell, Patrick, Yang, Yufan, Robbins, Sarah, Franklin-Guild, Rebecca J., Thachil, Anil J., Altier, Craig, Anderson, Renee, Putzel, Gregory G., McQueary, Holly, Goodman, Laura B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9167539/
https://www.ncbi.nlm.nih.gov/pubmed/35659110
http://dx.doi.org/10.1186/s42523-022-00178-9
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author Menard, Julie
Goggs, Robert
Mitchell, Patrick
Yang, Yufan
Robbins, Sarah
Franklin-Guild, Rebecca J.
Thachil, Anil J.
Altier, Craig
Anderson, Renee
Putzel, Gregory G.
McQueary, Holly
Goodman, Laura B.
author_facet Menard, Julie
Goggs, Robert
Mitchell, Patrick
Yang, Yufan
Robbins, Sarah
Franklin-Guild, Rebecca J.
Thachil, Anil J.
Altier, Craig
Anderson, Renee
Putzel, Gregory G.
McQueary, Holly
Goodman, Laura B.
author_sort Menard, Julie
collection PubMed
description BACKGROUND: Multidrug resistance in companion animals poses significant risks to animal and human health. Prolonged antimicrobial drug (AMD) treatment in animals is a potential source of selection pressure for antimicrobial resistance (AMR) including in the gastrointestinal microbiota. We performed a prospective study of dogs treated for septic peritonitis, pyometra, or bacterial pneumonia and collected repeated fecal samples over 60 days. Bacterial cultures and direct molecular analyses of fecal samples were performed including targeted resistance gene profiling. RESULTS: Resistant Escherichia coli increased after 1 week of treatment (D1:21.4% vs. D7:67.9% P < 0.001) and returned to baseline proportions by D60 (D7:67.9% vs D60:42.9%, P = 0.04). Dogs with septic peritonitis were hospitalized significantly longer than those with pneumonia or pyometra. Based on genetic analysis, Simpson’s diversity index significantly decreased after 1 week of treatment (D1 to D7, P = 0.008), followed by a gradual increase to day 60 (D1 and D60, P = 0.4). Detection of CTX-M was associated with phenotypic resistance to third-generation cephalosporins in E. coli (OR 12.1, 3.3–68.0, P < 0.001). Lincosamide and macrolide-resistance genes were more frequently recovered on days 14 and 28 compared to day 1 (P = 0.002 and P = 0.004 respectively). CONCLUSION: AMR was associated with prescribed drugs but also developed against AMDs not administered during the study. Companion animals may be reservoirs of zoonotic multidrug resistant pathogens, suggesting that veterinary AMD stewardship and surveillance efforts should be prioritized. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-022-00178-9.
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spelling pubmed-91675392022-06-06 Effect of antimicrobial administration on fecal microbiota of critically ill dogs: dynamics of antimicrobial resistance over time Menard, Julie Goggs, Robert Mitchell, Patrick Yang, Yufan Robbins, Sarah Franklin-Guild, Rebecca J. Thachil, Anil J. Altier, Craig Anderson, Renee Putzel, Gregory G. McQueary, Holly Goodman, Laura B. Anim Microbiome Research Article BACKGROUND: Multidrug resistance in companion animals poses significant risks to animal and human health. Prolonged antimicrobial drug (AMD) treatment in animals is a potential source of selection pressure for antimicrobial resistance (AMR) including in the gastrointestinal microbiota. We performed a prospective study of dogs treated for septic peritonitis, pyometra, or bacterial pneumonia and collected repeated fecal samples over 60 days. Bacterial cultures and direct molecular analyses of fecal samples were performed including targeted resistance gene profiling. RESULTS: Resistant Escherichia coli increased after 1 week of treatment (D1:21.4% vs. D7:67.9% P < 0.001) and returned to baseline proportions by D60 (D7:67.9% vs D60:42.9%, P = 0.04). Dogs with septic peritonitis were hospitalized significantly longer than those with pneumonia or pyometra. Based on genetic analysis, Simpson’s diversity index significantly decreased after 1 week of treatment (D1 to D7, P = 0.008), followed by a gradual increase to day 60 (D1 and D60, P = 0.4). Detection of CTX-M was associated with phenotypic resistance to third-generation cephalosporins in E. coli (OR 12.1, 3.3–68.0, P < 0.001). Lincosamide and macrolide-resistance genes were more frequently recovered on days 14 and 28 compared to day 1 (P = 0.002 and P = 0.004 respectively). CONCLUSION: AMR was associated with prescribed drugs but also developed against AMDs not administered during the study. Companion animals may be reservoirs of zoonotic multidrug resistant pathogens, suggesting that veterinary AMD stewardship and surveillance efforts should be prioritized. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-022-00178-9. BioMed Central 2022-06-04 /pmc/articles/PMC9167539/ /pubmed/35659110 http://dx.doi.org/10.1186/s42523-022-00178-9 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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 Research Article
Menard, Julie
Goggs, Robert
Mitchell, Patrick
Yang, Yufan
Robbins, Sarah
Franklin-Guild, Rebecca J.
Thachil, Anil J.
Altier, Craig
Anderson, Renee
Putzel, Gregory G.
McQueary, Holly
Goodman, Laura B.
Effect of antimicrobial administration on fecal microbiota of critically ill dogs: dynamics of antimicrobial resistance over time
title Effect of antimicrobial administration on fecal microbiota of critically ill dogs: dynamics of antimicrobial resistance over time
title_full Effect of antimicrobial administration on fecal microbiota of critically ill dogs: dynamics of antimicrobial resistance over time
title_fullStr Effect of antimicrobial administration on fecal microbiota of critically ill dogs: dynamics of antimicrobial resistance over time
title_full_unstemmed Effect of antimicrobial administration on fecal microbiota of critically ill dogs: dynamics of antimicrobial resistance over time
title_short Effect of antimicrobial administration on fecal microbiota of critically ill dogs: dynamics of antimicrobial resistance over time
title_sort effect of antimicrobial administration on fecal microbiota of critically ill dogs: dynamics of antimicrobial resistance over time
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9167539/
https://www.ncbi.nlm.nih.gov/pubmed/35659110
http://dx.doi.org/10.1186/s42523-022-00178-9
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