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

Abstract 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 pe...

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Main Authors: Julie Menard, Robert Goggs, Patrick Mitchell, Yufan Yang, Sarah Robbins, Rebecca J. Franklin-Guild, Anil J. Thachil, Craig Altier, Renee Anderson, Gregory G. Putzel, Holly McQueary, Laura B. Goodman
Format: Article
Language:English
Published: BMC 2022-06-01
Series:Animal Microbiome
Subjects:
Online Access:https://doi.org/10.1186/s42523-022-00178-9
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author Julie Menard
Robert Goggs
Patrick Mitchell
Yufan Yang
Sarah Robbins
Rebecca J. Franklin-Guild
Anil J. Thachil
Craig Altier
Renee Anderson
Gregory G. Putzel
Holly McQueary
Laura B. Goodman
author_facet Julie Menard
Robert Goggs
Patrick Mitchell
Yufan Yang
Sarah Robbins
Rebecca J. Franklin-Guild
Anil J. Thachil
Craig Altier
Renee Anderson
Gregory G. Putzel
Holly McQueary
Laura B. Goodman
author_sort Julie Menard
collection DOAJ
description Abstract 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
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spelling doaj.art-e1c92e8c55ad432c99cd73edbaa80c0d2022-12-22T00:55:49ZengBMCAnimal Microbiome2524-46712022-06-014111810.1186/s42523-022-00178-9Effect of antimicrobial administration on fecal microbiota of critically ill dogs: dynamics of antimicrobial resistance over timeJulie Menard0Robert Goggs1Patrick Mitchell2Yufan Yang3Sarah Robbins4Rebecca J. Franklin-Guild5Anil J. Thachil6Craig Altier7Renee Anderson8Gregory G. Putzel9Holly McQueary10Laura B. Goodman11Department of Veterinary Diagnostic and Clinical Sciences, Faculty of Veterinary Medicine, University of CalgaryDepartment of Clinical Sciences, College of Veterinary Medicine, Cornell UniversityDepartment of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell UniversityDepartment of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell UniversityDepartment of Clinical Sciences, College of Veterinary Medicine, Cornell UniversityDepartment of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell UniversityDepartment of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell UniversityDepartment of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell UniversityDepartment of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell UniversityMicrobiome Core Lab and Jill Roberts IBD Institute, Weill Cornell Medicine, Cornell UniversityDepartment of Public and Ecosystem Health, College of Veterinary Medicine, Cornell UniversityDepartment of Public and Ecosystem Health, College of Veterinary Medicine, Cornell UniversityAbstract 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 abstracthttps://doi.org/10.1186/s42523-022-00178-9Antimicrobial resistance genesVeterinarySepsisMicrobiotaEscherichia coliEnterococcus
spellingShingle Julie Menard
Robert Goggs
Patrick Mitchell
Yufan Yang
Sarah Robbins
Rebecca J. Franklin-Guild
Anil J. Thachil
Craig Altier
Renee Anderson
Gregory G. Putzel
Holly McQueary
Laura B. Goodman
Effect of antimicrobial administration on fecal microbiota of critically ill dogs: dynamics of antimicrobial resistance over time
Animal Microbiome
Antimicrobial resistance genes
Veterinary
Sepsis
Microbiota
Escherichia coli
Enterococcus
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 Antimicrobial resistance genes
Veterinary
Sepsis
Microbiota
Escherichia coli
Enterococcus
url https://doi.org/10.1186/s42523-022-00178-9
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