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Epidemiology of extended-spectrum beta-lactamase-producing Escherichia coli at the human-animal-environment interface in a farming community of central Uganda

BACKGROUND: Extended-spectrum beta-lactamase-producing Escherichia coli (ESBL-Ec) represents a significant global public health concern. The epidemiology of ESBL-Ec in Uganda is not well understood although it is harbored by humans, animals, and the environment. This study explains the epidemiology...

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Autores principales: Muleme, James, Musoke, David, Balugaba, Bonny E., Kisaka, Stevens, Makumbi, Frederick E., Buregyeya, Esther, Isunju, John Bosco, Wambi, Rogers, Mugambe, Richard K., Kankya, Clovice, Munyeme, Musso, Ssempebwa, John C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10270331/
https://www.ncbi.nlm.nih.gov/pubmed/37310955
http://dx.doi.org/10.1371/journal.pgph.0001344
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author Muleme, James
Musoke, David
Balugaba, Bonny E.
Kisaka, Stevens
Makumbi, Frederick E.
Buregyeya, Esther
Isunju, John Bosco
Wambi, Rogers
Mugambe, Richard K.
Kankya, Clovice
Munyeme, Musso
Ssempebwa, John C.
author_facet Muleme, James
Musoke, David
Balugaba, Bonny E.
Kisaka, Stevens
Makumbi, Frederick E.
Buregyeya, Esther
Isunju, John Bosco
Wambi, Rogers
Mugambe, Richard K.
Kankya, Clovice
Munyeme, Musso
Ssempebwa, John C.
author_sort Muleme, James
collection PubMed
description BACKGROUND: Extended-spectrum beta-lactamase-producing Escherichia coli (ESBL-Ec) represents a significant global public health concern. The epidemiology of ESBL-Ec in Uganda is not well understood although it is harbored by humans, animals, and the environment. This study explains the epidemiology of ESBL-Ec using a one health approach in selected farming households in Wakiso district, Uganda. METHODOLOGY: Environmental, human, and animal samples were collected from 104 households. Additional data were obtained using observation checklists and through interviews with household members using a semi-structured questionnaire. Surface swabs, soil, water, human and animal fecal samples were introduced onto ESBL chromogenic agar. The isolates were identified using biochemical tests and double-disk synergy tests. To assess associations, prevalence ratios (PRs) were computed using a generalized linear model (GLM) analysis with modified Poisson and a log link with robust standard errors in R software. RESULTS: Approximately 83% (86/104) households had at least one positive ESBL-Ec isolate. The overall prevalence of ESBL-Ec at the human-animal-environment interface was approximately 25.0% (95% CI: 22.7–28.3). Specifically, humans, animals and the environment had an ESBL-Ec prevalence of 35.4%, 55.4%, and 9.2% respectively. Having visitors (adj PR = 1.19, 95% CI: 1.04–1.36), utilizing veterinary services (adj PR = 1.39, 95% CI: 1.20–1.61) and using animal waste for gardening (adj PR = 1.29, 95% CI: 1.05–1.60) were positively associated with household ESBL-Ec contamination. Covering the drinking water container with a lid (adj PR = 0.84 95% CI: 0.73–0.96) was associated with absence of ESBL-Ec in a household. CONCLUSION: There is wider dissemination of ESBL-Ec in the environment, humans, and animals, indicating poor infection prevention and control (IPC) measures in the area. Improved collaborative one health mitigation strategies such as safe water chain, farm biosecurity, household and facility-based IPC measures are recommended to reduce the burden of antimicrobial resistance at community level.
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spelling pubmed-102703312023-06-16 Epidemiology of extended-spectrum beta-lactamase-producing Escherichia coli at the human-animal-environment interface in a farming community of central Uganda Muleme, James Musoke, David Balugaba, Bonny E. Kisaka, Stevens Makumbi, Frederick E. Buregyeya, Esther Isunju, John Bosco Wambi, Rogers Mugambe, Richard K. Kankya, Clovice Munyeme, Musso Ssempebwa, John C. PLOS Glob Public Health Research Article BACKGROUND: Extended-spectrum beta-lactamase-producing Escherichia coli (ESBL-Ec) represents a significant global public health concern. The epidemiology of ESBL-Ec in Uganda is not well understood although it is harbored by humans, animals, and the environment. This study explains the epidemiology of ESBL-Ec using a one health approach in selected farming households in Wakiso district, Uganda. METHODOLOGY: Environmental, human, and animal samples were collected from 104 households. Additional data were obtained using observation checklists and through interviews with household members using a semi-structured questionnaire. Surface swabs, soil, water, human and animal fecal samples were introduced onto ESBL chromogenic agar. The isolates were identified using biochemical tests and double-disk synergy tests. To assess associations, prevalence ratios (PRs) were computed using a generalized linear model (GLM) analysis with modified Poisson and a log link with robust standard errors in R software. RESULTS: Approximately 83% (86/104) households had at least one positive ESBL-Ec isolate. The overall prevalence of ESBL-Ec at the human-animal-environment interface was approximately 25.0% (95% CI: 22.7–28.3). Specifically, humans, animals and the environment had an ESBL-Ec prevalence of 35.4%, 55.4%, and 9.2% respectively. Having visitors (adj PR = 1.19, 95% CI: 1.04–1.36), utilizing veterinary services (adj PR = 1.39, 95% CI: 1.20–1.61) and using animal waste for gardening (adj PR = 1.29, 95% CI: 1.05–1.60) were positively associated with household ESBL-Ec contamination. Covering the drinking water container with a lid (adj PR = 0.84 95% CI: 0.73–0.96) was associated with absence of ESBL-Ec in a household. CONCLUSION: There is wider dissemination of ESBL-Ec in the environment, humans, and animals, indicating poor infection prevention and control (IPC) measures in the area. Improved collaborative one health mitigation strategies such as safe water chain, farm biosecurity, household and facility-based IPC measures are recommended to reduce the burden of antimicrobial resistance at community level. Public Library of Science 2023-06-13 /pmc/articles/PMC10270331/ /pubmed/37310955 http://dx.doi.org/10.1371/journal.pgph.0001344 Text en © 2023 Muleme 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
Muleme, James
Musoke, David
Balugaba, Bonny E.
Kisaka, Stevens
Makumbi, Frederick E.
Buregyeya, Esther
Isunju, John Bosco
Wambi, Rogers
Mugambe, Richard K.
Kankya, Clovice
Munyeme, Musso
Ssempebwa, John C.
Epidemiology of extended-spectrum beta-lactamase-producing Escherichia coli at the human-animal-environment interface in a farming community of central Uganda
title Epidemiology of extended-spectrum beta-lactamase-producing Escherichia coli at the human-animal-environment interface in a farming community of central Uganda
title_full Epidemiology of extended-spectrum beta-lactamase-producing Escherichia coli at the human-animal-environment interface in a farming community of central Uganda
title_fullStr Epidemiology of extended-spectrum beta-lactamase-producing Escherichia coli at the human-animal-environment interface in a farming community of central Uganda
title_full_unstemmed Epidemiology of extended-spectrum beta-lactamase-producing Escherichia coli at the human-animal-environment interface in a farming community of central Uganda
title_short Epidemiology of extended-spectrum beta-lactamase-producing Escherichia coli at the human-animal-environment interface in a farming community of central Uganda
title_sort epidemiology of extended-spectrum beta-lactamase-producing escherichia coli at the human-animal-environment interface in a farming community of central uganda
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10270331/
https://www.ncbi.nlm.nih.gov/pubmed/37310955
http://dx.doi.org/10.1371/journal.pgph.0001344
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