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

James Muleme; David Musoke; Bonny E Balugaba; Stevens Kisaka; Frederick E Makumbi; Esther Buregyeya; John Bosco Isunju; Rogers Wambi; Richard K Mugambe; Clovice Kankya; Musso Munyeme; John C Ssempebwa

doi:10.1371/journal.pgph.0001344

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

PLOS Glob Public Health. 2023 Jun 13;3(6):e0001344. doi: 10.1371/journal.pgph.0001344. eCollection 2023.

Authors

Affiliations

¹ Department of Disease Control and Environmental Health, Makerere University School of Public Health, Kampala, Uganda.
² Department of Biosecurity Ecosystems and Veterinary Public Health, Makerere University College of Veterinary Medicine Animal Resources and Biosecurity, Kampala, Uganda.
³ Department of Epidemiology and Biostatistics, Makerere University School of Public Health, Kampala, Uganda.
⁴ Clinical Laboratories, Mulago National Referral Hospital, Kampala, Uganda.
⁵ Department of Disease Control, University of Zambia, Lusaka, Zambia.

Abstract

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.

Copyright: © 2023 Muleme et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Grants and funding

JM was supported by the Consortium for Advanced Research Training in Africa (CARTA). CARTA is jointly led by the African Population and Health Research Center and the University of the Witwatersrand and funded by the Carnegie Corporation of New York (Grant No. G-19-57145), Swedish International Development Cooperation Agency (Sida) (Grant No:54100113), Uppsala Monitoring Center, Norwegian Agency for Development Cooperation (Norad), and by the Wellcome Trust [reference no. 107768/Z/15/Z] and the United Kingdom Foreign, Commonwealth & Development Office, with support from the Developing Excellence in Leadership, Training and Science in Africa (DELTAS Africa) programme. In addition, the Climate Change and Infectious Diseases: One Health Approach (CIDIMOH) project under the Norwegian Programme for Capacity Development in Higher Education and Research for Development (NORHED II) supported JM to carry out part of the laboratory component during sample analysis. The statements made and views expressed are solely the responsibility of the Fellow. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.