Clinically relevant antimicrobial resistance at the wildlife–livestock–human interface in Nairobi: An epidemiological study

Background Antimicrobial resistance is one of the great challenges facing global health security in the modern era. Wildlife, particularly those that use urban environments, are an important but understudied component of epidemiology of antimicrobial resistance. We investigated antimicrobial resista...

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Main Authors: Hassell, James M., Ward, M.J., Muloi, Dishon M., Bettridge, Judy M., Robinson, Timothy P., Kariuki, S., Ogendo, A., Kiiru, J., Imboma, Titus, Kang'ethe, Erastus K., Öghren, E.M., Williams, N.J., Begon, M., Woolhouse, Mark E.J., Fèvre, Eric M.
Format: Journal Article
Language:Inglés
Published: Elsevier 2019
Subjects:
Online Access:https://hdl.handle.net/10568/101623
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author Hassell, James M.
Ward, M.J.
Muloi, Dishon M.
Bettridge, Judy M.
Robinson, Timothy P.
Kariuki, S.
Ogendo, A.
Kiiru, J.
Imboma, Titus
Kang'ethe, Erastus K.
Öghren, E.M.
Williams, N.J.
Begon, M.
Woolhouse, Mark E.J.
Fèvre, Eric M.
author_browse Begon, M.
Bettridge, Judy M.
Fèvre, Eric M.
Hassell, James M.
Imboma, Titus
Kang'ethe, Erastus K.
Kariuki, S.
Kiiru, J.
Muloi, Dishon M.
Ogendo, A.
Robinson, Timothy P.
Ward, M.J.
Williams, N.J.
Woolhouse, Mark E.J.
Öghren, E.M.
author_facet Hassell, James M.
Ward, M.J.
Muloi, Dishon M.
Bettridge, Judy M.
Robinson, Timothy P.
Kariuki, S.
Ogendo, A.
Kiiru, J.
Imboma, Titus
Kang'ethe, Erastus K.
Öghren, E.M.
Williams, N.J.
Begon, M.
Woolhouse, Mark E.J.
Fèvre, Eric M.
author_sort Hassell, James M.
collection Repository of Agricultural Research Outputs (CGSpace)
description Background Antimicrobial resistance is one of the great challenges facing global health security in the modern era. Wildlife, particularly those that use urban environments, are an important but understudied component of epidemiology of antimicrobial resistance. We investigated antimicrobial resistance overlap between sympatric wildlife, humans, livestock, and their shared environment across the developing city of Nairobi, Kenya. We use these data to examine the role of urban wildlife in the spread of clinically relevant antimicrobial resistance. Methods 99 households across Nairobi were randomly selected on the basis of socioeconomic stratification. A detailed survey was administered to household occupants, and samples (n=2102) were collected from the faeces of 75 wildlife species inhabiting household compounds (ie, the household and its perimeter; n=849), 13 livestock species (n=656), and humans (n=333), and from the external environment (n=288). Escherichia coli, our sentinel organism, was cultured and a single isolate from each sample tested for sensitivity to 13 antibiotics. Diversity of antimicrobial resistant phenotypes was compared between urban wildlife, humans, livestock, and the environment, to investigate whether wildlife are a net source for antimicrobial resistance in Nairobi. Generalised linear mixed models were used to determine whether the prevalence of antimicrobial resistant phenotypes and multidrug-resistant E coli carriage in urban wildlife is linked to variation in ecological traits, such as foraging behaviour, and to determine household-level risk factors for sharing of antimicrobial resistance between humans, wildlife, and livestock. Findings E coli were isolated from 485 samples collected from wildlife between Sept 6,2015, and Sept 28, 2016. Wildlife carried a low prevalence of E coli isolates susceptible to all antibiotics tested (45 [9%] of 485 samples) and a high prevalence of clinically relevant multidrug resistance (252 [52%] of 485 samples), which varied between taxa and by foraging traits. Multiple isolates were resistant to one agent from at least seven antimicrobial classes tested for, and a single isolate was resistant to all antibiotics tested for in the study. The phenotypic diversity of antimicrobial-resistant E coli in wildlife was lower than in livestock, humans, and the environment. Within household compounds, statistical models identified two interfaces for exchange of antimicrobial resistance: between both rodents, humans and their rubbish, and seed-eating birds, humans and their rubbish; and between seed-eating birds, cattle, and bovine manure. Interpretation Urban wildlife carry a high burden of clinically relevant antimicrobial-resistant E coli in Nairobi, exhibiting resistance to drugs considered crucial for human medicine by WHO. Identifiable traits of the wildlife contribute to this exposure; however, compared with humans, livestock, and the environment, low phenotypic diversity in wildlife is consistent with the hypothesis that wildlife are a net sink rather than source of clinically relevant resistance. Wildlife that interact closely with humans, livestock, and both human and livestock waste within households, are exposed to more antimicrobial resistant phenotypes, and could therefore act as conduits for the dissemination of clinically relevant antimicrobial resistance to the wider environment. These results provide novel insight into the broader epidemiology of antimicrobial resistance in complex urban environments, characteristic of lower-middle-income countries.
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spelling CGSpace1016232024-08-27T10:36:32Z Clinically relevant antimicrobial resistance at the wildlife–livestock–human interface in Nairobi: An epidemiological study Hassell, James M. Ward, M.J. Muloi, Dishon M. Bettridge, Judy M. Robinson, Timothy P. Kariuki, S. Ogendo, A. Kiiru, J. Imboma, Titus Kang'ethe, Erastus K. Öghren, E.M. Williams, N.J. Begon, M. Woolhouse, Mark E.J. Fèvre, Eric M. epidemiology health livestock wildlife antimicrobial resistance Background Antimicrobial resistance is one of the great challenges facing global health security in the modern era. Wildlife, particularly those that use urban environments, are an important but understudied component of epidemiology of antimicrobial resistance. We investigated antimicrobial resistance overlap between sympatric wildlife, humans, livestock, and their shared environment across the developing city of Nairobi, Kenya. We use these data to examine the role of urban wildlife in the spread of clinically relevant antimicrobial resistance. Methods 99 households across Nairobi were randomly selected on the basis of socioeconomic stratification. A detailed survey was administered to household occupants, and samples (n=2102) were collected from the faeces of 75 wildlife species inhabiting household compounds (ie, the household and its perimeter; n=849), 13 livestock species (n=656), and humans (n=333), and from the external environment (n=288). Escherichia coli, our sentinel organism, was cultured and a single isolate from each sample tested for sensitivity to 13 antibiotics. Diversity of antimicrobial resistant phenotypes was compared between urban wildlife, humans, livestock, and the environment, to investigate whether wildlife are a net source for antimicrobial resistance in Nairobi. Generalised linear mixed models were used to determine whether the prevalence of antimicrobial resistant phenotypes and multidrug-resistant E coli carriage in urban wildlife is linked to variation in ecological traits, such as foraging behaviour, and to determine household-level risk factors for sharing of antimicrobial resistance between humans, wildlife, and livestock. Findings E coli were isolated from 485 samples collected from wildlife between Sept 6,2015, and Sept 28, 2016. Wildlife carried a low prevalence of E coli isolates susceptible to all antibiotics tested (45 [9%] of 485 samples) and a high prevalence of clinically relevant multidrug resistance (252 [52%] of 485 samples), which varied between taxa and by foraging traits. Multiple isolates were resistant to one agent from at least seven antimicrobial classes tested for, and a single isolate was resistant to all antibiotics tested for in the study. The phenotypic diversity of antimicrobial-resistant E coli in wildlife was lower than in livestock, humans, and the environment. Within household compounds, statistical models identified two interfaces for exchange of antimicrobial resistance: between both rodents, humans and their rubbish, and seed-eating birds, humans and their rubbish; and between seed-eating birds, cattle, and bovine manure. Interpretation Urban wildlife carry a high burden of clinically relevant antimicrobial-resistant E coli in Nairobi, exhibiting resistance to drugs considered crucial for human medicine by WHO. Identifiable traits of the wildlife contribute to this exposure; however, compared with humans, livestock, and the environment, low phenotypic diversity in wildlife is consistent with the hypothesis that wildlife are a net sink rather than source of clinically relevant resistance. Wildlife that interact closely with humans, livestock, and both human and livestock waste within households, are exposed to more antimicrobial resistant phenotypes, and could therefore act as conduits for the dissemination of clinically relevant antimicrobial resistance to the wider environment. These results provide novel insight into the broader epidemiology of antimicrobial resistance in complex urban environments, characteristic of lower-middle-income countries. 2019-06 2019-06-20T13:41:55Z 2019-06-20T13:41:55Z Journal Article https://hdl.handle.net/10568/101623 en Open Access Elsevier Hassell, J.M., Ward, M.J., Muloi, D., Bettridge, J.M., Robinson, T.P., Kariuki, S., Ogendo, A., Kiiru, J., Imboma, T., Kang'ethe, E.K., Öghren, E.M., Williams, N.J., Begon, M., Woolhouse, M.E.J. and Fèvre, E.M. 2019. Clinically relevant antimicrobial resistance at the wildlife–livestock–human interface in Nairobi: An epidemiological study. Lancet Planetary Health 3(6): e259–e269.
spellingShingle epidemiology
health
livestock
wildlife
antimicrobial resistance
Hassell, James M.
Ward, M.J.
Muloi, Dishon M.
Bettridge, Judy M.
Robinson, Timothy P.
Kariuki, S.
Ogendo, A.
Kiiru, J.
Imboma, Titus
Kang'ethe, Erastus K.
Öghren, E.M.
Williams, N.J.
Begon, M.
Woolhouse, Mark E.J.
Fèvre, Eric M.
Clinically relevant antimicrobial resistance at the wildlife–livestock–human interface in Nairobi: An epidemiological study
title Clinically relevant antimicrobial resistance at the wildlife–livestock–human interface in Nairobi: An epidemiological study
title_full Clinically relevant antimicrobial resistance at the wildlife–livestock–human interface in Nairobi: An epidemiological study
title_fullStr Clinically relevant antimicrobial resistance at the wildlife–livestock–human interface in Nairobi: An epidemiological study
title_full_unstemmed Clinically relevant antimicrobial resistance at the wildlife–livestock–human interface in Nairobi: An epidemiological study
title_short Clinically relevant antimicrobial resistance at the wildlife–livestock–human interface in Nairobi: An epidemiological study
title_sort clinically relevant antimicrobial resistance at the wildlife livestock human interface in nairobi an epidemiological study
topic epidemiology
health
livestock
wildlife
antimicrobial resistance
url https://hdl.handle.net/10568/101623
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