Epidemiological connectivity between humans and animals across an urban landscape

Urbanization is predicted to be a key driver of disease emergence through human exposure to novel, animal-borne pathogens. However, while we suspect that urban landscapes are primed to expose people to novel animal-borne diseases, evidence for the mechanisms by which this occurs is lacking. To address this, we studied how bacterial genes are shared between wild animals, livestock, and humans (n = 1,428) across Nairobi, Kenya—one of the world’s most rapidly developing cities. Applying a multilayer network framework, we show that low biodiversity (of both natural habitat and vertebrate wildlife communities), coupled with livestock management practices and more densely populated urban environments, promotes sharing of Escherichia coli–borne bacterial mobile genetic elements between animals and humans. These results provide empirical support for hypotheses linking resource provision, the biological simplification of urban landscapes, and human and livestock demography to urban dynamics of cross-species pathogen transmission at a landscape scale. Urban areas where high densities of people and livestock live in close association with synanthropes (species such as rodents that are more competent reservoirs for zoonotic pathogens) should be prioritized for disease surveillance and control

Genomic epidemiology of Escherichia coli:Antimicrobial resistance through a One Health lens in sympatric humans, livestock and peri-domestic wildlife in Nairobi, Kenya

BackgroundLivestock systems have been proposed as a reservoir for antimicrobial-resistant (AMR) bacteria and AMR genetic determinants that may infect or colonise humans, yet quantitative evidence regarding their epidemiological role remains lacking. Here, we used a combination of genomics, epidemiology and ecology to investigate patterns of AMR gene carriage in Escherichia coli, regarded as a sentinel organism.MethodsWe conducted a structured epidemiological survey of 99 households across Nairobi, Kenya, and whole genome sequenced E. coli isolates from 311 human, 606 livestock and 399 wildlife faecal samples. We used statistical models to investigate the prevalence of AMR carriage and characterise AMR gene diversity and structure of AMR genes in different host populations across the city. We also investigated household-level risk factors for the exchange of AMR genes between sympatric humans and livestock.ResultsWe detected 56 unique acquired genes along with 13 point mutations present in variable proportions in human and animal isolates, known to confer resistance to nine antibiotic classes. We find that AMR gene community composition is not associated with host species, but AMR genes were frequently co-located, potentially enabling the acquisition and dispersal of multi-drug resistance in a single step. We find that whilst keeping livestock had no influence on human AMR gene carriage, the potential for AMR transmission across human-livestock interfaces is greatest when manure is poorly disposed of and in larger households.ConclusionsFindings of widespread carriage of AMR bacteria in human and animal populations, including in long-distance wildlife species, in community settings highlight the value of evidence-based surveillance to address antimicrobial resistance on a global scale. Our genomic analysis provided an in-depth understanding of AMR determinants at the interfaces of One Health sectors that will inform AMR prevention and control

Population genomics of <i>Escherichia coli</i> in livestock-keeping households across a rapidly developing urban landscape

Quantitative evidence for the risk of zoonoses and the spread of antimicrobial resistance remains lacking. Here, as part of the UrbanZoo project, we sampled Escherichia coli from humans, livestock and peri-domestic wildlife in 99 households across Nairobi, Kenya, to investigate its distribution among host species in this rapidly developing urban landscape. We performed whole-genome sequencing of 1,338 E. coli isolates and found that the diversity and sharing patterns of E. coli were heavily structured by household and strongly shaped by host type. We also found evidence for inter-household and inter-host sharing and, importantly, between humans and animals, although this occurs much less frequently. Resistome similarity was differently distributed across host and household, consistent with being driven by shared exposure to antimicrobials. Our results indicate that a large, epidemiologically structured sampling framework combined with WGS is needed to uncover strain-sharing events among different host populations in complex environments and the major contributing pathways that could ultimately drive the emergence of zoonoses and the spread of antimicrobial resistance

Genomic epidemiology of Escherichia coli: antimicrobial resistance through a One Health lens in sympatric humans, livestock and peri-domestic wildlife in Nairobi, Kenya

&lt;p&gt;&lt;strong&gt;&lt;span&gt;Background&lt;/span&gt;&lt;/strong&gt;&lt;/p&gt; &lt;p&gt;&lt;span&gt;Livestock systems have been proposed as a reservoir for antimicrobial-resistant (AMR) bacteria and AMR genetic determinants that may infect or colonise humans, yet quantitative evidence regarding their epidemiological role remains lacking. Here we used a combination of genomics, epidemiology and ecology to investigate patterns of AMR gene carriage in &lt;em&gt;Escherichia&lt;/em&gt; &lt;em&gt;coli&lt;/em&gt;, regarded as a sentinel organism.&lt;/span&gt;&lt;/p&gt; &lt;p&gt;&lt;strong&gt;&lt;span&gt;Methods&lt;/span&gt;&lt;/strong&gt;&lt;/p&gt; &lt;p&gt;&lt;span&gt;We conducted a structured epidemiological survey of 99 households across Nairobi, Kenya, and whole genome sequenced &lt;em&gt;E&lt;/em&gt;. &lt;em&gt;coli&lt;/em&gt; isolates from 311 human, 606 livestock, and 399 wildlife faecal samples. We used statistical models to investigate the prevalence of AMR carriage and characterise AMR gene diversity and structure of AMR genes in different host populations across the city. We also investigated house-hold level risk factors for exchange of AMR genes between sympatric humans and livestock.&lt;/span&gt;&lt;/p&gt; &lt;p&gt;&lt;strong&gt;&lt;span&gt;Findings&lt;/span&gt;&lt;/strong&gt;&lt;/p&gt; &lt;p&gt;&lt;span&gt;We detected 56 unique acquired genes along with 13 point mutations present in variable proportions in human and animal isolates, known to confer resistance to nine antibiotic classes. We find that AMR gene community composition is not associated with host species, but AMR genes were frequently co-located, potentially enabling the acquisition and dispersal of multi-drug resistance in a single step. We find that whilst keeping livestock had no influence on human AMR gene carriage, the potential for AMR transmission across human-livestock interfaces is greatest when manure is poorly disposed of and in larger households.&lt;/span&gt;&lt;/p&gt; &lt;p&gt;&lt;strong&gt;&lt;span&gt;Conclusions&lt;/span&gt;&lt;/strong&gt;&lt;/p&gt; &lt;p&gt;&lt;span&gt;Findings of widespread carriage of AMR bacteria in human and animal populations, including in long-distance wildlife species, in community settings, highlight the value of evidence-based surveillance to address antimicrobial resistance on a global scale. Our genomic analysis provided in-depth understanding of AMR determinants at the interfaces of One-Health sectors that will inform AMR prevention and control.&lt;/span&gt;&lt;/p&gt;&lt;p&gt;Funding provided by: Medical Research Council&lt;br&gt;Crossref Funder Registry ID: https://ror.org/03x94j517&lt;br&gt;Award Number: G1100783/1&lt;/p&gt

Epidemiological connectivity between humans and animals across an urban landscape

Urbanization is predicted to be a key driver of disease emergence through human exposure to novel, animal-borne pathogens. However, while we suspect that urban landscapes are primed to expose people to novel animal-borne diseases, evidence for the mechanisms by which this occurs is lacking. To address this, we studied how bacterial genes are shared between wild animals, livestock, and humans (n = 1,428) across Nairobi, Kenya—one of the world’s most rapidly developing cities. Applying a multilayer network framework, we show that low biodiversity (of both natural habitat and vertebrate wildlife communities), coupled with livestock management practices and more densely populated urban environments, promotes sharing of Escherichia coli –borne bacterial mobile genetic elements between animals and humans. These results provide empirical support for hypotheses linking resource provision, the biological simplification of urban landscapes, and human and livestock demography to urban dynamics of cross-species pathogen transmission at a landscape scale. Urban areas where high densities of people and livestock live in close association with synanthropes (species such as rodents that are more competent reservoirs for zoonotic pathogens) should be prioritized for disease surveillance and control. </jats:p

Landscape genomics of Escherichia coli in livestock-keeping households across a rapidly developing urban city

Abstract The keeping of livestock has been posited as a risk factor for the emergence of zoonoses and the spread of antimicrobial resistance. However, quantitative evidence regarding the major sources of pathogenic and drug-resistant bacteria and transmission routes between hosts remains lacking. In the largest epidemiological study of this nature to date, we sampled Escherichia coli from humans, livestock, food, wildlife and the environment of 99 households across Nairobi, Kenya to gain a deeper understanding of sharing of bacteria among hosts and potential reservoirs. By analysing whole genome sequencing data from 1,338 E. coli isolates, we reconstruct sharing patterns for the sampled E. coli and its antimicrobial resistance determinants. We find that the diversity and sharing patterns of E. coli is heavily structured by household, which is the primary epidemiological interface for bacterial strain sharing. Strain sharing within households was strongly shaped by host type. We also find evidence for inter-household and inter-host sharing, and importantly, between humans and animals, although this occurs much less frequently. We find similar strain sharing patterns for the E. coli accessory genome, suggesting that it is shaped by recent evolutionary history and is strongly associated with the core genome. Resistome similarity, however, were quite differently distributed across host and household, consistent with their being driven by shared exposure to antimicrobials. Our results indicate that there is potential for the exchange of bacteria between humans, livestock and wildlife in the same household in a tropical urban setting, with wider mixing occurring over a period of months or years, but this does not drive the distribution of antimicrobial resistance.</jats:p

Population genomics of Escherichia coli in livestock-keeping households across a rapidly developing urban landscape

AbstractQuantitative evidence for the risk of zoonoses and the spread of antimicrobial resistance remains lacking. Here, as part of the UrbanZoo project, we sampled Escherichia coli from humans, livestock and peri-domestic wildlife in 99 households across Nairobi, Kenya, to investigate its distribution among host species in this rapidly developing urban landscape. We performed whole-genome sequencing of 1,338 E. coli isolates and found that the diversity and sharing patterns of E. coli were heavily structured by household and strongly shaped by host type. We also found evidence for inter-household and inter-host sharing and, importantly, between humans and animals, although this occurs much less frequently. Resistome similarity was differently distributed across host and household, consistent with being driven by shared exposure to antimicrobials. Our results indicate that a large, epidemiologically structured sampling framework combined with WGS is needed to uncover strain-sharing events among different host populations in complex environments and the major contributing pathways that could ultimately drive the emergence of zoonoses and the spread of antimicrobial resistance.</jats:p

Genomic epidemiology of Escherichia coli: antimicrobial resistance through a One Health lens in sympatric humans, livestock and peri-domestic wildlife in Nairobi, Kenya

Background Livestock systems have been proposed as a reservoir for antimicrobial-resistant (AMR) bacteria and AMR genetic determinants that may infect or colonise humans, yet quantitative evidence regarding their epidemiological role remains lacking. Here we used a combination of genomics, epidemiology and ecology to investigate patterns of AMR gene carriage in Escherichia coli, regarded as a sentinel organism. Methods We conducted a structured epidemiological survey of 99 households across Nairobi, Kenya, and whole genome sequenced E. coli isolates from 311 human, 606 livestock, and 399 wildlife faecal samples. We used statistical models to investigate the prevalence of AMR carriage and characterise AMR gene diversity and structure of AMR genes in different host populations across the city. We also investigated house-hold level risk factors for exchange of AMR genes between sympatric humans and livestock. Findings We detected 56 unique acquired genes along with 13 point mutations present in variable proportions in human and animal isolates, known to confer resistance to nine antibiotic classes. We find that AMR gene community composition is not associated with host species, but AMR genes were frequently co-located, potentially enabling the acquisition and dispersal of multi-drug resistance in a single step. We find that whilst keeping livestock had no influence on human AMR gene carriage, the potential for AMR transmission across human-livestock interfaces is greatest when manure is poorly disposed of and in larger households. Conclusions Findings of widespread carriage of AMR bacteria in human and animal populations, including in long-distance wildlife species, in community settings, highlight the value of evidence-based surveillance to address antimicrobial resistance on a global scale. Our genomic analysis provided in-depth understanding of AMR determinants at the interfaces of One-Health sectors that will inform AMR prevention and control. Data contains sample ID, source types (Source_Level1 contains the granular species group, Source_Level2 contains grouping of the species data further into humans, monogastrics which include pigs and rabbits, ruminants which include cattle, sheep, and goats, w_avian which includes wildlife avian i.e. birds, w_bats which include wildlife bats i.e. bats; Source_Level3 contains three groups, humans, livestock, and wildlife; Source_Level4 contains functional groups humans, livestock birds, livestock mammals, wild bird), livestock type present in the household, and predicted antibiotic resistance genes.Muloi, Dishon; Hassel, James; Wee, Bryan et al. (2024). Genomic epidemiology of Escherichia coli: antimicrobial resistance through a One Health lens in sympatric humans, livestock and peri-domestic wildlife in Nairobi, Kenya [Dataset]. Dryad. https://doi.org/10.5061/dryad.qnk98sfk

Additional file 1 of Genomic epidemiology of Escherichia coli: antimicrobial resistance through a One Health lens in sympatric humans, livestock and peri-domestic wildlife in Nairobi, Kenya

Additional file 1