Dataset Information

Bacterial strain sharing between humans, animals, and the environment among urban households.

ABSTRACT: Identifying bacterial transmission pathways is crucial to inform strategies aimed at curbing the spread of pathogenic and antibiotic-resistant bacteria, especially in rapidly urbanizing low- and middle-income countries. In this study, we assessed bacterial strain-sharing and dissemination of antibiotic resistance across humans, domesticated poultry, canines, household soil, and drinking water in urban informal settlements in Nairobi, Kenya. We collected 321 samples from 50 households and performed Pooling Isolated Colonies-seq (PIC-seq) by sequencing pools of up to five Escherichia coli colonies per sample to capture strain diversity, strain-sharing patterns, and overlap of antibiotic-resistant genes (ARGs). Bacterial strains isolated from the household environment carried clinically relevant ARGs, reinforcing the role of the environment in antibiotic resistance dissemination. Strain-sharing rates and resistome similarities across sample types were strongly correlated within households, suggesting clonal spread of bacteria is a main driver of dissemination of ARGs in the domestic urban environment. Within households, E. coli strain-sharing was rare between humans and animals but more frequent between humans and drinking water. E. coli contamination in stored drinking water was also associated with higher strain-sharing between humans in the same household. Our study demonstrates that contaminated drinking water facilitates human to human strain sharing and water treatment can disrupt transmission.

SUBMITTER: Kim DD

PROVIDER: S-EPMC11326342 | biostudies-literature | 2024 Aug

REPOSITORIES: biostudies-literature

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Bacterial strain sharing between humans, animals, and the environment among urban households.

Kim Daehyun D DD Swarthout Jenna M JM Worby Colin J CJ Chieng Benard B Mboya John J Earl Ashlee M AM Njenga Sammy M SM Pickering Amy J AJ

medRxiv : the preprint server for health sciences 20240807

Identifying bacterial transmission pathways is crucial to inform strategies aimed at curbing the spread of pathogenic and antibiotic-resistant bacteria, especially in rapidly urbanizing low- and middle-income countries. In this study, we assessed bacterial strain-sharing and dissemination of antibiotic resistance across humans, domesticated poultry, canines, household soil, and drinking water in urban informal settlements in Nairobi, Kenya. We collected 321 samples from 50 households and perform ...[more]

PMID: 39148836

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Project description:The prevalence and propagation of antimicrobial resistance (AMR) are serious global public health concerns. The large and the ever-increasing use of antibiotics in livestock is also considered a great concern. The extent of the similarity of acquired antibiotic resistance genes (ARGs) between humans and food animals and the driving factors underlying AMR transfer between them are not clear, although a link between ARGs in both hosts was proposed. To address this question, with swine and chicken as examples of food animals, we analyzed over 1,000 gut metagenomes of humans and food animals from over the world. A relatively high abundance and diversity of ARGs were observed in swine compared with those in humans as a whole. Commensal bacteria, particularly species from Clostridiales, contribute the most ARGs associated with mobile genetic elements (MGEs) and were found in both humans and food animals. Further studies demonstrate that overrepresented MGEs, namely, Tn4451/Tn4453 and TnAs3, are attributed mainly to the sharing between humans and food animals. A member of large resolvase family site-specific recombinases, TnpX, is found in Tn4451/Tn4453 which facilitates the insertions of the transient circular molecule. Although the variance in the transferability of ARGs in humans is higher than that in swine, a higher average transferability was observed in swine than that in humans. In conclusion, the potential antibiotic resistance hot spots with higher transferability in food animals observed in the present study emphasize the importance of surveillance for emerging resistance threats before they spread. IMPORTANCE Antimicrobial resistance (AMR) has proven to be a global public health concern. To conquer this increasingly worrying trend, an overarching, One Health approach has been used that brings together different sectors, but the fundamental knowledge of the relationship between humans, food animals, and their environments is not mature yet or is lacking in some aspect. With swine and chicken as examples of food animals, a large global data set of over 1,000 human and food animal gut metagenomes was analyzed with a focus on acquired antibiotic resistance genes (ARGs) associated with mobile genetic elements (MGEs) to answer this question. Outputs from this work open a new avenue to further our understanding of ARG transferability in food animals. It is a necessary milestone to better equip governmental agencies to monitor and pre-empt antibiotic resistance hot spots. This work will assist and give guidance on how to decipher other links within any One Health initiatives with expected positive feedback to human health.

Project description:Anthropogenic environments such as those created by intensive farming of livestock, have been proposed to provide ideal selection pressure for the emergence of antimicrobial-resistant Escherichia coli bacteria and antimicrobial resistance genes (ARGs) and spread to humans. Here, we performed a longitudinal study in a large-scale commercial poultry farm in China, collecting E. coli isolates from both farm and slaughterhouse; targeting animals, carcasses, workers and their households and environment. By using whole-genome phylogenetic analysis and network analysis based on single nucleotide polymorphisms (SNPs), we found highly interrelated non-pathogenic and pathogenic E. coli strains with phylogenetic intermixing, and a high prevalence of shared multidrug resistance profiles amongst livestock, human and environment. Through an original data processing pipeline which combines omics, machine learning, gene sharing network and mobile genetic elements analysis, we investigated the resistance to 26 different antimicrobials and identified 361 genes associated to antimicrobial resistance (AMR) phenotypes; 58 of these were known AMR-associated genes and 35 were associated to multidrug resistance. We uncovered an extensive network of genes, correlated to AMR phenotypes, shared among livestock, humans, farm and slaughterhouse environments. We also found several human, livestock and environmental isolates sharing closely related mobile genetic elements carrying ARGs across host species and environments. In a scenario where no consensus exists on how antibiotic use in the livestock may affect antibiotic resistance in the human population, our findings provide novel insights into the broader epidemiology of antimicrobial resistance in livestock farming. Moreover, our original data analysis method has the potential to uncover AMR transmission pathways when applied to the study of other pathogens active in other anthropogenic environments characterised by complex interconnections between host species.

Project description:The role of canines in transmitting antibiotic resistant bacteria to humans in the urban environment is poorly understood. To elucidate this role, we utilized genomic sequencing and phylogenetics to characterize the burden and transmission dynamics of antibiotic resistant Escherichia coli (ABR-Ec) cultured from canine and human feces present on urban sidewalks in San Francisco, California. We collected a total of fifty-nine ABR-Ec from human (n=12) and canine (n=47) fecal samples from the Tenderloin and South of Market (SoMa) neighborhoods of San Francisco. We then analyzed phenotypic and genotypic antibiotic resistance (ABR) of the isolates, as well as clonal relationships based on cgMLST and single nucleotide polymorphisms (SNPs) of the core genomes. Using Bayesian inference, we reconstructed the transmission dynamics between humans and canines from multiple local outbreak clusters using the marginal structured coalescent approximation (MASCOT). Overall, we found human and canine samples to carry similar amounts and profiles of ABR genes. Our results provide evidence for multiple transmission events of ABR-Ec between humans and canines. In particular, we found one instance of likely transmission from canines to humans as well as an additional local outbreak cluster consisting of one canine and one human sample. Based on this analysis, it appears that canine feces act as an important reservoir of clinically relevant ABR-Ec within the urban environment. Our findings support that public health measures should continue to emphasize proper canine feces disposal practices, access to public toilets and sidewalk and street cleaning. Importance: Antibiotic resistance in E. coli is a growing public health concern with global attributable deaths projected to reach millions annually. Current research has focused heavily on clinical routes of antibiotic resistance transmission to design interventions while the role of alternative reservoirs such as domesticated animals remain less well understood. Our results suggest canines are part of the transmission network that disseminates high-risk multidrug resistance in E. coli within the urban San Francisco community. As such, this study highlights the need to consider canines, and potentially domesticated animals more broadly, when designing interventions to reduce the prevalence of antibiotic resistance in the community. Additionally, it showcases the utility of genomic epidemiology to reconstruct the pathways by which antimicrobial resistance spreads.

Dataset Information

Bacterial strain sharing between humans, animals, and the environment among urban households.

Publications

Bacterial strain sharing between humans, animals, and the environment among urban households.

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