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Editor's Pick Research Article | Clinical Science and Epidemiology

One Health Genomic Surveillance of Escherichia coli Demonstrates Distinct Lineages and Mobile Genetic Elements in Isolates from Humans versus Livestock

Catherine Ludden, Kathy E. Raven, Dorota Jamrozy, Theodore Gouliouris, Beth Blane, Francesc Coll, Marcus de Goffau, Plamena Naydenova, Carolyne Horner, Juan Hernandez-Garcia, Paul Wood, Nazreen Hadjirin, Milorad Radakovic, Nicholas M. Brown, Mark Holmes, Julian Parkhill, Sharon J. Peacock
Philippe J. Sansonetti, Editor
Catherine Ludden
aLondon School of Hygiene & Tropical Medicine, London, United Kingdom
bWellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, United Kingdom
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Kathy E. Raven
cDepartment of Medicine, University of Cambridge, Addenbrooke’s Hospital, Cambridge, United Kingdom
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Dorota Jamrozy
bWellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, United Kingdom
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Theodore Gouliouris
cDepartment of Medicine, University of Cambridge, Addenbrooke’s Hospital, Cambridge, United Kingdom
dClinical Microbiology and Public Health Laboratory, Public Health England, Cambridge, United Kingdom
eCambridge University Hospitals NHS Foundation Trust, Cambridge, United Kingdom
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Beth Blane
cDepartment of Medicine, University of Cambridge, Addenbrooke’s Hospital, Cambridge, United Kingdom
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Francesc Coll
aLondon School of Hygiene & Tropical Medicine, London, United Kingdom
bWellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, United Kingdom
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Marcus de Goffau
bWellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, United Kingdom
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Plamena Naydenova
cDepartment of Medicine, University of Cambridge, Addenbrooke’s Hospital, Cambridge, United Kingdom
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Carolyne Horner
fBritish Society for Antimicrobial Chemotherapy, Birmingham, United Kingdom
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Juan Hernandez-Garcia
gDepartment of Veterinary Medicine, University of Cambridge, Cambridge, United Kingdom
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Paul Wood
hRoyal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, United Kingdom
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Nazreen Hadjirin
gDepartment of Veterinary Medicine, University of Cambridge, Cambridge, United Kingdom
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Milorad Radakovic
gDepartment of Veterinary Medicine, University of Cambridge, Cambridge, United Kingdom
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Nicholas M. Brown
dClinical Microbiology and Public Health Laboratory, Public Health England, Cambridge, United Kingdom
eCambridge University Hospitals NHS Foundation Trust, Cambridge, United Kingdom
fBritish Society for Antimicrobial Chemotherapy, Birmingham, United Kingdom
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Mark Holmes
gDepartment of Veterinary Medicine, University of Cambridge, Cambridge, United Kingdom
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Julian Parkhill
bWellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, United Kingdom
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Sharon J. Peacock
aLondon School of Hygiene & Tropical Medicine, London, United Kingdom
bWellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, United Kingdom
cDepartment of Medicine, University of Cambridge, Addenbrooke’s Hospital, Cambridge, United Kingdom
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Philippe J. Sansonetti
Pasteur Institute
Roles: Editor
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DOI: 10.1128/mBio.02693-18
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ABSTRACT

Livestock have been proposed as a reservoir for drug-resistant Escherichia coli that infect humans. We isolated and sequenced 431 E. coli isolates (including 155 extended-spectrum β-lactamase [ESBL]-producing isolates) from cross-sectional surveys of livestock farms and retail meat in the East of England. These were compared with the genomes of 1,517 E. coli bacteria associated with bloodstream infection in the United Kingdom. Phylogenetic core genome comparisons demonstrated that livestock and patient isolates were genetically distinct, suggesting that E. coli causing serious human infection had not directly originated from livestock. In contrast, we observed highly related isolates from the same animal species on different farms. Screening all 1,948 isolates for accessory genes encoding antibiotic resistance revealed 41 different genes present in variable proportions in human and livestock isolates. Overall, we identified a low prevalence of shared antimicrobial resistance genes between livestock and humans based on analysis of mobile genetic elements and long-read sequencing. We conclude that within the confines of our sampling framework, there was limited evidence that antimicrobial-resistant pathogens associated with serious human infection had originated from livestock in our region.

IMPORTANCE The increasing prevalence of E. coli bloodstream infections is a serious public health problem. We used genomic epidemiology in a One Health study conducted in the East of England to examine putative sources of E. coli associated with serious human disease. E. coli from 1,517 patients with bloodstream infections were compared with 431 isolates from livestock farms and meat. Livestock-associated and bloodstream isolates were genetically distinct populations based on core genome and accessory genome analyses. Identical antimicrobial resistance genes were found in livestock and human isolates, but there was limited overlap in the mobile elements carrying these genes. Within the limitations of sampling, our findings do not support the idea that E. coli causing invasive disease or their resistance genes are commonly acquired from livestock in our region.

  • Copyright © 2019 Ludden et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

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One Health Genomic Surveillance of Escherichia coli Demonstrates Distinct Lineages and Mobile Genetic Elements in Isolates from Humans versus Livestock
Catherine Ludden, Kathy E. Raven, Dorota Jamrozy, Theodore Gouliouris, Beth Blane, Francesc Coll, Marcus de Goffau, Plamena Naydenova, Carolyne Horner, Juan Hernandez-Garcia, Paul Wood, Nazreen Hadjirin, Milorad Radakovic, Nicholas M. Brown, Mark Holmes, Julian Parkhill, Sharon J. Peacock
mBio Jan 2019, 10 (1) e02693-18; DOI: 10.1128/mBio.02693-18

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One Health Genomic Surveillance of Escherichia coli Demonstrates Distinct Lineages and Mobile Genetic Elements in Isolates from Humans versus Livestock
Catherine Ludden, Kathy E. Raven, Dorota Jamrozy, Theodore Gouliouris, Beth Blane, Francesc Coll, Marcus de Goffau, Plamena Naydenova, Carolyne Horner, Juan Hernandez-Garcia, Paul Wood, Nazreen Hadjirin, Milorad Radakovic, Nicholas M. Brown, Mark Holmes, Julian Parkhill, Sharon J. Peacock
mBio Jan 2019, 10 (1) e02693-18; DOI: 10.1128/mBio.02693-18
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KEYWORDS

ESBL
Escherichia coli
antimicrobial resistance
genomics
livestock

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