Genomic and Temporal Trends in Canine ExPEC Reflect Those of Human ExPEC

ABSTRACT Companion animals and humans are known to share extraintestinal pathogenic Escherichia coli (ExPEC), but the extent of E. coli sequence types (STs) that cause extraintestinal diseases in dogs is not well understood. Here, we generated whole-genome sequences of 377 ExPEC collected by the Uni...

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Main Authors: Paarthiphan Elankumaran, Max L. Cummins, Glenn F. Browning, Marc S. Marenda, Cameron J. Reid, Steven P. Djordjevic
Format: Article
Language:English
Published: American Society for Microbiology 2022-06-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.01291-22
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author Paarthiphan Elankumaran
Max L. Cummins
Glenn F. Browning
Marc S. Marenda
Cameron J. Reid
Steven P. Djordjevic
author_facet Paarthiphan Elankumaran
Max L. Cummins
Glenn F. Browning
Marc S. Marenda
Cameron J. Reid
Steven P. Djordjevic
author_sort Paarthiphan Elankumaran
collection DOAJ
description ABSTRACT Companion animals and humans are known to share extraintestinal pathogenic Escherichia coli (ExPEC), but the extent of E. coli sequence types (STs) that cause extraintestinal diseases in dogs is not well understood. Here, we generated whole-genome sequences of 377 ExPEC collected by the University of Melbourne Veterinary Hospital from dogs over an 11-year period from 2007 to 2017. Isolates were predominantly from urogenital tract infections (219, 58.1%), but isolates from gastrointestinal specimens (51, 13.5%), general infections (72, 19.1%), and soft tissue infections (34, 9%) were also represented. A diverse collection of 53 STs were identified, with 18 of these including at least five sequences. The five most prevalent STs were ST372 (69, 18.3%), ST73 (31, 8.2%), ST127 (22, 5.8%), ST80 (19, 5.0%), and ST58 (14, 3.7%). Apart from ST372, all of these are prominent human ExPEC STs. Other common ExPEC STs identified included ST12, ST131, ST95, ST141, ST963, ST1193, ST88, and ST38. Virulence gene profiles, antimicrobial resistance carriage, and trends in plasmid carriage for specific STs were generally reflective of those seen in humans. Many of the prominent STs were observed repetitively over an 11-year time span, indicating their persistence in the dogs in the community, which is most likely driven by household sharing of E. coli between humans and their pets. The case of ST372 as a dominant canine lineage observed sporadically in humans is flagged for further investigation. IMPORTANCE Pathogenic E. coli that causes extraintestinal infections (ExPEC) in humans and canines represents a significant burden in hospital and veterinary settings. Despite the obvious interrelationship between dogs and humans favoring both zoonotic and anthropozoonotic infections, whole-genome sequencing projects examining large numbers of canine-origin ExPEC are lacking. In support of anthropozoonosis, we found that most STs from canine infections are dominant human ExPEC STs (e.g., ST73, ST127, ST131) with similar genomic traits, such as plasmid carriage and virulence gene burden. In contrast, we identified ST372 as the dominant canine ST and a sporadic cause of infection in humans, supporting zoonotic transfer. Furthermore, we highlight that, as is the case in humans, STs in canine disease are consistent over time, implicating the gastrointestinal tract as the major community reservoir, which is likely augmented by exposure to human E. coli via shared diet and proximity.
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spelling doaj.art-c380f5b70add4029a8a650ffb79d27642022-12-22T02:38:53ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-06-0110310.1128/spectrum.01291-22Genomic and Temporal Trends in Canine ExPEC Reflect Those of Human ExPECPaarthiphan Elankumaran0Max L. Cummins1Glenn F. Browning2Marc S. Marenda3Cameron J. Reid4Steven P. Djordjevic5Australian Institute for Microbiology and Infection, School of Life Sciences, Faculty of Science, University of Technology Sydney, Ultimo, New South Wales, AustraliaAustralian Institute for Microbiology and Infection, School of Life Sciences, Faculty of Science, University of Technology Sydney, Ultimo, New South Wales, AustraliaAsia-Pacific Centre for Animal Health, Department of Veterinary Biosciences, Melbourne Veterinary School, Faculty of Veterinary and Agricultural Sciences, University of Melbourne, Parkville and Werribee, Victoria, AustraliaAsia-Pacific Centre for Animal Health, Department of Veterinary Biosciences, Melbourne Veterinary School, Faculty of Veterinary and Agricultural Sciences, University of Melbourne, Parkville and Werribee, Victoria, AustraliaAustralian Institute for Microbiology and Infection, School of Life Sciences, Faculty of Science, University of Technology Sydney, Ultimo, New South Wales, AustraliaAustralian Institute for Microbiology and Infection, School of Life Sciences, Faculty of Science, University of Technology Sydney, Ultimo, New South Wales, AustraliaABSTRACT Companion animals and humans are known to share extraintestinal pathogenic Escherichia coli (ExPEC), but the extent of E. coli sequence types (STs) that cause extraintestinal diseases in dogs is not well understood. Here, we generated whole-genome sequences of 377 ExPEC collected by the University of Melbourne Veterinary Hospital from dogs over an 11-year period from 2007 to 2017. Isolates were predominantly from urogenital tract infections (219, 58.1%), but isolates from gastrointestinal specimens (51, 13.5%), general infections (72, 19.1%), and soft tissue infections (34, 9%) were also represented. A diverse collection of 53 STs were identified, with 18 of these including at least five sequences. The five most prevalent STs were ST372 (69, 18.3%), ST73 (31, 8.2%), ST127 (22, 5.8%), ST80 (19, 5.0%), and ST58 (14, 3.7%). Apart from ST372, all of these are prominent human ExPEC STs. Other common ExPEC STs identified included ST12, ST131, ST95, ST141, ST963, ST1193, ST88, and ST38. Virulence gene profiles, antimicrobial resistance carriage, and trends in plasmid carriage for specific STs were generally reflective of those seen in humans. Many of the prominent STs were observed repetitively over an 11-year time span, indicating their persistence in the dogs in the community, which is most likely driven by household sharing of E. coli between humans and their pets. The case of ST372 as a dominant canine lineage observed sporadically in humans is flagged for further investigation. IMPORTANCE Pathogenic E. coli that causes extraintestinal infections (ExPEC) in humans and canines represents a significant burden in hospital and veterinary settings. Despite the obvious interrelationship between dogs and humans favoring both zoonotic and anthropozoonotic infections, whole-genome sequencing projects examining large numbers of canine-origin ExPEC are lacking. In support of anthropozoonosis, we found that most STs from canine infections are dominant human ExPEC STs (e.g., ST73, ST127, ST131) with similar genomic traits, such as plasmid carriage and virulence gene burden. In contrast, we identified ST372 as the dominant canine ST and a sporadic cause of infection in humans, supporting zoonotic transfer. Furthermore, we highlight that, as is the case in humans, STs in canine disease are consistent over time, implicating the gastrointestinal tract as the major community reservoir, which is likely augmented by exposure to human E. coli via shared diet and proximity.https://journals.asm.org/doi/10.1128/spectrum.01291-22Escherichia coliExPECST372antimicrobial resistancecaninedogs
spellingShingle Paarthiphan Elankumaran
Max L. Cummins
Glenn F. Browning
Marc S. Marenda
Cameron J. Reid
Steven P. Djordjevic
Genomic and Temporal Trends in Canine ExPEC Reflect Those of Human ExPEC
Microbiology Spectrum
Escherichia coli
ExPEC
ST372
antimicrobial resistance
canine
dogs
title Genomic and Temporal Trends in Canine ExPEC Reflect Those of Human ExPEC
title_full Genomic and Temporal Trends in Canine ExPEC Reflect Those of Human ExPEC
title_fullStr Genomic and Temporal Trends in Canine ExPEC Reflect Those of Human ExPEC
title_full_unstemmed Genomic and Temporal Trends in Canine ExPEC Reflect Those of Human ExPEC
title_short Genomic and Temporal Trends in Canine ExPEC Reflect Those of Human ExPEC
title_sort genomic and temporal trends in canine expec reflect those of human expec
topic Escherichia coli
ExPEC
ST372
antimicrobial resistance
canine
dogs
url https://journals.asm.org/doi/10.1128/spectrum.01291-22
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AT marcsmarenda genomicandtemporaltrendsincanineexpecreflectthoseofhumanexpec
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