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

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 o...

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Autores principales: Elankumaran, Paarthiphan, Cummins, Max L., Browning, Glenn F., Marenda, Marc S., Reid, Cameron J., Djordjevic, Steven P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9241711/
https://www.ncbi.nlm.nih.gov/pubmed/35674442
http://dx.doi.org/10.1128/spectrum.01291-22
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author Elankumaran, Paarthiphan
Cummins, Max L.
Browning, Glenn F.
Marenda, Marc S.
Reid, Cameron J.
Djordjevic, Steven P.
author_facet Elankumaran, Paarthiphan
Cummins, Max L.
Browning, Glenn F.
Marenda, Marc S.
Reid, Cameron J.
Djordjevic, Steven P.
author_sort Elankumaran, Paarthiphan
collection PubMed
description 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 pubmed-92417112022-06-30 Genomic and Temporal Trends in Canine ExPEC Reflect Those of Human ExPEC Elankumaran, Paarthiphan Cummins, Max L. Browning, Glenn F. Marenda, Marc S. Reid, Cameron J. Djordjevic, Steven P. Microbiol Spectr Research Article 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. American Society for Microbiology 2022-06-08 /pmc/articles/PMC9241711/ /pubmed/35674442 http://dx.doi.org/10.1128/spectrum.01291-22 Text en Copyright © 2022 Elankumaran et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Elankumaran, Paarthiphan
Cummins, Max L.
Browning, Glenn F.
Marenda, Marc S.
Reid, Cameron J.
Djordjevic, Steven P.
Genomic and Temporal Trends in Canine ExPEC Reflect Those of Human ExPEC
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 Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9241711/
https://www.ncbi.nlm.nih.gov/pubmed/35674442
http://dx.doi.org/10.1128/spectrum.01291-22
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