Molecular epidemiology of Clostridioides difficile in companion animals: Genetic overlap with human strains and public health concerns

IntroductionThe changing epidemiology of Clostridioides difficile reflects a well-established and intricate community transmission network. With rising numbers of reported community-acquired infections, recent studies tried to identify the role played by non-human reservoirs in the pathogen's t...

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Main Authors: Frederico Alves, Rita Castro, Miguel Pinto, Alexandra Nunes, Constança Pomba, Manuela Oliveira, Leonor Silveira, João Paulo Gomes, Mónica Oleastro
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-01-01
Series:Frontiers in Public Health
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Online Access:https://www.frontiersin.org/articles/10.3389/fpubh.2022.1070258/full
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author Frederico Alves
Rita Castro
Miguel Pinto
Alexandra Nunes
Alexandra Nunes
Constança Pomba
Constança Pomba
Manuela Oliveira
Leonor Silveira
João Paulo Gomes
João Paulo Gomes
Mónica Oleastro
author_facet Frederico Alves
Rita Castro
Miguel Pinto
Alexandra Nunes
Alexandra Nunes
Constança Pomba
Constança Pomba
Manuela Oliveira
Leonor Silveira
João Paulo Gomes
João Paulo Gomes
Mónica Oleastro
author_sort Frederico Alves
collection DOAJ
description IntroductionThe changing epidemiology of Clostridioides difficile reflects a well-established and intricate community transmission network. With rising numbers of reported community-acquired infections, recent studies tried to identify the role played by non-human reservoirs in the pathogen's transmission chain. This study aimed at describing the C. difficile strains circulating in canine and feline populations, and to evaluate their genetic overlap with human strains to assess the possibility of interspecies transmission.MethodsFecal samples from dogs (n = 335) and cats (n = 140) were collected from two populations (group A and group B) in Portugal. C. difficile isolates were characterized for toxigenic profile and PCR-ribotyping. The presence of genetic determinants of antimicrobial resistance was assessed in all phenotypically resistant isolates. To evaluate the genetic overlap between companion animals and human isolates from Portugal, RT106 (n = 42) and RT014/020 (n = 41) strains from both sources were subjected to whole genome sequencing and integrated with previously sequenced RT106 (n = 43) and RT014/020 (n = 142) genomes from different countries. The genetic overlap was assessed based on core-single nucleotide polymorphism (SNP) using a threshold of 2 SNP.ResultsThe overall positivity rate for C. difficile was 26% (76/292) in group A and 18.6% (34/183) in group B. Toxigenic strains accounted for 50% (38/76) and 52.9% (18/34) of animal carriage rates, respectively. The most prevalent ribotypes (RT) were the toxigenic RT106 and RT014/020, and the non-toxigenic RT010 and RT009. Antimicrobial resistance was found for clindamycin (27.9%), metronidazole (17.1%) and moxifloxacin (12.4%), associated with the presence of the ermB gene, the pCD-METRO plasmid and point mutations in the gyrA gene, respectively. Both RT106 and RT014/020 genetic analysis revealed several clusters integrating isolates from animal and human sources, supporting the possibility of clonal interspecies transmission or a shared environmental contamination source.DiscussionThis study shows that companion animals may constitute a source of infection of toxigenic and antimicrobial resistant human associated C. difficile isolates. Additionally, it contributes with important data on the genetic proximity between C. difficile isolates from both sources, adding new information to guide future work on the role of animal reservoirs in the establishment of community associated transmission networks and alerting for potential public health risk.
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spelling doaj.art-f300153076b84156b481d6877e3573a72023-01-06T18:26:23ZengFrontiers Media S.A.Frontiers in Public Health2296-25652023-01-011010.3389/fpubh.2022.10702581070258Molecular epidemiology of Clostridioides difficile in companion animals: Genetic overlap with human strains and public health concernsFrederico Alves0Rita Castro1Miguel Pinto2Alexandra Nunes3Alexandra Nunes4Constança Pomba5Constança Pomba6Manuela Oliveira7Leonor Silveira8João Paulo Gomes9João Paulo Gomes10Mónica Oleastro11National Reference Laboratory of Gastrointestinal Infections, Department of Infectious Diseases, National Institute of Health Doutor Ricardo Jorge (INSA), Lisbon, PortugalNational Reference Laboratory of Gastrointestinal Infections, Department of Infectious Diseases, National Institute of Health Doutor Ricardo Jorge (INSA), Lisbon, PortugalGenomics and Bioinformatics Unit, Department of Infectious Diseases, National Institute of Health Doutor Ricardo Jorge (INSA), Lisbon, PortugalGenomics and Bioinformatics Unit, Department of Infectious Diseases, National Institute of Health Doutor Ricardo Jorge (INSA), Lisbon, PortugalFaculty of Veterinary Medicine, Lusófona University, Lisbon, PortugalGenevet–Veterinary Molecular Diagnostic Laboratory, Carnaxide, PortugalCIISA–Centre for Interdisciplinary Research in Animal Health, Faculty of Veterinary Medicine, University of Lisbon, Lisbon, PortugalCIISA–Centre for Interdisciplinary Research in Animal Health, Faculty of Veterinary Medicine, University of Lisbon, Lisbon, PortugalNational Reference Laboratory of Gastrointestinal Infections, Department of Infectious Diseases, National Institute of Health Doutor Ricardo Jorge (INSA), Lisbon, PortugalGenomics and Bioinformatics Unit, Department of Infectious Diseases, National Institute of Health Doutor Ricardo Jorge (INSA), Lisbon, PortugalFaculty of Veterinary Medicine, Lusófona University, Lisbon, PortugalNational Reference Laboratory of Gastrointestinal Infections, Department of Infectious Diseases, National Institute of Health Doutor Ricardo Jorge (INSA), Lisbon, PortugalIntroductionThe changing epidemiology of Clostridioides difficile reflects a well-established and intricate community transmission network. With rising numbers of reported community-acquired infections, recent studies tried to identify the role played by non-human reservoirs in the pathogen's transmission chain. This study aimed at describing the C. difficile strains circulating in canine and feline populations, and to evaluate their genetic overlap with human strains to assess the possibility of interspecies transmission.MethodsFecal samples from dogs (n = 335) and cats (n = 140) were collected from two populations (group A and group B) in Portugal. C. difficile isolates were characterized for toxigenic profile and PCR-ribotyping. The presence of genetic determinants of antimicrobial resistance was assessed in all phenotypically resistant isolates. To evaluate the genetic overlap between companion animals and human isolates from Portugal, RT106 (n = 42) and RT014/020 (n = 41) strains from both sources were subjected to whole genome sequencing and integrated with previously sequenced RT106 (n = 43) and RT014/020 (n = 142) genomes from different countries. The genetic overlap was assessed based on core-single nucleotide polymorphism (SNP) using a threshold of 2 SNP.ResultsThe overall positivity rate for C. difficile was 26% (76/292) in group A and 18.6% (34/183) in group B. Toxigenic strains accounted for 50% (38/76) and 52.9% (18/34) of animal carriage rates, respectively. The most prevalent ribotypes (RT) were the toxigenic RT106 and RT014/020, and the non-toxigenic RT010 and RT009. Antimicrobial resistance was found for clindamycin (27.9%), metronidazole (17.1%) and moxifloxacin (12.4%), associated with the presence of the ermB gene, the pCD-METRO plasmid and point mutations in the gyrA gene, respectively. Both RT106 and RT014/020 genetic analysis revealed several clusters integrating isolates from animal and human sources, supporting the possibility of clonal interspecies transmission or a shared environmental contamination source.DiscussionThis study shows that companion animals may constitute a source of infection of toxigenic and antimicrobial resistant human associated C. difficile isolates. Additionally, it contributes with important data on the genetic proximity between C. difficile isolates from both sources, adding new information to guide future work on the role of animal reservoirs in the establishment of community associated transmission networks and alerting for potential public health risk.https://www.frontiersin.org/articles/10.3389/fpubh.2022.1070258/fullClostridioides difficilecompanion animalsone healthwhole genome sequencingSNP analysisantimicrobial resistance
spellingShingle Frederico Alves
Rita Castro
Miguel Pinto
Alexandra Nunes
Alexandra Nunes
Constança Pomba
Constança Pomba
Manuela Oliveira
Leonor Silveira
João Paulo Gomes
João Paulo Gomes
Mónica Oleastro
Molecular epidemiology of Clostridioides difficile in companion animals: Genetic overlap with human strains and public health concerns
Frontiers in Public Health
Clostridioides difficile
companion animals
one health
whole genome sequencing
SNP analysis
antimicrobial resistance
title Molecular epidemiology of Clostridioides difficile in companion animals: Genetic overlap with human strains and public health concerns
title_full Molecular epidemiology of Clostridioides difficile in companion animals: Genetic overlap with human strains and public health concerns
title_fullStr Molecular epidemiology of Clostridioides difficile in companion animals: Genetic overlap with human strains and public health concerns
title_full_unstemmed Molecular epidemiology of Clostridioides difficile in companion animals: Genetic overlap with human strains and public health concerns
title_short Molecular epidemiology of Clostridioides difficile in companion animals: Genetic overlap with human strains and public health concerns
title_sort molecular epidemiology of clostridioides difficile in companion animals genetic overlap with human strains and public health concerns
topic Clostridioides difficile
companion animals
one health
whole genome sequencing
SNP analysis
antimicrobial resistance
url https://www.frontiersin.org/articles/10.3389/fpubh.2022.1070258/full
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