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Longitudinal study of ESBL/AmpC-producing Enterobacterales strains sharing between cohabiting healthy companion animals and humans in Portugal and in the United Kingdom

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Abstract

Extended-spectrum beta-lactamase (ESBL)- and plasmid-mediated cephalosporinase (AmpC)-producing Enterobacterales (ESBL/AmpC-E) are an increasing healthcare problem in both human and veterinary medicine. The aim of this study was to investigate the possible sharing of ESBL/AmpC-E strains between healthy companion animals and humans of the same household in Portugal (PT) and the United Kingdom (UK). In a prospective longitudinal study, between 2018 and 2020, faecal samples were collected from healthy dogs (n=90), cats (n=20) and their cohabiting humans (n=119) belonging to 41 PT and 44 UK households. Samples were screened for the presence of ESBL/AmpC-E and carbapenemase-producing bacteria. Clonal relatedness between animal and human strains was established by using REP-PCR fingerprinting method, followed by whole-genome sequencing (WGS) of selected strains. ESBL/AmpC-E strains were detected in companion animals (PT=12.7%, n=8/63; UK=8.5%, n=4/47) and humans (PT=20.7%, n=12/58; UK=6.6%, n=4/61) in at least one timepoint. REP-PCR identified paired multidrug-resistant ESBL/AmpC-producing Escherichia coli strains from companion animals and owners in two Portuguese households (4.8%) and one UK household (2.3%). WGS analysis of nine E. coli strains from these three households confirmed that interhost sharing occurred only between the two animal-human pairs from Portugal. Three shared strains were identified: one CTX-M-15-producing E. coli strain in a cat-human pair (O15-H33-ST93) and two CTX-M-15- and CTX-M-55/CMY-2-producing E. coli strains, in a dog-human pair (O8:H9-ST410 and O11:H25-ST457, respectively) at different timepoints. These E. coli clonal lineages are human pandemic, highlighting the role of companion animals living in close contact with humans in the dissemination and persistence of antimicrobial resistance in the household environment.

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Data Availability

The sequencing data generated during the current study is available in the European Nucleotide Archive repository, under the project PRJEB51686. High-resolution phylogenetic tree linked to molecular data is available at Microreact platform, https://microreact.org/project/5UAN5To1F5FudrUvKx5cGH-esbl-producing-escherichia-coli-sharing.

Code availability

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Acknowledgements

We thank the participating animals and owners. We acknowledge the PET-Risk Consortium and all its members: Luís Telo Gama, Rodolfo Leal, Mafalda Lourenço, Hugo Pereira (Faculty of Veterinary Medicine, University of Lisbon, Lisbon, Portugal); Stefan Schwarz and Claudia Feudi (Freie Universität Berlin, Berlin, Germany); Scott Weese, Joyce Rousseau, Katie Clow and Rebecca Flancman (Ontario Veterinary College, Guelph, Canada); Ruth King (Royal Veterinary College, UK); Vincent Perreten (University of Bern, Bern, Switzerland).

Funding

This research was funded by JPIAMR/0002/2016 Project—PET-Risk Consortium, by CIISA and AL4AnimalS through FCT – Fundação para a Ciência e Tecnologia IP (UIDB/00276/2020 and LA/P/0059/2020, respectively) and Medical Research Council (MRC), UK (MR/R000042/1); J.M. and J.M.d.S were supported by a PhD fellowship (2020.07562.BD and 2020.06540.BD, respectively); A.J.A. was supported by CEEC 4th edition (2021.02058.CEECIND).

Author information

Authors and Affiliations

Authors

Contributions

Study conception and design were performed by Juliana Menezes, Anette Loeffler and Constança Pomba. All authors contributed to the material preparation and data collection. The first draft of the manuscript was written by Juliana Menezes and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Juliana Menezes or Constança Pomba.

Ethics declarations

Ethics approval

The study was conducted in accordance with the European Union Directive 2010/63/EU on the protection of animals used for scientific purposes and the Declaration of Helsinki. Ethical approval for collection of samples and data from humans, dogs and cats was obtained from Faculty of Veterinary Medicine, University of Lisbon Ethics Committee for Research and Education (CEBEA 027/2018), and Royal Veterinary College Ethics and Welfare Committee (URN 2017 1750-3).

Consent to participate

Written informed consent was obtained prior to enrolment from each human participant included in the study for themselves and their companion animals.

Consent for publication

Informed consent was obtained from all individual participants included in the study, for themselves and their companion animals.

Conflict of interest

The authors declare no competing interests.

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Supplementary information

ESM 1:

Table S1. Questionnaire responses on demographic, social, and clinical data of dogs (n=90), cats (n= 20), and their co-habiting humans (n=119) by country, 2018-2020.

Table S2. Overview of assembly statistics.

Table S3. Prevalence of ESBL/AmpC carriage within each demographic, social, and clinical characteristics of dogs (n=90), cats (n= 20), and their co-habiting humans (n=119), Portugal and the United Kingdom, 2018-2020.

Table S4. Antimicrobial resistance profiles of ESBL/AmpC-producing strains from faecal samples of companion animals and their co-habiting humans. Table S5. Genetic features of ESBL/AmpC-producing strains from faecal samples of companion animals and their co-habiting humans.

Table S6. Characteristics of ESBL/AmpC-producing Escherichia coli from faecal samples of companion animals and their co-habiting humans selected for WGS.

Figure S1. Dendrogram based on REP-PCR finger-printing data of 41 Escherichia coli strains from companion animals and their owners from Portugal. Generated by Bionumerics (Applied Maths, Sint-Martens-Latem, Belgium) software. The first five algorithms on the strain code represents the household code number. Star represents strains selected for WGS. ‘-’, negative for the gene.

Figure S2. Dendrogram based on REP-PCR finger-printing data of 30 Escherichia coli strains from companion animals and their owners from the United Kingdom. Generated by Bionumerics (Applied Maths, Sint-Martens-Latem, Belgium) software The first five algorithms on the strain code represents the household code number. Star represents strains selected for WGS. ‘-’, negative for the gene.

Figure S3. Longitudinal identification of ESBL/AmpC Enterobacterales positive households. First two letters in household number concerns to country of isolation: PT, Portuguese household, UK, United Kingdom household. Bacteria species abbreviation: CF, Citrobacter freundi; EC, Escherichia coli; HP, Hafnia paralvei; KP, Klebsiella pneumoniae. ST, sequence type. T0 concerns to baseline sampling, T1 was performed one month after T0; T2 was performed two months after T0. All the bacterial isolates were resistant to third generation cephalosporins. (DOCX 1809 kb)

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Menezes, J., Frosini, SM., Belas, A. et al. Longitudinal study of ESBL/AmpC-producing Enterobacterales strains sharing between cohabiting healthy companion animals and humans in Portugal and in the United Kingdom. Eur J Clin Microbiol Infect Dis 42, 1011–1024 (2023). https://doi.org/10.1007/s10096-023-04629-2

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