Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2024 Sep 3:15:1432240.
doi: 10.3389/fmicb.2024.1432240. eCollection 2024.

Transmission dynamics of ESBL/AmpC and carbapenemase-producing Enterobacterales between companion animals and humans

Juliana Menezes  1   2 , Siân-Marie Frosini  3 , Scott Weese  4 , Vincent Perreten  5 , Stefan Schwarz  6   7 , Andreia J Amaral  1   2   8 , Anette Loeffler  3 , Constança Pomba  1   2
Affiliations

Transmission dynamics of ESBL/AmpC and carbapenemase-producing Enterobacterales between companion animals and humans

Juliana Menezes et al. Front Microbiol. .

Abstract

Antimicrobial resistance mediated by extended-spectrum beta-lactamase (ESBL)- and plasmid-mediated cephalosporinase (AmpC)-producing Enterobacterales, as well as carbapenemase-producing Enterobacterales have globally increased among companion animals, posing a potential health risk to humans in contact with them. This prospective longitudinal study investigates the transfer of ESBL/AmpC- and carbapenemase-producing Enterobacterales between companion animals and their cohabitant humans in Portugal (PT) and the United Kingdom (UK) during animal infection. Fecal samples and nasal swabs collected from dogs and cats with urinary tract infection (UTI) or skin and soft tissue infection (SSTI), and their cohabitant humans were screened for resistant strains. Relatedness between animal and human strains was established by whole-genome sequencing (WGS). ESBL/AmpC-producing Enterobacterales were detected in companion animals (PT = 55.8%; UK = 36.4%) and humans (PT = 35.9%; UK = 12.5%). Carbapenemase-producing Enterobacterales carriage was observed in one dog from Portugal (2.6%) and another dog from the UK (4.5%). Transmission of index clinical ESBL-producing Escherichia coli and Klebsiella pneumoniae strains to cohabitant humans was observed in three Portuguese households (6.9%, n = 43), with repeated isolation of the index strains on fecal samples from the animals and their cohabiting humans. In addition, longitudinal sharing of E. coli strains carried by companion animals and their owners was observed in other two Portuguese households and two households from the UK. Furthermore, a multidrug-resistant ACT-24-producing Enterobacter hormaechei subsp. hoffmannii strains were also shared within another Portuguese household. These results highlight the importance of the household as an epidemiological unit in the efforts to mitigate the spread of antimicrobial resistance, further emphasizing the need for antimicrobial surveillance in this context, capable of producing data that can inform and evaluate public health actions.

Keywords: CMY-2; CTX-M-15 ESBL; CTX-M-27; Enterobacter hormaechei subsp. hoffmannii; ExPEC pathotypes; Klebsiella pneumoniae; animal–human sharing; one health.

PubMed Disclaimer

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Distribution of beta-lactam genes in Enterobacterales strains carried by companion animals and their cohabitant humans in Portugal and the United Kingdom. (A) Percentage of beta-lactam genes by country and (B) host. The bars are color-coded according to the gene, as indicated in the legend inset.
Figure 2
Figure 2
Distribution of ESBL/AmpC- or carbapenemase-producing Enterobacterales across fecal/nasal swabs sampling timepoints of 32 positive households in Portugal (PT) and nine households from the United Kingdom (UK). See the color key on the right side of the figure. SSTI, skin and soft tissue infection; UTI, urinary tract infection.
Figure 3
Figure 3
Core genome SNP analysis and genetic features of clinical and carriage ESBL/AmpC-producing Klebsiella pneumoniae strains from companion animals and their cohabitant humans. (A) Maximum likelihood phylogeny of the core genome of six K. pneumoniae strains and the K. pneumoniae subsp. pneumoniae MGH 78578 strain. Bootstrap support values are shown in bold on each node. (B) Heatmap shows the sequence types, antimicrobial resistance determinants, plasmid replicons, and virulence factors for each strain (see color key at the bottom of the figure).
Figure 4
Figure 4
Core genome SNP analysis and genetic features of clinical and carriage ESBL/AmpC-producing Escherichia coli strains from companion animals and their cohabitant humans. (A) Maximum likelihood phylogeny of the core genome of 33 E. coli strains and the E. coli K-12 MG1655 strain. Bootstrap support values are shown in bold on each node. (B) Heatmap shows the E. coli sequence types, antimicrobial resistance determinants, plasmid replicons, and pathotypes based on a repertoire of virulence factors for each strain (see color key on the right side of the figure).
Figure 5
Figure 5
Map of blaACT-24 genetic environment comparison between carriage Enterobacter hormaechei subsp. hoffmannii strains from a dog and their cohabitant human fecal samples. Antibiotic resistance genes are represented by red arrows, integrase by green arrows, and other genes with black arrows.
See this image and copyright information in PMC

References

    1. Abbas G., Khan I., Mohsin M., Sajjad-ur-Rahman S. U. R., Younas T., Ali S. (2019). High rates of CTX-M group-1 extended-spectrum β-lactamases producing Escherichia coli from pets and their owners in Faisalabad. Pakistan. Infect. Drug Resist. 12, 571–578. doi: 10.2147/IDR.S189884, PMID: - DOI - PMC - PubMed
    1. Adler A., Katz D. E., Marchaim D. (2016). The continuing plague of extended-spectrum β-lactamase–producing Enterobacteriaceae infections. Infect. Dis. Clin. N. Am. 30, 347–375. doi: 10.1016/j.idc.2016.02.003, PMID: - DOI - PubMed
    1. Andrews S. (2010) A quality control tool for high throughput sequence data. Available at: https://www.bioinformatics.babraham.ac.uk/projects/fastqc/ (Accessed: 10 January 2021).
    1. Argimón S., Abudahab K., Goater R. J. E., Fedosejev A., Bhai J., Glasner C., et al. (2016). Microreact: visualizing and sharing data for genomic epidemiology and phylogeography. Microbial genomics 2:e000093. doi: 10.1099/mgen.0.000093, PMID: - DOI - PMC - PubMed
    1. Baede V. O., Broens E. M., Spaninks M. P., Timmerman A. J., Graveland H., Wagenaar J. A., et al. (2017). Raw pet food as a risk factor for shedding of extended-spectrum beta-lactamase-producing Enterobacteriaceae in household cats. PLoS One 12:e0187239. doi: 10.1371/journal.pone.0187239, PMID: - DOI - PMC - PubMed