High Prevalence of bla CTXM-1/IncI1-Iγ/ST3 Plasmids in Extended-Spectrum β-Lactamase-Producing Escherichia coli Isolates Collected From Domestic Animals in Guadeloupe (French West Indies)

Abstract

Extended-spectrum β-lactamase-producing Enterobacteriaceae (ESBL-E) have been classified in the group of resistant bacteria of highest priority. We determined the prevalence of ESBL-E collected in feces from household and shelter pets in Guadeloupe (French West Indies). A single rectal swab was taken from 125 dogs and 60 cats between June and September 2019. The prevalence of fecal carriage of ESBL-E was 7.6% (14/185, 95% CI: 4.2-12.4), within the range observed worldwide. The only risk factor associated with a higher prevalence of ESBL-E rectal carriage was a stay in a shelter, suggesting that refuges could be hotspots for their acquisition. All but one (Klebsiella pneumoniae from a cat) were Escherichia coli. We noted the presence of a bla _CTX-M-1/IncI1-Iγ/sequence type (ST3) plasmid in 11 ESBL-producing E. coli isolates belonging to ST328 (n = 6), ST155 (n = 4) and ST953 (n = 1). A bla _CTX-M-15 gene was identified in the three remaining ESBL-E isolates. The bla _CTX-M-1 and most of the antimicrobial resistance genes were present in a well-conserved large conjugative IncI1-Iγ/ST3 plasmid characterized by two accessory regions containing antibiotic resistance genes. The plasmid has been detected worldwide in E. coli isolates from humans and several animal species, such as food-producing animals, wild birds and pets, and from the environment. This study shows the potential role of pets as a reservoir of antimicrobial-resistant bacteria or genes for humans and underlines the importance of basic hygiene measures by owners of companion animals.

Keywords: ESBL; Enterobacteriaceae; Escherichia coli; nanopore; pets; plasmid; shelter.

FIGURE 1

Maximum likelihood phylogenetic tree of 13 extended-spectrum β-lactamase-producing Escherichia coli isolates collected in Guadeloupe based on multiple sequence alignments of the 3,429 core genome loci. Sequence type (ST) is indicated for each isolate. Hosts, ESBL genes, site of inclusion, and an identical owner are indicated by vertical colored strips. Other antibiotic resistance genes characterized by ResFinder and Inc. incompatibility group characterized by PlasmidFinder are indicated by black dots and gray triangles, respectively.

FIGURE 2

Genetic organization of accessory region carrying antibiotic resistance genes among IncI1-Iγ/ST3 plasmids from six Escherichia coli isolates collected in Guadeloupe (reference pEC405, 1 to 12,177 bp).

FIGURE 3

Syntenic analysis of 6 IncI1-Iγ/ST3 plasmids from six Escherichia coli isolates collected in Guadeloupe. All isolates produced an extended-spectrum β-lactamase (bla_CTX–M–1) except for pEC345. The innermost black ring 1 represents the reference sequence of pEC405. The subsequent rings correspond to pairwise comparisons with pEC405: ring 2 represents pEC440; ring 3, pEC38; ring 4, pEC1; ring 5, pEc7; ring 6, pEC345. The last two rings represent a genetic map of pEC405.