First report of bla OXA-181 -carrying IncX3 plasmids in multidrug-resistant Enterobacter hormaechei and Serratia nevei recovered from canine and feline opportunistic infections

Abstract

ABSTRACT Whole-genome sequence analysis of six Enterobacter hormaechei and two Serratia nevei strains, using a hybrid assembly of Illumina and Oxford Nanopore Technologies sequencing, revealed the presence of the epidemic bla OXA-181 -carrying IncX3 plasmids co-harboring qnrS1 and ∆ ere (A) genes, as well as multiple multidrug resistance (MDR) plasmids disseminating in all strains, originated from dogs and cats in Thailand. The subspecies and sequence types (ST) of the E. hormaechei strains recovered from canine and feline opportunistic infections included E. hormaechei subsp. xiangfangensis ST171 ( n = 3), ST121 ( n = 1), and ST182 ( n = 1), as well as E. hormaechei subsp. steigerwaltii ST65 ( n = 1). Five of the six E. hormaechei strains harbored an identical 51,479-bp bla OXA-181 -carrying IncX3 plasmid. However, the bla OXA-181 plasmid (pCUVET22-969.1) of the E. hormaechei strain CUVET22-969 presented a variation due to the insertion of IS Kpn74 and IS Sbo1 into the virB region. Additionally, the bla OXA-181 plasmids of S. nevei strains were nearly identical to the others at the nucleotide level, with IS Ecl1 inserted upstream of the qnrS1 gene. The E. hormaechei and S. nevei lineages from canine and feline origins might acquire the epidemic bla OXA-181 -carrying IncX3 and MDR plasmids, which are shared among Enterobacterales, contributing to the development of resistance. These findings suggest the spillover of significant OXA-181-encoding plasmids to these bacteria, causing severe opportunistic infections in dogs and cats in Thailand. Surveillance and effective hygienic practice, especially in hospitalized animals and veterinary hospitals, should be urgently implemented to prevent the spread of these plasmids in healthcare settings and communities. IMPORTANCE bla OXA-181 is a significant carbapenemase-encoding gene, usually associated with an epidemic IncX3 plasmid found in Enterobacterales worldwide. In this article, we revealed six carbapenemase-producing (CP) Enterobacter hormaechei and two CP Serratia nevei strains harboring bla OXA-181 -carrying IncX3 and multidrug resistance plasmids recovered from dogs and cats in Thailand. The carriage of these plasmids can promote extensively drug-resistant properties, limiting antimicrobial treatment options in veterinary medicine. Since E. hormaechei and S. nevei harboring bla OXA-181 -carrying IncX3 plasmids have not been previously reported in dogs and cats, our findings provide the first evidence of dissemination of the epidemic plasmids in these bacterial species isolated from animal origins. Pets in communities can serve as reservoirs of significant antimicrobial resistance determinants. This situation places a burden on antimicrobial treatment in small animal practice and poses a public health threat.