Emergence of OXA-48-producing Enterobacter hormaechei in a Swiss companion animal clinic and their genetic relationship to clinical human isolates

Abstract

Background Enterobacter hormaechei producing the carbapenemase OXA-48 was identified repeatedly in infections in companion animals hospitalized at a Swiss veterinary clinic where OXA-48-producing Klebsiella pneumoniae was previously reported. Objectives To determine the genetic relatedness of animal and human E. hormaechei strains collected in Switzerland during 2017–22 and their mobile genetic elements. Methods Hybrid assemblies for phylogenetic and comparative analysis of animal (n = 9) and human (n = 25) isolates were obtained by sequencing with Illumina, PacBio and Oxford Nanopore Technologies. Antimicrobial susceptibility was tested by broth microdilution. Results The animal strains were identified as E. hormaechei subsp. xiangfangensis ST114 (n = 6) and ST418 (n = 2), and E. hormaechei subsp. hoffmannii ST78 (n = 1). Human E. hormaechei belonged to subspecies steigerwaltii (n = 10), xiangfangensis (n = 13), hoffmannii (n = 1) and hormaechei (n = 1), with a heterogeneous ST distribution differing from the animal strains, except for two ST114. Core-gene SNP analysis confirmed the clonality of the animal ST114 and ST418 isolates (0 to 10 SNPs), and close relatedness of animal and human ST114 strains (80–120 SNPs). The strains harboured the blaOXA-48 gene on ca. 63 kb IncL-type plasmids (n = 27); on ca. 72 kb IncL plasmids co-harbouring blaCTX-M-14 (n = 2); and on ca. 150–180 kb IncFIB (n = 4) or hybrid IncFIB/IncL (n = 1) plasmids. The blaOXA-48-harbouring plasmids and the blaDHA-1-carrying ISCR1 element in one animal ST114 and both ST418 clones were likely acquired from previously spreading K. pneumoniae strains. Conclusions Common ecological niches favour the spread of plasmid-borne carbapenemases among Enterobacterales and the emergence of MDR E. hormaechei clones.