Abstract
Salmonella enterica serotype Kentucky can be a common causative agent of salmonellosis, usually associated with consumption of contaminated poultry. Antimicrobial resistance (AMR) to multiple drugs, including ciprofloxacin, is an emerging problem within this serotype. We used whole-genome sequencing (WGS) to investigate the phylogenetic structure and AMR content of 121 S. e nterica serotype Kentucky sequence type 198 isolates from five continents. Population structure was inferred using phylogenomic analysis and whole genomes were compared to investigate changes in gene content, with a focus on acquired AMR genes. Our analysis showed that multidrug-resistant (MDR) S. enterica serotype Kentucky isolates belonged to a single lineage, which we estimate emerged circa 1989 following the acquisition of the AMR-associated Salmonella genomic island (SGI) 1 (variant SGI1-K) conferring resistance to ampicillin, streptomycin, gentamicin, sulfamethoxazole and tetracycline. Phylogeographical analysis indicates this clone emerged in Egypt before disseminating into Northern, Southern and Western Africa, then to the Middle East, Asia and the European Union. The MDR clone has since accumulated various substitution mutations in the quinolone-resistance-determining regions (QRDRs) of DNA gyrase (gyrA) and DNA topoisomerase IV (parC), such that most strains carry three QRDR mutations which together confer resistance to ciprofloxacin. The majority of AMR genes in the S. e nterica serotype Kentucky genomes were carried either on plasmids or SGI structures. Remarkably, each genome of the MDR clone carried a different SGI1-K derivative structure; this variation could be attributed to IS26-mediated insertions and deletions, which appear to have hampered previous attempts to trace the clone’s evolution using sub-WGS resolution approaches. Several different AMR plasmids were also identified, encoding resistance to chloramphenicol, third-generation cephalosporins, carbapenems and/or azithromycin. These results indicate that most MDR S. e nterica serotype Kentucky circulating globally result from the clonal expansion of a single lineage that acquired chromosomal AMR genes 30 years ago, and has continued to diversify and accumulate additional resistances to last-line oral antimicrobials. This article contains data hosted by Microreact.
Highlights
IntroductionCarbapenem-resistant, extended-spectrum β-lactamase (ESBL) producing Enterobacteriaceae and fluoroquinoloneresistant Salmonella have been recently listed as priority pathogens that pose the greatest threats to human health (critical and high threat levels, respectively) by the World Health Organization (WHO) [1]
Carbapenem-resistant, extended-spectrum β-lactamase (ESBL) producing Enterobacteriaceae and fluoroquinoloneresistant Salmonella have been recently listed as priority pathogens that pose the greatest threats to human health by the World Health Organization (WHO) [1]
All 121 S. enterica serotype Kentucky ST198 genomes were mapped to the draft reference genome for S. enterica serotype Kentucky ST198 strain 201001922, and 2066 single-nucleotide variants (SNVs) were identified in the core genome
Summary
Carbapenem-resistant, extended-spectrum β-lactamase (ESBL) producing Enterobacteriaceae and fluoroquinoloneresistant Salmonella have been recently listed as priority pathogens that pose the greatest threats to human health (critical and high threat levels, respectively) by the World Health Organization (WHO) [1] All these resistances have been observed in a single serotype of Salmonella enterica, serotype Kentucky, since the 2000s [2,3,4,5]. Between 2007 and 2012, the European Centers for Disease Control and Prevention (ECDC) reported 1301 isolations of S. enterica serotype Kentucky from 12 countries, including 955 (73.4 %) CIPR S. enterica serotype Kentucky [6] These isolates were found in patients across the world, but predominantly in Northern Africa, Europe and Southern Asia. Multilocus sequence typing (MLST) and PFGE have revealed that CIPR S. enterica serotype Kentucky is a single population belonging to sequence type (ST)198 and not ST152, which is a prevalent S. enterica serotype Kentucky ST found in poultry in the USA but rarely reported in humans [7]
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