Genomic epidemiology of emerging ESBL-producing Salmonella Kentucky bla CTX-M-14b in Europe

Emerg Microbes Infect. 2020 Dec;9(1):2124-2135. doi: 10.1080/22221751.2020.1821582.

Abstract

Global dissemination of ciprofloxacin-resistant Salmonella Kentucky has been observed over the past decades. In recent years, there have been reports of extended-spectrum β-lactamase (ESBL) producing S. Kentucky. Routine surveillance at the European Centre for Disease Prevention and Control (ECDC) detected cases with a ciprofloxacin-resistant S. Kentucky with the ESBL-gene bla CTX-M-14b. Ensuing research identified 78 cases in 2013-2018 in eight European countries. Compared to other S. Kentucky and non-typhoidal Salmonella infections, reported to the European Surveillance System, these cases were more likely to be elderly and to present urinary-tract infections. Bayesian time-scaled phylogeny on whole genome sequences of isolates from these cases and supplementary isolates from public sequence databases was used to infer the origin and spread of this clone. We dated the origin of the bla CTX-M-14b clone to approximately 2005 in Northern Africa, most likely in Egypt. The geographic origin predicted by the phylogenetic analysis is consistent with the patients' travel history. Next to multiple introductions of the clone to Europe from Egypt, our analysis suggests that in some parts of Europe the clone might have formed a stable population, from which further spread has occurred. Comparative genomics indicated that the bla CTX-M-14b gene is present on the bacterial chromosome, within the type VI secretion system region. The bla CTX-M-14b gene is integrated downstream of the hcp1 gene, on a 2854 bp plasmid fragment containing also ISEcp1. This is the first report of a chromosomally integrated CTX-M gene in Salmonella spp. in Europe, previous studies having identified similar genes only on plasmids.

Keywords: Salmonella Kentucky; bla CTX-M-14b; Chromosomal antibiotic resistance; ESBL; ESC; clonal expansion.

MeSH terms

  • Adolescent
  • Adult
  • Africa, Northern / epidemiology
  • Aged
  • Aged, 80 and over
  • Anti-Bacterial Agents / pharmacology*
  • Bayes Theorem
  • Child
  • Child, Preschool
  • Chromosomes, Bacterial
  • Ciprofloxacin / pharmacology
  • Drug Resistance, Multiple, Bacterial / genetics*
  • Egypt / epidemiology
  • Europe / epidemiology
  • Female
  • Genomics
  • Humans
  • Infant
  • Infant, Newborn
  • Male
  • Microbial Sensitivity Tests
  • Middle Aged
  • Molecular Epidemiology
  • Phylogeny
  • Plasmids
  • Salmonella Infections / epidemiology*
  • Salmonella Infections / microbiology
  • Salmonella enterica / drug effects
  • Salmonella enterica / genetics*
  • Salmonella enterica / isolation & purification
  • Whole Genome Sequencing
  • Young Adult
  • beta-Lactamases / genetics*

Substances

  • Anti-Bacterial Agents
  • Ciprofloxacin
  • beta-lactamase CTX-M-14
  • beta-Lactamases