Highly drug-resistant Salmonella enterica serotype Kentucky ST198-X1: a microbiological study

Simon Le Hello,Brahim Bouchrif,François-Xavier Weill,Dalèle Elhani,Khalid Zerouali,Lucile Sontag,Dorothée Harrois,Véronique Guibert

doi:10.1016/s1473-3099(13)70124-5

Abstract

Salmonella enterica is a major global food-borne pathogen, causing life-threatening infections. Ciprofloxacin and extended-spectrum cephalosporins (ESCs) are the drugs of choice for severe infections. We previously reported a ciprofloxacin-resistant S. enterica serotype Kentucky (S Kentucky) ST198-X1 strain that emerged in Egypt and spread throughout Africa and the Middle East from 2002 to 2008. We aimed to monitor recent trends in the location of transmission and antimicrobial resistance of this strain. We analysed isolates of S Kentucky collected by the French national surveillance system for salmonellosis in France from Jan 1, 2000, to Dec 31, 2011, and at two sites in Casablanca, Morocco, between Jan 1, 2003, and Dec 31, 2011. We analysed patterns of travel of patients infected with a ciprofloxacin-resistant strain of S Kentucky. We identified isolates showing resistance to ESCs or decreased susceptibility to carbapenems, characterised isolates by XbaI-pulsed field gel electrophoresis and multilocus sequence typing, and assessed mechanisms of bacterial resistance to antimicrobial drugs. 954 (1%) of 128,836 serotyped Salmonella spp isolates in France were identified as S Kentucky, as were 30 (13%) of 226 Salmonella spp isolates from Morocco. During 2000-08, 200 (40%) of 497 subculturable isolates of S Kentucky obtained in France were resistant to ciprofloxacin, compared with 376 (83%) of 455 isolates in 2009-11, suggesting a recent increase in ciprofloxacin resistance in France. Travel histories suggested S Kentucky infections originated predominantly in east Africa, north Africa, west Africa, and the Middle East, but also arose in India. We report several occurrences of acquisition of extended-spectrum β-lactamase (CTX-M-1, CTX-M-15), plasmid-encoded cephalosporinase (CMY-2), or carbapenemase (OXA-48, VIM-2) genes by ciprofloxacin-resistant isolates of S Kentucky ST198-X1 from the Mediterranean area since 2009. Many of these highly drug-resistant isolates were also resistant to most aminoglycosides, to co-trimoxazole (trimethoprim-sulfamethoxazole), and to azithromycin. The potential risk to public health posed by ciprofloxacin-resistant S Kentucky ST198-X1 warrants its inclusion in national programmes for the control of S. enterica in food-producing animals, in particular in poultry. Institut Pasteur, Institut de Veille Sanitaire, Fondation pour la Recherche Médicale, French Government Investissement d'Avenir programme.

Highlights

Antimicrobial drug-resistant bacteria are a serious challenge for the clinical care of patients and for Public Health in the 21st century.[1]
We previously reported a ciprofloxacinresistant S. enterica serotype Kentucky strain (Salmonella Kentucky ST198-X1 CIPR) that emerged in Egypt and spread throughout Africa and the Middle East from 2002 to 2008
We previously reported the international emergence of a multidrug-resistant S. enterica serotype Kentucky (Salmonella Kentucky) strain, identified as being multilocus sequence type (MLST) ST198 and as belonging to XbaI pulsed-field gel electrophoresis (PFGE) cluster

Summary

Introduction

Antimicrobial drug-resistant bacteria are a serious challenge for the clinical care of patients and for Public Health in the 21st century.[1]. The recent emergence of Enterobacteriaeceae resistant to all -lactam antibiotics, including ESCs and carbapenems, is of particular concern, because carbapenems are, in many cases the last option available for treating serious infection with ESC-resistant Gram-negative bacteria. The development pipeline for new antimicrobial drugs with bactericidal activity against Gram-negative bacteria has run dry.[2,3]. 1,730 deaths caused by a multidrug-resistant non-typhoidal Salmonella, resistant, in particular, to both ESCs and fluoroquinolones. This choice was based on the following observations (i) Salmonella is a prevalent zoonotic agent causing an estimated 1.7 million infections, resulting in 2,800 deaths per year in high-income regions of North America in. We previously reported a ciprofloxacinresistant S. enterica serotype Kentucky strain (Salmonella Kentucky ST198-X1 CIPR) that emerged in Egypt and spread throughout Africa and the Middle East from 2002 to 2008

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