Report of highly ciprofloxacin resistant Salmonella enterica serovar Kentucky isolates of human, food and animal origin in Germany

Objectives: Since a couple of years, the multidrug-resistant Salmonella enterica Serovar (S.) Kentucky clone ST198-X1 displaying high-level resistance to fluoroquinolones (ciprofloxacin, MIC > or = 4 mg/l) is spreading over Africa and the Middle East. Also European surveillance systems in France, England, Wales and Denmark as well as the USA recorded an increase of travel-associated human salmonellosis cases caused by this clone. As to date in Germany no surveillance data of this clone were available, we analyzed the trend and characteristics of S . Kentucky isolates received over the past years (1998-2012). To investigate possible routes of transmission animal and foodborne isolates were compared to human ones. Methods: Thirty-two S. Kentucky originating from animal, food and non-human sources from the National Reference Laboratory for Salmonella (NRL-Salm) at the Federal Institute for Risk Assessment (BfR), and in addition 30 human isolates from the National Reference Centre of Salmonella and other enterics at the Robert Koch Institute (RKI) were subjected to antimicrobial susceptibility testing, molecular typing methods (XbaI and BlnI pulsed-field gel electrophoresis [PFGE] and multilocus sequence typing [MLST]), as well as detection of resistance genes, class 1 integrons and the SGI1 flanking region by PCR/sequencing. Results: Since 2010 submissions of highly ciprofloxacin resistant S. Kentucky isolates, especially from turkey and turkey meat products, were increasingly recorded in Germany. Forty-nine of these isolates displayed ciprofloxacin MIC values of > 4 mg/l. As shown by molecular typing methods most of the German S. Kentucky isolates were identical to the clone described by Le Hello et al. (2011) belonging to ST198 and carried the multidrug resistance encoding region Salmonella genomic island 1 (SGI1). According to sequence analysis all ciprofloxacin resistant isolates showed double mutations in gyrA (Ser83 and Asp87) and a single mutation in parC (Ser80). Conclusions: Since the WHO lists fluoroquinolones among the "top-3" critically important drugs in human and veterinary medicine and since these antimicrobials are still agents of choice in therapy of systemic Salmonella infections, the spread of ST198-X1 S. Kentucky demands special attention. Turkey meat is supposed to be an important infection vehicle. The implementation of mitigation strategies for this highly resistant clone is strongly recommended.