Poultry production as the main reservoir of ciprofloxacin- and tigecycline-resistant extended-spectrum β-lactamase (ESBL)-producing Salmonella enterica serovar Kentucky ST198.2-2 causing human infections in China

Abstract

ABSTRACT Salmonella enterica serovar Kentucky ( S. Kentucky) has been regarded as a common serotype causing human nontyphoidal salmonellosis, frequently associated with the consumption of contaminated poultry products. Recently, multidrug-resistant (MDR) S . Kentucky ST198 with strong resistance to cefotaxime, ciprofloxacin, and tigecycline has emerged and been frequently detected in both poultry and humans in Europe and Asia. In this study, whole-genome sequencing (WGS) analysis divided 327 S . Kentucky ST198 isolates into two clades, of which ST198.2 is more prevalent than ST198.1 worldwide. We further compared the genomic characteristics of 70 ST198 isolates from animals and humans during 2019–2022 plus previously reported 38 isolates from 2013 to 2019 in China. One hundred five of the 108 isolates were ST198.2, which could be differentiated into two subclades. ST198.2-1 was prevalent in isolates during 2013–2019, while ST198.2-2 has increased to be the predominant subclade in isolates since 2019. CRISPR typing can differentiate the clade ST198.1 isolates from clade ST198.2 ones but cannot differentiate the two subclade isolates. The acquisition of a large multi-drug resistant region in ST198.2-2 enhanced bacterial resistance to β-lactam, aminoglycoside, amphenicol, and fosfomycin. In addition, compared with the extended-spectrum β-lactamase (ESBL)-encoding gene bla CTX-M-14b in ST198.2-1, co-existence of bla CTX-M-55 and bla TEM-1B was detected in most of the ST198.2-2 isolates. The emergence of ciprofloxacin- and tigecycline-resistant ESBL-producing S . Kentucky ST198.2-2 strains highlight the necessity for Salmonella surveillance. It is imperative to implement more effective measures to prevent and control transmission of these strains from poultry to humans. IMPORTANCE Salmonella enterica serovar Kentucky ( S . Kentucky) can cause human infections through consumption of contaminated food of animal origin, and the emergence of multidrug-resistant (MDR) ST198- S . Kentucky strains are of concern for human and animal health. Based on whole-genome sequencing (WGS) analysis, this study revealed that the clade ST198.2-2 S. Kentucky has increased to the predominant group in both chickens and humans in China since 2019, which is different to previous studies of the prevalent ST198.2-1 S . Kentucky before 2019. Acquirement of a multidrug resistance region (MRR) makes the ST198.2-2 S. Kentucky to be extensively drug-resistant (XDR) isolate compared with ST198.2-1 S. Kentucky. Besides, the ST198.2-2 S. Kentucky was mainly detected in chickens (chicken meat, intestinal contents, and slaughterhouse) and humans, indicating chicken is the main reservoir for these XDR S. Kentucky isolates. Therefore, it is necessary to implement continuous Salmonella surveillance and effective measures, such as the development of phages and novel antibiotics/compounds, to prevent the transmission of XDR ST198.2-2 S . Kentucky from chickens to humans across China.