Molecular characteristics of extended-spectrum β-lactamase/AmpC-producing Salmonella enterica serovar Virchow isolated from food-producing animals during 2010-2017 in South Korea.

Global dissemination of non-typhoidal Salmonella producing extended-spectrum β-lactamase (ESBL) is a public-health concern. Recently, the prevalence of Salmonella spp. resistant to third-generation cephalosporins has been increasing in food-producing animals in Korea. In this study, we investigated resistance mechanisms and molecular characteristics of S. Virchow isolates resistant to extended-spectrum cephalosporins (ESCs). We obtained 265 S. Virchow isolates from fecal and carcasses samples of cattle (n = 2), pigs (n = 7), and chickens (n = 256) during 2010-2017, and observed high ESC-resistance (63.8%, 169/265); most of the resistant isolates (96.4%) were obtained from chickens. ESC-resistant S. Virchow isolates (n = 169) showed significantly higher resistance rates to other antimicrobials (especially aminoglycosides and tetracycline, p-value <0.0001), as well as prevalence of multidrug resistance, than did ESC-susceptible S. Virchow isolates (n = 96). All ESC-resistant S. Virchow produced CTX-M-15-type ESBL (n = 147) and/or CMY-2-type AmpC β-lactamase (n = 23). ESC-resistant S. Virchow represented seven pulsotypes, predominantly composed of type II (58.6%) and III (26.0%), detected in 69 farms in 10 provinces, and 33 farms in 7 provinces, respectively. Genes encoding ESC-resistance were horizontally transferred by conjugation to recipient E. coli J53; this was demonstrated in 28.8% (42/146) of blaCTX-M-15-positive isolates and in 50.0% (11/22) of blaCMY-2-positive isolates. All conjugative plasmids carrying blaCTX-M-15 and blaCMY-2 genes belonged to ST2-IncHI2 and ST12/CC12-IncI1, respectively. Genetic features of transferred bla genes were involved with ISEcp1 in both blaCTX-M-15 and blaCMY-2; ISEcp1 plays a critical role in the efficient capture, expression, and mobilization of bla genes. In addition to blaCTX-M-15 genes, resistance markers to aminoglycosides and/or tetracycline were co-transferred to recipient E. coli J53. Our results show a high prevalence of ESBL-producing S. Virchow in chickens and chicken carcasses. Specific blaCTX-M-15 and blaCMY-2-carrying S. Virchow clones and plasmids were predominant in food-producing animals nationwide. Restriction of antimicrobial use and proper biosecurity practices at the farm level should be urgently implemented in the poultry industry.