Nationwide surveillance and characterization of the third-generation cephalosporin-resistant Salmonella enterica serovar infantis isolated from chickens in South Korea between 2010 and 2022

The occurrence of extended-spectrum beta-lactamase (ESBL)/AmpC beta-lactamase-producing Salmonella conferring resistance to third-generation cephalosporin has emerged as a global public health concern. In this study, we aimed to investigate the prevalence and molecular characterization of third-generation cephalosporin-resistant Salmonella enterica serovar Infantis. In total, 409 S. Infatis isolates were collected from the feces and carcasses of healthy and diseased food animals, including chickens (n = 348), pigs (n = 48), cattle (n = 8), and ducks (n = 5) between 2010 and 2022 nationwide in South Korea. Among them, 61.9 % (253/409) of S. Infantis strains displayed resistance to ceftiofur, with the most resistant isolates obtained from chickens (98.4 %, 249/253). Moreover, S. Infantis isolates showed high resistance (47.7-67.2 %) to streptomycin, ampicillin, nalidixic acid, sulfisoxazole, chloramphenicol, tetracycline, and trimethoprim/sulfamethoxazole. Additionally, the multidrug resistance (MDR) was significantly greater in the ceftiofur-resistant isolates compared to the ceftiofur-susceptible isolates (p < 0.05). All the ceftiofur-resistant S. Infantis strains produced CTX-M/CMY-2 beta-lactamase enzymes, with bla(CTX-M-65) comprising the most (98.4 %, 249/253), followed by bla(CTX-M-15) (1.2 %, 3/253), and bla(CMY-2) (0.4 %, 1/253). The ceftiofur-resistant S. Infantis belonged to 37 different pulsotypes, with X1A1 (26.1 %, 66/253), X1A2 (20.9 %, 53/253), and X5A3 (9.1 %) being the most prevalent, representing a total of 56.1 % (142/253). Furthermore, the S. Infantis sequence type (ST)32 was the most common, accounting for 91.9 % (34/37) of the three distinct STs (ST32, ST16, and ST11) detected across farms located in various provinces nationwide. Most of the bla(CMX-M-65) genes (77.5 %, 193/249), all of the bla(CTX-M-15) genes (100 %, 3/3), and the bla(CMY-2) gene (100 %, 1/1) were transferred to the recipient E. coli RG488 by conjugation. In addition, the majority of the transconjugants (98.9 %, 191/193) containing bla(CTX-M-65) genes belong to the IncFIB replicon type, playing an important role in the quick and widespread dissemination of S. Infantis. Thus, ceftiofur-resistant S. Infantis carrying the beta-lactamase genes in chickens has the potential to be transmitted to humans.