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 β-lactamase (ESBL)/AmpC β-lactamase-producing <i>Salmonella</i> 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 <i>Salmonella enterica</i> serovar Infantis. In total, 409 <i>S.</i> 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 <i>S.</i> Infantis strains displayed resistance to ceftiofur, with the most resistant isolates obtained from chickens (98.4 %, 249/253). Moreover, <i>S.</i> 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 (<i>p</i> < 0.05). All the ceftiofur-resistant <i>S.</i> Infantis strains produced CTX-M/CMY-2 β-lactamase enzymes, with <i>bla</i> _CTX-M-65 comprising the most (98.4 %, 249/253), followed by <i>bla</i> _CTX-M-15 (1.2 %, 3/253), and <i>bla</i> _CMY-2 (0.4 %, 1/253). The ceftiofur-resistant <i>S.</i> 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 <i>S.</i> 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 <i>bla</i> _CMX-M-65 genes (77.5 %, 193/249), all of the <i>bla</i> _CTX-M-15 genes (100 %, 3/3), and the <i>bla</i> _CMY-2 gene (100 %, 1/1) were transferred to the recipient <i>E. coli</i> RG488 by conjugation. In addition, the majority of the transconjugants (98.9 %, 191/193) containing <i>bla</i> _CTX-M-65 genes belong to the IncFIB replicon type, playing an important role in the quick and widespread dissemination of <i>S.</i> Infantis. Thus, ceftiofur-resistant <i>S.</i> Infantis carrying the β-lactamase genes in chickens has the potential to be transmitted to humans.