Antimicrobial Resistance Profiles and Molecular Characteristics of Extended-Spectrum β-Lactamase-Producing Salmonella enterica Serovar Typhimurium Isolates from Food Animals During 2010-2021 in South Korea

Abstract

Extended-spectrum β-lactamase (ESBL)-producing Salmonella is emerging as a worldwide public health concern. In this study, we aimed to investigate the antimicrobial resistance profiles and molecular characteristics of ESBL-producing Salmonella enterica serovar Typhimurium (S. Typhimurium). We obtained a total of 995 S. Typhimurium isolates from the feces and carcasses of pigs (n = 678), chickens (n = 202), and cattle (n = 115) during 2010-2021 in Korea. We found that 35 S. Typhimurium isolates (3.5%) showed resistance to ceftiofur: pigs (51.4%, 18/35) and cattle (42.9%, 15/35). All of the ceftiofur-resistant S. Typhimurium isolates demonstrated multidrug resistance. Moreover, ceftiofur-resistant S. Typhimurium isolates displayed significantly higher rates of resistance to chloramphenicol and trimethoprim/sulfamethoxazole than ceftiofur-susceptible S. Typhimurium isolates (p < 0.05). The ceftiofur-resistant S. Typhimurium isolates produced four different CTX-M-type β-lactamase, comprising bla_CTX-M-55 in the majority (51.4%, 18/35), followed by bla_CTX-M-65 (28.6%, 10/35), bla_CTX-M-14 (17.1%, 6/35), and bla_CTX-M-1 (2.9%, 1/35). Among the 35 ceftiofur-resistant S. Typhimurium isolates, 16 bla_CTX-M-55-positive isolates and one bla_CTX-M-1-positive isolate were transferred to recipient Escherichia coli RG488 by conjugation. The predominantly found transposable units were bla_CTX-M-55-orf477 (45.7%, 16/35), followed by bla_CTX-M-65-IS903 (28.6%, 10/35) and bla_CTX-M-14-IS903 (17.1%, 6/35). Ceftiofur-resistant S. Typhimurium represented 19 types, with types P1-19 (22.9%, 8/35) and P12-34 (22.9%, 8/35) making up the majority and being found in most farms nationwide. Sequence types (STs) were different by animal species: ST19 (48.6%, 17/35) and ST34 (42.9%, 15/35) were mostly found STs in pigs and cattle, respectively. These findings showed that food animals, especially pigs and cattle, act as reservoirs of bla_CTX-M-harboring S. Typhimurium that can potentially be spread to humans.

Keywords: ESBL; S. Typhimurium; blaCTX-M-55; blaCTX-M-65; ceftiofur; food animals.