High prevalence of <i>bla</i> _CTX-M-55 -carrying <i>Escherichia coli</i> in both ceftiofur-use and non-use pig farms

Abstract

ABSTRACT The emergence of third-generation cephalosporin-resistant bacteria poses a significant human health hazard worldwide. We aimed to investigate the prevalence of extended-spectrum β-lactamase (ESBL)/AmpC β-lactamase-producing third-generation cephalosporin-resistant Escherichia coli in ceftiofur-use and non-use pig farms. A total of 585 E. coli isolates were collected from pig feces ( n = 354) and farm environments ( n = 231) across various farms between 2022 and 2023 in South Korea. Among them, 61% of E. coli from pigs and 22.9% from the environment were resistant to ceftiofur, with significantly higher rates in ceftiofur-use farms. The most common ESBL gene detected was bla CTX-M-55 (59.9%), followed by bla CTX-M-15 (12.3%) and bla CTX-M-14 (7.4%). Resistance to non-beta-lactam antimicrobials varied, with bla CTX-M-55 -carrying E. coli showing high resistance. Gene transfer via conjugation was observed, particularly for bla CTX-M-1 (85.7%) and bla CTX-M-55 (46.6%). Of note, seven isolates co-harboring mcr-1 and bla CTX-M-55 were found in pigs. Replicon type IncFIB (85.3%) was mainly found in bla CTX-M-55 -carrying plasmids and IncI1 (91.7%) in bla CTX-M-1 . The most frequently observed sequence types were ST457, ST410, ST101, ST75, and ST10, which comprised 38.4% of the isolates. The transposable elements IS 26 -IS Ecp1-bla CTX-M-55 - orf477 (76%), IS Ecp1-bla CTX-M-55 - orf477 (22.7%), bla CTX-M-65 -IS 903 (50%), and bla CTX-M-14 -IS 903 (100%) were predominantly detected. This study implies that ceftiofur use, clonal, and horizontal transfer might cause a high prevalence of ESBLs in pig farms. Thus, these findings emphasize the importance of prudent antimicrobial use and biosecurity measures to combat antimicrobial resistance. IMPORTANCE Antimicrobial resistance in bacteria is a growing concern for both humans and animals. Pigs and their farm environment can carry and spread antimicrobial-resistant bacteria. Moreover, these resistant bacteria can be transmitted to humans and cause complications in treating infections. In this investigation, we present evidence for the widespread occurrence of third-generation cephalosporin-resistant extended-spectrum β-lactamase (ESBL)/AmpC β-lactamase (AmpC) genes in Escherichia coli isolates in ceftiofur-use pigs, which were clonally and horizontally transferred and detected significantly in ceftiofur non-use pigs and their farm environment. Furthermore, we observed different transposable elements, sequence types, and replicon types of E. coli that potentially participate in disseminating antimicrobial resistance. Our study will contribute to a better understanding of the emergence and dissemination of ceftiofur-resistant E. coli and develop a strategy for preventing its spreading to humans and other animals.

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