A Retrospective Analysis of Salmonella Isolates across 11 Animal Species (1982–1999) Led to the First Identification of Chromosomally Encoded blaSCO-1 in the USA

Authors: IDUU, NNEKA VIVIAN - Auburn University; RAIFORD, DONNA - Auburn University; CONLEY, AUSTIN - Auburn University; SCARIA, JOY - Oklahoma State University; NELSON, JULIE - South Dakota State University; RUESCH, LAURA - South Dakota State University; PRICE, STUART - Auburn University; YUE, MIN - Zhejiang University; GONG, JIANSEN - Chinese Academy Of Agricultural Sciences; WEI, LANJING - University Of Kansas; WANG, CHENGMING - Auburn University

Submitted to: Microorganisms
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/4/2024
Publication Date: 3/6/2024
Citation: Iduu, N., Raiford, D., Conley, A., Scaria, J., Nelson, J., Ruesch, L., Price, S., Yue, M., Gong, J., Wei, L., Wang, C. 2024. A Retrospective Analysis of Salmonella Isolates across 11 Animal Species (1982–1999) Led to the First Identification of Chromosomally Encoded blaSCO-1 in the USA. Microorganisms. 12, 528. https://doi.org/10.3390/microorganisms12030528.
DOI: https://doi.org/10.3390/microorganisms12030528

Interpretive Summary: Antimicrobial resistance (AMR) in Salmonella bacteria is a pressing public health concern in the United States, necessitating continuous surveillance. We conducted a retrospective analysis of 251 Salmonella isolates from 11 animal species recovered between 1982 and 1999, utilizing serotyping, antimicrobial susceptibility testing, and whole-genome sequencing (WGS). Phenotypic resistance was observed in 101 isolates, with S. Typhimurium, S. Dublin, S. Agona, and S. Muenster prevailing among 36 identified serovars. Notably, resistance to 12 of 17 antibiotics was detected, with ampicillin being most prevalent (79/251). We identified 38 resistance genes, primarily mediating aminoglycoside (n = 13) and ß-lactamase (n = 6) resistance. Plasmid analysis unveiled nine distinct plasmids associated with AMR genes in these isolates. Chromosomally encoded blaSCO-1 was present in three S. Typhimurium and two S. Muenster isolates from equine samples, conferring resistance to amoxicillin/clavulanic acid. Phylogenetic analysis revealed three distinct clusters for these five isolates, indicating evolutionary divergence. This study represents the first report of blaSCO-1 in the USA, and our recovered isolates harboring this gene as early as 1989 precede those of all other reports. The enigmatic nature of blaSCO-1 prompts further research into its function. Our findings highlight the urgency of addressing antimicrobial resistance in Salmonella for effective public health interventions.

Technical Abstract: Antimicrobial resistance (AMR) in non-typhoidal Salmonella is a pressing public health concern in the United States, necessitating continuous surveillance. We conducted a retrospective analysis of 251 Salmonella isolates from 11 animal species recovered between 1982 and 1999, utilizing serotyping, antimicrobial susceptibility testing, and whole-genome sequencing (WGS). Phenotypic resistance was observed in 101 isolates, with S. Typhimurium, S. Dublin, S. Agona, and S. Muenster prevailing among 36 identified serovars. Notably, resistance to 12 of 17 antibiotics was detected, with ampicillin being most prevalent (79/251). We identified 38 resistance genes, primarily mediating aminoglycoside (n = 13) and ß-lactamase (n = 6) resistance. Plasmid analysis unveiled nine distinct plasmids associated with AMR genes in these isolates. Chromosomally encoded blaSCO-1 was present in three S. Typhimurium and two S. Muenster isolates from equine samples, conferring resistance to amoxicillin/clavulanic acid. Phylogenetic analysis revealed three distinct clusters for these five isolates, indicating evolutionary divergence. This study represents the first report of blaSCO-1 in the USA, and our recovered isolates harboring this gene as early as 1989 precede those of all other reports. The enigmatic nature of blaSCO-1 prompts further research into its function. Our findings highlight the urgency of addressing antimicrobial resistance in Salmonella for effective public health interventions.