Our previous study revealed that Salmonella enterica serovar Schwarzengrund-contaminated areas of broiler chickens have expanded from West Japan to East Japan. The present study investigated the antimicrobial resistance and molecular characteristics of 124 S. Schwarzengrund isolates obtained from chicken meat produced in East and West Japan from 2008 to 2019. Comparing the isolates obtained in 2008 and 2015–2019, an increase in the proportion of those resistant to kanamycin [51.4–89.7% (p < 0.001)] was observed. In contrast, the proportion of isolates resistant to both streptomycin and tetracycline and those that harbored a 1.0-kb class 1 integron, aadA1, and tetA, significantly decreased from 100% in 2008 to 47.1% in 2015–2019 (p < 0.001). A 1.0-kb class 1 integron containing aadA1, harbored by 78 isolates, was different from that reported in globally distributed S. Schwarzengrund strains (1.9 kb, containing the dfrA12-aadA2 gene cassette). Twenty-five isolates from different product districts and years of isolation were typed as sequence type (ST) 241 with multilocus sequence typing. Our results suggest that S. Schwarzengrund, which contaminates chicken meat in Japan, shares a common ancestor regardless of the product district from 2008 to recent years. Moreover, S. Schwarzengrund ST241 may have spread from western to eastern Japan.

Background/Objectives: The acquisition of antimicrobial resistance by foodborne pathogens is a serious human health concern. In Japan, combinations of antimicrobial resistance genes in Salmonella from chicken meat were common among several serovars. Therefore, we hypothesized that different S. enterica serovars share a common antimicrobial resistance plasmid. Methods: Antimicrobial resistance transfer was tested in S. Infantis and S. Schwarzengrund, the major serovars used as donors. The plasmid structure was determined by subjecting S. Infantis Sal_238 and S. Schwarzengrund Sal_249 to short- and long-read sequencing. Results: The high homology between pSal_249Sch and pSal_238Inf suggests they have a common ancestor. Because the sequences of pSal_238Inf and pSal_249Sch were highly homologous to pESI (a plasmid for emerging S. Infantis), pSal_238Inf and pSal_249Sch were identified as pESI-like plasmids. S. Schwarzengrund is the third Salmonella serovar to expand its distribution related to pESI-like plasmid acquisition. Core-genome multilocus sequence-type analysis revealed that S. Schwarzengrund isolates with pESI-like plasmids from Japan (core-genome sequence-type [cgST] 167363 and cgST287831), the UK (cgST167363), and the USA (cgST167363, cgST196045, and cgST287831) were closely related; they are also suggested to share a common ancestor. The transfer of antimicrobial resistance was observed in combinations of both serovars. Specifically, the tentative plasmid sequence obtained via short-read sequencing, PCR, and conjugation experiments identified deletions of antimicrobial resistance genes (aadA, sul1, and tetA), class 1 integron, mercury resistance operon, and/or plasmid transfer region in the pESI-like plasmid. Conclusion: These data on the structural diversity of pESI-like plasmids suggest that some time has passed since S. Schwarzengrund acquired them.