A systematic review of expanding Salmonella enterica serovar Indiana from China: Prevalence, antimicrobial resistance and genomic characterization

Abstract

Salmonella Indiana has emerged as a significantly expanded foodborne pathogen in China, posing a formidable challenge to food safety and public health. This review summarized the prevalence, antimicrobial resistance, plasmid transferability, and population structure of S. Indiana isolates from China. S. Indiana exhibited a wide geographical distribution, encompassing at least 24 provinces or municipalities across China, with a notable epidemic presence in breeding animals and retail meat products, particularly chicken. Alarmingly, high-level antimicrobial resistances were observed, including nalidixic acid (96.3%), trimethoprim-sulfamethoxazole (93.5%), ciprofloxacin (91.8%), ampicillin (90.5%), sulfisoxazole (87.2%), chloramphenicol (84.8%), tetracycline (82.7%), cefotaxime (82.5%), and ceftriaxone (81.0%). Crucially, the ciprofloxacin resistance observed was attributed to a synergistic effect of plasmid-mediated quinolone resistance (PMQR) genes [aac(6′)-Ib-cr, oqxAB, qnr] and mutations in the quinolone resistance determining region (QRDR) (gyrA and parC). Furthermore, multiple drug resistance was facilitated by the IncHI2 plasmids, P1-like phage plasmids, and hybrid plasmids, which serve as reservoirs for a plethora of antimicrobial resistance genes. These plasmids actively engaged in gene exchange, mediated by mobile genetic elements such as insertion sequences, transposons, and prophages. Phylogenetic analysis revealed that Chinese S. Indiana isolates cluster within clade I and demonstrate international dissemination, sharing close genetic relationships with isolates from the United Kingdom and the United States. This review highlighted the urgency for necessary strategies to prevent the further dissemination of these emerging MDR pathogens. Concerted efforts aimed at enhancing surveillance, promoting prudent antimicrobial use, and fostering international collaboration are imperative to safeguard public health and maintain food safety standards.