Characterization of non-typhoidal Salmonella reveals the highly prevalent mcr-1-positive S. 1,4,[5],12:i:- within eggs are derived from chickens

Abstract

Salmonella is one of the most common foodborne pathogens. Antimicrobial-resistant Salmonella isolates, especially those resistant to colistin, pose a significant threat to public health worldwide. However, data about the prevalence of mcr-positive Salmonella in animals was few and the dissemination of mcr-positive Salmonella from animals to food, especially eggs, has not been fully addressed. The role of houseflies in the Salmonella transmission has also not been clarified. Here, we analyzed the prevalence and resistance characteristics of mcr-positive Salmonella in 1707 samples of animals (commercial laying hens, broilers, waterfowls and swine), eggs and flies from 23 farms in four cities of China between July 2021 and October 2022. Pulsed-field gel electrophoresis (PFGE) and whole-genome sequencing (WGS) analyses of Salmonella from different sources were further performed. Among animals, waterfowls had the highest isolation rate of Salmonella (18.1 %, 35/193), followed by swine (6.1 %, 23/377), laying hens (4.2 %, 21/505) and broilers (1.4 %, 7/489). Two of the 53 flies (3.8 %) carried Salmonella. The detection rate of Salmonella in eggs from farms was 26.7 %. All mcr-1-positive Salmonella isolates were S. 1,4,[5],12:i:- and were only found in hens (0.2 %) and eggs (11.1 %). PFGE and WGS analyses showed that the mcr-1-positive S. 1,4,[5],12:i:- from commercial laying hens and eggs in the same farm had no single nucleotide polymorphism (SNP) variation, indicating that the mcr-1-positive S. 1,4,[5],12:i:- in eggs were derived from hens. The phylogenomic analysis also showed that the mcr-1-positive S. 1,4,[5],12:i:- isolates from hens and eggs were closely related to previously reported mcr-1-positive Salmonella from human in China, further confirming that such mcr-1-positive Salmonella in animals could transmit to humans via the food chain. Furthermore, the bla_CTX-M-1G-positive S. Kentucky isolates from broiler and flies in the same farm had a limited number of variations (5–7 SNPs), proving the clonal transmission of Salmonella between broilers and flies. The S. Kentucky isolates carrying bla_CTX-M-1G from broilers were also closely related to the S. Kentucky isolates from chicken meats and humans. Our findings suggest that Salmonella including those carrying mcr-1 in animals could transmit to eggs/meats and potentially trigger human infections. The houseflies can play an important role in the Salmonella transmission within farms. Salmonella carrying mcr in animals and animal products should be monitored regularly and control measures are urgently needed to reduce the dissemination of such pathogens.