Genomic Investigation of Salmonella Isolates Recovered From a Pig Slaughtering Process in Hangzhou, China

Beibei Wu; Abdelaziz Ed-Dra; Hang Pan; Chenghang Dong; Chenghao Jia; Min Yue

doi:10.3389/fmicb.2021.704636

Genomic Investigation of Salmonella Isolates Recovered From a Pig Slaughtering Process in Hangzhou, China

Front Microbiol. 2021 Jul 8:12:704636. doi: 10.3389/fmicb.2021.704636. eCollection 2021.

Authors

Beibei Wu¹, Abdelaziz Ed-Dra², Hang Pan³, Chenghang Dong³, Chenghao Jia³, Min Yue^{2

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Affiliations

¹ Zhejiang Provincial Center for Disease Control and Prevention, Hangzhou, China.
² Hainan Institute of Zhejiang University, Sanya, China.
³ Department of Veterinary Medicine, Institute of Preventive Veterinary Sciences, Zhejiang University College of Animal Sciences, Hangzhou, China.
⁴ State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, National Clinical Research Center for Infectious Diseases, National Medical Center for Infectious Diseases, The First Affiliated Hospital, College of Medicine, Zhejiang University, Hangzhou, China.
⁵ Zhejiang Provincial Key Laboratory of Preventive Veterinary Medicine, Hangzhou, China.

Abstract

The pig industry is the principal source of meat products in China, and the presence of pathogens in pig-borne meat is a crucial threat to public health. Salmonella is the major pathogen associated with pig-borne diseases. However, route surveillance by genomic platforms along the food chain is still limited in China. Here, we conducted a study to evaluate the dynamic prevalence of Salmonella in a pig slaughtering process in Hangzhou, Zhejiang Province, China. Fifty-five of 226 (24.37%) samples were positive for Salmonella; from them, 78 different isolates were selected and subjected to whole genome sequencing followed by bioinformatics analyses to determine serovar distribution, MLST patterns, antimicrobial resistance genes, plasmid replicons, and virulence factors. Moreover, phenotypic antimicrobial resistance was performed using the broth dilution method against 14 antimicrobial agents belonging to 10 antimicrobial classes. Our results showed that samples collected from the dehairing area (66.66%) and the splitting area (57.14%) were the most contaminated. Phenotypic antimicrobial resistance classified 67 of 78 isolates (85.90%) as having multidrug resistance (MDR), while the highest resistance was observed in tetracycline (85.90%; 67/78) followed by ampicillin (84.62%; 66/78), chloramphenicol (71.80%; 56/78), and nalidixic acid (61.54%; 48/78). Additionally, serovar prediction showed the dominance of Salmonella Typhimurium ST19 (51.28%; 40/78) among the 78 studied isolates, while plasmid prediction reported the dominance of IncHI2A_1 (20.51%; 16/78), followed by IncX1_1 (17.95%; 14/78) and IncHI2_1 (11.54%; 9/78). Virulence factor prediction showed the detection of cdtB gene encoding typhoid toxins in two Salmonella Goldcoast ST358 and one Salmonella Typhimurium ST19, while one isolate of Salmonella London ST155 was positive for genes encoding for the siderophore "yersiniabactin" and the gene senB encoding for enterotoxin production. From this study, we conclude that pig slaughterhouses are critical points for the dissemination of virulent and multidrug-resistant Salmonella isolates along the food chain which require the implementation of management systems to control the critical points. Moreover, there is an urgent need for the implementation of the whole genome sequencing platform to monitor the emergence of virulent and multidrug-resistant clones along the food chain.

Keywords: Salmonella; antimicrobial resistance; pig slaughterhouse; plasmid replicons; virulence factors; whole genome sequencing.