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

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 stil...

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Main Authors: Beibei Wu, Abdelaziz Ed-Dra, Hang Pan, Chenghang Dong, Chenghao Jia, Min Yue
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-07-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.704636/full
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author Beibei Wu
Abdelaziz Ed-Dra
Hang Pan
Chenghang Dong
Chenghao Jia
Min Yue
Min Yue
Min Yue
Min Yue
author_facet Beibei Wu
Abdelaziz Ed-Dra
Hang Pan
Chenghang Dong
Chenghao Jia
Min Yue
Min Yue
Min Yue
Min Yue
author_sort Beibei Wu
collection DOAJ
description 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.
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spelling doaj.art-b5b2543d920d457bb9cf7321982e8a5c2022-12-21T17:59:57ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-07-011210.3389/fmicb.2021.704636704636Genomic Investigation of Salmonella Isolates Recovered From a Pig Slaughtering Process in Hangzhou, ChinaBeibei Wu0Abdelaziz Ed-Dra1Hang Pan2Chenghang Dong3Chenghao Jia4Min Yue5Min Yue6Min Yue7Min Yue8Zhejiang Provincial Center for Disease Control and Prevention, Hangzhou, ChinaHainan Institute of Zhejiang University, Sanya, ChinaDepartment of Veterinary Medicine, Institute of Preventive Veterinary Sciences, Zhejiang University College of Animal Sciences, Hangzhou, ChinaDepartment of Veterinary Medicine, Institute of Preventive Veterinary Sciences, Zhejiang University College of Animal Sciences, Hangzhou, ChinaDepartment of Veterinary Medicine, Institute of Preventive Veterinary Sciences, Zhejiang University College of Animal Sciences, Hangzhou, ChinaHainan Institute of Zhejiang University, Sanya, ChinaDepartment of Veterinary Medicine, Institute of Preventive Veterinary Sciences, Zhejiang University College of Animal Sciences, Hangzhou, ChinaState 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, ChinaZhejiang Provincial Key Laboratory of Preventive Veterinary Medicine, Hangzhou, ChinaThe 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.https://www.frontiersin.org/articles/10.3389/fmicb.2021.704636/fullSalmonellaantimicrobial resistanceplasmid repliconsvirulence factorspig slaughterhousewhole genome sequencing
spellingShingle Beibei Wu
Abdelaziz Ed-Dra
Hang Pan
Chenghang Dong
Chenghao Jia
Min Yue
Min Yue
Min Yue
Min Yue
Genomic Investigation of Salmonella Isolates Recovered From a Pig Slaughtering Process in Hangzhou, China
Frontiers in Microbiology
Salmonella
antimicrobial resistance
plasmid replicons
virulence factors
pig slaughterhouse
whole genome sequencing
title Genomic Investigation of Salmonella Isolates Recovered From a Pig Slaughtering Process in Hangzhou, China
title_full Genomic Investigation of Salmonella Isolates Recovered From a Pig Slaughtering Process in Hangzhou, China
title_fullStr Genomic Investigation of Salmonella Isolates Recovered From a Pig Slaughtering Process in Hangzhou, China
title_full_unstemmed Genomic Investigation of Salmonella Isolates Recovered From a Pig Slaughtering Process in Hangzhou, China
title_short Genomic Investigation of Salmonella Isolates Recovered From a Pig Slaughtering Process in Hangzhou, China
title_sort genomic investigation of salmonella isolates recovered from a pig slaughtering process in hangzhou china
topic Salmonella
antimicrobial resistance
plasmid replicons
virulence factors
pig slaughterhouse
whole genome sequencing
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.704636/full
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