Prevalence and Characterization of Staphylococcus aureus Isolated From Pasteurized Milk in China

Staphylococcus aureus is one of the most important food-borne pathogens globally. It produces various toxins and invasive enzymes and can be found in numerous food products. Milk is an important source of staphylococcal food poisoning. After pasteurization, this microorganism or its enterotoxins mig...

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Main Authors: Jingsha Dai, Shi Wu, Jiahui Huang, Qingping Wu, Feng Zhang, Jumei Zhang, Juan Wang, Yu Ding, Shuhong Zhang, Xiaojuan Yang, Tao Lei, Liang Xue, Haoming Wu
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-04-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.00641/full
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author Jingsha Dai
Shi Wu
Jiahui Huang
Qingping Wu
Feng Zhang
Feng Zhang
Jumei Zhang
Juan Wang
Yu Ding
Shuhong Zhang
Xiaojuan Yang
Tao Lei
Liang Xue
Haoming Wu
author_facet Jingsha Dai
Shi Wu
Jiahui Huang
Qingping Wu
Feng Zhang
Feng Zhang
Jumei Zhang
Juan Wang
Yu Ding
Shuhong Zhang
Xiaojuan Yang
Tao Lei
Liang Xue
Haoming Wu
author_sort Jingsha Dai
collection DOAJ
description Staphylococcus aureus is one of the most important food-borne pathogens globally. It produces various toxins and invasive enzymes and can be found in numerous food products. Milk is an important source of staphylococcal food poisoning. After pasteurization, this microorganism or its enterotoxins might still remain in pasteurized milk. Therefore, this study was to investigate the contamination of S. aureus in 258 pasteurized milk from 39 cities of China. The prevalence and levels of S. aureus in these samples as well as antibiotic susceptibility profiles, virulence genes, biofilm formation, and biofilm related genes, spa typing and MLST were used to determine the characterization among the isolates. It was found 3.9% of samples were detected S. aureus in 8 of 39 cities in China. The contaminated level were not very excessive which showed the MPN values of the most positive samples (9/10) were less than 1 MPN/g. All pasteurized milk-related S. aureus isolates have ability to produce biofilm and harbored icaA, icaD, eno, clfA, clfB, fnbA, fnbB, fib genes, other biofilm related genes icaC were showed in 91.7% of isolates and cna gene were showed in 50%, except bap gene which were free in all isolates. The antibiotic susceptibility test showed that all isolates were resistant or intermediate-resistant to different concentrations of the antibiotics. Furthermore, 75.0% of the isolates were resistant to three or more antibiotic classes, which indicated multidrug resistance. The isolates had virulence potential, which showed 66.7% (8/12) of the isolates carried one or more virulence-associated genes. Molecular typing by MLST and spa typing enabled classification of these isolates into a total of 11 sequence types (STs) and spa types, which indicated high genetic diversity. Most of these types were related to various clinical S. aureus infections. Thus, the findings of this study reflect the potential risk of S. aureus infection in China. Our study also provides comprehensive analysis of the prevalence of S. aureus in pasteurized milk and helps ensure more accurate treatment of human infection with effective antibiotics.
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spelling doaj.art-0d388b2b5d094b51a5561d1a5f1dd9ea2022-12-21T17:48:55ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-04-011010.3389/fmicb.2019.00641439159Prevalence and Characterization of Staphylococcus aureus Isolated From Pasteurized Milk in ChinaJingsha Dai0Shi Wu1Jiahui Huang2Qingping Wu3Feng Zhang4Feng Zhang5Jumei Zhang6Juan Wang7Yu Ding8Shuhong Zhang9Xiaojuan Yang10Tao Lei11Liang Xue12Haoming Wu13Guangdong Institute of Microbiology, State Key Laboratory of Applied Microbiology Southern China, Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, Guangdong Open Laboratory of Applied Microbiology, Guangzhou, ChinaGuangdong Institute of Microbiology, State Key Laboratory of Applied Microbiology Southern China, Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, Guangdong Open Laboratory of Applied Microbiology, Guangzhou, ChinaGuangdong Institute of Microbiology, State Key Laboratory of Applied Microbiology Southern China, Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, Guangdong Open Laboratory of Applied Microbiology, Guangzhou, ChinaGuangdong Institute of Microbiology, State Key Laboratory of Applied Microbiology Southern China, Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, Guangdong Open Laboratory of Applied Microbiology, Guangzhou, ChinaGuangdong Institute of Microbiology, State Key Laboratory of Applied Microbiology Southern China, Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, Guangdong Open Laboratory of Applied Microbiology, Guangzhou, ChinaSchool of Bioscience and Bioengineering, South China University of Technology, Guangzhou, ChinaGuangdong Institute of Microbiology, State Key Laboratory of Applied Microbiology Southern China, Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, Guangdong Open Laboratory of Applied Microbiology, Guangzhou, ChinaCollege of Food Science, South China Agricultural University, Guangzhou, ChinaDepartment of Food Science and Technology, Jinan University, Guangzhou, ChinaGuangdong Institute of Microbiology, State Key Laboratory of Applied Microbiology Southern China, Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, Guangdong Open Laboratory of Applied Microbiology, Guangzhou, ChinaGuangdong Institute of Microbiology, State Key Laboratory of Applied Microbiology Southern China, Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, Guangdong Open Laboratory of Applied Microbiology, Guangzhou, ChinaGuangdong Institute of Microbiology, State Key Laboratory of Applied Microbiology Southern China, Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, Guangdong Open Laboratory of Applied Microbiology, Guangzhou, ChinaGuangdong Institute of Microbiology, State Key Laboratory of Applied Microbiology Southern China, Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, Guangdong Open Laboratory of Applied Microbiology, Guangzhou, ChinaGuangdong Institute of Microbiology, State Key Laboratory of Applied Microbiology Southern China, Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, Guangdong Open Laboratory of Applied Microbiology, Guangzhou, ChinaStaphylococcus aureus is one of the most important food-borne pathogens globally. It produces various toxins and invasive enzymes and can be found in numerous food products. Milk is an important source of staphylococcal food poisoning. After pasteurization, this microorganism or its enterotoxins might still remain in pasteurized milk. Therefore, this study was to investigate the contamination of S. aureus in 258 pasteurized milk from 39 cities of China. The prevalence and levels of S. aureus in these samples as well as antibiotic susceptibility profiles, virulence genes, biofilm formation, and biofilm related genes, spa typing and MLST were used to determine the characterization among the isolates. It was found 3.9% of samples were detected S. aureus in 8 of 39 cities in China. The contaminated level were not very excessive which showed the MPN values of the most positive samples (9/10) were less than 1 MPN/g. All pasteurized milk-related S. aureus isolates have ability to produce biofilm and harbored icaA, icaD, eno, clfA, clfB, fnbA, fnbB, fib genes, other biofilm related genes icaC were showed in 91.7% of isolates and cna gene were showed in 50%, except bap gene which were free in all isolates. The antibiotic susceptibility test showed that all isolates were resistant or intermediate-resistant to different concentrations of the antibiotics. Furthermore, 75.0% of the isolates were resistant to three or more antibiotic classes, which indicated multidrug resistance. The isolates had virulence potential, which showed 66.7% (8/12) of the isolates carried one or more virulence-associated genes. Molecular typing by MLST and spa typing enabled classification of these isolates into a total of 11 sequence types (STs) and spa types, which indicated high genetic diversity. Most of these types were related to various clinical S. aureus infections. Thus, the findings of this study reflect the potential risk of S. aureus infection in China. Our study also provides comprehensive analysis of the prevalence of S. aureus in pasteurized milk and helps ensure more accurate treatment of human infection with effective antibiotics.https://www.frontiersin.org/article/10.3389/fmicb.2019.00641/fullStaphylococcus aureuspasteurized milkrisk assessmentvirulence genesantibiotic resistancebiofilm formation
spellingShingle Jingsha Dai
Shi Wu
Jiahui Huang
Qingping Wu
Feng Zhang
Feng Zhang
Jumei Zhang
Juan Wang
Yu Ding
Shuhong Zhang
Xiaojuan Yang
Tao Lei
Liang Xue
Haoming Wu
Prevalence and Characterization of Staphylococcus aureus Isolated From Pasteurized Milk in China
Frontiers in Microbiology
Staphylococcus aureus
pasteurized milk
risk assessment
virulence genes
antibiotic resistance
biofilm formation
title Prevalence and Characterization of Staphylococcus aureus Isolated From Pasteurized Milk in China
title_full Prevalence and Characterization of Staphylococcus aureus Isolated From Pasteurized Milk in China
title_fullStr Prevalence and Characterization of Staphylococcus aureus Isolated From Pasteurized Milk in China
title_full_unstemmed Prevalence and Characterization of Staphylococcus aureus Isolated From Pasteurized Milk in China
title_short Prevalence and Characterization of Staphylococcus aureus Isolated From Pasteurized Milk in China
title_sort prevalence and characterization of staphylococcus aureus isolated from pasteurized milk in china
topic Staphylococcus aureus
pasteurized milk
risk assessment
virulence genes
antibiotic resistance
biofilm formation
url https://www.frontiersin.org/article/10.3389/fmicb.2019.00641/full
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