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Article(id=1153429498730107175, tenantId=1146029695717560320, journalId=1149652044408987649, issueId=1153429493357203682, articleNumber=null, orderNo=null, doi=10.19812/j.cnki.jfsq11-5956/ts.20241008007, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=null, receivedDate=1728316800000, receivedDateStr=2024-10-08, revisedDate=null, revisedDateStr=null, acceptedDate=null, acceptedDateStr=null, onlineDate=1752928622181, onlineDateStr=2025-07-19, pubDate=1741968000000, pubDateStr=2025-03-15, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1752928622181, onlineIssueDateStr=2025-07-19, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1752928622181, creator=13701087609, updateTime=1752928622181, updator=13701087609, issue=Issue{id=1153429493357203682, tenantId=1146029695717560320, journalId=1149652044408987649, year='2025', volume='16', issue='5', pageStart='1', pageEnd='326', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=0, createTime=1752928620900, creator=13701087609, updateTime=1758690311058, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1177595773500932351, tenantId=1146029695717560320, journalId=1149652044408987649, issueId=1153429493357203682, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1177595773500932352, tenantId=1146029695717560320, journalId=1149652044408987649, issueId=1153429493357203682, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=262, endPage=268, ext={EN=ArticleExt(id=1153429499300532529, articleId=1153429498730107175, tenantId=1146029695717560320, journalId=1149652044408987649, language=EN, title=Molecular typing, antibiotic resistance characteristics, and virulence gene analysis of some food-borne methicillin-resistant Staphylococcus aureus in Ningxia, columnId=1151895321388347923, journalTitle=Journal of Food Safety & Quality, columnName=Food Analysis and Detection, runingTitle=null, highlight=null, articleAbstract=

Objective To investigate the type and drug resistance characteristics and virulence gene carrying of some food-borne methicillin-resistant Staphylococcus aureu (MRSA) in Ningxia. Methods MRSA isolates from some food risk monitoring in Ningxia were collected and subjected to drug susceptibility testing, pulsed-field gel electrophoresis (PFGE), and whole-genome sequencing analysis respectively. Results PFGE typing of 9 food-borne MRSA strains was divided into 3 clusters and 8 kinds of types, all of which were more than 85% provenance. ST typing of the whole genome sequencing results was divided into 4 kinds of ST types, 6 strains were ST59, and the other 3 strains were ST3355, ST7 and ST965, respectively. MRSA were all multi-drug resistant, which carrying different resistance genes and virulence genes, resulting in different drug resistance phenotypes. Conclusion Foodborne MRSA isolates have a large number of genes related to antibiotic resistance and pathogenicity, which pose a significant threat to human health. Therefore, it is of great importance to continuously monitor and take effective measures to reduce the contamination level of MRSA in food to ensure food safety.

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目的 了解宁夏地区部分食源性耐甲氧西林金黄色葡萄球菌(methicillin-resistant Staphylococcus aureu, MRSA)的分型特征和耐药特征以及与毒力基因携带情况。方法 收集宁夏地区部分食品风险监测分离的MRSA, 分别进行药物敏感试验、脉冲场凝胶电泳(pulsed-fiedld gel electrophoresis, PFGE)以及全基因组测序分析。结果 9株来自食源性的MRSA菌株PFGE分型分为3簇8种型别其源性都在85%以上, 全基因组测序结果ST分型分为4种ST型, 6株为ST59, 其余3株分别为ST3355、ST7、ST965。MRSA均为多重耐药, 携带耐药基因以及毒力基因也各不相同, 导致的耐药表型也存在差异。结论 食源性分离MRSA基因组中存在大量与耐药和致病相关基因, 这些基因给人类健康带来巨大威胁, 因此持续监测并采取有效措施降低食品中MRSA的污染水平, 以确保食品安全。

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* 魏琼(1986—), 女, 副主任技师, 主要研究方向为传染病微生物及食源性微生物检验。E-mail:
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沈梅(1985—), 女, 硕士, 副主任技师, 主要研究方向为传染病微生物、食源性和环境微生物检验。E-mail:

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沈梅(1985—), 女, 硕士, 副主任技师, 主要研究方向为传染病微生物、食源性和环境微生物检验。E-mail:

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沈梅(1985—), 女, 硕士, 副主任技师, 主要研究方向为传染病微生物、食源性和环境微生物检验。E-mail:

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articleId=1153429498730107175, language=CN, orderNo=1, keyword=耐甲氧西林金黄色葡萄球菌), Keyword(id=1177619372995653662, tenantId=1146029695717560320, journalId=1149652044408987649, articleId=1153429498730107175, language=CN, orderNo=2, keyword=分型特征), Keyword(id=1177619373066956832, tenantId=1146029695717560320, journalId=1149652044408987649, articleId=1153429498730107175, language=CN, orderNo=3, keyword=耐药特征), Keyword(id=1177619373205368867, tenantId=1146029695717560320, journalId=1149652044408987649, articleId=1153429498730107175, language=CN, orderNo=4, keyword=毒力基因)], refs=[Reference(id=1177619375424155718, tenantId=1146029695717560320, journalId=1149652044408987649, articleId=1153429498730107175, doi=null, pmid=null, pmcid=null, year=2023, volume=18, issue=10, pageStart=1117, pageEnd=1126, url=null, language=null, rfNumber=[1], rfOrder=0, authorNames=姜华, 何晓娟, 卢星辰, journalName=中国病原生物学杂志, refType=null, unstructuredReference=姜华, 何晓娟, 卢星辰, 等. 鸡肉源耐甲氧西林金黄色葡萄球菌全基因组测序及生物信息学分析[J]. 中国病原生物学杂志, 2023, 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Internation Journal of Infectious Diseases, 2023, 17: 1085., articleTitle=Whole genome characterization of methicillin-resistant Staphylococcus spp. isolates from aquaculture-cultivated shrimps, refAbstract=null)], funds=[Fund(id=1177619375201857603, tenantId=1146029695717560320, journalId=1149652044408987649, articleId=1153429498730107175, awardId=2022AAC03711, language=CN, fundingSource=宁夏自然科学基金项目(2022AAC03711), fundOrder=null, country=null)], companyList=[AuthorCompany(id=1177619370806227951, tenantId=1146029695717560320, journalId=1149652044408987649, articleId=1153429498730107175, xref=null, ext=[AuthorCompanyExt(id=1177619370814616560, tenantId=1146029695717560320, journalId=1149652044408987649, articleId=1153429498730107175, companyId=1177619370806227951, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=Ningxia Hui Autonomous Region Center for Disease Control and Prevention, Ningxia Academy of Preventive Medicine Yinchuan 750004, China), AuthorCompanyExt(id=1177619370818810865, tenantId=1146029695717560320, journalId=1149652044408987649, articleId=1153429498730107175, companyId=1177619370806227951, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=宁夏回族自治区疾病预防控制中心, 宁夏预防医学科学院 银川 750004)])], figs=[ArticleFig(id=1177619373670936616, tenantId=1146029695717560320, journalId=1149652044408987649, articleId=1153429498730107175, language=EN, label=Fig.1, caption=Cluster analysis diagram of PFGE, figureFileSmall=uKWE3RULCYDXx6Vp0LOAbA==, figureFileBig=NJIa8paD1oSVfsPJTicpgw==, tableContent=null), ArticleFig(id=1177619373784182826, tenantId=1146029695717560320, journalId=1149652044408987649, articleId=1153429498730107175, language=CN, label=图1, caption=PFGE聚类分析图, figureFileSmall=uKWE3RULCYDXx6Vp0LOAbA==, figureFileBig=NJIa8paD1oSVfsPJTicpgw==, tableContent=null), ArticleFig(id=1177619373880651820, tenantId=1146029695717560320, journalId=1149652044408987649, articleId=1153429498730107175, language=EN, label=Fig.2, caption=Heat map of MRSA virulence gene, figureFileSmall=r/BOa2Sf5AS3YxWGgKR0fw==, figureFileBig=9CGZ9QxhLionxqVj8iE7uQ==, tableContent=null), ArticleFig(id=1177619373960343598, tenantId=1146029695717560320, journalId=1149652044408987649, articleId=1153429498730107175, language=CN, label=图2, caption=MRSA毒力基因热图, figureFileSmall=r/BOa2Sf5AS3YxWGgKR0fw==, figureFileBig=9CGZ9QxhLionxqVj8iE7uQ==, tableContent=null), ArticleFig(id=1177619374090367024, tenantId=1146029695717560320, journalId=1149652044408987649, articleId=1153429498730107175, language=EN, label=Table 1, caption=

Drug susceptibility phenotype analysis of 9 strains of food-borne MRSA strains

, figureFileSmall=null, figureFileBig=null, tableContent=
抗生素 耐药株数 耐药率
/%		 中介
株数		 中介率
/%		 敏感
株数		 敏感率
/%
PEN 9 100 0 0 0 0
E/C 9 100 0 0 0 0
ERY 8 88.89 1 11.11 0 0
CLI 7 77.78 1 11.11 1 11.11
OXC 7 77.78 0 0 2 22.22
CFX 7 77.78 0 0 2 22.22
TET 5 55.56 0 0 4 44.44
GEN 3 33.33 2 22.22 4 44.45
LEV 2 22.22 0 0 7 77.78
NIT 2 22.22 0 0 7 77.78
VAN 0 0 0 0 9 100
TEC 0 0 1 11.11 8 88.89
RIF 0 0 0 0 9 100
SXT 0 0 0 0 9 100
DAP 0 0 0 0 9 100
LZD 0 0 0 0 9 100
), ArticleFig(id=1177619374283305011, tenantId=1146029695717560320, journalId=1149652044408987649, articleId=1153429498730107175, language=CN, label=表1, caption=

9株食源性MRSA的药敏表型分析

, figureFileSmall=null, figureFileBig=null, tableContent=
抗生素 耐药株数 耐药率
/%		 中介
株数		 中介率
/%		 敏感
株数		 敏感率
/%
PEN 9 100 0 0 0 0
E/C 9 100 0 0 0 0
ERY 8 88.89 1 11.11 0 0
CLI 7 77.78 1 11.11 1 11.11
OXC 7 77.78 0 0 2 22.22
CFX 7 77.78 0 0 2 22.22
TET 5 55.56 0 0 4 44.44
GEN 3 33.33 2 22.22 4 44.45
LEV 2 22.22 0 0 7 77.78
NIT 2 22.22 0 0 7 77.78
VAN 0 0 0 0 9 100
TEC 0 0 1 11.11 8 88.89
RIF 0 0 0 0 9 100
SXT 0 0 0 0 9 100
DAP 0 0 0 0 9 100
LZD 0 0 0 0 9 100
), ArticleFig(id=1177619374421717046, tenantId=1146029695717560320, journalId=1149652044408987649, articleId=1153429498730107175, language=EN, label=Table 2, caption=

Multidrug-resistance spectra of 9 strains of MRSA

, figureFileSmall=null, figureFileBig=null, tableContent=
菌株编号 耐药谱
NX15012 ERY-CLI-LEV-PEN-E/C
NX15070 OXC-ERY-CLI-LEV-GEN-PEN-E/C-CFX
NX15072 ERY-CLI-TET-PEN-E/C
NX16081 OXC-ERY-CLI-TET-GEN-PEN-E/C-CFX
NX17019 OXC-ERY-CLI-PEN-E/C-CFX
NX17293 OXC-TET-PEN-E/C-CFX
NX18024 OXC-ERY-CLI-PEN-E/C-CFX
NX19035 OXC-ERY-TET-PEN-E/C-CFX
NX20050 OXC-ERY-CLI-TET-GEN-PEN-E/C-CFX-NIT
), ArticleFig(id=1177619374564323384, tenantId=1146029695717560320, journalId=1149652044408987649, articleId=1153429498730107175, language=CN, label=表2, caption=

9株MRSA的多重耐药谱

, figureFileSmall=null, figureFileBig=null, tableContent=
菌株编号 耐药谱
NX15012 ERY-CLI-LEV-PEN-E/C
NX15070 OXC-ERY-CLI-LEV-GEN-PEN-E/C-CFX
NX15072 ERY-CLI-TET-PEN-E/C
NX16081 OXC-ERY-CLI-TET-GEN-PEN-E/C-CFX
NX17019 OXC-ERY-CLI-PEN-E/C-CFX
NX17293 OXC-TET-PEN-E/C-CFX
NX18024 OXC-ERY-CLI-PEN-E/C-CFX
NX19035 OXC-ERY-TET-PEN-E/C-CFX
NX20050 OXC-ERY-CLI-TET-GEN-PEN-E/C-CFX-NIT
), ArticleFig(id=1177619374631432250, tenantId=1146029695717560320, journalId=1149652044408987649, articleId=1153429498730107175, language=EN, label=Table 3, caption=

MLST typing of 9 strains of MRSA

, figureFileSmall=null, figureFileBig=null, tableContent=
菌株编号 ST分型
NX15012 ST59
NX15070 ST965
NX15072 ST7
NX16081 ST59
NX17019 ST59
NX17293 ST59
NX18024 ST59
NX19035 ST3355
NX20050 ST59
), ArticleFig(id=1177619374727901244, tenantId=1146029695717560320, journalId=1149652044408987649, articleId=1153429498730107175, language=CN, label=表3, caption=

9株MRSA的MLST分型

, figureFileSmall=null, figureFileBig=null, tableContent=
菌株编号 ST分型
NX15012 ST59
NX15070 ST965
NX15072 ST7
NX16081 ST59
NX17019 ST59
NX17293 ST59
NX18024 ST59
NX19035 ST3355
NX20050 ST59
), ArticleFig(id=1177619374895673406, tenantId=1146029695717560320, journalId=1149652044408987649, articleId=1153429498730107175, language=EN, label=Table 4, caption=

Drug resistance gene carrying table of 9 strains of MRSA

, figureFileSmall=null, figureFileBig=null, tableContent=
菌株 耐药基因数量 耐药基因
NX15012 0 未有
NX15070 7 β-内酰胺类(2)、氨基糖苷类(3)、酰胺类(1)大环内酯类和林克霉素类霉素类(1)
NX15072 4 β-内酰胺类(1)、氨基糖苷类(1)、林可酰胺(1)、四环素类(1)
NX16081 6 β-内酰胺类(2)、氨基糖苷类(2)、四环素类(1)、大环内酯类和林克霉素类霉素类(1)
NX17019 5 β-内酰胺类(2)、氨基糖苷类(2)、大环内酯类和林克霉素类霉素类(1)
NX17293 3 β-内酰胺类(2)、四环素类(1)
NX18024 4 β-内酰胺类(2)、大环内酯类和林克霉素类霉素类(2)
NX19035 3 β-内酰胺类(2)、四环素类(1)
NX20050 7 β-内酰胺类(2)、氨基糖苷类(3)、四环素类(1)、大环内酯类和林克霉素类霉素类(1)
), ArticleFig(id=1177619375046668352, tenantId=1146029695717560320, journalId=1149652044408987649, articleId=1153429498730107175, language=CN, label=表4, caption=

9株MRSA菌株耐药基因携带表

, figureFileSmall=null, figureFileBig=null, tableContent=
菌株 耐药基因数量 耐药基因
NX15012 0 未有
NX15070 7 β-内酰胺类(2)、氨基糖苷类(3)、酰胺类(1)大环内酯类和林克霉素类霉素类(1)
NX15072 4 β-内酰胺类(1)、氨基糖苷类(1)、林可酰胺(1)、四环素类(1)
NX16081 6 β-内酰胺类(2)、氨基糖苷类(2)、四环素类(1)、大环内酯类和林克霉素类霉素类(1)
NX17019 5 β-内酰胺类(2)、氨基糖苷类(2)、大环内酯类和林克霉素类霉素类(1)
NX17293 3 β-内酰胺类(2)、四环素类(1)
NX18024 4 β-内酰胺类(2)、大环内酯类和林克霉素类霉素类(2)
NX19035 3 β-内酰胺类(2)、四环素类(1)
NX20050 7 β-内酰胺类(2)、氨基糖苷类(3)、四环素类(1)、大环内酯类和林克霉素类霉素类(1)
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宁夏地区部分食源性耐甲氧西林金黄色葡萄球菌分子分型、耐药特征及毒力基因分析
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沈梅 , 魏琼 * , 杨丽娟 , 刘翔 , 马学旻
食品安全质量检测学报 | 食品分析与检测 2025,16(5): 262-268
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食品安全质量检测学报 | 食品分析与检测 2025, 16(5): 262-268
宁夏地区部分食源性耐甲氧西林金黄色葡萄球菌分子分型、耐药特征及毒力基因分析
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沈梅 , 魏琼* , 杨丽娟, 刘翔, 马学旻
作者信息
  • 宁夏回族自治区疾病预防控制中心, 宁夏预防医学科学院 银川 750004

    • 沈梅(1985—), 女, 硕士, 副主任技师, 主要研究方向为传染病微生物、食源性和环境微生物检验。E-mail:

通讯作者:

* 魏琼(1986—), 女, 副主任技师, 主要研究方向为传染病微生物及食源性微生物检验。E-mail:
Molecular typing, antibiotic resistance characteristics, and virulence gene analysis of some food-borne methicillin-resistant Staphylococcus aureus in Ningxia
Mei SHEN , Qiong WEI* , Li-Juan YANG, Xiang LIU, Xue-Min MA
Affiliations
  • Ningxia Hui Autonomous Region Center for Disease Control and Prevention, Ningxia Academy of Preventive Medicine Yinchuan 750004, China
出版时间: 2025-03-15 doi: 10.19812/j.cnki.jfsq11-5956/ts.20241008007
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摘要
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目的 了解宁夏地区部分食源性耐甲氧西林金黄色葡萄球菌(methicillin-resistant Staphylococcus aureu, MRSA)的分型特征和耐药特征以及与毒力基因携带情况。方法 收集宁夏地区部分食品风险监测分离的MRSA, 分别进行药物敏感试验、脉冲场凝胶电泳(pulsed-fiedld gel electrophoresis, PFGE)以及全基因组测序分析。结果 9株来自食源性的MRSA菌株PFGE分型分为3簇8种型别其源性都在85%以上, 全基因组测序结果ST分型分为4种ST型, 6株为ST59, 其余3株分别为ST3355、ST7、ST965。MRSA均为多重耐药, 携带耐药基因以及毒力基因也各不相同, 导致的耐药表型也存在差异。结论 食源性分离MRSA基因组中存在大量与耐药和致病相关基因, 这些基因给人类健康带来巨大威胁, 因此持续监测并采取有效措施降低食品中MRSA的污染水平, 以确保食品安全。

耐甲氧西林金黄色葡萄球菌  /  分型特征  /  耐药特征  /  毒力基因

Objective To investigate the type and drug resistance characteristics and virulence gene carrying of some food-borne methicillin-resistant Staphylococcus aureu (MRSA) in Ningxia. Methods MRSA isolates from some food risk monitoring in Ningxia were collected and subjected to drug susceptibility testing, pulsed-field gel electrophoresis (PFGE), and whole-genome sequencing analysis respectively. Results PFGE typing of 9 food-borne MRSA strains was divided into 3 clusters and 8 kinds of types, all of which were more than 85% provenance. ST typing of the whole genome sequencing results was divided into 4 kinds of ST types, 6 strains were ST59, and the other 3 strains were ST3355, ST7 and ST965, respectively. MRSA were all multi-drug resistant, which carrying different resistance genes and virulence genes, resulting in different drug resistance phenotypes. Conclusion Foodborne MRSA isolates have a large number of genes related to antibiotic resistance and pathogenicity, which pose a significant threat to human health. Therefore, it is of great importance to continuously monitor and take effective measures to reduce the contamination level of MRSA in food to ensure food safety.

methicillin-resistant Staphylococcus aureus  /  typing characteristic characteristics  /  antimicrobial resistance characteristics  /  virulence genes
沈梅, 魏琼, 杨丽娟, 刘翔, 马学旻. 宁夏地区部分食源性耐甲氧西林金黄色葡萄球菌分子分型、耐药特征及毒力基因分析. 食品安全质量检测学报, 2025 , 16 (5) : 262 -268 . DOI: 10.19812/j.cnki.jfsq11-5956/ts.20241008007
Mei SHEN, Qiong WEI, Li-Juan YANG, Xiang LIU, Xue-Min MA. Molecular typing, antibiotic resistance characteristics, and virulence gene analysis of some food-borne methicillin-resistant Staphylococcus aureus in Ningxia[J]. Journal of Food Safety & Quality, 2025 , 16 (5) : 262 -268 . DOI: 10.19812/j.cnki.jfsq11-5956/ts.20241008007
正文
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0 引言
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耐甲氧西林金黄色葡萄球菌(methicillin-resistant Staphylococcus aureu, MRSA)是金黄色葡萄球菌中特殊的一种, 它能够导致严重的菌血症和其他感染性疾病[1‒3]。MRSA通过耐药基因的水平获得或自身染色体的碱基突变进化出耐药机制, 使其能够在抗生素选择压力下长期生存, 导致多重耐药(multidrug resistant, MDR)的出现, 使得对MRSA的治疗变得更加复杂和困难[4‒5]。
欧洲的一项耐药菌感染所致死亡的调查发现, 在感染所致死亡率排名中, MRSA所致的死亡率高居第2位[6‒8]。近年来我国食源性疾病溯源调查也已发现MRSA导致食物中毒事件的发生, 例如, 成都市46份检出金黄色葡萄球菌的生肉样本, 其中6株为MRSA, 且在不同的肉类中均检出[9], 2014—2018年宝鸡市在肉类、面食凉拌菜等也检测出MRSA[10‒11]。此外速冻食品也有检出MRSA[12-13]的相关报道。食品中MRSA污染可对消费者造成较大的安全风险。各地都有食品来源MRSA致人严重感染的医疗事件报道[14‒16], 并且随着抗生素广泛的使用, 近年来MRSA在食源性产品中的分离率呈上升趋势[16‒17]。MRSA不仅对β-内酰胺酶类耐药, 而且对大环内酯类, 四环素类的等多种抗生素耐药[18‒20]。在抗生素的选择压力下, 多重耐药的“超级细菌”的出现成为严重的公共卫生问题[12]。但都是研究MRSA的某一特征, 没有进行综合性分析以及深入基因组水平的研究报道。伴随着测序技术在各领域的广泛应用, 基于全基因组测序的分子分型技术也被广泛应用在食源性疾病监测和疾病爆发的识别和溯源方面。因此, 为更好地了解食源性MRSA菌株流行特征以及耐药性特征, 为预防和控制MRSA的感染提供。本研究通过对9株食源性MRSA的药物敏感性, PFGE分子分型以及全基因组测序, 多水平综合分析详细阐述食源性MRSA的主要克隆型别、流行特征耐药特征以及毒力基因携带情况, 为后续控制食源性MRSA的污染, 处理突发公共卫生事件和临床治疗提供理论依据。
1 材料与方法
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1.1 材料与试剂
1.1.1 菌株来源
9株MRSA来源于2015—2020年宁夏食品安全风险监测项目中送检的食品样品。分别来自肉与肉制品、地方特色食品和餐饮食品3类。标准菌株金黄色葡萄球菌ATCC29213购自中国医学保藏中心, H9812沙门菌为国家疾控中心传染病所赠予。
1.1.2 试剂
血平板(广东环凯微生物科技有限公司); 药敏板、营养肉汤[复星诊断科技(上海)有限公司]; 溶葡萄球菌酶(1200 U/mL, 美国西格玛奥德里奇公司); SmaI (2000 U/mL)、XbaI (3000 U/mL)内切酶[自宝生物工程(大连有限公司)]; MiSeq v2 Reagent Kit(美国Illumina公司); 基因文库构建磁珠Agenourt XP beads (MF63880)、Qiagen 28104 PCR回收试剂盒、QIAquick聚合酶链式反应(polymerase chain reaction, PCR) Purification试剂盒(50 kit)(德国Qiagen公司); Seakem Glod琼脂糖(美国LONZA公司), 以上试剂均在有效期内使用。
1.2 仪器与设备
Q7 Pro实时荧光定量PCR仪(美国赛默飞世尔科技有限公司); CHEF-DR II脉冲场凝胶电泳电泳仪、Gel DocTM XR凝胶成像系统(美国伯乐生命医学产品有限公司); Miseq测序仪(美国Illumina公司); NP-80 Touch分光光度计(德国Implen GmbH公司)。
1.3 实验方法
1.3.1 分离培养及核酸提取
无菌接种实验室食源性分离的9株MRSA菌株于血平板, 37 ℃培养24 h。挑取菌落利用QIAquick PCR Purification试剂盒按照试剂盒说明书提取DNA, 利用分光光度计测量核酸浓度。核酸质量浓度在20 ng/µL最为合适。
1.3.2 药物敏感试验
利用微量肉汤稀释法对分离的9株MRSA进行药物敏感实验, 测定抗生素的最低抑菌浓度并进行耐药的读取, 抗生素包括青霉素(penicilin, PEN)、红霉素(erythromycin, ERY)、克林霉素(clindamycin, CLI)、苯唑西林(oxaclin, OXC)、头孢西丁(cefoxitin, CFX)、四环素(tetracycline, TET)、庆大霉素(gentamicin, GEN)、左氧氟沙星(levofloxacin, LEV)、呋喃妥因(nitrofurantoin, NIT)、万古霉素(vancomycin, VAN)、替考拉宁(teicoplani, TEC)、利福平(rifampicin, RIF)、复方新诺明(sulfamethoxazole- trimethoprin, SXT)、达托霉素(daptomycin, DAP)、利奈唑胺(linezolid, LZD)、红霉素/克林霉素(erythromycin/ clindamycin, E/C): 质控菌株为标准菌株金黄色葡萄球菌ATCC29213。结果判读参照美国临床实验室标准化委员会(Clinical and Laboratory Standards Institute, CLSI) M100[21]微量肉汤法相关标准进行折点判读。利用药敏软件转换数据显示菌株的敏感、中介和耐药情况。
1.3.3 脉冲场凝胶电泳分子分型
依据国家致病菌识别网方案中分子分型相关操作, 将MRSA制备成菌悬液并包埋于胶块中, 而后进行细胞裂解、洗涤胶块, 切胶块为2 cm的胶条进行酶切, 选择SmaI内切酶对MRSA进行酶切, 酶切条件37 ℃, 5.5 h。Marker选择沙门氏菌H9812, 其内切酶选择XbaI, 37 ℃酶切, 3 h。最后加样制备大胶块进行PFGE。电泳条件: 电压6 V/m, 脉冲时间4.0~40.0 s, 电泳温度14 ℃。电泳时间18 h。电泳结束对胶块染色脱色, 并利用凝胶成像系统获取电泳图片, 保存为TIFF格式。
1.3.4 全基因组测序
经检测浓度合格的核酸, 利用全基因组基因文库构建试剂盒以及基因文库构建磁珠按照说明书进行基因文库的构建; 利用QIAquick PCR Purification试剂盒依照说明书对PCR产物进行纯化。使用Illumina测序平台的MiSeq测序仪进行全基因组测序。
1.4 数据处理
PFGE数据使用BioNumerics 7.6软件处理成像图谱, 采用基于条带比较的DICE系数衡量各带型间的相似度, 相似度为100%则视为同一型别[22]。耐药基因与毒力基因注释将全基因组测序的fastqa格式下机数据, 利用MobaXterm服务器引用本地fastqa格式数据, 输入相关的指令进行拼接组装。将菌株基因组序列, 通过与在线网站Center for Genomic Epidemioology和VFDB数据库(http://www.mgc.ac.cn/VFS)中对基因组耐药基因以及毒力基因与已知序列进行比对检索, 并对检索数据进行统计分析。
2 结果与分析
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2.1 药物敏感试验
2.1.1 9株MRSA抗生素的耐受情况
如表1, 16种抗生素, 除去VAN、TEC、RIF、SXT、DAP、LZD, 其余抗生素都存在耐药菌株。耐药率最高的为PEN, 和E/C, 耐药率达到100%完全耐药, 其次是ERY耐药率88.89%、第3位是CLI、OXC和CFX, 对这3种抗生素的耐药效果一致, 耐药率为77.78%。对TET的耐药率为55.56%。对GEN、LEV、NIT的耐药率也超过了20%, 分别为33.33%、22.22%和22.22%。
2.1.2 多重耐药谱分析
如表2, 所有菌株的耐药种类都高达5种及以上, 且耐药谱多样化。9株MRSA具有8种不同的耐药谱。有2株MRSA的耐药谱一致, 其耐药谱为OXC-ERY-CLI-PEN- E/C-CFX, 同时耐6种抗生素。其中耐药最多的1株MRSA同时耐9种抗生素。
2.2 PFGE聚类分析
对9株MRSA菌株用SmaI酶切电泳。不同菌株条带数从15~18条不等, 利用BioNumerics 7.6分析软件进行聚类, 如图1。将相似度在85%以上且菌株数量大于2株及以上的作为一个聚类簇, 则9株MRSA可以分为3簇(A~C)和8个PFGE型别。9株菌株相似系数均80%~100%之间。其中B簇2株分别来自2018和2019年的餐饮食品类样本具有100%同源性。A簇为2株来自于2015年的肉与肉制品和2017年的餐饮食品。C簇是5株, 来源为2015年的肉与肉制品, 2016、2017和2020年的地方特色食品。
2.3 全基因组测序聚类分析(MLST分型)
MLST分型是基于7个管家基因(arcC, aroE, glpF, gmk, pta, tpi, yqiL)的等位基因号确定菌株的ST型别。通过PubMLST数据库录入测序拼接后的数据, 进行在线比对分析得到每株独有的ST型。9株MRSA菌株分4种不同的ST型别, 其中占比最大的是ST59型菌株, 共有6株占67%以上。其次为ST3355型、ST7型、ST965型各一株, 见表3。
2.4 耐药基因分析
9株食源性MRSA基因中含有大量抗生素耐药基因(antibiotic resistance genes, ARGs), 9个基因组共携带19种耐药基因, 其中NX15070基因组含ARGs最多为7种, 最少的也为3种。菌株携带耐药基因与耐药表型基本一致但也存在不同程度差异, 8株菌株基因组均包含相同的ARGs为2种β-内酰胺类耐药基因(mecA、blaZ), 这与耐药表型基本一致。5株携带四环素类耐药基因(tetK), 氨基糖苷类耐药基因[ant(6)-Ia], 和大环内酯类和林克霉素类霉素类耐药基因(ermB), 但本研究中菌株对大环内脂类抗生素耐药率高, 而其余几类抗生素的耐药率并不高。还有几个耐药基因只出现在各别MRSA基因组中, 例如氨基糖苷类[aph(3, )-III]出现在NX20050, NX15070, NX16081, NX17019。氨基糖苷类[aph(2,, )-III]仅出现在NX15070中。酰胺类[cat(pc221)]仅在NX15070中出现。林可酰胺类(lnuA)和氨基糖胺类(adaD)仅仅出现在NX15072中。而NX18024的大环内酯类和林克霉素类霉素类基因与其他都不相同是[sal(A)], 见表4。
2.5 毒力基因分析
利用MobaXterm v23.0软件通过VFDB数据库的注释功能, 获得每个基因组毒力因携带情况。对MRSA菌株进行毒力基因分析统计, 再整理数据形式, 利用TBtoolv 2.110绘制热图(图2)。本研究共9株MRSA, 其中NX18024毒力基因注释无毒力基因的携带。其余菌株均携带毒力基因, 携带的毒力基因最多的有65种, 这些毒力基因主要是黏附毒素编码基因(fnb、sdr、can、scn、clfA), 外毒素因子编码基因(set、luk), 胞外酶(ssp、coa、geh、hysA), 免疫调节因子编码基因(cap、sbi、adsA、hlg)信息传导(luk、hl、sel、esx、esa)以及与生物膜相关的编码基因(ica)。红色区域表示对该基因的高水平表达。根据基因表达情况菌株被分为两大类。第一大类对黏附素编码基因的表达较低, 其中NX19035和NX16081携带的毒力基因完全一致, 具有相同的毒力基因谱又被分为一组, 而NX15012未携带黏附素编码基因(clfA), 以及NX17019对黏附素编码基因(fnbA), NX17293和NX20050外毒素编码基因(luk) 都有较高表达水平又被划分为不同的组。第二类是对黏附素编码基因表达水平高而在免疫调节和信号传导方面基因表达水平低一些。
3 讨论与结论
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本研究9株食源性MRSA药敏结果表型显示对PEN的耐药率最高, 其次是青霉素类, 大环内酯类, 喹诺酮类, 这与周银娣等[23]报道的MRSA对耐药性基本一致, 但又略有差异。这可能与不同地区长期使用抗生素药物习惯不同导致, 同时也可能与不同来源标本中菌株耐药存在差异有关。VAN常作为治疗MRSA的最后防线[24‒25], 但由于药物的过量使用, 有些地区出现了耐VAN金黄色葡萄球菌。而本研究发现食源性MRSA菌株对VAN很敏感、同时对DAP、替可拉宁、利福平、复方新诺明, 利奈唑胺等抗生素的也非常敏感, 敏感率甚是至为100.0%, 未见耐药。这也与大多数研究者的结果一致[26‒27]。由此可见, 这几种药物仍可作为最后的防线用来治疗MRSA的感染。因此继续保持对抗生素耐药情况的监测以及重点对这几种药物进行长期监测可以为临床治疗用药提供坚实的理论依据。
随着抗生素在各种场所广泛使用, 菌株对抗生素出现了多重耐药的现象, 本研究9株MRSA菌株均呈现多重耐药, 耐药谱数量由5种到9种之多。沈聪等[3]研究发现鸡场周边土壤中喹诺酮类抗生素含量增加。韩国一养猪场土壤中也检测到大量抗生素残留[28], 抗生素的大量使用不可避免造成菌株的耐药情况的上升。本研究结合测序技术通过对耐药基因携带情况进行分析发现, 大部分菌株均携带耐药基因, 携带耐药基因的数量多, 达19种, 且菌株携带基因种类不一致。其中一株就携带7中耐药基因涉及4大类抗生素。携带耐药基因数量较多的为β-内酰胺类和氨基糖苷类为2~3类, 其余大环内酯类和林可霉素类、四环素类林可酰胺和酰胺类均只有一个耐药基因。菌株耐药基因的携带与菌株的耐药表型基本保持一致。9株食源性MRSA中仅有一株不携带任何耐药基因, 其原因可能是所引用的数据库没有相关信息, 亦或者是这株菌的耐药基因发生缺失, 随着基因组学技术的发展这个问题会进一步得到解答。
金黄色葡萄球菌的ST型别非常丰富, 多达上千种, 并且在不停的增加中[5,18,28]。欧洲地区最主要的CA-MRSA克隆是ST80, 其次是ST5、ST8、ST30和ST59。亚洲最流行的CA-MRSA克隆是ST59[5]。本研究发现9株食源性MRSA菌株有4个型别, 其中67%以上型别为ST59, 其次是ST965型、ST3355型和ST7型。这提示本地的食源性MRSA种群结构多样化, 食源性MRSA的主要克隆可能是ST59。不同的种类样本均有ST59型MRSA检出, 这与李兵兵等[4]报道的临床分离金黄色葡萄球菌以主要克隆株ST59、ST398和ST1为主, 以及CUI等[29]报道的青海地区猪源MRSA以ST398和ST59相似。ST59是社区获得性传染中的主要型别, 但是食源性MRSA是否通过食物链传导, 加剧社区获得性金黄色葡萄球菌ST59型的感染仍需进一步实验支持和研究[20,30]。
脉冲场凝胶电泳技术以其分辨力高, 目前广泛应用。它主要被用于疾病的暴发和溯源中[31]。主要是依据PFGE图谱条相似系数带判定菌株的亲缘关系。本研究结果显示9株MRSA中均可以被SmaI限制性内切酶酶切, 9株MRSA菌株依据条带相似性分为3簇, 8种型别, 其带型呈现多样性, 无明显优势带型。有两株菌株条带一致, 但通过聚类分析它被分不同的两簇中, 而条带不同的两株菌却被聚为一类。这与吴健灏等[19]的研究结果不同类型的食品有100%同源性, 不同年份的食品也有100%同源性结果相似。与宋明辉[15]的研究结果一致来自同一克隆系却被分在相距较远的两簇。来自不同来源的菌株显示有100%的同源性, 揭示各食品之间有交叉污染。并且依据条带的同源性发现, 食品中还存在持续污染的情况。此外还发现, 同源性高的菌株, 携带的耐药基因也相似度高。导致这种情况产生的原因有: (1)可能与餐饮工作人员生熟案板不分开; (2)餐饮单位工作卫生不干净; (3)生产食品的工作人员也是食品污染的源头之一。
细菌在生长繁殖过程中产生许多种致病因子, 这些致病因子导致细菌的感染发生甚至严重。90%的金黄色葡萄球菌引起的食物中毒事件与其产生毒素有关[17,31]。一些毒力因子被推测可能促进金黄色葡萄球菌的人体定殖, 比如肠毒素基因sec和egc locus[15]。还有一些黏附因子, 如clfB, fnbA和sas也被报道参与定殖过程[32]。MRSA也不例外, 也同时携带多种致病因子。一株食源性菌株携带20多种黏附相关基因[5], 了解这些致病因子的分布特点, 有助于对疾病的预防和控制。本研究中9株MRSA菌株携带的毒力基因有fnb、can、scn、set、luk、coa、geh、cap、sbi、adsA、hlg、luk、hla、sel、esx、esa、ica等65种毒力基因。它们作用分别为编码菌株黏附素、外毒素、胞外酶、免疫调节因子和生物膜形成有关基因, 还有些基因参与信号传导。其中黏附因子在细菌感染中起重要作用, 促使细菌定植, 并逃避宿主免疫系统的攻击。细菌黏附后, 通过特异性和非特异性结合, 使细菌聚集在一起, 形成生物膜, 生物膜的存在大大提高了细菌对抗菌药物的耐药性[19,29], 增加了细菌产生多重耐药的可能性, 给临床治疗带来莫大的困难。不同的细菌生物膜形成的能力各不相同, 因此对细菌介导生物膜形成的因子, 以及致病因子进行检测, 能够给预防和治疗疾病提供必要措施。针对各类因子的靶点进行药物研究, 干扰或阻断致病因素的形成, 为临床治疗提供理论依据。
综上所述, 本研究通过药物敏感试验、PFGE分子分型以及全基因组测序技术, 分析食源性MRSA耐药基因以及毒力基因特征, 补充了食源性MRSA研究数据的信息, 为预防和控制MRSA的感染提供了理论依据, 同时为临床治疗MRSA用药给予指导。
基金
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  • 宁夏自然科学基金项目(2022AAC03711)
文献
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参考文献 引证文献
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2025年第16卷第5期
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doi: 10.19812/j.cnki.jfsq11-5956/ts.20241008007
  • 接收时间：2024-10-08
  • 首发时间：2025-07-19
  • 出版时间：2025-03-15
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  • 收稿日期：2024-10-08
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宁夏自然科学基金项目(2022AAC03711)
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    宁夏回族自治区疾病预防控制中心, 宁夏预防医学科学院 银川 750004

通讯作者:

* 魏琼(1986—), 女, 副主任技师, 主要研究方向为传染病微生物及食源性微生物检验。E-mail:
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2种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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