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Article(id=1240972415283556612, tenantId=1146029695717560320, journalId=1227665162245664772, issueId=1240972413354176744, articleNumber=null, orderNo=null, doi=10.20043/j.cnki.MPM.202312350, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=null, receivedDate=1702828800000, receivedDateStr=2023-12-18, revisedDate=null, revisedDateStr=null, acceptedDate=null, acceptedDateStr=null, onlineDate=1773800479955, onlineDateStr=2026-03-18, pubDate=1715270400000, pubDateStr=2024-05-10, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1773800479955, onlineIssueDateStr=2026-03-18, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1773800479955, creator=13701087609, updateTime=1773800479955, updator=13701087609, issue=Issue{id=1240972413354176744, tenantId=1146029695717560320, journalId=1227665162245664772, year='2024', volume='51', issue='9', pageStart='1537', pageEnd='1728', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1773800479495, creator=13701087609, updateTime=1773800596829, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1240972905568334240, tenantId=1146029695717560320, journalId=1227665162245664772, issueId=1240972413354176744, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1240972905568334241, tenantId=1146029695717560320, journalId=1227665162245664772, issueId=1240972413354176744, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=1689, endPage=1694, ext={EN=ArticleExt(id=1240972415593935126, articleId=1240972415283556612, tenantId=1146029695717560320, journalId=1227665162245664772, language=EN, title=Drug resistance and genome sequencing analysis of staphylococcus aureus isolated from clinical isolates in Huai’an city, columnId=1228016572065837304, journalTitle=Modern Preventive Medicine, columnName=Experimental Technology and Applications, runingTitle=null, highlight=null, articleAbstract=
Objective

To investigate the drug resistance and molecular epidemiological characteristics of clinically isolated Staphylococcus aureus in Huai’an city, so as to provide references for the diagnosis, treatment, prevention and control of infection.

Methods

Staphylococcus aureus isolated from clinical samples were collected and methicillin-resistant Staphylococcus aureus（MRSA）was detected by cefoxitin or oxacillin resistance phenotype or mecA gene. The drug sensitivity test was carried out by microbroth dilution method. Based on the whole genome sequencing, the strains were analyzed by single nucleotide polymorphism and multi-locus sequence typing. The virulence and drug resistance genes of the strains were identified by online database.

Results

A total of 83 strains of Staphylococcus aureus were isolated from 7 types of clinical specimens, and MRSA accounted for 59.04%. The isolated strains had the highest resistance to penicillin (97.59%) and were sensitive to Nez Olamide, tigecyclines, vancomycin, teicoplanin, and nitrofurantoin, and multiple drug-resistant strains accounted for 57.83%. There were 20 ST types in 83 strains of Staphylococcus aureus, and ST398 (21.69%) was the main type. There were 187 292 SNP loci in 83 genomes. These strains carried 38 kinds of drug resistance genes, among which tet (38), blaZ, arlR, arlS, mgrA, norA, mepA, ErmC,LmrS, and mepR had higher carrying rates. These strains carried 8 enterotoxin genes including sea, seb, sec, sed, seh, selk, sell,and selq, among which selk and selq (both 32.53%) had the highest carrying rate, and ST1 strain carried the largest number of kinds of enterotoxin genes. The carrying rates of lukF-PV and lukS-PV genes encoded by PVL were 49.40% and 6.02%, respectively. The carrying rate of tsst-1 gene encoded by toxic shock syndrome toxin TSST-1 was 3.61%.

Conclusion

The drug resistance of Staphylococcus aureus isolated from Huai’an area is strong and the detection rate of MRSA is high. The ST types of strains are rich, and there is a certain correlation between ST types and pathogenicity.

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目的

探究淮安市临床分离金黄色葡萄球菌的耐药性及分子流行病学特征，为其感染的诊治和防控提供参考。

方法

收集从临床标本中分离的金黄色葡萄球菌，通过头孢西丁或苯唑西林耐药表型或 mecA基因检测耐甲氧西林金黄色葡萄球菌（methicillin-resistant Staphylococcus aureus，MRSA）。采用微量肉汤稀释法进行药敏试验。基于全基因组测序，对菌株进行单核苷酸多态性分析和多位点序列分型。利用在线数据库鉴定菌株携带的毒力和耐药基因。

结果

从7种类型临床标本中共分离到83株金黄色葡萄球菌，MRSA占59.04%。分离菌株对青霉素耐药率最高，为97.59%，对奈唑胺、替加环素、万古霉素、替考拉宁和呋喃妥因均敏感，多重耐药菌株占57.83%。83株金黄色葡萄球菌有20个ST型，ST398（21.69%）为主要型别。83个基因组存在187 292个SNPs位点。这些菌株携带有38种耐药基因，其中tet(38)、 blaZ、arlR、arlS、mgrA、norA、mepA、ErmC、LmrS、mepR携带率较高。携带sea、seb、sec、sed、seh、selk、sell、selq 8种肠毒素基因，selk和selq携带率最高，均为32.53%，ST1菌株携带肠毒素基因种类最多。杀白细胞素PVL编码基因lukF-PV和lukS-PV携带率分别为49.40%和6.02%。中毒性休克综合征毒素TSST-1编码基因tsst-1的携带率为3.61%。

结论

淮安地区临床分离金黄色葡萄球菌的耐药性较强，MRSA检出率较高。菌株ST型别丰富，ST型别与致病性存在一定相关性。

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邢亚东，E-mail:
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李兵兵和汪浩为共同第一作者

李兵兵（1986—），男，硕士，副研究员，研究方向：病原微生物溯源研究

汪浩（1987—），男，本科，副主任技师，研究方向：病原微检验

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李兵兵（1986—），男，硕士，副研究员，研究方向：病原微生物溯源研究

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汪浩（1987—），男，本科，副主任技师，研究方向：病原微检验

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Journal der Deutschen Dermatologischen Gesellschaft, 2020, 18(4): 315-322., articleTitle=Recurrent mucocutaneous infections caused by PVL-positive Staphylococcus aureus strains: a challenge in clinical practice, refAbstract=null)], funds=[Fund(id=1240986273368822107, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1240972415283556612, awardId=Y2018047, language=CN, fundingSource=江苏省预防医学科研课题(Y2018047), fundOrder=null, country=null), Fund(id=1240986273498845539, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1240972415283556612, awardId=HAP201906, language=CN, fundingSource=淮安市创新能力建设计划(HAP201906), fundOrder=null, country=null)], companyList=[AuthorCompany(id=1240986263235384276, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1240972415283556612, xref=1., ext=[AuthorCompanyExt(id=1240986263243772886, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1240972415283556612, companyId=1240986263235384276, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=Huai’an Center for Disease Control and Prevention, Huai’an, Anhui 223001, China), AuthorCompanyExt(id=1240986263247967191, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1240972415283556612, companyId=1240986263235384276, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=1.淮安市疾病预防控制中心，江苏 淮安 223001)]), AuthorCompany(id=1240986263533179871, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1240972415283556612, xref=2., ext=[AuthorCompanyExt(id=1240986263541568482, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1240972415283556612, companyId=1240986263533179871, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=2.涟水县疾病预防控制中心，江苏 淮安 223400)]), AuthorCompany(id=1240986264242017261, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1240972415283556612, xref=3., ext=[AuthorCompanyExt(id=1240986264258794480, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1240972415283556612, companyId=1240986264242017261, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=3.淮安市突发公共卫生事件应急检测重点实验室，江苏 淮安 223001)])], figs=[ArticleFig(id=1240986270176956680, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1240972415283556612, language=EN, label=Figure 1, caption=Drug-resistant phenotype of Staphylococcus aureus, figureFileSmall=e8SwmawxyOea66Rng5UlFw==, figureFileBig=CsWrB/0vJel4cLzqtcJ3gQ==, tableContent=null), ArticleFig(id=1240986270332145934, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1240972415283556612, language=CN, label=图1, caption=金黄色葡萄球菌耐药表型, figureFileSmall=e8SwmawxyOea66Rng5UlFw==, figureFileBig=CsWrB/0vJel4cLzqtcJ3gQ==, tableContent=null), ArticleFig(id=1240986270575415572, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1240972415283556612, language=EN, label=Figure 2, caption=The wg-SNP evolution tree of Staphylococcus aureus, figureFileSmall=HiQbndodaaJNfwQc+qk71A==, figureFileBig=XU5kNtCmYohzRuWyg5GJWw==, tableContent=null), ArticleFig(id=1240986270676078875, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1240972415283556612, language=CN, label=图2, caption=金黄色葡萄球菌wg-SNP进化树, figureFileSmall=HiQbndodaaJNfwQc+qk71A==, figureFileBig=XU5kNtCmYohzRuWyg5GJWw==, tableContent=null), ArticleFig(id=1240986270940320033, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1240972415283556612, language=EN, label=Figure 3, caption=Minimum spanning tree for MLST typing of Staphylococcus aureus, figureFileSmall=iYXjJK00dZnosoTsHHe9vg==, figureFileBig=gUHwgqfglyP3g8ra5BxgiA==, tableContent=null), ArticleFig(id=1240986271183589675, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1240972415283556612, language=CN, label=图3, caption=金黄色葡萄球菌MLST分型最小生成树, figureFileSmall=iYXjJK00dZnosoTsHHe9vg==, figureFileBig=gUHwgqfglyP3g8ra5BxgiA==, tableContent=null), ArticleFig(id=1240986271296835891, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1240972415283556612, language=EN, label=Table 1, caption=

Information table of strains

, figureFileSmall=null, figureFileBig=null, tableContent=
标本类型菌株数量（株）占比（%）
MRSA MSSA 合计
无菌部位标本血液4489.64
透析液2356.02
胸腹水2022.41
开放部位标本痰液1081821.69
分泌物30144453.01
脓液1456.02
尿液0111.20
合计493483100.00
), ArticleFig(id=1240986271405887802, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1240972415283556612, language=CN, label=表1, caption=

菌株信息表

, figureFileSmall=null, figureFileBig=null, tableContent=
标本类型菌株数量（株）占比（%）
MRSA MSSA 合计
无菌部位标本血液4489.64
透析液2356.02
胸腹水2022.41
开放部位标本痰液1081821.69
分泌物30144453.01
脓液1456.02
尿液0111.20
合计493483100.00
), ArticleFig(id=1240986271561077053, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1240972415283556612, language=EN, label=Table 2, caption=

Carriage of durg-resistance genes

, figureFileSmall=null, figureFileBig=null, tableContent=
耐受抗生素耐药基因携带情况[n (%)]χ2/Fisher确切概率法P值
MRSA (n=49)MSSA (n=34)
四环素类抗生素tet(38)48 (97.96)33 (97.06)c1.000
tet(K)6 (12.24)6 (17.65)0.138b0.711
tetM1 (2.04)1 (2.94)c1.000
TEM-1161 (2.04)1 (2.94)c1.000
tet(L)0 (0)1 (2.94)c0.410
β-内酰胺类抗生素blaZ40 (81.63)33 (97.06)3.169b0.075
OXA-4441 (2.04)0 (0)c1.000
OXA-221 (2.04)0 (0)c1.000
喹诺酮类抗生素arlR48 (97.96)33 (97.06)c1.000
arlS48 (97.96)33 (97.06)c1.000
mgrA49 (100.00)34 (100.00)——
norA49 (100.00)33 (97.06)c0.410
mepA48 (97.96)33 (97.06)c1.000
qacA0 (0)1 (2.94)c0.410
大环内酯类抗生素ErmC44 (89.80)28 (82.35)0.428b0.513
ErmB8 (16.33)2 (5.88)1.198b0.274
ErmA0 (0)2 (5.88)c0.165
LmrS48 (97.96)34 (100.00)c1.000
mel0 (0)1 (2.94)c0.410
甘氨酰环素类抗生素mepR49 (100.00)34 (100.00)——
林可酰胺类抗生素lnuG8 (16.33)2 (5.88)1.198b0.274
cfrA1 (2.04)1 (2.94)c1.000
lnuA1 (2.04)3 (8.82)0.806b0.369
lsaE1 (2.04)1 (2.94)c1.000
磷霉素FosD9 (18.37)1 (2.94)3.169b0.075
FosB7 (14.29)15 (44.12)9.170a0.002
FosB11 (2.04)3 (8.82)0.806b0.369
核苷类抗生素sta1 (2.04)1 (2.94)c1.000
夫西地酸fusB4 (8.16)0 (0)1.408b0.235
氨基糖苷类抗生素ANT(4')-Ib1 (2.04)2 (5.88)0.105b0.746
ANT(6)-Ia0 (0)1 (2.94)c0.410
APH(3')-IIIa5 (10.20)1 (2.94)0.682b0.409
AAC(6')-Ie-APH(2'')-Ia3 (6.12)2 (5.88)0.000b1.000
aad(6)5 (10.20)1 (2.94)0.682b0.409
苯尼考抗生素catQ0 (0)1 (2.94)c0.410
fexA1 (2.04)1 (2.94)c1.000
二氨基嘧啶类抗生素dfrG1 (2.04)1 (2.94)c1.000
氯霉素catA80 (0)2 (5.88)c0.165
), ArticleFig(id=1240986271875649861, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1240972415283556612, language=CN, label=表2, caption=

耐药基因携带情况

, figureFileSmall=null, figureFileBig=null, tableContent=
耐受抗生素耐药基因携带情况[n (%)]χ2/Fisher确切概率法P值
MRSA (n=49)MSSA (n=34)
四环素类抗生素tet(38)48 (97.96)33 (97.06)c1.000
tet(K)6 (12.24)6 (17.65)0.138b0.711
tetM1 (2.04)1 (2.94)c1.000
TEM-1161 (2.04)1 (2.94)c1.000
tet(L)0 (0)1 (2.94)c0.410
β-内酰胺类抗生素blaZ40 (81.63)33 (97.06)3.169b0.075
OXA-4441 (2.04)0 (0)c1.000
OXA-221 (2.04)0 (0)c1.000
喹诺酮类抗生素arlR48 (97.96)33 (97.06)c1.000
arlS48 (97.96)33 (97.06)c1.000
mgrA49 (100.00)34 (100.00)——
norA49 (100.00)33 (97.06)c0.410
mepA48 (97.96)33 (97.06)c1.000
qacA0 (0)1 (2.94)c0.410
大环内酯类抗生素ErmC44 (89.80)28 (82.35)0.428b0.513
ErmB8 (16.33)2 (5.88)1.198b0.274
ErmA0 (0)2 (5.88)c0.165
LmrS48 (97.96)34 (100.00)c1.000
mel0 (0)1 (2.94)c0.410
甘氨酰环素类抗生素mepR49 (100.00)34 (100.00)——
林可酰胺类抗生素lnuG8 (16.33)2 (5.88)1.198b0.274
cfrA1 (2.04)1 (2.94)c1.000
lnuA1 (2.04)3 (8.82)0.806b0.369
lsaE1 (2.04)1 (2.94)c1.000
磷霉素FosD9 (18.37)1 (2.94)3.169b0.075
FosB7 (14.29)15 (44.12)9.170a0.002
FosB11 (2.04)3 (8.82)0.806b0.369
核苷类抗生素sta1 (2.04)1 (2.94)c1.000
夫西地酸fusB4 (8.16)0 (0)1.408b0.235
氨基糖苷类抗生素ANT(4')-Ib1 (2.04)2 (5.88)0.105b0.746
ANT(6)-Ia0 (0)1 (2.94)c0.410
APH(3')-IIIa5 (10.20)1 (2.94)0.682b0.409
AAC(6')-Ie-APH(2'')-Ia3 (6.12)2 (5.88)0.000b1.000
aad(6)5 (10.20)1 (2.94)0.682b0.409
苯尼考抗生素catQ0 (0)1 (2.94)c0.410
fexA1 (2.04)1 (2.94)c1.000
二氨基嘧啶类抗生素dfrG1 (2.04)1 (2.94)c1.000
氯霉素catA80 (0)2 (5.88)c0.165
), ArticleFig(id=1240986272571904329, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1240972415283556612, language=EN, label=Table 3, caption=

Carriage of virulence genes

, figureFileSmall=null, figureFileBig=null, tableContent=
毒力因子名称相关毒力基因谱ST型菌株数
MRSA（株）MSSA（株）合计（株）占比（%）
肠毒素seh-sec-sell-sea-selq-selkST1911012.05
sed-selk-selq-sell-secST50111.20
seb-selq-selk-seaST596067.23
sea-sell-secST881011.20
selk-selq-sebST59、ST4513、N281910.84
sec-sellST188、ST23150333.61
selk-selqST3981011.20
sea-sedST71011.20
sedST80111.20
seaST7、ST88、ST30、ST4071、ST64267.23
sehST10111.20
sebST250222.41
杀白细胞素PVL lukF-PVST15、ST7、ST1、ST188、ST1281、ST8、N1、ST88、ST1、ST25、ST630、ST4071、ST5、ST616203643.37
lukF-PV-lukS-PVST398、ST221456.02
中毒性休克综合征毒素 TSST-1tsst-1ST1281、ST30、ST1880333.61
), ArticleFig(id=1240986273062637903, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1240972415283556612, language=CN, label=表3, caption=

毒力基因携带情况

, figureFileSmall=null, figureFileBig=null, tableContent=
毒力因子名称相关毒力基因谱ST型菌株数
MRSA（株）MSSA（株）合计（株）占比（%）
肠毒素seh-sec-sell-sea-selq-selkST1911012.05
sed-selk-selq-sell-secST50111.20
seb-selq-selk-seaST596067.23
sea-sell-secST881011.20
selk-selq-sebST59、ST4513、N281910.84
sec-sellST188、ST23150333.61
selk-selqST3981011.20
sea-sedST71011.20
sedST80111.20
seaST7、ST88、ST30、ST4071、ST64267.23
sehST10111.20
sebST250222.41
杀白细胞素PVL lukF-PVST15、ST7、ST1、ST188、ST1281、ST8、N1、ST88、ST1、ST25、ST630、ST4071、ST5、ST616203643.37
lukF-PV-lukS-PVST398、ST221456.02
中毒性休克综合征毒素 TSST-1tsst-1ST1281、ST30、ST1880333.61
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淮安市临床分离金黄色葡萄球菌耐药性及全基因组测序分析
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李兵兵 1, 3 , 汪浩 2, 3 , 杨鹏飞 1, 3 , 宋志洲 2 , 孙敏 1, 3 , 邢亚东 1, 3
现代预防医学 | 实验技术及其应用 2024,51(9): 1689-1694
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现代预防医学 | 实验技术及其应用 2024, 51(9): 1689-1694
淮安市临床分离金黄色葡萄球菌耐药性及全基因组测序分析
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李兵兵1, 3, 汪浩2, 3, 杨鹏飞1, 3, 宋志洲2, 孙敏1, 3, 邢亚东1, 3
作者信息
  • 1.淮安市疾病预防控制中心，江苏 淮安 223001
  • 2.涟水县疾病预防控制中心，江苏 淮安 223400
  • 3.淮安市突发公共卫生事件应急检测重点实验室，江苏 淮安 223001

    • 李兵兵（1986—），男，硕士，副研究员，研究方向：病原微生物溯源研究

    汪浩（1987—），男，本科，副主任技师，研究方向：病原微检验

通讯作者:

邢亚东，E-mail:
Drug resistance and genome sequencing analysis of staphylococcus aureus isolated from clinical isolates in Huai’an city
Bing-bing LI1, 3, Hao WANG2, 3, Peng-fei YANG1, 3, Zhi-zhou SONG2, Min SUN1, 3, Ya-dong XING1, 3
Affiliations
  • Huai’an Center for Disease Control and Prevention, Huai’an, Anhui 223001, China
出版时间: 2024-05-10 doi: 10.20043/j.cnki.MPM.202312350
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摘要
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目的

探究淮安市临床分离金黄色葡萄球菌的耐药性及分子流行病学特征，为其感染的诊治和防控提供参考。

方法

收集从临床标本中分离的金黄色葡萄球菌，通过头孢西丁或苯唑西林耐药表型或 mecA基因检测耐甲氧西林金黄色葡萄球菌（methicillin-resistant Staphylococcus aureus，MRSA）。采用微量肉汤稀释法进行药敏试验。基于全基因组测序，对菌株进行单核苷酸多态性分析和多位点序列分型。利用在线数据库鉴定菌株携带的毒力和耐药基因。

结果

从7种类型临床标本中共分离到83株金黄色葡萄球菌，MRSA占59.04%。分离菌株对青霉素耐药率最高，为97.59%，对奈唑胺、替加环素、万古霉素、替考拉宁和呋喃妥因均敏感，多重耐药菌株占57.83%。83株金黄色葡萄球菌有20个ST型，ST398（21.69%）为主要型别。83个基因组存在187 292个SNPs位点。这些菌株携带有38种耐药基因，其中tet(38)、 blaZ、arlR、arlS、mgrA、norA、mepA、ErmC、LmrS、mepR携带率较高。携带sea、seb、sec、sed、seh、selk、sell、selq 8种肠毒素基因，selk和selq携带率最高，均为32.53%，ST1菌株携带肠毒素基因种类最多。杀白细胞素PVL编码基因lukF-PV和lukS-PV携带率分别为49.40%和6.02%。中毒性休克综合征毒素TSST-1编码基因tsst-1的携带率为3.61%。

结论

淮安地区临床分离金黄色葡萄球菌的耐药性较强，MRSA检出率较高。菌株ST型别丰富，ST型别与致病性存在一定相关性。

金黄色葡萄球菌  /  耐药性  /  分子流行病学
Objective

To investigate the drug resistance and molecular epidemiological characteristics of clinically isolated Staphylococcus aureus in Huai’an city, so as to provide references for the diagnosis, treatment, prevention and control of infection.

Methods

Staphylococcus aureus isolated from clinical samples were collected and methicillin-resistant Staphylococcus aureus（MRSA）was detected by cefoxitin or oxacillin resistance phenotype or mecA gene. The drug sensitivity test was carried out by microbroth dilution method. Based on the whole genome sequencing, the strains were analyzed by single nucleotide polymorphism and multi-locus sequence typing. The virulence and drug resistance genes of the strains were identified by online database.

Results

A total of 83 strains of Staphylococcus aureus were isolated from 7 types of clinical specimens, and MRSA accounted for 59.04%. The isolated strains had the highest resistance to penicillin (97.59%) and were sensitive to Nez Olamide, tigecyclines, vancomycin, teicoplanin, and nitrofurantoin, and multiple drug-resistant strains accounted for 57.83%. There were 20 ST types in 83 strains of Staphylococcus aureus, and ST398 (21.69%) was the main type. There were 187 292 SNP loci in 83 genomes. These strains carried 38 kinds of drug resistance genes, among which tet (38), blaZ, arlR, arlS, mgrA, norA, mepA, ErmC,LmrS, and mepR had higher carrying rates. These strains carried 8 enterotoxin genes including sea, seb, sec, sed, seh, selk, sell,and selq, among which selk and selq (both 32.53%) had the highest carrying rate, and ST1 strain carried the largest number of kinds of enterotoxin genes. The carrying rates of lukF-PV and lukS-PV genes encoded by PVL were 49.40% and 6.02%, respectively. The carrying rate of tsst-1 gene encoded by toxic shock syndrome toxin TSST-1 was 3.61%.

Conclusion

The drug resistance of Staphylococcus aureus isolated from Huai’an area is strong and the detection rate of MRSA is high. The ST types of strains are rich, and there is a certain correlation between ST types and pathogenicity.

Staphylococcus aureus  /  Drug resistance  /  Molecular epidemiology
李兵兵, 汪浩, 杨鹏飞, 宋志洲, 孙敏, 邢亚东. 淮安市临床分离金黄色葡萄球菌耐药性及全基因组测序分析. 现代预防医学, 2024 , 51 (9) : 1689 -1694 . DOI: 10.20043/j.cnki.MPM.202312350
Bing-bing LI, Hao WANG, Peng-fei YANG, Zhi-zhou SONG, Min SUN, Ya-dong XING. Drug resistance and genome sequencing analysis of staphylococcus aureus isolated from clinical isolates in Huai’an city[J]. Modern Preventive Medicine, 2024 , 51 (9) : 1689 -1694 . DOI: 10.20043/j.cnki.MPM.202312350
正文
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金黄色葡萄球菌(Staphylococcus aureus)是一种人畜共患病病原体，严重者会导致人和动物死亡[1-2]。抗生素大量使用造成的选择性压力导致金黄色葡萄球菌的耐药性逐渐增强[3]。耐甲氧西林金黄色葡萄球菌（methicillin-resistant Staphylococcus aureus，MRSA）是一种广泛耐药金黄色葡萄球菌，相较于甲氧西林敏感金黄色葡萄球菌（methicillin-sensitive Staphylococcus aureus，MSSA）耐药性更强、致死率更高，并且在临床上的检出率呈不断上升态势[4-6]。研究结果表明，不同地域、不同样本来源金黄色葡萄球菌的耐药性存在差异[7-8]，耐药性监测是有效控制耐药性发展以及为金黄色葡萄球菌感染疾病的临床用药提供指导的重要手段。
本研究对淮安市临床分离的金黄色葡萄球菌进行了耐药性测试，并通过全基因组测序分析了其遗传进化、耐药基因、毒力因子携带情况，以期能为金黄色葡萄球菌的预防和控制提供理论指导。
1　材料与方法
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1.1　菌株来源与鉴定
收集2020—2021年淮安市国家致病菌识别网监测哨点医院从临床标本中分离的金黄色葡萄球菌83株。金黄色葡萄球菌鉴定使用VITEK 2 Compat全自动生化鉴定仪；微量肉汤稀释法筛选MRSA菌株，根据美国国立临床标准实验室委员会(CLSI)标准（2022），苯唑西林MIC>4 μg/ml的菌株判定为MRSA；荧光PCR法检测83株菌携带mecA基因的情况。
1.2　核酸提取及基因组测序
使用天根生化科技（北京）有限公司细菌基因组DNA提取试剂盒提取菌株核酸，用Nanodrop对提取核酸的质量进行检测，经质控合格后送上海伯杰医疗科技有限公司进行基因组二代测序，测序平台为Illumina NovaSeq，测序深度大于100×。下机数据经过滤（fastp，v0.23.2）、组装拼接（SPAdes，v3.15.5），最终交付数据质量达到Coverage≥95%、Mismatch≤20、Q20≥1Gb、Q30≥85%。
1.3　MLST分子分型
获得菌株基因组序列后，与MLST在线数据库（https://pubmlst.org/saureus/）中已知序列比对，获取7个管家基因（arcC, aroE, glpF, gmK,pta, tpi, yqiL）的等位基因编号，根据等位基因编号得出菌株ST型。使用Bionumerics软件进行聚类分析，设定克隆复合群最小相同等位基因数为6，并绘制最小生成树。
1.4　遗传进化分析
以NC007795.1基因组为参考，利用在线软件CSI Phylogeny[9]（https://cge.cbs.dtu.dk/services/CSIPhylogeny/）进行SNP分析并构建系统进化树，使用iTOL（https://itol.embl.de/）[10]对进化树进行美化。
1.5　耐药基因及毒力基因注释
分别将菌株基因组序列与CARD数据库（http://arpcard.mcmaster.ca）和VFDB数据库（http://www.mgc.ac.cn/VFs/）中已知序列进行比对，分析菌株携带的耐药基因和毒力基因。
1.6　药敏试验
采用微量肉汤稀释法检测菌株对复方新诺明、头孢西丁、阿奇霉素、克拉霉素、青霉素、苯唑西林、红霉素、克林霉素、利奈唑胺、替加环素、四环素、万古霉素、利福平、氯霉素、庆大霉素、莫西沙星、左氧氟沙星、替考拉宁、呋喃妥因、诺氟沙星20种抗生素的敏感性，根据CLSI标准（2022）进行折点判读。ATCC25923为质控菌株。
1.7　统计方法
应用SPSS（19.0）软件对数据进行统计分析（理论频数T≥5时用χ2检验；理论频数1≤T<5时用χ2检验校正；理论频数T<1时，用Fisher确切概率法进行统计），以α=0.05为检验水准。
2　结果
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2.1　菌株来源分布
83株金黄色葡萄球菌分离自7种类型临床标本，开放部位标本和无菌部位标本分别分离52和31株。分离自分泌物（53.01%）、痰液（21.69%）和血液（9.64%）三种标本的菌株合计占比84.34%，具体菌株来源信息见表1。83株金黄色葡萄球菌中检出49株MRSA，检出率为59.04%。49株MRSA中8株分离自无菌部位，41株分离自开放部位。MRSA中具有苯唑西林和头孢西丁耐药表型的有28株，其中有3株不携带mecA基因；携带mecA基因的有46株，其中21株对苯唑西林和头孢西丁敏感，见图1和图2B。
2.2　耐药表型
20种抗生素中，除利奈唑胺、替加环素、万古霉素、替考拉宁和呋喃妥因外，其余抗生素均有耐药菌株存在，耐药率最高的为青霉素，为97.59%；耐药率超过50%的有阿奇霉素、克拉霉素、红霉素，分别为61.45%、61.45%、62.65%；对头孢西丁、苯唑西林、克林霉素、左氧氟沙星和诺氟沙星的耐药率超过20%，分别为33.73%、33.73%、21.69%、22.89%、36.14%，其余抗生素耐药率较低，见图1。对三种及以上抗生素耐药的多重耐药菌株占57.83%，三耐菌株、四耐菌株、五耐菌株、六耐菌株分别有22株、15株、9株、2株。MSSA对复方新诺明、氯霉素和庆大霉素的耐药率高于MRSA，对其余抗生素的耐药率低于MRSA，但是除了头孢西丁和苯唑西林（均χ2=29.319，P<0.001）外，MRSA和MSSA对其余抗生素耐药率的差异不显著（均P>0.05）。
2.3　MLST分子分型
83株金黄色葡萄球菌分属18个已知ST型和2个新的ST型，ST型占比由高到低依次为ST398、ST1、 ST59、ST630、ST22、ST188、ST4513、ST7、ST15、ST25、ST88、ST1281，分别为21.69%、13.25%、 12.05%、9.64%、8.43%、4.82%、4.82%、3.61%、3.61%、3.61%、2.41%、2.41%，其余ST型均只有1株菌。
MRSA存在9个已知ST型和2个新的ST型，以ST398、ST1和ST59为主；MSSA存在14个已知ST型，以ST22、ST398和ST188为主。ST4513、ST6、ST7、ST88仅存在于MRSA，ST188、ST15、ST25、ST1281、ST2315、ST30、ST4071、ST5、ST8仅存在于MSSA。最小生成树上，以ST1、ST22、ST59、ST398、ST630为节点聚类成5个克隆复合群，见图3。
2.4　wg-SNP遗传进化分析
83株金黄色葡萄球菌全基因组测序数据组装到参考基因组上，共获得187 292个SNPs位点（过滤阀值MAF>0.05）。MSSA进化树有4个分支，见图2A，相同ST型菌株在进化树上的距离较近；部分相同类型标本来源菌株聚在一起。MRSA进化树有3大分枝，见图2B，相同ST型菌株在进化树上的距离较近，其中ST398菌株单独聚为一个分支，ST59和ST4513菌株在同一分支上，其余ST型菌株聚为一个分支。
2.5　耐药基因分析
如表2所示，83个基因组共携带38种耐药基因，这些菌株最多携带17种耐药基因，最少携带4种耐药基因，这些耐药基因主要介导对四环素类、β-内酰胺类、喹诺酮类、大环内酯类、林可酰胺类、磷霉素类等13类抗生素的耐药。携带率超过50%的耐药基因有tet(38)、 blaZ、arlR、arlS、mgrA、norA、mepA、ErmC、LmrS、mepR。菌株携带耐药基因情况与其耐药表型之间存在一定差异，甘氨酰环素类耐药基因、四环素类耐药基因、喹诺酮类耐药基因、β-内酰胺类耐药基因携带率较高，但本研究中的菌株对上述3类抗生素耐药率并不高。除磷霉素耐药基因FosB（χ2=9.170，P=0.002）外，MRSA和MSSA携带耐药基因差异不显著（均P>0.05）。
2.6　毒力基因注释
83株金黄色葡萄球菌基因组携带sea、seb、sec、sed、seh、selk、sell、selq 8种肠毒素基因。携带率由高到低依次为selk、 selq、 sea、 seb 、sec、sell、seh、sed，分别为32.53%、32.53%、28.92%、20.48%、18.07%、18.07%、13.25%、3.61%。携带肠毒素的42株菌株有（30株MRSA，12株MSSA）12种肠毒素谱，以seh-sec-sell-sea-selq-selk、 selk-selq-seb、
seb-selq-selk-sea和sea为主。肠毒素基因谱与菌株ST型有一定相关性，例如携带seh-sec-sell-sea-selq-selk肠毒素谱的菌株均为ST1型，携带seb-selq-selk-sea的菌株均为ST59型，毒力基因携带情况见表3。
杀白细胞素PVL编码基因lukF-PV和 lukS-PV携带率分别为49.40%和6.02%。36株菌株只携带lukF-PV 基因，无单独携带lukS-PV基因的菌株，同时携带lukF-PV和 lukS-PV的菌株有5株，ST型别为ST398和ST22，其中4株为MSSA，1株为MRSA。中毒性休克综合征毒素TSST-1的编码基因tsst-1的携带率较低，仅为3.61%，ST型别分别为ST1281、ST30、ST188，均为MSSA。
3　讨论
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耐药性金黄色葡萄球菌已被世界卫生组织列为需重点关注的细菌之一，对金黄色葡萄球菌的临床分布及耐药情况进行调查分析，可减少其所致感染的发生和暴发流行，并对提高抗感染治疗具有重要的临床意义。本研究中收集的金黄色葡萄球菌的主要标本来源与谭艳[11]报道的结果相同，这可能与金黄色葡萄球菌的分布特征以及医院送检标本类型有关。83株金黄色葡萄球菌中MRSA检出率为59.04%，与洪捷[12]报道的江苏省临床样本中MRSA的检出率基本一致，MRSA菌株主要分离自分泌物，与李洁群[13]报道结果相同。部分MRSA对苯唑西林和头孢西丁耐药表型与其携带mecA基因情况不一致，这提示mecA基因介导的MRSA耐药机制还受其他一些因素的影响，值得我们进一步去研究。
本研究中的金黄色葡萄球菌的耐药表型与陈培超[14]报道的医院环境中分离的金黄色葡萄球菌的耐药表型相似，均对青霉素的耐药率最高，对利奈唑胺、万古霉素、替考拉宁和呋喃妥因敏感；与孙盼盼[3]、李雅倩[15]报道的临床标本分离金黄色葡萄球菌的耐药表型均有较大差异，这可能与长期以来不同地区临床用药差异或不同研究中选择菌株的主要来源标本以及人群存在差异有关。本研究中多重耐药菌株占比较高，除复方新诺明、氯霉素和庆大霉素外，MRSA的耐药率高于MSSA，本耐药数据可为本地临床治疗金黄色葡萄球菌所致感染用药提供数据支撑。
金黄色葡萄球菌的ST型别丰富，多达几千种，并还在不停的增加中。本研究中83株菌有20种ST型，其中两个为新ST型，说明本地金黄色葡萄球菌种群结构丰富。MRSA以ST398、ST1和ST59为主，主要聚集在CC1、CC398和CC59克隆群上，与徐娅雯[16]报道的扬州地区MRSA以ST398和ST59为主相似；MSSA以ST22、ST398和ST188为主。ST398是本地主要流行型别，该型别金黄色葡萄球菌是全球最主要的家畜养殖相关ST型之一，在社区和医院中广泛传播，该型别菌株的毒力和耐药性在不断增强，需引起足够重视[4,17]。
通过基因注释发现本研究中菌株携带的耐药基因类型丰富，83个基因组中共鉴定出38种耐药基因，除FosB外MRSA和MSSA耐药基因携带情况差异不显著（均P>0.05）。菌株携带耐药基因情况与其耐药表型之间存在一定差异，这可能与基因注释的算法或存在新的耐药机制有关，菌株耐药机制需进一步验证。
肠毒素是导致金黄色葡萄球菌食物中毒的主要原因，目前已知的肠毒素或类肠毒素已有20余种。本研究中菌株共检测到携带8种肠毒素基因，selk和selq携带率最高（均32.53%）。5种经典肠毒素中sea（28.92%）、seb（20.48%）、sec（18.07%）携带率较高，这几种肠毒素主要由ST1和ST59型菌株携带。携带seh-sec-sell-sea-selq-selk肠毒素菌株均为ST1，携带seb-selq-selk-sea菌株均为ST59，与李辉[4]报道结果一致。MRSA肠毒素携带率高于MSSA，MRSA肠毒素谱主要为seh-sec-sell-sea-selq-sel、seb-selq-selk-sea和selk-selq-seb，MSSA肠毒素谱主要为sec-sell。杀白细胞素PVL由lukF-PV 和 lukS-PV基因共同编码合成，可诱导细胞凋亡，使金黄色葡萄球菌具有更强的侵袭性和毒力[18]，本研究中大部分菌株只携带lukF-PV基因，同时携带2种基因的菌株只有6.02%，只携带lukF-PV基因菌株产杀白细胞素PVL能力还需进一步进行验证。中毒性休克综合征毒素TSST-1的编码基因tsst-1的携带率较低（3.61%），由ST1281、ST30、ST188型MSSA菌株携带。
综上，通过对本市临床分离金黄色葡萄球菌的耐药性和基因组特征分析，丰富了金黄色葡萄球菌相关病原学数据，为更好地为遏制金黄色葡萄球菌感染传播和暴发流行提供了数据支撑。
基金
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  • 江苏省预防医学科研课题(Y2018047)
  • 淮安市创新能力建设计划(HAP201906)
文献
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2024年第51卷第9期
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doi: 10.20043/j.cnki.MPM.202312350
  • 接收时间：2023-12-18
  • 首发时间：2026-03-18
  • 出版时间：2024-05-10
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  • 收稿日期：2023-12-18
基金
江苏省预防医学科研课题(Y2018047)
淮安市创新能力建设计划(HAP201906)
作者信息
    1.淮安市疾病预防控制中心，江苏 淮安 223001
    2.涟水县疾病预防控制中心，江苏 淮安 223400
    3.淮安市突发公共卫生事件应急检测重点实验室，江苏 淮安 223001

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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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