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Article(id=1241065988666479020, tenantId=1146029695717560320, journalId=1227665162245664772, issueId=1241065978004557893, articleNumber=null, orderNo=null, doi=10.20043/j.cnki.MPM.202411391, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=null, receivedDate=1732032000000, receivedDateStr=2024-11-20, revisedDate=null, revisedDateStr=null, acceptedDate=null, acceptedDateStr=null, onlineDate=1773822789589, onlineDateStr=2026-03-18, pubDate=1740412800000, pubDateStr=2025-02-25, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1773822789589, onlineIssueDateStr=2026-03-18, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1773822789589, creator=13701087609, updateTime=1773822789589, updator=13701087609, issue=Issue{id=1241065978004557893, tenantId=1146029695717560320, journalId=1227665162245664772, year='2025', volume='52', issue='4', pageStart='577', pageEnd='768', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1773822787047, creator=13701087609, updateTime=1773823194927, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1241067688831808347, tenantId=1146029695717560320, journalId=1227665162245664772, issueId=1241065978004557893, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1241067688831808348, tenantId=1146029695717560320, journalId=1227665162245664772, issueId=1241065978004557893, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=736, endPage=741, ext={EN=ArticleExt(id=1241065989081715135, articleId=1241065988666479020, tenantId=1146029695717560320, journalId=1227665162245664772, language=EN, title=Serovars and antimicrobial resistance and antimicrobial resistance genes of Salmonella in Haidian District, Beijing, 2016-2023, columnId=1228016571713520579, journalTitle=Modern Preventive Medicine, columnName=Health Supervison, runingTitle=null, highlight=null, articleAbstract=
Objective

To mailto:analyze the serovars, antimicrobial resistance status and distribution of antimicrobial resistance genes of Salmonella in Haidian District, Beijing. To discover the connection between antimicrobial resistance phenotypes and genotypes, and to explore the impact of disinfectant use during the COVID-19 on antimicrobial resistance of Salmonella.

Methods

Serotyping and drug susceptibility testing were performed on 107 strains andnext-generation sequencing (NGS) was performed on 27 strains of Salmonella collected from 2021 to 2023.

Results

Salmonella enteritidis had the highest proportion (57.01%). Ceftazidime/avibactam and ertapenem had the highest susceptibility rates (100.0%). Ciprofloxacin had the highest intermediate rate (63.6%), and nalidixic acid had the highest resistance rate (74.8%). Antibiotic susceptibility tests showed increased resistance to multiple drugs. Among 27 strains, the carrying rate of aminoglycoside resistance genes was 100.0%. Most strains carried four or fewer resistance genes (88.9%). Salmonella enteritidis with drug-resistant genotypes of aph(6)-Id, aac(6')-Iaa, aph(3'')-Ib, blaTEM-1B and sul2 accounted for the largest proportion (42.9%). Other serovarsSalmonella with only one type of aminoglycoside resistance gene accounted for the largest proportion (53.8%). The phenotypic and genotypic resistance patterns of Salmonella to streptomycin (sensitivity 100.0%, positive predictive value 77.8%), ampicillin (sensitivity 55.6%, positive predictive value 100.0%), cefotaxime (sensitivity 60.0%, positive predictive value 80.0%), sulfamethoxazole-trimethoprim (sensitivity 60.0%, positive predictive value 85.7%), and chloramphenicol (sensitivity 50.0%, positive predictive value 100.0%) showed good agreement.

Conclusion

The antimicrobial resistance situation of Salmonella in Haidian District is serious. The impact of disinfectants and the correlation between phenotypes and genotypes should be focused on in the future.

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目的

分析北京市海淀区沙门菌血清分布、耐药现状以及耐药基因分布，找出沙门菌耐药表型和耐药基因型之间的联系，并探究新冠疫情期间广泛使用消毒剂对沙门菌耐药性的影响。

方法

对2016—2023年北京市海淀区检出的107株沙门菌进行血清分型和药敏试验，并对2021—2023年间收集到的27株沙门菌进行了高通量测序（next-generation sequencing，NGS）。

结果

肠炎沙门菌占比最高，为57.01%；药物敏感率最高的为头孢他啶/阿维巴坦和厄他培南，敏感率均为100.0%，中介率最高的为环丙沙星63.6%，耐药率最高的为萘啶酸74.8%。药敏试验结果发现新冠期间氨苄西林、头孢噻肟、萘啶酸、四环素、复方新诺明、阿奇霉素、链霉素和环丙沙星的耐药率均显著增加。27株沙门菌中氨基糖苷类耐药基因携带率最高为100.0%；携带4类及4类以下耐药基因的株数占沙门菌总株数的88.9%；耐药基因型为aph(6)-Id、aac(6’)-Iaa、aph(3’’)-Ib、blaTEM-1B、sul2的肠炎沙门菌占比最多，为42.9%，仅含有氨基糖苷类1种耐药基因的沙门菌占比最多，为53.8%。沙门菌对于链霉素（敏感性100.0%，阳性预测值77.8%）、氨苄西林（敏感性55.6%，阳性预测值100.0%）、头孢噻肟（敏感性60.0%，阳性预测值80.0%）、复方新诺明（敏感性60.0%，阳性预测值85.7%）和氯霉素（敏感性50.0%，阳性预测值100.0%）的耐药表型和耐药基因型之间的匹配性较好。

结论

海淀区沙门菌耐药情况十分严峻，使用消毒剂对沙门菌抗生素耐药性的影响以及耐药表型与耐药基因型之间相关性的研究是下一步应该关注的重点。

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白婧，E-mail：maomaobaibb@163com
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郝春芬（1972—），女，本科，副主任技师，研究方向：食品卫生检验

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Journal of Applied Microbiology, 2022, 133(5): 2902-2914., articleTitle=‘To be,or not to be’-The dilemma of ‘silent’ antimicrobial resistance genes in bacteria, refAbstract=null)], funds=[Fund(id=1241065997336105792, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065988666479020, awardId=2022-3-027, language=CN, fundingSource=首都高层次公共卫生人才建设项目(2022-3-027), fundOrder=null, country=null)], companyList=[AuthorCompany(id=1241065991627657722, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065988666479020, xref=1., ext=[AuthorCompanyExt(id=1241065991636046331, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065988666479020, companyId=1241065991627657722, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=Microbiological laboratory, Beijing Haidian District Center for Disease Control and Prevention, Beijing 100094, China), AuthorCompanyExt(id=1241065991640240636, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065988666479020, companyId=1241065991627657722, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=1.北京市海淀区疾病预防控制中心微生物检验科，北京 100094)]), AuthorCompany(id=1241065991749292547, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065988666479020, xref=2., ext=[AuthorCompanyExt(id=1241065991757681156, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065988666479020, companyId=1241065991749292547, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=2.北京市疾病预防控制中心)])], figs=[ArticleFig(id=1241065996262363891, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065988666479020, language=EN, label=Table 1, caption=

Serovars of Salmonella strains

, figureFileSmall=null, figureFileBig=null, tableContent=
群分类血清型菌株数（株）构成比（%）
B阿贡纳沙门菌21.87
鼠伤寒沙门菌1110.28
德尔卑沙门菌21.87
斯坦利沙门菌10.93
胥伐成格隆沙门菌10.93
C1布伦登卢普沙门菌65.61
奥雷宁堡沙门菌10.93
田纳西沙门菌10.93
婴儿沙门菌32.80
C2慕尼黑沙门菌21.87
科特布斯沙门菌10.93
纽波特沙门菌10.93
茨昂威沙门菌10.93
C3肯塔基沙门菌54.67
D肠炎沙门菌6157.01
都柏林沙门菌10.93
E1伦敦沙门菌54.67
E4山夫登堡沙门菌10.93
其他群古巴沙门菌10.93
合计107100.00
), ArticleFig(id=1241065996358832893, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065988666479020, language=CN, label=表1, caption=

沙门菌的血清型分布

, figureFileSmall=null, figureFileBig=null, tableContent=
群分类血清型菌株数（株）构成比（%）
B阿贡纳沙门菌21.87
鼠伤寒沙门菌1110.28
德尔卑沙门菌21.87
斯坦利沙门菌10.93
胥伐成格隆沙门菌10.93
C1布伦登卢普沙门菌65.61
奥雷宁堡沙门菌10.93
田纳西沙门菌10.93
婴儿沙门菌32.80
C2慕尼黑沙门菌21.87
科特布斯沙门菌10.93
纽波特沙门菌10.93
茨昂威沙门菌10.93
C3肯塔基沙门菌54.67
D肠炎沙门菌6157.01
都柏林沙门菌10.93
E1伦敦沙门菌54.67
E4山夫登堡沙门菌10.93
其他群古巴沙门菌10.93
合计107100.00
), ArticleFig(id=1241065996480467718, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065988666479020, language=EN, label=Table 2, caption=

Antimicrobial resistance of Salmonella

, figureFileSmall=null, figureFileBig=null, tableContent=
抗生素类别抗生素名称2016—2019（n=76）2020—2023（n=31）2016—2023（n=107）
敏感中介耐药敏感中介耐药敏感中介耐药
β-内酰胺类
青霉素类氨苄西林37（48.7）1（1.3）38（50.0）0（0.0）0（0.0）31（100.0）37（34.6）1（0.9）69（64.5）
氨苄西林-舒巴坦39（51.3）5（6.6）32（42.1）0（0.0）13（41.9）18（58.1）39（36.4）18（16.8）50（46.7）
头孢菌素类头孢噻肟73（96.1）0（0.0）3（3.9）7（22.6）1（3.2）23（74.2）80（74.8）1（0.9）26（24.3）
头孢他啶73（96.1）0（0.0）3（3.9）29（93.5）0（0.0）2（6.5）102（95.3）0（0.0）5（4.7）
头孢他啶/阿维巴坦76（100.0）0（0.0）0（0.0）31（100.0）0（0.0）0（0.0）107（100.0）0（0.0）0（0.0）
碳青霉烯类厄他培南76（100.0）0（0.0）0（0.0）31（100.0）0（0.0）0（0.0）107（100.0）0（0.0）0（0.0）
美罗培南74（97.4）2（2.6）0（0.0）30（96.8）0（0.0）1（3.2）104（97.2）2（1.9）1（0.9）
氨基糖苷类阿米卡星74（97.4）0（0.0）2（2.6）28（90.3）0（0.0）3（9.7）102（95.3）0（0.0）5（4.7）
链霉素18（23.7）19（25.0）39（51.3）4（12.9）0（0.0）27（87.1）22（20.6）19（17.8）66（61.7）
喹诺酮类萘啶酸24（31.6）0（0.0）52（68.4）3（9.7）0（0.0）28（90.3）27（25.2）0（0.0）80（74.8）
环丙沙星15（19.7）57（75.0）4（5.3）0（0.0）11（35.5）20（64.5）15（14.0）68（63.6）24（22.4）
四环素类四环素58（76.3）0（0.0）18（23.7）10（32.3）1（3.2）20（64.5）68（63.6）1（0.9）38（35.5）
替加环素75（98.7）0（0.0）1（1.3）31（100.0）0（0.0）0（0.0）106（99.1）0（0.0）1（0.9）
氯霉素类氯霉素68（89.5）0（0.0）8（10.5）22（71.0）2（6.5）7（22.6）90（84.1）2（1.9）15（14.0）
磺胺类复方新诺明68（89.5）0（0.0）8（10.5）8（25.8）0（0.0）23（74.2）76（71.0）0（0.0）31（29.0）
大环内酯类阿奇霉素72（94.7）0（0.0）4（5.3）17（54.8）0（0.0）14（45.2）89（83.2）0（0.0）18（16.8）
), ArticleFig(id=1241065996597908238, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065988666479020, language=CN, label=表2, caption=

沙门菌的耐药情况

, figureFileSmall=null, figureFileBig=null, tableContent=
抗生素类别抗生素名称2016—2019（n=76）2020—2023（n=31）2016—2023（n=107）
敏感中介耐药敏感中介耐药敏感中介耐药
β-内酰胺类
青霉素类氨苄西林37（48.7）1（1.3）38（50.0）0（0.0）0（0.0）31（100.0）37（34.6）1（0.9）69（64.5）
氨苄西林-舒巴坦39（51.3）5（6.6）32（42.1）0（0.0）13（41.9）18（58.1）39（36.4）18（16.8）50（46.7）
头孢菌素类头孢噻肟73（96.1）0（0.0）3（3.9）7（22.6）1（3.2）23（74.2）80（74.8）1（0.9）26（24.3）
头孢他啶73（96.1）0（0.0）3（3.9）29（93.5）0（0.0）2（6.5）102（95.3）0（0.0）5（4.7）
头孢他啶/阿维巴坦76（100.0）0（0.0）0（0.0）31（100.0）0（0.0）0（0.0）107（100.0）0（0.0）0（0.0）
碳青霉烯类厄他培南76（100.0）0（0.0）0（0.0）31（100.0）0（0.0）0（0.0）107（100.0）0（0.0）0（0.0）
美罗培南74（97.4）2（2.6）0（0.0）30（96.8）0（0.0）1（3.2）104（97.2）2（1.9）1（0.9）
氨基糖苷类阿米卡星74（97.4）0（0.0）2（2.6）28（90.3）0（0.0）3（9.7）102（95.3）0（0.0）5（4.7）
链霉素18（23.7）19（25.0）39（51.3）4（12.9）0（0.0）27（87.1）22（20.6）19（17.8）66（61.7）
喹诺酮类萘啶酸24（31.6）0（0.0）52（68.4）3（9.7）0（0.0）28（90.3）27（25.2）0（0.0）80（74.8）
环丙沙星15（19.7）57（75.0）4（5.3）0（0.0）11（35.5）20（64.5）15（14.0）68（63.6）24（22.4）
四环素类四环素58（76.3）0（0.0）18（23.7）10（32.3）1（3.2）20（64.5）68（63.6）1（0.9）38（35.5）
替加环素75（98.7）0（0.0）1（1.3）31（100.0）0（0.0）0（0.0）106（99.1）0（0.0）1（0.9）
氯霉素类氯霉素68（89.5）0（0.0）8（10.5）22（71.0）2（6.5）7（22.6）90（84.1）2（1.9）15（14.0）
磺胺类复方新诺明68（89.5）0（0.0）8（10.5）8（25.8）0（0.0）23（74.2）76（71.0）0（0.0）31（29.0）
大环内酯类阿奇霉素72（94.7）0（0.0）4（5.3）17（54.8）0（0.0）14（45.2）89（83.2）0（0.0）18（16.8）
), ArticleFig(id=1241065996778263322, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065988666479020, language=EN, label=Table 3, caption=

Combination and distribution of Salmonella resistance genes

, figureFileSmall=null, figureFileBig=null, tableContent=
含耐药基因类别（类）耐药基因组合肠炎沙门菌（n=14）其他沙门菌（n=13）合计（n=27）
株数
(株）		占比
（%）		株数
(株）		占比
（%）		株数
(株）		占比
（%）
1aac(6’)-Iaa214.3753.8933.3
2aac(6’)-Iaa、blaTEM-1B214.300.027.4
aac(6’)-Ia、-tet(B)00.017.713.7
aac(6’)-Iaa、fosA700.017.713.7
3aph(6)-Id、aac(6’)-Iaa、aph(3’’)-Ib、blaTEM-1B、sul2642.900.0622.2
4aph(6)-Id、aac(6’)-Ia、-aph(3’’)-Ib、blaTEM-1B、sul2、tet(A)428.600.0414.8
aac(6’)-Iaa、aac(3)-Id、aph(3’)-Ia、aadA7、blaTEM-1B、sul1、tet(A)00.017.713.7
6aac(6’)-Iaa、aadA1、aadA2、blaTEM-1B、sul2、sul3、tet(A)、tet(M)、cmlA1、floR、dfrA1200.017.713.7
7aph(6)-Id、aac(6’)-Iaa、aph(3’’)-Ib、aadA16、sul1、sul2、tet(B)、tet(M)、aac(6’)-Ib-cr、floR、arr-3、dfrA2700.017.713.7
10aac(6’)-Iaa、aadA7、aac(3)-Id、aac(3)-Ild、aadA17、aph(3’)-Ia、rmtB、blaCTX-M-55、sul1、tet(A)、floR、arr-2、dfrA14、fosA3、mphA、lnu(F)00.017.713.7
), ArticleFig(id=1241065996908286751, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065988666479020, language=CN, label=表3, caption=

沙门菌的耐药基因组合及分布

, figureFileSmall=null, figureFileBig=null, tableContent=
含耐药基因类别（类）耐药基因组合肠炎沙门菌（n=14）其他沙门菌（n=13）合计（n=27）
株数
(株）		占比
（%）		株数
(株）		占比
（%）		株数
(株）		占比
（%）
1aac(6’)-Iaa214.3753.8933.3
2aac(6’)-Iaa、blaTEM-1B214.300.027.4
aac(6’)-Ia、-tet(B)00.017.713.7
aac(6’)-Iaa、fosA700.017.713.7
3aph(6)-Id、aac(6’)-Iaa、aph(3’’)-Ib、blaTEM-1B、sul2642.900.0622.2
4aph(6)-Id、aac(6’)-Ia、-aph(3’’)-Ib、blaTEM-1B、sul2、tet(A)428.600.0414.8
aac(6’)-Iaa、aac(3)-Id、aph(3’)-Ia、aadA7、blaTEM-1B、sul1、tet(A)00.017.713.7
6aac(6’)-Iaa、aadA1、aadA2、blaTEM-1B、sul2、sul3、tet(A)、tet(M)、cmlA1、floR、dfrA1200.017.713.7
7aph(6)-Id、aac(6’)-Iaa、aph(3’’)-Ib、aadA16、sul1、sul2、tet(B)、tet(M)、aac(6’)-Ib-cr、floR、arr-3、dfrA2700.017.713.7
10aac(6’)-Iaa、aadA7、aac(3)-Id、aac(3)-Ild、aadA17、aph(3’)-Ia、rmtB、blaCTX-M-55、sul1、tet(A)、floR、arr-2、dfrA14、fosA3、mphA、lnu(F)00.017.713.7
), ArticleFig(id=1241065997025727273, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065988666479020, language=EN, label=Table 4, caption=

Analysis of the correlation between Salmonella drug resistance phenotypes and genotypes

, figureFileSmall=null, figureFileBig=null, tableContent=
耐药类别药物名称耐药基因基因耐药株数（株）表型耐药敏感性（%）阳性预测值（%）
耐药基因阳性株数（株）耐药基因阴性株数（株）
氨基糖苷类链霉素aph(3’)-Ia、aph(3’)-Ib、aph(6)-Id、aac(3)-Id、aac(3)-Ild、aac(6’)-Iaa、aadA7、aadA16、aadA17、rmtB、aadA1、aadA227210100.077.8
阿米卡星20100.07.4
β-内酰胺类氨苄西林blaTEM-1B、blaCTX-M-5515151255.6100.0
头孢噻肟12860.080.0
头孢他啶10100.06.7
厄他培南000.00.0
美罗培南000.00.0
磺胺类和甲氧嘧啶类复方新诺明sul1、sul2、sul3、dfrA12、dfrA14、dfrA271412860.085.7
四环素类四环素tet(A)、tet(B)、tet(M)971041.277.8
替加环素000.00.0
喹诺酮类萘啶酸aac(6’)-Ib-cr11214.5100.0
环丙沙星1165.9100.0
氯霉素类氯霉素cmlA1、floR22250.0100.0
大环内酯类阿奇霉素mphA11118.3100.0
利福霉素类-arr-2、arr-32----
磷霉素类-fosA3、fosA72----
林可酰胺类-lnu(F)1----
), ArticleFig(id=1241065997172527924, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241065988666479020, language=CN, label=表4, caption=

沙门菌耐药表型与耐药基因型相关性分析

, figureFileSmall=null, figureFileBig=null, tableContent=
耐药类别药物名称耐药基因基因耐药株数（株）表型耐药敏感性（%）阳性预测值（%）
耐药基因阳性株数（株）耐药基因阴性株数（株）
氨基糖苷类链霉素aph(3’)-Ia、aph(3’)-Ib、aph(6)-Id、aac(3)-Id、aac(3)-Ild、aac(6’)-Iaa、aadA7、aadA16、aadA17、rmtB、aadA1、aadA227210100.077.8
阿米卡星20100.07.4
β-内酰胺类氨苄西林blaTEM-1B、blaCTX-M-5515151255.6100.0
头孢噻肟12860.080.0
头孢他啶10100.06.7
厄他培南000.00.0
美罗培南000.00.0
磺胺类和甲氧嘧啶类复方新诺明sul1、sul2、sul3、dfrA12、dfrA14、dfrA271412860.085.7
四环素类四环素tet(A)、tet(B)、tet(M)971041.277.8
替加环素000.00.0
喹诺酮类萘啶酸aac(6’)-Ib-cr11214.5100.0
环丙沙星1165.9100.0
氯霉素类氯霉素cmlA1、floR22250.0100.0
大环内酯类阿奇霉素mphA11118.3100.0
利福霉素类-arr-2、arr-32----
磷霉素类-fosA3、fosA72----
林可酰胺类-lnu(F)1----
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2016—2023年北京市海淀区沙门菌血清型、耐药性及耐药基因分析
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郝春芬 1 , 张晓媛 2 , 刘伟 1 , 韩思媛 1 , 白婧 1
现代预防医学 | 卫生监督 2025,52(4): 736-741
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现代预防医学 | 卫生监督 2025, 52(4): 736-741
2016—2023年北京市海淀区沙门菌血清型、耐药性及耐药基因分析
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郝春芬1, 张晓媛2, 刘伟1, 韩思媛1, 白婧1
作者信息
  • 1.北京市海淀区疾病预防控制中心微生物检验科，北京 100094
  • 2.北京市疾病预防控制中心

    • 郝春芬（1972—），女，本科，副主任技师，研究方向：食品卫生检验

通讯作者:

白婧，E-mail：maomaobaibb@163com
Serovars and antimicrobial resistance and antimicrobial resistance genes of Salmonella in Haidian District, Beijing, 2016-2023
Chun-fen HAO1, Xiao-yuan ZHANG2, Wei LIU1, Si-yuan HAN1, Jing BAI1
Affiliations
  • Microbiological laboratory, Beijing Haidian District Center for Disease Control and Prevention, Beijing 100094, China
出版时间: 2025-02-25 doi: 10.20043/j.cnki.MPM.202411391
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摘要
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目的

分析北京市海淀区沙门菌血清分布、耐药现状以及耐药基因分布，找出沙门菌耐药表型和耐药基因型之间的联系，并探究新冠疫情期间广泛使用消毒剂对沙门菌耐药性的影响。

方法

对2016—2023年北京市海淀区检出的107株沙门菌进行血清分型和药敏试验，并对2021—2023年间收集到的27株沙门菌进行了高通量测序（next-generation sequencing，NGS）。

结果

肠炎沙门菌占比最高，为57.01%；药物敏感率最高的为头孢他啶/阿维巴坦和厄他培南，敏感率均为100.0%，中介率最高的为环丙沙星63.6%，耐药率最高的为萘啶酸74.8%。药敏试验结果发现新冠期间氨苄西林、头孢噻肟、萘啶酸、四环素、复方新诺明、阿奇霉素、链霉素和环丙沙星的耐药率均显著增加。27株沙门菌中氨基糖苷类耐药基因携带率最高为100.0%；携带4类及4类以下耐药基因的株数占沙门菌总株数的88.9%；耐药基因型为aph(6)-Id、aac(6’)-Iaa、aph(3’’)-Ib、blaTEM-1B、sul2的肠炎沙门菌占比最多，为42.9%，仅含有氨基糖苷类1种耐药基因的沙门菌占比最多，为53.8%。沙门菌对于链霉素（敏感性100.0%，阳性预测值77.8%）、氨苄西林（敏感性55.6%，阳性预测值100.0%）、头孢噻肟（敏感性60.0%，阳性预测值80.0%）、复方新诺明（敏感性60.0%，阳性预测值85.7%）和氯霉素（敏感性50.0%，阳性预测值100.0%）的耐药表型和耐药基因型之间的匹配性较好。

结论

海淀区沙门菌耐药情况十分严峻，使用消毒剂对沙门菌抗生素耐药性的影响以及耐药表型与耐药基因型之间相关性的研究是下一步应该关注的重点。

沙门菌  /  抗生素耐药性  /  耐药基因  /  消毒剂
Objective

To mailto:analyze the serovars, antimicrobial resistance status and distribution of antimicrobial resistance genes of Salmonella in Haidian District, Beijing. To discover the connection between antimicrobial resistance phenotypes and genotypes, and to explore the impact of disinfectant use during the COVID-19 on antimicrobial resistance of Salmonella.

Methods

Serotyping and drug susceptibility testing were performed on 107 strains andnext-generation sequencing (NGS) was performed on 27 strains of Salmonella collected from 2021 to 2023.

Results

Salmonella enteritidis had the highest proportion (57.01%). Ceftazidime/avibactam and ertapenem had the highest susceptibility rates (100.0%). Ciprofloxacin had the highest intermediate rate (63.6%), and nalidixic acid had the highest resistance rate (74.8%). Antibiotic susceptibility tests showed increased resistance to multiple drugs. Among 27 strains, the carrying rate of aminoglycoside resistance genes was 100.0%. Most strains carried four or fewer resistance genes (88.9%). Salmonella enteritidis with drug-resistant genotypes of aph(6)-Id, aac(6')-Iaa, aph(3'')-Ib, blaTEM-1B and sul2 accounted for the largest proportion (42.9%). Other serovarsSalmonella with only one type of aminoglycoside resistance gene accounted for the largest proportion (53.8%). The phenotypic and genotypic resistance patterns of Salmonella to streptomycin (sensitivity 100.0%, positive predictive value 77.8%), ampicillin (sensitivity 55.6%, positive predictive value 100.0%), cefotaxime (sensitivity 60.0%, positive predictive value 80.0%), sulfamethoxazole-trimethoprim (sensitivity 60.0%, positive predictive value 85.7%), and chloramphenicol (sensitivity 50.0%, positive predictive value 100.0%) showed good agreement.

Conclusion

The antimicrobial resistance situation of Salmonella in Haidian District is serious. The impact of disinfectants and the correlation between phenotypes and genotypes should be focused on in the future.

Salmonella  /  Antimicrobial resistance  /  Antimicrobial resistance genes  /  Disinfectants
郝春芬, 张晓媛, 刘伟, 韩思媛, 白婧. 2016—2023年北京市海淀区沙门菌血清型、耐药性及耐药基因分析. 现代预防医学, 2025 , 52 (4) : 736 -741 . DOI: 10.20043/j.cnki.MPM.202411391
Chun-fen HAO, Xiao-yuan ZHANG, Wei LIU, Si-yuan HAN, Jing BAI. Serovars and antimicrobial resistance and antimicrobial resistance genes of Salmonella in Haidian District, Beijing, 2016-2023[J]. Modern Preventive Medicine, 2025 , 52 (4) : 736 -741 . DOI: 10.20043/j.cnki.MPM.202411391
正文
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沙门菌是全球范围内引起腹泻的四大病原体之一，疾病的严重程度主要取决于宿主因素和沙门菌血清型。临床上抗生素的使用是应对细菌感染最有效的方法之一，但农业养殖和临床治疗中频繁且不合理的抗生素滥用使得致病菌耐药问题日益凸显[1]，同时消毒剂的使用会导致细菌对消毒剂和抗生素产生交叉耐药性[2]。世界卫生组织（World Health Organization, WHO）在2024年人类健康领域抗生素耐药性（Antimicrobial Resistance, AMR）研究议程中，已经将沙门菌抗生素耐药问题列为2030年前亟待解决的研究重点之一[3]。为了从遗传水平探明沙门菌的耐药机制问题，越来越多的研究关注到用全基因组测序技术对菌株的整个基因组进行测序得到全基因组序列，并分析耐药基因型与耐药表型之间的相关性[4-5]，以期通过新技术挖掘未知潜在的耐药机制和预测耐药表型。我区从2016年开始对沙门菌抗生素耐药性进行监测，并于2021年开展了沙门菌株的全基因组测序工作。本研究主要对海淀区2016—2023年沙门菌抗生素耐药监测结果进行分析，掌握沙门菌耐药性的流行特征以及消毒剂使用对沙门菌耐药性的影响，并对耐药基因型与耐药表型进行比对分析，探究二者之间的相关性，为预测沙门菌耐药趋势以及指导地区合理用药提供科学指导。
1　材料与方法
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1.1　菌株来源
生物样本为2016年1月至2023年12月就诊于北京大学第三医院肠道门诊、北京市海淀医院肠道门诊以及北京市上地医院肠道门诊主诉症状为腹泻的患者大便标本。从上述生物样本中分离培养得到107株沙门菌菌。
1.2　试验方法
1.2.1　血清鉴定
沙门菌分离培养按照当年国家致病菌识别网技术手册进行，沙门菌血清鉴定参照Kauffman-White沙门菌抗原表（2007版）报告最终的血清型。
1.2.2　药敏试验
按照美国临床实验室标准化委员会（Clinical and Laboratory Standards Institute, CLSI）出版的药敏试验指南选取氨苄西林、氨苄西林-舒巴坦、头孢噻肟、头孢他啶、头孢他啶/阿维巴坦、阿米卡星、链霉素、萘啶酸、环丙沙星、四环素、替加环素、氯霉素、复方新诺明、阿奇霉素、厄他培南和美罗培南共16种抗生素进行药敏试验。药敏试验采用微量肉汤法，试验操作按照上海星佰生物技术有限公司革兰阴性需氧菌药敏检测板使用说明书进行，根据微生物的生长情况判断出各抗菌药物的最低抑菌浓度（Minimum Inhibitory Concentration, MIC），参考CLSI药敏试验指南最新版本各抗菌药物折点浓度判读试验结果，敏感（Susceptible, S），中介（Intermediate, I）以及耐药（Resistant, R）。
1.2.3　全基因组测序
参照国家致病菌识别网技术手册中细菌纯培养物二代基因组测序操作规范使用QIAamp DNA Mini Kit试剂盒提取沙门菌菌株核酸，用Qubit测量核酸浓度，控制OD260/ OD280在1.7~1.9之间。合格的样本通过Illunina MiSeq平台进行全基因组测序，采用微未来服务器对测序原始数据进行组装，并将测序结果上传至国家致病菌识别网系统和https://cge.cbs.dtu.dk//services/ResFinder/数据库得到预测的血清结果和耐药基因。
1.3　统计学分析
用分析软件GraphPad Prism 8.0对试验结果进行统计分析，药物敏感率、中介率和耐药率各自之间的差异比较采用卡法检验，检验水准α=0.05。参照Genders等人[6]的计算公式计算耐药基因和耐药表型之间的敏感性和阳性预测值。敏感性用来判断基因耐药对表型耐药的灵敏度，阳性预测值则决定了是否能够通过检测菌株的耐药基因来判断实际的表型耐药情况。
2　结果
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2.1　沙门菌血清型分布
肠炎沙门菌占比为57.01%，其次是鼠伤寒沙门菌和布伦登卢普沙门菌，占比分别为10.28%和5.61%。见表1。对2021—2023年间收集到的27株沙门菌进行了全基因组测序，测序得到的27株沙门菌血清型结果与经典的血清凝集结果一致。
2.2　沙门菌药敏试验结果
2016—2023年，头孢他啶/阿维巴坦和厄他培南的药物敏感率最高为100.0%；中介率最高为环丙沙星（中介率63.6%）；耐药率最高为萘啶酸（耐药率74.8%）。见表2。
本文将2016—2019年收集到的76株沙门菌定义为新冠疫情前收集到的菌株，将2020—2023年收集到的31株沙门菌定义为疫情期间收集到的菌株。16种抗生素的药敏试验表明，氨苄西林、头孢噻肟、萘啶酸、四环素、复方新诺明和阿奇霉素这6种抗生素疫情期间药物敏感率下降（χ2值分别为23.070，63.000，5.598，18.450，43.370和25.050，P值均≤0.05），耐药率增加（χ2值分别为24.040，59.070，5.598，16.030，43.370和25.050，P值均≤0.05）；氨苄西林-舒巴坦和氯霉素疫情期间药物敏感率下降（χ2值分别为25.030和5.643，P值均≤0.05），中介率增加（χ2值分别为19.670和4.997，P值均≤0.05）；链霉素疫情期间药物中介率下降（χ2=9.423，P=0.002），耐药率增加（χ2=11.930，P<0.001）；环丙沙星疫情期间药物敏感率和中介率均下降（χ2=7.116，P=0.008；χ2=14.840，P<0.001），耐药率增加（χ2=44.430，P<0.001）。疫情期间氨苄西林、氨苄西林-舒巴坦和环丙沙星的药物敏感率均下降为0.0%。
2.3　沙门菌耐药基因分布情况
对2021—2023年间收集到的27株沙门菌进行了二代测序(Next-generation sequencing，NGS)，结果显示27株沙门菌共携带11大类32种耐药基因。氨基糖苷类耐药基因携带率为100.0%，其次是β-内酰胺类和磺胺类，携带率分别是55.6%和51.9%）。氨基糖苷类耐药基因中，aac(6’)-Iaa的携带率为100.0%；携带β-内酰胺类耐药基因的15株沙门菌，仅有1株携带blaCTX-M-55，其余携带的此类耐药基因均为blaTEM-1B；14株携带磺胺类耐药基因的沙门菌中，12株沙门菌携带了sul2基因，仅有2株未携带此类磺胺类耐药基因。27株沙门菌携4类及4类以下耐药基因的株数占总株数的88.9%。见表3。
在肠炎沙门菌中只检测到氨基糖苷类、β-内酰胺类、磺胺类和四环素类这4类耐药基因，其中耐药基因型为aph(6)-Id、aac(6’)-Iaa、aph(3’)-Ib、blaTEM-1B、sul2的肠炎沙门菌占比最多，为42.9%；其他血清型沙门菌中，仅含有氨基糖苷类1种耐药基因的沙门菌占比最多，为53.8%（7/13），耐药基因型为aac(6’)-Iaa，其余6株沙门菌耐药基因型各不相同。见表3。
2.4　沙门菌耐药表型与耐药基因相关性分析
敏感度用来衡量耐药基因型对耐药表型的灵敏度。耐药基因型对链霉素、阿米卡星和头孢他啶的敏感度较高，均达到100.0%；其次为头孢噻肟、复方新诺明、氨苄西林和氯霉素，敏感度呈现中等偏上水平，分别为60.0%、60.0%、55.6%和50.0%；对其他测试抗生素敏感度较低，均未达到50.0%。阳性预测值用来判断耐药基因型阳性是否表现为表型耐药的概率。氨苄西林、萘啶酸、环丙沙星、氯霉素和阿奇霉素的阳性预测值均为100.0%；复方新诺明、头孢噻肟、链霉素和四环素的阳性预测值较高，分别为85.7%、80.0%、77.8%和77..8%；其他测试抗生素阳性预测值较低，均未达到50.0%。由此可见，链霉素、氨苄西林、头孢噻肟、复方新诺明和氯霉素耐药基因和耐药表型匹配度较好。见表4。
3　讨论
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北京市海淀区从2016年开始对辖区内肠道门诊患者大便标本的沙门菌株进行耐药监测，白婧等人通过耐药监测发现2016—2019年间，52.6%的沙门菌为多重耐药株，2019年海淀区更是检出了2株耐18种抗生素的“超级耐药菌”[7]。本研究结果显示，沙门菌对萘啶酸的耐药率为74.8%，对环丙沙星的的中介率达到了63.6%，高于北京市2018—2021年的平均水平[4]。2020年至2023年全球人民经历了新型冠状病毒带来的重大疫情，为了广泛的控制或杀死病原微生物，疫情期间消毒剂被大量使用，有研究显示仅2020年1年全球表面消毒剂的销售额就达到了45亿美元，增速为2019年的30%[8]。而消毒剂长期大量或不恰当的应用使得细菌在对消毒剂产生抗性的同时对抗生素也产生交叉耐药性，导致细菌对抗生素耐药性增加[9]。例如细菌细胞膜通透性的降低、主动外排泵作用的表达以及作用靶位点基因的改变等，这些共同耐药机制会导致细菌对抗身素敏感性降低。另外，当细菌面临消毒剂的持续诱导和选择压力时，细菌会利用质粒、转座子以及基因盒等可移动遗传元件，通过结合、移动、转导和转化的方式从其他细菌处获得抗性基因，其中就包括抗生素耐药基因。这种在不同菌株间水平转移抗性基因的方式不仅增加了消毒剂抗性传播的风险也同时加剧了抗生素耐药基因在不同菌株间的广泛传播[10]。本研究结果显示，相较于疫情前，测试的16种抗生素中除碳青霉烯类的厄他培南和美罗培南以外，疫情期间收集到的沙门菌株对受试的其他种类抗生素中的1种或几种敏感性或中介性有所下降，耐药性增加。随着消毒剂在社会生活和家庭生活中被广泛应用，长期低剂量使用消毒剂对沙门菌抗生素耐药性的影响应该引起足够的关注。
27株沙门菌NGS二代测序结果发现，所有测试菌株均携带aac(6’)-Iaa基因，该基因与链霉素耐药相关，编码氨基糖苷乙酰转移酶，这与北京市食品来源的沙门菌株耐药基因检测结果相一致[11]。虽然链霉素不是沙门菌感染的一线用药，但其作为促生长剂常被用在禽畜养殖中，耐药基因在食物链中广泛传递。本研究中55.6%的菌株携带β-内酰胺类耐药基因中，其中93.3%携带blaTEM-1B型耐药基因，且85.7%的肠炎沙门菌携带此类耐药基因，有研究表明blaTEM-1B型耐药基因主要分布在人源的肠炎沙门和鼠伤寒沙门菌变种中[12]，这与本研究结果相一致。本研究还发现肠炎沙门菌与其他血清型沙门菌耐药基因分布区别较大，在肠炎沙门菌中只检测到氨基糖苷、β-内酰胺、磺胺和四环素这4类耐药基因，且同时含有其中3类或4类耐药基因的肠炎沙门菌菌株占比最多为71.4%，而61.4%的其他血清型沙门菌仅含有aac(6’)-Iaa这一种耐药基因，另外5株其他血清型沙门菌耐药基因普十分丰富，最多1株含有多达10类耐药基因。很多研究均表明，耐药基因分布和抗生素耐药率在不同血清型沙门菌之间有所不同[12-13]，有针对性的地区耐药监测工作的开展和对于该地区优势血清型沙门菌株耐药基因的细致研究对临床经验用药更具有指导意义。
耐药基因和耐药表型的匹配程度关系到是否可以通过全基因组测序技术检测沙门菌携带的耐药基因来预测沙门菌的表型耐药情况。本研究结果显示，耐药基因的表达率较高，特别是链霉素、氨苄西林、头孢噻肟、复方新诺明和氯霉素耐药基因和耐药表型的匹配度较好，这说明沙门菌的耐药表型和耐药基因高度相关。值得注意的是沙门菌对喹诺酮类的萘啶酸和环丙沙星耐药率较高，但测试菌株耐药基因携带率较低，这主要是因为本研究只检测了沙门菌携带的固有耐药基因，而未对突变基因进行检测。喹诺酮类药物的耐药机制主要为耐药决定区（QRDR）发生氨基酸（gyrA、gyrB、parC）点突变所致，有研究表明本研究检测到的aac(6’)-Ib-cr乙酰化酶基因为PMQR基因，仅引起低水平的耐药，只有菌株同时携带QRDR突变基因和PMQR基因时才会引起沙门菌对喹诺酮类药物普遍耐药[12]。氨基糖苷类和β-内酰胺类耐药基因在海淀区沙门菌中携带率较高，但阿米卡星和头孢他啶的耐药率普遍较低，对于这2种药物耐药基因未产生表型耐药。耐药性的表达受限于耐药基因的表达方式和表达水平，同时受到环境等相关因素的影响，如果控制耐药基因表达的因素一旦改变，某种机制发挥作用将这些“沉默”的耐药基因切换到“激活”模式，菌株的耐药性将会发生改变，这对于临床治疗来说将会成为一个潜在的威胁[14]。全基因组测序技术相较于传统的药敏实验可以提供更多潜在的耐药信息，对于预测某地区菌株的耐药趋势以及防控策略的制定至关重要。
本研究显示部分耐药基因型与耐药表型之间仍存在一些差异，这也将是我们下一步关注和探究的重点。在今后的研究中，除了常用药物的耐药基因外，可以运用全基因组测序技术等新一代细菌耐药监测工具对菌株中普遍存在的一些功能基因进行监测，从分子水平理解和细分耐药的遗传因素，这不仅有助于进一步探明细菌的耐药机制，同时对于细菌潜在耐药趋势的预测也可以更高效的指导监管和监督工作的开展。
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  • 首都高层次公共卫生人才建设项目(2022-3-027)
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2025年第52卷第4期
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doi: 10.20043/j.cnki.MPM.202411391
  • 接收时间：2024-11-20
  • 首发时间：2026-03-18
  • 出版时间：2025-02-25
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  • 收稿日期：2024-11-20
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首都高层次公共卫生人才建设项目(2022-3-027)
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    1.北京市海淀区疾病预防控制中心微生物检验科，北京 100094
    2.北京市疾病预防控制中心

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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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