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Article(id=1241522927514997503, tenantId=1146029695717560320, journalId=1227665162245664772, issueId=1241522919977841545, articleNumber=null, orderNo=null, doi=10.20043/j.cnki.MPM.202310202, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=null, receivedDate=1696953600000, receivedDateStr=2023-10-11, revisedDate=null, revisedDateStr=null, acceptedDate=null, acceptedDateStr=null, onlineDate=1773931732299, onlineDateStr=2026-03-19, pubDate=1710000000000, pubDateStr=2024-03-10, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1773931732299, onlineIssueDateStr=2026-03-19, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1773931732299, creator=13701087609, updateTime=1773931732299, updator=13701087609, issue=Issue{id=1241522919977841545, tenantId=1146029695717560320, journalId=1227665162245664772, year='2024', volume='51', issue='5', pageStart='769', pageEnd='960', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1773931730503, creator=13701087609, updateTime=1773931880386, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1241523548695622547, tenantId=1146029695717560320, journalId=1227665162245664772, issueId=1241522919977841545, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1241523548695622548, tenantId=1146029695717560320, journalId=1227665162245664772, issueId=1241522919977841545, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=930, endPage=936, ext={EN=ArticleExt(id=1241522927896679188, articleId=1241522927514997503, tenantId=1146029695717560320, journalId=1227665162245664772, language=EN, title=Distribution, drug resistance, and genome sequencing analysis of Salmonella in domestic sewage in Jining city, columnId=1228016571713520579, journalTitle=Modern Preventive Medicine, columnName=Health Supervison, runingTitle=null, highlight=null, articleAbstract=
Objective

To understand the distribution, serotype, and drug resistance of Salmonella in domestic sewage in Jining city, and to analyze the whole genome sequencing so as to provide scientific basis for the prevention and control of Salmonella.

Methods

From February to March in 2023, two samples of sewage from the intake of 3 urban sewage plants with 500 ml each were collected continuously for 7 weeks. A total of 42 sewage samples were collected for culture, isolation, and identification of Salmonella. The isolated Salmonella was tested for serum agglutination test and fluorescent quantitative PCR serotyping. In total 41 strains of Salmonella were tested for minimum inhibitory concentration (MIC) of 17 drugs in 9 classes by microbroth dilution method, followed by genome sequencing and phylogenetic analysis.

Results

The isolation rate of Salmonella from domestic sewage in Jining city was high. Among 24 positive samples, 41 strains of Salmonella were isolated, belonging to 9 serotypes, mainly S. Agona and S. Kentucky. Liying and Jidong sewage treatment plants had their own unique serotypes. Only one strain of S. Give was not resistant, and the other 40 strains of Salmonella were multi-drug resistant. The resistance rates to sulfamethoxazole, tetracycline, ampicillin, and streptomycin were more than 90%, and the resistance rate to ampicillin/sulbactam was more than 80%. There were 19 kinds of drug resistance spectra, of which SXT-TET-STR-AMP-AMS ranked the first place. The resistance spectra of different serotypes of Salmonella were different. S. Kentucky, S. Gold Coast, and S. Infant were multi-drug resistant seriously. The resistance spectrum of the same serotype was also inconsistent in different sewage plants, and the resistance was the most serious in Liying sewage plant. The CARD database was used to predict drug resistance genes, mainly predicting 18 drug resistance genes in 8 types of drug resistance families, and the drug resistance phenotypes and drug resistance genes were almost all consistent. The ST types of different serotypes of Salmonella were different, and ST13 S. Agona was dominant. The phylogenetic tree was divided into 6 clusters, and strains in different sewage plants were in different branches, indicating that their genomes were different and had different sources.

Conclusion

There are various serotypes of salmonella in domestic sewage in Jining city, suggesting that they might have exist and spread in the population. Almost all strains are multi-drug resistant bacteria, carrying resistance genes extensively. Some types of strains live persistently and distribute across regions, leading to the potential risk to population. It is necessary to carry out continuous monitor, and scientific prevention and control measures need to be formulated to control the epidemic of salmonella and the aggravation of drug resistance.

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目的

了解济宁市城区生活污水中沙门菌分布、血清型、耐药特征，并进行全基因组测序分析，为沙门菌的防控提供科学依据。

方法

2023年2—3月，每周采集城区3个污水厂进水口污水各2份，每份500 ml，连续采集7周，合计42份污水样本，对污水样本进行沙门菌的培养、分离、鉴定，分离出的沙门菌进行血清凝集试验和荧光定量PCR血清分型，利用微量肉汤稀释法对41株沙门菌进行9类17种药物的最低抑菌浓度(minimum inhibitory concentration，MIC)检测，进行全基因组测序及系统进化分析。

结果

济宁市城区生活污水沙门菌分离率较高，42份样本中阳性样本24份，共分离出41株沙门菌，属9种血清型，以阿贡纳和肯塔基为主，李营和济东污水厂有其独有的血清型。只有1株吉韦沙门菌不耐药，其余40株沙门菌均为多重耐药菌，对复方新诺明、四环素、氨苄西林、链霉素耐药率达90%以上，对氨苄西林/舒巴坦耐药率达80%以上，共19种耐药谱，SXT-TET-STR-AMP-AMS占首位，不同血清型沙门菌的耐药谱不同，肯塔基沙门菌、黄金海岸沙门菌、婴儿沙门菌的多重耐药非常严重，同种血清型在不同污水厂中的耐药谱也不一致，李营污水厂的沙门菌耐药现象最严重。利用CARD数据库进行耐药基因预测，主要预测出8类耐药家族的18个耐药基因，耐药表型与耐药基因几乎全部一致。不同血清型沙门菌的ST分型不同，以ST13的阿贡纳沙门菌为主，进化树分为6个簇，不同污水厂的沙门菌在不同分支，提示基因组有差异，不同源。

结论

济宁市城区生活污水中沙门菌血清型多样，提示可能已在人群中存在并传播，耐药严重，携带耐药基因广泛，有些型别菌株持续存在且跨区域分布，有致病风险，需持续监测，并制定对科学的防控措施以控制沙门菌的流行及耐药的加重。

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尹强，E-mail:
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王胜男（1989—），女，本科，主管技师，研究方向：从事病原微生物检验研究

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王胜男（1989—），女，本科，主管技师，研究方向：从事病原微生物检验研究

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王胜男（1989—），女，本科，主管技师，研究方向：从事病原微生物检验研究

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Acta Microbiologica Sinica, 2016, 56(2): 169-179., articleTitle=Classification and prevalence of plasmid-mediated quinolone resistance qnr genes in China-A review, refAbstract=null), Reference(id=1241678351081993161, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522927514997503, doi=null, pmid=null, pmcid=null, year=2022, volume=43, issue=7, pageStart=996, pageEnd=1001, url=null, language=null, rfNumber=[25], rfOrder=38, authorNames=闫梅英, 阚飙, journalName=中华流行病学杂志, refType=null, unstructuredReference=闫梅英， 阚飙.建设部门协同机制和监测网络应对沙门菌感染疫情[J].中华流行病学杂志，2022，43（7）：996-1001., articleTitle=建设部门协同机制和监测网络应对沙门菌感染疫情, refAbstract=null), Reference(id=1241678352969429964, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522927514997503, doi=null, pmid=null, pmcid=null, year=2022, volume=43, issue=7, pageStart=996, pageEnd=1001, url=null, language=null, rfNumber=[25], rfOrder=39, authorNames=Yan MY, Kan B, journalName=Chinese Journal of Epidemiology, refType=null, unstructuredReference=Yan MY, Kan B. Establishment of multi-sector collaborative mechanism and surveillance network for Salmonella infection outbreak response and control[J]. Chinese Journal of Epidemiology, 2022, 43(7): 996-1001., articleTitle=Establishment of multi-sector collaborative mechanism and surveillance network for Salmonella infection outbreak response and control, refAbstract=null)], funds=null, companyList=[AuthorCompany(id=1241678290335887748, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522927514997503, xref=1., ext=[AuthorCompanyExt(id=1241678290344276358, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522927514997503, companyId=1241678290335887748, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=Department of Microbiology, Jining Center for Disease Control and Prevention, Jining, Shandong 272000, China), AuthorCompanyExt(id=1241678290352664967, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522927514997503, companyId=1241678290335887748, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=1.济宁市疾病预防控制中心微生物检验科，山东 济宁 272000)]), AuthorCompany(id=1241678292361736594, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522927514997503, xref=2., ext=[AuthorCompanyExt(id=1241678292374319508, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522927514997503, companyId=1241678292361736594, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=2.任城区疾病预防控制中心微生物检验科)])], figs=[ArticleFig(id=1241678320681677466, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522927514997503, language=EN, label=Figure 1, caption=Heat map of drug resistance phenotypes of Salmonella in domestic sewage in Jining, figureFileSmall=hpCcmzk4neIVfvqa7O4Wzg==, figureFileBig=AZFcee5Ar+HHbdsfxT1uIw==, tableContent=null), ArticleFig(id=1241678321558287006, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522927514997503, language=CN, label=图1, caption=济宁市城区生活污水中沙门菌耐药表型热力图, figureFileSmall=hpCcmzk4neIVfvqa7O4Wzg==, figureFileBig=AZFcee5Ar+HHbdsfxT1uIw==, tableContent=null), ArticleFig(id=1241678322007077544, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522927514997503, language=EN, label=Figure 2, caption=Heat map of drug resistance genes of Salmonella in urban sewage of Jining city, figureFileSmall=ofwyKUkdbozgfzLsCsNNPA==, figureFileBig=rlH4WTLbMVQE5jpkyBbN7A==, tableContent=null), ArticleFig(id=1241678322392953518, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522927514997503, language=CN, label=图2, caption=济宁市城区生活污水中沙门菌耐药基因携带热力图, figureFileSmall=ofwyKUkdbozgfzLsCsNNPA==, figureFileBig=rlH4WTLbMVQE5jpkyBbN7A==, tableContent=null), ArticleFig(id=1241678323030487736, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522927514997503, language=EN, label=Figure 3, caption=Phylogenetic tree of Salmonella in urban sewage of Jining city, figureFileSmall=nv7V2upBPWtp5fBK1xEYKA==, figureFileBig=SASQFGlRQcCb1amBSEL8DA==, tableContent=null), ArticleFig(id=1241678323311506107, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522927514997503, language=CN, label=图3, caption=济宁市城区生活污水中沙门菌进化树, figureFileSmall=nv7V2upBPWtp5fBK1xEYKA==, figureFileBig=SASQFGlRQcCb1amBSEL8DA==, tableContent=null), ArticleFig(id=1241678323839988425, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522927514997503, language=EN, label=Figure 4, caption=Spatial and temporal distribution of Salmonella in domestic sewage in Jining city, figureFileSmall=Ntw6Kp2OsqD5TyfFCIolzg==, figureFileBig=+oc2Bj3PEcq4oMe1LBfoeA==, tableContent=null), ArticleFig(id=1241678324427190992, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522927514997503, language=CN, label=图4, caption=济宁市城区生活污水中沙门菌的时空分布, figureFileSmall=Ntw6Kp2OsqD5TyfFCIolzg==, figureFileBig=+oc2Bj3PEcq4oMe1LBfoeA==, tableContent=null), ArticleFig(id=1241678324737569492, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522927514997503, language=EN, label=Table 1, caption=

Detection of Salmonella in domestic sewage in Jining city

, figureFileSmall=null, figureFileBig=null, tableContent=
污水厂检测样本数阳性样本数阳性率（%）菌株数血清型（菌株数）独有沙门菌血清型
李营14964.2814婴儿（3），德尔卑（1），阿贡纳（4），黄金海岸（2），肯塔基（2），哈瓦那（2）德尔卑，黄金海岸，哈瓦那
安居14535.719肯塔基（4），阿贡纳（4），婴儿（1）
济东141071.4218吉韦（1），伦敦（1），阿贡纳（15）肠炎（1）吉韦，伦敦，肠炎
), ArticleFig(id=1241678324867592924, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522927514997503, language=CN, label=表1, caption=

济宁市城区生活污水中沙门菌的检出情况

, figureFileSmall=null, figureFileBig=null, tableContent=
污水厂检测样本数阳性样本数阳性率（%）菌株数血清型（菌株数）独有沙门菌血清型
李营14964.2814婴儿（3），德尔卑（1），阿贡纳（4），黄金海岸（2），肯塔基（2），哈瓦那（2）德尔卑，黄金海岸，哈瓦那
安居14535.719肯塔基（4），阿贡纳（4），婴儿（1）
济东141071.4218吉韦（1），伦敦（1），阿贡纳（15）肠炎（1）吉韦，伦敦，肠炎
), ArticleFig(id=1241678325333160677, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522927514997503, language=EN, label=Table 2, caption=

Susceptibility results of Salmonella in domestic sewage in Jining city

, figureFileSmall=null, figureFileBig=null, tableContent=
抗生素类别抗生素名称敏感中介耐药
氯霉素类氯霉素(CHL)23（56.10）1（2.43）17（41.46）
磺胺类复方新诺明(SXT)4（9.76）0（0.00）37（90.24）
多肽类多粘菌素E (CT)0（0.00）40（97.56）1（2.43）
碳青霉烯类厄他培南(ETP)41（100.00）0（0.00）0（0.00）
美罗培南(MEM)41（100.00）0（0.00）0（0.00）
β-内酰胺类头孢噻肟(CTX)27（65.85）0（0.00）14（34.14）
头孢他啶(CAZ)30（73.17）5（12.19）6（14.63）
头孢他啶/阿维巴坦(CZA)41（100.00）0 (0.00)0 (0.00)
氨苄西林（AMP）1 (2.43)0 (0.00)40 (97.56)
氨苄西林/舒巴坦（AMS）1 (2.43)4 (9.76)36 (87.80)
四环素类四环素(TET)3 (7.32)1 (2.43)37 (90.24)
甘胺酰环素类替加环素(TIG)21 (51.21)0 (0.00)20 (48.78)
喹诺酮类萘啶酸(NAL)23 (56.09)0 (0.00)18 (43.90)
环丙沙星(CIP)1 (2.43)21 (51.22)19 (46.34)
氨基糖苷类阿米卡星(AMI)40 (97.56)0 (0.00)1 (2.43)
链霉素(STR)0 (0.00)3 (7.31)38 (92.68)
), ArticleFig(id=1241678326218158826, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522927514997503, language=CN, label=表2, caption=

济宁市城区生活污水中沙门菌的药敏结果

, figureFileSmall=null, figureFileBig=null, tableContent=
抗生素类别抗生素名称敏感中介耐药
氯霉素类氯霉素(CHL)23（56.10）1（2.43）17（41.46）
磺胺类复方新诺明(SXT)4（9.76）0（0.00）37（90.24）
多肽类多粘菌素E (CT)0（0.00）40（97.56）1（2.43）
碳青霉烯类厄他培南(ETP)41（100.00）0（0.00）0（0.00）
美罗培南(MEM)41（100.00）0（0.00）0（0.00）
β-内酰胺类头孢噻肟(CTX)27（65.85）0（0.00）14（34.14）
头孢他啶(CAZ)30（73.17）5（12.19）6（14.63）
头孢他啶/阿维巴坦(CZA)41（100.00）0 (0.00)0 (0.00)
氨苄西林（AMP）1 (2.43)0 (0.00)40 (97.56)
氨苄西林/舒巴坦（AMS）1 (2.43)4 (9.76)36 (87.80)
四环素类四环素(TET)3 (7.32)1 (2.43)37 (90.24)
甘胺酰环素类替加环素(TIG)21 (51.21)0 (0.00)20 (48.78)
喹诺酮类萘啶酸(NAL)23 (56.09)0 (0.00)18 (43.90)
环丙沙星(CIP)1 (2.43)21 (51.22)19 (46.34)
氨基糖苷类阿米卡星(AMI)40 (97.56)0 (0.00)1 (2.43)
链霉素(STR)0 (0.00)3 (7.31)38 (92.68)
), ArticleFig(id=1241678327027659507, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522927514997503, language=EN, label=Table 3, caption=

Drug resistance patterns of different serotypes of Salmonella in domestic sewage in Jining city

, figureFileSmall=null, figureFileBig=null, tableContent=
血清型污水厂耐药谱菌株数
阿贡纳沙门菌李营SXT-TET-TIG-CIP-STR-AMP-AMS2
SXT-TET-STR-AMP-AMS2
安居SXT-TET-TIG-STR-AMP-AMS2
SXT-TET-NAL-STR-AMP-AMS2
济东SXT-TET-STR-AMP-AMS5
SXT-TET-CIP-STR-AMP-AMS4
SXT-TET-TIG-STR-AMP-AMS2
SXT-TET-NAL-STR-AMP-AMS1
SXT-CTX-CAZ-TET-STR-AMP-AMS1
SXT-TET-CIP-NAL-STR-AMP-AMS1
CHL-SXT-CTX-TET-TIG-CIP-STR-AMP-AMS1
肯塔基沙门菌李营CHL-SXT-CTX-CAZ-TET-TIG-CIP-NAL-AMI-STR-AMP-AMS1
CHL-SXT-CTX-CAZ-TET-TIG-CIP-NAL-STR-AMP-AMS1
安居CHL-CTX-TET-TIG-CIP-NAL-AMP2
CHL-SXT-CTX-CAZ-TET-TIG-CIP-NAL-STR-AMP1
CHL-SXT-CTX-TET-TIG-CIP-NAL-STR-AMP1
哈瓦那沙门菌李营CHL-SXT-STR-AMP-AMS2
德尔卑沙门菌李营CHL-SXT-TET-CIP-NAL-STR-AMP-AMS1
婴儿沙门菌李营CHL-SXT-CTX-TET-TIG-CIP-NAL-STR-AMP-AMS1
CHL-SXT-CTX-TET-TIG-NAL-STR-AMP-AMS2
安居CHL-SXT-CTX-TET-TIG-NAL-STR-AMP-AMS1
黄金海岸沙门菌李营CHL-SXT-CTX-CAZ-TET-TIG-CIP-NAL-STR-AMP-AMS2
伦敦沙门菌济东CHL-SXT-TET-TIG-CIP-STR-AMP-AMS1
吉韦沙门菌济东STR（I）1
肠炎沙门菌济东CT-NAL-STR-AMP-AMS1
), ArticleFig(id=1241678327690359545, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522927514997503, language=CN, label=表3, caption=

济宁市城区生活污水中不同血清型沙门菌的耐药谱

, figureFileSmall=null, figureFileBig=null, tableContent=
血清型污水厂耐药谱菌株数
阿贡纳沙门菌李营SXT-TET-TIG-CIP-STR-AMP-AMS2
SXT-TET-STR-AMP-AMS2
安居SXT-TET-TIG-STR-AMP-AMS2
SXT-TET-NAL-STR-AMP-AMS2
济东SXT-TET-STR-AMP-AMS5
SXT-TET-CIP-STR-AMP-AMS4
SXT-TET-TIG-STR-AMP-AMS2
SXT-TET-NAL-STR-AMP-AMS1
SXT-CTX-CAZ-TET-STR-AMP-AMS1
SXT-TET-CIP-NAL-STR-AMP-AMS1
CHL-SXT-CTX-TET-TIG-CIP-STR-AMP-AMS1
肯塔基沙门菌李营CHL-SXT-CTX-CAZ-TET-TIG-CIP-NAL-AMI-STR-AMP-AMS1
CHL-SXT-CTX-CAZ-TET-TIG-CIP-NAL-STR-AMP-AMS1
安居CHL-CTX-TET-TIG-CIP-NAL-AMP2
CHL-SXT-CTX-CAZ-TET-TIG-CIP-NAL-STR-AMP1
CHL-SXT-CTX-TET-TIG-CIP-NAL-STR-AMP1
哈瓦那沙门菌李营CHL-SXT-STR-AMP-AMS2
德尔卑沙门菌李营CHL-SXT-TET-CIP-NAL-STR-AMP-AMS1
婴儿沙门菌李营CHL-SXT-CTX-TET-TIG-CIP-NAL-STR-AMP-AMS1
CHL-SXT-CTX-TET-TIG-NAL-STR-AMP-AMS2
安居CHL-SXT-CTX-TET-TIG-NAL-STR-AMP-AMS1
黄金海岸沙门菌李营CHL-SXT-CTX-CAZ-TET-TIG-CIP-NAL-STR-AMP-AMS2
伦敦沙门菌济东CHL-SXT-TET-TIG-CIP-STR-AMP-AMS1
吉韦沙门菌济东STR（I）1
肠炎沙门菌济东CT-NAL-STR-AMP-AMS1
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济宁市城区生活污水中沙门菌分布、耐药特征及全基因组测序分析
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王胜男 1 , 祝园园 2 , 杜照中 1 , 聂天艳 1 , 尹强 1
现代预防医学 | 卫生监督 2024,51(5): 930-936
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现代预防医学 | 卫生监督 2024, 51(5): 930-936
济宁市城区生活污水中沙门菌分布、耐药特征及全基因组测序分析
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王胜男1, 祝园园2, 杜照中1, 聂天艳1, 尹强1
作者信息
  • 1.济宁市疾病预防控制中心微生物检验科，山东 济宁 272000
  • 2.任城区疾病预防控制中心微生物检验科

    • 王胜男（1989—），女，本科，主管技师，研究方向：从事病原微生物检验研究

通讯作者:

尹强，E-mail:
Distribution, drug resistance, and genome sequencing analysis of Salmonella in domestic sewage in Jining city
Sheng-nan WANG1, Yuan-yuan ZHU2, Zhao-zhong DU1, Tian-yan NIE1, Qiang YIN1
Affiliations
  • Department of Microbiology, Jining Center for Disease Control and Prevention, Jining, Shandong 272000, China
出版时间: 2024-03-10 doi: 10.20043/j.cnki.MPM.202310202
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摘要
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目的

了解济宁市城区生活污水中沙门菌分布、血清型、耐药特征，并进行全基因组测序分析，为沙门菌的防控提供科学依据。

方法

2023年2—3月，每周采集城区3个污水厂进水口污水各2份，每份500 ml，连续采集7周，合计42份污水样本，对污水样本进行沙门菌的培养、分离、鉴定，分离出的沙门菌进行血清凝集试验和荧光定量PCR血清分型，利用微量肉汤稀释法对41株沙门菌进行9类17种药物的最低抑菌浓度(minimum inhibitory concentration，MIC)检测，进行全基因组测序及系统进化分析。

结果

济宁市城区生活污水沙门菌分离率较高，42份样本中阳性样本24份，共分离出41株沙门菌，属9种血清型，以阿贡纳和肯塔基为主，李营和济东污水厂有其独有的血清型。只有1株吉韦沙门菌不耐药，其余40株沙门菌均为多重耐药菌，对复方新诺明、四环素、氨苄西林、链霉素耐药率达90%以上，对氨苄西林/舒巴坦耐药率达80%以上，共19种耐药谱，SXT-TET-STR-AMP-AMS占首位，不同血清型沙门菌的耐药谱不同，肯塔基沙门菌、黄金海岸沙门菌、婴儿沙门菌的多重耐药非常严重，同种血清型在不同污水厂中的耐药谱也不一致，李营污水厂的沙门菌耐药现象最严重。利用CARD数据库进行耐药基因预测，主要预测出8类耐药家族的18个耐药基因，耐药表型与耐药基因几乎全部一致。不同血清型沙门菌的ST分型不同，以ST13的阿贡纳沙门菌为主，进化树分为6个簇，不同污水厂的沙门菌在不同分支，提示基因组有差异，不同源。

结论

济宁市城区生活污水中沙门菌血清型多样，提示可能已在人群中存在并传播，耐药严重，携带耐药基因广泛，有些型别菌株持续存在且跨区域分布，有致病风险，需持续监测，并制定对科学的防控措施以控制沙门菌的流行及耐药的加重。

血清型  /  耐药谱  /  耐药基因  /  多位点序列分型  /  系统进化树
Objective

To understand the distribution, serotype, and drug resistance of Salmonella in domestic sewage in Jining city, and to analyze the whole genome sequencing so as to provide scientific basis for the prevention and control of Salmonella.

Methods

From February to March in 2023, two samples of sewage from the intake of 3 urban sewage plants with 500 ml each were collected continuously for 7 weeks. A total of 42 sewage samples were collected for culture, isolation, and identification of Salmonella. The isolated Salmonella was tested for serum agglutination test and fluorescent quantitative PCR serotyping. In total 41 strains of Salmonella were tested for minimum inhibitory concentration (MIC) of 17 drugs in 9 classes by microbroth dilution method, followed by genome sequencing and phylogenetic analysis.

Results

The isolation rate of Salmonella from domestic sewage in Jining city was high. Among 24 positive samples, 41 strains of Salmonella were isolated, belonging to 9 serotypes, mainly S. Agona and S. Kentucky. Liying and Jidong sewage treatment plants had their own unique serotypes. Only one strain of S. Give was not resistant, and the other 40 strains of Salmonella were multi-drug resistant. The resistance rates to sulfamethoxazole, tetracycline, ampicillin, and streptomycin were more than 90%, and the resistance rate to ampicillin/sulbactam was more than 80%. There were 19 kinds of drug resistance spectra, of which SXT-TET-STR-AMP-AMS ranked the first place. The resistance spectra of different serotypes of Salmonella were different. S. Kentucky, S. Gold Coast, and S. Infant were multi-drug resistant seriously. The resistance spectrum of the same serotype was also inconsistent in different sewage plants, and the resistance was the most serious in Liying sewage plant. The CARD database was used to predict drug resistance genes, mainly predicting 18 drug resistance genes in 8 types of drug resistance families, and the drug resistance phenotypes and drug resistance genes were almost all consistent. The ST types of different serotypes of Salmonella were different, and ST13 S. Agona was dominant. The phylogenetic tree was divided into 6 clusters, and strains in different sewage plants were in different branches, indicating that their genomes were different and had different sources.

Conclusion

There are various serotypes of salmonella in domestic sewage in Jining city, suggesting that they might have exist and spread in the population. Almost all strains are multi-drug resistant bacteria, carrying resistance genes extensively. Some types of strains live persistently and distribute across regions, leading to the potential risk to population. It is necessary to carry out continuous monitor, and scientific prevention and control measures need to be formulated to control the epidemic of salmonella and the aggravation of drug resistance.

Serotype  /  Drug resistance spectrum  /  Drug resistance gene  /  Multilocus sequence typing  /  Phylogenetic tree
王胜男, 祝园园, 杜照中, 聂天艳, 尹强. 济宁市城区生活污水中沙门菌分布、耐药特征及全基因组测序分析. 现代预防医学, 2024 , 51 (5) : 930 -936 . DOI: 10.20043/j.cnki.MPM.202310202
Sheng-nan WANG, Yuan-yuan ZHU, Zhao-zhong DU, Tian-yan NIE, Qiang YIN. Distribution, drug resistance, and genome sequencing analysis of Salmonella in domestic sewage in Jining city[J]. Modern Preventive Medicine, 2024 , 51 (5) : 930 -936 . DOI: 10.20043/j.cnki.MPM.202310202
正文
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沙门菌（Salmonella）是一种常见的食源性疾病致病菌，广泛存在于食用动物乳制品和肉中，通过粪–口途径引起细菌性食物中毒、伤寒、副伤寒等疾病。非伤寒沙门菌（NTS）经常在污水中发现，是发达国家和发展中国家引起腹泻的主要原因之一[1]。随着抗菌药物在临床治疗和畜牧业生产中的广泛应用，由于耐药基因的产生与转移，许多抗生素的作用效果逐渐减弱，沙门菌的耐药问题也日益[2-3]。全基因组测序(whole genome sequencing, WGS)作为一种快速且分辨率更高的方法,可通过测序数据预测血清型、分析耐药基因与毒力因子等,国外已有学者将其运用在沙门菌的监测与疫情调查中[4-5]。实时的监测是预防和控制疾病传播的关键，基于污水中细菌和病毒等病原微生物的监测和分析，在传染病的监测和预警方面发挥巨大的潜力[6]。污水厂通过污水管网承接了城市千家万户排放的污水，沙门菌可通过粪便样本或厨房用水经污水管网进入污水厂，相比于直接对粪便样本和食物样本的监测，污水厂进水口的污水覆盖的人数和食品数量更加广泛，包括已出现症状不能及时进行检测或者未出现症状而不进行检测的潜伏期感染者以及携带者、已被沙门菌污染的食物等，经济高效、省时，提早了预警时间；通过对污水中沙门菌的全基因组测序，能够追踪本地沙门菌基因组变异特征，发现隐匿传播，进一步对人群进行主动监测，有助于阐明传播链。本研究旨在通过对济宁市城区生活污水的监测，分析污水中沙门菌的分布、血清型和耐药特征，并利用全基因组测序技术发现沙门菌携带的主要耐药基因，揭示耐药机制，通过系统进化分析，深入揭示城区沙门菌的流行特征。在不接触人群、不从人体采集样本的条件下，一定程度地反映本区域沙门菌的流行规律和病原特征，同时逐步建立沙门菌的监测和预警数据库，为控制本地区沙门菌的流行及耐药的加重提供科学的决策依据。
1　材料与方法
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1.1　材料
1.1.1　样本采集
2023年2—3月，在济宁市城区李营污水厂（LY）、安居污水厂（AJ）、济东污水厂(JD)每周分别采集2份进水口污水，连续采集7周，共计42份样本。
1.1.2　仪器和试剂
Multifuge X3 FR高速冷冻离心机（ThermoFisher）；恒温培养箱(上海精宏)；MALDI Biotyper质谱仪（美国布鲁克）；比浊仪（法国梅里埃）；JYQ-I型全自动加样器、细菌鉴定/药敏分析仪（山东鑫科）；GENTIER 96实时荧光定量PCR仪（西安天隆）。改良亚硒酸盐煌绿增菌肉汤（SBG）、沙门菌显色培养基、木糖赖氨酸脱氧胆盐（XLD）琼脂、沙门菌鞭毛诱导软琼脂（广州环凯）；脑心浸液琼脂、MH琼脂（OXOID）；肠道菌药敏试剂盒（山东鑫科）；沙门菌血清型分子鉴定多重试剂盒（北京美正）；DNA纯化mini试剂盒（凯杰51306）；沙门菌属诊断血清（宁波天润）；沙门菌诊断血清（丹麦SSI）。
1.2　方法
1.2.1　菌株分离鉴定
取500 ml水样10 000 r/min离心5 min，取沉淀加入100 ml SBG增菌液中，过夜增菌，接种到沙门菌显色培养基、XLD培养基，37℃培养18～24 h，挑取可疑菌落进行质谱鉴定，一个平板挑取1～2个菌落，将质谱鉴定为沙门菌的菌落纯分至脑心浸液琼脂平板，进行后续试验。
1.2.2　血清凝集
按沙门菌血清凝集试剂操作说明进行试验，凝集不出的用沙门菌血清型分子鉴定的方法进行补充。提取细菌核酸，按照试剂盒说明设置PCR程序，进行结果判读。
1.2.3　药敏试验
药敏试验采用《国家致病菌识别网技术手册（2020版）》规定的肠道菌药敏操作方法，测试9类17种药物。结果解释按照识别网沙门菌的折点标准。因本研究中没有伤寒沙门菌，故不对阿奇霉素的结果进行判定。耐三种及三种以上不同类别抗生素定义为多重耐药株（multi-drug resistance，MDR）,质控菌株为大肠埃希菌ATCC25922。
1.2.4　全基因组测序
使用DNA纯化mini试剂盒（凯杰51306）提取菌株核酸，送至诺禾致源公司（北京）进行二代测序。测序公司进行DNA样品质控，质控合格的样本进行建库测序,利用Illumina nova 6000测序平台进行双端测序，过滤Raw Data，生成Clean Data。本实验室利用FastQC进行数据质控，后利用CLC Genomics Workbench 21.0（QIAGEN）拼接，得到fasta格式序列。以沙门菌NC_003197为参考序列进行进化分析，利用iTOL[7]修饰进化树。通过PubMLST数据库[8]获得MLST分型，利用CARD数据库[9]进行耐药基因的分析。
2　结果
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2.1　济宁市城区生活污水中沙门菌的检出情况
42份污水样本共分离出41株沙门菌，属9种血清型，阿贡纳沙门菌23株，肯塔基沙门菌6株，婴儿沙门菌4株，哈瓦那沙门菌2株，黄金海岸沙门菌2株，德尔卑沙门菌1株，吉韦沙门菌1株，伦敦沙门菌1株，肠炎沙门菌1株，整体上以阿贡纳和肯塔基为主。李营和济东污水厂样本阳性率较高，分离菌株数多。各污水厂沙门菌的血清型分布不一致，李营和济东污水厂有独有的血清型，李营污水厂沙门菌血清型有6种之多，独有血清型有3种。阿贡纳沙门菌在3个污水厂都有检出，且是济东污水厂的优势血清型。见表1。
2.2　药敏结果
41株沙门菌对复方新诺明、氨苄西林、四环素、链霉素高耐，耐药率达90%以上；对氨苄西林/舒巴坦耐药率达80%以上；对氯霉素、替加环素、萘啶酸、环丙沙星的耐药率在40%左右；对碳青霉烯类、β-内酰胺类的头孢他啶/阿维巴坦药物全部敏感。见表2。
2.3　耐药谱
41株沙门菌有40株为多重耐药菌，共19种耐药谱，以SXT-TET-STR-AMP-AMS，SXT-TET-TIG-STR-AMP-AMS，SXT-TET-CIP-STR-AMP-AMS为主。相同血清型沙门菌有一致的耐药谱，不同血清型沙门菌的耐药谱差异较大，阿贡纳沙门菌的耐药谱最为多样，肯塔基沙门菌、黄金海岸沙门菌、婴儿沙门菌多重耐药非常严重，吉韦沙门菌不耐药，同种血清型在不同污水厂的耐药谱也不一致。李营污水厂的沙门菌耐药较严重，其中的肯塔基沙门菌、黄金海岸沙门菌、婴儿沙门菌分别耐12种、11种、10种药物。济东污水厂的阿贡纳沙门菌耐药谱多样，SXT-TET-STR-AMP-AMS居首位。见表3、见图1。（菌株命名规则：污水厂+检测周次-菌落顺序，如JD1-1为济东污水厂第一周的污水样本中检测出的第一个菌落）。
2.4　耐药基因
利用CARD数据库进行菌株的耐药基因分析，将预测出的18个主要耐药基因构建热力图，涉及到8类耐药家族，为四环素类、β-内酰胺类、氨基糖苷类、磺胺类、喹诺酮类、氯霉素类、大环内酯类、甲氧苄啶类。氨基糖苷类耐药基因最多，为AAC (6')-Iy、AAC (6')-Iaa、AAC (3)-Id、APH (6)-Id、APH (3'')-Ib、APH (3')-Ia、aadA7、ANT (3'')-IIa。不同血清型的沙门菌所携带的耐药基因也不一致。婴儿沙门菌单独携带CTX-M-65介导对β-内酰胺类耐药。一株肯塔基沙门菌（LY4-1）单独携带rmtB介导对阿米卡星的耐药。德尔卑沙门菌（LY7-4）和一株阿贡纳沙门菌(JD3-1)对氯霉素耐药但不携带耐药基因floR。一株肠炎沙门菌（JD7-1）对多粘菌素耐药也不携带相关耐药基因。经综合分析，耐药基因预测与耐药表型几乎全部一致。见图2。
2.5　基因组分析
不同血清型沙门菌的ST分型不同，以ST13的阿贡纳沙门菌为主，其次为ST198的肯塔基沙门菌和ST32的婴儿沙门菌。如图3进化树所示，大体分为6个簇,同种血清型大都聚集成簇，同一簇中，不同污水厂的沙门菌在不同分支上，提示基因组有差异，不同源。在阿贡纳沙门菌簇中，LY7-2、LY7-3和JD污水厂的序列一致，提示该种型别的沙门菌在李营和济东共存，已发生区域扩散。济东污水厂中的阿贡纳沙门菌在第3W～6W都有检出且序列一致，李营污水厂中的婴儿沙门菌在第2W、4W检出且序列一致，提示该菌在该区域较长时间流行。安居污水厂中的4株阿贡纳沙门菌在不同分支，提示来源不同。见图3、4。
3　讨论
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济宁市城区生活污水中2023年2—3月共检测出41株9种不同血清型的沙门菌，分别为阿贡纳、肯塔基、婴儿、肠炎、黄金海岸、德尔卑、伦敦、哈瓦那、吉韦。这些血清型沙门菌都可感染人体而致病，也在生畜肉和生禽肉等食品中检出[10-11]。城区生活污水来自厨房与卫生间下水道，检测污水中的沙门菌可以反应出人体感染和食品携带的沙门菌的种类和分布，有研究表明，人源性和水源性沙门菌主要血清型一致[12]，所以对城区生活污水进行沙门菌的实时监测，是切实可行的。
本研究检测出的沙门菌耐药严重，对复方新诺明、四环素、氨苄西林、链霉素耐药率达90%以上，对氨苄西林/舒巴坦耐药率达80%以上，耐药谱SXT-TET-STR-AMP-AMS占首位，这与吴春敏等[10]、郑之北等[13]、郭凯等[14]、Martone-Rocha S等[15]的研究一致。德尔卑沙门菌和阿贡纳沙门菌是临床上除鼠伤寒和肠炎外最常见的沙门菌致病血清型，其在动物、食品和低龄儿童中的检出率高，致病力强[16]。本研究检测出的德尔卑和阿贡纳沙门菌，耐药表型与其一致。本研究中肯塔基沙门菌为ST198型的超耐沙门菌，耐药基因携带情况与曲梅等[17]研究一致，ST198肯塔基沙门菌是20世纪90年代中期在埃及首先被发现，是肯塔基沙门菌多耐药流行株的共同祖先。这意味着多重耐药肯塔基沙门菌在我市发生了一定传播，对公共卫生造成威胁。此外肯塔基沙门菌在禽肉中流行率的上升提示了该血清型沙门菌在食物链上存在传播的潜在风险[18]，需加强做好畜禽养殖、屠宰等源头阶段沙门菌的防控，以减少肯塔基沙门菌对本市的威胁。本研究检测出的ST358型黄金海岸耐药谱与杨杰的研究结果一致[19]，因其近几年在全国的流行趋势逐渐升高[20],此种血清型沙门菌对公共卫生具有一定的潜在风险，需引起关注。
相同血清型沙门菌有一致的耐药谱，不同血清型沙门菌的耐药谱差异较大。有研究表明，无论是核心耐药基因的SNP位点还是附属耐药基因的分布情况均与血清型具有较强的相关性[21]。不同的沙门菌血清型(或ST型)间获得性耐药基因的类型与分布具有显著差异，这与沙门菌泛基因组学研究的结果一致[22]。通过耐药基因预测，本研究中18个耐药基因涉及到8类耐药家族，氨基糖苷类耐药基因最多为AAC (6')-Iy、AAC (6')-Iaa、AAC (3)-Id、APH (6)-Id、APH (3'')-Ib、APH (3')-Ia、aadA7、ANT (3'')-IIa，这与肖颖等[23]研究结果一致，也检测出blaCTX-M、blaTEM、blaCMY、 fosA、qnrB、qnrS、sul2、tetA耐药基因。它们可能是导致近年来沙门菌对氨基糖苷类、β-内酰胺类、磷霉素类、喹诺酮类、磺胺类以及四环素类抗生素的耐药性呈逐渐增强趋势的重要因素，且由于氨基糖苷类耐药的AAC(3)、APH(4)基因，β-内酰胺类耐药的blaCMY、blaCTX-M和 blaTEM基因，及氟喹诺酮类耐药的 qnrB、qnrS 基因的占比逐年增长[21]。Qnr基因作为质粒介导的喹诺酮耐药性的主要原因，在喹诺酮耐药性的传播中起着重要作用，它能在不同细菌间进行水平传播[24]。所以本市的沙门菌耐药情况是比较严重的，非常有必要对本市沙门菌进行持续的耐药监测，以及时发现耐药表型及耐药基因的转变，且要加强抗生素的合理利用以遏制耐药加重的严峻态势。
通过全基因组测序分析，获得了沙门菌的ST型别，耐药基因预测，并构建系统发育树，首次从基因组水平揭示了本市三个污水厂沙门菌的流行信息。通过早期发现序列一致及高度相似的菌株聚集簇，发现新的变异型和多耐药菌株及其引起的扩散，基因组学监测正成为沙门菌病乃至其他食源性疾病监测的主要手段[25]。
本研究系首次对本市城区生活污水中的沙门菌进行监测，并首次采用WGS技术进行MLST分型、耐药基因预测及系统进化分析，揭示了本市沙门菌流行和耐药严峻的情况，丰富了本市沙门菌监测数据库，为科学防控沙门菌提供了依据。根据调查数据及时发布预警，进行科普宣传，提高公众的自我防控意识；根据系统进化分析，对聚集成簇的沙门菌展开主动调查，对同时期的人源沙门菌、食源沙门菌进行测序分析，以从基因组水平上进行溯源追踪，并结合流行病学调查，识别潜在的传染源，明确传播链，以控制沙门菌引起的暴发；根据耐药监测结果，下一步将进行本地人源沙门菌、食源沙门菌耐药特征与耐药基因的研究，揭示污水、人源、食源沙门菌之间的关联，控制本地沙门菌耐药的加重。将构建融合食源、人源、污水来源沙门菌的全面系统的监测预警网络，以及时监测、应对常见沙门菌感染暴发，及时发现新流行亚型、新耐药克隆株，并预防其扩散。
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2024年第51卷第5期
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doi: 10.20043/j.cnki.MPM.202310202
  • 接收时间：2023-10-11
  • 首发时间：2026-03-19
  • 出版时间：2024-03-10
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  • 收稿日期：2023-10-11
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    1.济宁市疾病预防控制中心微生物检验科，山东 济宁 272000
    2.任城区疾病预防控制中心微生物检验科

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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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