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Article(id=1228016571830956270, tenantId=1146029695717560320, journalId=1227665162245664772, issueId=1228016566646801206, articleNumber=null, orderNo=null, doi=10.20043/j.cnki.MPM.202504273, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=null, receivedDate=1744560000000, receivedDateStr=2025-04-14, revisedDate=null, revisedDateStr=null, acceptedDate=null, acceptedDateStr=null, onlineDate=1770711566169, onlineDateStr=2026-02-10, pubDate=1758729600000, pubDateStr=2025-09-25, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1770711566169, onlineIssueDateStr=2026-02-10, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1770711566169, creator=13701087609, updateTime=1770711566169, updator=13701087609, issue=Issue{id=1228016566646801206, tenantId=1146029695717560320, journalId=1227665162245664772, year='2025', volume='52', issue='18', pageStart='3265', pageEnd='3456', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1770711564932, creator=13701087609, updateTime=1770711815039, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1228017615784833769, tenantId=1146029695717560320, journalId=1227665162245664772, issueId=1228016566646801206, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1228017615784833770, tenantId=1146029695717560320, journalId=1227665162245664772, issueId=1228016566646801206, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=3410, endPage=3416, ext={EN=ArticleExt(id=1228016572166500608, articleId=1228016571830956270, tenantId=1146029695717560320, journalId=1227665162245664772, language=EN, title=Molecular evolution of H11N3 avian influenza virus from air sampled at live poultry wholesale market,Changsha, China, columnId=1228016572065837304, journalTitle=Modern Preventive Medicine, columnName=Experimental Technology and Applications, runingTitle=null, highlight=null, articleAbstract=
Objective

To conduct molecular surveillance and evolutionary analysis of avian influenza virus (AIV) in air samples collected from the live poultry wholesale market in Changsha, providing laboratory data for the prevention and control of human AIV infections.

Methods

Air samples were collected from poultry stalls in live poultry wholesale market in Changsha. AIV nucleic acid detection and nucleotide sequencing were performed. The sequencing results were analyzed using BLAST, key amino acid (aa) residue alignment, and nucleotide evolutionary analysis.

Results

All 27 air samples from the live poultry wholesale market tested positive for AIV nucleic acid (100% positivity rate). Two AIV nucleotide sequences (CS17 and CS11) were obtained. For CS17, the HA and NA genes exhibited the highest nucleotide similarities to A/duck/Bangladesh/38285/2019(H11N3)(98.47%) and A/mallard/South Korea/JB21-58/2019 (H5N3) (98.94%), respectively. For CS11, the HA and NA genes showed the highest nucleotide similarities to A/environment/Fujian/EV01/2020(H11N3)(95.34%) and A/duck/Wenzhou/771/2013 (H7N3) (95.30%), respectively. Internal gene analysis revealed that CS17 originated from H3N8, H4N6, H3N2, and H6N1 viruses, while CS11 was derived from H7N9, H3N2, and related viruses. Both CS17 and CS11 were identified as H11N3 subtype AIV (abbreviated as H11N3-CS17 and H11N3-CS11, respectively).The H11N3-CS17, H11N3-CS11, and 101 H11N3 strains (retrieved from GISAID) exhibited conserved molecular features in their HA proteins. All strains retained a single basic amino acid (aa) at the HA cleavage site and preserved Q/G residues at the receptor-binding sites. No critical mutations were observed at R293K (NA protein), S31N (M2 protein), E627K, or D701N (PB2 protein), nor deletions in the 69-73 (NA protein) or 218-230 (NS1 protein) regions. Notably, specific mutations were identified: L89V (PB2 protein), and N30D and T215A (M1 protein). Phylogenetic analysis indicated that the HA and NA genes of both strains belonged to the Eurasian lineage. H11N3-CS17 clustered into a subclade with H11N3 viruses from ducks in Bangladesh and Japan, while H11N3-CS11 formed a subclade with H11N3 viruses from domestic ducks and live poultry market environments in China.

Conclusion

Two H11N3 subtype AIV strains were identified in air samples from the live poultry wholesale market in Changsha. These strains exhibited molecular features of low pathogenicity and avian receptor specificity but displayed distinct genetic reassortment and evolutionary subclades, warranting further surveillance.

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目的

对长沙市活禽批发市场空气开展禽流感病毒（Avian influenza virus，AIV）分子监测和进化研究，为人感染AIV防控提供实验室数据。

方法

采集长沙市活禽批发市场禽类销售店铺空气样品，开展AIV核酸检测和核苷酸测序，测序结果BLAST分析、关键氨基酸（amino acid,aa）位点比对及核苷酸进化分析。

结果

27份活禽批发市场空气样品AIV核酸阳性率100%，获得2份空气样品的AIV核苷酸序列（CS17和CS11），CS17的 HA和NA基因核苷酸相似性最高的病毒分别为A/duck/Bangladesh/38285/2019(H11N3) (98.47%)和A/mallard/South Korea/JB21-58/2019(H5N3) (98.94%)，CS11的HA和 NA基因核苷酸相似性最高的病毒分别为A/environment/Fujian/EV01/2020(H11N3)（95.34%）和A/duck/Wenzhou/771/2013(H7N3) (95.30%)，CS17内部基因来源于H3N8、H4N6、H3N2及H6N1 病毒，CS11内部基因来源于H7N9、H3N2等病毒，CS17和CS11鉴定为H11N3亚型AIV（分别简称为H11N3-CS17和H11N3-CS11）。H11N3-CS17、H11N3-CS11 及GISAID 下载的101株H11N3 HA蛋白裂解位点均为1个碱性aa、受体结合位点为Q和G，未发生R293K（NA蛋白）、S31N（M2蛋白）、E627K及D701N（PB2）位点aa突变，未发生69～73位点（NA蛋白）及218～230位点（NS1蛋白）aa缺失，发生了L89V（PB2蛋白）、N30D和T215A（M1蛋白）aa位点突变。H11N3-CS17、H11N3-CS11 HA和NA基因属于欧亚大分支，H11N3-CS17主要与孟加拉国及日本鸭H11N3病毒聚集形成一个亚分支，H11N3-CS11主要与国内鸭及活禽市场环境H11N3病毒聚集形成一个亚分支。

结论

从长沙市活禽批发市场空气中鉴定出2株H11N3亚型AIV，表现为低致病性和禽类受体的分子特征，但具有不同的基因重配和进化亚分支，需要进一步监测。

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陈腊梅，E-mail：
, copyrightStatement=本刊刊出的所有文章不代表中华预防医学会和本刊编委会的观点，除非特别声明。, copyrightOwner=中华预防医学会和四川大学华西公共卫生学院, extLink=null, articleAbsUrl=null, sourceXml=rGAVcVm3t1kDMAbZVkG6JQ==, magXml=NZ5gxZoCDh7cxekM/nGq1g==, pdfUrl=null, pdf=oiSDRww5qjmhIKpB1Yf0VA==, pdfFileSize=1040302, pdfExtLink=null, richHtmlUrl=null, mobilePdfUrl=null, reviewReport=null, pdfFirstPage=null, abstractGraph=PbmYzGdAjL7q7gp2i0cl/A==, abstractGraphContent=null, abstractVideo=null, citation=null, cebUrl=null, magXmlContent=phGtyK8vFkZ9ajZO4rb2hw==, mapNumber=null, authorCompany=null, fund=null, authors=

张如胜（1977—），男，硕士，主任技师，研究方向：新发传染病的分子流行病学研究

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张如胜（1977—），男，硕士，主任技师，研究方向：新发传染病的分子流行病学研究

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张如胜（1977—），男，硕士，主任技师，研究方向：新发传染病的分子流行病学研究

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Journal of Virology, 2008, 82(3): 1146-1154., articleTitle=A single-amino-acid substitution in the NS1 protein changes the pathogenicity of H5N1 avian influenza viruses in mice, refAbstract=null)], funds=[Fund(id=1228016579976295260, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1228016571830956270, awardId=2023JJ60399, language=CN, fundingSource=湖南省自然科学基金(2023JJ60399), fundOrder=null, country=null), Fund(id=1228016580102124385, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1228016571830956270, awardId=R2023169, language=CN, fundingSource=湖南省卫生健康高层次人才重大科研专项(R2023169), fundOrder=null, country=null), Fund(id=1228016580232147819, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1228016571830956270, awardId=202203094936, language=CN, fundingSource=湖南省卫生健康委科研项目(202203094936), fundOrder=null, country=null), Fund(id=1228016580370559860, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1228016571830956270, awardId=kq2403183, language=CN, fundingSource=长沙市自然科学基金项目(kq2403183), fundOrder=null, country=null)], companyList=[AuthorCompany(id=1228016573164745033, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1228016571830956270, xref=1．, ext=[AuthorCompanyExt(id=1228016573168939338, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1228016571830956270, companyId=1228016573164745033, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=Changsha Center for Disease Control and Prevention, Changsha， Hunan 410007, China), AuthorCompanyExt(id=1228016573181522252, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1228016571830956270, companyId=1228016573164745033, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=1．长沙市疾病预防控制中心（长沙市卫生综合监督执法局），湖南　长沙　410007)]), AuthorCompany(id=1228016573319934294, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1228016571830956270, xref=2．, ext=[AuthorCompanyExt(id=1228016573328322903, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1228016571830956270, companyId=1228016573319934294, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=2．开福区疾病预防控制中心（开福区卫生综合监督执法局）)])], figs=[ArticleFig(id=1228016579061936903, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1228016571830956270, language=EN, label=Fig.1, caption=Phylogenetic analysis of the HA (A) and NA(B) genes of the influenza H11N3 viruses isolates CS17 and CS11 from air samples at live poultry wholesale market in Changsha, China, figureFileSmall=smzuO4ybfXY0Q3V6CdnNzQ==, figureFileBig=PbmYzGdAjL7q7gp2i0cl/A==, tableContent=null), ArticleFig(id=1228016579200348949, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1228016571830956270, language=CN, label=图1, caption=长沙市活禽批发市场环境H11N3亚型AIV HA(A) 及NA(B)基因进化分析

注：本研究的H11N3病毒标记为▲。

, figureFileSmall=smzuO4ybfXY0Q3V6CdnNzQ==, figureFileBig=PbmYzGdAjL7q7gp2i0cl/A==, tableContent=null), ArticleFig(id=1228016579435229998, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1228016571830956270, language=EN, label=Table 1, caption=

The BLAST analysis of genes of H11N3 subtype AIV isolates CS17 and CS11 from air samples

, figureFileSmall=null, figureFileBig=null, tableContent=
毒株基因GenBank登录号最高相似性病毒株相似性(%)
CS17PB2PV258289A/environment/Japan/KU-4h/2021(H3N8)2 267/2 280(99.43)
PB1PV258290A/duck/Vietnam/HN5959/2019(H4N6)2 154/2 180(98.81)
PAPV258291A/duck/China/402D27/2019(H3N2)2 117/2 151(98.42)
HAPV258292A/duck/Bangladesh/38285/2019(H11N3)1 672/1 698(98.47)
NPPV258293A/Anser albifrons/South Korea/22MC-64/2022(H6N1)1 488/1 497(99.40)
NAPV258294A/mallard/South Korea/JB21-58/2019(H5N3)1 395/1 410(98.94)
MPV258295A/duck/China/JX02M/2023(H4N6)979/982(99.69)
NSPV258296A/Spot-billed duck(Anas poecilohyncha)/Korea/KNU23/2022(H3N8)830/837(99.16)
CS11PB2PV258297A/duck/Zhejiang/S4488/2014(H7N9) 2 214/2 280(97.11)
HAPV258298A/environment/Fujian/EV01/2020(H11N3) 1 618/1 697(95.34)
NPPV258299A/chicken/Guangxi/165C7/2014(H3N2)1 505/1 564(96.23)
NAPV258300A/duck/Wenzhou/771/2013(H7N3) 1 338/1 404(95.30)
MPV258301A/duck/Zhejiang/4.29_HZBX008-O/2018(mixed) 1 004/1 027(97.76)
NSPV258302A/duck/Anhui/LY/2021(H3N2)882/890(99.10)
), ArticleFig(id=1228016579556864819, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1228016571830956270, language=CN, label=表1, caption=

空气样品CS17和CS11 H11N3亚型AIV各基因BLAST核苷酸相似性分析

, figureFileSmall=null, figureFileBig=null, tableContent=
毒株基因GenBank登录号最高相似性病毒株相似性(%)
CS17PB2PV258289A/environment/Japan/KU-4h/2021(H3N8)2 267/2 280(99.43)
PB1PV258290A/duck/Vietnam/HN5959/2019(H4N6)2 154/2 180(98.81)
PAPV258291A/duck/China/402D27/2019(H3N2)2 117/2 151(98.42)
HAPV258292A/duck/Bangladesh/38285/2019(H11N3)1 672/1 698(98.47)
NPPV258293A/Anser albifrons/South Korea/22MC-64/2022(H6N1)1 488/1 497(99.40)
NAPV258294A/mallard/South Korea/JB21-58/2019(H5N3)1 395/1 410(98.94)
MPV258295A/duck/China/JX02M/2023(H4N6)979/982(99.69)
NSPV258296A/Spot-billed duck(Anas poecilohyncha)/Korea/KNU23/2022(H3N8)830/837(99.16)
CS11PB2PV258297A/duck/Zhejiang/S4488/2014(H7N9) 2 214/2 280(97.11)
HAPV258298A/environment/Fujian/EV01/2020(H11N3) 1 618/1 697(95.34)
NPPV258299A/chicken/Guangxi/165C7/2014(H3N2)1 505/1 564(96.23)
NAPV258300A/duck/Wenzhou/771/2013(H7N3) 1 338/1 404(95.30)
MPV258301A/duck/Zhejiang/4.29_HZBX008-O/2018(mixed) 1 004/1 027(97.76)
NSPV258302A/duck/Anhui/LY/2021(H3N2)882/890(99.10)
), ArticleFig(id=1228016579682693954, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1228016571830956270, language=EN, label=Table 2, caption=

Analysis of the important amino acids in H11N3 subtype AIV isolates CS17 and CS11 from air Samples

, figureFileSmall=null, figureFileBig=null, tableContent=
病毒蛋白位点氨基酸位置H11N3-CS17H11N3-CS11H11N3-EV01H11N3-JS
HA裂解位点337～345PAI ASRGLFPAI ASR GLFPAI ASR GLFPAI ASR GLF
Q226L226/238aQQQQ
G228S228/240aGGGG
NAR294K294/293aRRRR
69～73缺失否否否否
PB2L89V89VVVV
E627K627EEEE
D701N701DDDD
PB1H99Y99H未检测HH
I368V368I未检测VI
PB1-F2全长90aa未检测90aa90aa
M1N30D30DDDD
T215A215AAAA
M2S31N31SSSS
NS1P42S42ASAS
218～230缺失否否否否
病毒蛋白H11N3-BangladeshH11N3-North CarolinaH9N2-11197H7N9-CS1H6N6-GZ090H5N6-CS1H5N1-HN1H3N8-1000
HAPAI ASR GLFPAI ATR GLFPSR SSR GLFPEI PKG RGLFPQI ETR GLFPLR ERR RKR GLFPLR ERR RKR GLFREK QTR GLF
QQLLQQQQ
GGGGGGGG
NARRRRRRRR
否否否否否否否否
PB2VVVVVVVV
EEEEEEEE
DDDDDDDD
PB1HHHHHHHH
IIVVIIII
PB1-F290aa90aa90aa52aa90aa非功能性蛋白90aa52aa
M1DDDDDD未知D
AAAAAA未知A
M2SSNNSNSN
NS1SASSSSSS
否否是是是否否是
), ArticleFig(id=1228016579800134475, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1228016571830956270, language=CN, label=表2, caption=

空气样品CS17和CS11 H11N3亚型AIV分离株基因编码蛋白关键位点分析

, figureFileSmall=null, figureFileBig=null, tableContent=
病毒蛋白位点氨基酸位置H11N3-CS17H11N3-CS11H11N3-EV01H11N3-JS
HA裂解位点337～345PAI ASRGLFPAI ASR GLFPAI ASR GLFPAI ASR GLF
Q226L226/238aQQQQ
G228S228/240aGGGG
NAR294K294/293aRRRR
69～73缺失否否否否
PB2L89V89VVVV
E627K627EEEE
D701N701DDDD
PB1H99Y99H未检测HH
I368V368I未检测VI
PB1-F2全长90aa未检测90aa90aa
M1N30D30DDDD
T215A215AAAA
M2S31N31SSSS
NS1P42S42ASAS
218～230缺失否否否否
病毒蛋白H11N3-BangladeshH11N3-North CarolinaH9N2-11197H7N9-CS1H6N6-GZ090H5N6-CS1H5N1-HN1H3N8-1000
HAPAI ASR GLFPAI ATR GLFPSR SSR GLFPEI PKG RGLFPQI ETR GLFPLR ERR RKR GLFPLR ERR RKR GLFREK QTR GLF
QQLLQQQQ
GGGGGGGG
NARRRRRRRR
否否否否否否否否
PB2VVVVVVVV
EEEEEEEE
DDDDDDDD
PB1HHHHHHHH
IIVVIIII
PB1-F290aa90aa90aa52aa90aa非功能性蛋白90aa52aa
M1DDDDDD未知D
AAAAAA未知A
M2SSNNSNSN
NS1SASSSSSS
否否是是是否否是
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长沙市活禽批发市场空气中H11N3亚型禽流感病毒分子进化研究
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张如胜 1 , 扶会媛 1 , 裴瑞青 1 , 黄政 1 , 罗璨 1 , 陈静芳 1 , 陈姗 1 , 陈腊梅 2
现代预防医学 | 实验技术及其应用 2025,52(18): 3410-3416
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现代预防医学 | 实验技术及其应用 2025, 52(18): 3410-3416
长沙市活禽批发市场空气中H11N3亚型禽流感病毒分子进化研究
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张如胜1, 扶会媛1, 裴瑞青1, 黄政1, 罗璨1, 陈静芳1, 陈姗1, 陈腊梅2
作者信息
  • 1．长沙市疾病预防控制中心（长沙市卫生综合监督执法局），湖南　长沙　410007
  • 2．开福区疾病预防控制中心（开福区卫生综合监督执法局）

    • 张如胜（1977—），男，硕士，主任技师，研究方向：新发传染病的分子流行病学研究

通讯作者:

陈腊梅，E-mail：
Molecular evolution of H11N3 avian influenza virus from air sampled at live poultry wholesale market,Changsha, China
Ru-sheng ZHANG1, Hui-yuan FU1, Rui-qing PEI1, Zheng HUANG1, Can LUO1, Jing-fang CHEN1, Shan CHEN1, La-mei CHEN2
Affiliations
  • Changsha Center for Disease Control and Prevention, Changsha， Hunan 410007, China
出版时间: 2025-09-25 doi: 10.20043/j.cnki.MPM.202504273
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摘要
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目的

对长沙市活禽批发市场空气开展禽流感病毒（Avian influenza virus，AIV）分子监测和进化研究，为人感染AIV防控提供实验室数据。

方法

采集长沙市活禽批发市场禽类销售店铺空气样品，开展AIV核酸检测和核苷酸测序，测序结果BLAST分析、关键氨基酸（amino acid,aa）位点比对及核苷酸进化分析。

结果

27份活禽批发市场空气样品AIV核酸阳性率100%，获得2份空气样品的AIV核苷酸序列（CS17和CS11），CS17的 HA和NA基因核苷酸相似性最高的病毒分别为A/duck/Bangladesh/38285/2019(H11N3) (98.47%)和A/mallard/South Korea/JB21-58/2019(H5N3) (98.94%)，CS11的HA和 NA基因核苷酸相似性最高的病毒分别为A/environment/Fujian/EV01/2020(H11N3)（95.34%）和A/duck/Wenzhou/771/2013(H7N3) (95.30%)，CS17内部基因来源于H3N8、H4N6、H3N2及H6N1 病毒，CS11内部基因来源于H7N9、H3N2等病毒，CS17和CS11鉴定为H11N3亚型AIV（分别简称为H11N3-CS17和H11N3-CS11）。H11N3-CS17、H11N3-CS11 及GISAID 下载的101株H11N3 HA蛋白裂解位点均为1个碱性aa、受体结合位点为Q和G，未发生R293K（NA蛋白）、S31N（M2蛋白）、E627K及D701N（PB2）位点aa突变，未发生69～73位点（NA蛋白）及218～230位点（NS1蛋白）aa缺失，发生了L89V（PB2蛋白）、N30D和T215A（M1蛋白）aa位点突变。H11N3-CS17、H11N3-CS11 HA和NA基因属于欧亚大分支，H11N3-CS17主要与孟加拉国及日本鸭H11N3病毒聚集形成一个亚分支，H11N3-CS11主要与国内鸭及活禽市场环境H11N3病毒聚集形成一个亚分支。

结论

从长沙市活禽批发市场空气中鉴定出2株H11N3亚型AIV，表现为低致病性和禽类受体的分子特征，但具有不同的基因重配和进化亚分支，需要进一步监测。

活禽市场  /  空气  /  禽流感病毒  /  H11N3亚型  /  基因  /  进化分析
Objective

To conduct molecular surveillance and evolutionary analysis of avian influenza virus (AIV) in air samples collected from the live poultry wholesale market in Changsha, providing laboratory data for the prevention and control of human AIV infections.

Methods

Air samples were collected from poultry stalls in live poultry wholesale market in Changsha. AIV nucleic acid detection and nucleotide sequencing were performed. The sequencing results were analyzed using BLAST, key amino acid (aa) residue alignment, and nucleotide evolutionary analysis.

Results

All 27 air samples from the live poultry wholesale market tested positive for AIV nucleic acid (100% positivity rate). Two AIV nucleotide sequences (CS17 and CS11) were obtained. For CS17, the HA and NA genes exhibited the highest nucleotide similarities to A/duck/Bangladesh/38285/2019(H11N3)(98.47%) and A/mallard/South Korea/JB21-58/2019 (H5N3) (98.94%), respectively. For CS11, the HA and NA genes showed the highest nucleotide similarities to A/environment/Fujian/EV01/2020(H11N3)(95.34%) and A/duck/Wenzhou/771/2013 (H7N3) (95.30%), respectively. Internal gene analysis revealed that CS17 originated from H3N8, H4N6, H3N2, and H6N1 viruses, while CS11 was derived from H7N9, H3N2, and related viruses. Both CS17 and CS11 were identified as H11N3 subtype AIV (abbreviated as H11N3-CS17 and H11N3-CS11, respectively).The H11N3-CS17, H11N3-CS11, and 101 H11N3 strains (retrieved from GISAID) exhibited conserved molecular features in their HA proteins. All strains retained a single basic amino acid (aa) at the HA cleavage site and preserved Q/G residues at the receptor-binding sites. No critical mutations were observed at R293K (NA protein), S31N (M2 protein), E627K, or D701N (PB2 protein), nor deletions in the 69-73 (NA protein) or 218-230 (NS1 protein) regions. Notably, specific mutations were identified: L89V (PB2 protein), and N30D and T215A (M1 protein). Phylogenetic analysis indicated that the HA and NA genes of both strains belonged to the Eurasian lineage. H11N3-CS17 clustered into a subclade with H11N3 viruses from ducks in Bangladesh and Japan, while H11N3-CS11 formed a subclade with H11N3 viruses from domestic ducks and live poultry market environments in China.

Conclusion

Two H11N3 subtype AIV strains were identified in air samples from the live poultry wholesale market in Changsha. These strains exhibited molecular features of low pathogenicity and avian receptor specificity but displayed distinct genetic reassortment and evolutionary subclades, warranting further surveillance.

Live poultry market  /  Air sample  /  Avian influenza virus  /  H11N3 subtype  /  Gene  /  Evolutionary analysis
张如胜, 扶会媛, 裴瑞青, 黄政, 罗璨, 陈静芳, 陈姗, 陈腊梅. 长沙市活禽批发市场空气中H11N3亚型禽流感病毒分子进化研究. 现代预防医学, 2025 , 52 (18) : 3410 -3416 . DOI: 10.20043/j.cnki.MPM.202504273
Ru-sheng ZHANG, Hui-yuan FU, Rui-qing PEI, Zheng HUANG, Can LUO, Jing-fang CHEN, Shan CHEN, La-mei CHEN. Molecular evolution of H11N3 avian influenza virus from air sampled at live poultry wholesale market,Changsha, China[J]. Modern Preventive Medicine, 2025 , 52 (18) : 3410 -3416 . DOI: 10.20043/j.cnki.MPM.202504273
正文
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禽流感病毒（Avian influenza virus，AIV）来源于禽，根据血凝素（Hemagglutinin, HA）和神经氨酸酶（Neuraminidase, NA）抗原性的差异，可分为18个HA亚型（H1～H18）和11个NA亚型（N1～N11），全球已有多种亚型AIV跨物种感染人类，其中长沙市已发现了人感染H7N9、H5N6、H9N2及H3N8等亚型AIV病例[1-4]，且已发生病例均与活禽市场有流行病学关联[4-7]。既往研究显示AIV可以通过气溶胶传播，譬如人感染AIV的部分病例并未直接接触活禽或者可能被活禽排泄物污染的物品，后续研究在部分病例关联的活禽市场空气中检出AIV污染，提示活禽市场中AIV气溶胶传播是造成人类感染AIV的感染途径之一[8-9]。既往长沙市辖区活禽市场环境AIV监测主要采集家禽口咽/泄殖腔拭子，家禽粪便、家禽笼具涂抹、砧板涂抹、污水、家禽饮用水等环境样品[10-11]，近年来已采集空气样品进行AIV等病原微生物监测研究[12-14]，但辖区活禽市场空气中AIV的分子进化特征尚未有研究报道。
AIV由8个独立的RNA片段(PB2、PB1、PA、HA、NP、NA、M、NS)组成，片段之间容易发生重组、变异，AIV的致病特征、受体特征、耐药性等与病毒基因编码氨基酸（amino acid,aa）位点密切相关[15-17]，且已有研究表明AIV各基因片段发生了适应性变异，导致病毒跨物种传播能力以及对哺乳动物的致病性增强[18]，开展AIV的分子进化分析可以预警病毒传播至普通人群的风险。活禽批发市场作为中小型农贸市场供货源头的禽类场所，禽种类繁多、来源广泛且交易量大，市场空气中AIV污染状况及分子进化特征值得关注。本研究选择湖南省长沙市1家大型活禽批发市场开展空气中AIV监测及分子进化分析，为人感染AIV疫情防控提供实验室数据。
1　材料与方法
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1.1　样品采集
选择长沙市辖区一家活禽批发市场作为监测点，该市场主要面向辖区农贸市场提供鸡、鸭、鸽、鹅等各类活禽，每日销售量在万只以上。本研究于2022年不定期（4、5、6、8、9、11月）对家禽批发销售店铺进行空气样品采集，按照店铺位置顺序每次采集4~5家店铺，每个店铺每次采集1份空气样品，共采集空气样品27份，空气样品采集位置为店铺活禽圈养区，圈养区面积约4～6 m2，每个店铺每次采集1份样品，采样位置距离地面1.0 m左右，利用气溶胶采样器（法国Bertin CORIOLIS®μ）在每个采样点以200 L/min的速度采集10 min，将总共 2.0 m3 空气直接收集到含有3 ml病毒保存液（北京友康生物科技有限公司）的锥形小瓶中，盖紧盖子并做好标记，4℃冷藏送长沙市疾病预防控制中心实验室保存备用[8,13-14]。
1.2　AIV核酸检测
利用Thermo KingFisher Flex磁珠法核酸提取仪和Fisher ScientificTM LabServTM预分装磁珠法病毒总核酸提取试剂盒（美国Thermo Fisher Scientific公司）对收集的空气样品保存液进行常规核酸提取。利用AIV实时荧光PCR核酸检测试剂盒（深圳梓健生物科技有限公司）及ABI 7500型Real-time PCR仪（美国Thermo Fisher Scientific公司）对提取的样品核酸进行AIV检测，扩增条件及结果判定参照试剂盒说明书。
1.3　AIV高通量核苷酸序列测定
采用《全国流感监测技术指南》（2017年版）AIV通用引物（Uni-12/Inf1 ：5’-GGGGGGAGCAAAAGCAGG-3’， Uni-12/Inf3： 5’-GGGGGGAGCGAAAGCAGG-3’，Uni-13/Inf1 ：5’-CGGGTTATTAGTAGAAACAAGG-3’）、illumina miseq测序仪及配套试剂盒（美国illumina公司）对实时荧光PCR 循环阈值（Cycle Threshold value，CT）小于30的AIV空气样品保存液阳性核酸进行高通量核苷酸测序，测序下机数据使用FastQC软件对测序质量进行可视化，采用cutadapt工具切除接头序列并过滤低质量序列reads，最后利用SPAdes-3.13.0软件拼接后提交至国际基因序列数据库（Genetic Sequence Database，Genbank），在线基本局部相似性搜索工具（Basic local alignment search tool, BLAST）进行核苷酸相似性分析（http：//BLAST.ncbi.nlm.nih.gov/BLAST.cgi）。
1.4　AIV基因组aa关键位点分析
从全球流感数据共享倡议（Global Initiative on Sharing All Influenza Data，GISAID）和美国国家生物技术信息中心（National Center for Biotechnology Information, NCBI）分别下载全部H11N3及H9N2、H7N9、H6N6、H5N1、H5N6、H3N8亚型AIV 代表株基因编码aa序列，利用BioEdit软件将下载的AIV和本研究中空气来源的H11N3亚型AIV基因编码关键aa位点进行多重比对和分子特征分析。
1.5　AIV HA、NA基因分子进化分析
从GISAID下载全部H11N3亚型AIV HA和NA基因核苷酸序列，首先利用MEGA X软件进行DNA序列ALIGN Clustal W比对，对首尾长度不一致的核苷酸序列进行删除，然后利用MODELS程序Find Best DNA/Protein Models（ML）进行进化分析模型预测，根据预测结果选择最优模型和方法构建H11N3亚型AIV HA和NA基因进化树。
2　结果
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2.1　AIV监测情况
利用AIV实时荧光PCR核酸检测试剂盒对2022年长沙市1家活禽批发市场来源的空气样品进行检测，结果显示，27份空气样品AIV核酸阳性率为100%（27/27）。
2.2　AIV高通量核苷酸测序结果
选择9份实时荧光PCR CT值小于30的AIV核酸阳性空气样品进行高通量核苷酸测序和BLAST比对，鉴定结果显示2株空气来源的AIV为H11N3亚型，其中编号为CS17的H11N3亚型AIV（A/environment/Hunan/CS17/2022，H11N3-CS17) HA基因与孟加拉国鸭H11N3 亚型AIV(A/duck/Bangladesh/38285/2019)核苷酸相似性最高（98.47%），NA基因与韩国野生绿头鸭H5N3亚型AIV（A/mallard/South Korea/JB21-58/2019）核苷酸相似性最高（98.94%），内部基因PB2、PB1、PA、NP、M及NS分别与日本环境H3N8、越南鸭H4N6、国内鸭H3N2、韩国白额雁H6N1、国内鸭H4N6及朝鲜斑嘴鸭H3N8亚型AIV核苷酸相似性最高。编号为CS11 的H11N3亚型AIV（A/environment/Hunan/CS11/2022, H11N3-CS11) HA基因与国内福建活禽市场环境H11N3亚型AIV(A/environment/Fujian/EV01/2020)核苷酸相似性最高 (95.34%)，NA基因与国内温州鸭H7N3亚型AIV（A/duck/Wenzhou/771/2013) 核苷酸相似性最高 (95.30%)，内部基因PB2、NP、M及NS分别与国内浙江鸭H7N9、广西鸡H3N2、浙江鸭混合亚型及安徽鸭H3N2亚型AIV核苷酸相似性最高，本研究中的H11N3-CS17和H11N3-CS11病毒核苷酸序列GenBank登录号为：PV258289—PV258302。具体比对结果见表1。
2.3　AIV全基因组aa关键位点分析
H11N3-CS17和 H11N3-CS11 HA蛋白裂解位点第337～345位aa为PAIASRGLF，GISAID下载的全部101株H11N3亚型AIV（以下简称101株H11N3病毒）HA蛋白裂解位点均为1个碱性aa序列（51株病毒为PAIATRGLF，46株病毒为PAIASRGLF，4株病毒为PAIAARGLFG）。H11N3-CS17、H11N3-CS11及101株H11N3病毒HA蛋白受体结合位点（Receptor binding site，RBS）第238和240位（对应H3流感病毒第226和228位）aa均为Q和G，与H9N2和H7N9亚型AIV代表株表现为L和G不同。H11N3-CS17、H11N3-CS11及101株H11N3病毒NA蛋白第293位aa为R，M2蛋白第31位aa为S，与H9N2、H7N9、H5N6及H3N8亚型AIV代表株M2蛋白出现S31N位点突变不同；NA蛋白69～73位点及NS1蛋白第218～230aa未发生缺失，与H9N2、H7N9、H6N6及H3N8亚型AIV代表株NS1蛋白第218～230aa缺失不同；PB2蛋白发生了L89V突变，但未发生E627K和D701N突变。
H11N3-CS17、101株H11N3病毒PB1蛋白均未发生H99Y突变，H11N3-CS17及GISAID下载的95株H11N3病毒PB1蛋白第368位aa为I，GISAID下载的其他6株H11N3病毒发生I368V突变；H11N3-CS17及101株H11N3病毒PB1-F2蛋白绝大多数为90aa，仅有4株北美H11N3病毒为87aa，另外H9N2、H6N6及H5N1亚型AIV代表株为90aa，H7N9和H3N8亚型AIV代表株为52aa，H5N6亚型AIV代表株为非功能性 PB1-F2 蛋白。H11N3-CS17、H11N3-CS11、101株H11N3病毒及其他亚型代表株（不包括H5N1亚型AIV代表株）M1蛋白发生了N30D和 T215A突变。H11N3-CS11、A/duck/Jiangsu/10-d4/2011(H11N3)（H11N3-JS）、A/duck/Bangladesh/38285/2019(H11N3)（H11N3-Bangladesh）及GISAID 下载的74株H11N3病毒NS1蛋白发生 P42S 突变，H11N3-CS17、A/environment/Fujian/EV01/2020(H11N3)（H11N3-EV01）、A/blue-winged teal/North Carolina/NC674-362/2005(H11N3)（H11N3- North Carolina）及GISAID 下载的27株H11N3病毒发生P42A突变。具体比对结果见表2。
2.4　AIV HA、NA基因进化树构建
根据模型预测结果，HA和NA基因进化树模型分别选择广义时间可逆模型(General Time Reversible Model，GTR）和Tamura三参数模型(Tamura 3-parameter Model，T92），方法选择最大似然法（Maximum Likelihood Tree），步展值（bootstrap）设为1 000次。H11N3 病毒 HA和NA基因进化树均形成欧亚和北美两大分支，本研究中的H11N3-CS17、H11N3-CS11属于欧亚大分支，在欧亚大分支中，H11N3病毒 HA和NA基因已进化形成若干亚分支。
HA基因进化树显示H11N3-CS17与孟加拉国鸭H11N3病毒（A/duck/Bangladesh/38285/2019）亲缘关系近，主要与孟加拉国和日本鸭H11N3病毒聚集形成一个亚分支，H11N3-CS11与国内福州鸭H11N3病毒（A/duck/Fuzhou/D6/2020）亲缘关系近，主要与国内福建、浙江和江苏鸭及活禽市场环境H11N3病毒聚集形成一个亚分支。HA基因欧亚大分支的另外几个亚分支分别由国内山东天鹅、瑞典和荷兰绿头鸭、澳大利亚野生水禽以及越南鸭H11N3病毒组成。北美大分支主要由美国马里兰州小种鸭及北美其他地区野生禽H11N3病毒组成。见图1（A）。
NA基因进化树显示, H11N3-CS17与国内山东天鹅H11N3病毒（A/Swan/Shandong/W4154/2021）亲缘关系近，主要与日本及孟加拉国鸭H11N3病毒聚集形成一个亚分支，H11N3-CS11与国内福建活禽市场环境H11N3病毒（A/environment/Fujian/EV01/2020）亲缘关系近，主要与国内福建、浙江及江苏鸭等H11N3病毒聚集形成一个亚分支。其他亚分支由荷兰、瑞典、越南、日本、新西兰、澳大利亚鸭及野生禽H11N3病毒组成。北美大分支主要由美国等北美地区的野生禽H11N3病毒组成。见图1（B）。
3　讨论
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禽类感染AIV后通过呼吸道和消化道将病毒排放到圈养环境中，同时通过禽类扇动翅膀等方式将环境中的AIV形成气溶胶，并持续污染圈养环境，造成禽类和跨物种传播风险[8]。本研究于2022年不定期采集1家活禽批发市场空气样品27份，基本覆盖该市场大型家禽批发销售店铺，在每个店铺的活禽圈养区采集1份空气样品进行AIV监测，结果显示2022年长沙市活禽批发市场空气中AIV阳性率为100%（27/27），高于或等于国内外活禽市场空气中AIV污染阳性率，譬如广东省广州市（12/14，85.71%）、江西省南昌市（275/807，34.10%）、越南河内（27/30，90.00%）、香港（6/13，46.15%）及柬埔寨（100%）[8,19-21]，表明2022年长沙市活禽批发市场空气中AIV污染较重，原因与本研究选择的活禽批发市场禽类数量及种类多，禽类感染AIV后导致空气污染有关，另外与新冠疫情期间市场空气环境消毒措施相对不规范等原因有关，提示长沙市活禽批发市场需要加强通风消毒和个人防护，降低AIV经气溶胶传播至市场中禽类和市民的风险。
H11亚型AIV是一种低致病性AIV，包括9种不同NA亚型。自1956年首次从英格兰的家鸭中分离出H11病毒以来，已有多个国家报道分离出该亚型的病毒，Kuratko等[22]和Pawar等[23]分别从印度的白鹭和日本的绿头鸭中分离出H11N1病毒。Zhang等人从中国东部活禽市场采集的鸡样品中分离出H11N2病毒[24]。H11病毒通常与其他亚型AIV共同感染，在感染的鸭中没有发现显著的临床症状，但已有研究表明能感染哺乳动物（猪），甚至人类[25-26]。
目前，已有从禽类及相关环境分离出H11N3病毒的研究报告。2009年4月，越南从家鸭中分离出3株H11N3病毒[27]。2011年，中国江苏首次从鸭中分离出H11N3病毒[28]。2020年，国内福建报道了来源于活禽市场鸭的H11N3病毒[29-30]。考虑到实时荧光PCR检测CT值为>30的样品难以测序成功[14]，本研究从27份空气样品中选择9份CT值<30的AIV阳性空气样品核酸进行测序，成功获得2份H11N3病毒（H11N3-CS17和H11N3-CS11）核苷酸序列，另外7份空气样品仅有3份获得部分H9N2亚型AIV序列。本研究中的H11N3-CS17和H11N3-CS11由不同来源的亚型AIV重配而成，其中H11N3-CS17主要由南亚、东亚和国内鸭、野生绿头鸭及白额雁来源的H11N3、H5N3、H3N8、H4N6、H3N2、H6N1病毒重配而成，H11N3-CS11主要由国内禽来源的H11N3、H7N3、H7N9、H3N2等病毒重配而成，与H11N3-CS17的重配基因片段来源不同。国内研究显示福建活禽市场环境H11N3病毒（A/environment/Fujian/EV01/2020）携带有鸭H7N2和H4N6等病毒基因，提示H11N3病毒可能在不同地区经历不同类型的重组，可能与鸟类的迁徙或通过家禽供应链传播病毒有关[29]。
AIV的基因特征与病毒致病性相关，可以根据HA蛋白裂解位点碱性aa的数量多少来判断病毒的致病性强弱，且HA蛋白的RBS区域aa如为QSG则表现为特异性结合α-2,3禽类受体，LSS则表现为对α-2,6人类受体亲和[31]。本研究显示H11N3-CS17、H11N3-CS11及101株H11N3病毒均表现为低致病性分子特征和α-2,3禽类受体特征，与H9N2和H7N9病毒代表株的人类受体不同，提示当前的H11N3病毒仅具有禽类受体结合能力，跨物种感染的风险较低[29]，且参与比对的全部H11N3病毒对神经氨酸酶抑制剂和金刚烷胺类药物敏感，与H9N2、H7N9、H5N6及H3N8病毒代表株表现为金刚烷胺类药物耐药不同。H11N3-CS17、H11N3-CS11及101株H11N3病毒发生了L89V（PB2蛋白）、N30D和 T215A（M1蛋白）突变，但未发生E627K和D701N突变，NA蛋白69～73位点及NS1蛋白第218～230aa未发生缺失，提示病毒毒力暂未增强[32]。
研究显示国内福建活禽市场环境H11N3病毒(A/environment/Fujian/EV01/2020)的所有基因片段都属于欧亚大分支[29]。进化分析显示H11N3病毒欧亚大分支已进化形成若干亚分支，本研究中2022年分离的H11N3-CS17、H11N3-CS11属于不同的亚分支，其中H11N3-CS17的HA和NA基因主要与分离自孟加拉国和日本的鸭H11N3病毒聚集形成一个亚分支，H11N3-CS11的HA和NA基因主要与分离自国内鸭及活禽市场环境的H11N3病毒聚集形成一个亚分支，提示H11N3病毒通过重配正在不断进化，需要进一步加强H11N3病毒的分子监测[29]。
本研究的局限性在于活禽批发市场空气AIV监测时间在COVID-19 爆发的防控阶段，采样时间不规律，且获得的H11N3病毒阳性空气样品未能成功分离培养，未进一步开展相关研究。
本研究显示H11N3病毒虽表现为低致病性和禽类受体结合的分子特征，且目前尚未有人类感染病例的报道，但全球范围内的H11N3病毒仍在持续进化与重配，形成了不同的亚分支。已有研究证实，该病毒具备感染哺乳动物及通过气溶胶传播的潜力[29]。因此，在活禽市场等环境中污染的H11N3病毒仍存在跨物种传播至人类的可能性。建议相关部门加强活禽市场中罕见亚型低致病性AIV的监测，尽早推进疫苗研发，以降低活禽市场的AIV生物安全风险，从而有效防控跨物种传播及潜在的流感大流行。
基金
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  • 湖南省自然科学基金(2023JJ60399)
  • 湖南省卫生健康高层次人才重大科研专项(R2023169)
  • 湖南省卫生健康委科研项目(202203094936)
  • 长沙市自然科学基金项目(kq2403183)
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参考文献 引证文献
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2025年第52卷第18期
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doi: 10.20043/j.cnki.MPM.202504273
  • 接收时间：2025-04-14
  • 首发时间：2026-02-10
  • 出版时间：2025-09-25
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  • 收稿日期：2025-04-14
基金
湖南省自然科学基金(2023JJ60399)
湖南省卫生健康高层次人才重大科研专项(R2023169)
湖南省卫生健康委科研项目(202203094936)
长沙市自然科学基金项目(kq2403183)
作者信息
    1．长沙市疾病预防控制中心（长沙市卫生综合监督执法局），湖南　长沙　410007
    2．开福区疾病预防控制中心（开福区卫生综合监督执法局）

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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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