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Circulation, Evolution and Transmission of H5N8 virus, 2016–2018

  • Author Footnotes
    1 These authors contributed equally to this work.
    Jianjun Chen
    Correspondence
    Corresponding authors at: Wuhan Institute of Virology, Chinese Academy of Sciences, 44 Xiaohongshan, Wuhan, Hubei 430071, P.R. China.
    Footnotes
    1 These authors contributed equally to this work.
    Affiliations
    CAS Key Laboratory of Special Pathogens and Biosafety, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071, China

    National Virus Resource Center, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071, China

    Center for Influenza Research and Early warning (CASCIRE), Chinese Academy of Sciences, Beijing 100101, China
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  • Author Footnotes
    1 These authors contributed equally to this work.
    Bilin Liang
    Footnotes
    1 These authors contributed equally to this work.
    Affiliations
    CAS Key Laboratory of Special Pathogens and Biosafety, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071, China

    National Virus Resource Center, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071, China

    University of Chinese Academy Sciences, Beijing 101409, China
    Search for articles by this author
  • Juefu Hu
    Affiliations
    CAS Key Laboratory of Special Pathogens and Biosafety, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071, China

    National Virus Resource Center, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071, China
    Search for articles by this author
  • Haizhou Liu
    Affiliations
    CAS Key Laboratory of Special Pathogens and Biosafety, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071, China

    National Virus Resource Center, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071, China
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  • Jianqing Sun
    Affiliations
    Qinghai Lake National Nature Reserve, Xining 810099, China
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  • Mingxin Li
    Affiliations
    CAS Key Laboratory of Special Pathogens and Biosafety, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071, China
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  • Quanjiao Chen
    Affiliations
    CAS Key Laboratory of Special Pathogens and Biosafety, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071, China

    Center for Influenza Research and Early warning (CASCIRE), Chinese Academy of Sciences, Beijing 100101, China
    Search for articles by this author
  • Yubang He
    Affiliations
    Qinghai Lake National Nature Reserve, Xining 810099, China
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  • Di Liu
    Correspondence
    Corresponding authors at: Wuhan Institute of Virology, Chinese Academy of Sciences, 44 Xiaohongshan, Wuhan, Hubei 430071, P.R. China.
    Affiliations
    CAS Key Laboratory of Special Pathogens and Biosafety, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071, China

    National Virus Resource Center, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071, China

    Center for Influenza Research and Early warning (CASCIRE), Chinese Academy of Sciences, Beijing 100101, China

    University of Chinese Academy Sciences, Beijing 101409, China
    Search for articles by this author
  • Author Footnotes
    1 These authors contributed equally to this work.

      Highlights

      • The H5N8 was introduced into Qinghai Lake, with distinct genotype in 2016 and 2017.
      • LPAIVs in wild birds contributed to the high diversity of global H5N8 viruses.
      • The major reassortment events may occur during 2016–2017.
      • Continued circulation among wild birds resulted in the global distribution.

      Summary

      Objectives

      A second wave of highly pathogenic avian influenza A virus (HPAIV) H5N8 clade 2.3.4.4 has spread globally, causing outbreaks among wild birds and domestic poultry since autumn 2016. The circulation and evolutionary dynamics of the virus remain largely unknown.

      Methods

      We performed surveillance for H5N8 in Qinghai Lake in China since the emergence of the virus (from 2016 to 2018). By analyzing recovered viruses in Qinghai Lake and all related viruses worldwide (449 strains), we identified the genotypes, estimated their genesis and reassortment, and evaluated their global distribution and transmission.

      Results

      Through surveillance of wild migratory birds around Qinghai Lake between 2016 and 2018, we revealed that the H5N8 was introduced into Qinghai Lake bird populations (QH-H5N8), with distinct gene constellations in 2016 and 2017. A global analysis of QH-H5N8-related viruses showed that avian influenza viruses with low pathogenicity in wild birds contributed to the high diversity of genotypes; the major reassortment events possibly occurred during the 2016 breeding season and the following winters.

      Conclusions

      Continued circulation of QH-H5N8-related viruses among wild birds has resulted in the global distribution of high genotypic diversity. Thus, these viruses pose an ongoing threat to wild and domestic bird populations and warrant continuous surveillance.

      Keywords

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      References

        • Claas E.C.
        • Osterhaus A.D.
        • van Beek R.
        • De Jong J.C.
        • Rimmelzwaan G.F.
        • Senne D.A.
        • et al.
        Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus.
        Lancet. 1998; 351: 472-477
        • Subbarao K.
        • Klimov A.
        • Katz J.
        • Regnery H.
        • Lim W.
        • Hall H.
        • et al.
        Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness.
        Science. 1998; 279: 393-396
      1. World Health Organization. Cumulative number of confirmed human cases for avian influenza A(H5N1) reported to WHO, 2003–2018. http://www.who.int/influenza/human_animal_interface/H5N1_cumulative_table_archives/en/.

        • Smith G.J.
        • Donis R.O.
        World health organization/world organisation for animal health/food and agriculture organization H5 evolution working Group. Nomenclature updates resulting from the evolution of avian influenza A(H5) virus clades 2.1.3.2a, 2.2.1, and 2.3.4 during 2013–2014.
        Influenza Other Respir Viruses. 2015; 9: 271-276
        • Su S.
        • Bi Y.
        • Wong G.
        • Gray G.C.
        • Gao G.F.
        • Li S.
        Epidemiology, evolution, and recent outbreaks of avian influenza virus in china.
        J Virol. 2015; 89: 8671-8676
        • Liu J.
        • Xiao H.
        • Lei F.
        • Zhu Q.
        • Qin K.
        • Zhang X.W.
        • et al.
        Highly pathogenic H5N1 influenza virus infection in migratory birds.
        Science. 2005; 309: 1206
        • Abdelwhab E.M.
        • Hassan M.K.
        • Abdel-Moneim A.S.
        • Naguib M.M.
        • Mostafa A.
        • Hussein I.T.M.
        • et al.
        Introduction and enzootic of A/H5N1 in Egypt: virus evolution, pathogenicity and vaccine efficacy ten years on.
        Infect Genet Evol. 2016; 40: 80-90
        • Guan Y.
        • Smith G.J.
        The emergence and diversification of panzootic H5N1 influenza viruses.
        Virus Res. 2013; 178: 35-43
        • Hu X.
        • Liu D.
        • Wang M.
        • Yang L.
        • Wang M.
        • Zhu Q.
        • et al.
        Clade 2.3.2 avian influenza virus (H5N1), Qinghai lake region, China, 2009–2010.
        Emerg Infect Dis. 2011; 17: 560-562
        • Global Consortium for H5N8 and Related Influenza Viruses
        Role for migratory wild birds in the global spread of avian influenza H5N8.
        Science. 2016; 354: 213-217
        • Bi Y.
        • Chen J.
        • Zhang Z.
        • Li M.
        • Cai T.
        • Sharshov K.
        • et al.
        Highly pathogenic avian influenza H5N1 clade 2.3.2.1c virus in migratory birds, 2014–2015.
        Virol Sin. 2016; 31: 300-305
        • Li M.X.
        • Liu H.Z.
        • Bi Y.H.
        • Sun J.Q.
        • Wong G.
        • Liu D.
        • et al.
        Highly pathogenic avian influenza A(H5N8) virus in wild migratory Birds, Qinghai Lake, China.
        Emerg Infect Dis. 2017; 23: 637-641
        • Liu J.
        • Xiao H.
        • Lei F.
        • Zhu Q.
        • Qin K.
        • Zhang X.W.
        • et al.
        Highly pathogenic H5N1 influenza virus infection in migratory birds.
        Science. 2005; 309: 1206
        • Li Y.
        • Liu L.
        • Zhang Y.
        • Duan Z.
        • Tian G.
        • Zeng X.
        • et al.
        New avian influenza virus (H5N1) in wild birds, Qinghai, China.
        Emerg Infect Dis. 2011; 17: 265
        • Hu X.
        • Liu D.
        • Wang M.
        • Yang L.
        • Wang M.
        • Zhu Q.
        • et al.
        Clade 2.3. 2 avian influenza virus (H5N1), Qinghai lake region, China, 2009–2010.
        Emerg Infect Dis. 2011; 17: 560
        • Bi Y.
        • Chen J.
        • Zhang Z.
        • Li M.
        • Cai T.
        • Sharshov K.
        • et al.
        Highly pathogenic avian influenza H5N1 clade 2.3. 2.1c virus in migratory birds, 2014–2015.
        Virol Sin. 2016; 31: 300-305
        • Li M.
        • Liu H.
        • Bi Y.
        • Sun J.
        • Wong G.
        • Liu D.
        • et al.
        Highly pathogenic avian influenza A (H5N8) virus in wild migratory birds, Qinghai Lake, China.
        Emerg Infect Dis. 2017; 23: 637
        • Prosser D.J.
        • Cui P.
        • Takekawa J.Y.
        • Tang M.
        • Hou Y.
        • Collins B.M.
        • et al.
        Wild bird migration across the Qinghai–Tibetan plateau: a transmission route for highly pathogenic H5N1.
        PLoS ONE. 2011; 6: e17622
      2. Anonymous. Qinghai Laike home to 200,000 migratory birds. 2018 August; Available from: http://www.ecns.cn/hd/2018-08-20/detail-ifyxccrz0968790.shtml.

      3. World Organisation for Animal Health. Update on highly pathogenic avian influenza in animals (typeH5 and H7)). 2018; Available from: http://www.oie.int/en/animal-health-in-the-world/update-on-avian-influenza/2017/.

        • Napp S.
        • Majo N.
        • Sanchez-Gonzalez R.
        • Vergara-Alert J.
        Emergence and spread of highly pathogenic avian influenza A(H5N8) in Europe in 2016-2017.
        Transbound Emerg Dis. 2018; 65: 1217-1226
        • Poen M.J.
        • Bestebroer T.M.
        • Vuong O.
        • Scheuer R.D.
        • van der Jeugd H.P.
        • Kleyheeg E.
        • et al.
        Local amplification of highly pathogenic avian influenza H5N8 viruses in wild birds in the Netherlands, 2016 to 2017.
        Euro Surveill. 2018; 23
        • Liu H.
        • Xiong C.
        • Chen J.
        • Chen G.
        • Zhang J.
        • Li Y.
        • et al.
        Two genetically diverse H7N7 avian influenza viruses isolated from migratory birds in central China.
        Emerg Microbes Infect. 2018; 7: 62
        • Zhang H.
        • Xu B.
        • Chen Q.
        • Chen J.
        • Chen Z.
        Characterization of an H10N8 influenza virus isolated from Dongting lake wetland.
        Virol J. 2011; 8: 42
        • Cheung P.P.
        • Leung Y.H.
        • Chow C.K.
        • Ng C.F.
        • Tsang C.L.
        • Wu Y.O.
        • et al.
        Identifying the species-origin of faecal droppings used for avian influenza virus surveillance in wild-birds.
        J Clin Virol. 2009; 46: 90-93
        • Hoffmann E.
        • Stech J.
        • Guan Y.
        • Webster R.G.
        • Perez D.R.
        Universal primer set for the full-length amplification of all influenza A viruses.
        Arch Virol. 2001; 146: 2275-2289
        • Sievers F.
        • Wilm A.
        • Dineen D.
        • Gibson T.J.
        • Karplus K.
        • Li W.
        • et al.
        Fast, scalable generation of high-quality protein multiple sequence alignments using clustal omega.
        Mol Syst Biol. 2011; 7: 539
        • Stamatakis A.
        RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies.
        Bioinformatics. 2014; 30: 1312-1313
        • Yu G.
        • Smith D.K.
        • Zhu H.
        • Guan Y.
        • Lam T.T.-Y.
        • et al.
        ggtree: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data.
        Methods Ecol Evol. 2017; 8: 28-36
        • Rambaut A.
        • Lam T.T.
        • Max Carvalho L.
        • Pybus O.G.
        Exploring the temporal structure of heterochronous sequences using tempest (formerly path-o-gen).
        Virus Evol. 2016; 2: vew007
        • Bouckaert R.
        • Heled J.
        • Kuhnert D.
        • Vaughan T.
        • Wu C.H.
        • Xie D.
        • et al.
        BEAST 2: a software platform for Bayesian evolutionary analysis.
        PLoS Comput Biol. 2014; 10e1003537
        • Bi Y.
        • Chen Q.
        • Wang Q.
        • Chen J.
        • Jin T.
        • Wong G.
        • et al.
        Genesis, evolution and prevalence of H5N6 avian influenza viruses in China.
        Cell Host Microbe. 2016; 20: 810-821
        • El-Shesheny R.
        • Barman S.
        • Feeroz M.M.
        • Hasan M.K.
        • Jones-Engel L.
        • Franks J.
        • et al.
        Genesis of influenza A(H5N8) viruses.
        Emerg Infect Dis. 2017; 23: 1368-1371
        • Duffy S.
        • Shackelton L.A.
        • Holmes E.C.
        Rates of evolutionary change in viruses: patterns and determinants.
        Nat Rev Genet. 2008; 9: 267-276
        • Rejmanek D.
        • Hosseini P.R.
        • Mazet J.A.
        • Daszak P.
        • Goldstein T.
        Evolutionary dynamics and global diversity of influenza A virus.
        J Virol. 2015; 89: 10993-11001
        • Palm E.C.
        • Newman S.H.
        • Prosser D.J.
        • Xiao X.
        • Ze L.
        • Batbayar N.
        • et al.
        Mapping migratory flyways in Asia using dynamic Brownian bridge movement models.
        Mov Ecol. 2015; 3: 3
        • Barron D.G.
        • Brawn J.D.
        • Weatherhead P.J.
        Meta‐analysis of transmitter effects on avian behaviour and ecology.
        Methods Ecol Evol. 2010; 1: 180-187
        • Gilbert M.
        • Newman S.H.
        • Takekawa J.Y.
        • Loth L.
        • Biradar C.
        • Prosser D.J.
        • et al.
        Flying over an infected landscape: distribution of highly pathogenic avian influenza H5N1 risk in South Asia and satellite tracking of wild waterfowl.
        Ecohealth. 2010; 7: 448-458
        • Takekawa J.Y.
        • Prosser D.J.
        • Collins B.M.
        • Douglas D.C.
        • Perry W.M.
        • Yan B.
        • et al.
        Movements of wild ruddy shelducks in the central Asian flyway and their spatial relationship to outbreaks of highly pathogenic avian influenza H5N1.
        Viruses. 2013; 5: 2129-2152
        • Takekawa J.Y.
        • Prosser D.J.
        • Collins B.M.
        • Douglas D.C.
        • Perry W.M.
        • Yan B.
        • et al.
        Movements of wild ruddy shelducks in the central Asian flyway and their spatial relationship to outbreaks of highly pathogenic avian influenza H5N1.
        Viruses. 2013; 5: 2129-2152
        • Muzaffar S.B.
        • Takekawa J.Y.
        • Prosser D.J.
        • Douglas D.C.
        • Yan B.
        • Xing Z.
        • et al.
        Seasonal movements and migration of pallas's gulls larus ichthyaetus from Qinghai Lake, China.
        Forktail. 2008; 24: 100-107
        • Liu J.
        • Xiao H.
        • Lei F.
        • Zhu Q.
        • Qin K.
        • Zhang X.W.
        • et al.
        Highly pathogenic H5N1 influenza virus infection in migratory birds.
        Science. 2005; 309: 1206
        • Wang G.
        • Zhan D.
        • Li L.
        • Lei F.
        • Liu B.
        • Liu D.
        • et al.
        H5N1 avian influenza re-emergence of lake Qinghai: phylogenetic and antigenic analyses of the newly isolated viruses and roles of migratory birds in virus circulation.
        J Gen Virol. 2008; 89: 697-702
        • Li Y.
        • Liu L.
        • Zhang Y.
        • Duan Z.
        • Tian G.
        • Zeng X.
        • et al.
        New avian influenza virus (H5N1) in wild birds, Qinghai, China.
        EMERG Infect Dis. 2011; 17: 265-267
        • Sharshov K.
        • Silko N.
        • Sousloparov I.
        • Zaykovskaya A.
        • Shestopalov A.
        • Drozdov I.
        Avian influenza (H5N1) outbreak among wild birds, Russia, 2009.
        Emerg Infect Dis. 2010; 16: 349-351
        • Kwon J.H.
        • Jeong S.
        • Lee D.H.
        • Swayne D.E.
        • Kim Y.J.
        • Lee S.H.
        • et al.
        New reassortant clade 2.3.4.4b avian influenza A (H5N6) virus in wild birds, South Korea, 2017–18.
        Emerg Infect Dis. 2018; 24: 1953-1955
        • Marchenko V.
        • Goncharova N.
        • Susloparov I.
        • Kolosova N.
        • Gudymo A.
        • Svyatchenko S.
        • et al.
        Isolation and characterization of H5Nx highly pathogenic avian influenza viruses of clade 2.3.4.4 in Russia.
        Virology. 2018; 525: 216-223
        • Fusaro A.
        • Monne I.
        • Mulatti P.
        • Zecchin B.
        • Bonfanti L.
        • Ormelli S.
        • et al.
        Genetic diversity of highly pathogenic avian influenza A(H5N8/H5N5) viruses in Italy, 2016–17.
        Emerg Infect Dis. 2017; 23: 1543-1547
        • Lee D.H.
        • Bahl J.
        • Torchetti M.K.
        • Killian M.L.
        • Ip H.S.
        • DeLiberto T.J.
        • et al.
        Highly pathogenic avian influenza viruses and generation of novel reassortants, United States, 2014–2015.
        Emerg Infect Dis. 2016; 22: 1283-1285
        • Ip H.S.
        • Torchetti M.K.
        • Crespo R.
        • Kohrs P.
        • DeBruyn P.
        • Mansfield K.G.
        • et al.
        Novel Eurasian highly pathogenic avian influenza A H5 viruses in wild birds, Washington, USA, 2014.
        Emerg Infect Dis. 2015; 21: 886-890
        • Saito T.
        • Tanikawa T.
        • Uchida Y.
        • Takemae N.
        • Kanehira K.
        • Tsunekuni R.
        Intracontinental and intercontinental dissemination of Asian H5 highly pathogenic avian influenza virus (clade 2.3.4.4) in the winter of 2014–2015.
        Rev Med Virol. 2015; 25: 388-405
        • Lee D.H.
        • Torchetti M.K.
        • Hicks J.
        • Killian M.L.
        • Bahl J.
        • Pantin-Jackwood M.
        • et al.
        Transmission dynamics of highly pathogenic avian influenza virus A (H5Nx) clade 2.3.4.4, North America, 2014–2015.
        Emerg Infect Dis. 2018; 24: 1840-1848
      4. World Health Organization. Cumulative number of confirmed human cases of avian influenza A(H5N1) reported to WHO. 2018; Availble from: http://www.who.int/influenza/human_animal_interface/H5N1_cumulative_table_archives/en/.

        • Olsen B.
        • Munster V.J.
        • Wallensten A.
        • Waldenstrom J.
        • Osterhaus A.D.
        • Fouchier R.A.
        Global patterns of influenza a virus in wild birds.
        Science. 2006; 312: 384-388
        • Saad M.D.
        • Ahmed L.S.
        • Gamal-Eldein M.A.
        • Fouda M.K.
        • Khalil F.
        • Yingst S.L.
        • et al.
        Possible avian influenza (H5N1) from migratory bird, Egypt.
        Emerg Infect Dis. 2007; 13: 1120-1121