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Phylogeography of Highly Pathogenic H5 Avian Influenza Viruses in China

Virologica Sinica volume 35, pages 548–555 (2020)Cite this article

Abstract

The spread of H5 highly pathogenic avian influenza viruses poses serious threats to the poultry industry, wild bird ecology and human health. Circulation of H5 viruses between poultry and wild birds is a significant public health threat in China. Thus, viral migration networks in this region need to be urgently studied. Here, we conducted molecular genetic analyses of the hemagglutinin genes of H5 highly pathogenic avian influenza viruses in multiple hosts from 2000 to 2018 in China. Our aim was to clarify the roles of different hosts in the evolution of H5 viruses. We used a flexible Bayesian statistical framework to simulate viral space diffusion and continuous-time Markov chains to infer the dynamic evolutionary process of spatiotemporal dissemination. Bayesian phylogeographic analysis of H5 viruses showed for the first time that H5 viruses in poultry and wild birds were present in Guangdong Province. Furthermore, Guangdong, Jiangsu, Shanghai and Hunan acted as the epicenters for the spread of various H5 subtypes viruses in poultry, and Henan, Shanghai, Hong Kong and Inner Mongolia acted as epicenters for the spread of various H5 subtypes viruses in wild birds. Thus, H5 viruses exhibited distinct evolutionary dynamics in poultry and wild birds. Our findings extend our understanding of the transmission and spread of highly pathogenic H5 avian influenza viruses in China.

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References

  • Bertran K, Dolz R, Majó N (2014) Pathobiology of avian influenza virus infection in minor gallinaceous species: a review. Avian Pathol 43:9–25

    PubMed  Google Scholar 

  • Bi Y, Zhang Z, Liu W, Yin Y, Lei F (2015) Highly pathogenic avian influenza A(H5N1) virus struck migratory birds in China in 2015. Sci Rep 5:12986

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bi Y, Chen J, Zhang Z, Li M, Cai T, Sharshov K, Susloparov I, Shestopalov A, Wong G, He Y (2016a) Highly pathogenic avian influenza H5N1 Clade 2.3.2.1c virus in migratory birds, 2014–2015. Virol Sin 31:300–305

    PubMed  Google Scholar 

  • Bi Y, Chen Q, Wang Q, Chen J, Jin T, Wong G, Quan C, Liu J, Wu J, Yin R (2016b) Genesis, evolution and prevalence of H5N6 avian influenza viruses in China. Cell Host Microbe 20:810–821

    CAS  PubMed  Google Scholar 

  • Bielejec F, Baele G, Vrancken B, Suchard MA, Rambaut A, Lemey P (2016) Sprea D3: interactive visualization of spatiotemporal history and trait evolutionary processes. Mol Biol Evol 33:2167–2169

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brown JD, Stallknecht DE, Swayne DE (2008) Experimental infection of swans and geese with highly pathogenic avian influenza virus (H5N1) of Asian lineage. Emerg Infect Dis 14:136–142

    PubMed  PubMed Central  Google Scholar 

  • Chen H, Smith GJD, Zhang SY, Qin K, Wang J, Li KS, Webster RG, Peiris JSM, Guan Y (2005) Avian flu: H5N1 virus outbreak in migratory waterfowl. Nature 436:191–192

    CAS  PubMed  Google Scholar 

  • Chen H, Smith GJD, Li KS, Wang J, Fan XH, Rayner JM, Vijaykrishna D, Zhang JX, Zhang LJ, Guo CT et al (2006) Establishment of multiple sublineages of H5N1 influenza virus in Asia: implications for pandemic control. Proc Natl Acad Sci USA 103:2845–2850

    CAS  PubMed  Google Scholar 

  • Claes F, Kuznetsov D, Liechti R, Dobschuetz SV, Bao DT, Gleizes A, Conversa D, Colonna A, Demaio E, Ramazzotto S, Larfaoui F, Pinto J, Le Mercier P, Xenarios I, Dauphin G (2014) The EMPRES-i genetic module: a novel tool linking epidemiological outbreak information and genetic characteristics of influenza viruses. Database (Oxford). 2014: bau008

  • Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973

    CAS  PubMed  PubMed Central  Google Scholar 

  • Duan L, Bahl J, Smith GJD, Wang J, Vijaykrishna D, Zhang LJ, Zhang JX, Li KS, Fan XH, Cheung CL, Huang K, Poon LL, Shortridge KF, Webster RG, Peiris JS, Chen H, Guan Y (2008) The development and genetic diversity of H5N1 influenza virus in China, 1996–2006. Virology 380:243–254

    CAS  PubMed  PubMed Central  Google Scholar 

  • El-Shesheny R, Barman S, Feeroz MM, Hasan MK, Jones-Engel L, Franks J, Turner J, Seiler P, Walker D, Friedman K, Kercher L, Begum S, Akhtar S, Datta AK, Krauss S, Kayali G, McKenzie P, Webby RJ, Webster RG (2017) Genesis of influenza A (H5N8) viruses. Emerg Infect Dis 23:1368–1371

    PubMed  PubMed Central  Google Scholar 

  • Flyway EAA (2011) Implementation strategy for the East Asian—Australasian flyway partnership: 2007–2011. Department of the Environment 3:1-8

  • Flyway EAA (2015) East Asian–Australasian flyway. New Zealand

  • Gu M, Liu W, Cao Y, Peng D, Wang X, Wan H, Zhao G, Xu Q, Zhang W, Song Q (2011) Novel reassortant highly pathogenic avian influenza (H5N5) viruses in domestic ducks, China. Emerg Infect Dis 17:1060–1063

    PubMed  PubMed Central  Google Scholar 

  • Guan Y, Smith GJD, Webby R, Webster RG (2009) Molecular epidemiology of H5N1 avian influenza. Rev Sci Tech 28:39–47

    CAS  PubMed  Google Scholar 

  • Huang PY, Lee CCD, Yip CH, Cheung CL, Yu G, Lam TTY, Smith DK, Zhu H, Guan Y (2016) Genetic characterization of highly pathogenic H5 influenza viruses from poultry in Taiwan, 2015. Infect Genet Evol 38:96–100

    CAS  PubMed  Google Scholar 

  • Keawcharoen J, Van Riel D, Van Amerongen G, Bestebroer T, Beyer WE, van Lavieren R, Osterhaus AD, Fouchier RA, Kuiken T (2008) Wild ducks as long-distance vectors of highly pathogenic avian influenza virus (H5N1). Emerg Infect Dis 14:600–607

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kilpatrick AM, Chmura AA, Gibbons DW, Fleischer RC, Marra PP, Daszak P (2006) Predicting the global spread of H5N1 avian influenza. Proc Natl Acad Sci USA 103:19368–19373

    CAS  PubMed  Google Scholar 

  • Kim YI, Park SJ, Kwon HI, Kim EH, Si YJ, Jeong JH, Lee IW, Nguyen HD, Kwon JJ, Choi WS, Song MS, Kim CJ, Choi YK (2017) Genetic and phylogenetic characterizations of a novel genotype of highly pathogenic avian influenza (HPAI) H5N8 viruses in 2016/2017 in South Korea. Infect Genet Evol 53:56–67

    CAS  PubMed  Google Scholar 

  • Lam TT, Wang J, Shen Y, Zhou B, Duan L, Cheung CL, Ma C, Lycett SJ, Leung CY, Chen X, Li L, Hong W, Chai Y, Zhou L, Liang H, Ou Z, Liu Y, Farooqui A, Kelvin DJ, Poon LL, Smith DK, Pybus OG, Leung GM, Shu Y, Webster RG, Webby RJ, Peiris JS, Rambaut A, Zhu H, Guan Y (2013) The genesis and source of the H7N9 influenza viruses causing human infections in China. Nature 502:241–244

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee YJ, Kang HM, Lee EK, Song BM, Jeong J, Kwon YK, Kim HR, Lee KJ, Hong MS, Jang I, Choi KS, Kim JY, Lee HJ, Kang MS, Jeong OM, Baek JH, Joo YS, Park YH, Lee HS (2014) Novel reassortant influenza A(H5N8) viruses, South Korea, 2014. Emerg Infect Dis 20:1086–1089

    Google Scholar 

  • Lee DH, Torchetti MK, Winker K, Ip HS, Song CS, Swayne DE (2015) Intercontinental spread of asian-origin H5N8 to North America through Beringia by migratory birds. J Virol 89:6521–6524

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee DH, Bahl J, Torchetti MK, Killian ML, Ip HS, DeLiberto TJ, Swayne DE (2016) Highly pathogenic avian influenza viruses and generation of novel reassortants, United States, 2014–2015. Emerg Infect Dis 22:1283–1285

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lemey P, Rambaut A, Drummond AJ, Suchard MA (2009) Bayesian phylogeography finds its roots. PLoS Comput Biol 5:e1000520

    PubMed  PubMed Central  Google Scholar 

  • Leung YHC, Lau EHY, Juan ZL, Yi G, Cowling BJ, Peiris JSM (2012) Avian influenza and ban on overnight poultry storage in live poultry markets, Hong Kong. Emerg Infect Dis 18:1339–1341

    PubMed  PubMed Central  Google Scholar 

  • Li Y, Liu L, Zhang Y, Duan Z, Tian G, Zeng X, Shi J, Zhang L, Chen H (2011) New avian influenza virus (H5N1) in wild birds, Qinghai, China. Emerg Infect Dis 17:265–267

    PubMed  PubMed Central  Google Scholar 

  • Li M, Liu H, Bi Y, Sun J, Wong G, Liu D, Li L, Liu J, Chen Q, Wang H, He Y, Shi W, Gao GF, Chen J (2017) Highly pathogenic avian influenza A(H5N8) virus in wild migratory birds, Qinghai Lake, China. Emerg Infect Dis 23:637–641

    PubMed  PubMed Central  Google Scholar 

  • Li R, Zhang T, Bai Y, Li H, Wang Y, Bi Y, Chang J, Xu B (2018) Live poultry trading drives China’s H7N9 viral evolution and geographical network propagation. Front Public Health 6:210

    PubMed  PubMed Central  Google Scholar 

  • Minin VN, Bloomquist EW, Suchard MA (2008) Smooth skyride through a rough skyline: Bayesian coalescent-based inference of population dynamics. Mol Biol Evol 25:1459–1471

    CAS  PubMed  PubMed Central  Google Scholar 

  • OIE (2019) OIE situation report for avian influenza. https://www.oie.int/en/animal-health-in-the-world/update-on-avian-influenza/2019/. Accessed 26 May 2019

  • Olsen B, Munster V, Wallensten A, Jonas W, Osterhaus A, Fouchier R (2006) Global patterns of influenza a virus in wild birds. Science 312:384–388

    CAS  PubMed  Google Scholar 

  • Pan M, Gao R, Lu Q, Huang S, Zhou Z, Yang L, Li X, Zhao X, Zou X, Tong W et al (2015) Human infection with a novel highly pathogenic avian influenza A (H5N6) virus: virological and clinical findings. J Infect 72:52–59

    PubMed  Google Scholar 

  • Rambaut A, Drummond AJ, Dong X, Baele G, Suchard MA (2018) Posterior summarization in bayesian phylogenetics using tracer 1.7. Syst Biol 67:901–904

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reperant LA, Fuckar NS, Osterhaus AD, Dobson AP, Kuiken T (2010) Spatial and temporal association of outbreaks of H5N1 influenza virus infection in wild birds with the 0 degrees C isotherm. PLoS Pathog 6:e1000854

    PubMed  PubMed Central  Google Scholar 

  • Shapiro B, Rambaut A, Drummond AJ (2006) Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. Mol Biol Evol 23:7–9

    CAS  PubMed  Google Scholar 

  • Smith GJ, Fan XH, Wang J, Li KS, Qin K, Zhang JX, Vijaykrishna D, Cheung CL, Huang K, Rayner JM, Peiris JS, Chen H, Webster RG, Guan Y (2006) Emergence and predominance of an H5N1 influenza variant in China. Proc Natl Acad Sci USA 103:16936–16941

    CAS  PubMed  Google Scholar 

  • Smith GJ, Vijaykrishna D, Ellis TM, Dyrting KC, Leung YH, Bahl J, Wong CW, Kai H, Chow MK, Duan L, Chan AS, Zhang LJ, Chen H, Luk GS, Peiris JS, Guan Y (2009) Characterization of avian influenza viruses A (H5N1) from wild birds, Hong Kong, 2004–2008. Emerg Infect Dis 15:402–407

    CAS  PubMed  PubMed Central  Google Scholar 

  • Su S, Bi Y, Wong G, Gray GC, Gao GF, Li S (2015) Epidemiology, evolution, and recent outbreaks of avian influenza virus in China. J Virol 89:8671–8676

    CAS  PubMed  PubMed Central  Google Scholar 

  • The Global Consortium for H5N8 and Related Influenza Viruses (2016) Role for migratory wild birds in the global spread of avian influenza H5N8. Science 354:213–217

    PubMed Central  Google Scholar 

  • Tian H, Cui Y, Dong L, Zhou S, Li X, Huang S, Yang R, Xu B (2015a) Spatial, temporal and genetic dynamics of highly pathogenic avian influenza A (H5N1) virus in China. BMC Infect Dis 15:54

    PubMed  PubMed Central  Google Scholar 

  • Tian H, Zhou S, Dong L, Cui Y, Li X, Wu Y, Cazelles B, Huang S, Yang R, Xu B (2015b) Avian influenza H5N1 viral and bird migration networks in Asia. Proc Natl Acad Sci USA 112:172–177

    CAS  PubMed  Google Scholar 

  • Van Kerkhove MD, Vong S, Guitian J, Holl D, Mangtani P, San S, Ghani AC (2009) Poultry movement networks in Cambodia: implications for surveillance and control of highly pathogenic avian influenza (HPAI/H5N1). Vaccine 27:6345–6352

    PubMed  Google Scholar 

  • Vijaykrishna D, Bahl J, Riley S, Duan L, Zhang J, Chen H, Peiris J, Smith G, Guan Y (2008) Evolutionary dynamics and emergence of panzootic H5N1 influenza viruses. PLoS Pathog 4:e1000161

    PubMed  PubMed Central  Google Scholar 

  • WHO/OIE/FAO H5N1 Evolution Working Group (2008) Toward a unified nomenclature system for highly pathogenic avian influenza virus (H5N1). Emerg Infect Dis 14:e1

    Google Scholar 

  • World Health Organization (WHO) (2015) Evolution of the influenza A(H5) haemagglutinin: WHO/OIE/FAO H5 Working Group reports a new clade designated 2.3.4.4. https://www.who.int/influenza/gisrs_laboratory/h5_nomenclature_clade2344/en/. Accessed 26 May 2019

  • Wu X, Tian H, Zhou S, Chen L, Xu B (2014) Impact of global change on transmission of human infectious diseases. Sci China Earth Sci 57:189–203

    PubMed  Google Scholar 

  • Yang L, Zhu W, Li X, Bo H, Zhang Y, Zou S, Gao R, Dong J, Zhao X, Chen W, Dong L, Zou X, Xing Y, Wang D, Shu Y (2017) Genesis and Dissemination of Highly Pathogenic H5N6 Avian Influenza Viruses. J Virol 91. pii: e02199-16

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Acknowledgements

This study was partially supported by the National Research Program of the Ministry of Science and Technology of the People’s Republic of China (2016YFA0600104) and by donations from Delos Living LLC and the Cyrus Tang Foundation to Tsinghua University.

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Affiliations

  1. Department of Earth System Science, Tsinghua University, Beijing, 100084, China

    Xiaowen Li, Xueying Li & Bing Xu

  2. Center for Healthy Cities, Institute for China Sustainable Urbanization, Tsinghua University, Beijing, 100084, China

    Xiaowen Li, Xueying Li & Bing Xu

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  1. Xiaowen Li
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  2. Xueying Li
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  3. Bing Xu
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Contributions

XWL and BX conceived and designed the research. XYL provided helpful suggestions regarding the study. XWL and BX wrote the manuscript.

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Correspondence to Bing Xu.

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Li, X., Li, X. & Xu, B. Phylogeography of Highly Pathogenic H5 Avian Influenza Viruses in China. Virol. Sin. 35, 548–555 (2020). https://doi.org/10.1007/s12250-020-00193-7

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  • DOI: https://doi.org/10.1007/s12250-020-00193-7

Keywords

  • Influenza
  • H5 viruses
  • Phylogeography
  • Spatial dispersion
  • Population dynamics
  • China