J Vet Sci.  2017 Aug;18(S1):269-280. 10.4142/jvs.2017.18.S1.269.

Evolution, global spread, and pathogenicity of highly pathogenic avian influenza H5Nx clade 2.3.4.4

Affiliations
  • 1U.S. National Poultry Research Center, Agricultural Research Service, U.S. Department of Agriculture, Athens, GA 30605, USA. David.Swayne@ars.usda.gov
  • 2Avian Diseases Laboratory, College of Veterinary Medicine, Konkuk University, Seoul 05029, Korea.

Abstract

Novel subtypes of Asian-origin (Goose/Guangdong lineage) H5 highly pathogenic avian influenza (HPAI) viruses belonging to clade 2.3.4, such as H5N2, H5N5, H5N6, and H5N8, have been identified in China since 2008 and have since evolved into four genetically distinct clade 2.3.4.4 groups (A-D). Since 2014, HPAI clade 2.3.4.4 viruses have spread rapidly via migratory wild aquatic birds and have evolved through reassortment with prevailing local low pathogenicity avian influenza viruses. Group A H5N8 viruses and its reassortant viruses caused outbreaks in wide geographic regions (Asia, Europe, and North America) during 2014-2015. Novel reassortant Group B H5N8 viruses caused outbreaks in Asia, Europe, and Africa during 2016-2017. Novel reassortant Group C H5N6 viruses caused outbreaks in Korea and Japan during the 2016-2017 winter season. Group D H5N6 viruses caused outbreaks in China and Vietnam. A wide range of avian species, including wild and domestic waterfowl, domestic poultry, and even zoo birds, seem to be permissive for infection by and/or transmission of clade 2.3.4.4 HPAI viruses. Further, compared to previous H5N1 HPAI viruses, these reassortant viruses show altered pathogenicity in birds. In this review, we discuss the evolution, global spread, and pathogenicity of H5 clade 2.3.4.4 HPAI viruses.

Keyword

epidemiology; influenza in birds; poultry; transmission; virulence

MeSH Terms

Animals
Asia/epidemiology
Birds/virology
China/epidemiology
Disease Outbreaks
Europe/epidemiology
Influenza A Virus, H5N2 Subtype/pathogenicity
Influenza A Virus, H5N8 Subtype/pathogenicity
Influenza in Birds/*epidemiology/virology
North America/epidemiology
Poultry/virology

Figure

  • Fig. 1 Geographic map showing movement patterns of highly pathogenic avian influenza (HPAI) clade 2.3.4.4 viruses.


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Reference

1. Berhane Y, Kobasa D, Embury-Hyatt C, Pickering B, Babiuk S, Joseph T, Bowes V, Suderman M, Leung A, Cottam-Birt C, Hisanaga T, Pasick J. Pathobiological characterization of a novel reassortant highly pathogenic H5N1 virus isolated in British Columbia, Canada, 2015. Sci Rep. 2016; 6:23380.
Article
2. Bertran K, Lee DH, Balzli C, Pantin-Jackwood MJ, Spackman E, Swayne DE. Age is not a determinant factor in susceptibility of broilers to H5N2 clade 2.3.4.4 high pathogenicity avian influenza virus. Vet Res. 2016; 47:116.
Article
3. Bertran K, Swayne DE, Pantin-Jackwood MJ, Kapczynski DR, Spackman E, Suarez DL. Lack of chicken adaptation of newly emergent Eurasian H5N8 and reassortant H5N2 high pathogenicity avian influenza viruses in the U.S. is consistent with restricted poultry outbreaks in the Pacific flyway during 2014-2015. Virology. 2016; 494:190–197.
Article
4. Bi Y, Chen Q, Wang Q, Chen J, Jin T, Wong G, Quan C, Liu J, Wu J, Yin R, Zhao L, Li M, Ding Z, Zou R, Xu W, Li H, Wang H, Tian K, Fu G, Huang Y, Shestopalov A, Li S, Xu B, Yu H, Luo T, Lu L, Xu X, Luo Y, Liu Y, Shi W, Liu D, Gao GF. Genesis, evolution and prevalence of H5N6 avian influenza viruses in China. Cell Host Microbe. 2016; 20:810–821.
Article
5. DeJesus E, Costa-Hurtado M, Smith D, Lee DH, Spackman E, Kapczynski DR, Torchetti MK, Killian ML, Suarez DL, Swayne DE, Pantin-Jackwood MJ. Changes in adaptation of H5N2 highly pathogenic avian influenza H5 clade 2.3.4.4 viruses in chickens and mallards. Virology. 2016; 499:52–64.
Article
6. Du Y, Chen M, Yang J, Jia Y, Han S, Holmes EC, Cui J. Molecular evolution and emergence of H5N6 avian influenza virus in central China. J Virol. 2017; 91:e00143–e00117.
Article
7. Fan S, Zhou L, Wu D, Gao X, Pei E, Wang T, Gao Y, Xia X. A novel highly pathogenic H5N8 avian influenza virus isolated from a wild duck in China. Influenza Other Respir Viruses. 2014; 8:646–653.
Article
8. Fouchier RA, Munster VJ. Epidemiology of low pathogenic avian influenza viruses in wild birds. Rev Sci Tech. 2009; 28:49–58.
Article
9. Ghafouri SA, GhalyanchiLangeroudi A, Maghsoudloo H, Kh Farahani R, Abdollahi H, Tehrani F, Fallah MH. Clade 2.3.4.4 avian influenza A (H5N8) outbreak in commercial poultry, Iran, 2016: the first report and update data. Trop Anim Health Prod. 2017; 49:1089–1093.
Article
10. 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.
11. Globig A, Starick E, Homeier T, Pohlmann A, Grund C, Wolf P, Zimmermann A, Wolf C, Heim D, Schlößer H, Zander S, Beer M, Conraths FJ, Harder TC. Epidemiological and molecular analysis of an outbreak of highly pathogenic avian influenza H5N8 clade a German zoo: effective disease control with minimal culling. Transbound Emerg Dis. 2016; DOI: 10.1111/tbed.12570. Epub ahead of print.
12. Gu M, Liu W, Cao Y, Peng D, Wang X, Wan H, Zhao G, Xu Q, Zhang W, Song Q, Li Y, Liu X. Novel reassortant highly pathogenic avian influenza (H5N5) viruses in domestic ducks, China. Emerg Infect Dis. 2011; 17:1060–1063.
Article
13. Hill SC, Lee YJ, Song BM, Kang HM, Lee EK, Hanna A, Gilbert M, Brown IH, Pybus OG. Wild waterfowl migration and domestic duck density shape the epidemiology of highly pathogenic H5N8 influenza in the Republic of Korea. Infect Genet Evol. 2015; 34:267–277.
Article
14. Jeong J, Kang HM, Lee EK, Song BM, Kwon YK, Kim HR, Choi KS, Kim JY, Lee HJ, Moon OK, Jeong W, Choi J, Baek JH, Joo YS, Park YH, Lee HS, Lee YJ. Highly pathogenic avian influenza virus (H5N8) in domestic poultry and its relationship with migratory birds in South Korea during 2014. Vet Microbiol. 2014; 173:249–257.
Article
15. Jeong J, Woo C, Ip HS, An I, Kim Y, Lee K, Jo SD, Son K, Lee S, Oem JK, Wang SJ, Kim Y, Shin J, Sleeman J, Jheong W. Identification of Two novel reassortant avian influenza a (H5N6) viruses in whooper swans in Korea, 2016. Virol J. 2017; 14:60.
Article
16. Kanehira K, Uchida Y, Takemae N, Hikono H, Tsunekuni R, Saito T. Characterization of an H5N8 influenza A virus isolated from chickens during an outbreak of severe avian influenza in Japan in April 2014. Arch Virol. 2015; 160:1629–1643.
Article
17. Kang HM, Lee EK, Song BM, Heo GB, Jung J, Jang I, Bae YC, Jung SC, Lee YJ. Experimental infection of mandarin duck with highly pathogenic avian influenza A (H5N8 and H5N1) viruses. Vet Microbiol. 2017; 198:59–63.
Article
18. 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. 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. 2017; 53:56–67.
Article
19. Kwon JH, Lee DH, Jeong JH, Yuk SS, Erdene-Ochir TO, Noh JY, Hong WT, Jeong S, Gwon GB, Lee SW, Choi IS, Song CS. Isolation of an H5N8 highly pathogenic avian influenza virus strain from wild birds in Seoul, a highly urbanized area in South Korea. J Wildl Dis. 2017; 53:630–635.
Article
20. Kwon JH, Lee DH, Swayne DE, Noh JY, Yuk SS, Erdene-Ochir TO, Hong WT, Jeong JH, Jeong S, Gwon GB, Lee S, Song CS. Reassortant clade 2.3.4.4 avian influenza A(H5N6) virus in a wild mandarin duck, South Korea, 2016. Emerg Infect Dis. 2017; 23:822–826.
Article
21. Kwon JH, Lee DH, Swayne DE, Noh JY, Yuk SS, Erdene-Ochir TO, Hong WT, Jeong JH, Jeong S, Gwon GB, Song CS. Highly pathogenic avian influenza A(H5N8) viruses reintroduced into South Korea by migratory waterfowl, 2014-2015. Emerg Infect Dis. 2016; 22:507–510.
Article
22. Lee DH, Bahl J, Torchetti MK, Killian ML, Ip HS, DeLiberto TJ, Swayne DE. Highly pathogenic avian influenza viruses and generation of novel reassortants, United States, 2014-2015. Emerg Infect Dis. 2016; 22:1283–1285.
Article
23. Lee DH, Kwon JH, Noh JY, Park JK, Yuk SS, Erdene-Ochir TO, Lee JB, Park SY, Choi IS, Lee SW, Song CS. Pathogenicity of the Korean H5N8 highly pathogenic avian influenza virus in commercial domestic poultry species. Avian Pathol. 2016; 45:208–211.
Article
24. Lee DH, Sharshov K, Swayne DE, Kurskaya O, Sobolev I, Kabilov M, Alekseev A, Irza V, Shestopalov A. Novel reassortant influenza A(H5N8) virus in wild aquatic birds, Russia, 2016. Emerg Infect Dis. 2017; 23:359–360.
Article
25. Lee DH, Sharshov K, Swayne DE, Kurskaya O, Sobolev I, Kabilov M, Alekseev A, Irza V, Shestopalov A. Novel reassortant influenza A(H5N8) virus in wild aquatic birds, Russia, 2016. Emerg Infect Dis. 2017; 23:359–360.
Article
26. Lee DH, Torchetti MK, Winker K, Ip HS, Song CS, Swayne DE. Intercontinental spread of Asian-origin H5N8 to North America through Beringia by migratory birds. J Virol. 2015; 89:6521–6524.
Article
27. Lee MS, Chen LH, Chen YP, Liu YP, Li WC, Lin YL, Lee F. Highly pathogenic avian influenza viruses H5N2, H5N3, and H5N8 in Taiwan in 2015. Vet Microbiol. 2016; 187:50–57.
Article
28. 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. Novel reassortant influenza A(H5N8) viruses, South Korea, 2014. Emerg Infect Dis. 2014; 20:1087–1089.
Article
29. Li J, Gu M, Liu D, Liu B, Jiang K, Zhong L, Liu K, Sun W, Hu J, Wang X, Hu S, Liu X, Liu X. Phylogenetic and biological characterization of three K1203 (H5N8)-like avian influenza A virus reassortants in China in 2014. Arch Virol. 2016; 161:289–302.
Article
30. 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. Highly pathogenic avian influenza A(H5N8) virus in wild migratory birds, Qinghai Lake, China. Emerg Infect Dis. 2017; 23:637–641.
Article
31. Marchenko VY, Susloparov IM, Kolosova NP, Goncharova NI, Shipovalov AV, Durymanov AG, Ilyicheva TN, Budatsirenova LV, Ivanova VK, Ignatyev GA, Ershova SN, Tulyahova VS, Mikheev VN, Ryzhikov AB. Influenza A(H5N8) virus isolation in Russia, 2014. Arch Virol. 2015; 160:2857–2860.
Article
32. Nagarajan S, Kumar M, Murugkar HV, Tripathi S, Shukla S, Agarwal S, Dubey G, Nagi RS, Singh VP, Tosh C. Novel reassortant highly pathogenic avian influenza (H5N8) virus in zoos, India. Emerg Infect Dis. 2017; 23:717–719.
Article
33. Núñez A, Brookes SM, Reid SM, Garcia-Rueda C, Hicks DJ, Seekings JM, Spencer YI, Brown IH. Highly pathogenic avian influenza H5N8 : equivocal pathogenicity and implications for surveillance following natural infection in breeder ducks in the United Kingdom. Transbound Emerg Dis. 2016; 63:5–9.
Article
34. Okamatsu M, Ozawa M, Soda K, Takakuwa H, Haga A, Hiono T, Matsuu A, Uchida Y, Iwata R, Matsuno K, Kuwahara M, Yabuta T, Usui T, Ito H, Onuma M, Sakoda Y, Saito T, Otsuki K, Ito T, Kida H. Characterization of highly pathogenic avian influenza virus A(H5N6), Japan, November 2016. Emerg Infect Dis. 2017; 23:691–695.
Article
35. Olsen B, Munster VJ, Wallensten A, Waldenström J, Osterhaus AD, Fouchier RA. Global patterns of influenza a virus in wild birds. Science. 2006; 312:384–388.
Article
36. Pohlmann A, Starick E, Harder T, Grund C, Höper D, Globig A, Staubach C, Dietze K, Strebelow G, Ulrich RG, Schinköthe J, Teifke JP, Conraths FJ, Mettenleiter TC, Beer M. Outbreaks among wild birds and domestic poultry caused by reassorted influenza A(H5N8) clade 2.3.4.4 viruses, Germany, 2016. Emerg Infect Dis. 2017; 23:633–636.
Article
37. Qi X, Cui L, Yu H, Ge Y, Tang F. Whole-genome sequence of a reassortant H5N6 avian influenza virus isolated from a live poultry market in China, 2013. Genome Announc. 2014; 2:e00706–e00714.
Article
38. Röhm C, Horimoto T, Kawaoka Y, Süss J, Webster RG. Do hemagglutinin genes of highly pathogenic avian influenza viruses constitute unique phylogenetic lineages? Virology. 1995; 209:664–670.
Article
39. Selim AA, Erfan AM, Hagag N, Zanaty A, Samir AH, Samy M, Abdelhalim A, Arafa AA, Soliman MA, Shaheen M, Ibraheem EM, Mahrous I, Hassan MK, Naguib MM. Highly pathogenic avian influenza virus (H5N8) clade 2.3.4.4 infection in migratory birds, Egypt. Emerg Infect Dis. 2017; 23:1048–1051.
Article
40. Song BM, Lee EK, Lee YN, Heo GB, Lee HS, Lee YJ. Phylogeographical characterization of H5N8 viruses isolated from poultry and wild birds during 2014-2016 in South Korea. J Vet Sci. 2017; 18:89–94.
Article
41. Song Y, Cui J, Song H, Ye J, Zhao Z, Wu S, Xu C, Jiao P, Liao M. New reassortant H5N8 highly pathogenic avian influenza virus from waterfowl in Southern China. Front Microbiol. 2015; 6:1170.
Article
42. Spackman E, Pantin-Jackwood MJ, Kapczynski DR, Swayne DE, Suarez DL. H5N2 highly pathogenic avian influenza viruses from the US 2014-2015 outbreak have an unusually long pre-clinical period in turkeys. BMC Vet Res. 2016; 12:260.
Article
43. Spackman E, Prosser DJ, Pantin-Jackwood MJ, Berlin AM, Stephens CB. The pathogenesis of clade 2.3.4.4 H5 highly pathogenic avian influenza viruses in ruddy duck (Oxyura jamaicensis) and lesser scaup (Aythya affinis). J Wildl Dis. 2017; Epub ahead of print. DOI: 10.7589/2017-01-003.
44. Sun H, Pu J, Hu J, Liu L, Xu G, Gao GF, Liu X, Liu J. Characterization of clade 2.3.4.4 highly pathogenic H5 avian influenza viruses in ducks and chickens. Vet Microbiol. 2016; 182:116–122.
Article
45. Swayne D, Bertran K, Kapczynski D, Pantin-Jackwood M, Spackman E, Lee DH, Suarez D. Impact of emergence of avian influenza in North America and preventative measures. Proceedings of the Sixty-Fifth Western Poultry Disease Conference 2016. 24-27 April 2016; Vancouver, Canada.
46. Swayne DE. Animal Influenza. 2nd ed. Ames: John Wiley & Sons;2016.
47. Swayne DE, Pantin-Jackwood M. Pathogenicity of avian influenza viruses in poultry. Dev Biol (Basel). 2006; 124:61–67.
48. Swayne DE, Suarez DL, Spackman E, Jadhao S, Dauphin G, Kim-Torchetti M, McGrane J, Weaver J, Daniels P, Wong F, Selleck P, Wiyono A, Indriani R, Yupiana Y, Sawitri Siregar E, Prajitno T, Smith D, Fouchier R. Antibody titer has positive predictive value for vaccine protection against challenge with natural antigenic-drift variants of H5N1 high-pathogenicity avian influenza viruses from Indonesia. J Virol. 2015; 89:3746–3762.
Article
49. Tanikawa T, Kanehira K, Tsunekuni R, Uchida Y, Takemae N, Saito T. Pathogenicity of H5N8 highly pathogenic avian influenza viruses isolated from a wild bird fecal specimen and a chicken in Japan in 2014. Microbiol Immunol. 2016; 60:243–252.
Article
50. Usui T, Soda K, Tomioka Y, Ito H, Yabuta T, Takakuwa H, Otsuki K, Ito T, Yamaguchi T. Characterization of clade 2.3.4.4 H5N8 highly pathogenic avian influenza viruses from wild birds possessing atypical hemagglutinin polybasic cleavage sites. Virus Genes. 2017; 53:44–51.
Article
51. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol Rev. 1992; 56:152–179.
Article
52. WHO/OIE/FAO H5N1 Evolution Working Group. Toward a unified nomenclature system for highly pathogenic avian influenza virus (H5N1). Emerg Infect Dis. 2008; 14:e1.
53. Wu H, Peng X, Xu L, Jin C, Cheng L, Lu X, Xie T, Yao H, Wu N. Novel reassortant influenza A(H5N8) viruses in domestic ducks, eastern China. Emerg Infect Dis. 2014; 20:1315–1318.
Article
54. Yuan R, Wang Z, Kang Y, Wu J, Zou L, Liang L, Song Y, Zhang X, Ni H, Lin J, Ke C. Continuing reassortant of H5N6 subtype highly pathogenic avian influenza virus in Guangdong. Front Microbiol. 2016; 7:520.
Article
55. Zhao G, Gu X, Lu X, Pan J, Duan Z, Zhao K, Gu M, Liu Q, He L, Chen J, Ge S, Wang Y, Chen S, Wang X, Peng D, Wan H, Liu X. Novel reassortant highly pathogenic H5N2 avian influenza viruses in poultry in China. PLoS One. 2012; 7:e46183.
Article
56. Zhou LC, Liu J, Pei EL, Xue WJ, Lyu JM, Cai YT, Wu D, Wu W, Liu YY, Jin HY, Gao YW, Wang ZH, Wang TH. Novel avian influenza A(H5N8) viruses in migratory birds, China,2013-2014. Emerg Infect Dis. 2016; 22:1121–1123.
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