Clin Exp Vaccine Res.  2017 Jul;6(2):95-103. 10.7774/cevr.2017.6.2.95.

Recent outbreaks of highly pathogenic avian influenza viruses in South Korea

Affiliations
  • 1Infectious Disease Research Center, Korea Research Institute of Bioscience and Biotechnology, Daejeon, Korea. syoon@kribb.re.kr
  • 2University of Science and Technology (UST), Daejeon, Korea.

Abstract

Outbreaks of H5 highly pathogenic avian influenza viruses (HPAIVs) have caused economic loss for the poultry industry and posed a threat to public health. In South Korea, novel reassortants of HPAIVs such as H5N6 and H5N8 had been circulating in poultry. Here, we will discuss the identity of recent novel reassortants of Korean H5 HPAIVs and the recent advances in vaccine development, which will be useful for controlling HPAIV transmission in poultry and for effectively preventing future epidemics and pandemics.

Keyword

Avian influenza; H5N1 subtype; H5N6 subtype; H5N8 subtype; Epidemiology; Vaccines

MeSH Terms

Animals
Disease Outbreaks*
Epidemiology
Influenza in Birds*
Korea*
Pandemics
Poultry
Public Health
Vaccines
Vaccines

Figure

  • Fig. 1 Predicting the evolution of Chinese H5Nx viruses. A genealogical tree of hemagglutinin sequences of H5Nx viruses by 2014 in China and H5N6 highly pathogenic avian influenza virus (HPAIV), 2016 in Korea. Nodes are colored according to the fitness ranking. Overall amino acids similarities of the input sequences were 86.2%-98.4%, while those of the lineage to which Korean H5N6 virus belonged were 97.5%-98.4%. A box indicates a H5N6 HPAIV in Korea, 2016.


Cited by  1 articles

The difference of detection rate of avian influenza virus in the wild bird surveillance using various methods
Gang-San Kim, Tae-Sik Kim, Joo-Sung Son, Van Dam Lai, Jung-Eun Park, Seung-Jun Wang, Weon-Hwa Jheong, In-Pil Mo
J Vet Sci. 2019;20(5):.    doi: 10.4142/jvs.2019.20.e56.


Reference

1. Medina RA, Garcia-Sastre A. Influenza A viruses: new research developments. Nat Rev Microbiol. 2011; 9:590–603. PMID: 21747392.
Article
2. Tong S, Zhu X, Li Y, et al. New world bats harbor diverse influenza A viruses. PLoS Pathog. 2013; 9:e1003657. PMID: 24130481.
Article
3. Yoon SW, Webby RJ, Webster RG. Evolution and ecology of influenza A viruses. Curr Top Microbiol Immunol. 2014; 385:359–375. PMID: 24990620.
Article
4. Kim YI, Pascua PN, Kwon HI, et al. Pathobiological features of a novel, highly pathogenic avian influenza A(H5N8) virus. Emerg Microbes Infect. 2014; 3:e75. PMID: 26038499.
Article
5. Gu M, Zhao G, Zhao K, et al. Novel variants of clade 2.3.4 highly pathogenic avian influenza A(H5N1) viruses, China. Emerg Infect Dis. 2013; 19:2021–2024. PMID: 24274396.
Article
6. Pasick J, Berhane Y, Joseph T, et al. Reassortant highly pathogenic influenza A H5N2 virus containing gene segments related to Eurasian H5N8 in British Columbia, Canada, 2014. Sci Rep. 2015; 5:9484. PMID: 25804829.
Article
7. DeJesus E, Costa-Hurtado M, Smith D, et al. 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. PMID: 27632565.
Article
8. Si YJ, Lee IW, Kim EH, et al. Genetic characterisation of novel, highly pathogenic avian influenza (HPAI) H5N6 viruses isolated in birds, South Korea, November 2016. Euro Surveill. 2017; 22:30434. PMID: 28079520.
Article
9. Torremorell M, Alonso C, Davies PR, et al. Investigation into the airborne dissemination of H5N2 highly pathogenic avian influenza virus during the 2015 spring outbreaks in the midwestern United States. Avian Dis. 2016; 60:637–643. PMID: 27610723.
Article
10. Stoute S, Chin R, Crossley B, et al. Highly pathogenic Eurasian H5N8 avian influenza outbreaks in two commercial poultry flocks in California. Avian Dis. 2016; 60:688–693. PMID: 27610732.
Article
11. Adlhoch C, Brown IH, Angelova SG, et al. Highly pathogenic avian influenza A(H5N8) outbreaks: protection and management of exposed people in Europe, 2014/15 and 2016. Euro Surveill. 2016; 21:30419. PMID: 27983512.
Article
12. Kaplan BS, Russier M, Jeevan T, et al. Novel highly pathogenic avian A(H5N2) and A(H5N8) influenza viruses of clade 2.3.4.4 from north America have limited capacity for replication and transmission in mammals. mSphere. 2016; 1:e00003–e00016. PMID: 27303732.
Article
13. Kwon JH, Lee DH, Swayne DE, et al. 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. PMID: 28240976.
Article
14. Lee EK, Song BM, Lee YN, et al. Multiple novel H5N6 highly pathogenic avian influenza viruses, South Korea, 2016. Infect Genet Evol. 2017; 51:21–23. PMID: 28284997.
Article
15. Sonnberg S, Webby RJ, Webster RG. Natural history of highly pathogenic avian influenza H5N1. Virus Res. 2013; 178:63–77. PMID: 23735535.
Article
16. de Vries E, Guo H, Dai M, Rottier PJ, van Kuppeveld FJ, de Haan CA. Rapid emergence of highly pathogenic avian influenza subtypes from asubtype H5N1 hemagglutinin variant. Emerg Infect Dis. 2015; 21:842–846. PMID: 25897518.
17. Abolnik C. Evolution of H5 highly pathogenic avian influenza: sequence data indicate stepwise changes in the cleavage site. Arch Virol. 2017; 3. 30. [Epub]. DOI: 10.1007/s00705-017-3337-x.
Article
18. Lee CW, Suarez DL, Tumpey TM, et al. Characterization of highly pathogenic H5N1 avian influenza A viruses isolated from South Korea. J Virol. 2005; 79:3692–3702. PMID: 15731263.
Article
19. Yoon H, Park CK, Nam HM, Wee SH. Virus spread pattern within infected chicken farms using regression model: the 2003-2004 HPAI epidemic in the Republic of Korea. J Vet Med B Infect Dis Vet Public Health. 2005; 52:428–431. PMID: 16364017.
Article
20. Kim HR, Park CK, Lee YJ, et al. An outbreak of highly pathogenic H5N1 avian influenza in Korea, 2008. Vet Microbiol. 2010; 141:362–366. PMID: 19800184.
Article
21. Lee YJ, Choi YK, Kim YJ, et al. Highly pathogenic avian influenza virus (H5N1) in domestic poultry and relationship with migratory birds, South Korea. Emerg Infect Dis. 2008; 14:487–490. PMID: 18325269.
Article
22. Kim HR, Lee YJ, Park CK, et al. Highly pathogenic avian influenza (H5N1) outbreaks in wild birds and poultry, South Korea. Emerg Infect Dis. 2012; 18:480–483. PMID: 22377052.
Article
23. Jeong J, Kang HM, Lee EK, et al. 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. PMID: 25192767.
Article
24. Lee YJ, Kang HM, Lee EK, et al. Novel reassortant influenza A(H5N8) viruses, South Korea, 2014. Emerg Infect Dis. 2014; 20:1087–1089. PMID: 24856098.
Article
25. 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. PMID: 28316230.
Article
26. 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. PMID: 27738169.
27. Kwon JH, Lee DH, Swayne DE, et al. Highly pathogenic avian influenza A(H5N8) viruses reintroduced into South Korea by migratory waterfowl, 2014-2015. Emerg Infect Dis. 2016; 22:507–510. PMID: 26890406.
Article
28. Kang HM, Lee EK, Song BM, et al. Experimental infection of mandarin duck with highly pathogenic avian influenza A (H5N8 and H5N1) viruses. Vet Microbiol. 2017; 198:59–63. PMID: 28062008.
Article
29. Lee MS, Chen LH, Chen YP, et al. Highly pathogenic avian influenza viruses H5N2, H5N3, and H5N8 in Taiwan in 2015. Vet Microbiol. 2016; 187:50–57. PMID: 27066708.
Article
30. Short KR, Richard M, Verhagen JH, et al. One health, multiple challenges: the inter-species transmission of influenza A virus. One Health. 2015; 1:1–13. PMID: 26309905.
Article
31. 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. PMID: 25212611.
Article
32. Su S, Bi Y, Wong G, Gray GC, Gao GF, Li S. Epidemiology, evolution, and recent outbreaks of avian influenza virus in China. J Virol. 2015; 89:8671–8676. PMID: 26063419.
Article
33. Jeong J, Woo C, Ip HS, et al. Identification of two novel reassortant avian influenza a (H5N6) viruses in whooper swans in Korea, 2016. Virol J. 2017; 14:60. PMID: 28327168.
Article
34. Jiang H, Wu P, Uyeki TM, et al. Preliminary epidemiologic assessment of human infections with highly pathogenic avian influenza A(H5N6) virus, China. Clin Infect Dis. 2017; 4. 12. [Epub]. DOI: 10.1093/cid/cix334.
Article
35. Neher RA, Russell CA, Shraiman BI. Predicting evolution from the shape of genealogical trees. Elife. 2014; 3:DOI: 10.7554/eLife.03568.
Article
36. Gao R, Cao B, Hu Y, et al. Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med. 2013; 368:1888–1897. PMID: 23577628.
37. Uyeki TM. Human infection with highly pathogenic avian influenza A (H5N1) virus: review of clinical issues. Clin Infect Dis. 2009; 49:279–290. PMID: 19522652.
Article
38. Check E. Avian flu special: is this our best shot? Nature. 2005; 435:404–406. PMID: 15917769.
39. Chen H. H5N1 avian influenza in China. Sci China C Life Sci. 2009; 52:419–427. PMID: 19471864.
Article
40. Webby RJ, Perez DR, Coleman JS, et al. Responsiveness to a pandemic alert: use of reverse genetics for rapid development of influenza vaccines. Lancet. 2004; 363:1099–1103. PMID: 15064027.
Article
41. Tian G, Zhang S, Li Y, et al. Protective efficacy in chickens, geese and ducks of an H5N1-inactivated vaccine developed by reverse genetics. Virology. 2005; 341:153–162. PMID: 16084554.
Article
42. Capua I, Cattoli G. Prevention and control of highly pathogenic avian influenza with particular reference to H5N1. Virus Res. 2013; 178:114–120. PMID: 23611921.
Article
43. 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.
44. Zeng X, Chen P, Liu L, et al. Protective Efficacy of an H5N1 inactivated vaccine against challenge with lethal H5N1, H5N2, H5N6, and H5N8 influenza viruses in chickens. Avian Dis. 2016; 60(1 Suppl):253–255. PMID: 27309064.
Article
45. Choi Y, Chang J. Viral vectors for vaccine applications. Clin Exp Vaccine Res. 2013; 2:97–105. PMID: 23858400.
Article
46. Niqueux E, Guionie O, Amelot M, Jestin V. Prime-boost vaccination with recombinant H5-fowlpox and Newcastle disease virus vectors affords lasting protection in SPF Muscovy ducks against highly pathogenic H5N1 influenza virus. Vaccine. 2013; 31:4121–4128. PMID: 23845804.
Article
47. Pantin-Jackwood MJ, Kapczynski DR, DeJesus E, et al. Efficacy of a recombinant Turkey herpesvirus H5 vaccine against challenge with H5N1 clades 1.1.2 and 2.3.2.1 highly pathogenic avian influenza viruses in domestic ducks (Anas platyrhynchos domesticus). Avian Dis. 2016; 60:22–32. PMID: 26953940.
Article
48. Wang J, Ge A, Xu M, et al. Construction of a recombinant duck enteritis virus (DEV) expressing hemagglutinin of H5N1 avian influenza virus based on an infectious clone of DEV vaccine strain and evaluation of its efficacy in ducks and chickens. Virol J. 2015; 12:126. PMID: 26263920.
Article
49. Chen H. Avian influenza vaccination: the experience in China. Rev Sci Tech. 2009; 28:267–274. PMID: 19618631.
Article
50. van den Berg T, Lambrecht B, Marche S, Steensels M, Van Borm S, Bublot M. Influenza vaccines and vaccination strategies in birds. Comp Immunol Microbiol Infect Dis. 2008; 31:121–165. PMID: 17889937.
Article
51. Kim SH, Samal SK. Newcastle disease virus as a vaccine vector for development of human and veterinary vaccines. Viruses. 2016; 8:E183. PMID: 27384578.
Article
52. Ge J, Deng G, Wen Z, et al. Newcastle disease virus-based live attenuated vaccine completely protects chickens and mice from lethal challenge of homologous and heterologous H5N1 avian influenza viruses. J Virol. 2007; 81:150–158. PMID: 17050610.
Article
53. Park JK, Lee DH, Yuk SS, et al. Virus-like particle vaccine confers protection against a lethal newcastle disease virus challenge in chickens and allows a strategy of differentiating infected from vaccinated animals. Clin Vaccine Immunol. 2014; 21:360–365. PMID: 24403523.
Article
54. Stachyra A, Gora-Sochacka A, Sirko A. DNA vaccines against influenza. Acta Biochim Pol. 2014; 61:515–522. PMID: 25210719.
Article
55. Jiang Y, Yu K, Zhang H, et al. Enhanced protective efficacy of H5 subtype avian influenza DNA vaccine with codon optimized HA gene in a pCAGGS plasmid vector. Antiviral Res. 2007; 75:234–241. PMID: 17451817.
Article
56. Laddy DJ, Yan J, Corbitt N, Kobasa D, Kobinger GP, Weiner DB. Immunogenicity of novel consensus-based DNA vaccines against avian influenza. Vaccine. 2007; 25:2984–2989. PMID: 17306909.
Article
57. Stachyra A, Redkiewicz P, Kosson P, et al. Codon optimization of antigen coding sequences improves the immune potential of DNA vaccines against avian influenza virus H5N1 in mice and chickens. Virol J. 2016; 13:143. PMID: 27562235.
Article
58. Smith LR, Wloch MK, Ye M, et al. Phase 1 clinical trials of the safety and immunogenicity of adjuvanted plasmid DNA vaccines encoding influenza A virus H5 hemagglutinin. Vaccine. 2010; 28:2565–2572. PMID: 20117262.
Article
59. Shen X, Soderholm J, Lin F, et al. Influenza A vaccines using linear expression cassettes delivered via electroporation afford full protection against challenge in a mouse model. Vaccine. 2012; 30:6946–6954. PMID: 22406460.
Article
60. Saczynska V, Romanik A, Florys K, et al. A novel hemagglutinin protein produced in bacteria protects chickens against H5N1 highly pathogenic avian influenza viruses by inducing H5 subtype-specific neutralizing antibodies. PLoS One. 2017; 12:e0172008. PMID: 28212428.
Article
61. Wu CY, Yeh YC, Yang YC, et al. Mammalian expression of virus-like particles for advanced mimicry of authentic influenza virus. PLoS One. 2010; 5:e9784. PMID: 20339535.
Article
62. Nwe N, He Q, Damrongwatanapokin S, et al. Expression of hemagglutinin protein from the avian influenza virus H5N1 in a baculovirus/insect cell system significantly enhanced by suspension culture. BMC Microbiol. 2006; 6:16. PMID: 16504108.
Article
63. Ernst WA, Kim HJ, Tumpey TM, et al. Protection against H1, H5, H6 and H9 influenza A infection with liposomal matrix 2 epitope vaccines. Vaccine. 2006; 24:5158–5168. PMID: 16713037.
Article
64. Crawford J, Wilkinson B, Vosnesensky A, et al. Baculovirus-derived hemagglutinin vaccines protect against lethal influenza infections by avian H5 and H7 subtypes. Vaccine. 1999; 17:2265–2274. PMID: 10403594.
Article
65. Cornelissen LA, de Vries RP, de Boer-Luijtze EA, Rigter A, Rottier PJ, de Haan CA. A single immunization with soluble recombinant trimeric hemagglutinin protects chickens against highly pathogenic avian influenza virus H5N1. PLoS One. 2010; 5:e10645. PMID: 20498717.
Article
66. Saczynska V. Influenza virus hemagglutinin as a vaccine antigen produced in bacteria. Acta Biochim Pol. 2014; 61:561–572. PMID: 25195143.
Article
67. Liu G, Zhang F, Shi J, et al. A subunit vaccine candidate derived from a classic H5N1 avian influenza virus in China protects fowls and BALB/c mice from lethal challenge. Vaccine. 2013; 31:5398–5404. PMID: 24055355.
Article
68. Lamb RA, Zebedee SL, Richardson CD. Influenza virus M2 protein is an integral membrane protein expressed on the infected-cell surface. Cell. 1985; 40:627–633. PMID: 3882238.
Article
69. Pinto LH, Lamb RA. The M2 proton channels of influenza A and B viruses. J Biol Chem. 2006; 281:8997–9000. PMID: 16407184.
Article
70. Neirynck S, Deroo T, Saelens X, Vanlandschoot P, Jou WM, Fiers W. A universal influenza A vaccine based on the extracellular domain of the M2 protein. Nat Med. 1999; 5:1157–1163. PMID: 10502819.
Article
71. Hughey PG, Roberts PC, Holsinger LJ, Zebedee SL, Lamb RA, Compans RW. Effects of antibody to the influenza A virus M2 protein on M2 surface expression and virus assembly. Virology. 1995; 212:411–421. PMID: 7571410.
Article
72. Zhao G, Lin Y, Du L, et al. An M2e-based multiple antigenic peptide vaccine protects mice from lethal challenge with divergent H5N1 influenza viruses. Virol J. 2010; 7:9. PMID: 20082709.
Article
73. Elaish M, Ngunjiri JM, Ali A, et al. Supplementation of inactivated influenza vaccine with norovirus P particle-M2e chimeric vaccine enhances protection against heterologous virus challenge in chickens. PLoS One. 2017; 12:e0171174. PMID: 28151964.
Article
74. Dabaghian M, Latify AM, Tebianian M, et al. Vaccination with recombinant 4 x M2e.HSP70c fusion protein as a universal vaccine candidate enhances both humoral and cell-mediated immune responses and decreases viral shedding against experimental challenge of H9N2 influenza in chickens. Vet Microbiol. 2014; 174:116–126. PMID: 25293397.
75. De Filette M, Martens W, Smet A, et al. Universal influenza A M2e-HBc vaccine protects against disease even in the presence of pre-existing anti-HBc antibodies. Vaccine. 2008; 26:6503–6507. PMID: 18835315.
Article
76. Wu F, Yuan XY, Huang WS, Chen YH. Heterosubtypic protection conferred by combined vaccination with M2e peptide and split influenza vaccine. Vaccine. 2009; 27:6095–6101. PMID: 19056447.
Article
77. Ndifon W, Wingreen NS, Levin SA. Differential neutralization efficiency of hemagglutinin epitopes, antibody interference, and the design of influenza vaccines. Proc Natl Acad Sci U S A. 2009; 106:8701–8706. PMID: 19439657.
Article
78. Uranowska K, Tyborowska J, Jurek A, Szewczyk B, Gromadzka B. Hemagglutinin stalk domain from H5N1 strain as a potentially universal antigen. Acta Biochim Pol. 2014; 61:541–550. PMID: 25210720.
Article
79. Ekiert DC, Wilson IA. Broadly neutralizing antibodies against influenza virus and prospects for universal therapies. Curr Opin Virol. 2012; 2:134–141. PMID: 22482710.
Article
80. Nayak B, Kumar S, DiNapoli JM, et al. Contributions of the avian influenza virus HA, NA, and M2 surface proteins to the induction of neutralizing antibodies and protective immunity. J Virol. 2010; 84:2408–2420. PMID: 20032181.
Article
81. Steel J, Lowen AC, Wang TT, et al. Influenza virus vaccine based on the conserved hemagglutinin stalk domain. MBio. 2010; 1:e00018–e00010. PMID: 20689752.
Article
82. Suguitan AL Jr, Cheng X, Wang W, Wang S, Jin H, Lu S. Influenza H5 hemagglutinin DNA primes the antibody response elicited by the live attenuated influenza A/Vietnam/1203/2004 vaccine in ferrets. PLoS One. 2011; 6:e21942. PMID: 21760928.
Article
Full Text Links
  • CEVR
Actions
Cited
CITED
export Copy
Close
Share
  • Twitter
  • Facebook
Similar articles
Copyright © 2024 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: koreamed@kamje.or.kr