Clin Exp Vaccine Res.  2016 Jul;5(2):117-124. 10.7774/cevr.2016.5.2.117.

Influenza virus vaccine for neglected hosts: horses and dogs

Affiliations
  • 1College of Pharmacy, Korea University, Sejong, Korea. sds1@korea.ac.kr
  • 2Research Unit, Green Cross Veterinary Products, Yongin, Korea.

Abstract

This study provides information regarding vaccine research and the epidemiology of influenza virus in neglected hosts (horses and dogs). Equine influenza virus (EIV) causes a highly contagious disease in horses and other equids, and outbreaks have occurred worldwide. EIV has resulted in costly damage to the horse industry and has the ability of cross the host species barrier from horses to dogs. Canine influenza is a virus of equine or avian origin and infects companion animals that live in close contact with humans; this results in possible exposure to the seasonal epizootic influenza virus. There have been case reports of genetic reassortment between human and canine influenza viruses, which results in high virulence and the ability of transmission to ferrets. This emphasizes the need for vaccine research on neglected hosts to update knowledge on current strains and to advance technology for controlling influenza outbreaks for public health.

Keyword

Influenza A virus; H3N8 subtype; H3N2 subtype; Disease transmission; Infectious; Influenza vaccine

MeSH Terms

Animals
Disease Outbreaks
Dogs*
Epidemiology
Ferrets
Horses*
Humans
Influenza A virus
Influenza Vaccines
Influenza, Human*
Orthomyxoviridae*
Pets
Public Health
Seasons
Virulence
Influenza Vaccines

Figure

  • Fig. 1 Increased number influenza vaccine patents according to each animal species from 1993 to 2012. Patents for canine influenza virus occupied less than 5% of major veterinary influenza vaccines (A), and showed the highest rate of increase from 2002 (B). Equine influenza virus vaccines presented a downward trend from 2007 (B).

  • Fig. 2 Ratio of patents for influenza vaccine technology according to each animal species in six major intellectual property offices. United States leads in applications for patents for equine influenza virus vaccines. China and Japan had a high number of patents for equine influenza virus vaccines. KIPO, Korean Intellectual Property Office; USPTO, United States Patent and Trademark Office; JPO, Japan Patent Office; EPO, European Patent Office; SIPO, State Intellectual Property Office; WIPO, The World Intellectual Property Organization.

  • Fig. 3 Distribution of patent applicants of animal influenza vaccines. Merial Ltd. presented balanced patent applications for all veterinary species. The University of Pittsburgh and Pfizer Inc. applied for the highest number of patents for equine influenza virus and canine influenza virus vaccines, respectively.


Reference

1. Morens DM, Taubenberger JK. An avian outbreak associated with panzootic equine influenza in 1872: an early example of highly pathogenic avian influenza? Influenza Other Respir Viruses. 2010; 4:373–377.
Article
2. Sovinova O, Tumova B, Pouska F, Nemec J. Isolation of a virus causing respiratory disease in horses. Acta Virol. 1958; 2:52–61.
3. Waddell GH, Teigland MB, Sigel MM. A new influenza virus associated with equine respiratory disease. J Am Vet Med Assoc. 1963; 143:587–590.
4. Webster RG. Are equine 1 influenza viruses still present in horses? Equine Vet J. 1993; 25:537–538.
Article
5. Watson J, Halpin K, Selleck P, et al. Isolation and characterisation of an H3N8 equine influenza virus in Australia, 2007. Aust Vet J. 2011; 89:Suppl 1. 35–37.
Article
6. Daly JM, Lai AC, Binns MM, Chambers TM, Barrandeguy M, Mumford JA. Antigenic and genetic evolution of equine H3N8 influenza A viruses. J Gen Virol. 1996; 77(Pt 4):661–671.
Article
7. Murcia PR, Baillie GJ, Stack JC, et al. Evolution of equine influenza virus in vaccinated horses. J Virol. 2013; 87:4768–4771.
Article
8. Karamendin K, Kydyrmanov A, Kasymbekov Y, et al. Continuing evolution of equine influenza virus in Central Asia, 2007-2012. Arch Virol. 2014; 159:2321–2327.
Article
9. Crawford PC, Dubovi EJ, Castleman WL, et al. Transmission of equine influenza virus to dogs. Science. 2005; 310:482–485.
Article
10. Payungporn S, Crawford PC, Kouo TS, et al. Influenza A virus (H3N8) in dogs with respiratory disease, Florida. Emerg Infect Dis. 2008; 14:902–908.
Article
11. Songserm T, Amonsin A, Jam-on R, et al. Fatal avian influenza A H5N1 in a dog. Emerg Infect Dis. 2006; 12:1744–1747.
Article
12. Maas R, Tacken M, Ruuls L, Koch G, van Rooij E, Stockhofe-Zurwieden N. Avian influenza (H5N1) susceptibility and receptors in dogs. Emerg Infect Dis. 2007; 13:1219–1221.
Article
13. Song D, Kang B, Lee C, et al. Transmission of avian influenza virus (H3N2) to dogs. Emerg Infect Dis. 2008; 14:741–746.
Article
14. Song D, Lee C, Kang B, et al. Experimental infection of dogs with avian-origin canine influenza A virus (H3N2). Emerg Infect Dis. 2009; 15:56–58.
Article
15. Sun Y, Sun S, Ma J, et al. Identification and characterization of avian-origin H3N2 canine influenza viruses in northern China during 2009-2010. Virology. 2013; 435:301–307.
Article
16. Bunpapong N, Nonthabenjawan N, Chaiwong S, et al. Genetic characterization of canine influenza A virus (H3N2) in Thailand. Virus Genes. 2014; 48:56–63.
Article
17. Song D, Moon HJ, An DJ, et al. A novel reassortant canine H3N1 influenza virus between pandemic H1N1 and canine H3N2 influenza viruses in Korea. J Gen Virol. 2012; 93(Pt 3):551–554.
Article
18. Kawaoka Y, Bean WJ, Webster RG. Evolution of the hemagglutinin of equine H3 influenza viruses. Virology. 1989; 169:283–292.
Article
19. Lai AC, Chambers TM, Holland RE Jr, et al. Diverged evolution of recent equine-2 influenza (H3N8) viruses in the Western Hemisphere. Arch Virol. 2001; 146:1063–1074.
Article
20. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol Rev. 1992; 56:152–179.
Article
21. Qi T, Guo W, Huang W, et al. Isolation and genetic characterization of H3N8 equine influenza virus from donkeys in China. Vet Microbiol. 2010; 144:455–460.
Article
22. Hayward JJ, Dubovi EJ, Scarlett JM, Janeczko S, Holmes EC, Parrish CR. Microevolution of canine influenza virus in shelters and its molecular epidemiology in the United States. J Virol. 2010; 84:12636–12645.
Article
23. Yang X, Liu C, Liu F, et al. Identification and genetic characterization of avian-origin H3N2 canine influenza viruses isolated from the Liaoning province of China in 2012. Virus Genes. 2014; 49:342–347.
Article
24. Ogilvie TH. Large animal internal medicine. Ames, IA: Blackwell Publishing;2005.
25. McGavin MD, Zachary JF. Pathologic basis of veterinary disease. St. Louis, MO: Mosby Elsevier;2007.
26. Wiley DC, Wilson IA, Skehel JJ. Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature. 1981; 289:373–378.
Article
27. Shors T. Understanding viruses. Sudbury, MA: Jones and Bartlett Publishers;2009.
28. Webster RG, Sharp GB, Claas EC. Interspecies transmission of influenza viruses. Am J Respir Crit Care Med. 1995; 152(4 Pt 2):S25–S30.
Article
29. Murphy BR, Sly DL, Tierney EL, et al. Reassortant virus derived from avian and human influenza A viruses is attenuated and immunogenic in monkeys. Science. 1982; 218:1330–1332.
Article
30. Na W, Lyoo KS, Song EJ, et al. Viral dominance of reassortants between canine influenza H3N2 and pandemic (2009) H1N1 viruses from a naturally co-infected dog. Virol J. 2015; 12:134.
Article
31. Gorman OT, Bean WJ, Kawaoka Y, Donatelli I, Guo YJ, Webster RG. Evolution of influenza A virus nucleoprotein genes: implications for the origins of H1N1 human and classical swine viruses. J Virol. 1991; 65:3704–3714.
Article
32. Daly JM, Blunden AS, Macrae S, et al. Transmission of equine influenza virus to English foxhounds. Emerg Infect Dis. 2008; 14:461–464.
Article
33. Kirkland PD, Finlaison DS, Crispe E, Hurt AC. Influenza virus transmission from horses to dogs, Australia. Emerg Infect Dis. 2010; 16:699–702.
Article
34. Songserm T, Amonsin A, Jam-on R, et al. Avian influenza H5N1 in naturally infected domestic cat. Emerg Infect Dis. 2006; 12:681–683.
Article
35. Giese M, Harder TC, Teifke JP, et al. Experimental infection and natural contact exposure of dogs with avian influenza virus (H5N1). Emerg Infect Dis. 2008; 14:308–310.
Article
36. Yin X, Zhao FR, Zhou DH, Wei P, Chang HY. Serological report of pandemic and seasonal human influenza virus infection in dogs in southern China. Arch Virol. 2014; 159:2877–2882.
37. Song D, Kim H, Na W, et al. Canine susceptibility to human influenza viruses (A/pdm 09H1N1, A/H3N2 and B). J Gen Virol. 2015; 96(Pt 2):254–258.
Article
38. Moon H, Hong M, Kim JK, et al. H3N2 canine influenza virus with the matrix gene from the pandemic A/H1N1 virus: infection dynamics in dogs and ferrets. Epidemiol Infect. 2015; 143:772–780.
Article
39. Lyoo KS, Na W, Yeom M, et al. Virulence of a novel reassortant canine H3N2 influenza virus in ferret, dog and mouse models. Arch Virol. 2016; 161:1915–1923.
Article
40. Yamanaka T, Nemoto M, Tsujimura K, Kondo T, Matsumura T. Interspecies transmission of equine influenza virus (H3N8) to dogs by close contact with experimentally infected horses. Vet Microbiol. 2009; 139:351–355.
Article
41. Paillot R. A systematic review of recent advances in equine influenza vaccination. Vaccines (Basel). 2014; 2:797–831.
42. Chambers TM, Holland RE, Tudor LR, et al. A new modified live equine influenza virus vaccine: phenotypic stability, restricted spread and efficacy against heterologous virus challenge. Equine Vet J. 2001; 33:630–636.
Article
43. Minke JM, Toulemonde CE, Coupier H, et al. Efficacy of a canarypox-vectored recombinant vaccine expressing the hemagglutinin gene of equine influenza H3N8 virus in the protection of ponies from viral challenge. Am J Vet Res. 2007; 68:213–219.
Article
44. Minke JM, Toulemonde CE, Dinic S, Cozette V, Cullinane A, Audonnet JC. Effective priming of foals born to immune dams against influenza by a canarypox-vectored recombinant influenza H3N8 vaccine. J Comp Pathol. 2007; 137:Suppl 1. S76–S80.
Article
45. Larson LJ, Henningson J, Sharp P, et al. Efficacy of the canine influenza virus H3N8 vaccine to decrease severity of clinical disease after cochallenge with canine influenza virus and Streptococcus equi subsp. zooepidemicus. Clin Vaccine Immunol. 2011; 18:559–564.
Article
46. Deshpande MS, Jirjis FF, Tubbs AL, et al. Evaluation of the efficacy of a canine influenza virus (H3N8) vaccine in dogs following experimental challenge. Vet Ther. 2009; 10:103–112.
47. Kang YM, Kim HM, Ku KB, Park EH, Yum J, Seo SH. H3N2 canine influenza virus causes severe morbidity in dogs with induction of genes related to inflammation and apoptosis. Vet Res. 2013; 44:92.
Article
48. Lee C, Jung K, Oh J, et al. Protective efficacy and immunogenicity of an inactivated avian-origin H3N2 canine influenza vaccine in dogs challenged with the virulent virus. Vet Microbiol. 2010; 143:184–188.
Article
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