Pathogenicity and vaccine efficacy of different clades of Asian H5N1 avian influenza A viruses in domestic ducks

Journal of Virology

Volumn 82, Issue 22, 2008, Pages 11374-11382

  Kim, Jeong Ki ^a   Seiler, Patrick ^a   Forrest, Heather L ^a   Khalenkov, Alexey M ^a   Franks, John ^a   Kumar, Mahesh ^b   Karesh, William B ^c   Gilbert, Martin ^c   Sodnomdarjaa, R ^d   Douangngeun, Bounlom ^e   Govorkova, Elena A ^a   Webster, Robert G ^a,f  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b ZOETIS   (United States)

^c WILDLIFE CONSERVATION SOCIETY   (United States)

^d State Central Veterinary Laboratory   (Mongolia)

^e National Animal Health Centre   (Laos)

^f UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INACTIVATED VIRUS VACCINE; INFLUENZA VACCINE; NEUTRALIZING ANTIBODY; PLACEBO; VIRUS HEMAGGLUTININ; IMMUNOLOGICAL ADJUVANT; INACTIVATED VACCINE; OIL; VIRUS ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; ASIA; AVIAN INFLUENZA; CLADISTICS; CLOACA; CONTROLLED STUDY; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG EFFICACY; DUCK; EMULSION; IMMUNOGENICITY; INFLUENZA VACCINATION; INFLUENZA VIRUS A H5N1; LETHALITY; MORBIDITY; MORTALITY; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; SEROLOGY; TRACHEA; VIRUS HEMAGGLUTINATION; VIRUS SHEDDING; ANIMAL; BLOOD; DOMESTIC ANIMAL; HEMAGGLUTINATION INHIBITION TEST; IMMUNOLOGY; SURVIVAL; VIROLOGY;

ANAS; ANAS PLATYRHYNCHOS; ANATIDAE; AVES; AVIAN INFLUENZA VIRUS; INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANIMALS, DOMESTIC; ANTIBODIES, VIRAL; ASIA; CLOACA; DUCKS; HEMAGGLUTINATION INHIBITION TESTS; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA IN BIRDS; INFLUENZA VACCINES; OILS; SURVIVAL ANALYSIS; TRACHEA; VACCINES, INACTIVATED; VIRUS SHEDDING;

EID: 55549087911     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01176-08     Document Type: Article

References (50)

1. Bender, C., H. Hall, J. Huang, A. Klimov, N. Cox, A. Hay, V. Gregory, K. Cameron, W. Lim, and K. Subbarao. 1999. Characterization of the surface proteins of influenza A (H5N1) viruses isolated from humans in 1997-1998. Virology 254:115-123.
2. Capua, I., and S. Marangon. 2006. Control of avian influenza in poultry. Emerg. Infect. Dis. 12:1319-1324.
3. Chen, H., G. Deng, Z. Li, G. Tian, Y. Li, P. Jiao, L. Zhang, Z. Liu, R. G. Webster, and K. Yu. 2004. The evolution of H5N1 influenza viruses in ducks in southern China. Proc. Natl. Acad. Sci. USA 101:10452-10457.
4. Claas, E. C. J., A. D. M. E. Osterhaus, R. van Beek, J. C. De Jong, G. F. Rimmelzwaan, D. A. Senne, S. Krauss, K. F. Shortridge, and R. G. Webster. 1998. Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus. Lancet 351:472-477.
5. Cooley, A. J., H. Van Campen, M. S. Philpott, B. C. Easterday, and V. S. Hinshaw. 1989. Pathological lesions in the lungs of ducks infected with influenza A viruses. Vet. Pathol. 26:1-5.
6. De Jong, J. C., E. C. J. Claas, A. D. M. E. Osterhaus, R. G. Webster, and W. L. Lim. 1997. A pandemic warning? Nature 389:554.
7. Ellis, T. M., C. Y. Leung, M. K. Chow, L. A. Bissett, W. Wong, Y. Guan, and J. S. Malik Peiris. 2004. Vaccination of chickens against H5N1 avian influenza in the face of an outbreak interrupts virus transmission. Avian Pathol. 33:405-412.
8. Epstein, S. L., C.-Y. Lo, J. A. Misplon, and J. R. Bennink. 1998. Mechanism of protective immunity against influenza virus infection in mice without antibodies. J. Immunol. 160:322-327.
9. Gilbert, M., P. Chaitaweesub, T. Parakamawongsa, S. Premashthira, T. Tiensin, W. Kalpravidh, H. Wagner, and J. Slingenbergh. 2006. Free-grazing ducks and highly pathogenic avian influenza, Thailand. Emerg. Infect. Dis. 12:227-234.
10. Govorkova, E. A., R. J. Webby, J. Humberd, J. P. Seiler, and R. G. Webster. 2006. Immunization with reverse-genetics-produced H5N1 influenza vaccine protects ferrets against homologous and heterologous challenge. J. Infect. Dis. 194:159-167.
11. Guan, Y., M. Peiris, K. F. Kong, K. C. Dyrting, T. M. Ellis, T. Sit, L. J. Zhang, and K. F. Shortridge. 2002. H5N1 influenza viruses isolated from geese in Southeastern China: evidence for genetic reassortment and interspecies transmission to ducks. Virology 292:16-23.
12. Hien, T. T., N. T. Liem, N. T. Dung, L. T. San, P. P. Mai, N. van V. Chau, P. T. Suu, V. C. Dong, L. T. Q. Mai, N. T. Thi, D. B. Khoa, L. P. Phat, N. T. Truong, H. T. Long, C. V. Tung, L. T. Giang, N. D. Tho, L. H. Nga, N. T. K. Tien, L. H. San, L. V. Tuan, C. Dolecek, T. T. Thanh, M. de Jong, C. Schultsz, P. Cheng, W. Lim, P. Horby, et al. 2004. Avian influenza A (H5N1) in 10 patients in Vietnam. N. Engl. J. Med. 350:1179-1188.
13. Hinshaw, V. S., W. J. Bean, J. Geraci, P. Fiorelli, G. Early, and R. G. Webster. 1986. Characterization of two influenza A viruses from a pilot whale. J. Virol. 58:655-656.
14. Hoffmann, E., A. S. Lipatov, R. J. Webby, E. A. Govorkova, and R. G. Webster. 2005. Role of specific hemagglutinin amino acids in the immunogenicity and protection of H5N1 influenza virus vaccines. Proc. Natl. Acad. Sci. USA 102:12915-12920.
15. Hoffmann, E., G. Neumann, Y. Kawaoka, G. Hobom, and R. G. Webster. 2000. A DNA transfection system for generation of influenza A virus from eight plasmids. Proc. Natl. Acad. Sci. USA 97:6108-6113.
16. Hoffmann, E., S. Krauss, D. Perez, R. Webby, and R. G. Webster. 2002. Eight-plasmid system for rapid generation of influenza virus vaccines. Vaccine 20:3165-3170.
17. Hulse-Post, D. J., K. M. Sturm-Ramirez, J. Humberd, P. Seiler, E. A. Govorkova, S. Krauss, C. Scholtissek, P. Puthavathana, C. Buranathai, T. D. Nguyen, H. T. Long, T. S. P. Naipospos, H. Chen, T. M. Ellis, Y. Guan, J. S. M. Peiris, and R. G. Webster. 2005. Role of domestic ducks in the propagation and biological evolution of highly pathogenic H5N1 influenza viruses in Asia. Proc. Natl. Acad. Sci. USA 102:10682-10687.
18. Karunakaran, D., J. A. Newman, D. A. Halvorson, and A. Abraham. 1987. Evaluation of inactivated influenza vaccines in market turkeys. Avian Dis. 31:498-503.
19. Kaverin, N. V., I. A. Rudneva, E. A. Govorkova, T. A. Timofeeva, A. A. Shilov, K. S. Kochergin-Nikitsky, P. S. Krylov, and R. G. Webster. 2007. Epitope mapping of the hemagglutinin molecule of a highly pathogenic H5N1 influenza virus by using monoclonal antibodies. J. Virol. 81:12911-12917.
20. Keawcharoen, J., K. Oraveerakul, T. Kuiken, R. A. M. Fouchier, A. Amonsin, S. Payungporn, S. Noppornpanth, S. Wattanodorn, A. Theamboonlers, R. Tantilertcharoen, R. Pattanarangsan, N. Arya, P. Ratanakorn, D. M. E. Osterhaus, and Y. Poovorawan. 2004. Avian influenza H5N1 in tigers and leopards. Emerg. Infect. Dis. 10:2189-2191.
21. Kida, H., L. E. Brown, and R. G. Webster. 1982. Biological activity of monoclonal antibodies to operationally defined antigenic regions on the hemagglutinin molecule of A/Seal/Massachusetts/1/80 (H7N7) influenza virus. Virology 122:38-47.
22. Li, K. S., Y. Guan, J. Wang, G. J. D. Smith, K. M. Xu, L. Duan, A. P. Rahardjo, P. Puthavathana, C. Buranathai, T. D. Nguyen, A. T. S. Estoepangestie, A. Chaisingh, P. Auewarakul, H. T. Long, N. T. H. Hanh, R. J. Webby, L. L. M. Poon, H. Chen, K. F. Shortridge, K. Y. Yuen, R. G. Webster, and J. S. M. Peiris. 2004. Genesis of a highly pathogenic and potentially pandemic H5N1 influenza virus in eastern Asia. Nature 430:209-213.
23. Liu, M., J. M. Wood, T. Ellis, S. Krauss, P. Seiler, C. Johnson, E. Hoffmann, J. Humberd, D. Hulse, Y. Zhang, R. G. Webster, and D. R. Perez. 2003. Preparation of a standardized, efficacious agricultural H5N3 vaccine by reverse genetics. Virology 314:580-590.
24. Olsen, B., V. J. Munster, A. Wallensten, J. Waldenström, A. D. M. E. Osterhaus, and R. A. M. Fouchier. 2006. Global patterns of influenza a virus in wild birds. Science 312:384-388.
25. Palmer, D. E., M. T. Colman, W. R. Dowdle, and G. C. Schild. 1975. Advanced laboratory techniques for influenza diagnosis. Immunol. Ser. 6:51-52.
26. Pantin-Jackwood, M. J., and D. E. Swayne. 2007. Pathobiology of Asian highly pathogenic avian influenza H5N1 virus infections in ducks. Avian Dis. 51:250-259.
27. Peiris, J. S. M., W. C. Yu, C. W. Leung, C. Y. Cheung, W. F. Ng, J. M. Nicholls, T. K. Ng, K. H. Chan, S. T. Lai, W. L. Lim, K. Y. Yuen, and Y. Guan. 2004. Re-emergence of fatal human influenza A subtype H5N1 disease. Lancet 363:617-619.
28. Pensaert, M., K. Ottis, J. Vandeputte, M. M. Kaplan, and P. A. Bachmann. 1981. Evidence for the natural transmission of influenza A virus from wild ducts to swine and its potential importance for man. Bull. W. H. O. 59:75-78.
29. Perkins, L. E., and D. E. Swayne. 2002. Pathogenicity of a Hong Kong-origin H5N1 highly pathogenic avian influenza virus for emus, geese, ducks, and pigeons. Avian Dis. 46:53-63.
30. Puthavathana, P., P. Auewarakul, P. C. Charoenying, K. Sangsiriwut, P. Pooruk, K. Boonnak, R. Khanyok, P. Thawachsupa, R. Kijphati, and P. Sawanpanyalert. 2005. Molecular characterization of the complete genome of human influenza H5N1 virus isolates from Thailand. J. Gen. Virol. 86:423-433.
31. Reed, L. J., and H. Muench. 1938. A simple method for estimating fifty percent endpoints. Am. J. Epidemiol. 27:493-497.
32. Scholtissek, C., H. Bürger, P. A. Bachmann, and C. Hannoun. 1983. Genetic relatedness of hemagglutinins of the H1 subtype of influenza A viruses isolated from swine and birds. Virology 129:521-523.
33. Sturm-Ramirez, K. M., D. J. Hulse-Post, E. A. Govorkova, J. Humberd, P. Seiler, P. Puthavathana, C. Buranathai, T. D. Nguyen, A. Chaisingh, H. T. Long, T. S. P. Naipospos, H. Chen, T. M. Ellis, Y. Guan, J. S. M. Peiris, and R. G. Webster. 2005. Are ducks contributing to the endemicity of highly pathogenic H5N1 influenza virus in Asia? J. Virol. 79:11269-11279.
34. Sturm-Ramirez, K. M., T. Ellis, B. Bousfield, L. Bissett, K. Dyrting, J. E. Rehg, L. Poon, Y. Guan, M. Peiris, and R. G. Webster. 2004. Reemerging H5N1 influenza viruses in Hong Kong in 2002 are highly pathogenic to ducks. J. Virol. 78:4892-4901.
35. Suarez, D. L. 2000. Evolution of avian influenza viruses. Vet. Microbiol. 74:15-27.
36. Subbarao, K., A. Klimov, J. Katz, H. Regnery, W. Lim, H. Hall, M. Perdue, D. Swayne, C. Bender, J. Huang, M. Hemphill, T. Rowe, M. Shaw, X. Xu, K. Fukuda, and N. Cox. 1998. Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness. Science 279:393-396.
37. Swayne, D. E. 2008. Avian influenza vaccines and therapies for poultry. Comp. Immunol. Microbiol. Infect. Dis. doi:10.1016/j.cimid.2008.01.006.
38. Swayne, D. E., and D. L. Suarez. 2000. Highly pathogenic avian influenza. Rev. Sci. Technol. 19:463-482.
39. Swayne, D. E., and M. Pantin-Jackwood. 2006. Pathogenicity of avian influenza viruses in poultry. Dev. Biol. 124:61-67.
40. Swayne, D. E., J. R. Beck, M. L. Perdue, and C. W. Beard. 2001. Efficacy of vaccines in chickens against highly pathogenic Hong Kong H5N1 avian influenza. Avian Dis. 45:355-365.
41. Thomas, P. G., R. Keating, D. J. Hulse-Post, and P. C. Doherty. 2006. Cell-mediated protection in influenza infection. Emerg. Infect. Dis. 12:48-54.
42. Tian, G., S. Zhang, Y. Li, Z. Bu, P. Liu, J. Zhou, C. Li, J. Shi, K. Yu, and H. Chen. 2005. Protective efficacy in chickens, geese and ducks of an H5N1-inactivated vaccine developed by reverse genetics. Virology 341:153-162.
43. Timoney, P. J. 1996. Equine influenza. Comp. Immunol. Microbiol. Infect. Dis. 19:205-211.
44. Tumpey, T. M., D. L. Suarez, L. E. Perkins, D. A. Senne, J. Lee, Y. J. Lee, I. P. Mo, H. W. Sung, and D. E. Swayne. 2003. Evaluation of a highpathogenicity H5N1 avian influenza A virus isolated from duck meat. Avian Dis. 47:951-955.
45. Villarreal, C. L. 2006. Control and eradication strategies of avian influenza in Mexico. Dev. Biol. 124:125-126.
46. Webster, R. G., R. J. Webby, E. Hoffmann, J. Rodenberg, M. Kumar, H-J. Chu, P. Seiler, S. Krauss, and T. Songserm. 2006. The immunogenicity and efficacy against H5N1 challenge of reverse genetics-derived H5N3 influenza vaccine in ducks and chickens. Virology 351:303-311.
47. Webster, R. G., V. S. Hinshaw, W. J. Bean, K. L. Van Wyke, J. R. Geraci, D. J. St. Aubin, and G. Petursson. 1981. Characterization of an influenza A virus from seals. Virology 113:712-724.
48. Webster, R. G., W. J. Bean, O. T. Gorman, T. M. Chambers, and Y. Kawaoka. 1992. Evolution and ecology of influenza A viruses. Microbiol. Rev. 56:152-179.
49. Wood, J. M., Y. Kawaoka, L. A. Newberry, E. Bordwell, and R. G. Webster. 1985. Standardization of inactivated H5N2 influenza vaccine and efficacy against lethal A/Chicken/Pennsylvania/1370/83 infection. Avian Dis. 29:867-872.
50. Xu, X., K. Subbarao, N. J. Cox, and Y. Guo. 1999. Genetic characterization of the pathogenic influenza A/Goose/Guangdong/1/96 (H5N1) virus: similarity of its hemagglutinin gene to those of H5N1 viruses from the 1997 outbreaks in Hong Kong. Virology 261:15-19.