Experimental challenge and pathology of highly pathogenic avian influenza virus H5N1 in dunlin (Calidris alpina), an intercontinental migrant shorebird species

Influenza and other Respiratory Viruses

Volumn 5, Issue 5, 2011, Pages 365-372

  Hall, Jeffrey S ^a   Franson, J Christian ^a   Gill, Robert E ^b   Meteyer, Carol U ^a   Teslaa, Joshua L ^a   Nashold, Sean ^a   Dusek, Robert J ^a   Ip, Hon S ^a  

^a NATIONAL WILDLIFE HEALTH CENTER   (United States)

^b U S GEOLOGICAL SURVEY   (United States)

Author keywords

Dunlin; Experimental infection; Highly pathogenic avian influenza virus; Pathology; Shorebird

Indexed keywords

VIRUS ANTIGEN; VIRUS RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AVIAN INFLUENZA; BRAIN TISSUE; CALIDRIS ALPINA; CONTROLLED STUDY; DISEASE PREDISPOSITION; EXPERIMENTAL STUDY; HISTOPATHOLOGY; INFLUENZA VIRUS A H5N1; MORBIDITY; MORTALITY; NONHUMAN; PATHOGENESIS; PATHOLOGY; PRIORITY JOURNAL; SHOREBIRD; VIRUS EXCRETION; VIRUS SHEDDING;

ANIMAL MIGRATION; ANIMALS; ASIA; CHARADRIIFORMES; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA IN BIRDS; NORTH AMERICA; SEASONS;

EID: 80051562611     PISSN: 17502640     EISSN: 17502659     Source Type: Journal    
DOI: 10.1111/j.1750-2659.2011.00238.x     Document Type: Article

References (36)

1. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol Rev 1992; 56:152-179.
2. Stallknecht DE, Brown JD. Wild birds and the epidemiology of avian influenza. J Wildl Dis 2007; 43(Suppl):S15-S20.
3. Kawaoka Y, Chambers TM, Sladen WL, Webster RG. Is the gene pool of influenza viruses in shorebirds and gulls different from that in wild ducks? Virology 1988; 163:247-250.
4. Hanson BA, Luttrell MP, Goekjian VH, et al. Is the occurrence of avian influenza virus in Charadriiformes species and location dependent? J Wildl Dis 2008; 44:351-361.
5. Honda E, Kida H, Matsuura Y, et al. Survey of influenza viruses in feral birds in 1979 and isolation of a strain possessing Hav6Nav5 from cloaca of an eastern dunlin. Jpn J Vet Res 1981; 29:83-87.
6. Ito T, Okazaki K, Kawaoka Y, Webster RG, Kida H. Perpetuation of influenza A viruses in Alaskan waterfowl reservoirs. Arch Virol 1995; 140:1163-1172.
7. Makarova NV, Kaverin NV, Krauss S, Senne D, Webster RG. Transmission of Eurasian avian H2 influenza virus to shorebirds in North America. J Gen Virol 1999; 80:3167-3171.
8. Fouchier RAM, Olsen B, Bestebroer TM, et al. Influenza A virus surveillance in wild birds in Northern Europe in 1999 and 2000. Avian Dis 2003; 47:857-860.
9. Krauss S, Walker D, Pryor SP, et al. Influenza A viruses of migrating wild aquatic birds in North America. Vector Borne Zoonotic Dis 2004; 4:177-189.
10. Krauss S, Obert CA, Franks J, et al. Influenza in migratory birds and evidence of limited intercontinental virus exchange. PLoS Pathog 2007; 3:1684-1693.
11. Olsen B, Munster VJ, Wallensten A, Waldenström J, Osterhaus ADME, Fouchier RAM. Global patterns of influenza A virus in wild birds. Science 2006; 312:384-388.
12. Jackwood MW, Stallknecht DE. Molecular epidemiologic studies on North American H9 avian influenza virus isolates from waterfowl and shorebirds. Avian Dis 2007; 51:448-450.
13. Munster VJ, Baas C, Lexmond P, et al. Spatial, temporal, and species variation in preva-lence of influenza A viruses in wild migratory birds. PLoS Pathog 2007; 3:1-9.
14. Wahlgren J, Waldenstrom J, Sahlin S, et al. Gene segment reassortment between American and Asian lineages of avian influenza virus from waterfowl in the 10 Beringia area. Vector Borne Zoonotic Dis 2008; 8:783-790.
15. Winker K, Spackman E, Swayne DE. Rarity of influenza A virus in Spring shorebirds, Southern Alaska. Emerg Infect Dis 2008; 14:1314-1315.
16. Ip HS, Flint PL, Franson JC, et al. Prevalence of influenza A viruses in wild migratory birds in Alaska: patterns of variation in detection at a crossroads of intercontinental flyways. Virol J 2008; 5:71.
17. Fernández G, Buchanan JB, Gill RE Jr, Lanctot R, Warnock N. (2008) Conservation Plan for Dunlin with Breeding Populations in North America (Calidris alpina arcticola, C. a. pacifica, and C. a. hudsonia), Version 1.0. Manomet, MA: Manomet Center for Conservation Sciences.
18. Winker K, McCracken KG, Gibson DD, et al. Movements of birds and avian influenza from Asia into Alaska. Emerg Infect Dis 2007; 13:547-552.
19. United States Interagency Strategic Plan: an early detection system for highly pathogenic H5N1 avian influenza in wild migratory birds. 2006. Available at (Accessed June 2009).
20. Brown JD, Stallknecht DE, Beck JR, Suarez DL, Swayne DE. Susceptibility of North American ducks and gulls to H5N1 highly pathogenic avian influenza viruses. Emerg Infect Dis 2006; 12:1663-1670.
21. Brown JD, Stallknecht DE, Valeika S, Swayne DE. Susceptibility of wood ducks to H5N1 highly pathogenic avian influenza virus. J Wildl Dis 2007; 43:660-667.
22. Brown JD, Stallknecht DE, Swayne DE. Experimental infection of swans and geese with highly pathogenic avian influenza virus (H5N1) of Asian lineage. Emerg Infect Dis 2008; 14:136-142.
23. Pasick J, Berhane Y, Embury-Hyatt C, et al. Susceptibility of Canada geese (Branta Canadensis) to highly pathogenic avian influenza virus (H5N1). Emerg Infect Dis 2007; 13:1821-1827.
24. Hall JS, Ip HS, Franson JC, et al. Experimental infection of a North American raptor, American kestrel (Falco sparverius), with highly pathogenic avian influenza virus (H5N1). PLoS ONE 2009; 4:e7555. doi:
25. Neufeld JL, Embury-Hyatt C, Berhane Y, et al. Pathology of highly pathogenic avian influenza (H5N1) infection in Canada geese (Branta canadensis): preliminary studies. Vet Pathol 2009; 46:966-970.
26. Brown JD, Stallknecht DE, Swayne DE. Experimental infections of herring gulls (Larus argentatus) with H5N1 highly pathogenic avian influenza viruses by intranasal inoculation of virus and ingestion of virus-infected chicken meat. Avian Pathol 2008; 37:393-397.
27. Warnock ND, Gill RE. Dunlin (Calidris alpina), The Birds of North America Online, Pool A. (ed). Ithaca: Cornell Lab of Ornithology, 1996; Retrieved from the Birds of North America Online: ; doi: (Accessed June 2009).
28. Reed LJ, Muench H. A simple method for estimating fifty per cent endpoints. Am J Hyg 1938; 27:493-497.
29. Brown JD, Luttrell MP, Berghaus RD, et al. Prevalence of antibodies to type A influenza virus in wild avian species using two serologic assays. J Wildl Dis 2010; 46:896-911.
30. Spackman E, Senne DA, Myers TJ, et al. Development of a real-time reverse transcriptase PCR assay for type A influenza virus and the avian H5 and H7 hemagglutinin subtypes. J Clin Microbiol 2002; 40:3256-3260.
31. van Gils A, Munster VJ, Radersma R, et al. Hampered foraging and migratory performance in swans infected with low-pathogenic avian influenza A virus. PLoS ONE 2007; 1:e184.
32. Latorre-Margalef N, Gunnarsson G, Munster VJ, et al. Effects of influenza A virus infection on migrating mallard ducks. Proc Biol Sci 2008; 9:2345-2349.
33. Reperant LA, van Amerongen G, van de Bildt MWG, et al. Highly pathogenic avian influenza virus (H5N1) infection in red foxes fed infected bird carcasses. Emerg Infect Dis 2008; 14:1835-841.
34. Ward FP, Laybourne RC. A difference in prey selection by adult and immature peregrine falcons during autumn migration. ICBP Technical Bulletin No. 5, 1985.
35. Samour J. Avian influenza in Saudi falcons. Falco Newsletter. 2006:27:21. Available at (Accessed June 2009).
36. Alexander DJ. Summary of avian influenza activity in Europe, Asia, Africa, and Australasia, 2002-2006. Avian Dis 2007; 51:161-166.