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Volume 25, Number 10—October 2019

Serologic Evidence of Exposure to Highly Pathogenic Avian Influenza H5 Viruses in Migratory Shorebirds, Australia

Michelle WilleComments to Author , Simeon Lisovski, Alice Risely, Marta Ferenczi, David Roshier, Frank Y.K. Wong, Andrew C. Breed, Marcel Klaassen, and Aeron C. Hurt
Author affiliations: World Health Organization Collaborating Centre for Reference and Research on Influenza, Melbourne, Victoria, Australia (M. Wille, A.C. Hurt); Deakin University, Geelong, Victoria, Australia (S. Lisovski, A. Risely, M. Ferenczi, D. Roshier, M. Klaassen); Commonwealth Scientific and Industrial Research Organisation, Australian Animal Health Laboratory, Geelong (F.Y.K. Wong); Department of Agriculture and Water Resources, Canberra, Capital Territory, Australia (A.C. Breed); University of Queensland, St. Lucia, Queensland, Australia (A.C. Breed)

Main Article


Antigens used to assess exposure of red-necked stints and Pacific black ducks to highly pathogenic avian influenza H5 viruses, Australia*

H5 virus clade† Strain
1.1.1 A/Cambodia/X0810301/2013(H5N1) A/Indonesia/NIHRD11771/2011(H5N1) A/barn swallow/Hong Kong/D10-1161/2010(H5N1) A/duck/Vietnam/NCVD-1584/2012(H5N1) A/Guizhou/1/2013(H5N1) A/gyrfalcon/Washington/41088-6/2014(H5N8)
LPAI H5 A/duck/Victoria/0305-2/2012(H5N3)
A/wild bird/Queensland/P17-14428-30-01/2017(H5N1)‡

*All HPAI virus strains were 6:2 recombinant viruses on a PR8 backbone with the multi-basic cleavage site removed. All LPAI strains were gamma-irradiated. HPAI, highly pathogenic avian influenza; LPAI, low pathogenicity avian influenza.
†Clade notation as defined by World Health Organization/World Organization for Animal Health/Food and Agriculture Organization H5N1 Evolution Working Group (28).
‡Only used for hemagglutinin inhibition assays for serum samples from Pacific black ducks.

Main Article

  1. Guan  Y, Peiris  JSM, Lipatov  AS, Ellis  TM, Dyrting  KC, Krauss  S, et al. Emergence of multiple genotypes of H5N1 avian influenza viruses in Hong Kong SAR. Proc Natl Acad Sci U S A. 2002;99:89505. DOIPubMed
  2. Xu  X, Subbarao , Cox  NJ, Guo  Y. 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. 1999;261:159. DOIPubMed
  3. Chen  H, Smith  GJD, Zhang  SY, Qin  K, Wang  J, Li  KS, et al. Avian flu: H5N1 virus outbreak in migratory waterfowl. Nature. 2005;436:1912. DOIPubMed
  4. Liu  J, Xiao  H, Lei  F, Zhu  Q, Qin  K, Zhang  XW, et al. Highly pathogenic H5N1 influenza virus infection in migratory birds. Science. 2005;309:1206. DOIPubMed
  5. Feare  CJ. Role of wild birds in the spread of highly pathogenic avian influenza virus H5N1 and implications for global surveillance. Avian Dis. 2010;54(Suppl):20112. DOIPubMed
  6. Lee  YJ, Kang  HM, Lee  EK, Song  BM, Jeong  J, Kwon  YK, et al. Novel reassortant influenza A(H5N8) viruses, South Korea, 2014. Emerg Infect Dis. 2014;20:10879. DOIPubMed
  7. Global Consortium for H5N8 and Related Influenza Viruses. Role for migratory wild birds in the global spread of avian influenza H5N8. Science. 2016;354:2137. DOI
  8. Verhagen  JH, Herfst  S, Fouchier  RAM. Infectious disease. How a virus travels the world. Science. 2015;347:6167. DOIPubMed
  9. Bevins  SN, Dusek  RJ, White  CL, Gidlewski  T, Bodenstein  B, Mansfield  KG, et al. Widespread detection of highly pathogenic H5 influenza viruses in wild birds from the Pacific Flyway of the United States. Sci Rep. 2016;6:28980. DOIPubMed
  10. Bodewes  R, Kuiken  T. Changing role of wild birds in the epidemiology of avian influenza A viruses. Adv Virus Res. 2018;100:279307. DOIPubMed
  11. Pantin-Jackwood  MJ, Costa-Hurtado  M, Bertran  K, DeJesus  E, Smith  D, Swayne  DE. Infectivity, transmission and pathogenicity of H5 highly pathogenic avian influenza clade (H5N8 and H5N2) United States index viruses in Pekin ducks and Chinese geese. Vet Res (Faisalabad). 2017;48:33. DOIPubMed
  12. Grillo  VL, Arzey  KE, Hansbro  PM, Hurt  AC, Warner  S, Bergfeld  J, et al. Avian influenza in Australia: a summary of 5 years of wild bird surveillance. Aust Vet J. 2015;93:38793. DOIPubMed
  13. Olsen  B, Munster  VJ, Wallensten  A, Waldenström  J, Osterhaus  ADME, Fouchier  RAM. Global patterns of influenza a virus in wild birds. Science. 2006;312:3848. DOIPubMed
  14. Kuiken  T. Is low pathogenic avian influenza virus virulent for wild waterbirds? Proc Bio Sci. 2013;280(1763):20130990.
  15. Clemens  RS, Kendall  BE, Guillet  J, Fuller  RA. Review of Australian shorebird survey data, with notes on their suitability for comprehensive population trend analysis. Stilt. 2012;62:317.
  16. Studds  CE, Kendall  BE, Murray  NJ, Wilson  HB, Rogers  DI, Clemens  RS, et al. Rapid population decline in migratory shorebirds relying on Yellow Sea tidal mudflats as stopover sites. Nat Commun. 2017;8:14895. DOIPubMed
  17. Minton  C, Wahl  J, Gibbs  H, Jessop  R, Hassell  C, Boyle  A. Recoveries and flag sightings of waders which spend the non-breeding season in Australia. Stilt. 2011;50:1743.
  18. Krauss  S, Stallknecht  DE, Negovetich  NJ, Niles  LJ, Webby  RJ, Webster  RG. Coincident ruddy turnstone migration and horseshoe crab spawning creates an ecological ‘hot spot’ for influenza viruses. Proc Biol Sci. 1699;2010:33739.
  19. Winker  K, Spackman  E, Swayne  DE. Rarity of influenza A virus in spring shorebirds, southern Alaska. Emerg Infect Dis. 2008;14:13146. DOIPubMed
  20. Hanson  BA, Luttrell  MP, Goekjian  VH, Niles  L, Swayne  DE, Senne  DA, et al. Is the occurrence of avian influenza virus in Charadriiformes species and location dependent? J Wildl Dis. 2008;44:35161. DOIPubMed
  21. Curran  JM, Ellis  TM, Robertson  ID. Surveillance of Charadriiformes in northern Australia shows species variations in exposure to avian influenza virus and suggests negligible virus prevalence. Avian Dis. 2014;58:199204. DOIPubMed
  22. Iverson  SA, Takekawa  JY, Schwarzbach  S, Cardona  CJ, Warnock  N, Bishop  MA, et al. Low prevalence of avian influenza virus in shorebirds on the Pacific Coast of North America. Waterbirds. 2008;31:60210.
  23. McCallum  HI, Roshier  DA, Tracey  JP, Joseph  L, Heinsohn  R. Will Wallace’s line save Australia from avian influenza? Ecol Soc. 2008;13:41. DOI
  24. Ferenczi  M, Beckmann  C, Warner  S, Loyn  R, O’Riley  K, Wang  X, et al. Avian influenza infection dynamics under variable climatic conditions, viral prevalence is rainfall driven in waterfowl from temperate, south-east Australia. Vet Res (Faisalabad). 2016;47:23. DOIPubMed
  25. McNally  J, Falconer  DD. Trapping and banding operations Lara Lake. Emu. 1953;53:5170. DOI
  26. Brown  JD, Stallknecht  DE, Berghaus  RD, Luttrell  MP, Velek  K, Kistler  W, et al. Evaluation of a commercial blocking enzyme-linked immunosorbent assay to detect avian influenza virus antibodies in multiple experimentally infected avian species. Clin Vaccine Immunol. 2009;16:8249. DOIPubMed
  27. Shriner  SA, VanDalen  KK, Root  JJ, Sullivan  HJ. Evaluation and optimization of a commercial blocking ELISA for detecting antibodies to influenza A virus for research and surveillance of mallards. J Virol Methods. 2016;228:1304. DOIPubMed
  28. World Health Organization/World Organisation for Animal Health/Food and Agriculture Organization (WHO/OIE/FAO) H5N1 Evolution Working Group. Revised and updated nomenclature for highly pathogenic avian influenza A (H5N1) viruses. Influenza Other Respir Viruses. 2014;8:3848. DOI
  29. Tracey  JP, Woods  R, Roshier  D, West  P, Saunders  GR. The role of wild birds in the transmission of avian influenza for Australia: an ecological perspective. Emu. 2004;104:10924. DOI
  30. Curran  JM, Ellis  TM, Robertson  ID. Serological surveillance of wild waterfowl in Northern Australia for avian influenza virus shows variations in prevalence and a cyclical periodicity of infection. Avian Dis. 2015;59:4927. DOIPubMed
  31. Gilbert  M, Koel  BF, Bestebroer  TM, Lewis  NS, Smith  DJ, Fouchier  RAM. Serological evidence for non-lethal exposures of Mongolian wild birds to highly pathogenic avian influenza H5N1 virus. PLoS One. 2014;9:e113569. DOIPubMed
  32. World Health Organization. Antigenic and genetic characteristics of zoonotic influenza viruses and development of candidate vaccine viruses for pandemic preparedness. 2019 Feb 21 [cited 2019 May 16].
  33. Poen  MJ, Verhagen  JH, Manvell  RJ, Brown  I, Bestebroer  TM, van der Vliet  S, et al. Lack of virological and serological evidence for continued circulation of highly pathogenic avian influenza H5N8 virus in wild birds in the Netherlands, 14 November 2014 to 31 January 2016. Euro Surveill. 2016;21:e30349. DOIPubMed
  34. Hill  SC, Hansen  R, Watson  S, Coward  V, Russell  C, Cooper  J, et al. Comparative micro-epidemiology of pathogenic avian influenza virus outbreaks in a wild bird population. Philos Trans R Soc Lond B Biol Sci. 2019;374:20180259. DOIPubMed
  35. Hill  SC, Manvell  RJ, Schulenburg  B, Shell  W, Wikramaratna  PS, Perrins  C, et al. Antibody responses to avian influenza viruses in wild birds broaden with age. Proc Biol Sci. 2016;283(1845).
  36. Ramos  R, Garnier  R, González-Solís  J, Boulinier  T. Long antibody persistence and transgenerational transfer of immunity in a long-lived vertebrate. Am Nat. 2014;184:76476. DOIPubMed
  37. Wille  M, Latorre-Margalef  N, Tolf  C, Stallknecht  DE, Waldenström  J. No evidence for homosubtypic immunity of influenza H3 in Mallards following vaccination in a natural experimental system. Mol Ecol. 2017;26:142031. DOIPubMed
  38. Magor  KE. Immunoglobulin genetics and antibody responses to influenza in ducks. Dev Comp Immunol. 2011;35:100816. DOIPubMed
  39. Poen  MJ, Bestebroer  TM, Vuong  O, Scheuer  RD, van der Jeugd  HP, Kleyheeg  E, et al. Local amplification of highly pathogenic avian influenza H5N8 viruses in wild birds in the Netherlands, 2016 to 2017. Euro Surveill. 2018;23.
  40. Bahnson  CS, Poulson  RL, Krauss  S, Webster  RG, Stallknecht  DE. Neutralizing antibodies to type A influenza viruses in shorebirds at Delaware Bay, New Jersey, USA. J Wildl Dis. 2018;54:70815. DOIPubMed
  41. de Araujo  J, de Azevedo  SM Jr, Gaidet  N, Hurtado  RF, Walker  D, Thomazelli  LM, et al. Avian influenza virus (H11N9) in migratory shorebirds wintering in the Amazon Region, Brazil. PLoS One. 2014;9:e110141. DOIPubMed
  42. Kwon  JH, Lee  DH, Swayne  DE, Noh  JY, Yuk  SS, Jeong  S, et al. Experimental infection of H5N1 and H5N8 highly pathogenic avian influenza viruses in Northern Pintail (Anas acuta). Transbound Emerg Dis. 2018;65:136771. DOIPubMed
  43. Son  K, Kim  YK, Oem  JK, Jheong  WH, Sleeman  JM, Jeong  J. Experimental infection of highly pathogenic avian influenza viruses, Clade H5N6 and H5N8, in Mandarin ducks from South Korea. Transbound Emerg Dis. 2018;65:899903. DOIPubMed
  44. Kwon  J-H, Noh  J-Y, Jeong  J-H, Jeong  S, Lee  S-H, Kim  Y-J, et al. Different pathogenicity of two strains of clade H5N6 highly pathogenic avian influenza viruses bearing different PA and NS gene in domestic ducks. Virology. 2019;530:118. DOIPubMed
  45. Pantin-Jackwood  MJ, Costa-Hurtado  M, Shepherd  E, DeJesus  E, Smith  D, Spackman  E, et al. Pathogenicity and transmission of H5 and H7 highly pathogenic avian influenza viruses in Mallards. J Virol. 2016;90:996782. DOIPubMed
  46. Hall  JS, Franson  JC, Gill  RE, Meteyer  CU, TeSlaa  JL, Nashold  S, et al. Experimental challenge and pathology of highly pathogenic avian influenza virus H5N1 in dunlin (Calidris alpina), an intercontinental migrant shorebird species. Influenza Other Respir Viruses. 2011;5:36572. DOIPubMed
  47. Hall  JS, Krauss  S, Franson  JC, TeSlaa  JL, Nashold  SW, Stallknecht  DE, et al. Avian influenza in shorebirds: experimental infection of ruddy turnstones (Arenaria interpres) with avian influenza virus. Influenza Other Respir Viruses. 2013;7:8592. DOIPubMed
  48. Fereidouni  SR, Starick  E, Beer  M, Wilking  H, Kalthoff  D, Grund  C, et al. Highly pathogenic avian influenza virus infection of mallards with homo- and heterosubtypic immunity induced by low pathogenic avian influenza viruses. PLoS One. 2009;4:e6706. DOIPubMed
  49. Latorre-Margalef  N, Brown  JD, Fojtik  A, Poulson  RL, Carter  D, Franca  M, et al. Competition between influenza A virus subtypes through heterosubtypic immunity modulates re-infection and antibody dynamics in the mallard duck. PLoS Pathog. 2017;13:e1006419. DOIPubMed
  50. Reperant  LA, van de Bildt  MW, van Amerongen  G, Buehler  DM, Osterhaus  AD, Jenni-Eiermann  S, et al. Highly pathogenic avian influenza virus H5N1 infection in a long-distance migrant shorebird under migratory and non-migratory states. PLoS One. 2011;6:e27814. DOIPubMed

Main Article

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