Research article Open Access
Like 0


In 2014, H5N8 clade highly pathogenic avian influenza (HPAI) viruses of the A/Goose/Guangdong/1/1996 lineage emerged in poultry and wild birds in Asia, Europe and North America. Here, wild birds were extensively investigated in the Netherlands for HPAI H5N8 virus (real-time polymerase chain reaction targeting the matrix and H5 gene) and antibody detection (haemagglutination inhibition and virus neutralisation assays) before, during and after the first virus detection in Europe in late 2014. Between 21 February 2015 and 31 January 2016, 7,337 bird samples were tested for the virus. One HPAI H5N8 virus-infected Eurasian wigeon () sampled on 25 February 2015 was detected. Serological assays were performed on 1,443 samples, including 149 collected between 2007 and 2013, 945 between 14 November 2014 and 13 May 2015, and 349 between 1 September and 31 December 2015. Antibodies specific for HPAI H5 clade were absent in wild bird sera obtained before 2014 and present in sera collected during and after the HPAI H5N8 emergence in Europe, with antibody incidence declining after the 2014/15 winter. Our results indicate that the HPAI H5N8 virus has not continued to circulate extensively in wild bird populations since the 2014/15 winter and that independent maintenance of the virus in these populations appears unlikely.


Article metrics loading...

Loading full text...

Full text loading...



  1. Kuiken T. Is low pathogenic avian influenza virus virulent for wild waterbirds? Proc. Biol. Sci. 2013;280(1763):20130990.  https://doi.org/http://dx.doi.org/10.1098/rspb.2013.0990  . PMID: 23740783 
  2. 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(5738):1206.  https://doi.org/10.1126/science.1115273  PMID: 16000410 
  3. Zhao K, Gu M, Zhong L, Duan Z, Zhang Y, Zhu Y, et al. Characterization of three H5N5 and one H5N8 highly pathogenic avian influenza viruses in China. Vet Microbiol. 2013;163(3-4):351-7.  https://doi.org/10.1016/j.vetmic.2012.12.025  PMID: 23375651 
  4. Jeong J, Kang HM, Lee EK, Song BM, Kwon YK, Kim HR, 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(3-4):249-57.  https://doi.org/10.1016/j.vetmic.2014.08.002  PMID: 25192767 
  5. World Organisation for Animal Health (OIE). Update on highly pathogenic avian influenza in animals (typeH5 and H7). Paris: OIE; 2014. [Accessed 02 Feb 2016]. Available from: http://www.oie.int/animal-health-in-the-world/update-on-avian-influenza/2014/
  6. World Organisation for Animal Health (OIE). Update on highly pathogenic avian influenza in animals (typeH5 and H7). Paris: OIE; 2015. [Accessed 02 Feb 2016]. Available from: http://www.oie.int/animal-health-in-the-world/update-on-avian-influenza/2015/
  7. Verhagen JH, Herfst S, Fouchier RAM. How a virus travels the world. Science. 2015;347(6222):616-7.  https://doi.org/10.1126/science.aaa6724  PMID: 25657235 
  8. Marchenko VY, Susloparov IM, Kolosova NP, Goncharova NI, Shipovalov AV, Durymanov AG, et al. Influenza A(H5N8) virus isolation in Russia, 2014. Arch Virol. 2015;160(11):2857-60.  https://doi.org/10.1007/s00705-015-2570-4  PMID: 26306756 
  9. Hall JS, Dusek RJ, Spackman E. Rapidly Expanding Range of Highly Pathogenic Avian Influenza Viruses. Emerg Infect Dis. 2015;21(7):1251-2.  https://doi.org/10.3201/eid2107.150403  PMID: 26079209 
  10. Kim HM, Kim CK, Lee NJ, Chu H, Kang C, Kim K, et al. Pathogenesis of novel reassortant avian influenza virus A (H5N8) Isolates in the ferret. Virology. 2015;481:136-41.  https://doi.org/10.1016/j.virol.2015.02.042  PMID: 25776760 
  11. Kim YI, Pascua PN, Kwon HI, Lim GJ, Kim EH, Yoon SW, et al. Pathobiological features of a novel, highly pathogenic avian influenza A(H5N8) virus. Emerg Microbes Infect. 2014;3(10):e75.  https://doi.org/10.1038/emi.2014.75  PMID: 26038499 
  12. Richard M, Herfst S, van den Brand JMA, Lexmond P, Bestebroer TM, Rimmelzwaan GF, et al. Low Virulence and Lack of Airborne Transmission of the Dutch Highly Pathogenic Avian Influenza Virus H5N8 in Ferrets. PLoS One. 2015;10(6):e0129827.  https://doi.org/10.1371/journal.pone.0129827  PMID: 26090682 
  13. European Food Safety Authority (EFSA). Highly pathogenic avian influenza A subtype H5N8. EFSA Journal.2014;12(12):3941.  https://doi.org/10.2903/j.efsa.2014.3941 
  14. Verhagen JH, van der Jeugd HP, Nolet BA, Slaterus R, Kharitonov SP, de Vries PP, et al. Wild bird surveillance around outbreaks of highly pathogenic avian influenza A(H5N8) virus in the Netherlands, 2014, within the context of global flyways. Euro Surveill. 2015;20(12):21069.  https://doi.org/10.2807/1560-7917.ES2015.20.12.21069  PMID: 25846491 
  15. Koel BF, van der Vliet S, Burke DF, Bestebroer TM, Bharoto EE, Yasa IWW, et al. Antigenic variation of clade 2.1 H5N1 virus is determined by a few amino acid substitutions immediately adjacent to the receptor binding site. MBio. 2014;5(3):e01070-14.  https://doi.org/10.1128/mBio.01070-14  PMID: 24917596 
  16. 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(12):e113569.  https://doi.org/10.1371/journal.pone.0113569  PMID: 25502318 
  17. Munster VJ, Baas C, Lexmond P, Bestebroer TM, Guldemeester J, Beyer WE, et al. Practical considerations for high-throughput influenza A virus surveillance studies of wild birds by use of molecular diagnostic tests. J Clin Microbiol. 2009;47(3):666-73.  https://doi.org/10.1128/JCM.01625-08  PMID: 19109483 
  18. Hirst GK. Studies of Antigenic Differences among Strains of Influenza a by Means of Red Cell Agglutination. J Exp Med. 1943;78(5):407-23.  https://doi.org/10.1084/jem.78.5.407  PMID: 19871338 
  19. World Organisation for Animal Health (OIE). Ch. 2.3.4. Avian Influenza (infection with avian influenza viruses). OIE Terrestrial Manual 2015. Paris: OIE; 2015. [Accessed 02 Feb 2016]. Available from: http://www.oie.int/fileadmin/Home/eng/Health_standards/tahm/2.03.04_AI.pdf
  20. Rimmelzwaan GF, Baars M, van Beek R, de Lijster P, de Jong JC, Claas EC, et al. Influenza virus subtype cross-reactivities of haemagglutination inhibiting and virus neutralising serum antibodies induced by infection or vaccination with an ISCOM-based vaccine. Vaccine. 1999;17(20-21):2512-6.  https://doi.org/10.1016/S0264-410X(99)00063-8  PMID: 10418897 
  21. Kim HR, Kwon YK, Jang I, Lee YJ, Kang HM, Lee EK, et al. Pathologic changes in wild birds infected with highly pathogenic avian influenza A(H5N8) viruses, South-Korea, 2014. Emerg Infect Dis. 2015;21(5):775-80.  https://doi.org/10.3201/eid2105.141967  PMID: 25897841 
  22. Brown J, Poulson R, Carter D, Lebarbenchon C, Pantin-Jackwood M, Spackman E, et al. Susceptibility of avian species to North American H13 low pathogenic avian influenza viruses. Avian Dis. 2012;56(4) Suppl;969-75.  https://doi.org/10.1637/10158-040912-Reg.1  PMID: 23402121 
  23. Tolf C, Latorre-Margalef N, Wille M, Bengtsson D, Gunnarsson G, Grosbois V, et al. Individual variation in influenza A virus infection histories and long-term immune responses in Mallards. PLoS One. 2013;8(4):e61201.  https://doi.org/10.1371/journal.pone.0061201  PMID: 23637797 
  24. Verhagen JH, Höfle U, van Amerongen G, van de Bildt M, Majoor F, Fouchier RAM, et al. Long-Term Effect of Serial Infections with H13 and H16 Low-Pathogenic Avian Influenza Viruses in Black-Headed Gulls. J Virol. 2015;89(22):11507-22.  https://doi.org/10.1128/JVI.01765-15  PMID: 26339062 
  25. Wibawa H, Henning J, Waluyati DE, Usman TB, Lowther S, Bingham J, et al. Comparison of serological assays for detecting antibodies in ducks exposed to H5 subtype avian influenza virus. BMC Vet Res. 2012;8:117.  https://doi.org/10.1186/1746-6148-8-117  PMID: 22823985 

Data & Media loading...

Submit comment
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error