Archives of Virology

, Volume 163, Issue 5, pp 1195–1207 | Cite as

Spatial transmission of H5N6 highly pathogenic avian influenza viruses among wild birds in Ibaraki Prefecture, Japan, 2016–2017

  • Ryota Tsunekuni
  • Yuji Yaguchi
  • Yuki Kashima
  • Kaoru Yamashita
  • Nobuhiro Takemae
  • Junki Mine
  • Taichiro Tanikawa
  • Yuko Uchida
  • Takehiko Saito
Original Article

Abstract

From 29 November 2016 to 24 January 2017, sixty-three cases of H5N6 highly pathogenic avian influenza virus (HPAIV) infections were detected in wild birds in Ibaraki Prefecture, Japan. Here, we analyzed the genetic, temporal, and geographic correlations of these 63 HPAIVs to elucidate their dissemination throughout the prefecture. Full-genome sequence analysis of the Ibaraki isolates showed that 7 segments (PB2, PB1, PA, HA, NP, NA, NS) were derived from G1.1.9 strains while the M segment was from G1.1 strains; both groups of strains circulated in south China. Pathological studies revealed severe systemic infection in dead swans (the majority of dead birds and the only species necropsied), thus indicating high susceptibility to H5N6 HPAIVs. Coalescent phylogenetic analysis using the 7 G1.1.9-derived segments enabled detailed analysis of the short-term evolution of these highly homologous HPAIVs. This analysis revealed that the H5N6 HPAIVs isolated from wild birds in Ibaraki Prefecture were divided into 7 groups. Spatial analysis demonstrated that most of the cases concentrated around Senba Lake originated from a single source, and progeny viruses were transmitted to other locations after the infection expanded in mute swans. In contrast, within just a 5-km radius of the area in which cases were concentrated, three different intrusions of H5N6 HPAIVs were evident. Multi-segment analysis of short-term evolution showed that not only was the invading virus spread throughout Ibaraki Prefecture but also that, despite the small size of this region, multiple invasions had occurred during winter 2016–2017.

Notes

Acknowledgements

In this research, we used the supercomputer of AFFRIT, MAFF, Japan.

Author contributions

RT designed the study, characterized viruses, and drafted the manuscript; YY, YK, and KY conducted pathology diagnosis and virus isolation; TS designed and coordinated the study and drafted the manuscript; NT, JM, TT, and YU characterized the viruses; all authors have read and approved the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

This article does not contain any studies with human participants or live animals performed by any of the authors.

Supplementary material

705_2018_3752_MOESM1_ESM.pdf (105 kb)
Supplementary material 1 (PDF 105 kb) Online Resource 1: Accession numbers of sequences of Ibaraki isolates
705_2018_3752_MOESM2_ESM.pdf (396 kb)
Supplementary material 2 (PDF 396 kb) Online Resource 2: Pathologic findings in dead mute swans. Brain (a, b), lung (c, d,), and rachis (e, f) were collected from dead mute swans. Tissue sections were stained with hematoxylin and eosin (a, c, e). In immunohistochemical analysis for AIV M protein, the antigen stains red (b, d, f)
705_2018_3752_MOESM3_ESM.pdf (261 kb)
Supplementary material 3 (PDF 260 kb) Online Resource 3: Pathologic finding in a dead mute swan: hemorrhage in the conjunctiva (a). Tissue sections were stained with hematoxylin and eosin (b). In the immunohistochemical analysis for AIV M protein, the antigen stains red (c)
705_2018_3752_MOESM4_ESM.pdf (250 kb)
Supplementary material 4 (PDF 249 kb) Online Resource 4: Phylogenetic tree based on the HA gene. Branches in clade 2.3.4.4 are filled in beige and that of the Ibaraki isolates is shown as a red line
705_2018_3752_MOESM5_ESM.pdf (314 kb)
Supplementary material 5 (PDF 313 kb) Online Resource 5: Maximum-likelihood phylogenetic tree based on HA gene
705_2018_3752_MOESM6_ESM.pdf (314 kb)
Supplementary material 6 (PDF 314 kb) Online Resource 6: Maximum-likelihood phylogenetic tree based on NA gene
705_2018_3752_MOESM7_ESM.pdf (313 kb)
Supplementary material 7 (PDF 312 kb) Online Resource 7: Maximum-likelihood phylogenetic tree based on PB2 gene
705_2018_3752_MOESM8_ESM.pdf (371 kb)
Supplementary material 8 (PDF 371 kb) Online Resource 8: Maximum-likelihood phylogenetic tree based on PB1 gene
705_2018_3752_MOESM9_ESM.pdf (367 kb)
Supplementary material 9 (PDF 366 kb) Online Resource 9: Maximum-likelihood phylogenetic tree based on PA gene
705_2018_3752_MOESM10_ESM.pdf (368 kb)
Supplementary material 10 (PDF 367 kb) Online Resource 10: Maximum-likelihood phylogenetic tree based on NP gene
705_2018_3752_MOESM11_ESM.pdf (310 kb)
Supplementary material 11 (PDF 310 kb) Online Resource 11: Maximum-likelihood phylogenetic tree based on M gene
705_2018_3752_MOESM12_ESM.pdf (366 kb)
Supplementary material 12 (PDF 366 kb) Online Resource 12: Maximum-likelihood phylogenetic tree based on NS gene
705_2018_3752_MOESM13_ESM.pdf (211 kb)
Supplementary material 13 (PDF 211 kb) Online Resource 13: Occurrence rates of branch posteriors of the maximum clade credibility (MCC) tree. The graph shows five ranges of posterior values: 0 to 0.2, >0.2 to 0.4, >0.4 to 0.6, >0.6 to 0.8, and >0.8 to 1. MCC trees based on the HA or NA segment were generated under the same conditions as that using 7 segments. The branch posteriors of the MCC tree generated from 7 segments differed significantly (P < 0.01, Mann–Whitney U test) from those of the MCC tree generated by using the HA or NA segment

References

  1. 1.
    Xu X, Subbarao K, Cox NJ, Guo Y (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(1):15–19.  https://doi.org/10.1006/viro.1999.9820 CrossRefPubMedGoogle Scholar
  2. 2.
    Shortridge KF, Zhou NN, Guan Y, Gao P, Ito T, Kawaoka Y, Kodihalli S, Krauss S, Markwell D, Murti KG, Norwood M, Senne D, Sims L, Takada A, Webster RG (1998) Characterization of avian H5N1 influenza viruses from poultry in Hong Kong. Virology 252(2):331–342CrossRefPubMedGoogle Scholar
  3. 3.
    WHO (2005) Evolution of H5N1 avian influenza viruses in Asia. Emerg Infect Dis 11(10):1515–1521CrossRefGoogle Scholar
  4. 4.
    Enserink M (2006) Avian influenza. H5N1 moves into Africa, European Union, deepening global crisis. Science 311(5763):932.  https://doi.org/10.1126/science.311.5763.932a CrossRefPubMedGoogle Scholar
  5. 5.
    Leventhal A, Ramlawi A, Belbiesi A, Balicer RD (2006) Regional collaboration in the Middle East to deal with H5N1 avian flu. BMJ 333(7573):856–858.  https://doi.org/10.1136/bmj.38988.607836.68 CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    OIE (2017) Update on avian influenza in animals (types H5 and H7). http://www.oie.int/animal-health-in-the-world/update-on-avian-influenza/. Accessed 30 Jan 2018
  7. 7.
    Lee MS, Chen LH, Chen YP, Liu YP, Li WC, Lin YL, Lee F (2016) Highly pathogenic avian influenza viruses H5N2, H5N3, and H5N8 in Taiwan in 2015. Vet Microbiol 187:50–57.  https://doi.org/10.1016/j.vetmic.2016.03.012 CrossRefPubMedGoogle Scholar
  8. 8.
    Qi X, Cui L, Yu H, Ge Y, Tang F (2014) Whole-genome sequence of a reassortant H5N6 avian influenza virus isolated from a live poultry market in China, 2013. Genome Announc.  https://doi.org/10.1128/genomeA.00706-14 Google Scholar
  9. 9.
    Adlhoch C, Gossner C, Koch G, Brown I, Bouwstra R, Verdonck F, Penttinen P, Harder T (2014) Comparing introduction to Europe of highly pathogenic avian influenza viruses A(H5N8) in 2014 and A(H5N1) in 2005. Euro Surveill 19(50):20996CrossRefPubMedGoogle Scholar
  10. 10.
    Ramey AM, Reeves AB, TeSlaa JL, Nashold S, Donnelly T, Bahl J, Hall JS (2016) Evidence for common ancestry among viruses isolated from wild birds in Beringia and highly pathogenic intercontinental reassortant H5N1 and H5N2 influenza A viruses. Infect Genet Evolut 40:176–185CrossRefGoogle Scholar
  11. 11.
    Sturm-Ramirez KM, Ellis T, Bousfield B, Bissett L, Dyrting K, Rehg JE, Poon L, Guan Y, Peiris M, Webster RG (2004) Reemerging H5N1 influenza viruses in Hong Kong in 2002 are highly pathogenic to ducks. J Virol 78(9):4892–4901.  https://doi.org/10.1128/jvi.78.9.4892-4901.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Chen H, Smith GJ, Zhang SY, Qin K, Wang J, Li KS, Webster RG, Peiris JS, Guan Y (2005) Avian flu: H5N1 virus outbreak in migratory waterfowl. Nature 436(7048):191–192.  https://doi.org/10.1038/nature03974 CrossRefPubMedGoogle Scholar
  13. 13.
    Oprişan G, Coste H, Lupulescu E, Oprişoreanu AM, Szmal CO, Popovici N, Ionescu LE, Bicheru S, Enache N, Ceianu C, Czobor F, Olaru E, Alexandrescu V, Radu DL, Onu A, Popa MI (2006) Molecular analysis of the first avian influenza H5N1 isolates from fowl in Romania. Roum Arch Microbiol Immunol 65(3–4):79–82PubMedGoogle Scholar
  14. 14.
    Savić V, Labrović A, Zelenika T, Balenović M, Separović S, Jurinović L (2010) Multiple introduction of Asian H5N1 avian influenza virus in croatia by wild birds during 2005–2006 and isolation of the virus from apparently healthy black-headed gulls (Larus ridibundus). Vector Borne Zoonotic Dis 10(9):915–920CrossRefPubMedGoogle Scholar
  15. 15.
    Globig A, Staubach C, Beer M, Koppen U, Fiedler W, Nieburg M, Wilking H, Starick E, Teifke JP, Werner O, Unger F, Grund C, Wolf C, Roost H, Feldhusen F, Conraths FJ, Mettenleiter TC, Harder TC (2009) Epidemiological and ornithological aspects of outbreaks of highly pathogenic avian influenza virus H5N1 of Asian lineage in wild birds in Germany, 2006 and 2007. Transbound Emerg Dis 56(3):57–72.  https://doi.org/10.1111/j.1865-1682.2008.01061.x CrossRefPubMedGoogle Scholar
  16. 16.
    Bragstad K, Jorgensen PH, Handberg K, Hammer AS, Kabell S, Fomsgaard A (2007) First introduction of highly pathogenic H5N1 avian influenza A viruses in wild and domestic birds in Denmark, Northern Europe. Virol J 4:43.  https://doi.org/10.1186/1743-422X-4-43 CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Ducatez MF, Olinger CM, Owoade AA, Tarnagda Z, Tahita MC, Sow A, De Landtsheer S, Ammerlaan W, Ouedraogo JB, Osterhaus AD, Fouchier RA, Muller CP (2007) Molecular and antigenic evolution and geographical spread of H5N1 highly pathogenic avian influenza viruses in western Africa. J Gen Virol 88(Pt 8):2297–2306.  https://doi.org/10.1099/vir.0.82939-0 CrossRefPubMedGoogle Scholar
  18. 18.
    Ducatez MF, Olinger CM, Owoade AA, De Landtsheer S, Ammerlaan W, Niesters HG, Osterhaus AD, Fouchier RA, Muller CP (2006) Avian flu: multiple introductions of H5N1 in Nigeria. Nature 442(7098):37.  https://doi.org/10.1038/442037a CrossRefPubMedGoogle Scholar
  19. 19.
    Sakoda Y, Ito H, Uchida Y, Okamatsu M, Yamamoto N, Soda K, Nomura N, Kuribayashi S, Shichinohe S, Sunden Y, Umemura T, Usui T, Ozaki H, Yamaguchi T, Murase T, Ito T, Saito T, Takada A, Kida H (2012) Reintroduction of H5N1 highly pathogenic avian influenza virus by migratory water birds, causing poultry outbreaks in the 2010–2011 winter season in Japan. J Gen Virol 93(Pt 3):541–550.  https://doi.org/10.1099/vir.0.037572-0 CrossRefPubMedGoogle Scholar
  20. 20.
    Kim HR, Lee YJ, Park CK, Oem JK, Lee OS, Kang HM, Choi JG, Bae YC (2012) Highly pathogenic avian influenza (H5N1) outbreaks in wild birds and poultry, South Korea. Emerg Infect Dis 18(3):480–483.  https://doi.org/10.3201/eid1803.111490 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Krauss S, Stallknecht DE, Slemons RD, Bowman AS, Poulson RL, Nolting JM, Knowles JP, Webster RG (2016) The enigma of the apparent disappearance of Eurasian highly pathogenic H5 clade 2.3.4.4 influenza A viruses in North American waterfowl. Proc Natl Acad Sci USA 113(32):9033–9038.  https://doi.org/10.1073/pnas.1608853113 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Song BM, Lee EK, Lee YN, Heo GB, Lee HS, Lee YJ (2017) Phylogeographical characterization of H5N8 viruses isolated from poultry and wild birds during 2014–2016 in South Korea. J Vet Sci 18(1):89–94.  https://doi.org/10.4142/jvs.2017.18.1.89 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Saito T, Tanikawa T, Uchida Y, Takemae N, Kanehira K, Tsunekuni R (2015) Intracontinental and intercontinental dissemination of Asian H5 highly pathogenic avian influenza virus (clade 2.3.4.4) in the winter of 2014–2015. Rev Med Virol 25(6):388–405.  https://doi.org/10.1002/rmv.1857 CrossRefPubMedGoogle Scholar
  24. 24.
    Si YJ, Lee IW, Kim EH, Kim YI, Kwon HI, Park SJ, Nguyen HD, Kim SM, Kwon JJ, Choi WS, Beak YH, Song MS, Kim CJ, Webby RJ, Choi YK (2017) Genetic characterisation of novel, highly pathogenic avian influenza (HPAI) H5N6 viruses isolated in birds, South Korea, November 2016. Euro Surveill.  https://doi.org/10.2807/1560-7917.ES.2017.22.1.30434 PubMedPubMedCentralGoogle Scholar
  25. 25.
    Okamatsu M, Ozawa M, Soda K, Takakuwa H, Haga A, Hiono T, Matsuu A, Uchida Y, Iwata R, Matsuno K, Kuwahara M, Yabuta T, Usui T, Ito H, Onuma M, Sakoda Y, Saito T, Otsuki K, Ito T, Kida H (2017) Characterization of highly pathogenic avian influenza virus A(H5N6), Japan, November 2016. Emerg Infect Dis 23(4):691.  https://doi.org/10.3201/eid2304.161957 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    The Ministry of the Environment J (2017) Iwatekenno shibouyatyouni okeru koubyougenseitoriinhuruenzayouseijireino yatyoukansijuutennkuikino kaijo nituite. The announcement about control area related with the HPAI cases in wild bird. http://www.env.go.jp/nature/dobutsu/bird_flu/170424_iwatekaijo.pdf
  27. 27.
    Takemae N, Tsunekuni R, Sharshov K, Tanikawa T, Uchida Y, Ito H, Soda K, Usui T, Sobolev I, Shestopalov A, Yamaguchi T, Mine J, Ito T, Saito T (2017) Five distinct reassortants of H5N6 highly pathogenic avian influenza A viruses affected Japan during the winter of 2016-2017. Virology 512:8–20.  https://doi.org/10.1016/j.virol.2017.08.035 CrossRefPubMedGoogle Scholar
  28. 28.
    Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874.  https://doi.org/10.1093/molbev/msw054 CrossRefPubMedGoogle Scholar
  29. 29.
    Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30(4):772–780.  https://doi.org/10.1093/molbev/mst010 CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214.  https://doi.org/10.1186/1471-2148-7-214 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Rambaut A, Drummond AJ (2010) FigTree 1.3.1: tree figure drawing tool. Available: http://tree.bio.ed.ac.uk/software/figtree/. Accessed 30 Jan 2018
  33. 33.
    Bielejec F, Rambaut A, Suchard MA, Lemey P (2011) SPREAD: spatial phylogenetic reconstruction of evolutionary dynamics. Bioinformatics 27(20):2910–2912.  https://doi.org/10.1093/bioinformatics/btr481 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    The Ministry of the Environment J (2017) The flying situation of migratory birds in Japan from the autumn of 2016 to the sprig of 2017. http://www.env.go.jp/nature/dobutsu/bird_flu/migratory/ap_wr_transit/index.html
  35. 35.
    de Vries E, Guo H, Dai M, Rottier PJ, van Kuppeveld FJ, de Haan CA (2015) Rapid emergence of highly pathogenic avian influenza subtypes from a subtype H5N1 hemagglutinin variant. Emerg Infect Dis 21(5):842–846.  https://doi.org/10.3201/eid2105.141927 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Bi Y, Chen Q, Wang Q, Chen J, Jin T, Wong G, Quan C, Liu J, Wu J, Yin R, Zhao L, Li M, Ding Z, Zou R, Xu W, Li H, Wang H, Tian K, Fu G, Huang Y, Shestopalov A, Li S, Xu B, Yu H, Luo T, Lu L, Xu X, Luo Y, Liu Y, Shi W, Liu D, Gao GF (2016) Genesis, evolution and prevalence of H5N6 avian influenza viruses in China. Cell Host Microbe 20(6):810–821.  https://doi.org/10.1016/j.chom.2016.10.022 CrossRefPubMedGoogle Scholar
  37. 37.
    Vijaykrishna D, Bahl J, Riley S, Duan L, Zhang JX, Chen H, Peiris JS, Smith GJ, Guan Y (2008) Evolutionary dynamics and emergence of panzootic H5N1 influenza viruses. PLoS Pathog 4(9):e1000161.  https://doi.org/10.1371/journal.ppat.1000161 CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Fusaro A, Nelson MI, Joannis T, Bertolotti L, Monne I, Salviato A, Olaleye O, Shittu I, Sulaiman L, Lombin LH, Capua I, Holmes EC, Cattoli G (2010) Evolutionary dynamics of multiple sublineages of H5N1 influenza viruses in Nigeria from 2006 to 2008. J Virol 84(7):3239–3247.  https://doi.org/10.1128/JVI.02385-09 CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Lemey P, Rambaut A, Drummond AJ, Suchard MA (2009) Bayesian phylogeography finds its roots. PLoS Comput Biol 5(9):e1000520.  https://doi.org/10.1371/journal.pcbi.1000520 CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Tian H, Zhou S, Dong L, Van Boeckel TP, Cui Y, Newman SH, Takekawa JY, Prosser DJ, Xiao X, Wu Y, Cazelles B, Huang S, Yang R, Grenfell BT, Xu B (2015) Avian influenza H5N1 viral and bird migration networks in Asia. Proc Natl Acad Sci USA 112(22):E2980.  https://doi.org/10.1073/pnas.1505041112 CrossRefPubMedGoogle Scholar
  41. 41.
    Xi Z, Liu L, Rest JS, Davis CC (2014) Coalescent versus concatenation methods and the placement of Amborella as sister to water lilies. Syst Biol 63:919–932.  https://doi.org/10.5061/dryad.qb251) CrossRefPubMedGoogle Scholar
  42. 42.
    Liu L, Xi Z, Wu S, Davis CC, Edwards SV (2015) Estimating phylogenetic trees from genome-scale data. Ann N Y Acad Sci 1360:36–53.  https://doi.org/10.1111/nyas.12747 CrossRefPubMedGoogle Scholar
  43. 43.
    Fujimoto Y, Ito H, Shinya K, Yamaguchi T, Usui T, Murase T, Ozaki H, Ono E, Takakuwa H, Otsuki K, Ito T (2010) Susceptibility of two species of wild terrestrial birds to infection with a highly pathogenic avian influenza virus of H5N1 subtype. Avian Pathol 39(2):95–98.  https://doi.org/10.1080/03079451003599268 CrossRefPubMedGoogle Scholar
  44. 44.
    Soda K, Usui T, Uno Y, Yoneda K, Yamaguchi T, Ito T (2013) Pathogenicity of an H5N1 highly pathogenic avian influenza virus isolated in the 2010–2011 winter in Japan to mandarin ducks. J Vet Med Sci 75(5):619–624.  https://doi.org/10.1292/jvms.12-0487 CrossRefPubMedGoogle Scholar
  45. 45.
    Fujimoto Y, Usui T, Ito H, Ono E, Ito T (2015) Susceptibility of wild passerines to subtype H5N1 highly pathogenic avian influenza viruses. Avian Pathol 44(4):243–247.  https://doi.org/10.1080/03079457.2015.1043235 CrossRefPubMedGoogle Scholar
  46. 46.
    Hayashi T, Hiromoto Y, Chaichoune K, Patchimasiri T, Chakritbudsabong W, Prayoonwong N, Chaisilp N, Wiriyarat W, Parchariyanon S, Ratanakorn P, Uchida Y, Saito T (2011) Host cytokine responses of pigeons infected with highly pathogenic Thai avian influenza viruses of subtype H5N1 isolated from wild birds. PLoS One 6(8):e23103.  https://doi.org/10.1371/journal.pone.0023103 CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Kang Y, Liu L, Feng M, Yuan R, Huang C, Tan Y, Gao P, Xiang D, Zhao X, Li Y, Irwin DM, Shen Y, Ren T (2017) Highly pathogenic H5N6 influenza A viruses recovered from wild birds in Guangdong, southern China, 2014–2015. Sci Rep 7:44410.  https://doi.org/10.1038/srep44410 CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Jeong J, Woo C, Ip HS, An I, Kim Y, Lee K, Jo SD, Son K, Lee S, Oem JK, Wang SJ, Kim Y, Shin J, Sleeman J, Jheong W (2017) Identification of Two novel reassortant avian influenza a (H5N6) viruses in whooper swans in Korea, 2016. Virol J 14(1):60.  https://doi.org/10.1186/s12985-017-0731-7 CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Nagy A, Machova J, Hornickova J, Tomci M, Nagl I, Horyna B, Holko I (2007) Highly pathogenic avian influenza virus subtype H5N1 in Mute swans in the Czech Republic. Vet Microbiol 120(1–2):9–16.  https://doi.org/10.1016/j.vetmic.2006.10.004 CrossRefPubMedGoogle Scholar
  50. 50.
    Božić B, Pajić M, Petrović T, Pelić M, Samojlović M, Polaček V (2016) Pthogenic change in swan infected with highly pathogenic avian influenza (H5N8) virus. Arhiv veterinarske medicine 9(2):77–86Google Scholar
  51. 51.
    Brown JD, Stallknecht DE, Swayne DE (2008) Experimental infection of swans and geese with highly pathogenic avian influenza virus (H5N1) of Asian lineage. Emerg Infect Dis 14(1):136–142.  https://doi.org/10.3201/eid1401.070740 CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Sun H, Pu J, Hu J, Liu L, Xu G, Gao GF, Liu X, Liu J (2016) Characterization of clade 2.3.4.4 highly pathogenic H5 avian influenza viruses in ducks and chickens. Vet Microbiol 182:116–122.  https://doi.org/10.1016/j.vetmic.2015.11.001 CrossRefPubMedGoogle Scholar
  53. 53.
    Gorke M, Brandl R (1986) How to live in colonies: spatial foraging strategies of the black-headed gull. Oecologia 70:288–290CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  • Ryota Tsunekuni
    • 1
  • Yuji Yaguchi
    • 2
  • Yuki Kashima
    • 2
  • Kaoru Yamashita
    • 2
  • Nobuhiro Takemae
    • 1
  • Junki Mine
    • 1
  • Taichiro Tanikawa
    • 1
  • Yuko Uchida
    • 1
  • Takehiko Saito
    • 1
  1. 1.Division of Transboundary Animal Disease, National Institute of Animal HealthNational Agriculture and Food Research OrganizationTsukubaJapan
  2. 2.Ibaraki Prefecture Kenpoku Livestock Hygiene Service CenterMitoJapan

Personalised recommendations