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Volume 27, Number 2—February 2021
Research

Highly Pathogenic Avian Influenza A(H5N8) Virus Spread by Short- and Long-Range Transmission, France, 2016–17

François-Xavier BriandComments to Author , Eric Niqueux, Audrey Schmitz, Claire Martenot, Martine Cherbonnel, Pascale Massin, Florian Kerbrat, Marina Chatel, Carole Guillemoto, Cecile Guillou-Cloarec, Katell Ogor, Aurélie Le Prioux, Chantal Allée, Véronique Beven, Edouard Hirchaud, Yannick Blanchard, Axelle Scoizec, Sophie Le Bouquin, Nicolas Eterradossi, and Béatrice Grasland
Author affiliation: Agence Nationale de Sécurité Sanitaire
de l’Alimentation, de l’Environnement et du Travail, Ploufragan, France

Main Article

Figure 4

Maximum credibility tree of the 8 concatenated gene segments in highly pathogenic avian influenza H5N8 genotype A viruses, France, 2016–17. Tree generated using SDR06 model according to Bayesian method (38). Branch and leaf color indicates geoclusters. The estimated dates of common ancestors and their 95% CIs are indicated for geocluster 1 and geocluster 5

Figure 4. Maximum credibility tree of the 8 concatenated gene segments in highly pathogenic avian influenza H5N8 genotype A viruses, France, 2016–17. Tree generated using SDR06 model according to Bayesian method (38). Branch and leaf color indicates geoclusters. The estimated dates of common ancestors and their 95% CIs are indicated for geocluster 1 and geocluster 5

Main Article

References
  1. Olsen  B, Munster  VJ, Wallensten  A, Waldenström  J, Osterhaus  AD, Fouchier  RA. Global patterns of influenza a virus in wild birds. Science. 2006;312:384–8. DOIPubMedGoogle Scholar
  2. Nao  N, Yamagishi  J, Miyamoto  H, Igarashi  M, Manzoor  R, Ohnuma  A, et al. Genetic predisposition to acquire a polybasic cleavage site for highly pathogenic avian influenza virus hemagglutinin. MBio. 2017;8:e02298–16. DOIPubMedGoogle Scholar
  3. OFFLU. Influenza A cleavage sites. 2020 Jul 8 [cited 2020 Nov 30]. http://www.offlu.net/fileadmin/home/en/resource-centre/pdf/Influenza_A_Cleavage_Sites.pdf
  4. Pantin-Jackwood  MJ, Swayne  DE. Pathogenesis and pathobiology of avian influenza virus infection in birds. Rev Sci Tech. 2009;28:113–36. DOIPubMedGoogle Scholar
  5. Lee  DH, Criado  MF, Swayne  DE. Pathobiological origins and evolutionary history of highly pathogenic avian influenza viruses. Cold Spring Harb Perspect Med. 2020 Jan 21 [Epub ahead of print].
  6. European Commission. Council directive 2005/94/EC on community measures for the control of avian influenza and repealing directive 92/40/EEC. 2019 Jan 1 [cited 2020 Nov 30]. https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=celex%3A32005L0094
  7. WHO/OIE/FAO H5N1 Evolution Working Group. Toward a unified nomenclature system for highly pathogenic avian influenza virus (H5N1). Emerg Infect Dis. 2008;14:e1. DOIPubMedGoogle Scholar
  8. Fusaro  A, Zecchin  B, Vrancken  B, Abolnik  C, Ademun  R, Alassane  A, et al. Disentangling the role of Africa in the global spread of H5 highly pathogenic avian influenza. Nat Commun. 2019;10:5310. DOIPubMedGoogle Scholar
  9. Saito  T, Tanikawa  T, Uchida  Y, Takemae  N, Kanehira  K, Tsunekuni  R. 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. 2015;25:388–405. DOIPubMedGoogle Scholar
  10. Lee  DH, Torchetti  MK, Winker  K, Ip  HS, Song  CS, Swayne  DE. Intercontinental spread of Asian-origin H5N8 to North America through Beringia by migratory birds. J Virol. 2015;89:6521–4. DOIPubMedGoogle Scholar
  11. Lee  DH, Bertran  K, Kwon  JH, Swayne  DE. Evolution, global spread, and pathogenicity of highly pathogenic avian influenza H5Nx clade 2.3.4.4. J Vet Sci. 2017;18(S1):269–80. DOIPubMedGoogle Scholar
  12. Cattoli  G, Fusaro  A, Monne  I, Capua  I. H5N1 virus evolution in Europe—an updated overview. Viruses. 2009;1:1351–63. DOIPubMedGoogle Scholar
  13. Global Consortium for H5N8 and Related Influenza Viruses. Role for migratory wild birds in the global spread of avian influenza H5N8. Science. 2016;354:213–7. DOIPubMedGoogle Scholar
  14. King  J, Schulze  C, Engelhardt  A, Hlinak  A, Lennermann  SL, Rigbers  K, et al. Novel HPAIV H5N8 reassortant (clade 2.3.4.4b) detected in Germany. Viruses. 2020;12:281. DOIPubMedGoogle Scholar
  15. Hill  NJ, Hussein  IT, Davis  KR, Ma  EJ, Spivey  TJ, Ramey  AM, et al. Reassortment of influenza A viruses in wild birds in Alaska before H5 clade 2.3.4.4 outbreaks. Emerg Infect Dis. 2017;23:654–7. DOIPubMedGoogle Scholar
  16. Antigua  KJC, Choi  WS, Baek  YH, Song  MS. The emergence and decennary distribution of clade 2.3.4.4 HPAI H5Nx. Microorganisms. 2019;7:156. DOIPubMedGoogle Scholar
  17. Pohlmann  A, Starick  E, Grund  C, Höper  D, Strebelow  G, Globig  A, et al. Swarm incursions of reassortants of highly pathogenic avian influenza virus strains H5N8 and H5N5, clade 2.3.4.4b, Germany, winter 2016/17. Sci Rep. 2018;8:15. DOIPubMedGoogle Scholar
  18. Brown  I, Kuiken  T, Mulatti  P, Smietanka  K, Staubach  C, Stroud  D, et al.; European Food Safety Authority; European Centre for Disease Prevention and Control; European Union Reference Laboratory for Avian influenza. Avian influenza overview September - November 2017. EFSA J. 2017;15:e05141.PubMedGoogle Scholar
  19. Lycett  SJ, Pohlmann  A, Staubach  C, Caliendo  V, Woolhouse  M, Beer  M, et al.; Global Consortium for H5N8 and Related Influenza Viruses. Genesis and spread of multiple reassortants during the 2016/2017 H5 avian influenza epidemic in Eurasia. Proc Natl Acad Sci U S A. 2020;117:20814–25. DOIPubMedGoogle Scholar
  20. Guinat  C, Nicolas  G, Vergne  T, Bronner  A, Durand  B, Courcoul  A, et al. Spatio-temporal patterns of highly pathogenic avian influenza virus subtype H5N8 spread, France, 2016 to 2017. Euro Surveill. 2018;23.
  21. Bronner  A, Niqueux  E, Schmitz  A, Le Bouquin  S, Huneau-Salaûn  A, Guinat  C, et al. Description of the highly pathogenic avian influenza episode in France in 2016–2017 [in French]. Bulletin épidémiologique, santé animale et alimentation. 2017;79:13–7.
  22. Slomka  MJ, Coward  VJ, Banks  J, Löndt  BZ, Brown  IH, Voermans  J, et al. Identification of sensitive and specific avian influenza polymerase chain reaction methods through blind ring trials organized in the European Union. Avian Dis. 2007;51(Suppl):227–34. DOIPubMedGoogle Scholar
  23. Zhou  B, Donnelly  ME, Scholes  DT, St George  K, Hatta  M, Kawaoka  Y, et al. Single-reaction genomic amplification accelerates sequencing and vaccine production for classical and Swine origin human influenza a viruses. J Virol. 2009;83:10309–13. DOIPubMedGoogle Scholar
  24. Briand  FX, Schmitz  A, Ogor  K, Le Prioux  A, Guillou-Cloarec  C, Guillemoto  C, et al. Emerging highly pathogenic H5 avian influenza viruses in France during winter 2015/16: phylogenetic analyses and markers for zoonotic potential. Euro Surveill. 2017;22:30473. DOIPubMedGoogle Scholar
  25. Langmead  B, Salzberg  SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357–9. DOIPubMedGoogle Scholar
  26. Kumar  S, Stecher  G, Tamura  K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016;33:1870–4. DOIPubMedGoogle Scholar
  27. Martin  DP, Murrell  B, Golden  M, Khoosal  A, Muhire  B. RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol. 2015;1:vev003.
  28. Drummond  AJ, Suchard  MA, Xie  D, Rambaut  A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012;29:1969–73. DOIPubMedGoogle Scholar
  29. Baele  G, Lemey  P, Bedford  T, Rambaut  A, Suchard  MA, Alekseyenko  AV. Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. Mol Biol Evol. 2012;29:2157–67. DOIPubMedGoogle Scholar
  30. Hill  V, Baele  G. Bayesian estimation of past population dynamics in BEAST 1.10 using the Skygrid coalescent model. Mol Biol Evol. 2019;36:msz172.
  31. Lanfear  R, Hua  X, Warren  DL. Estimating the effective sample size of tree topologies from Bayesian phylogenetic analyses. Genome Biol Evol. 2016;8:2319–32. DOIPubMedGoogle Scholar
  32. Vaughan  TG. IcyTree: rapid browser-based visualization for phylogenetic trees and networks. Bioinformatics. 2017;33:2392–4. DOIPubMedGoogle Scholar
  33. Leigh  J, Bryant  D. POPART: full-feature software for haplotype network construction. Methods Ecol Evol. 2015;6:1110–6. DOIGoogle Scholar
  34. Agence nationale de sécurité sanitaire de l’alimentation, de l’environnement et du travail. Assessing avian influenza risk levels and their evolution [in French]. 2017 [cited 2017 Nov 07]. https://www.anses.fr/fr/system/files/SABA2017SA0203-partie2.pdf
  35. Fusaro  A, Monne  I, Mulatti  P, Zecchin  B, Bonfanti  L, Ormelli  S, et al. Genetic diversity of highly pathogenic avian influenza A(H5N8/H5N5) viruses in Italy, 2016–17. Emerg Infect Dis. 2017;23:1543–7. DOIPubMedGoogle Scholar
  36. Świętoń  E, Śmietanka  K. Phylogenetic and molecular analysis of highly pathogenic avian influenza H5N8 and H5N5 viruses detected in Poland in 2016-2017. Transbound Emerg Dis. 2018;65:1664–70. DOIPubMedGoogle Scholar
  37. Savić  V. Novel reassortant clade 2.3.4.4 avian influenza A(H5N5) virus in wild birds and poultry, Croatia, 2016–2017. Vet Arh. 2017;87:377–96. DOIGoogle Scholar
  38. Shapiro  B, Rambaut  A, Drummond  AJ. Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. Mol Biol Evol. 2006;23:7–9. DOIPubMedGoogle Scholar
  39. Souvestre  M, Guinat  C, Niqueux  E, Robertet  L, Croville  G, Paul  M, et al. Role of backyard flocks in transmission dynamics of highly pathogenic avian influenza A(H5N8) clade 2.3.4.4, France, 2016–2017. Emerg Infect Dis. 2019;25:551–4. DOIPubMedGoogle Scholar
  40. Moisson  M, Hamon  M, Malhere  C, Donguy  M, Niqueux  E, Scoizec  A, et al. The situation of HP H5N8 avian influenza in France as of 05/12/2016. 2016 [cited 2016 Dec 06]. https://www.plateforme-esa.fr/article/situation-de-l-influenza-aviaire-hp-h5n8-en-france-au-05122016
  41. Andronico  A, Courcoul  A, Bronner  A, Scoizec  A, Lebouquin-Leneveu  S, Guinat  C, et al. Highly pathogenic avian influenza H5N8 in south-west France 2016-2017: A modeling study of control strategies. Epidemics. 2019;28:100340. DOIPubMedGoogle Scholar
  42. Guinat  C, Artois  J, Bronner  A, Guérin  JL, Gilbert  M, Paul  MC. Duck production systems and highly pathogenic avian influenza H5N8 in France, 2016-2017. Sci Rep. 2019;9:6177. DOIPubMedGoogle Scholar

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Page created: December 07, 2020
Page updated: January 23, 2021
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