Surveillance of Highly Pathogenic Avian Influenza Viruses (H5Nx Subtypes) in Wild Birds in Iran, 2014-2019

Document Type : Original Articles

Authors

1 Department of clinical Science, Science & Research Branch, Islamic Azad University (IAU), Tehran, Iran

2 Department of Environment, Tehran, Iran

3 Wildlife diseases Research Laboratory, Razi Vaccine and Serum Research Institute, Agricultural Research, Education and Extension Organization (AREEO), Karaj, Iran

4 Department of Immunology, Faculty of Veterinary Medicine, University of Tehran, Iran

5 Department of Clinical Science, Faculty of Veterinary Medicine, University of Tehran, Iran

6 Research Institute of Wildlife Ecology, University of Veterinary Medicine Vienna, Austria

Abstract

After the emergence of the highly pathogenic avian influenza viruses (HPAIV) subtypes H5N6 in 2013 and H5N8 in 2014, a surveillance study using molecular epidemiology approaches was carried out during 2014 – 2019 in Iran to discover any potential introduction or outbreak of HPAIV in wild bird populations. All sick and dead wild birds found in nature, or in cases of an outbreak, a collection of representative samples was tested using the specific molecular methods for HPAIV H5 subtypes. Additionally, wild bird species in wetlands, several zoos, zoological gardens, or rehabilitation centers were tested for HPAIV. During the active surveillance plan, several individual and outbreak cases of HPAIV and orthoavulaviruses were identified. In general, more than 900 fecal materials, cloacal and oropharyngeal swabs, and/or tissue samples were collected from apparently healthy live birds representing several different species and families. In addition, tissue and swab samples were collected and investigated from any reported wild birds’ mortality cases in different parts of Iran in the framework of this study. No positive bird was found among apparently healthy live birds; however, the highly pathogenic influenza viruses of H5N1, H5N2, H5N6, and H5N8 were found in individual dead birds or mass die-off cases.

Keywords

Main Subjects


Article Title [French]

Surveillance des Virus de la Grippe Aviaire Hautement Pathogènes (Sous-Types H5Nx) chez les Oiseaux Sauvages en Iran, 2014-2019

Abstract [French]

Après l'émergence des sous-types de virus de la grippe aviaire hautement pathogène (VIAHP) H5N6 en 2013 et H5N8 en 2014, une étude de surveillance utilisant des approches d'épidémiologie moléculaire a été menée en 2014-2019 en Iran pour découvrir toute introduction ou épidémie potentielle de virus VIAHP dans les populations d'oiseaux sauvages. Tous les oiseaux sauvages malades et morts trouvés dans la nature, ou en cas d'épidémie, une collection d'échantillons représentatifs a été testée en utilisant les méthodes moléculaires spécifiques pour les sous-types VIAHP H5. De plus, des espèces d'oiseaux sauvages dans les zones humides, plusieurs zoos, jardins zoologiques ou centres de réhabilitation ont été testées pour le VIAHP. Au cours du plan de surveillance active, plusieurs cas individuels et épidémiques de VIAHP et d'orthoavulavirus ont été identifiés. En général, plus de 900 matières fécales, écouvillonnages cloacaux et oropharyngés et/ou échantillons de tissus ont été prélevés sur des oiseaux vivants apparemment en bonne santé représentant plusieurs espèces et familles différentes. En outre, des échantillons de tissus et d'écouvillons ont été collectés et étudiés à partir de tous les cas de mortalité d'oiseaux sauvages signalés dans différentes parties de l'Iran dans le cadre de cette étude. Aucun oiseau positif n'a été trouvé parmi les oiseaux vivants apparemment sains; cependant, les virus grippaux hautement pathogènes H5N1, H5N2, H5N6 et H5N8 ont été trouvés dans des oiseaux morts individuels ou dans des cas de mortalité massive.

Keywords [French]

  • virus de la grippe aviaire hautement pathogène (VIAHP)
  • Surveillance
  • oiseaux sauvages
  • épidémie
  • Iran
  1. Stallknecht DE, Brown JD. Ecology of Avian Influenza in Wild Birds. Avian Influenza2008. p. 43-58.
  2. Gu M, Zhao G, Zhao K, Zhong L, Huang J, Wan H, et al. Novel Variants of Clade 2.3.4 Highly Pathogenic Avian Influenza A(H5N1) Viruses, China. Emerg Infect Dis J. 2013;19(12):2021.
  3. Kim Y-I, Pascua PNQ, Kwon H-I, Lim G-J, Kim E-H, Yoon S-W, et al. Pathobiological features of a novel, highly pathogenic avian influenza A(H5N8) virus. Emerg Microbes Infec. 2014;3(1):1-13.
  4. Lee Y-J, Kang H-M, Lee E-K, Song B-M, Jeong J, Kwon Y-K, et al. Novel Reassortant Influenza A(H5N8) Viruses, South Korea, 2014. Emerg Infect Dis J. 2014;20(6):1086.
  5. Marchenko VY, Susloparov IM, Kolosova NP, Goncharova NI, Shipovalov AV, Durymanov AG, et al. Influenza A(H5N8) virus isolation in Russia, 2014. Arch Vir. 2015;160(11):2857-60.
  6. Bahl J, Pham TT, Hill NJ, Hussein ITM, Ma EJ, Easterday BC, et al. Ecosystem Interactions Underlie the Spread of Avian Influenza A Viruses with Pandemic Potential. Plos Pathog. 2016;12(5):e1005620.
  7. Globig A, Staubach C, Sauter-Louis C, Dietze K, Homeier-Bachmann T, Probst C, et al. Highly Pathogenic Avian Influenza H5N8 Clade 2.3.4.4b in Germany in 2016/2017. 2018;4(240).
  8. Bashashati M, Vasfi Marandi M, Sabouri F. Genetic diversity of early (1998) and recent (2010) avian influenza H9N2 virus strains isolated from poultry in Iran. Arch Vir. 2013;158(10):2089-100.
  9. Fallah Mehrabadi MH, Bahonar AR, Vasfi Marandi M, Sadrzadeh A, Tehrani F, Salman MD. Sero-survey of Avian Influenza in backyard poultry and wild bird species in Iran—2014. Prev Vet Med. 2016;128:1-5.
  10. Fereidouni SR, Werner O, Starick E, Beer M, Harder TC, Aghakhan M, et al. Avian influenza virus monitoring in wintering waterbirds in Iran, 2003-2007. Virol J. 2010;7(1):43.
  11. Vasfi Marandi M, Bozorgmehri Fard MH. Isolation of H9N2 subtype of avian influenza viruses during an outbreak in chickens in Iran. I Biomed J. 2002;6:13-7.
  12. Fereidouni SR, Harder TC, Gaidet N, Ziller M, Hoffmann B, Hammoumi S, et al. Saving resources: Avian influenza surveillance using pooled swab samples and reduced reaction volumes in real-time RT-PCR. J Virol Methods. 2012;186(1):119-25.
  13. Fereidouni SR, Harder TC, Starick E. Rapid pathotyping of recent H5N1 highly pathogenic avian influenza viruses and of H5 viruses with low pathogenicity by RT-PCR and restriction enzyme cleavage pattern (RECP). J Virol Methods. 2008;154(1):14-9.
  14. Fereidouni SR, Starick E, Grund C, Globig A, Mettenleiter TC, Beer M, et al. Rapid molecular subtyping by reverse transcription polymerase chain reaction of the neuraminidase gene of avian influenza A viruses. Vet Microbiol. 2009;135(3):253-60.
  15. Fan S, Zhou L, Wu D, Gao X, Pei E, Wang T, et al. A novel highly pathogenic H5N8 avian influenza virus isolated from a wild duck in China. Influenza Other Respir Viruses. 2014;8(6):646-53.
  16. 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. Eurosurveillance. 2015;20(12):21069.
  17. Wu H, Peng X, Xu L, Jin C, Cheng L, Lu X, et al. Novel Reassortant Influenza A(H5N8) Viruses in Domestic Ducks, Eastern China. Emerg Infect Dis J. 2014;20(8):1315.
  18. Fouchier RAM, Olsen B, Bestebroer TM, Herfst S, van der Kemp L, Rimmelzwaan GF, et al. Influenza A Virus Surveillance in Wild Birds in Northern Europe in 1999 and 2000. 2003;47. Avian Dis (s3):857-60, 4.
  19. Gaidet N, Dodman T, Caron A, Balança G, Desvaux S, Goutard F, et al. Avian Influenza Viruses in Water Birds, Africa. Emerg Infect Dis J. 2007;13(4):626.
  20. Sims L, Khomenko S, Kamata A, Belot G, Bastard J, Palamara E. H5N8 highly pathogenic avian influenza (HPAI) of clade 2.3. 4.4 detected through surveillance of wild migratory birds in theTyva Republic, the Russian Federation-potential for international spread. Empres Watch FAO. 2016;35.
  1. Ghafouri SA, GhalyanchiLangeroudi A, Maghsoudloo H, Kh Farahani R, Abdollahi H, Tehrani F, et al. Clade 2.3.4.4 avian influenza A (H5N8) outbreak in commercial poultry, Iran, 2016: the first report and update data. Trop Anim Health Pro. 2017;49(5):1089-93.
  2. Ssematimba A, Hagenaars TJ, de Wit JJ, Ruiterkamp F, Fabri TH, Stegeman JA, et al. Avian influenza transmission risks: Analysis of biosecurity measures and contact structure in Dutch poultry farming. Prev Vet Med. 2013;109(1):106-15.