Investigation of Avian Influenza Viruses (H9N2-H5nx) in Pigeons during Highly Pathogenic Avian Influenza Outbreaks in Iran, in 2016

Document Type: Original Articles

Authors

Department of Poultry Diseases Research, Razi Vaccine and Serum Research Institute, Agricultural Research, Education and Extension Organization (AREEO), Karaj, Iran

Abstract

Avian influenza (AI) virus (H9N2 and H5 subtypes) infections in birds cause major concerns around the world. The majority of the avian species, such as domestic, pet, and wild birds, are natural and experimental hosts of avian influenza viruses. There are global concerns about members of the Columbidae family, namely pigeons or doves, for their role as the potential interspecies bridge in influenza A viruses ecology. The acquired scientific data in this regard is still not clear since there are doubts about whether or not they transmit viruses between susceptible populations, and spread viruses among farms during outbreaks. To monitor H5 and H9 influenza virus infection status in the rural, backyard, and domestic birds, an annual active surveillance program was performed from September to October 2016. In December 2016, an outbreak of highly pathogenic avian influenza (HPAI) virus subtype H5N8 was detected in a layer farm in Tehran province, Iran. The present research was conducted to study H9N2 or H5 infections in pigeons within HPAI H5N8 2016 outbreaks and annual national AI surveillance in Iran. For this purpose, cloacal swabs and tissue samples (trachea, lung, brain, liver, heart, pancreas, and cecal tonsil) were collected and examined by real-time reverse transcription-polymerase chain reaction (RT-PCR) method and virus isolation. Results of the tests performed on the swab and tissue samples were negative for H5 nor H9N2 viruses. The samples in real-time RT-PCR that after three passages still showed negative results in HA and molecular tests were considered negative. Moreover, the Newcastle disease virus was isolated in most of the samples taken from dead pigeons, after inoculation in embryonated chicken eggs.

Keywords


Article Title [French]

Enquête sur les Virus de la Grippe Aviaire (H9n2-H5nx) chez les Pigeons Lors d'Épidémies de Grippe Aviaire Hautement Pathogènes en Iran, en 2016

Abstract [French]

Les infections par le virus de la grippe aviaire (sous-types H9N2 et H5) chez les oiseaux suscitent des préoccupations majeures dans le monde. La majorité des espèces aviaires, telles que les oiseaux domestiques, de compagnie et sauvages, sont des hôtes naturels et expérimentaux des virus de la grippe aviaire. Le rôle des membres de la famille des Columbidae, à savoir les pigeons ou les colombes, en tant que pont interspécifique potentiel dans l'écologie des virus de la grippe A est une préoccupation mondiale, pour. Les données scientifiques acquises à cet égard ne sont toujours pas claires, car il existe des doutes sur leur capacité à transmettre ou non des virus entre les populations sensibles et s'ils propagent des virus parmi les fermes pendant les épidémies. surv Afin d’évaluer la présence d'infection par le virus de la grippe H5 et H9 chez les oiseaux élevés en zone rurale, de basse-cour et domestiques, un programme annuel de surveillance active a été mené de septembre à octobre 2016. En décembre 2016, une épidémie du sous-type H5N8 du virus de l'influenza aviaire hautement pathogène (IAHP) a été détectée dans une ferme de poule pondeuses dans la province de Téhéran, en Iran. Cette étude a été menée afin d’évaluer la présence d’infections aux virus H9N2 ou H5 chez les pigeons dans l'épidémie de l'IAHP H5N8 2016 dans le contexte de la surveillance nationale annuelle de la grippe aviaire en Iran. À cette fin, des écouvillons cloacaux et des échantillons de tissus (trachée, poumon, cerveau, foie, cœur, pancréas et amygdales caecales) ont été collectés et examinés en temps réel par la méthode d’amplification en chaîne par polymérase couplée à une transcription inverse (RT-PCR) suivi de l'isolement du virus. Les résultats des tests effectués sur l'écouvillon et les échantillons de tissus étaient négatifs pour les virus H5 et H9N2. Les échantillons en RT-PCR en temps réel qui, après trois passages, montraient toujours des résultats négatifs en HA et des tests moléculaires étaient considérés comme négatifs. De plus, le virus de la maladie de Newcastle a été isolé dans la plupart des échantillons prélevés sur des pigeons morts, après inoculation dans des œufs de poule embryonnés.

Keywords [French]

  • Épidémie de H5
  • pigeon
  • TI-RCP en temps réel
  • Surveillance en Iran
Abolnik, C., 2014. A current review of avian influenza in pigeons and doves (Columbidae). Vet Microbiol 170, 181-196.

Alquttory, M., Ellakany, H.F., Ibrahim, M.S., 2016. Pigeon-Derived Highly Pathogenic Avian Influenza Virus H5N1 in Japanese Quails. Alexandria J Vet Sci 50, 109-114.

Boon, A.C., Sandbulte, M.R., Seiler, P., Webby, R.J., Songserm, T., Guan, Y., et al., 2007. Role of terrestrial wild birds in ecology of influenza A virus (H5N1). Emerg Infect Dis 13, 1720-1724.

Brown, J.D., Stallknecht, D.E., Berghaus, R.D., Swayne, D.E., 2009. Infectious and lethal doses of H5N1 highly pathogenic avian influenza virus for house sparrows (Passer domesticus) and rock pigeons (Columbia livia). J Vet Diagn Invest 21, 437-445.

Capua, I., Alexander, D.J., 2009. Avian influenza and Newcastle disease: a field and laboratory manual, Springer Science & Business Media, Berlin, Germany.

Ellis, T.M., Bousfield, R.B., Bissett, L.A., Dyrting, K.C., Luk, G.S., Tsim, S.T., et al., 2004. Investigation of outbreaks of highly pathogenic H5N1 avian influenza in waterfowl and wild birds in Hong Kong in late 2002. Avian Pathol 33, 492-505.

Fallah Mehrabadi, M.H., Bahonar, A.R., Vasfi Marandi, M., Sadrzadeh, A., Tehrani, F., Salman, M.D., 2016. Sero-survey of Avian Influenza in backyard poultry and wild bird species in Iran-2014. Prev Vet Med 128, 1-5.

Fang, T.H., Lien, Y.Y., Cheng, M.C., Tsai, H.J., 2006. Resistance of immune-suppressed pigeons to subtypes H5N2 and H6N1 low pathogenic avian influenza virus. Avian Dis 50, 269-272.

Franca, M., Stallknecht, D.E., Howerth, E.W., 2013. Expression and distribution of sialic acid influenza virus receptors in wild birds. Avian Pathol 42, 60-71.

Hayashi, T., Hiromoto, Y., Chaichoune, K., Patchimasiri, T., Chakritbudsabong, W., Prayoonwong, N., et al., 2011. Host cytokine responses of pigeons infected with highly pathogenic Thai avian influenza viruses of subtype H5N1 isolated from wild birds. PLoS One 6, e23103.

Hitchner, S., Domermuth, C., Purchase, H., Williams, J., 1980. Virus propagation in embryonating eggs. Isolation Identificat Avian Pathogens 2, 312-314.

Jia, B., Shi, J., Li, Y., Shinya, K., Muramoto, Y., Zeng, X., et al., 2008. Pathogenicity of Chinese H5N1 highly pathogenic avian influenza viruses in pigeons. Arch Virol 153, 1821-1826.

Kaleta, E.F., Honicke, A., 2004. Review of the literature on avian influenza A viruses in pigeons and experimental studies on the susceptibility of domestic pigeons to influenza A viruses of the haemagglutinin subtype H7. Dtsch Tierarztl Wochenschr 111, 467-472.

Klopfleisch, R., Werner, O., Mundt, E., Harder, T., Teifke, J.P., 2006. Neurotropism of highly pathogenic avian influenza virus A/chicken/Indonesia/2003 (H5N1) in experimentally infected pigeons (Columbia livia f. domestica). Vet Pathol 43, 463-470.

Kwon, J.H., Noh, Y.K., Lee, D.H., Yuk, S.S., Erdene-Ochir, T.O., Noh, J.Y., et al., 2017. Experimental infection with highly pathogenic H5N8 avian influenza viruses in the Mandarin duck (Aix galericulata) and domestic pigeon (Columba livia domestica). Vet Microbiol 203, 95-102.

Liu, Y., Zhou, J., Yang, H., Yao, W., Bu, W., Yang, B., et al., 2007. Susceptibility and transmissibility of pigeons to Asian lineage highly pathogenic avian influenza virus subtype H5N1. Avian Pathol 36, 461-465.

Mansour, S.M., ElBakrey, R.M., Ali, H., Knudsen, D.E., Eid, A.A., 2014. Natural infection with highly pathogenic avian influenza virus H5N1 in domestic pigeons (Columba livia) in Egypt. Avian Pathol 43, 319-324.

Monne, I., Ormelli, S., Salviato, A., De Battisti, C., Bettini, F., Salomoni, A., et al., 2008. Development and validation of a one-step real-time PCR assay for simultaneous detection of subtype H5, H7, and H9 avian influenza viruses. J Clin Microbiol 46, 1769-1773.

OIE, A., 2015. Manual of diagnostic tests and vaccines for terrestrial animals, Office International des Epizooties, Paris, France.

OIE, W., 2017. Update on highly pathogenic avian influenza in animals (type H5 and H7). Office International des Epizooties, Paris, France.

Panigrahy, B., Senne, D.A., Pedersen, J.C., Shafer, A.L., Pearson, J.E., 1996. Susceptibility of pigeons to avian influenza. Avian Dis 40, 600-604.

Pantin-Jackwood, M.J., Swayne, D.E., 2009. Pathogenesis and pathobiology of avian influenza virus infection in birds. Rev Sci Tech 28, 113-136.

Perkins, L.E., Swayne, D.E., 2002. Pathogenicity of a Hong Kong-origin H5N1 highly pathogenic avian influenza virus for emus, geese, ducks, and pigeons. Avian Dis 46, 53-63.

Perkins, L.E., Swayne, D.E., 2003. Varied pathogenicity of a Hong Kong-origin H5N1 avian influenza virus in four passerine species and budgerigars. Vet Pathol 40, 14-24.

Petersen, H., Matrosovich, M., Pleschka, S., Rautenschlein, S., 2012. Replication and adaptive mutations of low pathogenic avian influenza viruses in tracheal organ cultures of different avian species. PLoS One 7, e42260.

Siengsanan-Lamont, J., Robertson, I., Blacksell, S.D., Ellis, T., Fenwick, S., Saengchoowong, S., et al., 2011. Virological and molecular epidemiological investigations into the role of wild birds in the epidemiology of influenza A/H5N1 in central Thailand. Vet Microbiol 148, 213-218.

Smietanka, K., Minta, Z., Wyrostek, K., Jozwiak, M., Olszewska, M., Domanska-Blicharz, A.K., et al., 2011. Susceptibility of pigeons to clade 1 and 2.2 high pathogenicity avian influenza H5N1 virus. Avian Dis 55, 106-112.

Sturm-Ramirez, K.M., Ellis, T., Bousfield, B., Bissett, L., Dyrting, K., Rehg, J.E., et al., 2004. Reemerging H5N1 influenza viruses in Hong Kong in 2002 are highly pathogenic to ducks. J Virol 78, 4892-4901.

Swayne, D., Suarez, D., 2000. Highly pathogenic avian influenza. Rev Sci Techniq Office Int Epiz 19, 463-475.

Swayne, D.E., Senne, D.A., Suarez, D.L., 2008. Avian influenza. In: Dufour-Zavala, L., Swayne, D., Gilsson, J. (Eds.), Isolation, identification and characteruzation of Avian pathogens, American Association of Avian Pathologists, Athens, Georgia, pp. 128-134.

Werner, O., Starick, E., Teifke, J., Klopfleisch, R., Prajitno, T.Y., Beer, M., et al., 2007. Minute excretion of highly pathogenic avian influenza virus A/chicken/Indonesia/2003 (H5N1) from experimentally infected domestic pigeons (Columbia livia) and lack of transmission to sentinel chickens. J Gen Virol 88, 3089-3093.

Yamamoto, Y., Nakamura, K., Yamada, M., Mase, M., 2012. Limited susceptibility of pigeons experimentally inoculated with H5N1 highly pathogenic avian influenza viruses. J Vet Med Sci 74, 205-208.