Genetics of Japanese H5N8 high pathogenicity avian influenza viruses isolated in winter 2020-2021 and their genetic relationship with avian influenza viruses in Siberia.
Japan
avian flu
phylogenetic tree
phylogeography
reassortant virus
surveillance
Journal
Transboundary and emerging diseases
ISSN: 1865-1682
Titre abrégé: Transbound Emerg Dis
Pays: Germany
ID NLM: 101319538
Informations de publication
Date de publication:
Sep 2022
Sep 2022
Historique:
revised:
07
04
2022
received:
23
12
2021
accepted:
12
04
2022
pubmed:
22
4
2022
medline:
30
9
2022
entrez:
21
4
2022
Statut:
ppublish
Résumé
In winter 2020-2021, Japan experienced multiple serious outbreaks of H5N8 high pathogenicity avian influenza (HPAI)-52 outbreaks at poultry farms and 58 cases in wild birds or the environment-that occurred simultaneously with outbreaks in Europe. Here, we examined how the H5N8 HPAI viruses (HPAIVs) emerged and spread through Japan and across the Eurasian continent. Phylogenetic and phylogeographic analyses were performed using full genetic sequences of the viruses that caused 52 outbreaks at poultry farms or were isolated from 11 infected wild birds. Genetically, the viruses showed five genotypes (E1, E2, E3, E5 and E7) that have already been reported in Korea. The viruses showing the E3 genotype were found to have caused most of the HPAI outbreaks at poultry farms and were detected over the longest period of time. The internal genes of the viruses were genetically related to those of AIVs isolated through avian influenza surveillance activities in regions of Siberia including Buryatia, Yakutia and Amur regions, suggesting that the Japanese viruses emerged via reassortment events with AIVs genetically related to Siberian AIVs. In addition, H5N2 and H5N8 HPAIVs were isolated from wild birds during surveillance activities conducted in the Novosibirsk region of Siberia in summer 2020. Phylogenetic analyses revealed that these viruses possessed haemagglutinin genes that were related to those of H5N8 HPAIVs that were circulating in Europe in winter 2020-2021. These results suggest that the viruses in wild birds during summer in Siberia most likely spread in both Asia and Europe the following winter. Together, the present results emphasize the importance of continual monitoring of AIVs in Siberia for forecasting outbreaks not only in Asia but also further away in Europe.
Substances chimiques
Hemagglutinins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2195-e2213Subventions
Organisme : Russian Scientific Foundation
ID : 20-44-07001
Organisme : Ministry of Agriculture, Forestry and Fisheries of Japan (MAFF)
ID : JPJ008617.18065101
Organisme : Ministry of Agriculture, Forestry and Fisheries of Japan (MAFF)
ID : JPJ008837
Informations de copyright
© 2022 Wiley-VCH GmbH.
Références
Baek, Y. G., Lee, Y. N., Lee, D. H., Shin, J. I., Lee, J. H., Chung, D. H., Lee, E. K., Heo, G. B., Sagong, M., Kye, S. J., Lee, K. N., Lee, M. H., & Lee, Y. J. (2021). Multiple Reassortants of H5N8 Clade 2.3.4.4b Highly pathogenic avian influenza viruses detected in south Korea during the winter of 2020-2021. Viruses., 13(3), https://doi.org/10.3390/v13030490
Bielejec, F., Baele, G., Vrancken, B., Suchard, M. A., Rambaut, A., & Lemey, P. (2016). SpreaD3: Interactive visualization of spatiotemporal history and trait evolutionary processes. Molecular Biology and Evolution, 33(8), 2167-2169. https://doi.org/10.1093/molbev/msw082
Boere, G. C., & Stroud, D. A. (2006) The Flyway Concept: What it is and what it isn't. In: (Boere, G.C., Galbraith, C.A. and Stroud, D.A., Eds.), Waterbirds around the World, The Stationery Office, Edinburgh, UK, pp. 40-47.
Chen, H., Smith, G. J., Zhang, S. Y., Qin, K., Wang, J., Li, K. S., Webster, R. G., Peiris, J. S., & Guan, Y. (2005). Avian flu: H5N1 virus outbreak in migratory waterfowl. Nature, 436(7048), 191-192. https://doi.org/10.1038/nature03974
Drummond, A. J., Suchard, M. A., Xie, D., & Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29(8), 1969-1973. https://doi.org/10.1093/molbev/mss075
Ducatez, M. F., Olinger, C. M., Owoade, A. A., Tarnagda, Z., Tahita, M. C., Sow, A., De Landtsheer, S., Ammerlaan, W., Ouedraogo, J. B., Osterhaus, A. D., Fouchier, R. A., & Muller, C. P. (2007). Molecular and antigenic evolution and geographical spread of H5N1 highly pathogenic avian influenza viruses in western Africa. Journal of General Virology, 88(Pt 8), 2297-2306. https://doi.org/10.1099/vir.0.82939-0
Ellis, T. M., Bousfield, R. B., Bissett, L. A., Dyrting, K. C., Luk, G. S., Tsim, S. T., Sturm-Ramirez, K., Webster, R. G., Guan, Y., & Malik Peiris, J. S. (2004). Investigation of outbreaks of highly pathogenic H5N1 avian influenza in waterfowl and wild birds in Hong Kong in late 2002. Avian Pathology, 33(5), 492-505. https://doi.org/10.1080/03079450400003601
Hall, T. A. (1999). BioEdit: A user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95-98.
Isoda, N., Twabela, A. T., Bazarragchaa, E., Ogasawara, K., Hayashi, H., Wang, Z. J., Kobayashi, D., Watanabe, Y., Saito, K., Kida, H., & Sakoda, Y. (2020). Re-invasion of H5N8 high pathogenicity avian influenza virus clade 2.3.4.4b in Hokkaido, Japan, 2020. Viruses., 12(12), https://doi.org/10.3390/v12121439
Kanehira, K., Uchida, Y., Takemae, N., Hikono, H., Tsunekuni, R., & Saito, T. (2015). Characterization of an H5N8 influenza A virus isolated from chickens during an outbreak of severe avian influenza in Japan in April 2014. Archives of Virology, 160(7), 1629-1643. https://doi.org/10.1007/s00705-015-2428-9
Katoh, K., & Standley, D. M. (2016). A simple method to control over-alignment in the MAFFT multiple sequence alignment program. Bioinformatics, 32(13), 1933-1942. https://doi.org/10.1093/bioinformatics/btw108
Khalil, A. M., Fujimoto, Y., Kojima, I., Esaki, M., Ri, K., Masatani, T., Matsui, T., & Ozawa, M. (2021). Genetic characterization of H5N8 highly pathogenic avian influenza viruses isolated from falcated ducks and environmental water in Japan in November 2020. Pathogens, 10(2), https://doi.org/10.3390/pathogens10020171
Kilpatrick, A. M., Chmura, A. A., Gibbons, D. W., Fleischer, R. C., Marra, P. P., & Daszak, P. (2006). Predicting the global spread of H5N1 avian influenza. Proceedings of the National Academy of Sciences of the United States of America, 103(51), 19368-19373. https://doi.org/10.1073/pnas.0609227103
Lee, D. H., Criado, M. F., & Swayne, D. E. (2021). Pathobiological origins and evolutionary history of highly pathogenic avian influenza viruses. Cold Spring Harbor Perspectives in Medicine, 11(2), https://doi.org/10.1101/cshperspect.a038679
Lee, D. H., Torchetti, M. K., Winker, K., Ip, H. S., Song, C. S., & Swayne, D. E. (2015). Intercontinental spread of asian-origin H5N8 to North America through Beringia by migratory birds. Journal of Virology, 89(12), 6521-6524. https://doi.org/10.1128/JVI.00728-15
Lewis, N. S., Banyard, A. C., Whittard, E., Karibayev, T., Al Kafagi, T., Chvala, I., Byrne, A., Meruyert Akberovna, S., King, J., Harder, T., Grund, C., Essen, S., Reid, S. M., Brouwer, A., Zinyakov, N. G., Tegzhanov, A., Irza, V., Pohlmann, A., Beer, M., … Brown, I. H. (2021). Emergence and spread of novel H5N8, H5N5 and H5N1 clade 2.3.4.4 highly pathogenic avian influenza in 2020. Emerging Microbes and Infections, 10(1), 148-151. https://doi.org/10.1080/22221751.2021.1872355
Lipatov, A. S., Evseenko, V. A., Yen, H. L., Zaykovskaya, A. V., Durimanov, A. G., Zolotykh, S. I., Netesov, S. V., Drozdov, I. G., Onishchenko, G. G., Webster, R. G., & Shestopalov, A. M. (2007). Influenza (H5N1) viruses in poultry, Russian Federation, 2005-2006. Emerging Infectious Diseases, 13(4), 539-546. https://doi.org/10.3201/eid1304.061266
Mase, M., Tsukamoto, K., Imada, T., Imai, K., Tanimura, N., Nakamura, K., Yamamoto, Y., Hitomi, T., Kira, T., Nakai, T., Kiso, M., Horimoto, T., Kawaoka, Y., & Yamaguchi, S. (2005). Characterization of H5N1 influenza A viruses isolated during the 2003-2004 influenza outbreaks in Japan. Virology, 332(1), 167-176. https://doi.org/10.1016/j.virol.2004.11.016
Mine, J., Uchida, Y., Nakayama, M., Tanikawa, T., Tsunekuni, R., Sharshov, K., Takemae, N., Sobolev, I., Shestpalov, A., & Saito, T. (2019a). Genetics and pathogenicity of H5N6 highly pathogenic avian influenza viruses isolated from wild birds and a chicken in Japan during winter 2017-2018. Virology, 533, 1-11. https://doi.org/10.1016/j.virol.2019.04.011
Mine, J., Uchida, Y., Sharshov, K., Sobolev, I., Shestopalov, A., & Saito, T. (2019b). Phylogeographic evidence for the inter- and intracontinental dissemination of avian influenza viruses via migration flyways. PLoS One, 14(6), e0218506. https://doi.org/10.1371/journal.pone.0218506
Mine, J., Uchida, Y., Takemae, N., & Saito, T. (2020). Genetic characterization of influenza A viruses in Japanese swine in 2015 to 2019. Journal of Virology, 94(14), https://doi.org/10.1128/JVI.02169-19
Ozawa, M., Matsuu, A., Khalil, A. M., Nishi, N., Tokorozaki, K., Masatani, T., Horie, M., Okuya, K., Ueno, K., Kuwahara, M., & Toda, S. (2018). Phylogenetic variations of highly pathogenic H5N6 avian influenza viruses isolated from wild birds in the Izumi plain, Japan, during the 2016-17 winter season. Transboundary and Emerging Diseases, 66(2), 797-806. https://doi.org/10.1111/tbed.13087
Price, M. N., Dehal, P. S., & Arkin, A. P. (2010). FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS One, 5(3), e9490. https://doi.org/10.1371/journal.pone.0009490
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. Journal of General Virology, 93(Pt 3), 541-550. https://doi.org/10.1099/vir.0.037572-0
Sakuma, S., Uchida, Y., Kajita, M., Tanikawa, T., Mine, J., Tsunekuni, R., & Saito, T. (2021). First outbreak of an H5N8 highly pathogenic avian influenza virus on a chicken farm in Japan in 2020. Viruses., 13(3), https://doi.org/10.3390/v13030489
Sharshov, K., Sivay, M., Liu, D., Pantin-Jackwood, M., Marchenko, V., Durymanov, A., Alekseev, A., Damdindorj, T., Gao, G. F., Swayne, D. E., & Shestopalov, A. (2014). Molecular characterization and phylogenetics of a reassortant H13N8 influenza virus isolated from gulls in Mongolia. Virus Genes, 49(2), 237-249. https://doi.org/10.1007/s11262-014-1083-7
Shibata, A., Hiono, T., Fukuhara, H., Sumiyoshi, R., Ohkawara, A., Matsuno, K., Okamatsu, M., Osaka, H., & Sakoda, Y. (2018). Isolation and characterization of avian influenza viruses from raw poultry products illegally imported to Japan by international flight passengers. Transboundary and Emerging Diseases, 65(2), 465-475. https://doi.org/10.1111/tbed.12726
Shivakoti, S., Ito, H., Otsuki, K., & Ito, T. (2010). Characterization of H5N1 highly pathogenic avian influenza virus isolated from a mountain hawk eagle in Japan. Journal of Veterinary Medical Science, 72(4), 459-463. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/20009423
Sivay, M. V., Sayfutdinova, S. G., Sharshov, K. A., Alekseev, A. Y., Yurlov, A. K., Runstadler, J., & Shestopalov, A. M. (2012). Surveillance of influenza A virus in wild birds in the Asian portion of Russia in 2008. Avian Diseases, 56(3), 456-463. https://doi.org/10.1637/9868-080111-Reg.1
Smith, G. J., Donis, R. O., World Health Organization/World Organisation for Animal, H. F., & Agriculture Organization, H. E. W. G. (2015). Nomenclature updates resulting from the evolution of avian influenza A(H5) virus clades 2.1.3.2a, 2.2.1, and 2.3.4 during 2013-2014. Influenza and Other Respiratory Viruses, 9(5), 271-276. https://doi.org/10.1111/irv.12324
Sobolev, I., Sharshov, K., Dubovitskiy, N., Kurskaya, O., Alekseev, A., Leonov, S., Yushkov, Y., Irza, V., Komissarov, A., Fadeev, A., Danilenko, D., Mine, J., Tsunekuni, R., Uchida, Y., Saito, T., & Shestopalov, A. (2021). Highly pathogenic avian influenza A(H5N8) virus clade 2.3.4.4b, Western Siberia, Russia, 2020. Emerging Infectious Diseases, 27(8), 2224-2227. https://doi.org/10.3201/eid2708.204969
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
Tanikawa, T., Kanehira, K., Tsunekuni, R., Uchida, Y., Takemae, N., & Saito, T. (2016). Pathogenicity of H5N8 highly pathogenic avian influenza viruses isolated from a wild bird fecal specimen and a chicken in Japan in 2014. Microbiology and Immunology, 60(4), 243-252. https://doi.org/10.1111/1348-0421.12369
Tsunekuni, R., Hikono, H., Tanikawa, T., Kurata, R., Nakaya, T., & Saito, T. (2017). Recombinant avian paramyxovirus serotypes 2, 6, and 10 as vaccine vectors for highly pathogenic avian influenza in chickens with antibodies against newcastle disease virus. Avian Diseases, 61(3), 296-306. https://doi.org/10.1637/11512-100616-RegR1
Uchida, Y., Mase, M., Yoneda, K., Kimura, A., Obara, T., Kumagai, S., Saito, T., Yamamoto, Y., Nakamura, K., Tsukamoto, K., & Yamaguchi, S. (2008). Highly pathogenic avian influenza virus (H5N1) isolated from Whooper Swans, Japan. Emerging Infectious Diseases, 14(9), 1427-1429. https://doi.org/10.3201/eid1409.080655
Uchida, Y., Suzuki, Y., Shirakura, M., Kawaguchi, A., Nobusawa, E., Tanikawa, T., Hikono, H., Takemae, N., Mase, M., Kanehira, K., Hayashi, T., Tagawa, Y., Tashiro, M., & Saito, T. (2012). Genetics and infectivity of H5N1 highly pathogenic avian influenza viruses isolated from chickens and wild birds in Japan during 2010-11. Virus Research, 170(1-2), 109-117. https://doi.org/10.1016/j.virusres.2012.09.004
Verhagen, J. H., van der Jeugd, H. P., Nolet, B. A., Slaterus, R., Kharitonov, S. P., de Vries, P. P., Vuong, O., Majoor, F., Kuiken, T., & Fouchier, R. A. (2015). Wild bird surveillance around outbreaks of highly pathogenic avian influenza A(H5N8) virus in the Netherlands, 2014, within the context of global flyways. Euro Surveillance, 20(12), https://doi.org/10.2807/1560-7917.es2015.20.12.21069
Xu, X., Subbarao, C. N. J., & 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. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/10484749
Zhou, S., Tian, H., Wu, X., Xu, B., Yang, J., Chan, K. K., Huang, S., Dong, L., Brownstein, J., & Xu, B. (2016). Genetic evidence for avian influenza H5N1 viral transmission along the Black Sea-Mediterranean Flyway. Journal of General Virology, 97(9), 2129-2134. https://doi.org/10.1099/jgv.0.000534