Characterization of clade 2.3.2.1 H5N1 highly pathogenic avian influenza viruses isolated from wild birds (mandarin duck and Eurasian eagle owl) in 2010 in Korea

Viruses

Volumn 5, Issue 4, 2013, Pages 1153-1174

  Choi, Jun Gu ^a   Kang, Hyun Mi ^a   Jeon, Woo Jin ^a   Choi, Kang Seuk ^a   Kim, Kwang Il ^a   Song, Byung Min ^a   Lee, Hee Soo ^a   Kim, Jae Hong ^b   Lee, Youn Jeong ^a  

^a Animal Plant and Fisheries Quarantine and Inspection Agency   (South Korea)

^b Seoul National University   (South Korea)

Author keywords

Clade 2.3.2.1; H5n1; Highly pathogenic avian influenza

Indexed keywords

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AVIAN INFLUENZA VIRUS; BIRD DISEASE; CLADISTICS; CONTROLLED STUDY; DUCKS AND GEESE; EPIDEMIC; FECES ANALYSIS; FEMALE; GENETIC ANALYSIS; GENETIC SIMILARITY; INFLUENZA VIRUS A H5N1; KOREA; MOUSE; NONHUMAN; OWL; PHYLOGENY; SURVIVAL RATE; VIRAL GENETICS; VIRUS ISOLATION; VIRUS REPLICATION; VIRUS VIRULENCE; WEIGHT CHANGE;

ANIMALS; BODY WEIGHT; CHICKENS; DISEASE OUTBREAKS; DUCKS; FEMALE; GENOTYPE; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA IN BIRDS; MICE; PHYLOGENY; REPUBLIC OF KOREA; STRIGIFORMES; VIRUS REPLICATION;

AIX GALERICULATA; ANAS; ANIMALIA; AVES; AVIAN INFLUENZA VIRUS; GALLUS GALLUS; MUS; RAPTORES; STRIGIFORMES;

EID: 84876706454     PISSN: 19994915     EISSN: None     Source Type: Journal    
DOI: 10.3390/v5041153     Document Type: Article

References (47)

1. FAO/OIE/WHO, FAO-OIE-WHO Technical update: Current evolution of avian influenza H5N1 viruses. 7 September 2011.(http://www.oie.int/doc/ged/D11128.PDF)
2. Li, Y.; Shi, J.; Zhong, G.; Deng, G.; Tian, G.; Ge, J.; Zeng, X.; Song, J.; Zhao, D.; Liu, L.; Jiang, Y.; Guan, Y.; Bu, Z.; Chen, H. Continued evolution of H5N1 influenza viruses in wild birds, domestic poultry, and humans in China from 2004 to 2009. J. Virol. 2010,84, 8389-8397.
3. Jiang, W.-M.; Liu, S.; Chen, J.; Hou, G.-Y.; Li, J.-P.; Cao, Y.-F.; Zhuang, Q.-Y.; Li, Y.; Huang, B.-X.; Chen, J.-M. Molecular epidemiological surveys of H5 subtype highly pathogenic avian influenza viruses in poultry in China during 2007-2009. J.Gen.Virol.2010,91, 2491-2496.
4. Jadhao, S.; Nguyen, D.; Uyeki, T.; Shaw, M.; Maines, T.; Rowe, T.; Smith, C.; Huynh, L.; Nghiem, H.; Nguyen, D.; Nguyen, H.; Nguyen, H.; Hoang, L.; Nguyen, T.; Phuong, L.; Klimov, A.; Tumpey, T.; Cox, N.; Donis, R.; Matsuoka, Y.; Katz, J. Genetic analysis of avian influenza Aviruses isolated from domestic waterfowl in live-bird markets of Hanoi, Vietnam, preceding fatalH5N1 human infections in 2004. Arch.Virol. 2009,154, 1249-1261.
5. Kayali, G.; El-Shesheny, R.; Kutkat, M.A.; Kandeil, A.M.; Mostafa, A.; Ducatez, M.F.; McKenzie, P.P.; Govorkova, E.A.; Nasraa, M.H.; Webster, R.G.; Webby, R.J.; Ali, M.A. Continuing threat of influenza (H5N1) virus circulation in Egypt. Emerg.Infect.Dis.2011,17, 2306-2308.
6. Islam, M.R.; Haque, M.E.; Giasuddin, M.; Chowdhury, E.H.; Samad, M.A.; Parvin, R.; Nooruzzaman, M.; Rahman, M.M.; Monoura, P. New introduction of clade 2.3.2.1 avian influenza virus (H5N1) into Bangladesh. Transbound.Emerg.Dis.2012, 59, 460-463.
7. WHO/OIE/FAO H5N1 Evolution Working Group, Continued evolution of highly pathogenic avian influenza A (H5N1): updated nomenclature. Influenza Other Respi.Viruses 2012,6, 1-5.
8. Xu, X.; Subbarao, K.; Cox, N.J.; Guo, Y. Genetic characterization of the pathogenic influenza A/Goose/Guangdong/1/96 (H5N1) virus: similarity of its hemagglutiningene to those of H5N1 viruses from the 1997 outbreaks in Hong Kong. Virol.1999,261, 15-19.
9. Webster, R.G.; Bean, W.J.; Gorman, O.T.; Chambers, T.M.; Kawaoka, Y. Evolution and ecology of influenza A viruses. Microbiol.Rev.1992,56, 152-179.
10. Ellis, T.M.; Barry Bousfield, R.; Bissett, L.A.; Dyrting, K.C.; Luk, G.S.M.; Tsim, S.T.; Sturm-ramirez, K.; Webster, R.G.; Guan, Y.; Peiris, J.S.M. Investigation of outbreaks of highly pathogenic H5N1 avian influenza in waterfowl and wild birds in Hong Kong in late 2002. Avian Pathol.2004,33, 492-505.
11. Chen, H.; Li, Y.; Li, Z.; Shi, J.; Shinya, K.; Deng, G.; Qi, Q.; Tian, G.; Fan, S.; Zhao, H.; Sun, Y.; Kawaoka, Y. Properties and dissemination of H5N1 viruses isolated during an influenza outbreak in migratory waterfowl in western China. J.Virol.2006,80, 5976-5983.
12. Chen, H.; Smith, G.J.D.; Zhang, S.Y.; Qin, K.; Wang, J.; Li, K.S.; Webster, R.G.; Peiris, J.S.M.; Guan, Y. Avian flu H5N1 virus outbreak in migratory waterfowl. Nature 2005,436, 191-192.
13. Li, Y.; Liu, L.; Zhang, Y.; Duan, Z.; Tian, G.; Zeng, X.; Shi, J.; Zhang, L.; Chen, H. New avian influenza virus (H5N1) in wild birds, Qinghai, China. Emerg.Infect.Dis.2011,17, 265-267.
14. Sakoda, Y.; Sugar, S.; Batchluun, D.; Erdene-Ochir, T.-O.; Okamatsu, M.; Isoda, N.; Soda, K.; Takakuwa, H.; Tsuda, Y.; Yamamoto, N.; Kishida, N.; Matsuno, K.; Nakayama, E.; Kajihara, M.; Yokoyama, A.; Takada, A.; Sodnomdarjaa, R.; Kida, H. Characterization of H5N1 highly pathogenic avian influenza virus strains isolated from migratory waterfowl in Mongolia on the way back from the southern Asia to their northern territory. Virol.2010,406, 88-94.
15. Lee, C.-W.; Suarez, D.L.; Tumpey, T.M.; Sung, H.-W.; Kwon, Y.-K.; Lee, Y.-J.; Choi, J.-G.; Joh, S.-J.; Kim, M.-C.; Lee, E.-K.; Park, J.-M.; Lu, X.; Katz, J.M.; Spackman, E.; Swayne, D.E.; Kim, J.-H. Characterization of highly pathogenic H5N1 avian influenza A viruses isolated from South Korea. J. Virol. 2005, 79, 3692-3702.
16. Lee, Y.J.; Choi, Y.K.; Kim, Y.J.; Song, M.S.; Jeong, O.M.; Lee, E.K.; Jeon, W.J.; Jeong, W.; Joh, S.J.; Choi, K.S.; Her, M.; Kim, M.C.; Kim, A.; Kim, M.J.; Ho Lee, E.; Oh, T.G.; Moon, H.J.; Yoo, D.W.; Kim, J.H.; Sung, M.H.; Poo, H.; Kwon, J.H.; Kim, C.J. Highly pathogenic avian influenza virus (H5N1) in domestic poultry and relationship with migratory birds, South Korea. Emerg.Infect.Dis.2008,14, 487-490.
17. Kim, H.-R.; Park, C.-K.; Lee, Y.-J.; Woo, G.-H.; Lee, K.-K.; Oem, J.-K.; Kim, S.-H.; Jean, Y.-H.; Bae, Y.-C.; Yoon, S.-S.; Roh, I.-S.; Jeong, O.-M.; Kim, H.-Y.; Choi, J.-S.; Byun, J.-W.; Song, Y.-K.; Kwon, J.-H.; Joo, Y.-S. An outbreak of highly pathogenic H5N1 avian influenza in Korea, 2008. Vet.Microbiol.2010,141, 362-366.
18. Kim, H.-R.; Lee, Y.-J.; Park, C.-K.; Oem, J.-K.; Lee, O.-S.; Kang, H.-M.; Choi, J.-G.; Bae, Y.-C. Highly pathogenic avian influenza (H5N1) outbreaks in wild birds and poultry, South Korea. Emerg.Infect.Dis.2012, 18, 480-483.
19. Lee, D.-H.; Park, J.-K.; Youn, H.-N.; Lee, Y.-N.; Lim, T.-H.; Kim, M.-S.; Lee, J.-B.; Park, S.-Y.; Choi, I.-S.; Song, C.-S. Surveillance and isolation of HPAI H5N1 from wild mandarin ducks (Aix galericulata). J.Wildlife Dis.2011,47, 994-998.
20. Kim, H.-R.; Kim, B.-S.; Bae, Y.-C.; Moon, O.-K.; Oem, J.-K.; Kang, H.-M.; Choi, J.-G.; Lee, O.S.; Lee, Y.-J. H5N1 subtype highly pathogenic avian influenza virus isolated from healthy mallard captured in South Korea. Vet.Microbiol.2011,151, 386-389.
21. Kang, H.-M.; Batchuluun, D.; Kim, M.-C.; Choi, J.-G.; Erdene-Ochir, T.-O.; Paek, M.-R.; Sugir, T.; Sodnomdarjaa, R.; Kwon, J.-H.; Lee, Y.-J. Genetic analyses of H5N1 avian influenza virus in Mongolia, 2009 and its relationship with those of eastern Asia. Vet.Microbiol.2011,147, 170-175.
22. 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. Reintroduction of H5N1 highly pathogenic avian influenza virus by migratory water birds, causing poultry outbreaks in 2010-2011 winter season in Japan. J.Gen.Virol.2012,93, 541-550.
23. Sharshov, K.; Silko, N.; Sousloparov, I.; Zaykovskaya, A.; Shestopalov, A.; Drozdov, I., Avian influenza (H5N1) outbreak among wild birds, Russia, 2009. Emerg.Infect.Dis.2010, 16, 349-351.
24. Song, J.; Feng, H.; Xu, J.; Zhao, D.; Shi, J.; Li, Y.; Deng, G.; Jiang, Y.; Li, X.; Zhu, P.; Guan, Y.; Bu, Z.; Kawaoka, Y.; Chen, H. The PA protein directly contributes to the virulence of H5N1 avian influenza viruses in domestic ducks. J. Virol. 2011, 85, 2180-2188.
25. Choi, C.-Y.; Nam, H.-Y.; Lee, W.-S. Diets and foraging tactics of Eurasian eagle owls (Bubo bubo) in two different habitat types. Kor.J.Env.Eco.2007,21, 30-37.
26. Keawcharoen, J.; van Riel, D.; van Amerongen, G.; Bestebroer, T.; Beyer, W.E.; van Lavieren, R.; Osterhaus, A.D.; Fouchier, R.A.; Kuiken, T. Wild ducks as long-distance vectors of highly pathogenic avian influenza virus (H5N1). Emerg.Infect.Dis.2008,14, 600-607.
27. Kwon, Y.K.; Thomas, C.; Swayne, D.E. Variability in pathobiology of South Korean H5N1 high-pathogenicity avian influenza virus infection for 5 species of migratory waterfowl. Vet. Pathol.Online 2010, 47, 495-506.
28. Jeong, O.M.; Kim, M.C.; Kim, M.J.; Kang, H.M.; Kim, H.R.; Kim, Y.J.; Joh, S.J.; Kwon, J.H.; Lee, Y.J. Experimental infection of chickens, ducks and quails with the highly pathogenic H5N1 avian influenza virus. J.Vet.Sci.2009,10, 53-60.
29. Lee, Y.-J.; Kang, H.-M.; Choi, J.-G.; Jeong, O.-M.; Kim, M.-C.; Paek, M.-R.; Kim, H.-R.; Park, C.-K.; Jean, Y.-H.; Roh, I.-S.; Joo, Y.-S.; Kwon, J.-H. Higher virulence of the Korean clade 2.3.2.1 highly pathogenic avian influenza A (H5N1) virus isolated in 2008 in young duckling. J.Zoonoses 2011,2, 21-27.
30. Pantin-Jackwood, M.J.; Suarez, D.L.; Spackman, E.; Swayne, D.E. Age at infection affects the pathogenicity of Asian highly pathogenic avian influenza H5N1 viruses in ducks. Virus Res.2007,130, 151-161.
31. Isoda, N.; Sakoda, Y.; Kishida, N.; Bai, G.R.; Matsuda, K.; Umemura, T.; Kida, H. Pathogenicity of a highly pathogenic avian influenza virus, A/chicken/Yamaguchi/7/04 (H5N1) in different species of birds and mammals. Arch.Virol.2006,151, 1267-1279.
32. Pantin-Jackwood, M.J.; Smith, D.M.; Wasilenko, J.L.; Cagle, C.; Shepherd, E.; Sarmento, L.; Kapczynski, D.R.; Afonso, C.L. Effect of age on the pathogenesis and innate immune responses in Pekin ducks infected with different H5N1 highly pathogenic avian influenza viruses. Virus Res.2012, 167, 196-206.
33. Hulse-Post, D.J.; Franks, J.; Boyd, K.; Salomon, R.; Hoffmann, E.; Yen, H.L.; Webby, R.J.; Walker, D.; Nguyen, T.D.; Webster, R.G. Molecular changes in the polymerase genes (PA and PB1) associated with high pathogenicity of H5N1 influenza virus in mallard ducks. J.Virol. 2007,81, 8515-8524.
34. Marjuki, H.; Scholtissek, C.; Franks, J.; Negovetich, N.; Aldridge, J.; Salomon, R.; Finkelstein, D.; Webster, R. Three amino acid changes in PB1-F2 of highly pathogenic H5N1 avian influenza virus affect pathogenicity in mallard ducks. Arch.Virol.2010,155, 925-934.
35. Hu, J.; Zhao, K.; Liu, X.; Wang, X.; Chen, Z.; Liu, X. Two highly pathogenic avian influenza H5N1 viruses of clade 2.3.2.1 with similar genetic background but with different pathogenicity in mice and ducks. Transbound.Emerg.Dis.2012.doi: 10.1111/j.1865-1682.2012.01325.x.
36. Subbarao, E.K.; London, W.; Murphy, B.R. A single amino acid in the PB2 gene of influenza A virus is a determinant of host range. J. Virol.1993, 67, 1761-1764.
37. Li, Z.; Chen, H.; Jiao, P.; Deng, G.; Tian, G.; Li, Y.; Hoffmann, E.; Webster, R.G.; Matsuoka, Y.; Yu, K. Molecular basis of replicaton of duck H5N1 influenza viruses in a mammalian mouse model. J. Virol. 2005, 79, 12058-12064.
38. Gao, Y.; Zhang, Y.; Shinya, K.; Deng, G,; Jiang, Y.; Li, G.; Guan, Y.; Tian, G.; Li, Y.; Shi, J.; Liu, L.; Zeng, X.; Bu, Z.; Xia, X.; Kawaoka, Y.; Chen, H. Identification of amino acids in HA and PB2 critical for the transmission of H5N1 avian influenza viruses in a mammalian host. PLoS Pathog.2009, 5, e1000709.
39. Gabriel, G.; Dauber, B.; Wolff, T.; Planz, O.; Klenk, H.-D.; Stech, J. The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host. Proc. Natl. Acad. Sci. U. S. A.2005, 102, 18590-18595.
40. Conenello, G.M.; Zamarin, D.; Perrone, L.A.; Tumpey, T.; Palese, P. A single mutation in the PB1-F2 of H5N1 (HK/97) and 1918 influenza A viruses contributes to increased virulence. PLos Pathog.2007, 3, 1414-1421.
41. Matrosovich, M.; Tuzikov, A.; Bovin, N.; Gambaryan, A.; Klimov, A.; Castrucci, M.R.; Donatelli, I.; Kawaoka, Y. Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals. J.Virol.2000,74, 8502-8512.
42. Maines, T.R.; Lu, X.H.; Erb, S.M.; Edwards, L.; Guarner, J.; Greer, P.W.; Nguyen, D.C.; Szretter, K.J.; Chen, L.-M.; Thawatsupha, P.; Chittaganpitch, M.; Waicharoen, S.; Nguyen, D.T.; Nguyen, T.; Nguyen, H.H.T.; Kim, J.-H.; Hoang, L.T.; Kang, C.; Phuong, L.S.; Lim, W.; Zaki, S.; Donis, R. O.; Cox, N.J.; Katz, J.M.; Tumpey, T.M. Avian influenza (H5N1) viruses isolated from humans in Asia in 2004 exhibit increased virulence in mammals. J.Virol.2005,79, 11788-11800.
43. Lee, D.-H.; Lee, H.-J.; Lee, Y.-J.; Kang, H.-M.; Jeong, O.-M.; Kim, M.-C.; Kwon, J.-S.; Kwon, J.-H.; Kim, C.-B.; Lee, J.-B.; Park, S.-Y.; Choi, I.-S.; Song, C.-S. DNA barcoding techniques for avian influenza virus surveillance in migratory bird habitats. J.WildlifeDis.2010,46, 649-654.
44. Choi, J.-G.; Kang, H.-M.; Kim, M.-C.; Paek, M.-R.; Kim, H.-R.; Kim, B.-S.; Kwon, J.-H.; Kim, J.-H.; Lee, Y.-J. Genetic relationship of H3 subtype avian influenza viruses isolated from domestic ducks and wild birds in Korea and their pathogenic potential in chickens and ducks. Vet.Microbiol.2012,155, 147-157.
45. Hoffmann, E.; Stech, J.; Guan, Y.; Webster, R.G.; Perez, D.R. Universal primer set for the full-length amplification of all influenza A viruses. Arch.Virol.2001,146, 2275-2289.
46. Li, O.T.W.; Barr, I.; Leung, C.Y.H.; Chen, H.; Guan, Y.; Peiris, J.S.M.; Poon, L.L.M. Reliable universal RT-PCR assays for studying influenza polymerase subunit gene sequences from all 16 haemagglutinin subtypes. J.Virol.Methods 2007, 142, 218-222.
47. Tamura, K.; Peterson, D.; Peterson, N.; Stecher, G.; Nei, M.; Kumar, S. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol.Biol.Evol.2011,28, 2731-2739.