Highly Pathogenic Avian Influenza Virus (H5N1) in Domestic Poultry and Relationship With Migratory Birds, South Korea

Youn-Jeong Lee; Young-Ki Choi; Yong-Joo Kim; Min-Suk Song; Ok-Mi Jeong; Eun-Kyoung Lee; Woo-Jin Jeon; Wooseog Jeong; Seong-Joon Joh; Kang-seuk Choi; Moon Her; Min-Chul Kim; Aeran Kim; Min-Jeong Kim; Eun ho Lee; Tak-Gue Oh; Ho-Jin Moon; Dae-Won Yoo; Jae-Hong Kim; Moon-Hee Sung; Haryoung Poo; Jun-Hun Kwon; Chul-Joong Kim

Disclosures

Emerging Infectious Diseases. 2008;14(3):487-490. 

In This Article

Conclusions

Great interest has been focused on the role of migratory birds in the spread of H5N1 subtype and the exchange of virus strains between domestic and wild birds in Asia. Therefore, we surveyed avian influenza virus in migratory birds in South Korea to investigate whether the HPAI (H5N1) outbreaks in domestic poultry bore any relationship to bird migration in the same region. During our routine survey for influenza activity in migratory bird habitats, on December 21, 2006, 2 distinct subtype H5N1 strains were isolated from fecal samples from 2 migratory bird habitats -- one near the first outbreak farm in Chungcheongnam-Do, and the other from a stream in Chungcheongbuk-Do (Figure 1).

Our phylogenetic analysis of the hemagglutinin (HA) genes of all Korean isolates showed that the isolates belong to the A/bar-headed goose/QH/65/2005 (QH/2005)-like lineage that caused an outbreak among wild birds at Qinghai Lake in China during 2005, rather than the first HPAI (H5N1) lineage (A/chicken/Korea/ES/2003) that infected farms in Korea in 2003 (Figure 2). Notably, the 2 isolates from migratory bird habitats were closely related to the H5N1 subtype poultry virus strains: A/environment/Korea/W149/2006 was similar to the viruses that occurred in Chungcheongnam-Do, and A/environment/Korea/W150/2006 was similar to viruses that affected birds in Jeollabuk-Do. However, all H5N1 subtype virus strains have a series of basic amino acids at the HA cleavage site (PQGERRRKKR/G), which is a characteristic of influenza viruses that are highly pathogenic to chickens.[4,5] The intravenous pathogenicity index score of A/chicken/Korea/IS/2006 was 3.0 in chickens.

Phylogenetic trees for hemagglutinin (HA) genes of Korean influenza virus (H5N1) isolates from wild birds and poultry farms during 2006-2007. The DNA sequences were compiled and edited by using the Lasergene sequence analysis software package (DNASTAR, Madison, WI, USA). Multiple sequence alignments were made by using ClustalX.[10] Rooted phylograms were prepared with the neighbor-joining algorithm and then plotted by using NJplot.[11] Branch lengths are proportional to sequence divergence and can be measured relative to the scale bar shown (0.01-nt changes per site). Branch labels record the stability of the branches >1,000 bootstrap replicates. The tree was produced by referring to the proposed global nomenclature system for influenza virus (H5N1) (www.offlu.net). Boldface indicates isolates tested in the current study.

Phylogenetic analysis of the other genes showed a similar evolutionary pattern to the HA gene tree. All 2006-2007 isolates had a 20-aa deletion in the stalk region (residues 49-68) of neuraminidase (NA) compared with the NA of A/goose/Guangdong/1/96. Analysis of the raw sequencing traces showed no mutations in NA genes of all isolates associated with resistance to NA inhibitors. All 2006-2007 Korean HPAI (H5N1) isolates had glutamic acid at position 92 of the nonstructural protein 1, a position that is related to the ability of H5N1/97 virus to escape the host antiviral cytokine response,[12] and lysine at position 627 in the PB2 protein, which is commonly observed in QH viruses.[6] Lysine 627 in PB2 is conserved in authentic human influenza viruses and is associated with high virulence of influenza virus (H5N1) strains in mice.[13] Analysis of membrane (M) 2 protein sequences showed that none of the 2006-2007 HPAI (H5N1) Korean strains were resistant to amantadine.

In contrast to the 2003 H5N1 subtype isolates,[3] all of the 2006-2007 H5N1 subtype isolates were QH/05-like strains. Phylogenetic analysis showed that this sublineage spread wildly through Africa and Europe but not in eastern Asia, until the outbreak reported here. We cannot conclude whether wild migratory birds were the origin of the HPAI virus (H5N1) found in poultry or vice versa in South Korea, because the environmental isolates were obtained after the poultry outbreaks. However, the report of outbreaks of similar HPAI virus (H5N1) strains in Japan on January 13, 2007 (www.oie.int/eng) suggested that migratory birds could be a strong mediator for the spread of HPAI virus (H5N1) in South Korea and Japan, as occurred in 2003, because these 2 countries share similar wild bird migration routes. Therefore, continued monitoring of the domestic and wild bird populations is needed to better understand interspecies transmission and to clarify the importance of avian hosts in the ecology of influenza viruses.

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