Highly pathogenic avian influenza virus (H5N1) in domestic poultry and relationship with migratory birds, South Korea.During the 2006-2007 winter season in South Korea, several outbreaks of highly pathogenic avian influenza avian influenza: see influenza. virus (H5N1) were confirmed among domestic poultry and in migratory bird habitats. Phylogenetic phy·lo·ge·net·icadj. 1. Of or relating to phylogeny or phylogenetics. 2. Relating to or based on evolutionary development or history. analysis showed that all isolates were closely related and that all belong to the A/ bar-headed goose/Qinghai/5/2005-like lineage rather than the A/chicken/Korea/ES/2003--like lineage. ********** Highly pathogenic avian influenza (HPAI HPAI Highly Pathogenic Avian Influenza HPAI Hospital Pharmacists Association, Ireland HPAI Hewlett Packard Associates International ) virus (H5N1) has been detected repeatedly in domestic poultry and wild birds since 1997, and it poses a substantial threat to human health (1,2). Since the end of 2003, influenza virus influenza virus n. Any of three viruses of the genus Influenzavirus designated type A, type B, and type C, that cause influenza and influenzalike infections. (HhN1) strains have spread in an unprecedented manner in many Asian countries, and the outbreaks have resulted in >170 human deaths in Thailand, Vietnam, Cambodia, and Indonesia. These outbreaks have also caused serious economic losses in the poultry industry (www.oie.int), including South Korea in 2003--the first official report of subtype (programming) subtype - If S is a subtype of T then an expression of type S may be used anywhere that one of type T can and an implicit type conversion will be applied to convert it to type T. H5N1 in South Korea's history (3). Since the outbreak caused by subtype H5N1 from migratory waterfowl waterfowl, common term for members of the order Anseriformes, wild, aquatic, typically freshwater birds including ducks, geese, and screamers. In Great Britain the term is also used to designate species kept for ornamental purposes on private lakes or ponds, while in on Qinghai Lake Qinghai Lake, often known by its Mongol name, Koko Nor or "The Blue Lake" (Tibetan: mTsho sngon po), is located in what was the former Tibetan province of Amdo, now part of the Chinese province of Qinghai. (QH) in May 2005 (4,5), outbreaks of QH-like avian influenza virus (H5N1) have been reported in the People's Republic People's Republic n. A political organization founded and controlled by a national Communist party. of China, Mongolia, Russia, Europe, and Africa, and have been ascribed to the migration of wild birds (6,7). In contrast to virus found in countries on the western side of Qinghai Lake, the Fujian-like avian influenza virus (H5N1) sublineage has predominated in southern China since late 2005 (8), but no outbreaks were reported in Far-Eastern Asian countries such as South Korea and Japan until October 2006. Eventually, in November 2006 and January 2007, outbreaks of HPAI (H5N1) occurred in South Korea and Japan. Here we report the second outbreak of HPAI (HhN1) among poultry in South Korea since November 2006 and its relationship with 2 HPAI virus (H5N1) strains isolated from migratory bird habitats (i.e., in the environment). The Study All of the virus strains from domestic poultry used in this study were isolated by the Korean National Veterinary Research and Quarantine Service (NVRQS NVRQS National Veterinary Research and Quarantine Service (South Korea) ) in embryonated eggs that were inoculated with tissues and swab specimens collected from the oropharynx oropharynx /oro·phar·ynx/ (-far´inks) the part of the pharynx between the soft palate and the upper edge of the epiglottis. o·ro·phar·ynx n. and cloaca cloaca (klōā`kə), in biology, enlarged posterior end of the digestive tract of some animals. The cloaca, from the Latin word for sewer, of affected birds. Two subtype H5N1 strains were isolated in embryonated eggs that had been inoculated with fecal specimens obtained from migratory bird habitats by Chungbuk National University Chungbuk National University is one of major 10 national universities in Korea along with Seoul National University, Pusan National University, Kyungpook National University, Chonnam National University, Chungnam National University, Chonbuk National University, Gyeongsang and Chungnam National University Chungnam National University is one of national universities in Korea. History The Chungnam National University was established for South Chungcheong province in 1952 during the Korean War. . Viral genes were sequenced and analyzed as described (9). The full-length sequences for each segment were used in phylogenetic analyses. Gene sequences determined in this study have been deposited in GenBank under accession nos. EU233675-EU233746. On November 22, 2006, NVRQS confirmed the first case of HPAI (HhN1) at a chicken farm in Iksan, Jeollabuk-Do, in South Korea. The affected flock contained 6,500 chickens and had shown a sudden increase in severe clinical signs and high mortality rate (86%), as reported by farmers and veterinarians Veterinarians and veterinary surgeons (vets) are medical professionals who operate exclusively on animals. Well-known and notable veterinarians include:
On December 21, 2006, the fourth outbreak of HPAI (HhN1) was confirmed in Asan, Chungcheongnam-Do, in breeder ducks that had shown a severe drop in egg production but no deaths. During intensive observation within the surveillance zone from the fourth outbreak farm, another HPAI (HhN1) outbreak was confirmed in Cheonan, Chungcheongnam-Do, on January 20, 2007, in a layer chicken farm with a 1% mortality rate (Figure 1). Compared with the rates in the first outbreak, the mortality rates in the more recent outbreaks were low (1%-4%) at notification time. This low proportion of deaths could be attributed to the early reporting system between the farmers and NVRQS, when the mortality rate reached [approximately equal to] 1% of the flock on poultry farms, and to the culling culling removal of inferior animals from a group of breeding stock. The removal is premature, i.e. before completion of its life span, disposal of an animal from a herd or other group. of flocks on reverse transcription--PCR confirmation (usually within 1 day) to prevent the spread of the disease. This could have limited the recorded observations when the infecting influenza virus was eliminated before the full extent of its pathogenicity could be manifested, usually after several days of infection. 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 hemagglutinin /he·mag·glu·ti·nin/ (-gloo´ti-nin) an antibody that causes agglutination of erythrocytes. cold hemagglutinin one which acts only at temperatures near 4° C. (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/W 150/2006 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 cleavage site n. See restriction 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. [FIGURE 1 OMITTED] Phylogenetic analysis of the other genes showed a similar evolutionary pattern to the HA gene tree. All 20062007 isolates had a 20-aa deletion in the stalk region (residues 49-68) ofneuraminidase (NA) compared with the NA of A/goose/Guangdong/l/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 glutamic acid (gl  tăm`ĭk), organic compound, one of the 20 amino acids commonly found in animal proteins. 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 antiviral /an·ti·vi·ral/ (-vi´ral) destroying viruses or suppressing their replication, or an agent that so acts. an·ti·vi·ral adj. cytokine Cytokine Any of a group of soluble proteins that are released by a cell to send messages which are delivered to the same cell (autocrine), an adjacent cell (paracrine), or a distant cell (endocrine). response (12), and lysine lysine (lī`sēn), organic compound, one of the 20 amino acids commonly found in animal proteins. Only the l-stereoisomer appears in mammalian protein. 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 amantadine /aman·ta·dine/ (ah-man´tah-den) an antiviral compound used as the hydrochloride salt to treat influenza A; also used as an antidyskinetic in the treatment of parkinsonism and drug-induced extrapyramidal reactions. . [FIGURE 2 OMITTED] In contrast to the 2003 H5NI 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 VICE VERSA. On the contrary; on opposite sides. 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. All material published in Emerging Infectious Diseases is in the public domain and may be used and reprinted without special permission; proper citation, however, is required. Acknowledgments We thank Hyuk-Man Kwon, Eun-Im Yun, Kyeong-Hwa Han, Hee-Kyung Jang, and Won-Joung Kim for excellent technical assistance. We also thank the Animal Disease Control Division and the Veterinary Epidemiology Division of NVRQS for their efforts to control HPAI. This work was supported by grant no. RO1-2005-00010585-0 from the Basic Research Program of the Korea Science and Engineering Foundation and by grant no. C-AD15-2006-1401 from the Research Program of NVRQS. References (1.) Claas EC, Osterhaus AD, van Beek R, De Jong JC, Rimmelzwaan GF, Senne DA, et al. Human influenza A influenza A n. Influenza caused by infection with a strain of influenza virus type A. influenza A Infectious disease An avian virus, especially of ducks–which in China live near the pig reservoir and 'vector'; H5N1 virus related to a highly pathogenic avian influenza virus. Lancet. 1998;351:472-7. (2.) Peiris JS, Yu WC, Leung CW, Cheung CY, Ng WF, Nicholls JM, et al. Re-emergence of fatal human influenza A subtype H5N1 disease. Lancet. 2004;363:617-9. (3.) Lee CW, Suarez DL, Tumpey TM, Sung HW, Kwon YK, Lee YJ, et al. Characterization of highly pathogenic H5N1 avian influenza A viruses isolated from South Korea. J Virol. 2005;79:3692-702. (4.) Chen H, Smith GJ, Zhang SY, Qin K, Wang J, Li KS, et al. Avian flu: H5N1 virus outbreak in migratory waterfowl. Nature. 2005;436: 191-2. (5.) Liu J, Xiao H, Lei K Zhu Q, Qin K, Zhang XW, et al. Highly pathogenic H5N1 influenza virus infection in migratory birds. Science. 2005;309:1206. (6.) Chen H, Li Y, Li Z, Shi J, Shinya K, Deng G, et al. Properties and dissemination of HSN HSN Home Shopping Network HSN High Speed Network HSN Hereditary Sensory Neuropathy HSN Highly Saturated Nitrile HSN Healthy Schools Network, Inc. HSN Hopping Sequence Number HSN Historical Sample of the Netherlands HSN Haiti Support Network 1 viruses isolated during an influenza outbreak in migratory waterfowl in western China. J Virol. 2006;80: 5976-83. (7.) Olsen B, Munster V J, Wallensten A, Waldenstrom J, Osterhaus AD, Fouchier RA. Global patterns of influenza a virus in wild birds. Science. 2006;312:384-8. (8.) Smith GJ, Fan XH, Wang J, Li KS, Qin K, Zhang JX, et al. Emergence and predominance of an H5N1 influenza variant in China. Proc Natl Acad Sci U S A. 2006;103:16936-41. (9.) Lee YJ, Shin JY, Song MS, Lee YM, Choi JG, Lee EK, et al. Continuing evolution of H9 influenza viruses in Korean poultry. Virology virology, study of viruses and their role in disease. Many viruses, such as animal RNA viruses and viruses that infect bacteria, or bacteriophages, have become useful laboratory tools in genetic studies and in work on the cellular metabolic control of gene expression . 2007;359:313-23. (10.) Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment A multiple sequence alignment (MSA) is a sequence alignment of three or more biological sequences, generally protein, DNA, or RNA. In general, the input set of query sequences are assumed to have an evolutionary relationship by which they share a lineage and are descended from a aided by quality analysis tools. Nucleic Acids Nucleic acids The cellular molecules DNA and RNA that act as coded instructions for the production of proteins and are copied for transmission of inherited traits. Res. 1997;25:4876-82. (11.) Perriere G, Gouy M. WWW-query: an on-line retrieval system for biological sequence banks. Biochimie. 1996;78:364-9. (12.) Seo SH, Hoffmann E, Webster RG. Lethal H5NI influenza viruses escape host anti-viral cytokine responses. Nat Med. 2002;8:950-4. (13.) Hatta M, Gao R Halfmann P, Kawaoka Y. Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science. 2001;293:1840-2. Address for correspondence: Chul-Joong Kim, College of Veterinary Medicine veterinary medicine, diagnosis and treatment of diseases of animals. An early interest in animal diseases is found in ancient Greek writings on medicine. Veterinary medicine began to achieve the stature of a science with the organization of the first school in the , Chungnam National University, 220 Gung-Dong, Yuseoung Gu, Daejeon 305-764, South Korea; email: cjkim@cnu.ac.kr Youn-Jeong Lee, * (1) Young-Ki Choi, ([dagger]) (1) Yong-Joo Kim, * Min-Suk Song, ([dagger]) 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, ([dagger]) Tak-Gue Oh, ([dagger]) Ho-Jin Moon, ([double dagger]) Dae-Won Yoo, ([double dagger]) Jae-Hong Kim, ([section]) Moon-Hee Sung, ([paragraph]) Haryoung Poo poo Slang intr.v. pooed, poo·ing, poos To defecate. n. 1. Excrement. 2. An act of defecating. [Probably from pooh.] , # Jun-Hun Kwon, * and Chul-Joong Kim ([double dagger]) * Ministry of Agriculture and Forestry Ministry of Agriculture and Forestry
Seoul National University (SNU) is a national research university in Seoul, South Korea. Founded in 1946, SNU was the first national university in South Korea, and served as a model for the many national and public , Seoul, South Korea; ([paragraph]) Bioleaders Corporation, Daejeon, South Korea; and #Korea Research Institute of Bioscience and Biotechnology, Daejeon, South Korea (1) These authors contributed equally to this work. Dr Youn-Jeong Lee is a senior researcher at NVRQS. Her current research focuses on avian influenza viruses.
Table. History of highly pathogenic avian influenza (H5N1) suspected
cases, South Korea, 2006-2007
Outbreak Source/
Date reported no. breed * Age, wk Region
2006 Nov 22 1 Chicken/BB 45 Jeollabuk
Iksan
2006 Nov 27 2 Chicken/BB 40 Jeollabuk
Iksan
2006 Dec 10 3 Quail 16-28 Jeollabuk
Gimje
2006 Dec 21 4 Duck/B 30 Chungcheongnam
Asan
2007 Jan 20 5 Chicken/L 32 Chungcheongnam
Cheonan
2006 Dec 21 Environment Chungcheongnam
Cheonan
2006 Dec 21 Environment Chungcheongbuk
Cheongju
No.
Date reported animals/farm Clinical signs Isolate
2006 Nov 22 13,000 Depression, A/chicken/IS/2006
death A/chicken/IS2/2006
2006 Nov 27 12,000 Depression, A/chicken/IS3/2006
death
2006 Dec 10 290,000 Death A/quail/KJ4/2006
2006 Dec 21 9,000 Decrease in A/duck/Asan5/2006
egg production A/duck/Asan6/2006
2007 Jan 20 30,000 Depression, A/chicken/CA7/2007
death
2006 Dec 21 A/environment/Korea/
W149/2006
2006 Dec 21 A/environment/Korea/
W150/2006
* BB, broiler breeder; B, breeder; L, layer.
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