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Science 16 January 1998:
Vol. 279. no. 5349, pp. 393 - 396
DOI: 10.1126/science.279.5349.393
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Reports

Characterization of an Avian Influenza A (H5N1) Virus Isolated from a Child with a Fatal Respiratory Illness

Kanta Subbarao, * Alexander Klimov, Jacqueline Katz, Helen Regnery, Wilina Lim, Henrietta Hall, Michael Perdue, David Swayne, Catherine Bender, Jing Huang, Mark Hemphill, Thomas Rowe, Michael Shaw, Xiyan Xu, Keiji Fukuda, Nancy Cox

An avian H5N1 influenza A virus (A/Hong Kong/156/97) was isolated from a tracheal aspirate obtained from a 3-year-old child in Hong Kong with a fatal illness consistent with influenza. Serologic analysis indicated the presence of an H5 hemagglutinin. All eight RNA segments were derived from an avian influenza A virus. The hemagglutinin contained multiple basic amino acids adjacent to the cleavage site, a feature characteristic of highly pathogenic avian influenza A viruses. The virus caused 87.5 to 100 percent mortality in experimentally inoculated White Plymouth Rock and White Leghorn chickens. These results may have implications for global influenza surveillance and planning for pandemic influenza.

K. Subbarao, A. Klimov, J. Katz, H. Regnery, H. Hall, C. Bender, J. Huang, M. Hemphill, T. Rowe, M. Shaw, X. Xu, K. Fukuda, N. Cox, Influenza Branch, Centers for Disease Control and Prevention, Atlanta, GA 30333, USA.
W. Lim, Government Virus Unit, Queen Mary Hospital, Hong Kong, China.
M. Perdue and D. Swayne, Southeast Poultry Research Laboratory, Agriculture Research Service, U.S. Department of Agriculture, Athens, GA 30605, USA.
*   To whom correspondence should be addressed.

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Avian Influenza (H5N1) Viruses Isolated from Humans in Asia in 2004 Exhibit Increased Virulence in Mammals.
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Molecular Basis of Replication of Duck H5N1 Influenza Viruses in a Mammalian Mouse Model.
Z. Li, H. Chen, P. Jiao, G. Deng, G. Tian, Y. Li, E. Hoffmann, R. G. Webster, Y. Matsuoka, and K. Yu (2005)
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Highly Pathogenic H5N1 Influenza Virus Infection in Migratory Birds.
J. Liu, H. Xiao, F. Lei, Q. Zhu, K. Qin, X.-w. Zhang, X.-l. Zhang, D. Zhao, G. Wang, Y. Feng, et al. (2005)
Science 309, 1206
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p38 Mitogen-Activated Protein Kinase-Dependent Hyperinduction of Tumor Necrosis Factor Alpha Expression in Response to Avian Influenza Virus H5N1.
D. C. W. Lee, C.-Y. Cheung, A. H. Y. Law, C. K. P. Mok, M. Peiris, and A. S. Y. Lau (2005)
J. Virol. 79, 10147-10154
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Functional Chimeras of Human Immunodeficiency Virus Type 1 gp120 and Influenza A Virus (H3) Hemagglutinin.
K. M. Copeland, A. J. Elliot, and R. S. Daniels (2005)
J. Virol. 79, 6459-6471
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Isolation and Characterization of Avian Influenza Viruses, Including Highly Pathogenic H5N1, from Poultry in Live Bird Markets in Hanoi, Vietnam, in 2001.
D. C. Nguyen, T. M. Uyeki, S. Jadhao, T. Maines, M. Shaw, Y. Matsuoka, C. Smith, T. Rowe, X. Lu, H. Hall, et al. (2005)
J. Virol. 79, 4201-4212
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A. S. Lipatov, S. Andreansky, R. J. Webby, D. J. Hulse, J. E. Rehg, S. Krauss, D. R. Perez, P. C. Doherty, R. G. Webster, and M. Y. Sangster (2005)
J. Gen. Virol. 86, 1121-1130
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Characterization of Highly Pathogenic H5N1 Avian Influenza A Viruses Isolated from South Korea.
C.-W. Lee, D. L. Suarez, T. M. Tumpey, H.-W. Sung, Y.-K. Kwon, Y.-J. Lee, J.-G. Choi, S.-J. Joh, M.-C. Kim, E.-K. Lee, et al. (2005)
J. Virol. 79, 3692-3702
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Lethality to Ferrets of H5N1 Influenza Viruses Isolated from Humans and Poultry in 2004.
E. A. Govorkova, J. E. Rehg, S. Krauss, H.-L. Yen, Y. Guan, M. Peiris, T. D. Nguyen, T. H. Hanh, P. Puthavathana, H. T. Long, et al. (2005)
J. Virol. 79, 2191-2198
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Molecular characterization of the complete genome of human influenza H5N1 virus isolates from Thailand.
P. Puthavathana, P. Auewarakul, P. C. Charoenying, K. Sangsiriwut, P. Pooruk, K. Boonnak, R. Khanyok, P. Thawachsupa, R. Kijphati, and P. Sawanpanyalert (2005)
J. Gen. Virol. 86, 423-433
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Characterization of Avian H3N3 and H1N1 Influenza A Viruses Isolated from Pigs in Canada.
A. I. Karasin, K. West, S. Carman, and C. W. Olsen (2004)
J. Clin. Microbiol. 42, 4349-4354
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Influenza: Emergence and Control.
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J. Virol. 78, 8951-8959
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J. Virol. 78, 8609-8614
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Matrix Gene of Influenza A Viruses Isolated from Wild Aquatic Birds: Ecology and Emergence of Influenza A Viruses.
L. Widjaja, S. L. Krauss, R. J. Webby, T. Xie, and R. G. Webster (2004)
J. Virol. 78, 8771-8779
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Influenza A viruses in feral Canadian ducks: extensive reassortment in nature.
T. F. Hatchette, D. Walker, C. Johnson, A. Baker, S. P. Pryor, and R. G. Webster (2004)
J. Gen. Virol. 85, 2327-2337
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The evolution of H5N1 influenza viruses in ducks in southern China.
H. Chen, G. Deng, Z. Li, G. Tian, Y. Li, P. Jiao, L. Zhang, Z. Liu, R. G. Webster, and K. Yu (2004)
PNAS 101, 10452-10457
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Protection against lethal influenza virus challenge by RNA interference in vivo.
S. M. Tompkins, C.-Y. Lo, T. M. Tumpey, and S. L. Epstein (2004)
PNAS 101, 8682-8686
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H5N1 influenza: A protean pandemic threat.
Y. Guan, L. L. M. Poon, C. Y. Cheung, T. M. Ellis, W. Lim, A. S. Lipatov, K. H. Chan, K. M. Sturm-Ramirez, C. L. Cheung, Y. H. C. Leung, et al. (2004)
PNAS 101, 8156-8161
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Use of the DNA Flow-Thru Chip, a Three-Dimensional Biochip, for Typing and Subtyping of Influenza Viruses.
N. Kessler, O. Ferraris, K. Palmer, W. Marsh, and A. Steel (2004)
J. Clin. Microbiol. 42, 2173-2185
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Reemerging H5N1 Influenza Viruses in Hong Kong in 2002 Are Highly Pathogenic to Ducks.
K. M. Sturm-Ramirez, T. Ellis, B. Bousfield, L. Bissett, K. Dyrting, J. E. Rehg, L. Poon, Y. Guan, M. Peiris, and R. G. Webster (2004)
J. Virol. 78, 4892-4901
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The index influenza A virus subtype H5N1 isolated from a human in 1997 differs in its receptor-binding properties from a virulent avian influenza virus.
K. Iwatsuki-Horimoto, R. Kanazawa, S. Sugii, Y. Kawaoka, and T. Horimoto (2004)
J. Gen. Virol. 85, 1001-1005
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Structure of the Uncleaved Human H1 Hemagglutinin from the Extinct 1918 Influenza Virus.
J. Stevens, A. L. Corper, C. F. Basler, J. K. Taubenberger, P. Palese, and I. A. Wilson (2004)
Science 303, 1866-1870
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Alterations of pr-M Cleavage and Virus Export in pr-M Junction Chimeric Dengue Viruses.
P. Keelapang, R. Sriburi, S. Supasa, N. Panyadee, A. Songjaeng, A. Jairungsri, C. Puttikhunt, W. Kasinrerk, P. Malasit, and N. Sittisombut (2004)
J. Virol. 78, 2367-2381
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Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome.
R. A. M. Fouchier, P. M. Schneeberger, F. W. Rozendaal, J. M. Broekman, S. A. G. Kemink, V. Munster, T. Kuiken, G. F. Rimmelzwaan, M. Schutten, G. J. J. van Doornum, et al. (2004)
PNAS 101, 1356-1361
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Phenotypic Drug Susceptibility Assay for Influenza Virus Neuraminidase Inhibitors.
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The origin of the 1918 pandemic influenza virus: a continuing enigma.
A. H. Reid and J. K. Taubenberger (2003)
J. Gen. Virol. 84, 2285-2292
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Characterization of H9 Subtype Influenza Viruses from the Ducks of Southern China: a Candidate for the Next Influenza Pandemic in Humans?.
K. S. Li, K. M. Xu, J. S. M. Peiris, L. L. M. Poon, K. Z. Yu, K. Y. Yuen, K. F. Shortridge, R. G. Webster, and Y. Guan (2003)
J. Virol. 77, 6988-6994
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Pathology of Human Influenza A (H5N1) Virus Infection in Cynomolgus Macaques (Macaca fascicularis).
T. Kuiken, G. F. Rimmelzwaan, G. Van Amerongen, and A. D. M. E. Osterhaus (2003)
Vet. Pathol. 40, 304-310
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Neurovirulence in Mice of H5N1 Influenza Virus Genotypes Isolated from Hong Kong Poultry in 2001.
A. S. Lipatov, S. Krauss, Y. Guan, M. Peiris, J. E. Rehg, D. R. Perez, and R. G. Webster (2003)
J. Virol. 77, 3816-3823
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Existing antivirals are effective against influenza viruses with genes from the 1918 pandemic virus.
T. M. Tumpey, A. Garcia-Sastre, A. Mikulasova, J. K. Taubenberger, D. E. Swayne, P. Palese, and C. F. Basler (2002)
PNAS 99, 13849-13854
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Emergence of multiple genotypes of H5N1 avian influenza viruses in Hong Kong SAR.
Y. Guan, J. S. M. Peiris, A. S. Lipatov, T. M. Ellis, K. C. Dyrting, S. Krauss, L. J. Zhang, R. G. Webster, and K. F. Shortridge (2002)
PNAS 99, 8950-8955
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Evaluation of the Subtype Specificity of Monoclonal Antibodies Raised against H1 and H3 Subtypes of Human Influenza A Virus Hemagglutinins.
E. Vareckova, N. Cox, and A. Klimov (2002)
J. Clin. Microbiol. 40, 2220-2223
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Characterization of a Highly Pathogenic H5N1 Avian Influenza A Virus Isolated from Duck Meat.
T. M. Tumpey, D. L. Suarez, L. E. L. Perkins, D. A. Senne, J.-g. Lee, Y.-J. Lee, I.-P. Mo, H.-W. Sung, and D. E. Swayne (2002)
J. Virol. 76, 6344-6355
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Pathogenesis of Avian Influenza A (H5N1) Viruses in Ferrets.
L. A. Zitzow, T. Rowe, T. Morken, W.-J. Shieh, S. Zaki, and J. M. Katz (2002)
J. Virol. 76, 4420-4429
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H3N2 influenza viruses from domestic chickens in Italy: an increasing role for chickens in the ecology of influenza?.
L. Campitelli, C. Fabiani, S. Puzelli, A. Fioretti, E. Foni, A. De Marco, S. Krauss, R. G. Webster, and I. Donatelli (2002)
J. Gen. Virol. 83, 413-420
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Molecular Evolution of H6 Influenza Viruses from Poultry in Southeastern China: Prevalence of H6N1 Influenza Viruses Possessing Seven A/Hong Kong/156/97 (H5N1)-Like Genes in Poultry.
P. S. Chin, E. Hoffmann, R. Webby, R. G. Webster, Y. Guan, M. Peiris, and K. F. Shortridge (2002)
J. Virol. 76, 507-516
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Characterization of H5N1 Influenza Viruses That Continue To Circulate in Geese in Southeastern China.
R. G. Webster, Y. Guan, M. Peiris, D. Walker, S. Krauss, N. N. Zhou, E. A. Govorkova, T. M. Ellis, K. C. Dyrting, T. Sit, et al. (2002)
J. Virol. 76, 118-126
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Combined PCR-Heteroduplex Mobility Assay for Detection and Differentiation of Influenza A Viruses from Different Animal Species.
J. S. Ellis and M. C. Zambon (2001)
J. Clin. Microbiol. 39, 4097-4102
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Cocirculation of Avian H9N2 and Contemporary ""Human"" H3N2 Influenza A Viruses in Pigs in Southeastern China: Potential for Genetic Reassortment?.
J. S. M. Peiris, Y. Guan, D. Markwell, P. Ghose, R. G. Webster, and K. F. Shortridge (2001)
J. Virol. 75, 9679-9686
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Comparison of Efficacies of RWJ-270201, Zanamivir, and Oseltamivir against H5N1, H9N2, and Other Avian Influenza Viruses.
E. A. Govorkova, I. A. Leneva, O. G. Goloubeva, K. Bush, and R. G. Webster (2001)
Antimicrob. Agents Chemother. 45, 2723-2732
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X-ray structures of H5 avian and H9 swine influenza virus hemagglutinins bound to avian and human receptor analogs.
Y. Ha, D. J. Stevens, J. J. Skehel, and D. C. Wiley (2001)
PNAS
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Molecular Basis for High Virulence of Hong Kong H5N1 Influenza A Viruses.
M. Hatta, P. Gao, P. Halfmann, and Y. Kawaoka (2001)
Science 293, 1840-1842
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Recombination in the Hemagglutinin Gene of the 1918 ""Spanish Flu"".
M. J. Gibbs, J. S. Armstrong, and A. J. Gibbs (2001)
Science 293, 1842-1845
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Evolutionary and immunological implications of contemporary HIV-1 variation.
B. Korber, B. Gaschen, K. Yusim, R. Thakallapally, C. Kesmir, and V. Detours (2001)
Br. Med. Bull. 58, 19-42
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Pathogenesis of Influenza A (H5N1) Virus Infection in a Primate Model.
G. F. Rimmelzwaan, T. Kuiken, G. van Amerongen, T. M. Bestebroer, R. A. M. Fouchier, and A. D. M. E. Osterhaus (2001)
J. Virol. 75, 6687-6691
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Infection of a child in Hong Kong by an influenza A H3N2 virus closely related to viruses circulating in European pigs.
V. Gregory, W. Lim, K. Cameron, M. Bennett, S. Marozin, A. Klimov, H. Hall, N. Cox, A. Hay, and Y. P. Lin (2001)
J. Gen. Virol. 82, 1397-1406
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Mucosal Delivery of Inactivated Influenza Vaccine Induces B-Cell-Dependent Heterosubtypic Cross-Protection against Lethal Influenza A H5N1 Virus Infection.
T. M. Tumpey, M. Renshaw, J. D. Clements, and J. M. Katz (2001)
J. Virol. 75, 5141-5150
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Sequences in Influenza A Virus PB2 Protein That Determine Productive Infection for an Avian Influenza Virus in Mouse and Human Cell Lines.
Y. Yao, L. J. Mingay, J. W. McCauley, and W. S. Barclay (2001)
J. Virol. 75, 5410-5415
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Pattern of mutation in the genome of influenza A virus on adaptation to increased virulence in the mouse lung: Identification of functional themes.
E. G. Brown, H. Liu, L. C. Kit, S. Baird, and M. Nesrallah (2001)
PNAS
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Immunity to Influenza A H9N2 Viruses Induced by Infection and Vaccination.
X. Lu, M. Renshaw, T. M. Tumpey, G. D. Kelly, J. Hu-Primmer, and J. M. Katz (2001)
J. Virol. 75, 4896-4901
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Efficacy of Zanamivir against Avian Influenza A Viruses That Possess Genes Encoding H5N1 Internal Proteins and Are Pathogenic in Mammals.
I. A. Leneva, O. Goloubeva, R. J. Fenton, M. Tisdale, and R. G. Webster (2001)
Antimicrob. Agents Chemother. 45, 1216-1224
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