Comparative pathology of select agent influenza a virus infections

Veterinary Pathology

Volumn 47, Issue 5, 2010, Pages 893-914

  Kuiken, Thijs ^a   van den Brand, J ^a   van Riel, D ^a   Pantin Jackwood, M ^b   Swayne, D E ^b  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

animal models; influenza; pathobiology; pathogenesis; select agents

Indexed keywords

ANIMAL; ARTICLE; BIOLOGICAL WARFARE AGENT; COMPARATIVE STUDY; DISEASE MODEL; DISEASE TRANSMISSION; EPIDEMIC; HUMAN; IMMUNOLOGY; INFLUENZA; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H5N1; MICROBIOLOGY; PATHOLOGY; VIROLOGY; ZOONOSIS;

ANIMALS; BIOLOGICAL WARFARE AGENTS; DISEASE MODELS, ANIMAL; DISEASE OUTBREAKS; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA, HUMAN; ZOONOSES;

ANIMALIA; ANSERIFORMES; AVES; AVIAN INFLUENZA VIRUS; BACTERIA (MICROORGANISMS); CAVIA; FELIS CATUS; GALLIFORMES; INFLUENZA A VIRUS; MUSTELA PUTORIUS FURO; ORTHOMYXOVIRIDAE; SUS SCROFA DOMESTICA;

EID: 78649314599     PISSN: 03009858     EISSN: 15442217     Source Type: Journal    
DOI: 10.1177/0300985810378651     Document Type: Article

References (164)

1. Agyeman P., Duppenthaler A., Heininger U., Aebi C.: Influenza-associated myositis in children. Infection 32:199-203, 2004.
2. Alexander DJ, Allan WH, Parsons DG, Parsons G.: The pathogenicity of four avian influenza viruses for fowls, turkeys and ducks. Res Vet Sci 24:242-247, 1978.
3. Alexander DJ, Parsons G., Manvell RJ: Experimental assessment of the pathogenicity of eight influenza A viruses of H5 subtype for chickens, turkeys, ducks and quail. Avian Pathol 15:647-662, 1986.
4. Ball RS: Issues to consider for preparing ferrets as research subjects in the laboratory. ILAR J 47:348-357, 2006.
5. Barnard DL: Animal models for the study of influenza pathogenesis and therapy. Antiviral Res 82:A110-A122, 2009.
6. Bartz CR, Montali RJ: Influenza virus. In: Virus Infections of Carnivores, ed. Appel MJ, pp. 445-448. Elsevier, Amsterdam, Netherlands, 1987.
7. Baskin CR, Bielefeldt-Ohmann H., Tumpey TM, Sabourin PJ, Long JP, Garcia-Sastre A., Tolnay AE, Albrecht R., Pyles JA, Olson PH, Aicher LD, Rosenzweig ER, Murali-Krishna K., Clark EA, Kotur MS, Fornek JL, Proll S., Palermo RE, Sabourin CL, Katze MG: Early and sustained innate immune response defines pathology and death in nonhuman primates infected by highly pathogenic influenza virus. Proc Natl Acad Sci U S A 106:3455-3460, 2009.
8. Baskin CR, Garcia-Sastre A., Tumpey TM, Bielefeldt-Ohmann H., Carter VS, Nistal-Villan E., Katze MG: Integration of clinical data, pathology, and cDNA microarrays in influenza virus-infected pigtailed macaques (Macaca nemestrina). J Virol 78:10420-10432, 2004.
9. Basler CF, Reid AH, Dybing JK, Janczewski TA, Fanning TG, Zheng H., Salvatore M., Perdue ML, Swayne DE, Garcia-Sastre A., Palese P., Taubenberger JK: Sequence of the 1918 pandemic influenza virus nonstructural gene (NS) segment and characterization of recombinant viruses bearing the 1918 NS genes. Proc Natl Acad Sci U S A 98:2746-2751, 2001.
10. Beal AL, Cerra FB: Multiple organ failure syndrome in the 1990s: systemic inflammatory response and organ dysfunction. JAMA 271:226-233, 1994.
11. Beigel JH, Farrar J., Han AM, Hayden FG, Hyer R., de Jong MD, Lochindarat S., Nguyen TK, Nguyen TH, Tran TH, Nicoll A., Touch S., Yuen KY: Avian influenza A (H5N1) infection in humans. N Engl J Med 353:1374-1385, 2005.
12. Belser JA, Szretter KJ, Katz JM, Tumpey TM: Use of animal models to understand the pandemic potential of highly pathogenic avian influenza viruses. Adv Virus Res 73:55-97, 2009.
13. Beveridge WIB: Influenza: The Last Great Plague. Prodist, New York, NY, 1978.
14. Bingham J., Green DJ, Lowther S., Klippel J., Burggraaf S., Anderson DE, Wibawa H., Hoa DM, Long NT, Vu PP, Middleton DJ, Daniels PW: Infection studies with two highly pathogenic avian influenza strains (Vietnamese and Indonesian) in Pekin ducks (Anas platyrhynchos), with particular reference to clinical disease, tissue tropism and viral shedding. Avian Pathol 38:267-278, 2009.
15. Boltz DA, Rehg JE, McClaren J., Webster RG, Govorkova EA: Oseltamivir prophylactic regimens prevent H5N1 influenza morbidity and mortality in a ferret model. J Infect Dis 197:1315- 1323, 2008.
16. Boon AC, deBeauchamp J., Hollmann A., Luke J., Kotb M., Rowe S., Finkelstein D., Neale G., Lu L., Williams RW, Webby RJ: Host genetic variation affects resistance to infection with a highly pathogenic H5N1 influenza A virus in mice. J Virol 83:10417- 10426, 2009.
17. Boon AC, Sandbulte MR, Seiler P., Webby RJ, Songserm T., Guan Y., Webster RG: Role of terrestrial wild birds in ecology of influenza A virus (H5N1). Emerg Infect Dis 13:1720-1724, 2007.
18. Boukhvalova MS, Prince GA, Blanco Jorge CG: The cotton rat model of respiratory viral infections. Biologicals 37:152-159, 2009.
19. Brown JD, Stallknecht DE, Beck JR, Suarez DL, Swayne DE: The susceptibility of North American ducks and gulls to H5N1 highly pathogenic avian influenza viruses. Emerg Infect Dis 12:1665- 1670, 2006.
20. Brown JD, Stallknecht DE, Berghaus RD, Swayne DE: Infectious and lethal doses of H5N1 highly pathogenic avian influenza virus for house sparrows (Passer domesticus) and rock pigeons (Columbia livia). J Vet Diagn Invest 21:437-445, 2009.
21. Brown JD, Stallknecht DE, Swayne DE: Experimental infection of swans and geese with highly pathogenic avian influenza virus (H5N1) of Asian lineage. Emerg Infect Dis 14:136-142, 2008.
22. Brown JD, Stallknecht DE, Swayne DE: Experimental infections of herring gulls (Larus argentatus) with H5N1 highly pathogenic avian influenza viruses by intranasal inoculation of virus and ingestion of virus-infected chicken meat. Avian Pathol 37:393- 397, 2008.
23. Cameron CM, Cameron MJ, Bermejo-Martin JF, Ran L., Xu L., Turner PV, Ran R., Danesh A., Fang Y., Chan PK, Mytle N., Sullivan TJ, Collins TL, Johnson MG, Medina JC, Rowe T., Kelvin DJ: Gene expression analysis of host innate immune responses during lethal H5N1 infection in ferrets. J Virol 82:11308-11317, 2008.
24. Castleman WL, Crawford PC, Gibbs EPJ, Dubovi EJ, Donis R., Powe JR: Pathologic findings in dogs infected with newly emerged canine H3N8 influenza virus. FASEB J 20:A214, 2006.
25. Castranova V., Rabovsky J., Tucker JH, Miles PR: The alveolar type II epithelial cell: a multifunctional pneumocyte. Toxicol Appl Pharmacol 93:472-483, 1988.
26. Caswell JF, Williams KJ: Respiratory system. In: Jubb, Kennedy, and Palmer's Pathology of Domestic Animals, ed. Maxie MG, 5th ed., pp. 523-653. Saunders Elsevier, Edinburgh, Scotland, 2007.
27. Chen Y., Deng W., Jia C., Dai X., Zhu H., Kong Q., Huang L., Liu Y., Ma C., Li J., Xiao C., Liu Y., Wei Q., Qin C.: Pathological lesions and viral localization of influenza A (H5N1) virus in experimentally infected Chinese rhesus macaques: implications for pathogenesis and viral transmission. Arch Virol 154:227-233, 2009.
28. Chutinimitkul S., van Riel D., Munster VJ, van den Brand JM, Rimmelzwaan GF, Kuiken T., Osterhaus AD, Fouchier RA, de Wit E.: In vitro assessment of attachment pattern and replication efficiency of H5N1 influenza A viruses with altered receptor specificity. J Virol. 84:6825-6833, 2010.
29. Cilloniz C., Shinya K., Peng X., Korth MJ, Proll SC, Aicher LD, Carter VS, Chang JH, Kobasa D., Feldmann F., Strong JE, Feldmann H., Kawaoka Y., Katze MG: Lethal influenza virus infection in macaques is associated with early dysregulation of inflammatory related genes. PLoS Pathog 5:e1000604, 2009.
30. Corrin B., Nicholson AG: Pathology of the Lungs, 2nd ed. Churchill Livingstone Elsevier, Philadelphia, PA, 2006.
31. Cox NJ, Subbarao K.: Global epidemiology of influenza: past and present. Annu Rev Med 51:407-421, 2000.
32. de Wit E., Fouchier RA: Emerging influenza. J Clin Virol 41:1-6, 2008.
33. Dybing JK, Schultz-Cherry S., Swayne DE, Suarez DL, Perdue ML: Distinct pathogenesis of Hong Kong-origin H5N1 viruses in mice compared to that of other highly pathogenic H5 avian influenza viruses. J Virol 74:1443-1450, 2000.
34. Fodor E., Devenish L., Engelhardt OG, Palese P., Brownlee GG, Garcia-Sastre A.: Rescue of influenza A virus from recombinant DNA. J Virol 73:9679-9682, 1999.
35. Fouchier RA, Schneeberger PM, Rozendaal FW, Broekman JM, Kemink SA, Munster V., Kuiken T., Rimmelzwaan GF, Schutten M., van Doornum GJ, Koch G., Bosman A., Koopmans M., Osterhaus AD: Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome. Proc Natl Acad Sci U S A 101:1356-1361, 2004.
36. Friedewald WF, Hook EW: Influenza virus infection in the hamster: a study of inapparent virus infection and virus adaptation. J Exp Med 88:343-353, 1948.
37. Gao P., Watanabe S., Ito T., Goto H., Wells K., McGregor M., Cooley AJ, Kawaoka Y.: Biological heterogeneity, including systemic replication in mice, of H5N1 influenza A virus isolates from humans in Hong Kong. J Virol 73:3184-3189, 1999.
38. Garten RJ, Davis CT, Russell CA, Shu B., Lindstrom S., Balish A., Sessions WM, Xu X., Skepner E., Deyde V., Okomo-Adhiambo M., Gubareva L., Barnes J., Smith CB, Emery SL, Hillman MJ, Rivailler P., Smagala J., de Graaf M., Burke DF, Fouchier RA, Pappas C., Alpuche-Aranda CM, Lopez-Gatell H., Olivera H., Lopez I., Myers CA, Faix D., Blair PJ, Yu C., Keene KM, Dotson PD Jr, Boxrud D., Sambol AR, Abid SH, St George K., Bannerman T., Moore AL, Stringer DJ, Blevins P., Demmler-Harrison GJ, Ginsberg M., Kriner P., Waterman S., Smole S., Guevara HF, Belongia EA, Clark PA, Beatrice ST, Donis R., Katz J., Finelli L., Bridges CB, Shaw M., Jernigan DB, Uyeki TM, Smith DJ, Klimov AI, Cox NJ: Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 325:197-201, 2009.
39. Giebink GS, Berzins IK, Marker SC, Schiffman G.: Experimental otitis media after nasal inoculation of Streptococcus pneumoniae and influenza A virus in chinchillas. Infect Immun 30:445-450, 1980.
40. Giese M., Harder TC, Teifke JP, Klopfleisch R., Breithaupt A., Mettenleiter TC, Vahlenkamp TW: Experimental infection and natural contact exposure of dogs with avian influenza virus (H5N1). Emerg Infect Dis 14:308-310, 2008.
41. Gill JR, Sheng ZM, Ely SF, Guinee DG, Beasley MB, Suh J., Deshpande C., Mollura DJ, Morens DM, Bray M., Travis WD, Taubenberger JK: Pulmonary pathologic findings of fatal 2009 pandemic influenza A/H1N1 viral infections. Arch Pathol Lab Med 134:235-243, 2010.
42. Govorkova EA, Rehg JE, Krauss S., Yen HL, Guan Y., Peiris M., Nguyen TD, Hanh TH, Puthavathana P., Long HT, Buranathai C., Lim W., Webster RG, Hoffmann E.: Lethality to ferrets of H5N1 influenza viruses isolated from humans and poultry in 2004. J Virol 79:2191-2198, 2005.
43. Hamre D., Appel J., Loosli CG: Viremia in mice with pulmonary influenza A virus infections. J Lab Clin Med 47:182-193, 1956.
44. Hashimoto Y., Moki T., Takizawa T., Shiratsuchi A., Nakanishi Y.: Evidence for phagocytosis of influenza virus-infected, apoptotic cells by neutrophils and macrophages in mice. J Immunol 178:2448-2457, 2007.
45. Hatta M., Gao P., Halfmann P., Kawaoka Y.: Molecular basis for high virulence of Hong Kong H5N1 influenze A viruses. Science 293:1840-1842, 2001.
46. Hayden F.: Developing new antiviral agents for influenza treatment: what does the future hold? Clin Infect Dis 48:S3-S13, 2009.
47. Hayden F., Croisier A.: Transmission of avian influenza viruses to and between humans. J Infect Dis 192:1311-1314, 2005.
48. Herfst S., van den Brand JM, Schrauwen EJA, de Wit E., Munster VJ, van Amerongen G., Linster M., Zaaraoui F., van Ijcken WFJ, Rimmelzwaan GF, Osterhaus ADME, Fouchier RAM, Andeweg AC, Kuiken T.: New H1N1 influenza virus causes diffuse alveolar damage in macaques. Vet Pathol. In press.
49. Hers JF, Masurel N., Mulder J.: Bacteriology and histopathology of the respiratory tract and lungs in fatal Asian influenza. Lancet 2:1141-1143, 1958.
50. Hers JFP, Mulder J.: Broad aspects of the pathology and pathogenesis of human influenza. Am Rev Respir Dis 83:84-97, 1961.
51. Holt PG: Down-regulation of immune responses in the lower respiratory tract: the role of alveolar macrophages. Clin Exp Immunol 63:261-270, 1986.
52. Hulse-Post DJ, Sturm-Ramirez KM, Humberd J., Seiler P., Govorkova EA, Krauss S., Scholtissek C., Puthavathana P., Buranathai C., Nguyen TD, Long HT, Naipospos TS, Chen H., Ellis TM, Guan Y., Peiris JS, Webster RG: Role of domestic ducks in the propagation and biological evolution of highly pathogenic H5N1 influenza viruses in Asia. Proc Natl Acad Sci U S A 102:10682-10687, 2005.
53. Isoda N., Sakoda Y., Kishida N., Bai GR, 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 151:1267-1279, 2006.
54. Itoh Y., Shinya K., Kiso M., Watanabe T., Sakoda Y., Hatta M., Muramoto Y., Tamura D., Sakai-Tagawa Y., Noda T., Sakabe S., Imai M., Hatta Y., Watanabe S., Li C., Yamada S., Fujii K., Murakami S., Imai H., Kakugawa S., Ito M., Takano R., Iwatsuki-Horimoto K., Shimojima M., Horimoto T., Goto H., Takahashi K., Makino A., Ishigaki H., Nakayama M., Okamatsu M., Takahashi K., Warshauer D., Shult PA, Saito R., Suzuki H., Furuta Y., Yamashita M., Mitamura K., Nakano K., Nakamura M., Brockman-Schneider R., Mitamura H., Yamazaki M., Sugaya N., Suresh M., Ozawa M., Neumann G., Gern J., Kida H., Ogasawara K., Kawaoka Y.: In vitro and in vivo characterization of new swine-origin H1N1 influenza viruses. Nature 460:1021-1025, 2009.
55. Jia B., Shi J., Li Y., Shinya K., Muramoto Y., Zeng X., Tian G., Kawaoka Y., Chen H.: Pathogenicity of Chinese H5N1 highly pathogenic avian influenza viruses in pigeons. Arch Virol 153:1821-1826, 2008.
56. Jin H., Manetz S., Leininger J., Luke C., Subbarao K., Murphy B., Kemble G., Coelingh KL: Toxicological evaluation of live attenuated, cold-adapted H5N1 vaccines in ferrets. Vaccine 25:8664- 8672, 2007.
57. Johnson NP, Mueller J.: Updating the accounts: global mortality of the 1918-1920 "Spanish" influenza pandemic. Bull Hist Med 76:105-115, 2002.
58. Jones-Engel L., Engel GA, Schillaci MA, Babo R., Froehlich J.: Detection of antibodies to selected human pathogens among wild and pet macaques (Macaca tonkeana) in Sulawesi, Indonesia. Am J Primatol 54:171-178, 2001.
59. Kalthoff D., Breithaupt A., Teifke JP, Globig A., Harder T., Mettenleiter TC, Beer M.: Highly pathogenic avian influenza virus (H5N1) in experimentally infected adult mute swans. Emerg Infect Dis 14:1267-1270, 2008.
60. Kash JC, Basler CF, Garcia-Sastre A., Carter V., Billharz R., Swayne DE, Przygodzki RM, Taubenberger JK, Katze MG, Tumpey TM: Global host immune response: Pathogenesis and transcriptional profiling of type A influenza viruses expressing the hemagglutinin and neuraminidase genes from the 1918 pandemic virus. J Virol 78:9499-9511, 2004.
61. Kash JC, Tumpey TM, Proll SC, Carter V., Perwitasari O., Thomas MJ, Basler CF, Palese P., Taubenberger JK, Garcia-Sastre A., Swayne DE, Katze MG: Genomic analysis of increased host immune and cell death responses induced by 1918 influenza virus. Nature 443:578-581, 2006.
62. Kawai A., Kimoto T., Oishi I., Yamada T., Kunita N.: Viral infection of cynomolgus macaque (Macaca irus): survey of antiviral antibodies in 178 sera. Primates 9:409-418, 1968.
63. Keawcharoen J., van Riel D., van Amerongen G., Bestebroer T., Beyer WE, van Lavieren R., Osterhaus AD, Fouchier RA, Kuiken T.: Wild ducks as long-distance vectors of highly pathogenic avian influenza virus (H5N1). Emerg Infect Dis 14:600-607, 2008.
64. Kilbourne ED: Influenza. Plenum, New York, NY, 1987.
65. Kobasa D., Jones SM, Shinya K., Kash JC, Copps J., Ebihara H., Hatta Y., Kim JH, Halfmann P., Hatta M., Feldmann F., Alimonti JB, Fernando L., Li Y., Katze MG, Feldmann H., Kawaoka Y.: Aberrant innate immune response in lethal infection of macaques with the 1918 influenza virus. Nature 445:319-323, 2007.
66. Kobasa D., Takada A., Shinya K., Hatta M., Halfmann P., Theriault S., Suzuki H., Nishimura H., Mitamura K., Sugaya N., Usui T., Murata T., Maeda Y., Watanabe S., Suresh M., Suzuki S., Suzuki Y., Feldmann H., Kawaoka Y.: Enhanced virulence of influenza A viruses with the haemagglutinin of the 1918 pandemic virus. Nature 431:703-707, 2004.
67. Koen J.: A practical method for field diagnosis of swine diseases. J Am Vet Med Assoc 14:468-470, 1919.
68. Koopmans M., Wilbrink B., Conyn M., Natrop G., van der Nat H., Vennema H., Meijer A., van Steenbergen J., Fouchier R., Osterhaus A., Bosman A.: Transmission of H7N7 avian influenza A virus to human beings during a large outbreak in commercial poultry farms in the Netherlands. Lancet 363:587-593, 2004.
69. Korteweg C., Gu J.: Pathology, molecular biology, and pathogenesis of avian influenza A (H5N1) infection in humans. Am J Pathol 172:1155-1170, 2008.
70. Kreijtz JH, Osterhaus AD, Rimmelzwaan GF: Vaccination strategies and vaccine formulations for epidemic and pandemic influenza control. Hum Vaccin 5:126-135, 2009.
71. Kreijtz JH, Suezer Y., de Mutsert G., van den Brand JM, van Amerongen G., Schnierle BS, Kuiken T., Fouchier RA, Lower J., Osterhaus AD, Sutter G., Rimmelzwaan GF: Recombinant modified vaccinia virus Ankara expressing the hemagglutinin gene confers protection against homologous and heterologous H5N1 influenza virus infections in macaques. J Infect Dis 199:405-413, 2009.
72. Kuiken T., Rimmelzwaan GF, van Amerongen G., Osterhaus AD: Pathology of human influenza A (H5N1) virus infection in cynomolgus macaques (Macaca fascicularis). Vet Pathol 40:304-310, 2003.
73. Kuiken T., Taubenberger JK: Pathology of human influenza revisited. Vaccine 26:D59-D66, 2008.
74. Kwon YK, Lipatov AS, Swayne DE: Bronchointerstitial pneumonia in guinea pigs following inoculation with H5N1 high pathogenicity avian influenza virus. Vet Pathol 46:138-141, 2009.
75. Lamb FH, Brannin EB: The epidemic respiratory infection at Camp Cody, NM. J Am Med Assoc 72:1056-1062, 1919.
76. Lee CW, Suarez DL, Tumpey TM, Sung HW, Kwon YK, Lee YJ, Choi JG, Joh SJ, Kim MC, Lee EK, Park JM, Lu X., Katz JM, Spackman E., Swayne DE, Kim JH: Characterization of highly pathogenic H5N1 avian influenza A viruses isolated from South Korea. J Virol 79:3692-3702, 2005.
77. Li Z., Chen H., Jiao P., Deng G., Tian G., Li Y., Hoffmann E., Webster RG, Matsuoka Y., Yu K.: Molecular basis of replication of duck H5N1 influenza viruses in a mammalian mouse model. J Virol 79:12058-12064, 2005.
78. Likos AM, Kelvin DJ, Cameron CM, Rowe T., Kuehnert MJ, Norris PJ: Influenza viremia and the potential for blood-borne transmission. Transfusion 47:1080-1088, 2007.
79. Lipatov AS, Kwon YK, Pantin-Jackwood MJ, Swayne DE: Pathogenesis of H5N1 influenza virus infections in mice and ferret models differs according to respiratory tract or digestive system exposure. J Infect Dis 199:717-725, 2009.
80. Lipatov AS, Kwon YK, Sarmento LV, Lager KM, Spackman E., Suarez DL, Swayne DE: Domestic pigs have low susceptibility to H5N1 highly pathogenic avian influenza viruses. PLoS Pathog 4:e1000102, 2008.
81. Liu Y., Zhou J., Yang H., Yao W., Bu W., Yang B., Song W., Meng Y., Lin J., Han C., Zhu J., Ma Z., Zhao J., Wang X.: Susceptibility and transmissibility of pigeons to Asian lineage highly pathogenic avian influenza virus subtype H5N1. Avian Pathol 36:461-465, 2007.
82. Londt BZ, Nunez A., Banks J., Nili H., Johnson LK, Alexander DJ: Pathogenesis of highly pathogenic avian influenza A/turkey/Turkey/1/2005 H5N1 in Pekin ducks (Anas platyrhynchos) infected experimentally. Avian Pathol 37:619-627, 2008.
83. Lowen AC, Mubareka S., Tumpey TM, Garcia-Sastre A., Palese P.: The guinea pig as a transmission model for human influenza viruses. Proc Natl Acad Sci U S A 103:9988-9992, 2006.
84. Lu X., Tumpey TM, Morken T., Zaki SR, Cox NJ, Katz JM: A mouse model for the evaluation of pathogenesis and immunity to influenza A (H5N1) viruses isolated from humans. J Virol 73:5903-5911, 1999.
85. Maines TR, Chen LM, Matsuoka Y., Chen H., Rowe T., Ortin J., Falcon A., Nguyen TH, Mai LQ, Sedyaningsih ER, Harun S., Tumpey TM, Donis RO, Cox NJ, Subbarao K., Katz JM: Lack of transmission of H5N1 avian-human reassortant influenza viruses in a ferret model. Proc Natl Acad Sci U S A 103:12121-12126, 2006.
86. Maines TR, Lu XH, Erb SM, Edwards L., Guarner J., Greer PW, Nguyen DC, Szretter KJ, Chen LM, Thawatsupha P., Chittaganpitch M., Waicharoen S., Nguyen DT, Nguyen T., Nguyen HH, Kim JH, Hoang LT, Kang C., Phuong LS, Lim W., Zaki S., Donis RO, Cox NJ, Katz JM, Tumpey TM: Avian influenza (H5N1) viruses isolated from humans in Asia in 2004 exhibit increased virulence in mammals. J Virol 79:11788-11800, 2005.
87. Martin CM, Kunin CM, Gottlieb LS, Barnes MW, Liu C., Finland M.: Asian influenza A in Boston, 1957-1958: I. Observations in thirty-two influenza-associated fatal cases. AMA Arch Intern Med 103:515-531, 1959.
88. Matrosovich M., Tuzikov A., Bovin N., Gambaryan A., Klimov A., Castrucci MR, 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 74:8502-8512, 2000.
89. Mauad T., Hajjar LA, Callegari GD, da Silva LF, Schout D., Galas FR, Alves VA, Malheiros DM, Auler JO Jr, Ferreira AF, Borsato MR, Bezerra SM, Gutierrez PS, Caldini ET, Pasqualucci CA, Dolhnikoff M., Saldiva PH: Lung pathology in fatal novel human influenza A (H1N1) infection. Am J Respir Crit Care Med 181:72-79, 2010.
90. Memoli MJ, Tumpey TM, Jagger BW, Dugan VG, Sheng ZM, Qi L., Kash JC, Taubenberger JK: An early "classical" swine H1N1 influenza virus shows similar pathogenicity to the 1918 pandemic virus in ferrets and mice. Virology 393:338-345, 2009.
91. Mizgerd JP, Skerrett SJ: Animal models of human pneumonia. Am J Physiol Lung Cell Mol Physiol 294:L387-L398, 2008.
92. Morens DM, Taubenberger JK, Fauci AS: Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness. J Infect Dis 198:962-970, 2008.
93. Mulder J., Hers JFP: Influenza. Wolters-Noordhoff, Groningen, The Netherlands, 1972.
94. Munster VJ, de WE, van den Brand JM, Herfst S., Schrauwen EJ, Bestebroer TM, van de Vijver D., Boucher CA, Koopmans M., Rimmelzwaan GF, Kuiken T., Osterhaus AD, Fouchier RA: Pathogenesis and transmission of swine-origin 2009 A (H1N1) influenza virus in ferrets. Science 325:481-483, 2009.
95. Murphy BR, Hinshaw VS, Sly DL, London WT, Hosier NT, Wood FT, Webster RG, Chanock RM: Virulence of avian influenza A viruses for squirrel monkeys. Infect Immun 37:1119- 1126, 1982.
96. Myers KP, Olsen CW, Gray GC: Cases of swine influenza in humans: a review of the literature. Clin Infect Dis 44:1084- 1088, 2007.
97. Nelson R.: Influenza A H2N2 saga remains unexplained. Lancet Infect Dis 5:332, 2005.
98. Neufeld JL, Embury-Hyatt C., Berhane Y., Manning L., Ganske S., Pasick J.: Pathology of highly pathogenic avian influenza virus (H5N1) infection in Canada geese (Branta canadensis): preliminary studies. Vet Pathol 46:966-970, 2009.
99. Neumann G., Watanabe T., Ito H., Watanabe S., Goto H., Gao P., Hughes M., Perez DR, Donis R., Hoffmann E., Hobom G., Kawaoka Y.: Generation of influenza A viruses entirely from cloned cDNAs. Proc Natl Acad Sci U S A 96: 9345-9350, 1999.
100. Nishimura H., Itamura S., Iwasaki T., Kurata T., Tashiro M.: Characterization of human influenza A (H5N1) virus infection in mice: neuro-, pneumo- and adipotropic infection. J Gen Virol 81:2503-2510, 2000.
101. OIE. Avian influenza: article 10.4.1. In: Terrestrial Animal Health Code. 2009. http://www.oie.int/Eng/normes/mcode/en_chapitre_1.10.4.htm. Accessed July 1, 2010.
102. OIE. Highly pathogenic avian influenza, Spain. http://www.oie.int/wahis/public.php?page=single_report&pop=1&reportid=8521. Accessed July 1, 2010.
103. OIE. Highly pathogenic avian influenza, United Kingdom. http://www.oie.int/wahis/reports/en_fup_0000007028_20080512_112233.pdf. Accessed July 1, 2010.
104. Pantin-Jackwood MJ, Swayne DE: Pathobiology of Asian highly pathogenic avian influenza H5N1 virus infections in ducks. Avian Dis 51:250-259, 2007.
105. Pantin-Jackwood MJ, Swayne DE: Pathogenesis and pathobiology of avian influenza virus infection in birds. Rev Sci Tech 28:113-136, 2009.
106. Park CH, Ishinaka M., Takada A., Kida H., Kimura T., Ochiai K., Umemura T.: The invasion routes of neurovirulent A/Hong Kong/483/97 (H5N1) influenza virus into the central nervous system after respiratory infection in mice. Arch Virol 147:1425-1436, 2002.
107. Pasick J., Berhane Y., Embury-Hyatt C., Copps J., Kehler H., Handel K., Babiuk S., Hooper-McGrevy K., Li Y., Mai LQ, Lien PS: Susceptibility of Canada Geese (Branta canadensis) to highly pathogenic avian influenza virus (H5N1). Emerg Infect Dis 13:1821-1827, 2007.
108. Perkins LE, Swayne DE: Comparative susceptibility of selected avian and mammalian species to a Hong Kong-origin H5N1 high-pathogenicity avian influenza virus. Avian Dis 47:956- 967, 2003.
109. Perkins LE, Swayne DE: Pathogenicity of a Hong Kong-origin H5N1 highly pathogenic avian influenza virus for emus, geese, ducks, and pigeons. Avian Dis 46:53-63, 2002.
110. Perkins LE, Swayne DE: Varied pathogenicity of a Hong Kong-origin H5N1 avian influenza virus in four passerine species and budgerigars. Vet Pathol 40:14-24, 2003.
111. Perrone LA, Plowden JK, Garcia-Sastre A., Katz JM, Tumpey TM: H5N1 and 1918 pandemic influenza virus infection results in early and excessive infiltration of macrophages and neutrophils in the lungs of mice. PLoS Pathog 4:e1000115, 2008.
112. Pfeiffer J., Pantin-Jackwood M., To TL, Nguyen T., Suarez DL: Phylogenetic and biological characterization of highly pathogenic H5N1 avian influenza viruses (Vietnam 2005) in chickens and ducks. Virus Res 142:108-120, 2009.
113. Qi L., Kash JC, Dugan VG, Wang R., Jin G., Cunningham RE, Taubenberger JK: Role of sialic acid binding specificity of the 1918 influenza virus hemagglutinin protein in virulence and pathogenesis for mice. J Virol 83:3754-3761, 2009.
114. Ray CG, Icenogle TB, Minnich LL, Copeland JG, Grogan TM: The use of intravenous ribavirin to treat influenza virus-associated acute myocarditis. J Infect Dis 159:829-836, 1989.
115. Reid AH, Fanning TG, Hultin JV, Taubenberger JK: Origin and evolution of the 1918 "Spanish" influenza virus hemagglutinin gene. Proc Natl Acad Sci U S A 96:1651-1656, 1999.
116. Reid AH, Fanning TG, Janczewski TA, Lourens RM, Taubenberger JK: Novel origin of the 1918 pandemic influenza virus nucleoprotein gene. J Virol 78:12462-12470, 2004.
117. Reid AH, Fanning TG, Janczewski TA, McCall S., Taubenberger JK: Characterization of the 1918 "Spanish" influenza virus matrix gene segment. J Virol 76:10717-10723, 2002.
118. Reid AH, Fanning TG, Janczewski TA, Taubenberger JK: Characterization of the 1918 "Spanish" influenza virus neuraminidase gene. Proc Natl Acad Sci U S A 97:6785-6790, 2000.
119. Reperant LA, Rimmelzwaan GF, Kuiken T.: Avian influenza viruses in mammals. Rev Sci Tech 28:137-159, 2009.
120. Reperant LA, van Amerongen G., van de Bildt MW, Rimmelzwaan GF, Dobson AP, Osterhaus AD, Kuiken T.: Highly pathogenic avian influenza virus (H5N1) infection in red foxes fed infected bird carcasses. Emerg Infect Dis 14:1835-1841, 2008.
121. Rimmelzwaan G., van Riel D., Baars M., Bestebroer TM, van Amerongen G., Fouchier RAM, Osterhaus ADME, Kuiken T.: Influenza A virus (H5N1) infection in cats causes systemic disease with potential novel routes of virus spread within and between hosts. Am J Pathol 168:176-183, 2006.
122. Rimmelzwaan GF, Kuiken T., van Amerongen G., Bestebroer TM, Fouchier RA, Osterhaus AD: Pathogenesis of influenza A (H5N1) virus infection in a primate model. J Virol 75:6687- 6691, 2001.
123. Rothberg MB, Haessler SD: Complications of seasonal and pandemic influenza. Crit Care Med 38:e91-e97, 2009.
124. Rowe T., Cho DS, Bright RA, Zitzow LA, Katz JM: Neurological manifestations of avian influenza viruses in mammals. Avian Dis 47:1122-1126, 2003.
125. Rubin SA, Liu D., Pletnikov M., McCullers JA, Ye Z., Levandowski RA, Johannessen J., Carbone KM: Wild-type and attenuated influenza virus infection of the neonatal rat brain. J Neurovirol 10:305-314, 2004.
126. Saito T., Watanabe C., Takemae N., Chaisingh A., Uchida Y., Buranathai C., Suzuki H., Okamatsu M., Imada T., Parchariyanon S., Traiwanatam N., Yamaguchi S.: Pathogenicity of highly pathogenic avian influenza viruses of H5N1 subtype isolated in Thailand for different poultry species. Vet Microbiol 133:65-74, 2008.
127. Salomon R., Franks J., Govorkova EA, Ilyushina NA, Yen HL, Hulse-Post DJ, Humberd J., Trichet M., Rehg JE, Webby RJ, Webster RG, Hoffmann E.: The polymerase complex genes contribute to the high virulence of the human H5N1 influenza virus isolate A/Vietnam/1203/04. J Exp Med 203:689-697, 2006.
128. Saslaw S., Carlisle HN: Aerosol exposure of monkeys to influenza virus. Proc Soc Exp Biol Med 119:838-843, 1965.
129. Scholtissek C., Burger H., Kistner O., Shortridge KF: The nucleoprotein as a possible major factor in determining host specificity of influenza H3N2 viruses. Virology 147:287-294, 1985.
130. Schrauder A., Schweiger B., Buchholz U., Haas W., Sagebiel D., Guignard A., Hellenbrand W.: Laboratory exposure to influenza A H2N2, Germany, 2004-2005. Emerg Infect Dis 12:1997- 1998, 2006.
131. Seo SH, Hoffmann E., Webster RG: Lethal H5N1 influenza viruses escape host anti-viral cytokine responses. Nat Med 8:950-954, 2002.
132. Shope R.: Swine influenza: III. Filtration experiments and etiology. J Exp Med 54:373-385, 1931.
133. Stittelaar KJ, Tisdale M., van Amerongen G., van Lavieren RF, Pistoor F., Simon J., Osterhaus AD: Evaluation of intravenous zanamivir against experimental influenza A (H5N1) virus infection in cynomolgus macaques. Antiviral Res 80:225-228, 2008.
134. Stubbs EL: Fowl pest. In: Diseases of Poultry, ed. Biester HE, Schwarte LH, 2nd ed., pp. 603-614. Iowa State University Press, Ames, IA, 1948.
135. Studahl M.: Influenza virus and CNS manifestations. J Clin Virol 28:225-232, 2003.
136. Sturm-Ramirez KM, Ellis T., Bousfield B., Bissett L., Dyrting K., Rehg JE, Poon L., Guan Y., Peiris M., Webster RG: Reemerging H5N1 influenza viruses in Hong Kong in 2002 are highly pathogenic to ducks. J Virol 78:4892-4901, 2004.
137. Sturm-Ramirez KM, Hulse-Post DJ, Govorkova EA, Humberd J., Seiler P., Puthavathana P., Buranathai C., Nguyen TD, Chaisingh A., Long HT, Naipospos TSP, Chen H., Ellis TM, Guan Y., Peiris JSM, Webster RG: Are ducks contributing to the endemicity of highly pathogenic H5N1 influenza virus in Asia? J Virol 79:11269-11279, 2005.
138. Swayne DE: The global nature of avian influenza. In: Avian Influenza, ed. Swayne DE, pp. 123-143. Blackwell, Ames, IA, 2008.
139. Swayne DE: Understanding the complex pathobiology of high pathogenicity avian influenza viruses in birds. Avian Dis 51:242-249, 2007.
140. Swayne DE, Halvorson DA: Influenza. In: Diseases of Poultry, ed. Saif YM, Glisson JR, Fadly AM, McDougald LR, Nolan L, 12th ed., pp. 153-184. Blackwell, Ames, IA, 2008.
141. Taubenberger JK: The origin and virulence of the 1918 "Spanish" influenza virus. Proc Am Philos Soc 150:86-112, 2006.
142. Taubenberger JK, Hultin JV, Morens DM: Discovery and characterization of the 1918 pandemic influenza virus in historical context. Antivir Ther 12:581-591, 2007.
143. Taubenberger JK, Morens DM: Pandemic influenza-including a risk assessment of H5N1. Rev Sci Tech 28:187-202, 2009.
144. Taubenberger JK, Morens DM: The pathology of influenza virus infections. Annu Rev Pathol 3:499-522, 2008.
145. Taubenberger JK, Reid AH, Fanning TG: The 1918 influenza virus: A killer comes into view. Virology 274:241-245, 2000.
146. Taubenberger JK, Reid AH, Lourens RM, Wang R., Jin G., Fanning TG: Characterization of the 1918 influenza virus polymerase genes. Nature 437:889-893, 2005.
147. Teifke JP, Klopfleisch R., Globig A., Starick E., Hoffmann B., Wolf PU, Beer M., Mettenleiter TC, Harder TC: Pathology of natural infections by H5N1 highly pathogenic avian influenza virus in mute (Cygnus olor) and whooper (Cygnus cygnus) swans. Vet Pathol 44:137-143, 2007.
148. Terregino C., Milani A., Capua I., Marino AM, Cavaliere N.: Highly pathogenic avian influenza H5N1 subtype in mute swans in Italy. Vet Rec 158:491, 2006.
149. Tumpey TM, Basler CF, Aguilar PV, Zeng H., Solorzano A., Swayne DE, Cox NJ, Katz JM, Taubenberger JK, Palese P., Garcia-Sastre A.: Characterization of the reconstructed 1918 Spanish influenza pandemic virus. Science 310:77-80, 2005.
150. Tumpey TM, Maines TR, Van Hoeven N., Glaser L., Solorzano A., Pappas C., Cox NJ, Swayne DE, Palese P., Katz JM, Garcia-Sastre A.: A two-amino acid change in the hemagglutinin of the 1918 influenza virus abolishes transmission. Science 315:655- 659, 2007.
151. van den Brand JMA, Stittelaar KJ, van Amerongen G., Rimmelzwaan GF, Simon J., de Wit E., Munster V., Bestebroer T., Fouchier RA, Kuiken T., Osterhaus AD Severity of pneumonia due to new H1N1 influenza virus in ferrets is intermediate between that due to seasonal H1N1 virus and highly pathogenic avian influenza H5N1 virus. J Infect Dis 201:993-999, 2010.
152. van Hoeven N., Belser JA, Szretter KJ, Zeng H., Staeheli P., Swayne DE, Katz JM, Tumpey TM: Pathogenesis of 1918 pandemic and H5N1 influenza virus infections in a guinea pig model: antiviral potential of exogenous alpha interferon to reduce virus shedding. J Virol 83:2851-2861, 2009.
153. van Riel D., den Bakker M., Leijten L., Chutinimitkul S., Munster V., de Wit E., Rimmelzwaan G., Fouchier R., Osterhaus A., Kuiken T.: Seasonal and pandemic human influenza viruses attach better to human upper respiratory tract epithelium than avian influenza viruses. Am J Pathol 176:1614-1618, 2010.
154. van Riel D., Munster VJ, de Wit E., Rimmelzwaan GF, Fouchier RA, Osterhaus AD, Kuiken T.: Human and avian influenza viruses target different cells in the lower respiratory tract of humans and other mammals. Am J Pathol 171:1215- 1223, 2007.
155. van Riel D., Munster VJ, de Wit E., Rimmelzwaan GF, Fouchier RAM, Osterhaus ADME, Kuiken T.: H5N1 virus attachment to lower respiratory tract. Science 311:399, 2006.
156. Walsh JJ, Dietlein LF, Low FN, Burch GE, Mogabgab WJ: Bronchotracheal response in human influenza: type A, Asian strain, as studied by light and electron microscopic examination of bronchoscopic biopsies. Arch Intern Med 108:376- 388, 1961.
157. Ware LB, Matthay MA: The acute respiratory distress syndrome. N Engl J Med 342:1334-1349, 2000.
158. Watanabe T., Watanabe S., Shinya K., Kim JH, Hatta M., Kawaoka Y.: Viral RNA polymerase complex promotes optimal growth of 1918 virus in the lower respiratory tract of ferrets. Proc Natl Acad Sci U S A 106:588-592, 2009.
159. Wattrang E., Jessett DM, Yates P., Fuxler L., Hannant D.: Experimental infection of ponies with equine influenza A2 (H3N8) virus strains of different pathogenicity elicits varying interferon and interleukin-6 responses. Viral Immunol 16:57-67, 2003.
160. Webby RJ, Webster RG: Are we ready for pandemic influenza? Science 302:1519-1522, 2003.
161. Weingartl HM, Albrecht RA, Lager KM, Babiuk S., Marszal P., Neufeld J., Embury-Hyatt C., Lekcharoensuk P., Tumpey TM, Garcia-Sastre A., Richt JA: Experimental infection of pigs with the human 1918 pandemic influenza virus. J Virol 83:4287- 4296, 2009.
162. WHO. Confirmed human cases of avian influenza A (H5N1): 28 January 2010. http://www.who.int/csr/disease/avian_influenza/country/cases_table_2010_01_28/en/index.html. Accessed July 1, 2010.
163. Yen HL, Lipatov AS, Ilyushina NA, Govorkova EA, Franks J., Yilmaz N., Douglas A., Hay A., Krauss S., Rehg JE, Hoffmann E., Webster RG: Inefficient transmission of H5N1 influenza viruses in a ferret contact model. J Virol 81:6890-6898, 2007.
164. Zitzow LA, Rowe T., Morken T., Shieh WJ, Zaki S., Katz JM: Pathogenesis of avian influenza A (H5N1) viruses in ferrets. J Virol 76:4420-4429, 2002.