Pathogenesis of highly pathogenic avian influenza A virus (H7N1) infection in chickens inoculated with three different doses

References

• Alexander , D.J. 2000 . A review of avian influenza in different bird species . Veterinary Microbiology , 74 , 3 13 .
   PubMed Web of Science ®Google Scholar
• Alexander , D.J. 2007 . An overview of the epidemiology of avian influenza . Vaccine , 25 , 5637 5644 .
   PubMed Web of Science ®Google Scholar
• Alexander , D.J. , Parsons , G. & Manvell , R.J. 1986 . Experimental assessment of the pathogenicity of eight avian influenza A viruses of H5 subtype for chickens, turkeys, ducks and quail . Avian Pathology , 15 , 647 662 .
   PubMed Web of Science ®Google Scholar
• Barnes , H.J. , Nolan , L.K. & Vaillancourt , J.P. 2008 . Collibacillosis . In Y.M. Saif , A.M. Fadly , J.R. Glisson , L.R. McDougald , L.K. Nolan & D.E. Swayne Diseases of Poultry , 11th edn 691 712 . Ames, IA : Iowa State Press
   Google Scholar
• Beato , M.S. , Toffan , A. , De Nardi , R. , Cristalli , A. , Terregino , C. , Cattoli , G. and Capua , I. 2007 . A conventional, inactivated oil emulsion vaccine suppresses shedding and prevents viral meat colonisation in commercial (Pekin) ducks challenged with HPAI H5N1 . Vaccine , 25 : 4064 – 4072 .
   PubMed Web of Science ®Google Scholar
• Bingham , J. , Green , D.J. , Lowther , S. , Klippel , J. , Burggraaf , S. , Anderson , D.E. , et al. . 2009 . 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 Pathology , 38 , 267 278 .
   PubMed Web of Science ®Google Scholar
• Brown , C.C. , Olander , H.J. & Senne , D.A. 1992 . A pathogenesis study of highly pathogenic avian influenza virus H5N2 in chickens, using immunohistochemistry . Journal of Comparative Pathology , 107 , 341 348 .
   PubMed Web of Science ®Google Scholar
• Brown , J.D. , Stallknecht , D.E. & Swayne , D.E. 2008 . 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 Pathology , 37 , 393 397 .
   PubMed Web of Science ®Google Scholar
• Brown , J.D. , Stalknecht , D.E. , Berghaus , R.D. and Swayne , D.E. 2009 . Infectious and lethal doses of H5N1 highly pathogenic avian influenza virus for house sparrows (Passer domesticus) and rock pigeons (Columbia livia) . Journal of Veterinary Diagnostic Investigation , 21 : 437 – 455 .
   PubMed Web of Science ®Google Scholar
• Busquets , N. , Alba , A. , Napp , S. , Sánchez , A. , Serrano , E. , Rivas , R. , et al. . 2010a . Influenza A virus subtypes in wild birds in North-Eastern Spain (Catalonia) . Virus Research , 149 , 10 18 .
   PubMed Web of Science ®Google Scholar
• Busquets , N. , Abad , F.X. , Alba , A. , Dolz , R. , Allepuz , A. , Rivas , R. , et al. . 2010b . Persistence of highly pathogenic avian influenza virus (H7N1) in infected chickens: feather as a suitable sample for diagnosis . Journal of General Virology 91 2307 2313
   PubMed Web of Science ®Google Scholar
• Campitelli , L. , Di Martino , A. , Spagnolo , D. , Smith , G.J. , Di Trani , L. , Facchini , M. , et al. . 2008 . Molecular analysis of avian H7 influenza viruses circulating in Eurasia in 1999–2005: detection of multiple reassortant virus genotypes . Journal of General Virology , 89 , 48 59 .
   PubMed Web of Science ®Google Scholar
• Capua , I. , Marangon , S. , Selli , L. , Alexander , D.J. , Swayne , D.E. , Pozza , M.D. & Cancellotti , F.M. 1999 . Outbreaks of highly pathogenic avian influenza (H5N2) in Italy during October 1997 to January 1998 . Avian Pathology , 28 , 455 460
   PubMed Web of Science ®Google Scholar
• Capua , I. , Mutinelli , F. , Marangon , S. & Alexander , D.J. 2000 . H7N1 Avian influenza in Italy (1999–2000) in intensively reared chickens and turkeys . Avian Pathology , 29 , 537 543 .
   PubMed Web of Science ®Google Scholar
• Capua , I. , Mutinelli , F. & Hablovarid , M.H. 2002 . Avian embryo susceptibility to Italian H7N1 avian influenza viruses belonging to different genetic lineages . Archives of Virology 147 , 1611 1621 .
   PubMedGoogle Scholar
• Denbow , D.M. , Duke , G.E. & Chaplin , S.B. 1988 . Food intake, gastric secretion, and motility as affected by avian pancreatic polypeptide administered centrally in chickens . Peptides , 9 3 , 449 454 .
   PubMed Web of Science ®Google Scholar
• Ellis , T.M. , Bousfield , R.B. , Bissett , L.A. , Dyrting , K.C. , Luk , G.S.M. , Tsim , S.T. , et al. . 2004 . Investigation of outbreaks of highly pathogenic H5N1 avian influenza in waterfowl and wild birds in Hong Kong in late 2002 . Avian Pathology , 33 , 492 505 .
   PubMed Web of Science ®Google Scholar
• Feldmann , A. , Schafer , M.K.-H. , Garten , W. and Klenk , H-D. 2000 . Targeted infection of endothelial cells by avian influenza virus A/FPV/Rostock/34 (H7N1) in chicken embryos . Journal of Virology , 74 : 8018 – 8027 .
   PubMed Web of Science ®Google Scholar
• Feldmann , A. , Looser , N. , Wagner , R. & Klenk , H.-D. 2001 . Targeted influenza virus infection of endothelial cells and leucocytes . International Congress Series , 1219 , 557 571 .
   Google Scholar
• Fouchier , R.A.M. , Schneeberger , P.M. , Rozendaal , F.W. , Broekman , J.M. , Kemink , S.A.G. , Munster , V.J. , et al. . 2004 . Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome . Proceedings of the National Academy of Sciences of the United States of America 101 , 1356 1361 .
   PubMed Web of Science ®Google Scholar
• Fronhoffs , S. , Totzke , G. , Stier , S. , Wernert , N. , Rothe , M. , Bruning , T. , et al. . 2002 . A method for the rapid construction of cRNA standard curves in quantitative real-time reverse transcription polymerase chain reaction . Molecular and Cellular Probes 16 , 99 110 .
   PubMed Web of Science ®Google Scholar
• Goletic , T. , Gagic , A. , Residbegovic , E. , Kustura , A. and Kavazovic , A. 2010 . Highly pathogenic avian influenza virus subtype H5N1 in mute swans (Cygnus olor) in central Bosnia . Avian Diseases , 54 : 496 – 501 .
   PubMedGoogle Scholar
• Hooper , P. & Selleck , P. 1998 . Pathology of low and high virulent influenza virus infections . In D.E. Swayne & R.D. Slemons . Proceedings of the Fourth International Symposium on Avian Influenza , Athens, GA 134 141 . Athens, GA : US Animal Health Association, The University of Georgia .
   Google Scholar
• Jones , Y.J. & Swayne , D.E. 2004 . Comparative pathobiology of low and high pathogenicity H7N3 Chilean avian influenza viruses in chickens . Avian Diseases , 48 , 119 128 .
   PubMed Web of Science ®Google Scholar
• Joseph , T. , McAuliffe , J. , Lu , B. , Jin , H. , Kemble , G. & Subbarao , K. 2007 . Evaluation of replication and pathogenicity of avian influenza A H7 subtype 1 viruses in a mouse model . Journal of Virology , 81 , 10558 10566 .
   PubMed Web of Science ®Google Scholar
• Kawaoka , Y. and Webster , R.G. 1988 . Molecular mechanisms of acquisition of virulence in influenza virus in nature . Microbial Pathogenesis , 5 : 311 – 318 .
   PubMed Web of Science ®Google Scholar
• Kishida , N. , Sakoda , Y. , Eto , M. , Sunaga , Y. & Kida , H. 2004 . Co-infection of Staphylococcus aureus or Haemophilus paragallinarum exacerbates H9N2 influenza A virus infection in chickens . Archives of Virology , 149 , 2095 2104 .
   PubMed Web of Science ®Google Scholar
• Klopfleisch , R. , Werner , O. , Mundt , E. , Harder , T. & Teifke , J.P. 2006 Neurotropism of highly pathogenic avian influenza virus A/chicken/Indonesia/2003 (H5N1) in experimentally infected pigeons (Columbia livia f. domestica) . Veterinary Pathology , 43 463 470 .
   PubMed Web of Science ®Google Scholar
• Kobayashi , Y. , Horimoto , Y. , Kawaoka , Y. , Alexander , D.J. & Itakura , C. 1996a . Neuropathological studies of chickens infected with highly pathogenic avian influenza viruses . Journal of Comparative Pathology , 114 , 131 147 .
   PubMedGoogle Scholar
• Kobayashi , Y. , Horimoto , T. , Kawaoka , Y. , Alexander , D.J. & Itakura , C. 1996b . Pathological studies of chickens experimentally infected with two highly pathogenic avian influenza viruses . Avian Pathology , 25 , 285 304 .
   PubMed Web of Science ®Google Scholar
• Kreijtz , J.H.C.M. , Bodewes , R. , van Amerongen , G. , Kuiken , T. , Fouchier , R.A.M. Osterhaus , A.D.M.E. & Rimmelzwaan , G.F. 2007 . Primary influenza A virus infection induces cross-protective immunity against a lethal infection with a heterosubtypic virus strain in mice . Vaccine , 25 , 612 620 .
   PubMed Web of Science ®Google Scholar
• Kwon , Y.-K. , Joh , S.-J. , Kim , M.-C. , Sung , H.-W. , Lee , Y.-J. , Choi , J.-G. , et al. . 2005 . Highly pathogenic avian influenza (H5N1) in the commercial domestic ducks of South Korea . Avian Pathology , 34 , 367 370 .
   PubMed Web of Science ®Google Scholar
• Lipatov , A.S. , Krauss , S. , Guan , Y. , Peiris , M. , Rehg , J.E. , Perez , D.R. & Webster , R.G. 2003 . Neurovirulence in mice of H5N1 influenza virus genotypes isolated from Hong Kong poultry in 2001 . Journal of Virology , 77 , 3816 3823 .
   PubMedGoogle Scholar
• Liu , N.Q. , Lossinsky , A.S. , Popik , W. , Li , X. , Gujuluva , C. , Kriederman , B. , et al. . 2002 . Human immunodeficiency virus type 1 enters brain microvascular endothelia by macropinocytosis dependent on lipid rafts and the mitogen-activated protein kinase signaling pathway . Journal of Virology , 7 , 6689 6700 .
   Google Scholar
• Löndt , B.Z. , Nunez , A. , Banks , J. Nili Hassan , J. , Johnson L. K & Alexander , D.J. 2008 . Pathogenesis of highly pathogenic avian influenza A/turkey/Turkey/1/2005 H5N1 in Pekin ducks (Anas platyrhynchos) infected experimentally . Avian Pathology , 37 , 619 627 .
   PubMed Web of Science ®Google Scholar
• Lossinsky , A.S. and Shivers , R.R. 2004 . Structural pathways for macromolecular and cellular transport across the blood–brain barrier during inflammatory conditions. Review . Histology and Histopathology , 19 : 535 – 564 .
   PubMed Web of Science ®Google Scholar
• Majde , J.A. , Bohnet , S.G. , Ellis , G.A. , Churchill , L. , Leyva-Grado , V. , Wu , M. , et al. . 2007 . Detection of mouse-adapted human influenza virus in the olfactory bulbs of mice within hours after intranasal infection . Journal of Neurovirology , 13 , 399 409 .
   PubMed Web of Science ®Google Scholar
• Matsuda , K. , Park , C.H. , Sunden , Y. , Kimura , T. , Ochiai , K. , Kida , H. & Umemura , T. 2004 . The vagus nerve is one route of transneural invasion for intranasally inoculated influenza A virus in mice . Veterinary Pathology , 41 , 101 107 .
   PubMed Web of Science ®Google Scholar
• Mo , I.P. , Brugh , O.J. , Fletcher , G.N. , Rowland , M. and Swayne , D.E. 1996 . Comparative pathology of chickens experimentally inoculated with avian influenza viruses of low and high pathogenicity . Avian Diseases , 41 : 125 – 136 .
   Google Scholar
• Mori , I. , Komatsu , T. , Takeuchi , K. , Nakakuki , K. , Sudo , M. & Kimura , Y. 1995 . Viremia induced by influenza . Microbiology and Pathogenesis , 19 , 237 244 .
   PubMed Web of Science ®Google Scholar
• Muramoto , Y. , Ozaki , H. , Takada , A. , Park , C-H. , Sunden , Y. Umemura , T. 2006 . Highly pathogenic H5N1 influenza virus causes coagulopathy in chickens . Microbiology and Immunology , 50 : 73 – 81 .
   PubMed Web of Science ®Google Scholar
• Mutinelli , F. , Capua , I. , Terregino , C. & Cattoli , G. 2003 . Clinical, gross, and microscopic findings in different avian species naturally infected during the H7N1 low- and high-pathogenicity avian influenza low- and high-pathogenicity avian influenza epidemics in Italy during 1999 and 2000 . Avian Diseases , 47 , 844 848 .
   PubMed Web of Science ®Google Scholar
• Nakamura , K. , Imada , T. , Imai , K. , Yamamoto , Y. , Tanimura , N. , Yamada , M. , et al. . 2008 . Pathology of specific-pathogen-free chickens inoculated with H5N1 avian influenza viruses isolated in Japan in 2004 . Avian Diseases , 52 , 8 13 .
   PubMed Web of Science ®Google Scholar
• OIE . 2008 . Avian influenza . In Manual of Diagnostic Tests and Vaccines for Terrestrial Animals 2008 , 6th edn Office International des Epizooties (OIE). Available online at http://www.oie.int/eng/normes/mmanual/2008/pdf/2.03.04_AI.pdf .
   Google Scholar
• Pálmai , N. , Erdélyi , K. , Bálint , Á. , Márton , L. , Dán , Á. , Deim , Z. , et al. . 2007 . Pathobiology of highly pathogenic avian influenza virus (H5N1) infection in mute swans (Cygnus olor) , Avian Pathology , 36 , 245 249 .
   PubMed Web of Science ®Google Scholar
• Panigraphy , B. , Senne , D. A. and Pedersen , J. C. 2002 . Avian influenza virus subtypes inside and outside the live bird markets, 1993–2000: a spatial and temporal realationship . Avian Diseases , 46 : 298 – 307 .
   PubMedGoogle Scholar
• Pantin-Jackwood , M.J. and Swayne , D.E. 2009 . Pathogenesis and pathobiology of avian influenza virus infection in birds . Revue Scientifique et Technique , 28 : 113 – 136 .
   PubMed Web of Science ®Google Scholar
• Park , C.H. , Ishinaka , M. , Takada , A. , Kida , H. , Kimura , T. , Ochiai , K. & Umemura , T.T. 2002 . The invasion routes of neurovirulent A/Hong Kong/483/97 (H5N1) influenza virus into the central nervous system after respiratory infection in mice . Archives of Virology , 147 , 1425 1436 .
   PubMed Web of Science ®Google Scholar
• Pasick , Y. , Berhane , Y. , Hisanaga , T. , Kehler , H. , Hooper-McGrevy , K. , Handel , K. , et al. . 2010 . Diagnostic test results and pathology associated with the 2007 Canadian H7N3 highly pathogenic avian influenza outbreak . Avian Diseases , 54 , 213 219 .
   PubMedGoogle Scholar
• Perkins , L.E.L. & Swayne , D.E. 2001 . Pathobiology of A/chicken/Hong Kong/220/97 (H5N1) avian influenza virus in seven gallinaceous species . Veterinary Pathology , 38 , 149 164 .
   PubMed Web of Science ®Google Scholar
• Perkins , L.E.L. and Swayne , D.E. 2002 . Pathogenicity of a Hong Kong-origin H5N1 highly pathogenic avian influenza virus for emus, geese, ducks, and pigeons . Avian Diseases , 46 : 53 – 63 .
   PubMed Web of Science ®Google Scholar
• Perkins , L.E.L. and Swayne , D.E. 2003a . Comparative susceptibility of selected avian and mammalian species to a Hong Kong-Origin H5N1 high-pathogenicity avian influenza virus . Avian Diseases , 47 : 956 – 967 .
   PubMed Web of Science ®Google Scholar
• Perkins , L.E.L. & Swayne , D.E. 2003b . Varied pathogenicity of a Hong Kong-origin H5N1 avian influenza virus in four passerine species and budgerigars . Veterinary Pathology , 40 , 14 24 .
   PubMed Web of Science ®Google Scholar
• Reed , L.J. and Muench , H. 1938 . A simple method of estimating fifty percent endpoints . The American Journal of Hygiene , 27 : 493 – 497 .
   Google Scholar
• Rigoni , M. , Shinya , K. , Toffan , A. , Milani , A. , Bettini , F. , Kawaoka , Y. , et al. . 2007 . Pneumo- and neurotropism of avian origin italian highly pathogenic avian influenza H7N1 isolates in experimentally infected mice . Virology , 364 , 28 35 .
   PubMed Web of Science ®Google Scholar
• Rowe , T. , Cho , D.S. , Bright , R.A. , Zitzow , L.A. and Katz , J.M. 2003 . Neurological manifestations of avian influenza viruses in mammals . Avian Diseases , 47 : 1122 – 1126 .
   PubMed Web of Science ®Google Scholar
• Shortridge , K.F. , Zhou , N.N. , Guan , Y. , Gao , P. , Ito , T. , Kawaoka , Y. , et al. . 1998 . Characterization of avian H5N1 influenza viruses from poultry in Hong Kong . Virology , 252 , 331 342
   PubMed Web of Science ®Google Scholar
• Spackman , E. , Senne , D.A. , Myers , T.J. , Bulaga , L.L. , Garber , L.P. Perdue , M.L. 2002 . Development of a real-time reverse transcriptase PCR assay for type A influenza virus and the avian H5 and H7 hemaglutinin subtypes . Journal of Clinical Microbiology , 40 : 3256 – 3260 .
   PubMed Web of Science ®Google Scholar
• Suarez , D.L. , Perdue , M.L. , Cox , N. , Rowe , T. , Bender , C. , Huang , J. and Swayne , D.E. 1998 . Comparison of highly virulent H5N1 influenza A viruses isolated from humans and chickens from Hong Kong . Journal of Virology , 72 : 6678 – 6688 .
   PubMed Web of Science ®Google Scholar
• Subbarao , K. , Klimov , A. , Katz , J. , Regnery , H. , Lim , W. , Hall , H. , et al. . 1998 . Characterization of an avian influenza A H5N1 virus isolated from a child with a fatal respiratory illness . Science , 16 , 393 396 .
   Google Scholar
• Swayne , D.E. 1997 . Pathobiology of H5N2 Mexican avian influenza virus infections in chickens . Veterinary Pathology , 31 , 557 567 .
   Web of Science ®Google Scholar
• Swayne , D.E. 2007 . Understanding the complex pathology of high pathogenicity avian influenza viruses in birds . Avian Diseases , 51 , 242 249 .
   PubMed Web of Science ®Google Scholar
• Swayne , D.E. and Beck , J.R. 2005 . Experimental study to determine if low-pathogenicity and high-pathogenicity avian influenza viruses can be present in chicken breast and thigh meat following intranasal virus inoculation . Avian Diseases , 49 : 81 – 85 .
   PubMed Web of Science ®Google Scholar
• Swayne , D.E. and Halvorson , D.A. 2008 . “ Influenza ” . In Diseases of Poultry , 11th edn , Edited by: Saif , Y.M. , Fadly , A.M. , Glisson , J.R. , McDougald , L.R. , Nolan , L.K. and Swayne , D.E. 153 – 185 . Ames, IA : Iowa State Press .
   Google Scholar
• Tanaka , H. , Park , C. , Ninomiya , A. , Ozaki , H. , Takada , A. , Umemura , T. & Kida , H. 2003 . Neurotropism of the 1997 Hong Kong H5N1 influenza virus in mice . Veterinary Microbiology , 95 , 1 13 .
   PubMed Web of Science ®Google Scholar
• Tang , Y. , Wu , P. , Peng , D. , Wang , X. , Wan , H. , Zhang , P. , et al. . 2009 . Characterization of duck H5N1 influenza viruses with differing pathogenicity in mallard (Anas platyrhynchos) ducks . Avian Pathology , 38 , 457 467 .
   PubMed Web of Science ®Google Scholar
• Teifke , J.P. , Klopfleisch , R. , Globig , A. , Starick , E. , Hoffmann , B. , Wolf , P.U. , et al. . 2007 . Pathology of natural infections by H5N1 highly pathogenic avian influenza virus in mute (Cygnus olor) and whooper (Cygnus cygnus) swans . Veterinary Pathology , 44 , 137 143 .
   PubMed Web of Science ®Google Scholar
• Toffan , A. , Serena Beato , M. , De Nardi , R. , Bertoli E. , Salviato , A. , Cattoli , G. , et al. . 2008 . Conventional inactivated bivalent H5/H7 vaccine prevents viral localization in muscles of turkeys infected experimentally with low pathogenic avian influenza and highly pathogenic avian influenza H7N1 isolates . Avian Pathology , 37 , 407 412 .
   PubMed Web of Science ®Google Scholar
• Tweed , S.A. , Skowronski , D.M. , David , S.T. , Larder , A. , Petric , M. Lees , W. 2004 . Human illness from avian influenza H7N3, British Columbia . Emerging Infectious Diseases , 10 : 2196 – 2199 .
   PubMed Web of Science ®Google Scholar
• Van Riel , D. , van den Brand , J.M.A. , Munster , V.J. , Besteboer , T.M. , Fouchier , R.A.M. , Osterhaus , A.D.M.E. & Kuiken , T. 2009 . Pathology and virus distribution in chickens naturally infected with highly pathogenic avian influenza A virus (H7N7) during the 2003 outbreak in The Netherlands . Veterinary Pathology , 46 , 971 976 .
   PubMed Web of Science ®Google Scholar
• Vascellari , M. , Granato , A. , Trevisan , L. , Basilicata , L. , Toffan , A. , Milani , A. & Mutinelli , F. 2007 . Pathologic findings of highly pathogenic avian influenza virus A/Duck/Vietnam/12/05 (H5N1) in experimentally infected Pekin ducks, based on immunohistochemistry and in situ hybridization . Veterinary Pathology , 44 , 635 642 .
   PubMed Web of Science ®Google Scholar
• Verma , S. , Lo , Y. , Chapagain , M. , Lum , S. , Kumar , M. , Gurjav , U. , et al. . 2009 . West Nile virus infection modulates human brain microvascular endothelial cells tight junction proteins and cell adhesion molecules: transmigration across the in vitro blood–brain barrier . Virology , 382 , 425 433 .
   Google Scholar
• Yamamoto , Y. , Nakamura , K. , Kitagawa , K. , Ikenaga , N. , Yamada , M. , Mase , M. & Narita , M. 2007 . Severe nonpurulent encephalitis with mortality and feather lesions in call ducks (Anas platyrhyncha var. domestica) inoculated intravenously with H5N1 highly pathogenic avian influenza virus . Avian Diseases , 51 , 52 57 .
   PubMed Web of Science ®Google Scholar
• Zanella , A. 2003 . Avian influenza attributable to serovar H7N1 in light layers in Italy . Avian Diseases , 47 , 1177 1180 .
   PubMed Web of Science ®Google Scholar