Pathogenesis of influenza A/H5N1 virus infection in ferrets differs between intranasal and intratracheal routes of inoculation

American Journal of Pathology

Volumn 179, Issue 1, 2011, Pages 30-36

  Bodewes, Rogier ^a   Kreijtz, Joost H C M ^a   Van Amerongen, Geert ^a   Fouchier, Ron A M ^a   Osterhaus, Albert D M E ^a,b   Rimmelzwaan, Guus F ^a,b   Kuiken, Thijs ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b ViroClinics Biosciences BV   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRONCHOPNEUMONIA; CHOROIDITIS; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; FERRET; INFLUENZA A (H5N1); INFLUENZA VIRUS A H5N1; MENINGOENCEPHALITIS; NONHUMAN; PRIORITY JOURNAL; VIRUS PATHOGENESIS; VIRUS TRANSMISSION;

ADMINISTRATION, INTRANASAL; ANIMALS; BRAIN; BRAIN DISEASES; DISEASE MODELS, ANIMAL; DOGS; FEMALE; FERRETS; IMMUNOENZYME TECHNIQUES; INFLUENZA A VIRUS, H5N1 SUBTYPE; INTUBATION, INTRATRACHEAL; KIDNEY; LUNG DISEASES; ORTHOMYXOVIRIDAE INFECTIONS; VIRUS REPLICATION;

EID: 80051771826     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.03.026     Document Type: Article

References (54)

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24. A.S. Lipatov, Y.K. Kwon, M.J. Pantin-Jackwood, and D.E. Swayne Pathogenesis of H5N1 influenza virus infections in mice and ferret models differs according to respiratory tract or digestive system exposure J Infect Dis 199 2009 717 725
25. C.H. Park, M. Ishinaka, A. Takada, H. Kida, T. Kimura, K. Ochiai, and T. Umemura 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 2002 1425 1436
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27. M. Johnston, A. Zakharov, C. Papaiconomou, G. Salmasi, and D. Armstrong Evidence of connections between cerebrospinal fluid and nasal lymphatic vessels in humans, non-human primates and other mammalian species Cerebrospinal Fluid Res 1 2004 2
28. A.N. Abdel-Ghafar, T. Chotpitayasunondh, Z. Gao, F.G. Hayden, D.H. Nguyen, M.D. de Jong, A. Naghdaliyev, J.S. Peiris, N. Shindo, S. Soeroso, T.M. Uyeki Writing Committee of the Second World Health Organization Consultation on Clinical Aspects of Human Infection with Avian Influenza A Virus Update on avian influenza A (H5N1) virus infection in humans N Engl J Med 358 2008 261 273
29. A. Gambotto, S.M. Barratt-Boyes, M.D. de Jong, G. Neumann, and Y. Kawaoka Human infection with highly pathogenic H5N1 influenza virus Lancet 371 2008 1464 1475 (Pubitemid 351618340)
30. H. Tanaka, C.H. Park, A. Ninomiya, H. Ozaki, A. Takada, T. Umemura, and H. Kida Neurotropism of the 1997 Hong Kong H5N1 influenza virus in mice Vet Microbiol 95 2003 1 13 (Pubitemid 36829314)
31. X. Lu, T.M. Tumpey, T. Morken, S.R. Zaki, N.J. Cox, and J.M. Katz A mouse model for the evaluation of pathogenesis and immunity to influenza A (H5N1) viruses isolated from humans J Virol 73 1999 5903 5911 (Pubitemid 29274877)
32. G.F. Rimmelzwaan, D. van Riel, M. Baars, T.M. Bestebroer, G. van Amerongen, R.A. Fouchier, A.D. Osterhaus, and T. Kuiken 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 2006 176 183 quiz 364 (Pubitemid 43062571)
33. 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, C. Buranathai, W. Lim, R.G. Webster, and E. Hoffmann Lethality to ferrets of H5N1 influenza viruses isolated from humans and poultry in 2004 [Erratum appeared in J Virol 2006, 80:6195] J Virol 79 2005 2191 2198 (Pubitemid 40204576)
34. L.A. Zitzow, T. Rowe, T. Morken, W.J. Shieh, S. Zaki, and J.M. Katz Pathogenesis of avian influenza A (H5N1) viruses in ferrets J Virol 76 2002 4420 4429 (Pubitemid 34309579)
35. R. Gao, L. Dong, J. Dong, L. Wen, Y. Zhang, H. Yu, Z. Feng, M. Chen, Y. Tan, Z. Mo, H. Liu, Y. Fan, K. Li, C.K. Li, D. Li, W. Yang, and Y. Shu A systematic molecular pathology study of a laboratory confirmed H5N1 human case PLoS One 5 2010 e13315
36. M.D. de Jong, V.C. Bach, T.Q. Phan, M.H. Vo, T.T. Tran, B.H. Nguyen, M. Beld, T.P. Le, H.K. Truong, V.V. Nguyen, T.H. Tran, Q.H. Do, and J. Farrar Fatal avian influenza A (H5N1) in a child presenting with diarrhea followed by coma N Engl J Med 352 2005 686 691 (Pubitemid 40239216)
37. G.F. Rimmelzwaan, T. Kuiken, G. van Amerongen, T.M. Bestebroer, R.A. Fouchier, and A.D. Osterhaus Pathogenesis of influenza A (H5N1) virus infection in a primate model J Virol 75 2001 6687 6691 (Pubitemid 32578188)
38. R. Bodewes, G.F. Rimmelzwaan, and A.D. Osterhaus Animal models for the preclinical evaluation of candidate influenza vaccines Expert Rev Vaccines 9 2010 59 72
39. T. Kuiken, J. van den Brand, D. van Riel, M. Pantin-Jackwood, and D.E. Swayne Comparative pathology of select agent influenza a virus infections Vet Pathol 47 2010 893 914
40. J.W. van der Laan, C. Herberts, R. Lambkin-Williams, A. Boyers, A.J. Mann, and J. Oxford Animal models in influenza vaccine testing Expert Rev Vaccines 7 2008 783 793
41. D. van Riel, V.J. Munster, E. de Wit, G.F. Rimmelzwaan, R.A. Fouchier, A.D. Osterhaus, and T. Kuiken Human and avian influenza viruses target different cells in the lower respiratory tract of humans and other mammals Am J Pathol 171 2007 1215 1223 (Pubitemid 47582895)
42. H. Imai, K. Shinya, R. Takano, M. Kiso, Y. Muramoto, S. Sakabe, S. Murakami, M. Ito, S. Yamada, M.T. Le, C.A. Nidom, Y. Sakai-Tagawa, K. Takahashi, Y. Omori, T. Noda, M. Shimojima, S. Kakugawa, H. Goto, K. Iwatsuki-Horimoto, T. Horimoto, and Y. Kawaoka The HA and NS genes of human H5N1 influenza A virus contribute to high virulence in ferrets PLoS Pathog 6 2010 e1001106
43. R. Bodewes, J.H. Kreijtz, G. van Amerongen, M.M. Geelhoed-Mieras, R.J. Verburgh, J.G. Heldens, J. Bedwell, J.M. van den Brand, T. Kuiken, C.A. van Baalen, R.A. Fouchier, A.D. Osterhaus, and G.F. Rimmelzwaan A single immunization with CoVaccine HT-adjuvanted H5N1 influenza virus vaccine induces protective cellular and humoral immune responses in ferrets J Virol 84 2010 7943 7952
44. G.F. Rimmelzwaan, M. Baars, E.C. Claas, and A.D. Osterhaus Comparison of RNA hybridization, hemagglutination assay, titration of infectious virus and immunofluorescence as methods for monitoring influenza virus replication in vitro J Virol Methods 74 1998 57 66 (Pubitemid 28386804)
45. G. Karber Contribution to collective treatment of pharmacological experiments Naunyn Schmiedebergs Arch Exp Pathol Pharmakol 162 1931 480 483
46. J.M. van den Brand, K.J. Stittelaar, G. van Amerongen, G.F. Rimmelzwaan, J. Simon, E. de Wit, V. Munster, T. Bestebroer, R.A. Fouchier, T. Kuiken, and A.D. Osterhaus 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 2010 993 999
47. B.L. Haagmans, T. Kuiken, B.E. Martina, R.A. Fouchier, G.F. Rimmelzwaan, G. van Amerongen, D. van Riel, T. de Jong, S. Itamura, K.H. Chan, M. Tashiro, and A.D. Osterhaus Pegylated interferon-alpha protects type 1 pneumocytes against SARS coronavirus infection in macaques Nat Med 10 2004 290 293 (Pubitemid 38667620)
48. E.A. Govorkova, N.A. Ilyushina, D.A. Boltz, A. Douglas, N. Yilmaz, and R.G. Webster Efficacy of oseltamivir therapy in ferrets inoculated with different clades of H5N1 influenza virus Antimicrob Agents Chemother 51 2007 1414 1424 (Pubitemid 46586824)
49. D.A. Boltz, J.E. Rehg, J. McClaren, R.G. Webster, and E.A. Govorkova Oseltamivir prophylactic regimens prevent H5N1 influenza morbidity and mortality in a ferret model J Infect Dis 197 2008 1315 1323 (Pubitemid 351632763)
50. T.R. Maines, X.H. Lu, S.M. Erb, L. Edwards, J. Guarner, P.W. Greer, D.C. Nguyen, K.J. Szretter, L.M. Chen, P. Thawatsupha, M. Chittaganpitch, S. Waicharoen, D.T. Nguyen, T. Nguyen, H.H. Nguyen, J.H. Kim, L.T. Hoang, C. Kang, L.S. Phuong, W. Lim, S. Zaki, R.O. Donis, N.J. Cox, J.M. Katz, and T.M. Tumpey Avian influenza (H5N1) viruses isolated from humans in Asia in 2004 exhibit increased virulence in mammals J Virol 79 2005 11788 11800 (Pubitemid 41279297)
51. A.S. Lipatov, Y.K. Kwon, M.J. Pantin-Jackwood, and D.E. Swayne Pathogenesis of H5N1 influenza virus infections in mice and ferret models differs according to respiratory tract or digestive system exposure J Infect Dis 199 2009 717 725
52. C.H. Park, M. Ishinaka, A. Takada, H. Kida, T. Kimura, K. Ochiai, and T. Umemura 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 2002 1425 1436 (Pubitemid 34749774)
53. P.A. Rudd, R. Cattaneo, and V. von Messling Canine distemper virus uses both the anterograde and the hematogenous pathway for neuroinvasion [Erratum appeared in J Virol 2006, 80:11416] J Virol 80 2006 9361 9370 (Pubitemid 44435615)
54. M. Johnston, A. Zakharov, C. Papaiconomou, G. Salmasi, and D. Armstrong Evidence of connections between cerebrospinal fluid and nasal lymphatic vessels in humans, non-human primates and other mammalian species Cerebrospinal Fluid Res 1 2004 2