Animal models for the preclinical evaluation of candidate influenza vaccines

Expert Review of Vaccines

Volumn 9, Issue 1, 2010, Pages 59-72

  Bodewes, Rogier ^a   Rimmelzwaan, Guus F ^a   Osterhaus, Albert D M E ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Animal models; Influenza; Pandemic; Preclinical evaluations; Vaccine

Indexed keywords

INFLUENZA VACCINE;

CLINICAL EVALUATION; CLINICAL FEATURE; DRUG EFFICACY; DRUG SAFETY; HUMAN; IMMUNE RESPONSE; INFLUENZA; INFLUENZA VACCINATION; NONHUMAN; PANDEMIC; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; VIRUS TRANSMISSION;

ANIMALS; DRUG EVALUATION, PRECLINICAL; FERRETS; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA VACCINES; INFLUENZA, HUMAN; MACACA; MICE; MODELS, ANIMAL; ORTHOMYXOVIRIDAE INFECTIONS;

EID: 74349124127     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/erv.09.148     Document Type: Review

References (137)

1. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol. Rev. 56(1), 152-179 (1992).
2. Reperant LA, Rimmelzwaan GF, Kuiken T. Avian influenza viruses in mammals. Rev. Sci. Tech. 28(1), 137-159 (2009).
3. Centers for Disease Control and Prevention (CDC). Update: infections with a swine-origin influenza A (H1N1) virus - United States and other countries, April 28, 2009. MMWR Morb. Mortal. Wkly Rep. 58(16), 431-433 (2009).
4. Garten RJ, Davis CT, Russell CA et al. Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 325(5937), 197-201 (2009).
5. Zhang H, Chen L. Possible origin of current influenza A H1N1 viruses. Lancet Infect. Dis. 9(8), 456-457 (2009).
6. de Jong JC, Claas EC, Osterhaus AD, Webster RG, Lim WL. A pandemic warning? Nature 389(6651), 554 (1997).
7. Subbarao K, Klimov A, Katz J et al. Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness. Science 279(5349), 393-396 (1998).
8. Yang Y, Halloran ME, Sugimoto JD, Longini IM Jr. Detecting human-tohuman transmission of avian influenza A (H5N1). Emerg. Infect. Dis. 13(9), 1348-1353 (2007).
9. Ungchusak K, Auewarakul P, Dowell SF et al. Probable person-to-person transmission of avian influenza A (H5N1). N. Engl. J. Med. 352(4), 333-340 (2005).
10. Lin YP, Shaw M, Gregory V et al. Avian-to-human transmission of H9N2 subtype influenza A viruses: relationship between H9N2 and H5N1 human isolates. Proc. Natl Acad. Sci. USA 97(17), 9654-9658 (2000).
11. Fouchier RA, Schneeberger PM, Rozendaal FW et al. Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome. Proc. Natl Acad. Sci. USA 101(5), 1356-1361 (2004).
12. Olsen B, Munster VJ, Wallensten A et al. Global patterns of influenza a virus in wild birds. Science 312(5772), 384-388 (2006).
13. Crawford PC, Dubovi EJ, Castleman WL et al. Transmission of equine influenza virus to dogs. Science 310(5747), 482-485 (2005).
14. Cardona CJ, Xing Z, Sandrock CE, Davis CE. Avian influenza in birds and mammals. Comp. Immunol. Microbiol. Infect. Dis. 32(4), 255-273 (2009).
15. Thiry E, Zicola A, Addie D et al. Highly pathogenic avian influenza H5N1 virus in cats and other carnivores. Vet. Microbiol. 122(1-2), 25-31 (2007).
16. Baigent SJ, McCauley JW. Influenza type A in humans, mammals and birds: determinants of virus virulence, host-range and interspecies transmission. Bioessays 25(7), 657-671 (2003).
17. Suzuki Y, Ito T, Suzuki T et al. Sialic acid species as a determinant of the host range of influenza A viruses. J. Virol. 74(24), 11825-11831 (2000).
18. van Riel D, Munster VJ, de Wit E et al. Human and avian influenza viruses target different cells in the lower respiratory tract of humans and other mammals. Am. J. Pathol. 171(4), 1215-1223 (2007).
19. van Riel D, Munster VJ, de Wit E et al. H5N1 virus attachment to lower respiratory tract. Science 312(5772), 399 (2006).
20. Baskin CR, Bielefeldt-Ohmann H, Tumpey TM et al. Early and sustained innate immune response defines pathology and death in nonhuman primates infected by highly pathogenic influenza virus. Proc. Natl Acad. Sci. USA 106(9), 3455-3460 (2009).
21. de Jong MD, Simmons CP, Thanh TT et al. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat. Med. 12(10), 1203-1207 (2006).
22. Seo SH, Hoffmann E, Webster RG. The NS1 gene of H5N1 influenza viruses circumvents the host anti-viral cytokine responses. Virus Res. 103(1-2), 107-113 (2004).
23. de Wit E, Kawaoka Y, de Jong MD, Fouchier RA. Pathogenicity of highly pathogenic avian influenza virus in mammals. Vaccine 26(Suppl. 4), D54-D58 (2008).
24. Seo SH, Hoffmann E, Webster RG. Lethal H5N1 influenza viruses escape host anti-viral cytokine responses. Nat. Med. 8(9), 950-954 (2002).
25. Gambotto A, Barratt-Boyes SM, de Jong MD, Neumann G, Kawaoka Y. Human infection with highly pathogenic H5N1 influenza virus. Lancet 371(9622), 1464-1475 (2008).
26. Korteweg C, Gu J. Pathology, molecular biology, and pathogenesis of avian influenza A (H5N1) infection in humans. Am. J. Pathol. 172(5), 1155-1170 (2008).
27. Staeheli P, Grob R, Meier E, Sutcliffe JG, Haller O. Influenza virus-susceptible mice carry Mx genes with a large deletion or a nonsense mutation. Mol. Cell. Biol. 8(10), 4518-4523 (1988).
28. Pavlovic J, Haller O, Staeheli P. Human and mouse Mx proteins inhibit different steps of the influenza virus multiplication cycle. J. Virol. 66(4), 2564-2569 (1992).
29. Narasaraju T, Sim MK, Ng HH et al. Adaptation of human influenza H3N2 virus in a mouse pneumonitis model: insights into viral virulence, tissue tropism and host pathogenesis. Microbes Infect. 11(1), 2-11 (2009).
30. Wu R, Zhang H, Yang K et al. Multiple amino acid substitutions are involved in the adaptation of H9N2 avian influenza virus to mice. Vet. Microbiol. 138(1-2), 85-91 (2009).
31. Subbarao K, Luke C. H5N1 viruses and vaccines. PLoS Pathog. 3(3), e40 (2007).
32. de Wit E, Munster VJ, Spronken MI et al. Protection of mice against lethal infection with highly pathogenic H7N7 influenza A virus by using a recombinant lowpathogenicity vaccine strain. J. Virol. 79(19), 12401-12407 (2005).
33. Lu X, Tumpey TM, Morken T et al. A mouse model for the evaluation of pathogenesis and immunity to influenza A (H5N1) viruses isolated from humans. J. Virol. 73(7), 5903-5911 (1999).
34. Maines TR, Jayaraman A, Belser JA et al. Transmission and pathogenesis of swine-origin 2009 A(H1N1) influenza viruses in ferrets and mice. Science 325(5939), 484-487 (2009).
35. Itoh Y, Shinya K, Kiso M et al. In vitro and in vivo characterization of new swine-origin H1N1 influenza viruses. Nature 460(7258), 1021-1025 (2009).
36. Boon AC, deBeauchamp J, Hollmann A et al. Host genetic variation affects resistance to infection with a highly pathogenic H5N1 influenza A virus in mice. J. Virol. 83(20), 10417-10426 (2009).
37. Trammell RA, Toth LA. Genetic susceptibility and resistance to influenza infection and disease in humans and mice. Expert Rev. Mol. Diagn. 8(4), 515-529 (2008).
38. Kreijtz JH, Suezer Y, van Amerongen G et al. Recombinant modified vaccinia virus Ankara-based vaccine induces protective immunity in mice against infection with influenza virus H5N1. J. Infect. Dis. 195(11), 1598-1606 (2007).
39. Gao P, Watanabe S, Ito T et al. Biological heterogeneity, including systemic replication in mice, of H5N1 influenza A virus isolates from humans in Hong Kong. J. Virol. 73(4), 3184-3189 (1999).
40. Toth LA, Verhulst SJ. Strain differences in sleep patterns of healthy and influenzainfected inbred mice. Behav. Genet. 33(3), 325-336 (2003).
41. Ding M, Lu L, Toth LA. Gene expression in lung and basal forebrain during influenza infection in mice. Genes Brain Behav. 7(2), 173-183 (2008).
42. Ottolini MG, Blanco JC, Eichelberger MC et al. The cotton rat provides a useful small-animal model for the study of influenza virus pathogenesis. J. Gen. Virol. 86(Pt 10), 2823-2830 (2005).
43. Boukhvalova MS, Prince GA, Blanco JC. The cotton rat model of respiratory viral infections. Biologicals 37(3), 152-159 (2009).
44. Azoulay-Dupuis E, Lambre CR, Soler P, Moreau J, Thibon M. Lung alterations in guinea-pigs infected with influenza virus. J. Comp. Pathol. 94(2), 273-283 (1984).
45. Phair JP, Kauffman CA, Jennings R, Potter CW. Influenza virus infection of the guinea pig: immune response and resistance. Med. Microbiol. Immunol. 165(4), 241-254 (1979).
46. Wetherbee RE. Induction of systemic delayed hypersensitivity during experimental viral infection of the respiratory tract with a myxovirus or paramyxovirus. J. Immunol. 111(1), 157-163 (1973).
47. 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. USA 103(26), 9988-9992 (2006).
48. Van Hoeven N, Belser JA, Szretter KJ et al. Pathogenesis of 1918 pandemic and H5N1 influenza virus infections in a guinea pig model: antiviral potential of exogenous a interferon to reduce virus shedding. J. Virol. 83(7), 2851-2861 (2009).
49. Kwon YK, Lipatov AS, Swayne DE. Bronchointerstitial pneumonia in guinea pigs following inoculation with H5N1 high pathogenicity avian influenza virus. Vet. Pathol. 46(1), 138-141 (2009).
50. Steel J, Lowen AC, Mubareka S, Palese P. Transmission of influenza virus in a mammalian host is increased by PB2 amino acids 627K or 627E/701N. PLoS Pathog. 5(1), e1000252 (2009).
51. Tang X, Chong KT. Histopathology and growth kinetics of influenza viruses (H1N1 and H3N2) in the upper and lower airways of guinea pigs. J. Gen. Virol. 90(Pt 2), 386-391 (2009).
52. Lange E, Kalthoff D, Blohm U et al. Pathogenesis and transmission of the novel swine-origin influenza virus A/H1N1 after experimental infection of pigs. J. Gen. Virol. 90(Pt 9), 2119-2123 (2009).
53. Van Reeth K. Avian and swine influenza viruses: our current understanding of the zoonotic risk. Vet. Res. 38(2), 243-260 (2007).
54. Lipatov AS, Kwon YK, Sarmento LV et al. Domestic pigs have low susceptibility to H5N1 highly pathogenic avian influenza viruses. PLoS Pathog. 4(7), e1000102 (2008).
55. Kuiken T, Rimmelzwaan G, van Riel D et al. Avian H5N1 influenza in cats. Science 306(5694), 241 (2004).
56. Rimmelzwaan GF, van Riel D, Baars M et al. 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(1), 176-183 (2006).
57. Leschnik M, Weikel J, Mostl K et al. Subclinical infection with avian influenza A (H5N1) virus in cats. Emerg. Infect. Dis. 13(2), 243-247 (2007).
58. Smith W, Andrewes CH, Laidlaw PP. A virus obtained from influenza patients. Lancet ii, 66-68 (1933).
59. Reuman PD, Keely S, Schiff GM. Assessment of signs of influenza illness in the ferret model. J. Virol. Methods 24(1-2), 27-34 (1989).
60. Munster VJ, de Wit E, van den Brand JM et al. Pathogenesis and transmission of swine-origin 2009 A (H1N1) influenza virus in ferrets. Science 325(5939), 481-483 (2009).
61. Andrewes CH, Glover RE. Spread of infection from the respiratory tract of the ferret. Transmission of influenza A virus. Br. J. Exp. Pathol. 16, 291-302 (1941).
62. Herlocher ML, Elias S, Truscon R et al. Ferrets as a transmission model for influenza: sequence changes in HA1 of type A (H3N2) virus. J. Infect. Dis. 184(5), 542-546 (2001).
63. Maines TR, Chen LM, Matsuoka Y et al. Lack of transmission of H5N1 avianhuman reassortant influenza viruses in a ferret model. Proc. Natl Acad. Sci. USA 103(32), 12121-12126 (2006).
64. Govorkova EA, Rehg JE, Krauss S et al. Lethality to ferrets of H5N1 influenza viruses isolated from humans and poultry in 2004. J. Virol. 79(4), 2191-2198 (2005).
65. Zitzow LA, Rowe T, Morken T et al. Pathogenesis of avian influenza A (H5N1) viruses in ferrets. J. Virol. 76(9), 4420-4429 (2002).
66. 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(9), 1315-1323 (2008).
67. Baras B, Stittelaar KJ, Simon JH et al. Cross-protection against lethal H5N1 challenge in ferrets with an adjuvanted pandemic influenza vaccine. PLoS ONE 3(1), e1401 (2008).
68. Mahmood K, Bright RA, Mytle N et al. H5N1 VLP vaccine induced protection in ferrets against lethal challenge with highly pathogenic H5N1 influenza viruses. Vaccine 26(42), 5393-5399 (2008).
69. Peltola VT, Boyd KL, McAuley JL, Rehg JE, McCullers JA. Bacterial sinusitis and otitis media following influenza virus infection in ferrets. Infect. Immun. 74(5), 2562-2567 (2006).
70. Rimmelzwaan GF, Baars M, van Beek R et al. Induction of protective immunity against influenza virus in a macaque model: comparison of conventional and iscom vaccines. J. Gen. Virol. 78 ( Pt 4), 757-765 (1997).
71. Baas T, Baskin CR, Diamond DL et al. Integrated molecular signature of disease: analysis of influenza virus-infected macaques through functional genomics and proteomics. J. Virol. 80(21), 10813-10828 (2006).
72. Villinger F, Miller R, Mori K et al. IL-15 is superior to IL-2 in the generation of long-lived antigen specific memory CD4 and CD8 T cells in rhesus macaques. Vaccine 22(25-26), 3510-3521 (2004).
73. Baskin CR, Garcia-Sastre A, Tumpey TM et al. Integration of clinical data, pathology, and cDNA microarrays in influenza virus-infected pigtailed macaques (Macaca nemestrina). J. Virol. 78(19), 10420-10432 (2004).
74. Rimmelzwaan GF, Kuiken T, van Amerongen G et al. Pathogenesis of influenza A (H5N1) virus infection in a primate model. J. Virol. 75(14), 6687-6691 (2001).
75. 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(3), 304-310 (2003)
76. Kobasa D, Jones SM, Shinya K et al. Aberrant innate immune response in lethal infection of macaques with the 1918 influenza virus. Nature 445(7125), 319-323 (2007).
77. Berendt RF. Simian model for the evaluation of immunity to influenza. Infect. Immun. 9(1), 101-105 (1974).
78. Kreijtz JH, Suezer Y, de Mutsert G et al. 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(3), 405-413 (2009).
79. Itoh Y, Ozaki H, Tsuchiya H et al. A vaccine prepared from a non-pathogenic H5N1 avian influenza virus strain confers protective immunity against highly pathogenic avian influenza virus infection in cynomolgus macaques. Vaccine 26(4), 562-572 (2008).
80. Lowen AC, Steel J, Mubareka S et al. Blocking interhost transmission of influenza virus by vaccination in the guinea pig model. J. Virol. 83(7), 2803-2818 (2009).
81. Lowen AC, Palese P. Influenza virus transmission: basic science and implications for the use of antiviral drugs during a pandemic. Infect. Disord. Drug Targets 7(4), 318-328 (2007).
82. Suguitan AL Jr, McAuliffe J, Mills KL et al. Live, attenuated influenza A H5N1 candidate vaccines provide broad crossprotection in mice and ferrets. PLoS Med. 3(9), e360 (2006).
83. Jegerlehner A, Schmitz N, Storni T, Bachmann MF. Influenza A vaccine based on the extracellular domain of M2: weak protection mediated via antibodydependent NK cell activity. J. Immunol. 172(9), 5598-5605 (2004).
84. Geeraedts F, Goutagny N, Hornung V et al. Superior immunogenicity of inactivated whole virus H5N1 influenza vaccine is primarily controlled by Toll-like receptor signalling. PLoS Pathog. 4(8), e1000138 (2008).
85. Dupuis M, Denis-Mize K, LaBarbara A et al. Immunization with the adjuvant MF59 induces macrophage trafficking and apoptosis. Eur. J. Immunol. 31(10), 2910-2918 (2001).
86. +/H2 class I-deficient mice. Vaccine 23(45), 5231-5244 (2005).
87. + T-cell responses in humanized mice vaccinated with influenza virus vaccines. Blood 112(9), 3671-3678 (2008).
88. Cameron CM, Cameron MJ, Bermejo-Martin JF et al. Gene expression analysis of host innate immune responses during lethal H5N1 infection in ferrets. J. Virol. 82(22), 11308-11317 (2008).
89. Ochi A, Danesh A, Seneviratne C et al. Cloning, expression and immunoassay detection of ferret IFN-g. Dev. Comp. Immunol. 32(8), 890-897 (2008).
90. Nakata M, Itou T, Sakai T. Molecular cloning and phylogenetic analysis of inflammatory cytokines of the ferret (Mustela putorius furo). J. Vet. Med. Sci. 70(6), 543-550 (2008).
91. Svitek N, Rudd PA, Obojes K, Pillet S, von Messling V. Severe seasonal influenza in ferrets correlates with reduced interferon and increased IL-6 induction. Virology 376(1), 53-59 (2008).
92. Ljungberg K, Kolmskog C, Wahren B et al. DNA vaccination of ferrets with chimeric influenza A virus hemagglutinin (H3) genes. Vaccine 20(16), 2045-2052 (2002).
93. Leroux-Roels I, Borkowski A, Vanwolleghem T et al. Antigen sparing and cross-reactive immunity with an adjuvanted rH5N1 prototype pandemic influenza vaccine: a randomised controlled trial. Lancet 370(9587), 580-589 (2007).
94. Middleton D, Rockman S, Pearse M et al. Evaluation of vaccines for H5N1 influenza virus in ferrets reveals the potential for protective single-shot immunization. J. Virol. 83(15), 7770-7778 (2009).
95. Govorkova EA, Webby RJ, Humberd J, Seiler JP, Webster RG. Immunization with reverse-genetics-produced H5N1 influenza vaccine protects ferrets against homologous and heterologous challenge. J. Infect. Dis. 194(2), 159-167 (2006).
96. Lipatov AS, Hoffmann E, alomon R, Yen HL, Webster RG. Cross-protectiveness and immunogenicity of influenza A/Duck/Singapore/3/97(H5) vaccines against infection with A/Vietnam/1203/04(H5N1) virus in ferrets. J. Infect. Dis. 194(8), 1040-1043 (2006).
97. Lalor PA, Webby RJ, Morrow J et al. Plasmid DNA-based vaccines protect mice and ferrets against lethal challenge with A/Vietnam/1203/04 (H5N1) influenza virus. J. Infect. Dis. 197(12), 1643-1652 (2008).
98. Li S, Liu C, Klimov A et al. Recombinant influenza A virus vaccines for the pathogenic human A/Hong Kong/97 (H5N1) viruses. J. Infect. Dis. 179(5), 1132-1138 (1999).
99. Bell FR, Dudgeon JA. An epizootic in influenza in a ferret colony. J. Comp. Pathol. Ther. 58(3), 167-171 (1948).
100. Stittelaar KJ, de Swart RL, Osterhaus AD. Vaccination against measles: a neverending story. Expert Rev. Vaccines 1(2), 151-159 (2002).
101. Ruat C, Caillet C, Bidaut A, Simon J, Osterhaus AD. Vaccination of macaques with adjuvanted formalin-inactivated influenza A virus (H5N1) vaccines: protection against H5N1 challenge without disease enhancement. J. Virol. 82(5), 2565-2569 (2008).
102. Fan S, Gao Y, Shinya K et al. Immunogenicity and protective efficacy of a live attenuated H5N1 vaccine in nonhuman primates. PLoS Pathog. 5(5), e1000409 (2009).
103. DiNapoli JM, Yang L, Suguitan A Jr. et al. Immunization of primates with a Newcastle disease virus-vectored vaccine via the respiratory tract induces a high titer of serum neutralizing antibodies against highly pathogenic avian influenza virus. J. Virol. 81(21), 11560-11568 (2007).
104. Rimmelzwaan GF, Baars M, van Beek R et al. Influenza virus subtype crossreactivities of haemagglutination inhibiting and virus neutralising serum antibodies induced by infection or vaccination with an ISCOM-based vaccine. Vaccine 17(20-21), 2512-2516 (1999).
105. Rimmelzwaan GF, Baars M, van Amerongen G, van Beek R, Osterhaus AD. A single dose of an ISCOM influenza vaccine induces long-lasting protective immunity against homologous challenge infection but fails to protect cynomolgus macaques against distant drift variants of influenza A (H3N2) viruses. Vaccine 20(1-2), 158-163 (2001).
106. Van Reeth K, Labarque G, De Clercq S, Pensaert M. Efficacy of vaccination of pigs with different H1N1 swine influenza viruses using a recent challenge strain and different parameters of protection. Vaccine 19(31), 4479-4486 (2001).
107. Van Reeth K, Van Gucht S, Pensaert M. Correlations between lung proinflammatory cytokine levels, virus replication, and disease after swine influenza virus challenge of vaccinationimmune pigs. Viral Immunol. 15(4), 583-594 (2002).
108. Richt JA, Lekcharoensuk P, Lager KM et al. Vaccination of pigs against swine influenza viruses by using an NS1- truncated modified live-virus vaccine. J. Virol. 80(22), 11009-11018 (2006).
109. Wesley RD, Tang M, Lager KM. Protection of weaned pigs by vaccination with human adenovirus 5 recombinant viruses expressing the hemagglutinin and the nucleoprotein of H3N2 swine influenza virus. Vaccine 22(25-26), 3427-3434 (2004).
110. Heinen PP, Rijsewijk FA, de Boer-Luijtze EA, Bianchi AT. Vaccination of pigs with a DNA construct expressing an influenza virus M2-nucleoprotein fusion protein exacerbates disease after challenge with influenza A virus. J. Gen. Virol. 83(Pt 8), 1851-1859 (2002).
111. Swayne DE, Suarez DL. Current developments in avian influenza vaccines, including safety of vaccinated birds as food. Dev. Biol. (Basel) 130, 123-133 (2007).
112. Swayne DE. Avian influenza vaccines and therapies for poultry. Comp. Immunol. Microbiol. Infect. Dis. 32(4), 351-363 (2009).
113. Paillot R, Hannant D, Kydd JH, Daly JM. Vaccination against equine influenza: quid novi? Vaccine 24(19), 4047-4061 (2006).
114. Ulmer JB, Donnelly JJ, Parker SE et al. Heterologous protection against influenza by injection of DNA encoding a viral protein. Science 259(5102), 1745-1749 (1993).
115. Fynan EF, Webster RG, Fuller DH et al. DNA vaccines: protective immunizations by parenteral, mucosal, and gene-gun inoculations. Proc. Natl Acad. Sci. USA 90(24), 11478-11482 (1993).
116. Lu S, Wang S, Grimes-Serrano JM. Current progress of DNA vaccine studies in humans. Expert Rev. Vaccines 7(2), 175-191 (2008).
117. Drape RJ, Macklin MD, Barr LJ et al. Epidermal DNA vaccine for influenza is immunogenic in humans. Vaccine 24(21), 4475-4481 (2006).
118. Fiers W, De Filette M, El Bakkouri K et al. M2e-based universal influenza A vaccine. Vaccine 27(45), 6280-6283 (2009).
119. O'Hagan DT. MF59 is a safe and potent vaccine adjuvant that enhances protection against influenza virus infection. Expert Rev. Vaccines 6(5), 699-710 (2007).
120. Stephenson I, Nicholson KG, Hoschler K et al. Antigenically distinct MF59- adjuvanted vaccine to boost immunity to H5N1. N. Engl. J. Med. 359(15), 1631-1633 (2008).
121. O'Hagan DT, Wack A, Podda A. MF59 is a safe and potent vaccine adjuvant for flu vaccines in humans: what did we learn during its development? Clin. Pharmacol. Ther. 82(6), 740-744 (2007).
122. Hoelscher MA, Singh N, Garg S et al. A broadly protective vaccine against globally dispersed clade 1 and clade 2 H5N1 influenza viruses. J. Infect. Dis. 197(8), 1185-1188 (2008).
123. Van Kampen KR, Shi Z, Gao P et al. Safety and immunogenicity of adenovirusvectored nasal and epicutaneous influenza vaccines in humans. Vaccine 23(8), 1029-1036 (2005).
124. Gao W, Soloff AC, Lu X et al. Protection of mice and poultry from lethal H5N1 avian influenza virus through adenovirus-based immunization. J. Virol. 80(4), 1959-1964 (2006).
125. Rowe T, Abernathy RA, Hu-Primmer J et al. Detection of antibody to avian influenza A (H5N1) virus in human serum by using a combination of serologic assays. J. Clin. Microbiol. 37(4), 937-943 (1999).
126. Cassetti MC, Katz JM, Wood J. Report of a consultation on role of immunological assays to evaluate efficacy of influenza vaccines. Initiative for Vaccine Research and Global Influenza Programme, World Health Organization, Geneva, Switzerland, 25 January 2005. Vaccine 24(5), 541-543 (2006).
127. Cassetti MC, Couch R, Wood J, Pervikov Y. Report of meeting on the development of influenza vaccines with broad spectrum and long-lasting immune responses, World Health Organization, Geneva, Switzerland, 26-27 February 2004. Vaccine 23(13), 1529-1533 (2005).
128. Altman JD, Moss PA, Goulder PJ et al. Phenotypic analysis of antigen-specific T lymphocytes. Science 274(5284), 94-96 (1996).
129. + T-cell response is much less apparent following secondary challenge. J. Virol. 74(8), 3486-3493 (2000).
130. Fornek JL, Korth MJ, Katze MG. Use of functional genomics to understand influenza-host interactions. Adv. Virus Res. 70, 81-100 (2007).
131. 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(3 Suppl.), 956-967 (2003).
132. Maas R, Tacken M, Ruuls L et al. Avian influenza (H5N1) susceptibility and receptors in dogs. Emerg. Infect. Dis. 13(8), 1219-1221 (2007).
133. Choi YK, Nguyen TD, Ozaki H et al. Studies of H5N1 influenza virus infection of pigs by using viruses isolated in Vietnam and Thailand in 2004. J. Virol. 79(16), 10821-10825 (2005).
134. Isoda N, Sakoda Y, Kishida N et al. Pathogenicity of a highly pathogenic avian influenza virus, A/chicken/Yamaguchi/7/04 (H5N1) in different species of birds and mammals. Arch. Virol. 151(7), 1267-1279 (2006).
135. Reperant LA, van Amerongen G, van de Bildt MW et al. Highly pathogenic avian influenza virus (H5N1) infection in red foxes fed infected bird carcasses. Emerg. Infect. Dis. 14(12), 1835-1841 (2008).
136. Kalthoff D, Hoffmann B, Harder T, Durban M, Beer M. Experimental infection of cattle with highly pathogenic avian influenza virus (H5N1). Emerg. Infect. Dis. 14(7), 1132-1134 (2008). (Pubitemid 351920449)
137. Smith H, Sweet C. Lessons for human influenza from pathogenicity studies with ferrets. Rev. Infect. Dis. 10(1), 56-75 (1988).