Intranasal vaccination with an inactivated whole influenza virus vaccine induces strong antibody responses in serum and nasal mucus of healthy adults

References

• Murphy BR, Webster RG. Orthomyxoviruses. In: Fields BN, Knipe DM, M. HP, Chanock RM, Melnick JL, Monath TP, et al., eds. Fields Virology. Philadelphia: Lippincott Williams & Wilkins, 1996:1397-445.
   Google Scholar
• Murphy BR, Clements ML. The systemic and mucosal immune response of humans to influenza A virus. Curr Top Microbiol Immunol 1989; 146:107 - 16; http://dx.doi.org/10.1007/978-3-642-74529-4_12; PMID: 2659262
   PubMed Web of Science ®Google Scholar
• Murphy BR. Mucosal Immunity to Viruses. In: Ogra PL, Mestecky J, Lamm ME, Strober W, McGee JR, Bienenstock J, eds. Handbook of Mucosal Immunology. San Diego: Academic Press, 1994:333-43.
   Google Scholar
• Tamura S, Funato H, Hirabayashi Y, Kikuta K, Suzuki Y, Nagamine T, et al. Functional role of respiratory tract haemagglutinin-specific IgA antibodies in protection against influenza. Vaccine 1990; 8:479 - 85; http://dx.doi.org/10.1016/0264-410X(90)90250-P; PMID: 2251874
   PubMed Web of Science ®Google Scholar
• Tamura S, Funato H, Hirabayashi Y, Suzuki Y, Nagamine T, Aizawa C, et al. Cross-protection against influenza A virus infection by passively transferred respiratory tract IgA antibodies to different hemagglutinin molecules. Eur J Immunol 1991; 21:1337 - 44; http://dx.doi.org/10.1002/eji.1830210602; PMID: 1646112
   PubMed Web of Science ®Google Scholar
• Asahi Y, Yoshikawa T, Watanabe I, Iwasaki T, Hasegawa H, Sato Y, et al. Protection against influenza virus infection in polymeric Ig receptor knockout mice immunized intranasally with adjuvant-combined vaccines. J Immunol 2002; 168:2930 - 8; PMID: 11884464
   PubMed Web of Science ®Google Scholar
• Asahi-Ozaki Y, Yoshikawa T, Iwakura Y, Suzuki Y, Tamura S, Kurata T, et al. Secretory IgA antibodies provide cross-protection against infection with different strains of influenza B virus. J Med Virol 2004; 74:328 - 35; http://dx.doi.org/10.1002/jmv.20173; PMID: 15332283
   PubMed Web of Science ®Google Scholar
• Ito R, Ozaki YA, Yoshikawa T, Hasegawa H, Sato Y, Suzuki Y, et al. Roles of anti-hemagglutinin IgA and IgG antibodies in different sites of the respiratory tract of vaccinated mice in preventing lethal influenza pneumonia. Vaccine 2003; 21:2362 - 71; http://dx.doi.org/10.1016/S0264-410X(03)00078-1; PMID: 12744867
   PubMed Web of Science ®Google Scholar
• Renegar KB, Small PA Jr., Boykins LG, Wright PF. Role of IgA versus IgG in the control of influenza viral infection in the murine respiratory tract. J Immunol 2004; 173:1978 - 86; PMID: 15265932
   PubMed Web of Science ®Google Scholar
• Tamura S, Kurata T. Defense mechanisms against influenza virus infection in the respiratory tract mucosa. Jpn J Infect Dis 2004; 57:236 - 47; PMID: 15623947
   PubMed Web of Science ®Google Scholar
• Jodar L, Duclos P, Milstien JB, Griffiths E, Aguado MT, Clements CJ. Ensuring vaccine safety in immunization programmes--a WHO perspective. Vaccine 2001; 19:1594 - 605; http://dx.doi.org/10.1016/S0264-410X(00)00358-3; PMID: 11166881
   PubMed Web of Science ®Google Scholar
• Kuno-Sakai H, Kimura M, Ohta K, Shimojima R, Oh Y, Fukumi H. Developments in mucosal influenza virus vaccines. Vaccine 1994; 12:1303 - 10; http://dx.doi.org/10.1016/S0264-410X(94)80056-6; PMID: 7856295
   PubMed Web of Science ®Google Scholar
• Hashigucci K, Ogawa H, Ishidate T, Yamashita R, Kamiya H, Watanabe K, et al. Antibody responses in volunteers induced by nasal influenza vaccine combined with Escherichia coli heat-labile enterotoxin B subunit containing a trace amount of the holotoxin. Vaccine 1996; 14:113 - 9; http://dx.doi.org/10.1016/0264-410X(95)00174-Y; PMID: 8852406
   PubMed Web of Science ®Google Scholar
• Muszkat M, Yehuda AB, Schein MH, Friedlander Y, Naveh P, Greenbaum E, et al. Local and systemic immune response in community-dwelling elderly after intranasal or intramuscular immunization with inactivated influenza vaccine. J Med Virol 2000; 61:100 - 6; http://dx.doi.org/10.1002/(SICI)1096-9071(200005)61:1<100::AID-JMV16>3.0.CO;2-5; PMID: 10745240
   PubMed Web of Science ®Google Scholar
• Greenbaum E, Furst A, Kiderman A, Stewart B, Levy R, Schlesinger M, et al. Mucosal [SIgA] and serum [IgG] immunologic responses in the community after a single intra-nasal immunization with a new inactivated trivalent influenza vaccine. Vaccine 2002; 20:1232 - 9; http://dx.doi.org/10.1016/S0264-410X(01)00396-6; PMID: 11803086
   PubMed Web of Science ®Google Scholar
• Greenbaum E, Engelhard D, Levy R, Schlezinger M, Morag A, Zakay-Rones Z. Mucosal (SIgA) and serum (IgG) immunologic responses in young adults following intranasal administration of one or two doses of inactivated, trivalent anti-influenza vaccine. Vaccine 2004; 22:2566 - 77; http://dx.doi.org/10.1016/j.vaccine.2003.12.018; PMID: 15193382
   PubMed Web of Science ®Google Scholar
• Durrer P, Glück U, Spyr C, Lang AB, Zurbriggen R, Herzog C, et al. Mucosal antibody response induced with a nasal virosome-based influenza vaccine. Vaccine 2003; 21:4328 - 34; http://dx.doi.org/10.1016/S0264-410X(03)00457-2; PMID: 14505915
   PubMed Web of Science ®Google Scholar
• Treanor J, Nolan C, O’Brien D, Burt D, Lowell G, Linden J, et al. Intranasal administration of a proteosome-influenza vaccine is well-tolerated and induces serum and nasal secretion influenza antibodies in healthy human subjects. Vaccine 2006; 24:254 - 62; http://dx.doi.org/10.1016/j.vaccine.2005.07.088; PMID: 16129526
   PubMed Web of Science ®Google Scholar
• Atmar RL, Keitel WA, Cate TR, Munoz FM, Ruben F, Couch RB. A dose-response evaluation of inactivated influenza vaccine given intranasally and intramuscularly to healthy young adults. Vaccine 2007; 25:5367 - 73; http://dx.doi.org/10.1016/j.vaccine.2007.05.002; PMID: 17559990
   PubMed Web of Science ®Google Scholar
• Ichinohe T, Watanabe I, Ito S, Fujii H, Moriyama M, Tamura S, et al. Synthetic double-stranded RNA poly(I:C) combined with mucosal vaccine protects against influenza virus infection. J Virol 2005; 79:2910 - 9; http://dx.doi.org/10.1128/JVI.79.5.2910-2919.2005; PMID: 15709010
   PubMed Web of Science ®Google Scholar
• Ichinohe T, Tamura S, Kawaguchi A, Ninomiya A, Imai M, Itamura S, et al. Cross-protection against H5N1 influenza virus infection is afforded by intranasal inoculation with seasonal trivalent inactivated influenza vaccine. J Infect Dis 2007; 196:1313 - 20; http://dx.doi.org/10.1086/521304; PMID: 17922395
   PubMed Web of Science ®Google Scholar
• European Medicines Agency. Note for guidance on harmonisation of requirements for influenza vaccines (CPMP/BWP/214/96). In: (CPMP) CfPMP, ed. London: Committee for Proprietary Medical Products (CPMP), 1997.
   Google Scholar
• U.S. Food and Drug Administration. Guidance for Industry: Clinical Data Needed to Support the Licensure of Seasonal Inactivated Influenza Vaccines. In: Services USDoHaH, ed., 2007.
   Google Scholar
• European Medicines Agency. Guideline on dossier structure and content for pandemic influenza vaccine marketing authorization application (CPMP/VFG/4717/03-Rev.1). In: (CHMP) CfMPfHU, ed. London: Committee for Medicinal Products for Human Use (CHMP), 2008.
   Google Scholar
• Cox RJ. Correlates of protection to influenza virus, where do we go from here?. Hum Vaccin Immunother 2013; 9; In press http://dx.doi.org/10.4161/hv.22908; PMID: 23291930
   PubMed Web of Science ®Google Scholar
• Tamura S, Tanimoto T, Kurata T. Mechanisms of broad cross-protection provided by influenza virus infection and their application to vaccines. Jpn J Infect Dis 2005; 58:195 - 207; PMID: 16116250
   PubMed Web of Science ®Google Scholar
• Tamura S. Studies on the usefulness of intranasal inactivated influenza vaccines. Vaccine 2010; 28:6393 - 7; http://dx.doi.org/10.1016/j.vaccine.2010.05.019; PMID: 20493820
   PubMed Web of Science ®Google Scholar
• Okuno Y, Tanaka K, Baba K, Maeda A, Kunita N, Ueda S. Rapid focus reduction neutralization test of influenza A and B viruses in microtiter system. J Clin Microbiol 1990; 28:1308 - 13; PMID: 2380359
   PubMed Web of Science ®Google Scholar
• Lu BL, Webster RG, Hinshaw VS. Failure to detect hemagglutination-inhibiting antibodies with intact avian influenza virions. Infect Immun 1982; 38:530 - 5; PMID: 6292104
   PubMed Web of Science ®Google Scholar
• Rowe T, Abernathy RA, Hu-Primmer J, Thompson WW, Lu X, Lim W, et al. Detection of antibody to avian influenza A (H5N1) virus in human serum by using a combination of serologic assays. J Clin Microbiol 1999; 37:937 - 43; PMID: 10074505
   PubMed Web of Science ®Google Scholar
• Ainai A, Tamura S, Suzuki T, Ito R, Asanuma H, Tanimoto T, et al. Characterization of neutralizing antibodies in adults after intranasal vaccination with an inactivated influenza vaccine. J Med Virol 2012; 84:336 - 44; http://dx.doi.org/10.1002/jmv.22273; PMID: 22170556
   PubMed Web of Science ®Google Scholar
• Kurono Y, Mogi G. Secretory IgA and serum type IgA in nasal secretion and antibody activity against the M protein. Ann Otol Rhinol Laryngol 1987; 96:419 - 24; PMID: 3304089
   PubMed Web of Science ®Google Scholar
• Takada A, Matsushita S, Ninomiya A, Kawaoka Y, Kida H. Intranasal immunization with formalin-inactivated virus vaccine induces a broad spectrum of heterosubtypic immunity against influenza A virus infection in mice. Vaccine 2003; 21:3212 - 8; http://dx.doi.org/10.1016/S0264-410X(03)00234-2; PMID: 12804850
   PubMed Web of Science ®Google Scholar
• Tamura S, Hasegawa H, Kurata T. Estimation of the effective doses of nasal-inactivated influenza vaccine in humans from mouse-model experiments. Jpn J Infect Dis 2010; 63:8 - 15; PMID: 20093755
   PubMed Web of Science ®Google Scholar
• Lund JM, Alexopoulou L, Sato A, Karow M, Adams NC, Gale NW, et al. Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc Natl Acad Sci U S A 2004; 101:5598 - 603; http://dx.doi.org/10.1073/pnas.0400937101; PMID: 15034168
   PubMed Web of Science ®Google Scholar
• Diebold SS, Kaisho T, Hemmi H, Akira S, Reis e Sousa C. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 2004; 303:1529 - 31; http://dx.doi.org/10.1126/science.1093616; PMID: 14976261
   PubMed Web of Science ®Google Scholar
• Kang SM, Guo L, Yao Q, Skountzou I, Compans RW. Intranasal immunization with inactivated influenza virus enhances immune responses to coadministered simian-human immunodeficiency virus-like particle antigens. J Virol 2004; 78:9624 - 32; http://dx.doi.org/10.1128/JVI.78.18.9624-9632.2004; PMID: 15331695
   PubMed Web of Science ®Google Scholar
• Koyama S, Aoshi T, Tanimoto T, Kumagai Y, Kobiyama K, Tougan T, et al. Plasmacytoid dendritic cells delineate immunogenicity of influenza vaccine subtypes. Sci Transl Med 2010; 2:25ra24; http://dx.doi.org/10.1126/scitranslmed.3000759; PMID: 20424013
   PubMed Web of Science ®Google Scholar
• Clements ML, Betts RF, Tierney EL, Murphy BR. Resistance of adults to challenge with influenza A wild-type virus after receiving live or inactivated virus vaccine. J Clin Microbiol 1986; 23:73 - 6; PMID: 3700611
   PubMed Web of Science ®Google Scholar
• Clements ML, Betts RF, Tierney EL, Murphy BR. Serum and nasal wash antibodies associated with resistance to experimental challenge with influenza A wild-type virus. J Clin Microbiol 1986; 24:157 - 60; PMID: 3722363
   PubMed Web of Science ®Google Scholar
• Belshe RB, Gruber WC, Mendelman PM, Mehta HB, Mahmood K, Reisinger K, et al. Correlates of immune protection induced by live, attenuated, cold-adapted, trivalent, intranasal influenza virus vaccine. J Infect Dis 2000; 181:1133 - 7; http://dx.doi.org/10.1086/315323; PMID: 10720541
   PubMed Web of Science ®Google Scholar
• Murphy BR, Phelan MA, Nelson DL, Yarchoan R, Tierney EL, Alling DW, et al. Hemagglutinin-specific enzyme-linked immunosorbent assay for antibodies to influenza A and B viruses. J Clin Microbiol 1981; 13:554 - 60; PMID: 7240388
   PubMed Web of Science ®Google Scholar
• Takahashi Y, Hasegawa H, Hara Y, Ato M, Ninomiya A, Takagi H, et al. Protective immunity afforded by inactivated H5N1 (NIBRG-14) vaccine requires antibodies against both hemagglutinin and neuraminidase in mice. J Infect Dis 2009; 199:1629 - 37; http://dx.doi.org/10.1086/598954; PMID: 19385735
   PubMed Web of Science ®Google Scholar
• Hirota Y, Kaji M, Ide S, Goto S, Oka T. The hemagglutination inhibition antibody responses to an inactivated influenza vaccine among healthy adults: with special reference to the prevaccination antibody and its interaction with age. Vaccine 1996; 14:1597 - 602; http://dx.doi.org/10.1016/S0264-410X(96)00153-3; PMID: 9032887
   PubMed Web of Science ®Google Scholar
• Tobita K, Sugiura A, Enomote C, Furuyama M. Plaque assay and primary isolation of influenza A viruses in an established line of canine kidney cells (MDCK) in the presence of trypsin. Med Microbiol Immunol 1975; 162:9 - 14; http://dx.doi.org/10.1007/BF02123572; PMID: 1214709
   PubMed Web of Science ®Google Scholar
• Kadowaki S, Chen Z, Asanuma H, Aizawa C, Kurata T, Tamura S. Protection against influenza virus infection in mice immunized by administration of hemagglutinin-expressing DNAs with electroporation. Vaccine 2000; 18:2779 - 88; http://dx.doi.org/10.1016/S0264-410X(00)00087-6; PMID: 10812219
   PubMed Web of Science ®Google Scholar
• Reed LJ, Muench H. A simple method of estimating fifty per cent endpoint. Am J Hyg 1938; 27:493 - 7
   Google Scholar
• Davenport FM, Hennessy AV, Brandon FM, Webster RG, Barrett CD Jr., Lease GO. Comparisons of Serologic and Febrile Responses in Humans to Vaccination with Influenza a Viruses or Their Hemagglutinins. J Lab Clin Med 1964; 63:5 - 13; PMID: 14102904
   PubMed Web of Science ®Google Scholar
• Hierholzer JC, Suggs MT, Hall EC. Standardized viral hemagglutination and hemagglutination-inhibition tests. II. Description and statistical evaluation. Appl Microbiol 1969; 18:824 - 33; PMID: 4984203
   PubMedGoogle Scholar
• Phelan MA, Mayner RE, Bucher DJ, Ennis FA. Purification of influenza virus glycoproteins for the preparation and standardization of immunological potency testing reagents. J Biol Stand 1980; 8:233 - 42; http://dx.doi.org/10.1016/S0092-1157(80)80039-4; PMID: 7410447
   PubMedGoogle Scholar