Needle-free influenza vaccination

The Lancet Infectious Diseases

Volumn 10, Issue 10, 2010, Pages 699-711

  Amorij, Jean Pierre ^a,b,c   Hinrichs, Wouter L J ^a   Frijlink, Henderik W ^a   Wilschut, Jan C ^b   Huckriede, Anke ^b  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^c NETHERLANDS VACCINE INSTITUTE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOLOGICAL ADJUVANT; INACTIVATED VACCINE; INFLUENZA VACCINE; INTERFERON; LIVE VACCINE; SUBUNIT VACCINE;

ADAPTIVE IMMUNITY; ANTIBODY TITER; CELLULAR IMMUNITY; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG FORMULATION; DRUG SAFETY; HEALTH CARE PERSONNEL; HEMAGGLUTINATION INHIBITION; HUMAN; IMMUNE RESPONSE; INFLUENZA; INFLUENZA VACCINATION; MUCOSAL IMMUNITY; NEEDLE; NONHUMAN; PRIORITY JOURNAL; REVIEW; VIRUS NEUTRALIZATION; CLINICAL TRIAL (TOPIC); IMMUNOLOGY; INFLUENZA, HUMAN; INTRADERMAL DRUG ADMINISTRATION; INTRANASAL DRUG ADMINISTRATION; ORAL DRUG ADMINISTRATION; PROCEDURES; VACCINATION;

ADMINISTRATION, CUTANEOUS; ADMINISTRATION, INTRANASAL; ADMINISTRATION, ORAL; CLINICAL TRIALS AS TOPIC; HUMANS; IMMUNITY, MUCOSAL; INFLUENZA VACCINES; INFLUENZA, HUMAN; VACCINATION;

EID: 77957139107     PISSN: 14733099     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1473-3099(10)70157-2     Document Type: Review

References (198)

1. WHO Media Influenza Factsheet N°211 WHO, (accessed July 1, 2010). http://www.who.int/mediacentre/factsheets/2003/fs211/en/.
2. Guideline on dossier structure and content for pandemic influenza vaccine marketing authorisation application (2004) The European agency for the evaluation of medicinal products (EMEA): committee for proprietary medicinal products (CPMP), (accessed July 1, 2010). http://archives.who.int/prioritymeds/report/append/62EMEAguidelines.pdf.
3. The European Agency for the Evaluation of Medicinal Products (EMEA), (accessed July 1, 2010). http://www.ema.europa.eu/docs/en_GB/document_library/Scientific_guideline/2009/09/WC500003869.pdf.
4. The European Agency for the Evaluation of Medicinal Products (EMEA), (accessed July 1, 2010). http://www.ema.europa.eu/ema/index.jsp?curl=pages/special_topics/general/general_content_000267.jsp&murl=menus/special_topics/special_topics.jsp&mid=WC0b01ac058004b634.
5. Wilschut J, McElhaney JE, Palache AM Rapid Reference Influenza 2006, Mosby/Elsevier Science, London. 2nd edn.
6. Kersten G, Hirschberg H Needle-free vaccine delivery. Expert Opin Drug Deliv 2007, 4:459-474.
7. Mitragotri S Immunization without needles. Nat Rev Immunol 2005, 5:905-916.
8. Giudice EL, Campbell JD Needle-free vaccine delivery. Adv Drug Deliv Rev 2006, 58:68-89.
9. Azad N, Rojanasakul Y Vaccine delivery-current trends and future. Curr Drug Deliv 2006, 3:137-146.
10. O'Hagan DT, Rappuoli R Novel approaches to vaccine delivery. Pharm Res 2004, 21:1519-1530.
11. Kersten G, Hirschberg H Antigen delivery systems. Expert Rev Vaccines 2004, 3:453-462.
12. Nugent J, Po AL, Scott EM Design and delivery of non-parenteral vaccines. J Clin Pharm Ther 1998, 23:257-285.
13. WHO position paper (macroepidemiology). Wkly Epidemiol Rec 2005, 80:279-287. WHO.
14. Sendi P, Locher R, Bucheli B, Battegay M Intranasal influenza vaccine in a working population. Clin Infect Dis 2004, 38:974-980.
15. Liew FY, Russell SM, Appleyard G, Brand CM, Beale J Cross-protection in mice infected with influenza A virus by the respiratory route is correlated with local IgA antibody rather than serum antibody or cytotoxic T cell reactivity. Eur J Immunol 1984, 14:350-356.
16. Tumpey TM, Renshaw M, Clements JD, Katz JM Mucosal delivery of inactivated influenza vaccine induces B-cell-dependent heterosubtypic cross-protection against lethal influenza A H5N1 virus infection. J Virol 2001, 75:5141-5150.
17. Asahi-Ozaki Y, Yoshikawa T, Iwakura Y, et al. Secretory IgA antibodies provide cross-protection against infection with different strains of influenza B virus. J Med Virol 2004, 74:328-335.
18. Hasegawa H, Ichinohe T, Strong P, et al. Protection against influenza virus infection by intranasal administration of hemagglutinin vaccine with chitin microparticles as an adjuvant. J Med Virol 2005, 75:130-136.
19. Ichinohe T, Tamura S, Kawaguchi A, et al. Cross-protection against H5N1 influenza virus infection is afforded by intranasal inoculation with seasonal trivalent inactivated influenza vaccine. J Infect Dis 2007, 196:1313-1320.
20. Ekwueme DU, Weniger BG, Chen RT Model-based estimates of risks of disease transmission and economic costs of seven injection devices in sub-Saharan Africa. Bull World Health Organ 2002, 80:859-870.
21. Sugimura T, Ito Y, Tananari Y, et al. Improved antibody responses in infants less than 1 year old using intradermal influenza vaccination. Vaccine 2008, 26:2700-2705.
22. Amorij JP, Huckriede A, Wilschut J, Frijlink HW, Hinrichs WL Development of stable influenza vaccine powder formulations: challenges and possibilities. Pharm Res 2008, 25:1256-1273.
23. van Vliet SJ, den Dunnen J, Gringhuis SI, Geijtenbeek TB, van Kooyk Y Innate signaling and regulation of dendritic cell immunity. Curr Opin Immunol 2007, 19:435-440.
24. 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 2008, 4:e1000138.
25. Mosca F, Tritto E, Muzzi A, et al. Molecular and cellular signatures of human vaccine adjuvants. Proc Natl Acad Sci USA 2008, 105:10501-10506.
26. Marrack P, McKee AS, Munks MW Towards an understanding of the adjuvant action of aluminium. Nat Rev Immunol 2009, 9:287-293.
27. Jensen PE Recent advances in antigen processing and presentation. Nat Immunol 2007, 8:1041-1048.
28. Harwood NE, Batista FD New insights into the early molecular events underlying B cell activation. Immunity 2008, 28:609-619.
29. Neutra MR, Kozlowski PA Mucosal vaccines: the promise and the challenge. Nat Rev Immunol 2006, 6:148-158.
30. Minne A, Louahed J, Mehauden S, Baras B, Renauld JC, Vanbever R The delivery site of a monovalent influenza vaccine within the respiratory tract impacts on the immune response. Immunology 2007, 122:316-325.
31. Tafaghodi M, Abolghasem Sajadi Tabassi S, Jaafari MR, Zakavi SR, Momen-Nejad M Evaluation of the clearance characteristics of various microspheres in the human nose by gamma-scintigraphy. Int J Pharm 2004, 280:125-135.
32. Vidgren MT, Kublik H Nasal delivery systems and their effect on deposition and absorption. Adv Drug Deliv Rev 1998, 29:157-177.
33. Meitin CA, Bender BS, Small PA Enteric immunization of mice against influenza with recombinant vaccinia. Proc Natl Acad Sci USA 1994, 91:11187-11191.
34. Amorij JP, Westra TA, Hinrichs WL, Huckriede A, Frijlink HW Towards an oral influenza vaccine: Comparison between intragastric and intracolonic delivery of influenza subunit vaccine in a murine model. Vaccine 2007, 26:67-76.
35. Frijlink HW, De Boer AH Trends in the technology-driven development of new inhalation devices. Drug Discovery Today: Technologies 2005, 2:47-57.
36. Schellekens RC, Stellaard F, Mitrovic D, Stuurman FE, Kosterink JG, Frijlink HW Pulsatile drug delivery to ileo-colonic segments by structured incorporation of disintegrants in pH-responsive polymer coatings. J Control Release 2008, 132:91-98.
37. Glenn GM, O'Hagan DT Adjuvants: progress, regress and pandemic preparedness. Expert Rev Vaccines 2007, 6:651-652.
38. Smith DJ, King WF, Barnes LA, Trantolo D, Wise DL, Taubman MA Facilitated intranasal induction of mucosal and systemic immunity to mutans streptococcal glucosyltransferase peptide vaccines. Infect Immun 2001, 69:4767-4773.
39. Oien NL, Brideau RJ, Walsh EE, Wathen MW Induction of local and systemic immunity against human respiratory syncytial virus using a chimeric FG glycoprotein and cholera toxin B subunit. Vaccine 1994, 12:731-735.
40. Boyce TG, Hsu HH, Sannella EC, et al. Safety and immunogenicity of adjuvanted and unadjuvanted subunit influenza vaccines administered intranasally to healthy adults. Vaccine 2000, 19:217-226.
41. Gluck U, Gebbers JO, Gluck R Phase 1 evaluation of intranasal virosomal influenza vaccine with and without Escherichia coli heat-labile toxin in adult volunteers. J Virol 1999, 73:7780-7786.
42. Glueck R Pre-clinical and clinical investigation of the safety of a novel adjuvant for intranasal immunization. Vaccine 2001, 20(suppl 1):S42-S44.
43. Huckriede A, Bungener L, Stegmann T, et al. The virosome concept for influenza vaccines. Vaccine 2005, 23(suppl 1):S26-S38.
44. Mutsch M, Zhou W, Rhodes P, et al. Use of the inactivated intranasal influenza vaccine and the risk of Bell's palsy in Switzerland. N Engl J Med 2004, 350:896-903.
45. Pine S, Barackman J, Ott G, O'Hagan D Intranasal immunization with influenza vaccine and a detoxified mutant of heat labile enterotoxin from Escherichia coli (LTK63). J Control Release 2002, 85:263-270.
46. Stephenson I, Zambon MC, Rudin A, et al. Phase I evaluation of intranasal trivalent inactivated influenza vaccine with nontoxigenic Escherichia coli enterotoxin and novel biovector as mucosal adjuvants, using adult volunteers. J Virol 2006, 80:4962-4970.
47. Joseph A, Itskovitz-Cooper N, Samira S, et al. A new intranasal influenza vaccine based on a novel polycationic lipid-ceramide carbamoyl-spermine (CCS) I: immunogenicity and efficacy studies in mice. Vaccine 2006, 24:3990-4006.
48. Ko SY, Ko HJ, Chang WS, Park SH, Kweon MN, Kang CY alpha-Galactosylceramide can act as a nasal vaccine adjuvant inducing protective immune responses against viral infection and tumor. J Immunol 2005, 175:3309-3317.
49. Youn HJ, Ko SY, Lee KA, et al. A single intranasal immunization with inactivated influenza virus and alpha-galactosylceramide induces long-term protective immunity without redirecting antigen to the central nervous system. Vaccine 2007, 25:5189-5198.
50. Shim DH, Ko HJ, Volker G, et al. Efficacy of poly[di(sodium carboxylatophenoxy)phosphazene] (PCPP) as mucosal adjuvant to induce protective immunity against respiratory pathogens. Vaccine; 28: 2311-17.
51. Guy B, Pascal N, Francon A, et al. Design, characterization and preclinical efficacy of a cationic lipid adjuvant for influenza split vaccine. Vaccine 2001, 19:1794-1805.
52. Nishino M, Mizuno D, Kimoto T, et al. Influenza vaccine with Surfacten, a modified pulmonary surfactant, induces systemic and mucosal immune responses without side effects in minipigs. Vaccine 2009, 27:5620-5627.
53. Bracci L, Canini I, Puzelli S, et al. Type I IFN is a powerful mucosal adjuvant for a selective intranasal vaccination against influenza virus in mice and affects antigen capture at mucosal level. Vaccine 2005, 23:2994-3004.
54. Bracci L, Canini I, Venditti M, et al. Type I IFN as a vaccine adjuvant for both systemic and mucosal vaccination against influenza virus. Vaccine 2006, 24(suppl 2):S256-S257.
55. Arulanandam BP, O'Toole M, Metzger DW Intranasal interleukin-12 is a powerful adjuvant for protective mucosal immunity. J Infect Dis 1999, 180:940-949.
56. Joseph A, Louria-Hayon I, Plis-Finarov A, et al. Liposomal immunostimulatory DNA sequence (ISS-ODN): an efficient parenteral and mucosal adjuvant for influenza and hepatitis B vaccines. Vaccine 2002, 20:3342-3354.
57. Ichinohe T, Kawaguchi A, Tamura S, et al. Intranasal immunization with H5N1 vaccine plus poly I: poly C12U, a toll-like receptor agonist, protects mice against homologous and heterologous virus challenge. Microbes Infect 2007, 9:1333-1340.
58. Song SK, Moldoveanu Z, Nguyen HH, et al. Intranasal immunization with influenza virus and Korean mistletoe lectin C (KML-C) induces heterosubtypic immunity in mice. Vaccine 2007, 25:6359-6366.
59. Zanvit P, Havlickova M, Tacner J, et al. Protective and cross-protective mucosal immunization of mice by influenza virus type A with bacterial adjuvant. Immunol Lett 2008, 115:144-152.
60. Plante M, Jones T, Allard F, et al. Nasal immunization with subunit proteosome influenza vaccines induces serum HAI, mucosal IgA and protection against influenza challenge. Vaccine 2001, 20:218-225.
61. Lovgren K, Kaberg H, Morein B An experimental influenza subunit vaccine (iscom): induction of protective immunity to challenge infection in mice after intranasal or subcutaneous administration. Clin Exp Immunol 1990, 82:435-439.
62. Sjolander S, Drane D, Davis R, Beezum L, Pearse M, Cox J Intranasal immunisation with influenza-ISCOM induces strong mucosal as well as systemic antibody and cytotoxic T-lymphocyte responses. Vaccine 2001, 19:4072-4080.
63. Coulter A, Harris R, Davis R, et al. Intranasal vaccination with ISCOMATRIX adjuvanted influenza vaccine. Vaccine 2003, 21:946-949.
64. Helgeby A, Robson NC, Donachie AM, et al. The combined CTA1-DD/ISCOM adjuvant vector promotes priming of mucosal and systemic immunity to incorporated antigens by specific targeting of B cells. J Immunol 2006, 176:3697-3706.
65. Hu KF, Lovgren-Bengtsson K, Morein B Immunostimulating complexes (ISCOMs) for nasal vaccination. Adv Drug Deliv Rev 2001, 51:149-159.
66. Scheerlinck JP, Gekas S, Yen HH, et al. Local immune responses following nasal delivery of an adjuvanted influenza vaccine. Vaccine 2006, 24:3929-3936.
67. Read RC, Naylor SC, Potter CW, et al. Effective nasal influenza vaccine delivery using chitosan. Vaccine 2005, 23:4367-4374.
68. Bacon A, Makin J, Sizer PJ, et al. Carbohydrate biopolymers enhance antibody responses to mucosally delivered vaccine antigens. Infect Immun 2000, 68:5764-5770.
69. Amidi M, Romeijn SG, Verhoef JC, et al. N-Trimethyl chitosan (TMC) nanoparticles loaded with influenza subunit antigen for intranasal vaccination: Biological properties and immunogenicity in a mouse model. Vaccine 2007, 25:144-153.
70. Illum L, Jabbal-Gill I, Hinchcliffe M, Fisher AN, Davis SS Chitosan as a novel nasal delivery system for vaccines. Adv Drug Deliv Rev 2001, 51:81-96.
71. Huang J, Garmise RJ, Crowder TM, et al. A novel dry powder influenza vaccine and intranasal delivery technology: induction of systemic and mucosal immune responses in rats. Vaccine 2004, 23:794-801.
72. Garmise RJ, Staats HF, Hickey AJ Novel dry powder preparations of whole inactivated influenza virus for nasal vaccination. AAPS PharmSciTech 2007, 8:e81.
73. Smith DJ, Bot S, Dellamary L, Bot A Evaluation of novel aerosol formulations designed for mucosal vaccination against influenza virus. Vaccine 2003, 21:2805-2812.
74. Song JH, Nguyen HH, Cuburu N, et al. Sublingual vaccination with influenza virus protects mice against lethal viral infection. Proc Natl Acad Sci USA 2008, 105:1644-1649.
75. McCluskie MJ, Davis HL Oral, intrarectal and intranasal immunizations using CpG and non-CpG oligodeoxynucleotides as adjuvants. Vaccine 2000, 19:413-422.
76. Katz JM, Lu X, Young SA, Galphin JC Adjuvant activity of the heat-labile enterotoxin from enterotoxigenic Escherichia coli for oral administration of inactivated influenza virus vaccine. J Infect Dis 1997, 175:352-363.
77. Barackman JD, Ott G, Pine S, O'Hagan DT Oral administration of influenza vaccine in combination with the adjuvants LT-K63 and LT-R72 induces potent immune responses comparable to or stronger than traditional intramuscular immunization. Clin Diagn Lab Immunol 2001, 8:652-657.
78. Lu X, Clements JD, Katz JM Mutant Escherichia coli heat-labile enterotoxin [LT(R192G)] enhances protective humoral and cellular immune responses to orally administered inactivated influenza vaccine. Vaccine 2002, 20:1019-1029.
79. Conacher M, Alexander J, Brewer JM Oral immunisation with peptide and protein antigens by formulation in lipid vesicles incorporating bile salts (bilosomes). Vaccine 2001, 19:2965-2974.
80. Kunzi V, Klap JM, Seiberling MK, et al. Immunogenicity and safety of low dose virosomal adjuvanted influenza vaccine administered intradermally compared to intramuscular full dose administration. Vaccine 2009, 27:3561-3567.
81. Skountzou I, Quan FS, Jacob J, Compans RW, Kang SM Transcutaneous immunization with inactivated influenza virus induces protective immune responses. Vaccine 2006, 24:6110-6119.
82. Chen D, Endres RL, Erickson CA, Maa YF, Payne LG Epidermal powder immunization using non-toxic bacterial enterotoxin adjuvants with influenza vaccine augments protective immunity. Vaccine 2002, 20:2671-2679.
83. Chen D, Endres R, Maa YF, et al. Epidermal powder immunization of mice and monkeys with an influenza vaccine. Vaccine 2003, 21:2830-2836.
84. Sesardic D, Rijpkema S, Patel BP New adjuvants: EU regulatory developments. Expert Rev Vaccines 2007, 6:849-861.
85. Kanerva M, Mannonen L, Piiparinen H, Peltomaa M, Vaheri A, Pitkaranta A Search for Herpesviruses in cerebrospinal fluid of facial palsy patients by PCR. Acta Otolaryngol 2007, 127:775-779.
86. van Ginkel FW, Jackson RJ, Yoshino N, et al. Enterotoxin-based mucosal adjuvants alter antigen trafficking and induce inflammatory responses in the nasal tract. Infect Immun 2005, 73:6892-6902.
87. van der Laan JW, Herberts C, Lambkin-Williams R, Boyers A, Mann AJ, Oxford J Animal models in influenza vaccine testing. Expert Rev Vaccines 2008, 7:783-793.
88. Bodewes R, Rimmelzwaan GF, Osterhaus AD Animal models for the preclinical evaluation of candidate influenza vaccines. Expert Rev Vaccines 2010, 9:59-72.
89. Note for guidance on harmonization of requirements for influenza vaccines (1997) The European agency for the evaluation of medicinal products (EMEA) committee for proprietary medicinal products (CPMP), (accessed July 1, 2010). http://www.ema.europa.eu/docs/en_GB/document_library/Scientific_guideline/2009/09/WC500003945.pdf.
90. 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, 24:157-160.
91. Renegar KB, Small PA Immunoglobulin A mediation of murine nasal anti-influenza virus immunity. J Virol 1991, 65:2146-2148.
92. Mizuno D, Ide-Kurihara M, Ichinomiya T, Kubo I, Kido H Modified pulmonary surfactant is a potent adjuvant that stimulates the mucosal IgA production in response to the influenza virus antigen. J Immunol 2006, 176:1122-1130.
93. Rimmelzwaan GF, Fouchier RA, Osterhaus AD Influenza virus-specific cytotoxic T lymphocytes: a correlate of protection and a basis for vaccine development. Curr Opin Biotechnol 2007, 18:529-536.
94. McElhaney JE, Xie D, Hager WD, et al. T cell responses are better correlates of vaccine protection in the elderly. J Immunol 2006, 176:6333-6339.
95. He XS, Holmes TH, Zhang C, et al. Cellular immune responses in children and adults receiving inactivated or live attenuated influenza vaccines. J Virol 2006, 80:11756-11766.
96. Chen D, Weis KF, Chu Q, et al. Epidermal powder immunization induces both cytotoxic T-lymphocyte and antibody responses to protein antigens of influenza and hepatitis B viruses. J Virol 2001, 75:11630-11640.
97. Treanor J, Wright PF Immune correlates of protection against influenza in the human challenge model. Dev Biol (Basel) 2003, 115:97-104.
98. Wilschut J, de Jonge J, Huckriede A, Amorij JP, Hinrichs WL, Frijlink HW Preservation of influenza virosome structure and function during freeze-drying and storage. J Liposome Res 2007, 17:173-182.
99. Abramson JS Intranasal, cold-adapted, live, attenuated influenza vaccine. Pediatr Infect Dis J 1999, 18:1103-1104.
100. Belshe R, Lee MS, Walker RE, Stoddard J, Mendelman PM Safety, immunogenicity and efficacy of intranasal, live attenuated influenza vaccine. Expert Rev Vaccines 2004, 3:643-654.
101. Cox RJ, Brokstad KA, Ogra P Influenza virus: immunity and vaccination strategies. Comparison of the immune response to inactivated and live, attenuated influenza vaccines. Scand J Immunol 2004, 59:1-15.
102. Beyer WE, Palache AM, de Jong JC, Osterhaus AD Cold-adapted live influenza vaccine versus inactivated vaccine: systemic vaccine reactions, local and systemic antibody response, and vaccine efficacy. A meta-analysis. Vaccine 2002, 20:1340-1353.
103. Glezen WP Control of influenza. Tex Heart Inst J 2004, 31:39-41.
104. Fleming DM, Crovari P, Wahn U, et al. Comparison of the efficacy and safety of live attenuated cold-adapted influenza vaccine, trivalent, with trivalent inactivated influenza virus vaccine in children and adolescents with asthma. Pediatr Infect Dis J 2006, 25:860-869.
105. Greenbaum E, Furst A, Kiderman A, 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, 20:1232-1239.
106. 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, 22:2566-2577.
107. Samdal HH, Bakke H, Oftung F, et al. A non-living nasal influenza vaccine can induce major humoral and cellular immune responses in humans without the need for adjuvants. Hum Vaccin 2005, 1:85-90.
108. Muszkat M, Greenbaum E, Ben-Yehuda A, et al. Local and systemic immune response in nursing-home elderly following intranasal or intramuscular immunization with inactivated influenza vaccine. Vaccine 2003, 21:1180-1186.
109. 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, 25:5367-5373.
110. Haan L, Verweij WR, Holtrop M, et al. Nasal or intramuscular immunization of mice with influenza subunit antigen and the B subunit of Escherichia coli heat-labile toxin induces IgA- or IgG-mediated protective mucosal immunity. Vaccine 2001, 19:2898-2907.
111. McCluskie MJ, Weeratna RD, Clements JD, Davis HL Mucosal immunization of mice using CpG DNA and/or mutants of the heat-labile enterotoxin of Escherichia coli as adjuvants. Vaccine 2001, 19:3759-3768.
112. Hagiwar Y, Tsuji T, Iwasaki T, et al. Effectiveness and safety of mutant Escherichia coli heat-labile enterotoxin (LT H44A) as an adjuvant for nasal influenza vaccine. Vaccine 2001, 19:2071-2079.
113. Barchfeld GL, Hessler AL, Chen M, Pizza M, Rappuoli R, Van Nest GA The adjuvants MF59 and LT-K63 enhance the mucosal and systemic immunogenicity of subunit influenza vaccine administered intranasally in mice. Vaccine 1999, 17:695-704.
114. Halperin SA, Smith B, Clarke K, Treanor J, Mabrouk T, Germain M Phase I, randomized, controlled trial to study the reactogenicity and immunogenicity of a nasal, inactivated trivalent influenza virus vaccine in healthy adults. Hum Vaccin 2005, 1:37-42.
115. Ugwoke MI, Agu RU, Verbeke N, Kinget R Nasal mucoadhesive drug delivery: background, applications, trends and future perspectives. Adv Drug Deliv Rev 2005, 57:1640-1665.
116. Interferon as a mucosal adjuvant for influenza vaccine given intranasally (NCT00436046) Robert Johnson, (accessed July 1, 2010). http://clinicaltrials.gov/ct2/show/study/NCT00436046?sect=X501.
117. Sullivan VJ, Mikszta JA, Laurent P, Huang J, Ford B Noninvasive delivery technologies: respiratory delivery of vaccines. Expert Opin Drug Deliv 2006, 3:87-95.
118. Jiang G, Joshi SB, Peek LJ, et al. Anthrax vaccine powder formulations for nasal mucosal delivery. J Pharm Sci 2006, 95:80-96.
119. Huo Z, Sinha R, McNeela EA, et al. Induction of protective serum meningococcal bactericidal and diphtheria-neutralizing antibodies and mucosal immunoglobulin A in volunteers by nasal insufflations of the Neisseria meningitidis serogroup C polysaccharide-CRM197 conjugate vaccine mixed with chitosan. Infect Immun 2005, 73:8256-8265.
120. Garmise RJ, Mar K, Crowder TM, et al. Formulation of a dry powder influenza vaccine for nasal delivery. AAPS PharmSciTech 2006, 7:e19.
121. Soane RJ, Frier M, Perkins AC, Jones NS, Davis SS, Illum L Evaluation of the clearance characteristics of bioadhesive systems in humans. Int J Pharm 1999, 178:55-65.
122. McInnes FJ, Thapa P, Baillie AJ, et al. In vivo evaluation of nicotine lyophilised nasal insert in sheep. Int J Pharm 2005, 304:72-82.
123. Newman SP, Pitcairn GR, Dalby RN Drug delivery to the nasal cavity: in vitro and in vivo assessment. Crit Rev Ther Drug Carrier Syst 2004, 21:21-66.
124. Laube BL Devices for aerosol delivery to treat sinusitis. J Aerosol Med 2007, 20(suppl 1):s5-s17.
125. Groneberg DA, Paul H, Welte T Novel strategies of aerosolic pharmacotherapy. Exp Toxicol Pathol 2006, 57(suppl 2):49-53.
126. Holmgren J, Czerkinsky C Mucosal immunity and vaccines. Nat Med 2005, 11(suppl 4):s45-s53.
127. Lambrecht BN, Prins JB, Hoogsteden HC Lung dendritic cells and host immunity to infection. Eur Respir J 2001, 18:692-704.
128. von Garnier C, Filgueira L, Wikstrom M, et al. Anatomical location determines the distribution and function of dendritic cells and other APCs in the respiratory tract. J Immunol 2005, 175:1609-1618.
129. Holt PG Pulmonary dendritic cells in local immunity to inert and pathogenic antigens in the respiratory tract. Proc Am Thorac Soc 2005, 2:116-120.
130. Holmgren J, Czerkinsky C, Lycke N, Svennerholm AM Mucosal immunity: implications for vaccine development. Immunobiology 1992, 184:157-179.
131. Mann JJ, Waldman RH, Togo Y, Heiner GG, Dawkins AT, Kasel JA Antibody response in respiratory secretions of volunteers given live and dead influenza virus. J Immunol 1968, 100:726-735.
132. Kasel JA, Fulk RV, Togo Y, et al. Influenza antibody in human respiratory secretions after subcutaneous or respiratory immunization with inactivated virus. Nature 1968, 218:594-595.
133. Waldman RH, Mann JJ, Kasel JA Influenza virus neutralizing antibody in human respiratory secretions. J Immunol 1968, 100:80-85.
134. Waldman RH, Mann JJ, Small PA Immunization against influenza: prevention of illness in man by aerosolized inactivated vaccine. JAMA 1969, 207:520-524.
135. Waldman RH, Jurgensen PF, Olsen GN, Ganguly R, Johnson JE Immune response of the human respiratory tract-I: Immunoglobulin levels and influenza virus vaccine antibody response. J Immunol 1973, 111:38-41.
136. Waldman RH, Wigley FMSPA Specificity of respiratory secretion antibody against influenza virus. J Immunol 1970, 105:1477-1483.
137. Haigh W, Howell RW The efficacy of the A2/Aichi/68 strain in inhaled influenza immunisation against the A/England/42/72 variant. J Soc Occup Med 1973, 23:125-127.
138. Haigh W, Howell RW, Meichen FW A comparative trial of influenza immunization by inhalation and hypojet methods. Practitioner 1973, 211:365-370.
139. Wee JL, Scheerlinck JP, Snibson KJ, et al. Pulmonary delivery of ISCOMATRIX influenza vaccine induces both systemic and mucosal immunity with antigen dose sparing. Mucosal Immunol 2008, 1:489-496.
140. Amorij JP, Saluja V, Petersen AH, Hinrichs WL, Huckriede A, Frijlink HW Pulmonary delivery of an inulin-stabilized influenza subunit vaccine prepared by spray-freeze drying induces systemic, mucosal humoral as well as cell-mediated immune responses in BALB/c mice. Vaccine 2007, 25:8707-8717.
141. Dalby R, Spallek M, Voshaar T A review of the development of respimat soft mist inhaler. Int J Pharm 2004, 283:1-9.
142. de Boer AH, Hagedoorn P, Westerman EM, Le Brun PP, Heijerman HG, Frijlink HW Design and in vitro performance testing of multiple air classifier technology in a new disposable inhaler concept (Twincer) for high powder doses. Eur J Pharm Sci 2006, 28:171-178.
143. Lu D, Hickey AJ Pulmonary vaccine delivery. Expert Rev Vaccines 2007, 6:213-226.
144. Meyer P, Menzel M, Muellinger B, Weber N, Haeussinger K, Ziegler-Heitbrock L Inhalative vaccination with pneumococcal polysaccharide in patients with chronic obstructive pulmonary disease. Vaccine 2006, 24:5832-5838.
145. Minne A, Huaux F, Jaworska J, Rha RD, Hamelmann E, Vanbever R Safety evaluation of pulmonary influenza vaccination in healthy and asthmatic mice. Vaccine 2008, 26:2360-2368.
146. Senel S, Kremer M, Nagy K, Squier C Delivery of bioactive peptides and proteins across oral (buccal) mucosa. Curr Pharm Biotechnol 2001, 2:175-186.
147. Challacombe S, Coogan M, Williams D, Greenspan J Overview and research agenda arising from the 5th World Workshop on Oral Health and Disease in AIDS. Adv Dent Res 2006, 19:5-9.
148. Otten K, Wang HC, Wyde PR, Klein JR Modulation of gamma delta T cells in mouse buccal epithelium following antigen priming. Biochem Biophys Res Commun 2002, 294:626-629.
149. Gebert A, Pabst R M cells at locations outside the gut. Semin Immunol 1999, 11:165-170.
150. Childers NK, Powell WD, Tong G, Kirk K, Wiatrak B, Michalek SM Human salivary immunoglobulin and antigen-specific antibody activity after tonsillectomy. Oral Microbiol Immunol 2001, 16:265-269.
151. Bakke H, Samdal HH, Holst J, et al. Oral spray immunization may be an alternative to intranasal vaccine delivery to induce systemic antibodies but not nasal mucosal or cellular immunity. Scand J Immunol 2006, 63:223-231.
152. Canonica GW, Passalacqua G Noninjection routes for immunotherapy. J Allergy Clin Immunol 2003, 111:437-448.
153. Cuburu N, Kweon MN, Song JH, et al. Sublingual immunization induces broad-based systemic and mucosal immune responses in mice. Vaccine 2007, 25:8598-8610.
154. Avtushenko SS, Sorokin EM, Zoschenkova NY, Zacharova NG, Naichin AN Clinical and immunological characteristics of the emulsion form of inactivated influenza vaccine delivered by oral immunization. J Biotechnol 1996, 44:21-28.
155. Moldoveanu Z, Clements ML, Prince SJ, Murphy BR, Mestecky J Human immune responses to influenza virus vaccines administered by systemic or mucosal routes. Vaccine 1995, 13:1006-1012.
156. Lazzell V, Waldman RH, Rose C, Khakoo R, Jacknowitz A, Howard S Immunization against influenza in humans using an oral enteric-coated killed virus vaccine. J Biol Stand 1984, 12:315-321.
157. Bergmann KC, Waldman RH, Tischner H, Pohl WD Antibody in tears, saliva and nasal secretions following oral immunization of humans with inactivated influenza virus vaccine. Int Arch Allergy Appl Immunol 1986, 80:107-109.
158. Gazzaniga A, Maroni A, Sangalli ME, Zema L Time-controlled oral delivery systems for colon targeting. Expert Opin Drug Deliv 2006, 3:583-597.
159. Huang CM Topical vaccination: the skin as a unique portal to adaptive immune responses. Semin Immunopathol 2007, 29:71-80.
160. Yu RC, Abrams DC, Alaibac M, Chu AC Morphological and quantitative analyses of normal epidermal Langerhans cells using confocal scanning laser microscopy. Br J Dermatol 1994, 131:843-848.
161. Glenn GM, Kenney RT Mass vaccination: solutions in the skin. Curr Top Microbiol Immunol 2006, 304:247-268.
162. Chiu SS, Peiris JS, Chan KH, Wong WH, Lau YL Immunogenicity and safety of intradermal influenza immunization at a reduced dose in healthy children. Pediatrics 2007, 119:1076-1082.
163. Belshe RB, Newman FK, Cannon J, et al. Serum antibody responses after intradermal vaccination against influenza. N Engl J Med 2004, 351:2286-2294.
164. Kenney RT, Frech SA, Muenz LR, Villar CP, Glenn GM Dose sparing with intradermal injection of influenza vaccine. N Engl J Med 2004, 351:2295-2301.
165. Holland D, Booy R, De Looze F, et al. Intradermal influenza vaccine administered using a new microinjection system produces superior immunogenicity in elderly adults: a randomized controlled trial. J Infect Dis 2008, 198:650-658.
166. Chi RC, Rock MT, Neuzil KM Immunogenicity and safety of intradermal influenza vaccination in healthy older adults. Clin Infect Dis 2010, 50:1331-1338.
167. Nicholson KG, Thompson CI, Klap JM, et al. Safety and immunogenicity of whole-virus, alum-adjuvanted whole-virus, virosomal, and whole-virus intradermal influenza A/H9N2 vaccine formulations. Vaccine 2009, 28:171-178.
168. Chiu SS, Chan KH, Tu W, Lau YL, Peiris JS Immunogenicity and safety of intradermal versus intramuscular route of influenza immunization in infants less than 6 of age: a randomized controlled trial. Vaccine 2009, 27:4834-4839.
169. Gelinck LB, van den Bemt BJ, Marijt WA, et al. Intradermal influenza vaccination in immunocompromized patients is immunogenic and feasible. Vaccine 2009, 27:2469-2474.
170. Jo YM, Song JY, Hwang IS, et al. Dose sparing strategy with intradermal influenza vaccination in patients with solid cancer. J Med Virol 2009, 81:722-727.
171. Belshe RB, Newman FK, Wilkins K, et al. Comparative immunogenicity of trivalent influenza vaccine administered by intradermal or intramuscular route in healthy adults. Vaccine 2007, 25:6755-6763.
172. Auewarakul P, Kositanont U, Sornsathapornkul P, Tothong P, Kanyok R, Thongcharoen P Antibody responses after dose-sparing intradermal influenza vaccination. Vaccine 2007, 25:659-663.
173. Hunsaker BD, Perino LJ Efficacy of intradermal vaccination. Vet Immunol Immunopathol 2001, 79:1-13.
174. Vandervoort J, Ludwig A Microneedles for transdermal drug delivery: a minireview. Front Biosci 2008, 13:1711-1715.
175. Alarcon JB, Hartley AW, Harvey NG, Mikszta JA Preclinical evaluation of microneedle technology for intradermal delivery of influenza vaccines. Clin Vaccine Immunol 2007, 14:375-381.
176. Arnou R, Eavis P, Pardo JR, Ambrozaitis A, Kazek MP, Weber F Immunogenicity, large scale safety and lot consistency of an intradermal influenza vaccine in adults aged 18-60 years: Randomized, controlled, phase III trial. Hum Vaccin 2010, 6:346-354.
177. Arnou R, Icardi G, De Decker M, et al. Intradermal influenza vaccine for older adults: a randomized controlled multicenter phase III study. Vaccine 2009, 27:7304-7312.
178. The European Agency for the Evaluation of Medicinal Products (EMEA), (accessed July 1, 2010). http://www.ema.europa.eu/humandocs/Humans/EPAR/intanza/intanza.htm.
179. McAllister DV, Wang PM, Davis SP, et al. Microfabricated needles for transdermal delivery of macromolecules and nanoparticles: fabrication methods and transport studies. Proc Natl Acad Sci USA 2003, 100:13755-13760.
180. Mikszta JA, Alarcon JB, Brittingham JM, Sutter DE, Pettis RJ, Harvey NG Improved genetic immunization via micromechanical disruption of skin-barrier function and targeted epidermal delivery. Nat Med 2002, 8:415-419.
181. Van Damme P, Oosterhuis-Kafeja F, Van der Wielen M, Almagor Y, Sharon O, Levin Y Safety and efficacy of a novel microneedle device for dose sparing intradermal influenza vaccination in healthy adults. Vaccine 2009, 27:454-459.
182. Baxter J, Mitragotri S Needle-free liquid jet injections: mechanisms and applications. Expert Rev Med Devices 2006, 3:565-574.
183. Mitragotri S Current status and future prospects of needle-free liquid jet injectors. Nat Rev Drug Discov 2006, 5:543-548.
184. Jackson LA, Austin G, Chen RT, et al. Safety and immunogenicity of varying dosages of trivalent inactivated influenza vaccine administered by needle-free jet injectors. Vaccine 2001, 19:4703-4709.
185. Glenn GM, Flyer DC, Ellingsworth LR, et al. Transcutaneous immunization with heat-labile enterotoxin: development of a needle-free vaccine patch. Expert Rev Vaccines 2007, 6:809-819.
186. Mahor S, Gupta PN, Rawat A, Vyas SP A needle-free approach for topical immunization: antigen delivery via vesicular carrier system(s). Curr Med Chem 2007, 14:2898-2910.
187. Glenn GM, Kenney RT, Hammond SA, Ellingsworth LR Transcutaneous immunization and immunostimulant strategies. Immunol Allergy Clin North Am 2003, 23:787-813.
188. Vogt A, Mahe B, Costagliola D, et al. Transcutaneous anti-influenza vaccination promotes both CD4 and CD8 T cell immune responses in humans. J Immunol 2008, 180:1482-1489.
189. Garg S, Hoelscher M, Belser JA, et al. Needle-free skin patch delivery of a pandemic influenza vaccine protects mice from lethal viral challenge. Clin Vaccine Immunol 2007, 14:926-928.
190. Sarphie DF, Johnson B, Cormier M, Burkoth TL, Bellhouse BL Bioavailabillity following transdermal powdered delivery (TDP) of radiolabeled insulin to hairless guinea pigs. J Control Release 1997, 47:61-69.
191. Chen D, Endres RL, Erickson CA, et al. Epidermal immunization by a needle-free powder delivery technology: immunogenicity of influenza vaccine and protection in mice. Nat Med 2000, 6:1187-1190.
192. Dean HJ, Chen D Epidermal powder immunization against influenza. Vaccine 2004, 23:681-686.
193. Chen D, Periwal SB, Larrivee K, et al. Serum and mucosal immune responses to an inactivated influenza virus vaccine induced by epidermal powder immunization. J Virol 2001, 75:7956-7965.
194. Matriano JA, Cormier M, Johnson J, et al. Macroflux microprojection array patch technology: a new and efficient approach for intracutaneous immunization. Pharm Res 2002, 19:63-70.
195. Koutsonanos DG, del Pilar Martin M, Zarnitsyn VG, et al. Transdermal influenza immunization with vaccine-coated microneedle arrays. PLoS ONE 2009, 4:e4773.
196. Kim YC, Quan FS, Yoo DG, Compans RW, Kang SM, Prausnitz MR Enhanced memory responses to seasonal H1N1 influenza vaccination of the skin with the use of vaccine-coated microneedles. J Infect Dis 2010, 201:190-198.
197. Gill HS, Prausnitz MR Coating formulations for microneedles. Pharm Res 2007, 24:1369-1380.
198. Lee JW, Park JH, Prausnitz MR Dissolving microneedles for transdermal drug delivery. Biomaterials 2008, 29:2113-2124.