Adjuvants and alternative routes of administration towards the development of the ideal influenza vaccine

Human Vaccines

Volumn 7, Issue SUPPL., 2011, Pages 29-40

  Durando, Paolo ^a,b   Iudici, Rocco ^a   Alicino, Cristiano ^a   Alberti, Marisa ^a   De Florentis, Daniela ^a   Ansaldi, Filippo ^a,b   Icardi, Giancarlo ^a,b  

^a UNIVERSITY OF GENOA   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

Author keywords

Adjuvants; Cross reactivity; Immunogenicity; Influenza vaccines; Intradermal administration; MF59 oil in water emulsion; Microinjection system; Universal vaccine

Indexed keywords

DNA VACCINE; INFLUENZA VACCINE; INFLUENZA VIRUS HEMAGGLUTININ; LIVE VACCINE; MIFAMURTIDE;

CELL CULTURE; CROSS REACTION; DNA IMMUNIZATION; DRUG DOSAGE FORM COMPARISON; DRUG FEVER; DRUG FORMULATION; DRUG INDUCED HEADACHE; DRUG POTENCY; DRUG SAFETY; DRUG SCREENING; DRUG SYNTHESIS; GENETIC IMMUNIZATION; HUMAN; IMMUNE RESPONSE; IMMUNOGENICITY; INJECTION SITE ERYTHEMA; INJECTION SITE INDURATION; INJECTION SITE PAIN; INNATE IMMUNITY; MALAISE; MICROINJECTION; MYALGIA; NONHUMAN; REVIEW; SEASONAL INFLUENZA; VIRUS LOAD;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; HUMANS; INFLUENZA VACCINES; INFLUENZA, HUMAN; INJECTIONS, INTRADERMAL; POLYSORBATES; SQUALENE; VACCINATION;

EID: 80052916947     PISSN: 15548600     EISSN: 15548619     Source Type: Journal    
DOI: 10.4161/hv.7.0.14560     Document Type: Review

References (120)

1. Sprenger MJ, Mulder PG, Beyer WE, Van Strik R, Masurel N. Impact of influenza on mortality in relation to age and underlying disease 1967-1989. Int J Epidemiol 1993; 22:334-40.
2. Thompson WW, Shay DK, Weintraub E, Brammer L, Bridges CB, Cox NJ, et al. Influenza-associated hospitalizations in the United States. JAMA 2004; 292:1333-40. (Pubitemid 39223224)
3. Fleming D, Harcourt S, Smith G. Influenza and adult hospital admissions for respiratory conditions in England 1989-2001. Commun Dis Public Health 2003; 6:231-7.
4. Thompson WW, Shay DK, Weintraub E, Brammer L, Cox N, Anderson LJ, et al. Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA 2003; 289:179-86. (Pubitemid 36068705)
5. Gavazzi G, Krause KH. Ageing and infection. Lancet Infect Dis 2002; 2:659-66. (Pubitemid 35265061)
6. World Health Organization (WHO). Influenza vaccines. Wkly Epidemiol Rec 2005; 80:279-87.
7. Centers for Disease Control and Prevention. Prevention and control of seasonal influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2010. MMWR 2010; 59:1-62.
8. th ed. Washington DC: Public Health Foundation 2007; 235-56.
9. Fedson DS. Preparing for pandemic vaccination: an international policy agenda for vaccine development. J Public Health Policy 2005; 26:4-29. (Pubitemid 40632275)
10. Nichol KL. The efficacy, effectiveness and cost-effectiveness of inactivated influenza virus vaccines. Vaccine 2003; 21:1769-75. (Pubitemid 36398371)
11. Vu T, Farish S, Jenkins M, Kelly H. A meta-analysis of effectiveness of influenza vaccine in persons aged 65 years and over living in the community. Vaccine 2002; 20:1831-6. (Pubitemid 34242840)
12. st century: Optimizing protection of older adults. Vaccine 2009; 27:5043-53.
13. Kroon FP, van Dissel JT, de Jong JC, Zwinderman K, van Furth R. Antibody response after influenza vaccination in HIV-infected individuals: a consecutive 3 year study. Vaccine 2000; 18:3040-9. (Pubitemid 30303809)
14. Dorrell L, Hassan I, Marshall S, Chakraverty P, Ong E. Clinical and serological responses to an inactivated influenza vaccine in adults with HIV infection, diabetes, obstructive airways disease, elderly adults and healthy volunteers. Int J STD AIDS 1997; 8:776-9. (Pubitemid 27523764)
15. Blumberg EA, Albano C, Pruett T, Isaacs R, Fitzpatrick J, Bergin J, et al. The immunogenicity of influenza virus vaccine in solid organ transplant recipients. Clin Infect Dis 1996; 22:295-302. (Pubitemid 26056158)
16. European Centre for Disease Prevention and Control (ECDC). Technical report on the scientific panel on vaccines and immunization. Infant and children seasonal immunization against influenza on a routine basis during inter-pandemic period. Stockholm 2007. Available at: www.ecdc.europa.eu/ documents/pdf/Flu-vacc-18-Jan.pdf; [Last accessed 8 September 2010].
17. Ansaldi F, Bacilieri S, Durando P, Sticchi L, Valle L, Montomoli E, et al. Cross-protection by MF59-adjuvanted influenza vaccine: neutralizing and hemagglutination-inhibiting antibody activity against A(H3N2) drifted influenza viruses. Vaccine 2008; 26:1525-9.
18. Ansaldi F, Canepa P, Parodi V, Bacilieri S, Orsi A, Compagnino F, et al. Adjuvanted seasonal influenza vaccines and perpetual viral metamorphosis: the importance of cross-protection. Vaccine 2009; 27:3345-8.
19. Goodwin K, Viboud C, Simonsen L. Antibody response to influenza vaccination in the elderly: a quantitative review. Vaccine 2006; 24:1159-69. (Pubitemid 43202262)
20. Jefferson T, Di Pietrantonj C, Al-Ansary LA, Ferroni E, Thorning S, Thomas RE. Vaccines for preventing influenza in the elderly. Cochrane Database Syst Rev 2010; 2:4876.
21. Carrat F, Flahault A. Influenza vaccine: The challenge of antigenic drift. Vaccine 2007; 25:6852-62.
22. de Jong JC, Beyer WE, Palache AM, Rimmelzwaan GF, Osterhaus AD. Mismatch between the 1997/1998 influenza vaccine and the major epidemic A(H3N2) virus strain as the cause of an inadequate vaccine-induced antibody response to this strain in the elderly. J Med Virol 2000; 61:94-9.
23. Baldo V, Baldovin T, Floreani A, Fragapane E, Trivello R. Family Medicine Group. Response of influenza vaccines against heterovariant influenza virus strains in adults with chronic diseases. J Clin Immunol 2007; 27:542-7. (Pubitemid 47319253)
24. Ansaldi F, Icardi G, Gasparini R, Campello C, Puzelli S, Bella A, et al. New A/H3N2 influenza variant: a small genetic evolution but a heavy burden on the Italian population during the 2004-2005 season. J Clin Microbiol 2005; 43:3027-9. (Pubitemid 40828007)
25. Legrand J, Vergu E, Flahault A. Real-time monitoring of the influenza vaccine field effectiveness. Vaccine 2006; 24:6605-11. (Pubitemid 46127433)
26. Skowronski DM, Masaro C, Kwindt TL, Mak A, Petric M, Li Y, et al. Estimating vaccine effectiveness against laboratory-confirmed influenza using a sentinel physician network: results from the 2005-2006 season of dual A and B vaccine mismatch in Canada. Vaccine 2007; 25:2842-51. (Pubitemid 46412567)
27. Ellebedy AH, Webby RJ. Influenza vaccines. Vaccine 2009; 27:65-8.
28. Herzog C, Hartmann K, Künzi V, Kürsteiner O, Mischler R, Lazar H, et al. Eleven years of Inflexal V-a virosomal adjuvanted influenza vaccine. Vaccine 2009; 27:4381-7.
29. Calcagnile S, Zuccotti GV. The virosomal adjuvanted influenza vaccine. Expert Opin Biol Ther 2010; 10:191-200.
30. Durando P, Icardi G, Ansaldi F. MF59-adjuvanted vaccine: a safe and useful tool to enhance and broaden protection against seasonal influenza viruses in subjects at risk. Expert Opin Biol Ther 2010; 10:639-51.
31. Podda A, Del Giudice G. MF59-adjuvanted vaccines: increased immunogenicity with an optimal safety profile. Expert Rev Vaccines 2003; 2:197-203.
32. Pellegrini M, Nicolay U, Lindert K, Groth N, Della Cioppa G. MF59-adjuvanted versus non-adjuvanted influenza vaccines: integrated analysis from a large safety database. Vaccine 2009; 27:6959-65.
33. Schultze V, D'Agosto V, Wack A, Novicki D, Zorn J, Hennig R. Safety of MF59 adjuvant. Vaccine 2008; 26:3209-22.
34. Ruf BR, Colberg K, Frick M, Preusche A. Open, randomized study to compare the immunogenicity and reactogenicity of an influenza split vaccine with an MF59-adjuvanted subunit vaccine and a virosome-based subunit vaccine in elderly. Infection 2004; 32:191-8. (Pubitemid 39070597)
35. Baldo V, Menegon T, Bonello C, Floreani A, Trivello R. Collaborative Group. Comparison of three different influenza vaccines in institutionalised elderly. Vaccine 2001; 19:3472-560.
36. Pregliasco F, Mensi C, Serpilli W, Speccher L, Masella P, Belloni A. Immunogenicity and safety of three commercial influenza vaccines in institutionalized elderly. Aging 2001; 13:38-43.
37. de Bruijn IA, Meyer I, Gerez L, Nauta J, Giezeman K, Palache B. Antibody induction by virosomal, MF59-adjuvanted or conventional influenza vaccines in the elderly. Vaccine 2007; 26:119-27.
38. Baldo V, Baldovin T, Pellegrini M, Angiolelli G, Majori S, Floreani A, et al. Immunogenicity of three different influenza vaccines against homologous and heterologous strains in nursing home elderly residents. Clin Dev Immunol 2010; 2010:517198.
39. Nicholson KG, Colegate AE, Podda A, Stephenson I, Wood J, Ypma E, et al. Safety and antigenicity of non-adjuvanted and MF59-adjuvanted influenza A/Duck/Singapore/97 (H5N3) vaccine: a randomized trial of two potential vaccines against H5N1 influenza. Lancet 2001; 357:1937-43. (Pubitemid 32568336)
40. Clark TW, Pareek M, Hoschler K, Dillon H, Nicholson KG, Groth N, et al. Trial of 2009 influenza A (H1N1) monovalent MF59-adjuvanted vaccine. N Engl J Med 2009; 361:2424-35.
41. Gasparini R, Schioppa F, Lattanzi M, Barone M, Casula D, Pellegrini M, et al. Impact of prior or concomitant seasonal influenza vaccination on MF59-adjuvanted H1N1v vaccine (Focetria) in adult and elderly subjects. Int J Clin Pract 2010; 64:432-8.
42. Chu DW, Hwang SJ, Lim FS, Oh HM, Thongcharoen P, Yang PC, et al. H5N1 Flu Study Group for Hong Kong, Singapore, Taiwan and Thailand. Immunogenicity and tolerability of an AS03(A)-adjuvanted prepandemic influenza vaccine: a phase III study in a large population of Asian adults. Vaccine 2009; 27:7428-35.
43. Roman F, Vaman T, Gerlach B, Markendorf A, Gillard P, Devaster JM. Immunogenicity and safety in adults of one dose of influenza A H1N1v 2009 vaccine formulated with and without AS03A-adjuvant: preliminary report of an observer-blind, randomised trial. Vaccine 2010; 28:1740-5.
44. Leroux-Roels I, Roman F, Forgus S, Maes C, De Boever F, Dramé M, et al. Priming with AS03A-adjuvanted H5N1 influenza vaccine improves the kinetics, magnitude and durability of the immune response after a heterologous booster vaccination: an open nonrandomised extension of a double-blind randomised primary study. Vaccine 2010; 28:849-57.
45. Leroux-Roels I, Clement F, Leroux-Roels G, Dramé M, Moris P, Devaster JM, et al. Adjuvanted influenza vaccines improve anti-influenza cellular mediated immunity impaired in elderly. Poster presented at: Influenza Vaccines for the World, October 18-20, 2006; Vienna, Austria.
46. Leroux-Roels I, Oostvogels L, Hons E, Leroux-Roels G, Devaster J-M, Ripley Ballou W. Reactogenicity and safety of adjuvanted influenza vaccines administered in elderly. Poster presented at: Influenza Vaccines for the World, October 18-20, 2006; Vienna, Austria.
47. Wareing MD, Tannock GA. Live attenuated vaccine against influenza; an historical review. Vaccine 2001; 19:3320-30. (Pubitemid 32710280)
48. Rhorer J, Ambrose CS, Dickinson S, Hamilton H, Oleka NA, Malinoski FJ, et al. Efficacy of live attenuated influenza vaccine in children: A meta-analysis of nine randomized clinical trials. Vaccine 2009;27:1101-10.
49. Belshe RB, Edwards KM, Vesikari T, Black SV, Walker RE, Hultquist M, et al. CAIV-T Comparative Efficacy Study Group. Live attenuated versus inactivated influenza vaccine in infants and young children. N Engl J Med 2007; 356:685-96.
50. Belshe R, Lee MS, Walker RE, Stoddard J, Mendelman PM. Safety, immunogenicity and efficacy of intranasal, live attenuated influenza vaccine. Expert Rev Vaccines 2004; 3:643-54. (Pubitemid 39576751)
51. Ohmit SE, Victor JC, Rotthoff JR, Teich ER, Truscon RK, Baum LL, et al. Prevention of antigenically drifted influenza by inactivated and live attenuated vaccines. N Engl J Med 2006; 355:2513-22. (Pubitemid 44917499)
52. Assessment report as adopted by the CHMP with all information of a commercially confidential nature deleted. Available from: www.emea.europa.eu/ human-docs/PDFs/EPAR/intanza/H-957-en6.pdf; [Last accessed 14 September 2010].
53. Genzel Y, Reichl U. Continuous cell lines as a production system for influenza vaccines. Expert Rev Vaccines 2009; 8:1681-92.
54. Barrett PN, Portsmouth D, Ehrlich HJ. Developing cell culture-derived pandemic vaccines. Curr Opin Mol Ther 2010; 12:21-30.
55. Liu J, Shi X, Schwartz R, Kemble G. Use of MDCK cells for production of live attenuated influenza vaccine. Vaccine 2009; 27:6460-3.
56. Doroschenko A, Halperin SA. Trivalent MDCK cell culture-derived influenza vaccine Optaflu (Novartis Vaccines). Expert Rev Vaccines 2009; 8:679-88.
57. Webby RJ, Perez DR, Coleman JS, Guan Y, Knight JH, Govorkova EA, et al. Responsiveness to a pandemic alert: use of reverse genetics for rapid development of influenza vaccines. Lancet 2004; 363:1099-103. (Pubitemid 38452781)
58. Marsh GA, Tannock GA. The role of reverse genetics in the development of vaccines against respiratory viruses. Expert Opin Biol Ther 2005; 5:369-80. (Pubitemid 40516747)
59. Subbarao K, Katz JM. Influenza vaccines generated by reverse genetics. Curr Top Microbiol Immunol 2004; 283:313-42. (Pubitemid 38667564)
60. Palese P. Making better influenza virus vaccines? Emerg Infect Dis 2006; 12:61-5. (Pubitemid 43143537)
61. Kaiser J. A one-size-fits-all flu vaccine. Science 2006; 312:380-2.
62. Kodihalli S, Kobasa DL, Webster RG. Strategies for inducing protection against avian influenza A virus subtypes with DNA vaccines. Vaccine 2000; 18:2592-9. (Pubitemid 30207044)
63. Kim JH, Jacob J. DNA vaccines against influenza viruses. Curr Top Microbiol Immunol 2009; 333:197-210.
64. Yager EJ, Dean HJ, Fuller DH. Prospects for developing an effective particle-mediated DNA vaccine against influenza. Expert Rev Vaccines 2009; 8:1205-20.
65. O'Hagan DT. MF59 is a safe and potent vaccine adjuvant that enhances protection against influenza virus infection. Expert Rev Vaccines 2007; 6:699-710. (Pubitemid 47607847)
66. 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 2007; 82:740-4. (Pubitemid 350114825)
67. Mosca F, Tritto E, Muzzi A, Monaci E, Bagnoli F, Iavarone C, et al. Molecular and cellular signatures of human vaccine adjuvants. Proc Natl Acad Sci USA 2008; 105:10501-6.
68. Barberà JP. MF59-adjuvanted seasonal influenza vaccine. Aging health 2009; 5:475-81.
69. European Medicines Agency (EMA). Focetria, pandemic influenza vaccine (surface antigen, inactivated, adjuvanted) A/California/7/2009 (H1N1). Available at www.emea.europa.eu/influenza/vaccines/focetria/focetria-pi.html; [Last accessed 2 September 2010.
70. European Medicines Agency (EMA). Twenty-second pandemic pharmacovigilance update. Available at www.ema.europa.eu/docs/en-GB/document-library/Report/2010/ 08/WC500095870.pdf; [Last accessed 14 September 2010].
71. Podda A. The adjuvanted influenza vaccines with novel adjuvants: experience with the MF59-adjuvanted vaccine. Vaccine 2001; 19:2673-80. (Pubitemid 32234288)
72. Tsai T, Kyaw MH, Novicki D, Nacci P, Rai S, Clemens R. Exposure to MF59-adjuvanted influenza vaccines during pregnancy - a retrospective analysis. Vaccine 2010; 28:1877-80.
73. Gasparini R, Pozzi T, Montomoli E, Fragapane E, Senatore F, Minutello M, et al. Increased immunogenicity of the MF59-adjuvanted influenza vaccine compared to a conventional subunit vaccine in elderly subjects. Eur J Epidemiol 2001; 17:135-40. (Pubitemid 32900039)
74. Squarcione S, Sgricia S, Biasio LR, Perinetti E. Comparison of the reactogenicity and immunogenicity of a split and a subunit-adjuvanted influenza vaccine in elderly subjects. Vaccine 2003; 21:1268-74. (Pubitemid 36139959)
75. Minutello M, Senatore F, Cecchinelli G, Bianchi M, Andreani T, Podda A, et al. Safety and immunogenicity of an inactivated subunit influenza virus vaccine combined with MF59 adjuvant emulsion in elderly subjects, immunized for three consecutive influenza seasons. Vaccine 1999; 17:99-104. (Pubitemid 28494106)
76. Baldo V, Baldovin T, Floreani A, Carraro AM, Trivello R. Family Medicine Group of Pianiga. MF59-adjuvanted influenza vaccine confers superior immunogenicity in adult subjects (18-60 years of age) with chronic diseases who are at risk of post-influenza complications. Vaccine 2007; 25:3955-61. (Pubitemid 46616991)
77. Banzhoff A, Nacci P, Podda A. A new MF59-adjuvanted influenza vaccine enhanced the immune response in the elderly with chronic diseases: results from an immunogenicity meta-analysis. Gerontology 2003; 49:177-84. (Pubitemid 36438758)
78. Durando P, Fenoglio D, Boschini A, Ansaldi F, Icardi G, Sticchi L, et al. Safety and immunogenicity of two influenza virus subunit vaccines, with or without MF59 adjuvant, administered to human immunodeficiency virus type 1-seropositive and -seronegative adults. Clin Vaccine Immunol 2008; 15:253-9. (Pubitemid 352025530)
79. Iorio AM, Francisci D, Camilloni B, Stagni G, De Martino M, Toneatto D, et al. Antibody responses and HIV-1 viral load in HIV-1-seropositive subjects immunised with either the MF59-adjuvanted influenza vaccine or a conventional non-adjuvanted subunit vaccine during highly active anti-retroviral therapy. Vaccine 2003; 21:3629-37. (Pubitemid 37338187)
80. Paschke R, Pollok M, Geiger H, Ketteler M, Abendroth D, Gunther M, et al. Increased immunogenicity with an MF59-adjuvanted influenza vaccine compared to a conventional subunit vaccine in renal transplant recipients. J Prev Med Hyg 2003; 44:79-84.
81. Gabutti G, Guido M, Durando P, De Donno A, Quattrocchi M, Bacilieri S, et al. Safety and immunogenicity of conventional subunit and MF59-adjuvanted influenza vaccines in human immunodeficiency virus-1-seropositive patients. J Int Med Res 2005; 33:406-16. (Pubitemid 41057438)
82. Vesikari T, Pellegrini M, Karvonen A, Groth N, Borkowski A, O'Hagan DT, et al. Enhanced immunogenicity of seasonal influenza vaccines in young children using MF59 adjuvant. Pediatr Infect Dis J 2009; 28:563-71.
83. Vesikari T, Groth N, Karvonen A, Borkowski A, Pellegrini M. MF59-adjuvanted influenza vaccine (FLUAD) in children: safety and immunogenicity following a second year seasonal vaccination. Vaccine 2009; 27:6291-5.
84. Ansaldi F, Zancolli M, Durando P, Montomoli E, Sticchi L, Del Giudice G, et al. Antibody response against heterogeneous circulating influenza virus strains elicited by MF59- and non-adjuvanted vaccines during seasons with good or partial matching between vaccine strain and clinical isolates. Vaccine 2010; 28:4123-9.
85. Del Giudice G, Hilbert AK, Bugarini R, Minutello A, Popova O, Toneatto D, et al. An MF59-adjuvanted inactivated influenza vaccine containing A/Panama/1999 (H3N2) induced broader serological protection against heterovariant influenza virus strain A/Fujian/2002 than a subunit and a split influenza vaccine. Vaccine 2006; 24:3063-5.
86. Camilloni B, Neri M, Lepri E, Iorio AM. Cross-reactive antibodies in middle-aged and elderly volunteers after MF59-adjuvanted subunit trivalent influenza vaccine against B viruses of the B/Victoria or B/Yamagata lineages. Vaccine 2009; 27:4099-103.
87. Stephenson I, Bugarini R, Nicholson KG, Podda A, Wood JM, Zambon MC, et al. Cross-reactivity to highly pathogenic avian influenza H5N1 viruses after vaccination with non-adjuvanted and MF59-adjuvanted influenza A/Duck/Singapore/97 (H5N3) vaccine: a potential priming strategy. J Infect Dis 2005; 19:1210-5.
88. Banzhoff A, Gasparini R, Laghi-Pasini F, Staniscia T, Durando P, Montomoli E, et al. MF59-adjuvanted H5N1 vaccine induces immunologic memory and heterotypic antibody responses in non-elderly and elderly adults. PLoS One 2009; 4:4384.
89. Stephenson I, Nicholson KG, Hoschler K, Zambon MC, Hancock K, DeVos J, et al. Antigenically distinct MF59-adjuvanted vaccine to boost immunity to H5N1. N Engl J Med 2008; 359:1631-3.
90. Galli G, Hancock K, Hoschler K, DeVos J, Praus M, Bardelli M, et al. Fast rise of broadly cross-reactive antibodies after boosting long-lived human memory B cells primed by an MF59 adjuvanted prepandemic vaccine. Proc Natl Acad Sci USA 2009; 106:7962-7.
91. Fragapane E, Gasparini R, Schioppa F, Laghi-Pasini F, Montomoli E, Banzhoff A. A heterologous MF59(R)-adjuvanted H5N1 prepandemic influenza booster vaccine induces a robust, cross-reactive immune response in adults and the elderly. Clin Vaccine Immunol 2010; 17:1817-9.
92. Puig-Barberà J, Díez-Domingo J, Pérez Hoyos S, Belenguer Varea A, González Vidal D. Effectiveness of the MF59-adjuvanted influenza vaccine in preventing emergency admissions for pneumonia in the elderly over 64 years of age. Vaccine 2004; 23:283-9. (Pubitemid 39463043)
93. Puig-Barberà J, Díez-Domingo J, Varea AB, Chavarri GS, Rodrigo JA, Hoyos SP, et al. Effectiveness of MF59-adjuvanted subunit influenza vaccine in preventing hospitalisations for cardiovascular disease, cerebrovascular disease and pneumonia in the elderly. Vaccine 2007; 25:7313-21.
94. Iob A, Brianti G, Zamparo E, Gallo T. Evidence of increased clinical protection of an MF59-adjuvant influenza vaccine compared to a non-adjuvanted vaccine among elderly residents of long-term care facilities in Italy. Epidemiol Infect 2005; 133:687-93. (Pubitemid 41015560)
95. Nicolas JF, Guy B. Intradermal, epidermal and transcutaneous vaccination: from immunology to clinical practice. Expert Rev Vaccines 2008; 7:1201-14.
96. Lambert PH, Laurent PE. Intradermal vaccine delivery: will new delivery systems transform vaccine administration? Vaccine 2008; 26:3197-208.
97. Allan RS, Waithman J, Bedoui S, Jones CM, Villadangos JA, Zhan Y, et al. Migratory dendritic cells transfer antigen to a lymph node-resident dendritic cell population for efficient CTL priming. Immunity 2006; 25:153-62. (Pubitemid 44066832)
98. Sticchi L, Alberti M, Alicino C, Crovari P. The intradermal vaccination: past experiences and current perspectives. J Prev Med Hyg 2010; 51:7-14.
99. Holland D, Booy R, De Looze F, Eizenberg P, McDonald J, Karrasch J, 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; 198:650-8.
100. Arnou R, Icardi G, De Decker M, Ambrozaitis A, Kazek MP, Weber F, et al. Intradermal influenza vaccine for older adults: a randomized controlled multicenter phase III study. Vaccine 2009; 27:7304-12.
101. Leroux-Roels I, Vets E, Freese R, Seiberling M, Weber F, Salamand C, et al. Seasonal influenza vaccine delivered by intradermal microinjection: a randomized controlled safety and immunogenicity trial in adults. Vaccine 2008; 26:6614-9.
102. Beran J, Ambrozaitis A, Laiskonis A, Mickuviene N, Bacart P, Calozet Y, et al. Intradermal influenza vaccination of healthy adults using a new microinjection system: a 3 year randomized controlled safety and immunogenicity trial. BMC Med 2009; 7:13.
103. Reygrobellet C, Viala-Danten M, Meunier J, Weber F, Nguyen VH. Perception and acceptance of intradermal influenza vaccination: Patient reported outcomes from phase 3 clinical trials. Hum Vaccin 2010; 6:336-45.
104. Laurent PE, Bonnet S, Alchas P, Regolini P, Mikszta JA, Pettis R, et al. Evaluation of the clinical performance of a new intradermal vaccine administration technique and associated delivery system. Vaccine 2007; 25:8833-42. (Pubitemid 350192056)
105. Belshe RB, Newman FK, Cannon J, Duane C, Treanor J, Van Hoecke C, et al. Serum antibody responses after intradermal vaccination against influenza. N Engl J Med 2004; 351:2286-94. (Pubitemid 39552744)
106. Kenney RT, Frech SA, Muenz LR, Villar CP, Glenn GM. Dose sparing with intradermal injection of influenza vaccine. N Engl J Med 2004; 351:2295-301. (Pubitemid 39552745)
107. Auewarakul P, Kositanont U, Sornsathapornkul P, Tothong P, Kanyok R, Thongcharoen P. Antibody responses after dose-sparing intradermal influenza vaccination. Vaccine 2007; 25:659-63. (Pubitemid 44856109)
108. Belshe RB, Newman FK, Wilkins K, Graham IL, Babusis E, Ewell M, et al. Comparative immunogenicity of trivalent influenza vaccine administered by intradermal or intramuscular route in healthy adults. Vaccine 2007; 25:6755-63. (Pubitemid 47332726)
109. 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; 27:454-9.
110. 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; 6:346-54.
111. European Committee for Proprietary Medicinal Products (CPMP). Note for guidance on harmonization of requirements for influenza vaccines. CPMP/BWP/214/96. Available at: http://www.emea.europa.eu/pdfs/human/bwp/ 021496en.pdf; [Last accessed 7 September 2010].
112. Van Damme P, Arnou R, Kafeja F, Fiquet A, Richard P, Thomas S, et al. Evaluation of non-inferiority of intradermal versus adjuvanted seasonal influenza vaccine using two serological techniques: a randomized comparative study. BMC Infect Dis 2010; 10:134.
113. Jo YM, Song JY, Hwang IS, Lee J, Oh SC, Kim JS, et al. Dose sparing strategy with intradermal influenza vaccination in patients with solid cancer. J Med Virol 2009; 81:722-7.
114. Gelinck LB, van den Bemt BJ, Marijt WA, van der Bijl AE, Visser LG, Cats HA, et al. Intradermal influenza vaccination in immunocompromized patients is immunogenic and feasible. Vaccine 2009; 27:2469-74.
115. Morelon E, Noble CP, Daoud S, Cahen R, Goujon-Henry C, Weber F, et al. Immunogenicity and safety of intradermal influenza vaccination in renal transplant patients who were non-responders to conventional influenza vaccination. Vaccine 2010; 28:6885-90.
116. Chuaychoo B, Wongsurakiat P, Nana A, Kositanont U, Maranetra KN. The immunogenicity of intradermal influenza vaccination in COPD patients. Vaccine 2010; 28:4045-51.
117. Cassone A, Rappuoli R. Universal vaccines: shifting to one for many. MBio 2010; 1:42.
118. Epstein SL, Kong WP, Misplon JA, Lo CY, Tumpey TM, Xu L, et al. Protection against multiple influenza A subtypes by vaccination with highly conserved nucleoprotein. Vaccine 2005; 23:5404-10. (Pubitemid 41579312)
119. Steel J, Lowen AC, Wang T, Yondola M, Gao Q, Haye K, et al. Influenza virus vaccine based on the conserved hemagglutinin stalk domain. MBio 2010; 1:18.
120. Schotsaert M, De Filette M, Fiers W, Saelens X. Universal M2 ectodomain-based influenza A vaccines: preclinical and clinical developments. Expert Rev Vaccines 2009; 8:499-508.