Immunogenicity of intramuscular MF59- Adjuvanted and intradermal administered influenza enhanced vaccines in subjects aged over 60: A literature review

Human Vaccines and Immunotherapeutics

Volumn 11, Issue 3, 2015, Pages 553-563

  Camilloni, Barbara ^a   Basileo, Michela ^a   Valente, Stefano ^b   Nunzi, Emilia ^a   Iorio, Anna Maria ^a  

^a UNIVERSITY OF PERUGIA   (Italy)

^b Sanofi Pasteur MSD   (Italy)

Author keywords

Adjuvanted vaccine; Elderly; Immunogenicity; Influenza vaccine; Intradermal vaccine; Potentiated vaccine

Indexed keywords

HEMAGGLUTININ; INFLUENZA VACCINE; MIFAMURTIDE; IMMUNOLOGICAL ADJUVANT; MF59 OIL EMULSION; POLYSORBATE; SQUALENE; VIRUS ANTIBODY;

ADJUVANT THERAPY; ANTIBODY RESPONSE; BIOASSAY; DRUG EFFICACY; DRUG POTENTIATION; DRUG SAFETY; DRUG TOLERABILITY; ERYTHEMA; HEMAGGLUTINATION INHIBITION; HUMAN; IMMUNOGENICITY; INFECTION PREVENTION; INFLAMMATION; INFLUENZA; INFLUENZA VACCINATION; INJECTION SITE INDURATION; INJECTION SITE PAIN; INJECTION SITE REACTION; INNATE IMMUNITY; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SEASONAL INFLUENZA; SEROCONVERSION; SEROLOGY; SWELLING; SYSTEMATIC REVIEW; AGED; BLOOD; COMPARATIVE STUDY; IMMUNOLOGY; INFLUENZA, HUMAN; INTRADERMAL DRUG ADMINISTRATION; INTRAMUSCULAR DRUG ADMINISTRATION; MIDDLE AGED; VERY ELDERLY;

ADJUVANTS, IMMUNOLOGIC; AGED; AGED, 80 AND OVER; ANTIBODIES, VIRAL; HUMANS; INFLUENZA VACCINES; INFLUENZA, HUMAN; INJECTIONS, INTRADERMAL; INJECTIONS, INTRAMUSCULAR; MIDDLE AGED; POLYSORBATES; SQUALENE;

EID: 84928680062     PISSN: 21645515     EISSN: 2164554X     Source Type: Journal    
DOI: 10.1080/21645515.2015.1011562     Document Type: Review

References (69)

1. Thompson WW, Shay DK, Weintraub E, Brammer L, Bridges CB, Cox NJ, Fukuda K. Influenza-associated hospitalizations in the United States. JAMA 2004; 292:1333-40; PMID:15367555; http://dx.doi.org/10.1001/jama.292.11.1333.
2. Thompson WW, Shay DK, Weintraub E, Brammer L, Cox N, Anderson LJ, Fukuda K. Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA 2003; 289:179-86; PMID:12517228; http://dx.doi.org/10.1001/jama.289.2.179.
3. Gaillat J, Dennetiere G, Raffin-Bru E, Valette M, Blanc MC. Summer influenza outbreak in a home for the elderly: application of preventive measures. J Hosp Infect 2008; 70:272-7; PMID:18799243; http://dx.doi.org/10.1016/j.jhin.2008.07.009.
4. Gasparini R, Pozzi T, Montomoli E, Fragapane E, Senatore F, Minutello M, Podda A. Increased immunogenicity of the MF59-adjuvanted influenza vaccine compared to a conventional subunit vaccine in elderly subjects. Eur J Epidemiol 2001; 17:135-40; PMID:11599686; http://dx.doi.org/10.1023/A:1017919305501.
5. McElhaney JE, Hooton JW, Hooton N, Bleackley RC. Comparison of single versus booster dose of influenza vaccination on humoral and cellular immune responses in older adults. Vaccine 2005; 23:3294-300; PMID:15837235; http://dx.doi.org/10.1016/j.vaccine.2005.01.080.
6. Grubeck-Loebenstein B, Della Bella S, Iorio AM, Michel JP, Pawelec G, Solana R. Immunosenescence and vaccine failure in the elderly. Aging Clin Exp Res 2009; 21:201-9; PMID:19571643; http://dx.doi.org/10.1007/BF03324904.
7. Durando P, Iudici R, Alicino C, Alberti M, de FD, Ansaldi F, Icardi G. Adjuvants and alternative routes of administration towards the development of the ideal influenza vaccine. Hum Vaccin 2011; 7 Suppl:29-40; PMID:21245655; http://dx.doi.org/10.4161/hv.7.0.14560.
8. Atmar RL, Patel SM, Keitel WA. Intanza(®): a new intradermal vaccine for seasonal influenza. Expert Rev Vaccines 2010; 9:1399-409; PMID:21105776; http://dx.doi.org/10.1586/erv.10.134.
9. Icardi G, Orsi A, Ceravolo A, Ansaldi F. Current evidence on intradermal influenza vaccines administered by Soluvia licensed micro injection system. Hum Vaccin Immunother 2012; 8:67-75; PMID:22293531; http://dx.doi.org/10.4161/hv.8.1.18419.
10. Committee for Medicinal Products for Human Use (CHMP). Guideline on clinical evaluation of new vaccines 2005. DHHS/FDA/CBER. Guidance for industry, clinical data needed to support the licensure of pandemic influenza vaccines, draft guidance 2006. 2013.
11. Podda A, Del Giudice G. MF59-adjuvanted vaccines: increased immunogenicity with an optimal safety profile. Expert Rev Vaccines 2003; 2:197-203; PMID:12899571; http://dx.doi.org/10.1586/14760584.2.2.197.
12. 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; PMID:20218923; http://dx.doi.org/10.1517/14712591003724662.
13. 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; PMID:17931151; http://dx.doi.org/10.1586/14760584.6.5.699.
14. Banzhoff A, Pellegrini M, Del Giudice G, Fragapane E, Groth N, Podda A. MF59-adjuvanted vaccines for seasonal and pandemic influenza prophylaxis. Influenza Other Respi Viruses 2008; 2:243-9; PMID:19453401; http://dx.doi.org/10.1111/j.1750-2659.2008.00059.x.
15. El-Sahly H. MF59TM as a vaccine adjuvant: a review of safety and immunogenicity. Expert Rev Vaccines 2010; 9:1135-41; PMID:20923265; http://dx.doi.org/10.1586/erv.10.111.
16. Bos JD, Kapsenberg ML. The skin immune system: progress in cutaneous biology. Immunol Today 1993; 14:75-8; PMID:8447935; http://dx.doi.org/10.1016/0167-5699(93)90062-P.
17. 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; PMID:15525714; http://dx.doi.org/10.1056/NEJMoa043540.
18. Palucka K, Banchereau J, Mellman I. Designing vaccines based on biology of human dendritic cell subsets. Immunity 2010; 33:464-78; PMID:21029958; http://dx.doi.org/10.1016/j.immuni.2010.10.007.
19. Reber AJ, Chirkova T, Kim JH, Cao W, Biber R, Shay DK, Sambhara S. Immunosenescence and challenges of vaccination against influenza in the aging population. Aging Dis 2012; 3:68-90; PMID:22500272.
20. Ueno H, Klechevsky E, Schmitt N, Ni L, Flamar AL, Zurawski S, Zurawski G, Palucka K, Banchereau J, Oh S. Targeting human dendritic cell subsets for improved vaccines. Semin Immunol 2011; 23:21-7; PMID:21277223; http://dx.doi.org/10.1016/j.smim.2011.01.004.
21. Nicolas JF, Guy B. Intradermal, epidermal and transcutaneous vaccination: from immunology to clinical practice. Expert Rev Vaccines 2008; 7:1201-14; PMID:18844594; http://dx.doi.org/10.1586/14760584.7.8.1201.
22. Lambert PH, Laurent PE. Intradermal vaccine delivery: will new delivery systems transform vaccine administration? Vaccine 2008; 26:3197-208; PMID:18486285; http://dx.doi.org/10.1016/j.vaccine.2008.03.095.
23. Kupper TS, Fuhlbrigge RC. Immune surveillance in the skin: mechanisms and clinical consequences. Nat Rev Immunol 2004; 4:211-22; PMID:15039758; http://dx.doi.org/10.1038/nri1310.
24. Pearton M, Kang SM, Song JM, Anstey AV, Ivory M, Compans RW, Birchall JC. Changes in human Langerhans cells following intradermal injection of influenza virus-like particle vaccines. PLoS One 2010; 5: e12410; PMID:20811642; http://dx.doi.org/10.1371/journal.pone.0012410.
25. Allenspach EJ, Lemos MP, Porrett PM, Turka LA, Laufer TM. Migratory and lymphoid-resident dendritic cells cooperate to efficiently prime naive CD4 T cells. Immunity 2008; 29:795-806; PMID:18951047; http://dx.doi.org/10.1016/j.immuni.2008.08.013.
26. Banzhoff A, Nacci P, Podda A. A new MF59-adjuvanted influenza vaccine enhances the immune response in the elderly with chronic diseases: results from an immunogenicity meta-analysis. Gerontology 2003; 49:177-84; PMID:12679609; http://dx.doi.org/10.1159/000069172.
27. Podda A. The adjuvanted influenza vaccines with novel adjuvants: experience with the MF59-adjuvanted vaccine. Vaccine 2001; 19:2673-80; PMID:11257408; http://dx.doi.org/10.1016/S0264-410X(00)00499-0.
28. Arnou R, Icardi G, De Decker M, Ambrozaitis A, Kazek MP, Weber F, Van Damme P. Intradermal influenza vaccine for older adults: a randomized controlled multicenter phase III study. Vaccine 2009; 27:7304-12; PMID:19849996; http://dx.doi.org/10.1016/j.vaccine.2009.10.033.
29. Holland D, Booy R, De Looze F, Eizenberg P, McDonald J, Karrasch J, McKeirnan M, Salem H, Mills G, Reid 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; PMID:18652550; http://dx.doi.org/10.1086/590434.
30. Van Damme P, Arnou R, Kafeja F, Fiquet A, Richard P, Thomas S, Meghlaoui G, Samson SI, Ledesma E. Evaluation of non-inferiority of intradermal versus adjuvanted seasonal influenza vaccine using two serological techniques: a randomised comparative study. BMC Infect Dis 2010; 10:134-45; PMID:20504306; http://dx.doi.org/10.1186/1471-2334-10-134.
31. Scheifele DW, McNeil SA, Ward BJ, Dionne M, Cooper C, Coleman B, Loeb M, Rubinstein E, McElhaney J, Hatchette T, et al. Safety, immunogenicity, and tolerability of three influenza vaccines in older adults: Results of a randomized, controlled comparison. Hum Vaccin Immunother 2013; 9:2460-73; PMID:23839537; http://dx.doi.org/10.4161/hv.25580.
32. Katz JM, Hancock K, Xu X. Serologic assays for influenza surveillance, diagnosis and vaccine evaluation. Expert Rev Anti Infect Ther 2011; 9:669-83; PMID:21692672; http://dx.doi.org/10.1586/eri.11.51.
33. Schild GC, Pereira MS, Chakraverty P. Single-radialhemolysis: a new method for the assay of antibody to influenza haemagglutinin. Applications for diagnosis and seroepidemiologic surveillance of influenza. Bull World Health Organ 1975; 52:43-50; PMID:1082381.
34. Coudeville L, Bailleux F, Riche B, Megas F, Andre P, Ecochard R. Relationship between haemagglutinationinhibiting antibody titres and clinical protection against influenza: development and application of a bayesian random-effects model. BMC Med Res Methodol 2010; 10:18-29; PMID:20210985; http://dx.doi.org/10.1186/1471-2288-10-18.
35. Ansaldi F, Bacilieri S, Durando P, Sticchi L, Valle L, Montomoli E, Icardi G, Gasparini R, Crovari P. Crossprotection by MF59-adjuvanted influenza vaccine: neutralizing and haemagglutination-inhibiting antibody activity against A(H3N2) drifted influenza viruses. Vaccine 2008; 26:1525-9; PMID:18294741; http://dx.doi.org/10.1016/j.vaccine.2008.01.019.
36. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, Moher D, Becker BJ, Sipe TA, Thacker SB. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 2000; 283:2008-12; PMID:10789670; http://dx.doi.org/10.1001/jama.283.15.2008.
37. Ansaldi F, Zancolli M, Durando P, Montomoli E, Sticchi L, Del Giudice G, Icardi G. 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; PMID:20433807; http://dx.doi.org/10.1016/j.vaccine.2010.04.030.
38. Baldo V, Menegon T, Bonello C, Floreani A, Trivello R. Comparison of three different influenza vaccines in institutionalised elderly. Vaccine 2001; 19:3472-5; PMID:11348713; http://dx.doi.org/10.1016/S0264-410X(01)00060-3.
39. Baldo V, Baldovin T, Floreani A, Minuzzo M, Trivello R. Response to influenza vaccine in people with nonprotective HI antibody titers. Eur J Epidemiol 2006; 21:843-5; PMID:17082899; http://dx.doi.org/10.1007/s10654-006-9071-4.
40. Baldo V, Baldovin T, Pellegrini M, Angiolelli G, Majori S, Floreani A, Busana MC, Bertoncello C, Trivello R. Immunogenicity of three different influenza vaccines against homologous and heterologous strains in nursing home elderly residents. Clin Dev Immunol 2010; 2010:517198; PMID:20369059; http://dx.doi.org/10.1155/2010/517198.
41. Basileo M, Iorio A, Bartolini G, Bianchini C, Menculini G, Tozzi P, Camilloni B. Comparative study of immunogenicity of split, intradermal and MF59-adjuvanted influenza vaccines in elderly institutionalized subjects. Procedia Vaccinol 2014; 18-23; http://dx.doi.org/10.1016/j.provac.2014.07.004.
42. 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; PMID:19410623; http://dx.doi.org/10.1016/j.vaccine.2009.04.078.
43. Camilloni B, Neri M, Lepri E, Basileo M, Sigismondi N, Puzelli S, Donatelli I, Iorio AM. An influenza B outbreak during the 2007/2008 winter among appropriately immunized elderly people living in a nursing home. Vaccine 2010; 28:7536-41; PMID:20846530; http://dx.doi.org/10.1016/j.vaccine.2010.08.064.
44. de Bruijn I, 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; PMID:18063446; http://dx.doi.org/10.1016/j.vaccine.2007.10.051.
45. De Donato S, Granoff D, Minutello M, Lecchi G, Faccini M, Agnello M, Senatore F, Verweij P, Fritzell B, Podda A. Safety and immunogenicity of MF59-adjuvanted influenza vaccine in the elderly. Vaccine 1999; 17:3094-101; PMID:10462245; http://dx.doi.org/10.1016/S0264-410X(99)00138-3.
46. Del Giudice G, Hilbert AK, Bugarini R, Minutello A, Popova O, Toneatto D, Schoendorf I, Borkowski A, Rappuoli R, Podda A. 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; PMID:16464520; http://dx.doi.org/10.1016/j.vaccine.2006.01.015.
47. Della Cioppa G, Nicolay U, Lindert K, Leroux-Roels G, Clement F, Castellino F, Galli G, Groth N, Del Giudice G. Superior immunogenicity of seasonal influenza vaccines containing full dose of MF59 ((®) adjuvant: results from a dose-finding clinical trial in older adults. Hum Vaccin Immunother 2012; 8:216-27; PMID:22426371; http://dx.doi.org/10.4161/hv.18445.
48. Iorio AM, Camilloni B, Basileo M, Guercini F, Conti S, Ferrante F, Paccamiccio E, Iaboni S, Vecchioli M, Iorio A. Influenza vaccination in patients on long-term anticoagulant therapy. Vaccine 2006; 24:6624-8; PMID:16828939; http://dx.doi.org/10.1016/j.vaccine.2006.05.036.
49. Iorio AM, Neri M, Lepri E, Camilloni B, Basileo M, Sigismondi N, Fabiani C, Calzoletti L, Puzelli S, Donatelli I. An influenza A/H3 outbreak during the 2004/2005 winter in elderly vaccinated people living in a nursing home. Vaccine 2006; 24:6615-9; PMID:16828941; http://dx.doi.org/10.1016/j.vaccine.2006.05.037.
50. Li R, Fang H, Li Y, Liu Y, Pellegrini M, Podda A. Safety and immunogenicity of an MF59-adjuvanted subunit influenza vaccine in elderly Chinese subjects. Immun Ageing 2008; 5:2-10; PMID:18289372; http://dx.doi.org/10.1186/1742-4933-5-2.
51. Minutello M, Senatore F, Cecchinelli G, Bianchi M, Andreani T, Podda A, Crovari P. 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; PMID:9987141; http://dx.doi.org/10.1016/S0264-410X(98)00185-6.
52. Pregliasco F, Mensi C, Serpilli W, Speccher L, Masella P, Belloni A. Immunogenicity and safety of three commercial influenza vaccines in institutionalized elderly. Aging (Milano) 2001; 13:38-43; PMID:11292151.
53. 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 virosomebased subunit vaccine in elderly. Infection 2004; 32:191-8; PMID:15293073; http://dx.doi.org/10.1007/s15010-004-3204-z.
54. Sindoni D, La Fauci V, Squeri R, Cannavo G, Bacilieri S, Panatto D, Gasparini R, Amicizia D. Comparison between a conventional subunit vaccine and the MF59- Adjuvanted subunit influenza vaccine in the elderly: an evaluation of the safety, tolerability and immunogenicity. J Prev Med Hyg 2009; 50:121-6; PMID:20099444.
55. Song JY, Cheong HJ, Noh JY, Seo YB, Choi WS, Cho GJ, Hwang TG, KimWJ. Long-term and cross-reactive immunogenicity of inactivated trivalent influenza vaccine in the elderly: MF59-adjuvanted vaccine versus unadjuvanted vaccine. J Med Virol 2013; 85:1591-7; PMID:23852684; http://dx.doi.org/10.1002/jmv.23630.
56. 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; PMID:12559808; http://dx.doi.org/10.1016/S0264-410X(02)00401-2.
57. Camilloni B, Basileo M, Di Martino A, Donatelli I, Iorio AM. Antibody responses to intradermal or intramuscular MF59-adjuvanted influenza vaccines as evaluated in elderly institutionalized volunteers during a season of partial mismatching between vaccine and circulating A(H3N2) strains. Immun Ageing 2014; 11:10; PMID:24860610; http://dx.doi.org/10.1186/1742-4933-11-10.
58. Ansaldi F, Canepa P, Ceravolo A, Valle L, de Florentiis D, Oomen R, Vogel FR, Denis M, Samson SI, Icardi G. Intanza (®) 15 mcg intradermal influenza vaccine elicits cross-reactive antibody responses against heterologous A(H3N2) influenza viruses. Vaccine 2012; 30:2908-13; PMID:22342501; http://dx.doi.org/10.1016/j.vaccine.2012.02.003.
59. Ansaldi F, Orsi A, de Florentiis D, Parodi V, Rappazzo E, Coppelli M, Durando P, Icardi G. Head-to-head comparison of an intradermal and a virosome influenza vaccine in patients over the age of 60: Evaluation of immunogenicity, cross-protection, safety and tolerability. Hum Vaccin Immunother 2013; 9:591-8; PMID:23295262; http://dx.doi.org/10.4161/hv.23240.
60. Tsang P, Gorse GJ, Strout CB, Sperling M, Greenberg DP, Ozol-Godfrey A, Diazgranados C, Landolfi V. Immunogenicity and safety of Fluzone intradermal and high-dose influenza vaccines in older adults >/=65 years of age: A randomized, controlled, phase II trial. Vaccine 2013; 32:2507-17; PMID:24120672; http://dx.doi.org/10.1016/j.vaccine.2013.09.074.
61. Carrat F, Flahault A. Influenza vaccine: The challenge of antigenic drift. Vaccine 2007; 25:6852-62; PMID:17719149; http://dx.doi.org/10.1016/j.vaccine.2007.07.027.
62. McCullers JA, Saito T, Iverson AR. Multiple genotypes of influenza B virus circulated between 1979 and 2003. J Virol 2004; 78:12817-28; PMID:15542634; http://dx.doi.org/10.1128/JVI.78.23.12817-12828.2004.
63. Reed C, Meltzer MI, Finelli L, Fiore A. Public health impact of including two lineages of influenza B in a quadrivalent seasonal influenza vaccine. Vaccine 2012; 30:1993-8; PMID:22226861; http://dx.doi.org/10.1016/j.vaccine.2011.12.098.
64. Iorio AM, Camilloni B, Basileo M, Neri M, Lepri E, Spighi M. Effects of repeated annual influenza vaccination on antibody responses against unchanged vaccine antigens in elderly frail institutionalized volunteers. Gerontology 2007; 53:411-8; PMID:17975317; http://dx.doi.org/10.1159/000110579.
65. Keitel WA, Cate TR, Couch RB. Efficacy of sequential annual vaccination with inactivated influenza virus vaccine. Am J Epidemiol 1988; 127:353-64; PMID:3337087.
66. Kendal AP, Cate TR. Increased sensitivity and reduced specificity of hemagglutination inhibition tests with ether-treated influenza B/Singapore/222/79. J Clin Microbiol 1983; 18:930-4; PMID:6630472.
67. Monto AS, Maassab HF. Ether treatment of type B influenza virus antigen for the hemagglutination inhibition test. J Clin Microbiol 1981; 13:54-7; PMID:7462419.
68. McElhaney JE. Influenza vaccine responses in older adults. Ageing Res Rev 2011; 10:379-88; PMID:21055484; http://dx.doi.org/10.1016/j.arr.2010.10.008.
69. Public Health Agency of Canada. Statement on seasonal influenza vaccine for 2012-2013. Canada Communicable Disease Report 38 ACS-2. 2012.