Vaccine adjuvants: From 1920 to 2015 and beyond

Vaccines

Volumn 3, Issue 2, 2015, Pages 320-343

  Di Pasquale, Alberta ^a   Preiss, Scott ^a   Da Silva, Fernanda Tavares ^a   Garçon, Nathalie ^b  

^a GSK   (Belgium)

^b BIOASTER   (France)

Author keywords

Adaptive immune response; Adjuvant; Immune response; Immunogenicity; Innate immune response; Safety; Vaccine

Indexed keywords

VIRUS VACCINE;

ADAPTIVE IMMUNITY; ANTIBODY RESPONSE; ANTIGEN PRESENTING CELL; CLINICAL PRACTICE; HUMAN; IMMUNE RESPONSE; IMMUNOGENICITY; INFLAMMATION; INNATE IMMUNITY; MYOFASCIITIS; NONHUMAN; PATHOGENESIS; PERSIAN GULF SYNDROME; REVIEW; RISK ASSESSMENT; T LYMPHOCYTE ACTIVATION; VACCINATION; VIRUS INFECTION; VIRUS VIRULENCE;

EID: 85001019062     PISSN: None     EISSN: 2076393X     Source Type: Journal    
DOI: 10.3390/vaccines3020320     Document Type: Review

References (91)

1. Gross CP; Sepkowitz KA The myth of the medical breakthrough: Smallpox vaccination and Jenner reconsidered Int J Infect Dis IJID Off Publ Int Soc Infect Dis 1998 3 54–60
2. Strugnell R; Zepp F; Cunningham AL; Tantawhichien T Vaccine antigens Underst Mod Vaccines Perspect Vaccinol 2011 1 61–88
3. WHO Global Vaccine Action Plan 2011–2020 Available online: http://wwwwhoint/immunization/ global_vaccine_action_plan/GVAP_doc_2011_2020/en/ (accessed on 23 October 2014)
4. Zepp F Principles of vaccine design-Lessons from nature Vaccine 2010 28 C14–C24
5. Bonanni P; Santos J Vaccine evolution Underst Mod Vaccines Perspect Vaccinol 2011 1 1– 4
6. Cherry JD Historical review of pertussis and the classical vaccine J Infect Dis 1996 174 S259–S263
7. Miller E; Vurdien JE; White JM The epidemiology of pertussis in England and Wales Commun Dis Rep Rev 1992 2 R152–R154
8. Romanus V; Jonsell R; Bergquist SO Pertussis in Sweden after the cessation of general immunization in 1979 Pediatr Infect Dis J 1987 6 364–371
9. Sato Y; Sato H Development of acellular pertussis vaccines Biol J Int Assoc Biol Stand 1999 27 61–69
10. Pichichero ME; Deloria MA; Rennels MB; Anderson EL; Edwards KM; Decker MD; Englund JA; Steinhoff MC; Deforest A; Meade BD A safety and immunogenicity comparison of 12 acellular pertussis vaccines and one whole-cell pertussis vaccine given as a fourth dose in 15- to 20-month-old children Pediatrics 1997 100 772–788
11. Sheridan SL; Ware RS; Grimwood K; Lambert SB Number and order of whole cell pertussis vaccines in infancy and disease protection JAMA 2012 308 454–456
12. Wendelboe AM; van Rie A; Salmaso S; Englund JA Duration of immunity against pertussis after natural infection or vaccination Pediatr Infect Dis J 2005 24 S58–S61
13. Zhang L; Prietsch SOM; Axelsson I; Halperin SA Acellular vaccines for preventing whooping cough in children Cochrane Database Syst Rev 2012 doi:101002/14651858CD001478pub4
14. Storsaeter J; Wolter J Is there a need for a new generation of vaccines against pertussis? Expert Opin Emerg Drugs 2006 11 195–205
15. Geeraedts F; Goutagny N; Hornung V; Severa M; de Haan A; Pool J; Wilschut J; Fitzgerald KA; Huckriede A Superior immunogenicity of inactivated whole virus H5N1 influenza vaccine is primarily controlled by Toll-like receptor signalling PLOS Pathog 2008 4 e1000138
16. Moser M; Leo O Key concepts in immunology Vaccine 2010 28 C2–C13
17. Ishii KJ; Koyama S; Nakagawa A; Coban C; Akira S Host innate immune receptors and beyond: Making sense of microbial infections Cell Host Microbe 2008 3 352–363
18. Luckheeram RV; Zhou R; Verma AD; Xia B CD4+ T cells: Differentiation and functions Clin Dev Immunol 2012 doi:101155/2012/925135
19. Garlapati S Do we know the Th1/Th2/Th17 determinants of vaccine response? Expert Rev Vaccines 2012 11 1307–1310
20. Klein Klouwenberg P; Bont L Neonatal and infantile immune responses to encapsulated bacteria and conjugate vaccines Clin Dev Immunol 2008 doi:101155/2008/628963
21. Kapikian AZ; Mitchell RH; Chanock RM; Shvedoff RA; Stewart CE An epidemiologic study of altered clinical reactivity to respiratory syncytial (RS) virus infection in children previously vaccinated with an inactivated RS virus vaccine Am J Epidemiol 1969 89 405–421
22. Moghaddam A; Olszewska W; Wang B; Tregoning JS; Helson R; Sattentau QJ; Openshaw PJM A potential molecular mechanism for hypersensitivity caused by formalin-inactivated vaccines Nat Med 2006 12 905–907
23. Anderson LJ; Dormitzer PR; Nokes DJ; Rappuoli R; Roca A; Graham BS Strategic priorities for respiratory syncytial virus (RSV) vaccine development Vaccine 2013 31 B209–B215
24. Vogel F; Hem SL Immunologic adjuvants In Vaccines; Saunders Elsevier: Philadelphia PA USA 2004; pp 69–79
25. Marrack P; McKee AS; Munks MW Towards an understanding of the adjuvant action of aluminium Nat Rev Immunol 2009 9 287–293
26. Coffman RL; Sher A; Seder RA Vaccine adjuvants: Putting innate immunity to work Immunity 2010 33 492–503
27. Black RE; Cousens S; Johnson HL; Lawn JE; Rudan I; Bassani DG; Jha P; Campbell H; Walker CF; Cibulskis R; et al Global regional and national causes of child mortality in 2008: A systematic analysis Lancet 2010 375 1969–1987
28. WHO The global burden of disease: 2004 update Available online: http://wwwwhoint/ healthinfo/global_burden_disease/2004_report_update/en/ (accessed on 5 January 2014)
29. Leroux-Roels G Unmet needs in modern vaccinology: Adjuvants to improve the immune response Vaccine 2010 28 C25–C36
30. Kovaiou RD; Herndler-Brandstetter D; Grubeck-Loebenstein B Age-related changes in immunity: Implications for vaccination in the elderly Expert Rev Mol Med 2007 9 1–17
31. Gruver AL; Hudson LL; Sempowski GD Immunosenescence of ageing J Pathol 2007 211 144–156
32. Wilson-Welder JH; Torres MP; Kipper MJ; Mallapragada SK; Wannemuehler MJ; Narasimhan B Vaccine adjuvants: Current challenges and future approaches J Pharm Sci 2009 98 1278–1316
33. Marconi P; Argnani R; Epstein AL; Manservigi R HSV as a vector in vaccine development and gene therapy Adv Exp Med Biol 2009 655 118–144
34. Majhen D; Calderon H; Chandra N; Fajardo CA; Rajan A; Alemany R; Custers J Adenovirus-based vaccines for fighting infectious diseases and cancer: Progress in the field Hum Gene Ther 2014 25 301–317
35. Gilbert SC Clinical development of Modified Vaccinia virus Ankara vaccines Vaccine 2013 31 4241–4246
36. Khan KH DNA vaccines: Roles against diseases Germs 2013 3 26–35
37. Stanberry L; Strugnell R Vaccines of the future Underst Mod Vaccines Perspect Vaccinol 2011 1 151–199
38. Reed SG; Orr MT; Fox CB Key roles of adjuvants in modern vaccines Nat Med 2013 19 1597–1608
39. Didierlaurent AM; Morel S; Lockman L; Giannini SL; Bisteau M; Carlsen H; Kielland A; Vosters O; Vanderheyde N; Schiavetti F; et al AS04 an aluminum salt- and TLR4 agonist-based adjuvant system induces a transient localized innate immune response leading to enhanced adaptive immunity J Immunol Baltim Md 1950 2009 183 6186–6197
40. Morel S; Didierlaurent A; Bourguignon P; Delhaye S; Baras B; Jacob V; Planty C; Elouahabi A; Harvengt P; Carlsen H; et al Adjuvant System AS03 containing α-tocopherol modulates innate immune response and leads to improved adaptive immunity Vaccine 2011 29 2461–2473
41. Ballou WR; Cahill CP Two decades of commitment to malaria vaccine development: GlaxoSmithKline Biologicals Am J Trop Med Hyg 2007 77 289–295
42. Kester KE; Cummings JF; Ofori-Anyinam O; Ockenhouse CF; Krzych U; Moris P; Schwenk R; Nielsen RA; Debebe Z; Pinelis E; et al Randomized double-blind phase 2a trial of falciparum malaria vaccines RTSS/AS01B and RTSS/AS02A in malaria-naive adults: Safety efficacy and immunologic associates of protection J Infect Dis 2009 200 337–346
43. Leroux-Roels G; Leroux-Roels I; Clement F; Ofori-Anyinam O; Lievens M; Jongert E; Moris P; Ballou WR; Cohen J Evaluation of the immune response to RTSS/AS01 and RTSS/AS02 adjuvanted vaccines: Randomized double-blind study in malaria-naïve adults Hum Vaccines Immunother 2014 doi:104161/hv29375
44. Bejon P; Lusingu J; Olotu A; Leach A; Lievens M; Vekemans J; Mshamu S; Lang T; Gould J; Dubois M-C; et al Efficacy of RTSS/AS01E vaccine against malaria in children 5 to 17 months of age N Engl J Med 2008 359 2521–2532
45. Bovier PA Epaxal: A virosomal vaccine to prevent hepatitis A infection Expert Rev Vaccines 2008 7 1141–1150
46. Moser C; Müller M; Kaeser MD; Weydemann U; Amacker M Influenza virosomes as vaccine adjuvant and carrier system Expert Rev Vaccines 2013 12 779–791
47. Fox CB; Haensler J An update on safety and immunogenicity of vaccines containing emulsion-based adjuvants Expert Rev Vaccines 2013 12 747–758
48. Baz M; Luke CJ; Cheng X; Jin H; Subbarao K H5N1 vaccines in humans Virus Res 2013 178 78–98
49. Giannini SL; Hanon E; Moris P; van Mechelen M; Morel S; Dessy F; Fourneau MA; Colau B; Suzich J; Losonksy G; et al Enhanced humoral and memory B cellular immunity using HPV16/18 L1 VLP vaccine formulated with the MPL/aluminium salt combination (AS04) compared to aluminium salt only Vaccine 2006 24 5937–5949
50. Paavonen J; Naud P; Salmerón J; Wheeler CM; Chow S-N; Apter D; Kitchener H; Castellsague X; Teixeira JC; Skinner SR; et al Efficacy of human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine against cervical infection and precancer caused by oncogenic HPV types (PATRICIA): Final analysis of a double-blind randomised study in young women Lancet 2009 374 301–314
51. Harper DM; Franco EL; Wheeler CM; Moscicki A-B; Romanowski B; Roteli-Martins CM; Jenkins D; Schuind A; Costa Clemens SA; Dubin G Sustained efficacy up to 45 years of a bivalent L1 virus-like particle vaccine against human papillomavirus types 16 and 18: Follow-up from a randomised control trial Lancet 2006 367 1247–1255
52. Harper DM; Franco EL; Wheeler C; Ferris DG; Jenkins D; Schuind A; Zahaf T; Innis B; Naud P; de Carvalho NS; et al Efficacy of a bivalent L1 virus-like particle vaccine in prevention of infection with human papillomavirus types 16 and 18 in young women: A randomised controlled trial Lancet 2004 364 1757–1765
53. Roteli-Martins C; Naud P; de Borba P; Teixeira J; de Carvalho N; Zahaf T; Sanchez N; Geeraerts B; Descamps D Sustained immunogenicity and efficacy of the HPV-16/18 AS04-adjuvanted vaccine: Up to 84 years of follow-up Hum Vaccines Immunother 2012 8 390–397
54. De Carvalho N; Teixeira J; Roteli-Martins CM; Naud P; de Borba P; Zahaf T; Sanchez N; Schuind A Sustained efficacy and immunogenicity of the HPV-16/18 AS04-adjuvanted vaccine up to 73 years in young adult women Vaccine 2010 28 6247–6255
55. Tong NKC; Beran J; Kee SA; Miguel JL; Sánchez C; Bayas JM; Vilella A; de Juanes JR; Arrazola P; Calbo-Torrecillas F; et al Immunogenicity and safety of an adjuvanted hepatitis B vaccine in pre-hemodialysis and hemodialysis patients Kidney Int 2005 68 2298–2303
56. Kundi M New hepatitis B vaccine formulated with an improved adjuvant system Expert Rev Vaccines 2007 6 133–140
57. Ahmed SS; Plotkin SA; Black S; Coffman RL Assessing the safety of adjuvanted vaccines Sci Transl Med 2011 doi:101126/scitranslmed3002302
58. Lopalco PL; Johansen K; Ciancio B; de Carvalho Gomes H; Kramarz P; Giesecke J Monitoring and assessing vaccine safety: A European perspective Expert Rev Vaccines 2010 9 371–380
59. Wolf JJ; Kaplanski CV; Lebron JA Nonclinical safety assessment of vaccines and adjuvants Methods Mol Biol 2010 626 29–40
60. Centers for Disease Control and Prevention (CDC) Withdrawal of rotavirus vaccine recommendation Available online: http://wwwcdcgov/mmwr/preview/mmwrhtml/mm4843a5htm (accessed on 14 April 2015)
61. European Medicines Agency Questions and answers on the suspension of Hexavac Doc Ref EMEA/304888/2005; EMA: London UK 2005
62. Garçon N; Leroux-Roels G; Cheng W Vaccine adjuvants In Understanding Modern Vaccines: Perspectives in Vaccinology; Elsevier: Amsterdam The Netherlands 2011; pp 89–113
63. Garçon N; Segal L; Tavares F; van Mechelen M The safety evaluation of adjuvants during vaccine development: The AS04 experience Vaccine 2011 29 4453–4459
64. Mark A; Granström M The role of aluminium for adverse reactions and immunogenicity of diphtheria-tetanus booster vaccine Acta Paediatr Oslo Nor 1992 1994 83 159–163
65. Waddington CS; Walker WT; Oeser C; Reiner A; John T; Wilkins S; Casey M; Eccleston PE; Allen RJ; Okike I; et al Safety and immunogenicity of AS03B adjuvanted split virion versus non-adjuvanted whole virion H1N1 influenza vaccine in UK children aged 6 months-12 years: Open label randomised parallel group multicentre study Br Med J 2010 doi:101136/bmjc2649
66. Kosalaraksa P; Jeanfrau R; Frenette L; Dramé M; Madariaga M; Innis BL; Godeaux O; Izurieta P; Vaughn D AS03B-adjuvanted H5N1 influenza vaccine in children 6 months through 17 years of age: A Phase II/III randomized placebo-controlled observer-blind trial J Infect Dis 2014 doi:101093/infdis/jiu548
67. Levie K; Gjorup I; Skinhøj P; Stoffel M A 2-dose regimen of a recombinant hepatitis B vaccine with the immune stimulant AS04 compared with the standard 3-dose regimen of Engerix-B in healthy young adults Scand J Infect Dis 2002 34 610–614
68. Tavares Da Silva F; de Keyser F; Lambert P-H; Robinson WH; Westhovens R; Sindic C Optimal approaches to data collection and analysis of potential immune mediated disorders in clinical trials of new vaccines Vaccine 2013 31 1870–1876
69. Bonanni P; Cohet C; Kjaer SK; Latham NB; Lambert P-H; Reisinger K; Haupt RM A summary of the post-licensure surveillance initiatives for GARDASIL/SILGARD Vaccine 2010 28 4719–4730
70. Angelo M; Zima J; Tavares F; Baril L; Arellano F Post-licensure safety surveillance for AS04-adjuvanted Human Papillomavirus vaccine: More than 4 years of experience Pharmacoepidemiol Drug Saf 2014 23 456–465
71. Angelo M-G; David MPP; Baril L; Struyf F; Zima J; Arellano F Safety of human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine (CervarixTM): A pooled analysis of clinical trial data Hum Vaccin 2009 5 332–340
72. Verstraeten T; Descamps D; David M-P; Zahaf T; Hardt K; Izurieta P; Dubin G; Breuer T Analysis of adverse events of potential autoimmune aetiology in a large integrated safety database of AS04 adjuvanted vaccines Vaccine 2008 26 6630–6638
73. Grimaldi-Bensouda L; Guillemot D; Godeau B; Bénichou J; Lebrun-Frenay C; Papeix C; Labauge P; Berquin P; Penfornis A; Benhamou P-Y; et al Autoimmune disorders and quadrivalent human papillomavirus vaccination of young female subjects J Intern Med 2013 275 398–408
74. Langmuir AD Guillain-Barré syndrome: The swine influenza virus vaccine incident in the United States of America 1976–77: Preliminary communication J R Soc Med 1979 72 660–669
75. Schonberger LB; Bregman DJ; Sullivan-Bolyai JZ; Keenlyside RA; Ziegler DW; Retailliau HF; Eddins DL; Bryan JA Guillain-Barre syndrome following vaccination in the National Influenza Immunization Program United States 1976–1977 Am J Epidemiol 1979 110 105–123
76. Greene SK; Rett M; Weintraub ES; Li L; Yin R; Amato AA; Ho DT; Sheikh SI; Fireman BH; Daley MF; et al Risk of confirmed Guillain-Barre syndrome following receipt of monovalent inactivated influenza A (H1N1) and seasonal influenza vaccines in the Vaccine Safety Datalink Project 2009–2010 Am J Epidemiol 2012 175 1100–1109
77. Wise ME; Viray M; Sejvar JJ; Lewis P; Baughman AL; Connor W; Danila R; Giambrone GP; Hale C; Hogan BC; et al Guillain-Barre syndrome during the 2009–2010 H1N1 influenza vaccination campaign: Population-based surveillance among 45 million Americans Am J Epidemiol 2012 175 1110–1119
78. Dodd CN; Romio SA; Black S; Vellozzi C; Andrews N; Sturkenboom M; Zuber P; Hua W; Bonhoeffer J; Buttery J; et al International collaboration to assess the risk of Guillain Barré Syndrome following Influenza A (H1N1) 2009 monovalent vaccines Vaccine 2013 31 4448–4458
79. Isai A; Durand J; le Meur S; Hidalgo-Simon A; Kurz X Autoimmune disorders after immunisation with Influenza A/H1N1 vaccines with and without adjuvant: EudraVigilance data and literature review Vaccine 2012 30 7123–7129
80. Romio S; Weibel D; Dieleman JP; Olberg HK; de Vries CS; Sammon C; Andrews N; Svanström H; Mølgaard-Nielsen D; Hviid A; et al Guillain-Barré syndrome and adjuvanted pandemic influenza A (H1N1) 2009 vaccines: A multinational self-controlled case series in Europe PLOS ONE 2014 9 e82222
81. European Medicines Agency Assessment report Pandemrix EMA/691037/2013; EMA: London UK 2013
82. Asa PB; Cao Y; Garry RF Antibodies to squalene in Gulf War syndrome Exp Mol Pathol 2000 68 55–64
83. Lippi G; Targher G; Franchini M Vaccination squalene and anti-squalene antibodies: Facts or fiction? Eur J Intern Med 2010 21 70–73
84. WHO Safety of squalene Available online: http://wwwwhoint/vaccine_safety/committee/ topics/adjuvants/squalene/Jun_2006/en/ (accessed on 23 October 2014)
85. Israeli E; Agmon-Levin N; Blank M; Shoenfeld Y Macrophagic myofaciitis a vaccine (alum) autoimmune-related disease Clin Rev Allergy Immunol 2011 41 163–168
86. Siegrist C-A Vaccine adjuvants and macrophagic myofasciitis Arch Pédiatrie Organe Off Sociéte Fr Pédiatrie 2005 12 96–101
87. Verdier F; Burnett R; Michelet-Habchi C; Moretto P; Fievet-Groyne F; Sauzeat E Aluminium assay and evaluation of the local reaction at several time points after intramuscular administration of aluminium containing vaccines in the Cynomolgus monkey Vaccine 2005 23 1359–1367
88. WHO Statement from the Global Advisory Committee on Vaccine Safety on aluminium-containing vaccines Available online: http://wwwwhoint/vaccine_safety/committee/topics/aluminium/statement _112002/en/ (accessed on 20 March 2014)
89. Expanding immunization coverage Available online: http://wwwuniceforg/immunization/index_ coveragehtml (accessed 30 June 2014)
90. Begg N Trust in vaccines: Why it takes more than good faith Vaccines 2013 1 343–347
91. Hardt K; Schmidt-Ott R; Glismann S; Adegbola RA; Meurice F Sustaining vaccine confidence in the 21st century Vaccines 2013 1 204–224