Simplifying influenza vaccination during pandemics: Sublingual priming and intramuscular boosting of immune responses with heterologous whole inactivated influenza vaccine

AAPS Journal

Volumn 16, Issue 2, 2014, Pages 342-349

  Murugappan, Senthil ^a   Patil, Harshad P ^b   Frijlink, Henderik W ^a   Huckriede, Anke ^b   Hinrichs, Wouter L J ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

bird flu; H5N1; mucosal vaccine; sublingual vaccine tablet; whole inactivated virus

Indexed keywords

IMMUNOGLOBULIN G ANTIBODY; INFLUENZA VACCINE; VIRUS PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY TITER; ARTICLE; CONTROLLED STUDY; CRUSHING STRENGTH; DISEASE ASSOCIATION; DRUG STABILITY; DRUG USE; FREEZE DRYING; HEMAGGLUTINATION INHIBITION TEST; IMMUNE RESPONSE; IN VITRO STUDY; INFLUENZA VACCINATION; INFLUENZA VIRUS; INFLUENZA VIRUS A H5N1; MALE; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PANDEMIC; TABLET DISINTEGRATION TIME; TABLET PROPERTY; VIRUS IDENTIFICATION; VIRUS INACTIVATION; VIRUS PARTICLE; VIRUS STRAIN;

ADMINISTRATION, SUBLINGUAL; DISEASE OUTBREAKS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; IMMUNITY, MUCOSAL; IMMUNOGLOBULIN G; INFLUENZA VACCINES; INJECTIONS, INTRAMUSCULAR;

EID: 84895856358     PISSN: 15507416     EISSN: None     Source Type: Journal    
DOI: 10.1208/s12248-014-9565-z     Document Type: Article

References (47)

1. Wyman O. Influenza vaccine strategies for broad global access key findings and project methodology. 2007.
2. Jennings LC, Monto AS, Chan PKS, Szucs TD, Nicholson KG, Royal L. Stockpiling prepandemic influenza vaccines: a new cornerstone of pandemic preparedness plans. Lancet Infect Dis. 2008;8:650-8.
3. Longini IM, Nizam A, Xu S, Ungchusak K, Hanshaoworakul W, Cummings DAT, et al. Containing pandemic in fluenza at the source. Science. 2005;309:1083-7.
4. Luykx DM, Casteleijn MG, Jiskoot W, Westdijk J, Jongen PMJM. Physicochemical studies on the stability of influenza haemagglutinin in vaccine bulk material. Eur J Pharm Sci. 2004;23:65-75. (Pubitemid 39485999)
5. Coenen F, Tolboom JTBM, Frijlink HW. Stability of influenza sub-unit vaccine: does a couple of days outside the refrigerator matter? Vaccine. 2006;24:525-31. (Pubitemid 41832557)
6. Carrat F, Flahault A. In fl uenza vaccine: the challenge of antigenic drift. Vaccine. 2007;25:6852-62. (Pubitemid 47398929)
7. Wang H, Feng Z, Shu Y, Yu H, Zhou L, Zu R, et al. Probable limited person-to-person transmission of highly pathogenic avian influenza A H5N1. virus in China. Lancet. 2008;371:1427-34.
8. Ungchusak K, Auewarakul P. Probable person-to-person transmission of avian influenza A H5N1. N Engl J Med. 2005;352:333-40.
9. Imai M, Herfst S, Sorrell EM, Schrauwen EJ, Linster M, De Graaf M, et al. Transmission of influenza A/H5N1 viruses in mammals. Virus Res. 2013;178:15-20.
10. Russell CA, Fonville JM, Brown AEX, Burke DF, Smith DL, James SL, et al. The potential for respiratory droplet-transmissible A/H5N1 influenza virus to evolve in a mammalian host. Science. 2012;336:1541-7.
11. Herfst S, Schrauwen EJ, Linster M, Chutinimitkul S, de Wit E, Munster VJ, et al. Airborne transmission of influenza A/H5N1 virus between ferrets. Science. 2012;336:1534-41.
12. 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.
13. Baz M, Luke CJ, Cheng X, Jin H, Subbarao K. H5N1 vaccines in humans. Virus Res. 2013;178:78-98.
14. WHO. Updated unified nomenclature system for the highly pathogenic H5N1 avian influenza viruses.2011.
15. WHO. Continued evolution of highly pathogenic avian influenza A H5N1: updated nomenclature. Influenza Other Respir Viruses. 2012;6:1-5.
16. WHO. Antigenic and genetic characteristics of H5N1 viruses and candidate H5N1 vaccine viruses developed for potential use as pre-pandemic vaccines 2006; 81:328-30.
17. Belshe RB, Frey SE, Graham I, Mulligan MJ, Edupuganti S, Jackson L, et al. Safety and immunogenicity of influenza A H5 subunit vaccines: effect of vaccine schedule and antigenic variant. J Infect Dis. 2011;203:666-73.
18. Garmise RJ, Staats HF, Hickey AJ. Novel dry powder preparations of whole inactivated influenza virus for nasal vaccination. AAPS PharmSciTech. 2007;8:E81.
19. Amorij J-P, Meulenaar J, Hinrichs WLJ, Stegmann T, Huckriede A, Coenen F, et al. Rational design of an influenza subunit vaccine powder with sugar glass technology: preventing conformational changes of haemagglutinin during freezing and freeze-drying. Vaccine. 2007;25:6447-57. (Pubitemid 47198923)
20. Geeraedts F, Saluja V, Ter Veer W, Amorij JP, Frijlink HW, Wilschut J, et al. Preservation of the immunogenicity of dry-powder influenza H5N1 whole inactivated virus vaccine at elevated storage temperatures. AAPS J. 2010;12:215-22.
21. Audouy SAL, van der Schaaf G, Hinrichs WLJ, Frijlink HW, Wilschut J, Huckriede A. Development of a dried influenza whole inactivated virus vaccine for pulmonary immunization. Vaccine. 2011;29:1-8.
22. Murugappan S, Patil HP, Kanojia G, Ter Veer W, Meijerhof T, Frijlink HW, et al. Physical and immunogenic stability of spray freeze-dried influenza vaccine powder for pulmonary delivery: comparison of inulin, dextran, or a mixture of dextran and trehalose as protectants. Eur J Pharm Biopharm. 2013;85:716-25.
23. Boudreault A, Pavilanis V. Oral immunization against influenza virus. Arch Gesamte Virusforsch. 1972;38:177-82.
24. Shim B-S, Choi Y, Cheon IS, Song MK. Sublingual delivery of vaccines for the induction of mucosal immunity. Immune Netw. 2013;13:81-5.
25. Pedersen G, Cox R. The mucosal vaccine quandary: intranasal vs. sublingual immunization against in fluenza. Hum Vaccin Immunother. 2012;8:689-93.
26. Kweon M-NN. Sublingual mucosa: a new vaccination route for systemic and mucosal immunity. Cytokine 2011:10-4.
27. Pedersen GK, Ebensen T, Gjeraker IH, Svindland S, Bredholt G, Guzmán CA, et al. Evaluation of the sublingual route for administration of influenza H5N1 virosomes in combination with the bacterial second messenger c-di-GMP. PLoS One 2011;6: doi:10.1371/journal.pone.0026973.
28. Shim B-SS, Choi YK, Yun C-HH, Lee E-GG, Jeon YS, Park SMM, et al. Sublingual Immunization with M2-Based Vaccine Induces Broad Protective Immunity against Influenza. PLoS One 2011;6. doi:10.1371/journal.pone.0027953.
29. Song JH, Nguyen HH, Cuburu N, Horimoto T, Ko SY, Park SH, et al. Sublingual vaccination with influenza virus protects mice against lethal viral infection. Proc Natl Acad Sci U S A. 2008;105:1644-9. (Pubitemid 351346568)
30. Amorij J-P, Hinrichs WL, Frijlink HW, Wilschut JC, Huckriede A. Needle-free in fluenza vaccination. Lancet Infect Dis. 2010;10:699-711.
31. Bensadoun A, Weinstein D. Assay of proteins in the presence of interfering materials. Anal Biochem. 1976;70:241-50.
32. Rawas-Qalaji MM, Estelle F, Simons R, Simons KJ, Simons FE. Fast-disintegrating sublingual tablets: effect of epinephrine load on tablet characteristics. AAPS PharmSciTech 2006;7: doi:10.1208/pt070241.
33. Blum H, Beier H, Gross HJ. Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis. 1987;8:93-9.
34. Amorij J-P, Saluja V, Petersen AH, Hinrichs WLJ, 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;25:8707-17. (Pubitemid 350199597)
35. De Jong JC, Palache AM, Beyer WEP, Rimmelzwaan GF, Boon ACM, Osterhaus ADME. Haemagglutination-inhibiting antibody to influenza virus. Dev Biol (Basel). 2003;115:63-73.
36. Hobson D, Curry RL, Beare AS, Ward-Gardner A. The role of serum haemagglutination-inhibiting antibody in protection against challenge infection with influenza A2 and B viruses. J Hyg Lond. 1972;70:767-77.
37. FDA. Guidance for industry: clinical data needed to support the licensure of seasonal inactivated Influenza vaccines 2013.
38. Borde A, Ekman A, Holmgren J, Larsson A. Effect of protein release rates from tablet formulations on the immune response after sublingual immunization. Eur J Pharm Sci. 2012;47:695-700.
39. Baz M, Luke CJ, Cheng X, Jin H, Subbarao K. H5N1 vaccines in humans. Virus Res 2013:1-21.
40. Belshe RB, Frey SE, Graham I, Mulligan MJ, Edupuganti S, Jackson LA, et al. Safety and immunogenicity of influenza A H5 subunit vaccines: effect of vaccine schedule and antigenic variant. J Infect Dis. 2011;203:666-73.
41. Wu J, Fang H-H, Chen J-T, Zhou J-C, Feng Z-J, Li C-G, et al. Immunogenicity, safety, and cross-reactivity of an inactivated, adjuvanted, prototype pandemic influenza H5N1. vaccine: a phase II, double-blind, randomized trial. Clin Infect Dis. 2009;48:1087-95.
42. Goji NA, Nolan C, Hill H, Wolff M, Noah DL, Williams TB, et al. Immune responses of healthy subjects to a single dose of intramuscular inactivated influenza A/Vietnam/1203/2004 H5N1. Vaccine after priming with an antigenic variant. J Infect Dis. 2008;198:635-41.
43. Vemula S V, Ahi YS, Swaim A-M, Katz JM, Donis R, Sambhara S, et al. Broadly protective adenovirus-based multivalent vaccines against highly pathogenic avian influenza viruses for pandemic preparedness. PLoS One 2013;8: doi:10.1371/journal.pone.0062496.
44. Renegar KB, Small PA, Boykins LG, Wright PF. Role of IgA versus IgG in the control of influenza viral infection in the murine respiratory tract. J Immunol. 2004;173:1978-86. (Pubitemid 38971634)
45. Geeraedts F, Goutagny N, Hornung V, Severa M, de Haan A, Pool J, et al. Superior immunogenicity of inactivated whole virus H5N1 In fluenza vaccine is primarily controlled by toll-like receptor signalling.PLoS Pathog 2008;8: doi:10.1371/journal.ppat.1000138.
46. Cuburu N, Kweon M-N, Song J-H, Hervouet C, Luci C, Sun J-B, et al . Sublingual immunization induces broad-based systemic and mucosal immune responses in mice. Vaccine. 2007;25:8598-610. (Pubitemid 350192038)
47. Rudnic EM, Schwartz JB. Remington: the science and practice of pharmacy, oral solid dosage forms.Remington's pharmaceutical sciences. 21st ed. Lippincott Williams & Wilkins; 2006.