Immunogenicity and protection of oral influenza vaccines formulated into microparticles

Journal of Pharmaceutical Sciences

Volumn 101, Issue 10, 2012, Pages 3623-3635

  Shastri, Prathap Nagaraja ^a   Kim, Min Chul ^b   Quan, Fu Shi ^c   D'Souza, Martin J ^a   Kang, Sang Moo ^d  

^a MERCER UNIVERSITY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Kyung Hee University Hospital   (South Korea)

^d GEORGIA STATE UNIVERSITY   (United States)

Author keywords

Immunology; Microparticles; Oral delivery; Spray drying; Vaccines

Indexed keywords

EUDRAGIT; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN G2; INFLUENZA VACCINE; TREHALOSE;

AGED; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BAGG ALBINO MOUSE; CONTROLLED STUDY; DRUG ACTIVITY; DRUG DELIVERY SYSTEM; DRUG FORMULATION; FEMALE; HEMAGGLUTINATION TEST; IMMUNOGENICITY; IN VIVO CULTURE; INFLUENZA VACCINATION; INFLUENZA VIRUS; MOUSE; NONHUMAN; PARTICLE SIZE; SERUM;

EID: 84865357139     PISSN: 00223549     EISSN: 15206017     Source Type: Journal    
DOI: 10.1002/jps.23220     Document Type: Article

References (53)

1. Thompson WW, Shay DK, Weintraub E, Brammer L, Cox N, Anderson LJ, Fukuda K. 2003. Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA 289(2):179-186.
2. Hsieh YC, Wu TZ, Liu DP, Shao PL, Chang LY, Lu CY, Lee CY, Huang FY, Huang LM. 2006. Influenza pandemics: Past, present and future. J Formos Med Assoc 105(1):1-6.
3. Fouchier RA, Munster V, Wallensten A, Bestebroer TM, Herfst S, Smith D, Rimmelzwaan GF, Olsen B, Osterhaus AD. 2005. Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J Virol 79(5):2814-2822.
4. Germann TC, Kadau K, Longini IM Jr., Macken CA. 2006. Mitigation strategies for pandemic influenza in the United States. Proc Natl Acad Sci U S A 103(15):5935-5940.
5. Rappuoli R. 2007. Bridging the knowledge gaps in vaccine design. Nat Biotechnol 25(12):1361-1366.
6. Francis T Jr., Salk JE, Brace WM. 1946. The protective effect of vaccination against epidemic influenza B. J Am Med Assoc 131:275-278.
7. Al-Mazrou A, Scheifele DW, Soong T, Bjornson G. 1991. Comparison of adverse reactions to whole-virion and split-virion influenza vaccines in hospital personnel. CMAJ 145(3):213-218.
8. Eizenberg P, Booy R, Naser N, Mason G, Stamboulian D, Weber F. 2011. Acceptance of Intanza(R) 9 mug intradermal influenza vaccine in routine clinical practice in Australia and Argentina. Adv Ther 28(8):640-649.
9. Atmar RL, Patel SM, Keitel WA. 2010. Intanza((R)): A new intradermal vaccine for seasonal influenza. Expert Rev Vaccines 9(12):1399-1409.
10. Belshe RB, Newman FK, Wilkins K, Graham IL, Babusis E, Ewell M, Frey SE. 2007. Comparative immunogenicity of trivalent influenza vaccine administered by intradermal or intramuscular route in healthy adults. Vaccine 25(37-38):6755-6763.
11. Carter NJ, Curran MP. 2011. Live attenuated influenza vaccine (FluMist(R); Fluenz): A review of its use in the prevention of seasonal influenza in children and adults. Drugs 71(12):1591-1622.
12. Wright PF, Cherry JD, Foy HM, Glezen WP, Hall CB, McIntosh K, Monto AS, Parrott RH, Portnoy B, Taber LH. 1983. Antigenicity and reactogenicity of influenza A/USSR/77 virus vaccine in children-A multicentered evaluation of dosage and safety. Rev Infect Dis 5(4):758-764.
13. Hancock K, Veguilla V, Lu X, Zhong W, Butler EN, Sun H, Liu F, Dong L, DeVos JR, Gargiullo PM, Brammer TL, Cox NJ, Tumpey TM, Katz JM. 2009. Cross-reactive antibody responses to the 2009 pandemic H1N1 influenza virus. N Engl J Med 361(20):1945-1952.
14. Quan FS, Steinhauer D, Huang C, Ross TM, Compans RW, Kang SM. 2008. A bivalent influenza VLP vaccine confers complete inhibition of virus replication in lungs. Vaccine 26(26):3352-3361.
15. Kane A, Lloyd J, Zaffran M, Simonsen L, Kane M. 1999. Transmission of hepatitis B, hepatitis C and human immunodeficiency viruses through unsafe injections in the developing world: Model-based regional estimates. Bull World Health Organ 77(10):801-807.
16. Kermode M. 2004. Unsafe injections in low-income country health settings: Need for injection safety promotion to prevent the spread of blood-borne viruses. Health Promot Int 19(1):95-103.
17. La Montagne JR, Fauci AS. 2004. Intradermal influenza vaccination-Can less be more? N Engl J Med 351(22):2330-2332.
18. Gerdil C. 2003. The annual production cycle for influenza vaccine. Vaccine 21(16):1776-1779.
19. Modlin JF, Onorato IM, McBean AM, Albrecht P, Thoms ML, Nerhood L, Bernier R. 1990. The humoral immune response to type 1 oral poliovirus vaccine in children previously immunized with enhanced potency inactivated poliovirus vaccine or live oral poliovirus vaccine. Am J Dis Child 144(4):480-484.
20. Neutra MR, Kozlowski PA. 2006. Mucosal vaccines: The promise and the challenge. Nat Rev Immunol 6(2):148-158.
21. Chattaraj SC, Rathinavelu A, Das SK. 1999. Biodegradable microparticles of influenza viral vaccine: Comparison of the effects of routes of administration on the in vivo immune response in mice. J Control Release 58(2):223-232.
22. Baaten BJ, Clarke B, Strong P, Hou S. 2010. Nasal mucosal administration of chitin microparticles boosts innate immunity against influenza A virus in the local pulmonary tissue. Vaccine 28(25):4130-4137.
23. Yeboah KG, D'Souza M J. 2009. Evaluation of albumin microspheres as oral delivery system for Mycobacterium tuberculosis vaccines. J Microencapsul 26(2):166-179.
24. Lai YH, D'Souza MJ. 2007. Formulation and evaluation of an oral melanoma vaccine. J Microencapsul 24(3):235-252.
25. Meitin CA, Bender BS, Small PA Jr. 1994. Enteric immunization of mice against influenza with recombinant vaccinia. Proc Natl Acad Sci U S A 91(23):11187-11191.
26. O'Hagan DT, Singh M. 2003. Microparticles as vaccine adjuvants and delivery systems. Expert Rev Vaccines 2(2):269-283.
27. Hodges GM, Carr EA, Hazzard RA, Carr KE. 1995. Uptake and translocation of microparticles in small intestine. Morphology and quantification of particle distribution. Dig Dis Sci 40(5):967-975.
28. Akande J, Yeboah KG, Addo RT, Siddig A, Oettinger CW, D'Souza MJ. 2010. Targeted delivery of antigens to the gut-associated lymphoid tissues: 2. Ex vivo evaluation of lectin-labelled albumin microspheres for targeted delivery of antigens to the M-cells of the Peyer's patches. J Microencapsul 27(4):325-336.
29. Quan FS, Compans RW, Nguyen HH, Kang SM. 2008. Induction of heterosubtypic immunity to influenza virus by intranasal immunization. J Virol 82(3):1350-1359.
30. Gayakwad SG, Bejugam NK, Akhavein N, Uddin NA, Oettinger CE, D'Souza MJ. 2009. Formulation and in vitro characterization of spray-dried antisense oligonucleotide to NF-kappaB encapsulated albumin microspheres. J Microencapsul, 26(8):692-700.
31. Novak M, Moldoveanu Z, Schafer DP, Mestecky J, Compans RW. 1993. Murine model for evaluation of protective immunity to influenza virus. Vaccine 11(1):55-60.
32. Compans RW. 1974. Hemagglutination-inhibition: Rapid assay for neuraminic acid-containing viruses. J Virol 14(5):1307-1309.
33. McConnell EL, Basit AW, Murdan S. 2008. Measurements of rat and mouse gastrointestinal pH, fluid and lymphoid tissue, and implications for in-vivo experiments. J Pharm Pharmacol 60(1):63-70.
34. Quan FS, Huang C, Compans RW, Kang SM. 2007. Virus-like particle vaccine induces protective immunity against homologous and heterologous strains of influenza virus. J Virol 81(7):3514-3524.
35. Gupta RK, Singh M, O'Hagan DT. 1998. Poly(lactide-co-glycolide) microparticles for the development of single-dose controlled-release vaccines. Adv Drug Deliv Rev 32(3):225-246.
36. Tabata Y, Inoue Y, Ikada Y. 1996. Size effect on systemic and mucosal immune responses induced by oral administration of biodegradable microspheres. Vaccine 14(17-18):1677-1685.
37. Quan FS, Kim YC, Vunnava A, Yoo DG, Song JM, Prausnitz MR, Compans RW, Kang SM. 2010. Intradermal vaccination with influenza virus-like particles by using microneedles induces protection superior to that with intramuscular immunization. J Virol 84(15):7760-7769.
38. Quan FS, Kim YC, Yoo DG, Compans RW, Prausnitz MR, Kang SM. 2009. Stabilization of influenza vaccine enhances protection by microneedle delivery in the mouse skin. PLoS One 4(9):e7152.
39. Herrler G, Durkop I, Becht H, Klenk HD. 1988. The glycoprotein of influenza C virus is the haemagglutinin, esterase and fusion factor. J Gen Virol 69(Pt 4):839-846.
40. Quan FS, Li ZN, Kim MC, Yang D, Compans RW, Steinhauer DA, Kang SM. 2011. Immunogenicity of low-pH treated whole viral influenza vaccine. Virology 417(1):196-202.
41. Quan FS, Compans RW, Kang SM. 2012. Oral vaccination with inactivated influenza vaccine induces cross-protective immunity. Vaccine 30:180-188.
42. Kim YC, Quan FS, Yoo DG, Compans RW, Kang SM, Prausnitz MR. 2009. Improved influenza vaccination in the skin using vaccine coated microneedles. Vaccine 27(49):6932-6938.
43. Amorij JP, Westra TA, Hinrichs WL, Huckriede A, Frijlink HW. 2007. Towards an oral influenza vaccine: Comparison between intragastric and intracolonic delivery of influenza subunit vaccine in a murine model. Vaccine 26(1):67-76.
44. Neutra MR, Pringault E, Kraehenbuhl JP. 1996. Antigen sampling across epithelial barriers and induction of mucosal immune responses. Annu Rev Immunol 14:275-300.
45. des Rieux A, Fievez V, Garinot M, Schneider YJ, Preat V. 2006. Nanoparticles as potential oral delivery systems of proteins and vaccines: A mechanistic approach. J Control Release 116(1):1-27.
46. Takada A, Matsushita S, Ninomiya A, Kawaoka Y, Kida H. 2003. Intranasal immunization with formalin-inactivated virus vaccine induces a broad spectrum of heterosubtypic immunity against influenza A virus infection in mice. Vaccine 21(23):3212-3218.
47. Tumpey TM, Renshaw M, Clements JD, Katz JM. 2001. Mucosal delivery of inactivated influenza vaccine induces B-cell-dependent heterosubtypic cross-protection against lethal influenza A H5N1 virus infection. J Virol 75(11):5141-5150.
48. Sendi P, Locher R, Bucheli B, Battegay M. 2004. Intranasal influenza vaccine in a working population. Clin Infect Dis 38(7):974-980.
49. Sendi P, Locher R, Bucheli B, Battegay M. 2004. The decision to get vaccinated against influenza. Am J Med 116(12):856-858.
50. Huber VC, McKeon RM, Brackin MN, Miller LA, Keating R, Brown SA, Makarova N, Perez DR, Macdonald GH, McCullers JA. 2006. Distinct contributions of vaccine-induced immunoglobulin G1 (IgG1) and IgG2a antibodies to protective immunity against influenza. Clin Vaccine Immunol 13(9):981-990.
51. Neuberger MS, Rajewsky K. 1981. Activation of mouse complement by monoclonal mouse antibodies. Eur J Immunol 11(12):1012-1016.
52. Nimmerjahn F, Ravetch JV. 2005. Divergent immunoglobulin g subclass activity through selective Fc receptor binding. Science 310(5753):1510-1512.
53. Zho F, Neutra MR. 2002. Antigen delivery to mucosa-associated lymphoid tissues using liposomes as a carrier. Biosci Rep 22(2):355-369.