Serum and mucosal antibody responses to inactivated polio vaccine after sublingual immunization using a thermoresponsive gel delivery system

Human Vaccines and Immunotherapeutics

Volumn 10, Issue 12, 2014, Pages 3611-3621

  White, Jessica A ^a   Blum, Jeremy S ^a   Hosken, Nancy A ^b   Marshak, Joshua O ^b   Duncan, Lauren ^a   Zhu, Changcheng ^a   Norton, Elizabeth B ^d   Clements, John D ^d   Koelle, David M ^b,c   Chen, Dexiang ^a   Weldon, William C ^e   Oberste, M Steven ^e   Lal, Manjari ^a  

^a PATH   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c USA   (United States)

^d TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

Author keywords

Adjuvants; DmLT; Mucosal immune response; Poliovirus; Sublingual immunization; Thermoresponsive gel; Vaccine delivery

Indexed keywords

BACTERIAL TOXIN; IMMUNOGLOBULIN A ANTIBODY; NEUTRALIZING ANTIBODY; PHOSPHATE BUFFERED SALINE; POLIOMYELITIS VACCINE; GEL; IMMUNOGLOBULIN A; VIRUS ANTIBODY;

ANIMAL EXPERIMENT; ANTIBODY BLOOD LEVEL; ANTIBODY RESPONSE; ANTIBODY TITER; AQUEOUS SOLUTION; ARTICLE; BODY TEMPERATURE; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; DRUG MEGADOSE; ENZYME LINKED IMMUNOSORBENT ASSAY; FECES ANALYSIS; FEMALE; GEL; IMMUNIZATION; LOW DRUG DOSE; MOUSE; NONHUMAN; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; IMMUNOLOGY; MUCOSAL IMMUNITY; SUBLINGUAL DRUG ADMINISTRATION;

ADMINISTRATION, SUBLINGUAL; ANIMALS; ANTIBODIES, VIRAL; DRUG DELIVERY SYSTEMS; FEMALE; GELS; IMMUNITY, MUCOSAL; IMMUNIZATION; IMMUNOGLOBULIN A; MICE; MICE, INBRED BALB C; POLIOVIRUS VACCINE, INACTIVATED;

EID: 84922550483     PISSN: 21645515     EISSN: 2164554X     Source Type: Journal    
DOI: 10.4161/hv.32253     Document Type: Article

References (60)

1. Mestecky J. The common mucosal immune system and current strategies for induction of immune responses in external secretions. J Clin Immunol 1987; 7(4):265-76; PMID:3301884
2. Ogra PL, Faden H, Welliver RC. Vaccination strategies for mucosal immune responses. Clin Microbiol Rev 2001; 14(2):430-45; PMID:11292646; http://dx.doi. org/10.1128/CMR.14.2.430-445.2001
3. Freytag LC, Clements JD. Bacterial toxins as mucosal adjuvants. Curr Topics Microbiol Immunol 1999; 236:215-36; PMID:9893362
4. Holmgren J, Svennerholm AM. Vaccines against mucosal infections. Curr Opin Immunol 2012; 24 (3):343-53; PMID:22580196; http://dx.doi.org/ 10.1016/j.coi.2012.03.014
5. Negri DR, Riccomi A, Pinto D, Vendetti S, Rossi A, Cicconi R, Ruggiero P, Del Giudice G, De Magistris MT. Persistence of mucosal and systemic immune responses following sublingual immunization. Vaccine 2010; 28(25):4175-80; PMID:20412876; http://dx. doi.org/10.1016/j.vaccine.2010.04.013
6. Neutra MR, Kozlowski PA. Mucosal vaccines: the promise and the challenge. Nat Rev Immunol 2006; 6 (2):148-58; PMID:16491139; http://dx.doi.org/ 10.1038/nri1777
7. Pavot V, Rochereau N, Genin C, Verrier B, Paul S. New insights in mucosal vaccine development. Vaccine 2012; 30(2):142-54; PMID:22085556; http://dx.doi. org/10.1016/j.vaccine.2011.11.003
8. Yuki Y, Kivono H. Mucosal vaccines: Novel advances in technology and delivery. Exp Rev Vaccines 2009; 8 (8):1083-97; PMID:19627189; http://dx.doi.org/ 10.1586/erv.09.61
9. Czerkinsky C, çuburu N, Kweon M, Anjuere F, Holmgren J. Sublingual vaccination. Human Vaccines Immunotherap 2011; 7(1):110; http://dx.doi.org/ 10.4161/hv.7.1.13739
10. Gallorini S, Taccone M, Bonci A, Nardelli F, Casini D, Bonificio A, Kommareddy S, Bertholet S, O'Hagan DT, Baudner BC, et al. Sublingual immunization with a subunit influenza vaccine elicits comparable systemic immune response as intramuscular immunization, but also induces local IgA and TH17 responses. Vaccine 2014; 32(20):2382-8; PMID:24434044; http://dx.doi. org/10.1016/j.vaccine.2013.12.043
11. World Health Organization (WHO) Collaborative Study Group on Oral and Inactivated Poliovirus Vaccines. Combined immunization of infants with oral and inactivated poliovirus vaccines: Results of a randomized trial in the Gambia, Oman, and Thailand. Bull World Health Organization 1996; 74(3):253-68; PMID:8789924
12. Lang, Dennis. Safety Evaluation of Toxin Adjuvants Delivered Intranasally. Washington, DC: National Institute of Allergy and Infectious Diseases (NIAID); 2001.
13. Mestecky J, McGhee JR. Oral immunization: Past and present. In: Jiri Mestecky, Jerry R McGhee, eds. Current Topics in Microbiology and Immunology: New Strategies for Oral Immunization. Birmingham, AL, USA: International Symposium at the University of Alabama at Birmingham and Molecular Engineering Associates, Inc; 1989; 146:3-11.
14. Shim BS, Choi Y, Cheon IS, Song MK. Sublingual delivery of vaccines for the induction of mucosal immunity. Immune Network 2013; (3):81-85; http://dx.doi. org/10.4110/in.2013.13.3.81
15. Holmgren J, Czerkinsky C. Mucosal immunity and vaccines. Nat Med 2005; 11(4 Suppl):S45-53; PMID:15812489; http://dx.doi.org/10.1038/nm1213
16. Benmohamed L, Belkaid Y, Loing E, Brahimi K, Gras-Masse H, Druilhe P. Systemic immune responses induced by mucosal administration of lipopeptides without adjuvant. Eur J Immunol 2002; 32(8):2274-81; PMID:12209640; http://dx.doi.org/10.1002/ 1521-4141(200208)32:8%3c2274::AID-IMMU2274 %3e3.0.CO;2-C
17. Mestecky J, Nguyen H, Czerkinsky C, Kiyono H. Oral immunization: An update. Curr Opin Gastroenterol 2008; 24(6):713-9; PMID:19122521; http://dx.doi. org/10.1097/MOG.0b013e32830d58be
18. Park HJ, Ferko B, Byun YH, Song JH, Han GY, Roethl E, Egorov A, Muster T, Seong B, Kweon MN, et al. Sublingual immunization with a live attenuated influenza A virus lacking the nonstructural protein 1 induces broad protective immunity in mice. PLoS ONE 2012; 7(6):e39921; PMID:22761928; http://dx. doi.org/10.1371/journal.pone.0039921
19. Czerkinsky C, Holmgren J. Mucosal delivery routes for optimal immunization: Targeting immunity to the right tissues. Curr Topics Microbiol Immunol 2012;354:1-18; PMID:21053117
20. Kweon MN. Sublingual mucosa: A new vaccination route for systemic and mucosal immunity. Cytokine 2011; 54(1):1-5; PMID:21239178; http://dx.doi.org/ 10.1016/j.cyto.2010.12.014
21. Lawson LB, Freytag LC, Clements JD. Sublingual Delivery of Vaccines. New Orleans: Department of Microbiology and Immunology, Tulane University School of Medicine; 2011
22. Salk J, van Wezel AL, Stoeckel P, van Steenis G, Schlumberger M, Meyran M, Rey JL, Lapinleimu K, Böttiger M, Cohen H. Theoretical and practical considerations in the application of killed poliovirus vaccine for the control of paralytic poliomyelitis. Dev Biol Standard 1981; 47:181-98; PMID:7194827
23. Wilkhu J, McNeil SE, Kirby DK, Perrie Y. Formulation design considerations for oral vaccines. Therap Delivery 2011; 2(9):1141-64; PMID:22833911; http://dx.doi.org/10.4155/tde.11.82
24. Martina MPTH. Immunity to poliovirus after infection and vaccination. ; thesis. Bilthoven, The Netherlands: National Institute of Public Health and the Environment (RIVM); 1999.
25. Chen W, Patel GB, Yan H, Zhang J. Recent advances in the development of novel mucosal adjuvants and antigen delivery systems. Human Vaccines 2010; 6 (9):706-14; http://dx.doi.org/10.4161/hv.6.9.11561
26. Norton EB, Lawson LB, Freytag LC, Clements JD. Characterization of a mutant Escherichia coli heatlabile toxin, LT(R192G/L211A), as a safe and effective oral adjuvant. Clin Vaccine Immunol 2011; 18(4):546-51; PMID:21288994; http://dx.doi.org/10.1128/ CVI.00538-10
27. Pizza M, Giuliani MM, Fontana MR, Monaci E, Douce G, Dougan G, Mills KH, Rappuoli R, Del Giudice G. Mucosal vaccines: Non toxic derivatives of LT and CT as mucosal adjuvants. Vaccine 2001; 19(17-19):2534-41; PMID:11257389; http://dx.doi.org/ 10.1016/S0264-410X(00)00553-3
28. El-Kamary SS, Cohen MB, Bourgeois AL, Van De Verg L, Bauers N, Reymann M, Pasetti MF, Chen WH. Safety and immunogenicity of a single oral dose of recombinant double mutant heat-labile toxin derived from enterotoxigenic Escherichia coli. Clin Vaccine Immunol 2013; 20(11):1764-70; http://dx.doi.org/ 10.1128/CVI.00464-13
29. Leach S, Clements JD, Kaim J, Lundgren A. The adjuvant double mutant Escherichia coli heat labile toxin enhances IL-17A production in human T cells specific for bacterial vaccine antigens. PLoS ONE 2012; 7(12): e51718.
30. Summerton NA, Welch RW, Bondoc L, Yang HH, Pleune B, Ramachandran N, Harris AM, Bland D, Jackson WJ, Park S, et al. Toward the development of a stable, freeze-dried formulation of Helicobacter pylori killed whole cell vaccine adjuvanted with a novel mutant of Escherichia coli heat-labile toxin. Vaccine 2010; 28(5):1404-11; PMID:19897067; http://dx.doi. org/10.1016/j.vaccine.2009.10.147
31. Coeshott CM, Smithson SL, Verderber E, Samaniego A, Blonder JM, Rosenthal GJ, Westerink MA. Pluronic F127-based systemic vaccine delivery systems. Vaccine 2004; 22(19):2396-405; PMID:15193401; http://dx. doi.org/10.1016/j.vaccine.2003.11.064
32. Kang ML, Jiang HL, Kang SG, Guo DD, Lee DY, Cho CS, Yoo HS. Pluronic F127 enhances the effect as an adjuvant of chitosan microspheres in the intranasal delivery of Bordetella bronchiseptica antigens containing dermonecrotoxin. Vaccine 2007; 25(23):4602-10; PMID:17485148; http://dx.doi.org/10.1016/j.vaccine. 2007.03.038
33. Okayasu H, Sutter RW, Czerkinsky C, Ogra PL. Mucosal immunity and poliovirus vaccines: Impact on wild poliovirus infection and transmission. Vaccine 2011; 29(46):8205-14; PMID:21896299; http://dx. doi.org/10.1016/j.vaccine.2011.08.059
34. Mahmood K, Pelkowski S, Atherly D, Sitrin R, Donnelly JJ. Hexavalent IPV-based combination vaccines for public-sector markets of low-resource countries. Human Vaccines Immunotherap 2013; 9(9):1894-1902; PMID:23787559; http://dx.doi.org/10.4161/ hv.25407
35. Liao G, Li R, Li C, Sun M, Li Y, Chu J, et al. Safety and immunogenicity of inactivated poliovirus vaccine made from Sabin strains: A phase II randomized, positive- controlled trial. J Infect Dis 2012; 205:237-43; PMID:22158682; http://dx.doi.org/10.1093/infdis/ jir723
36. Westdijk J, Koedam P, Barro M, Steil BP, Collin N, Vedvick TS, Bakker WA, van der Ley P, Kersten G. Antigen sparing with adjuvanted inactivated polio vaccine based on Sabin strains. Vaccine 2013; 31(9):1298-304; PMID:23313617; http://dx.doi.org/10.1016/j. vaccine.2012.12.076
37. World Health Organization (WHO). Polio Vaccines: WHO Position Paper. Weekly EpidemiolRecord 2014; 89(9):73-92; PMID:24707513
38. GAVI Alliance. GAVI Alliance to Support Introduction of Inactivated Polio Vaccine in World's 73 Poorest Countries. Phnom Penh: GAVI; 2013.
39. World Health Organization (WHO). Polio Eradication and Endgame Strategic plan 2013-2018-Executive summary. Geneva: WHO; 2013.
40. World Health Organization (WHO). Framework for National Policy Makers in OPV-Using Countries. WHO/POLIO/05.11; Geneva: WHO; 2005.
41. Buisman AM, Abbink F, Schepp Rm, Sonsma JA, Herremans T, Kimman TG. Preexisting poliovirus-specific IgA in the circulation correlates with protection against virus excretion in the elderly. J Infect Dis 2008; 197 (5):698-706; PMID:18279050; http://dx.doi.org/ 10.1086/527487
42. Steil BP, Jorquera P, Westdijk J, Bakker WA, Johnston RE, Barro M. A mucosal adjuvant for the inactivated poliovirus vaccine. Vaccine 2014; 32(5):558-63; PMID:24333345; http://dx.doi.org/10.1016/j. vaccine.2013.11.101
43. Amero CD, Arnold JJ, Moustafa IM, Cameron CE, Foster MP. Identification of the oriI-binding site of poliovirus 3C protein by nuclear magnetic resonance spectroscopy. J Virol 2008; 82(9):4363-70; PMID:18305026; http://dx.doi.org/10.1128/JVI.02087-07
44. Hawken J, Troy SB. Adjuvants and inactivated polio vaccine: A systematic review. Vaccine 2012; 30 (49):6971-9; PMID:23041122; http://dx.doi.org/ 10.1016/j.vaccine.2012.09.059
45. EL-Gawad AE-GH, Soliman OA, Baker SA, Girgis GNS. Formulation and physical characterization of a novel sustained-release ophthalmic delivery system for Sparfloxacin: The Effect of the Biological Environment. Ophthalmol Res 2013; 1(1):1-22.
46. Lin H, Gebhardt M, Bian S, Kwon KA, Shim CK, Chung SJ, Kim DD. Enhancing effect of surfactants on fexofenadine HCl transport across the human nasal epithelial cell monolayer. Int J Pharma 2007; 330:23-31; PMID:16997520; http://dx.doi.org/10.1016/j.ijpharm. 2006.08.043
47. Yang M, Lai SK, Wang YY, Zhong W, Happe C, Zhang M, Fu J, Hanes J. Biodegradable nanoparticles composed entirely of safe materials that rapidly penetrate human mucus. Angewandte Chemie Int Edition 2011; 50:2597-600; http://dx.doi.org/10.1002/ anie.201006849
48. Li L, Mathias NR, Heran CL, Moench P, Wall DA, Smith RL. Carbopol-mediated paracellular transport enhancement in Calu-3 cell layers. J Pharma Sci 2006; 95:326-35; PMID:16374869; http://dx.doi.org/ 10.1002/jps.20541
49. Lu YJ, Yadav P, Celements JD, Forte S, Srivastava A, Thompson CM, Seid R, Look J, Alderson M, Tate A, et al. Options for inactivation, adjuvant, and route of topical administration of a killed, unencapsulated pneumococcal whole-cell vaccine. Clin Vaccine Immunol 2010; 17(6):1005-12; PMID:20427625; http://dx. doi.org/10.1128/CVI.00036-10
50. Norton EB, Lawson LB, Mahdi Z, Freytag LC, Clements JD. The A subunit of Escherichia coli heat-labile enterotoxin functions as a mucosal adjuvant and promotes IgG2a, IgA, and Th17 responses to vaccine antigens. Infect Immun 2012; 80 (7):2426-35; PMID:22526674; http://dx.doi.org/ 10.1128/IAI.00181-12
51. Martin J, Crossland G, Wood DJ, Minor PD. Characterization of formaldehyde-inactivated poliovirus preparations made from live attenuated strains. J General Virol 2003; 84:1781-8; PMID:12810872; http://dx. doi.org/10.1099/vir.0.19088-0
52. Ivanov AP, Dragunsky EM. ELISA as a possible alternative to the neutralization test for evaluating the immune response to poliovirus vaccines. Exp Rev Vaccines 2005; 4(2):167-72; PMID:15889990; http://dx. doi.org/10.1586/14760584.4.2.167
53. Simhon A, Lifshitz A, Abed Y, Lasch EE, Schoub B, Morag A. How to predict the immune status of poliovirus vaccines. A comparison of virus neutralization at a very low serum dilution versus ELISA in a cohort of infants. Int J Epidemiol 1990; 19 (1):164-8; PMID:2161806; http://dx.doi.org/ 10.1093/ije/19.1.164
54. Hird TR, Grassly NC. Systematic review of mucosal immunity induced by oral and inactivated poliovirus vaccines against virus shedding following oral poliovirus challenge. PloS Pathogens 2012; 8(4):e1002599.
55. Wright PF, Wieland-Alter W, Ilyushina NA, Hoen AG, Arita M, Boesch AW, Ackerman ME, Oberste S M, Pallansch M A, et al. Intestinal immunity is a determinant of clearance of poliovirus after oral vaccination. J Infect Dis 2014; 209 (10): 1628-1634 first published online January 23, 2014 doi:10.1093/infdis/jit671
56. Kaminski RW. Collection and processing of mucosal secretions from mice. Methods Mol Med 1999; 17:329-39; PMID:21380685
57. World Health Organization (WHO). Report of a WHO Informal Consultation on Polio Neutralizing Antibody Assays. WHO/EPI/RD/91.3. Geneva: WHO; 1991.
58. World Health Organization (WHO). Expanded Program on Immunization, editor. Manual for the virological investigation of polio. EPI/GEN/97.01.EPV1. Geneva: WHO; 1997.
59. Karber G. Archiv fuer Experimentelle Pathologie und Pharmakologie. Archiv fuer Experimentelle Pathologie und Pharmakologie 1931; 162:480-3.
60. Arnaboldi PM, Roth-Walter F, Mayer L. Suppression of Th1 and Th17, but not Th2, responses in a CD8 (C) T cell-mediated model of oral tolerance. Mucosal Immunol 2009; 2(5):427-38; PMID:19571798; http://dx.doi.org/10.1038/mi.2009.93