Single-injection vaccines: Progress, challenges, and opportunities

Journal of Controlled Release

Volumn 219, Issue , 2015, Pages 596-609

  McHugh, Kevin J ^a   Guarecuco, Rohiverth ^a   Langer, Robert ^a   Jaklenec, Ana ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Antigen stability; Global health; Microparticles; Protein encapsulation; Release kinetics; Single administration vaccines

Indexed keywords

ANTIGENS; COST EFFECTIVENESS; DEVELOPING COUNTRIES; DISEASES; TARGETED DRUG DELIVERY; VACCINES;

ANTIGEN DELIVERY SYSTEM; CONTROLLED RELEASE; CONTROLLED RELEASE SYSTEMS; GLOBAL HEALTH; IMMUNOLOGICAL MEMORY; MICRO-PARTICLES; PROTEIN ENCAPSULATION; RELEASE KINETICS;

CONTROLLED DRUG DELIVERY;

ALGINIC ACID; ANTIGEN; CHITOSAN; DIPHTHERIA TOXIN; HEPATITIS B SURFACE ANTIGEN; IMMUNOLOGICAL ADJUVANT; MICROSPHERE; POLYGLACTIN; TETANUS TOXOID; VACCINE; DELAYED RELEASE FORMULATION;

ANTIBODY RESPONSE; B LYMPHOCYTE; CONTROLLED DRUG RELEASE; CONTROLLED RELEASE FORMULATION; DRUG DEGRADATION; DRUG DELIVERY DEVICE; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG FORMULATION; DRUG RELEASE; DRUG SAFETY; DRUG STORAGE; EMULSION; HUMAN; IMMUNE RESPONSE; IMMUNOLOGICAL MEMORY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SINGLE DRUG DOSE; T LYMPHOCYTE; TETANUS PROPHYLAXIS; VACCINATION; ADMINISTRATION AND DOSAGE; ANIMAL; DELAYED RELEASE FORMULATION; DRUG ADMINISTRATION; INJECTION; PROCEDURES;

ANIMALS; ANTIGENS; DELAYED-ACTION PREPARATIONS; DRUG ADMINISTRATION SCHEDULE; DRUG DELIVERY SYSTEMS; HUMANS; INJECTIONS; VACCINATION; VACCINES;

EID: 85047696403     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2015.07.029     Document Type: Article

References (200)

1. World Health Organization The world health report 2002 http://www.who.int/whr/2002/en/whr02-en.pdf?ua=1 (accessed May 21, 2015)
2. S.L. Plotkin, and S.A. Plotkin A Short History of Vaccination 4th ed. 2004 WB Saunders Philadelphia
3. S.H.E. Kaufmann, and P.H. Lambert Grand Challenge for the Future. Vaccines for Poverty-related Diseases From Bench to Field 2005 Birkhäuser Verlag Boston
4. Global routine vaccination coverage-2012 Centers for Disease Control and Prevention, MMWR Morb. Mortal. Wkly Rep 62 2013 858-861
5. World Health Organization Global immunization data 2014 http://www.who.int/immunization/monitoring-surveillance/global-immunization-data.pdf?ua=1 (accessed May 16, 2015)
6. B.R. Bloom Vaccines for the third world Nature 342 1989 115 120
7. J. Banchereau, and R.M. Steinman Dendritic cells and the control of immunity Nature 392 1998 245 252
8. C.A. Siegrist Vaccine immunology S. Plotkin, W. Orenstein, P. Offit, Vaccines 6th ed. 2013 Elsevier China 14 32
9. A.S. Clem Fundamentals of vaccine immunology J. Global Infect. Dis. 3 2011 73 78
10. L. Moreland Secondary Immune Response 2004 Springer-Verlag New York
11. T.P. Levine, and B.M. Chain The cell biology of antigen processing Crit. Rev. Biochem. Mol. Biol. 26 1991 439 473
12. J.C. Seidman, S.A. Richard, C. Viboud, and M.A. Miller Quantitative review of antibody response to inactivated seasonal influenza vaccines Influenza Other Respir. Viruses 6 2012 52 62
13. W.L. Atkinson, L.K. Pickering, B. Schwartz, B.G. Weniger, J.K. Iskander, J.C. Watson, and et al. General recommendations on immunization. Recommendations of the Advisory Committee on Immunization Practices (ACIP) and the American Academy of Family Physicians (AAFP) MMWR Recomm. Rep. 51 2002 1 35
14. M.J. Newman, and M.F. Powell Immunological and formulation design considerations for subunit vaccines Pharm. Biotechnol. 6 1995 1 42
15. Centers for Disease Control and Prevention, General Recommendations on Immunization 13th ed. 2015 Washington D.C. Public Health Foundation Washington D.C.
16. R. Langer, and J. Folkman Polymers for the sustained release of proteins and other macromolecules Nature 263 1976 797 800
17. I. Preis, and R.S. Langer A single-step immunization by sustained antigen release J. Immunol. Methods 28 1979 193 197
18. A.M. Hauri, G.L. Armstrong, and Y.J. Hutin The global burden of disease attributable to contaminated injections given in health care settings Int. J. STD AIDS 15 2004 7 16
19. A.L. Creese, N. Sriyabbaya, G. Casabal, and G. Wiseso Cost-effectiveness appraisal of immunization programmes Bull. World Health Organ. 60 1982 621 632
20. C.L. Trotter, and W.J. Edmunds Modelling cost effectiveness of meningococcal serogroup C conjugate vaccination campaign in England and Wales BMJ 324 2002 809
21. J. Clemens, R. Brenner, M. Rao, N. Tafari, and C. Lowe Evaluating new vaccines for developing countries. Efficacy or effectiveness? JAMA 275 1996 390 397
22. A. Batson Sustainable introduction of affordable new vaccines: the targeting strategy Vaccine 16 Suppl. 1998 S93 S98
23. J.L. Cleland Single-administration vaccines: controlled-release technology to mimic repeated immunizations Trends Biotechnol. 17 1999 25 29
24. H. Brem, S. Piantadosi, P.C. Burger, M. Walker, R. Selker, N.A. Vick, and et al. Placebo-controlled trial of safety and efficacy of intraoperative controlled delivery by biodegradable polymers of chemotherapy for recurrent gliomas. The Polymer-brain Tumor Treatment Group Lancet 345 1995 1008 1012
25. Y. Ogawa, H. Okada, M. Yamamoto, and T. Shimamoto In vivo release profiles of leuprolide acetate from microcapsules prepared with polylactic acids or copoly(lactic/glycolic) acids and in vivo degradation of these polymers Chem. Pharm. Bull.(Tokyo) 36 1988 2576 2581
26. A. Sanchez, R.K. Gupta, M.J. Alonso, G.R. Siber, and R. Langer Pulsed controlled-released system for potential use in vaccine delivery J. Pharm. Sci. 85 1996 547 552
27. M.A. Tracy Development and scale-up of a microsphere protein delivery system Biotechnol. Prog. 14 1998 108 115
28. M. van de Weert, W.E. Hennink, and W. Jiskoot Protein instability in poly(lactic-co-glycolic acid) microparticles Pharm. Res. 17 2000 1159 1167
29. B. Baras, M.A. Benoit, and J. Gillard Parameters influencing the antigen release from spray-dried poly(dl-lactide) microparticles Int. J. Pharm. 200 2000 133 145
30. L. Feng, X.R. Qi, X.J. Zhou, Y. Maitani, S.C. Wang, Y. Jiang, and et al. Pharmaceutical and immunological evaluation of a single-dose hepatitis B vaccine using PLGA microspheres J. Control. Release 112 2006 35 42
31. K.S. Jaganathan, Y.U. Rao, P. Singh, D. Prabakaran, S. Gupta, A. Jain, and et al. Development of a single dose tetanus toxoid formulation based on polymeric microspheres: a comparative study of poly(d, l-lactic-co-glycolic acid) versus chitosan microspheres Int. J. Pharm. 294 2005 23 32
32. M. Singh, X.M. Li, H. Wang, J.P. McGee, T. Zamb, W. Koff, and et al. Controlled release microparticles as a single dose diphtheria toxoid vaccine: immunogenicity in small animal models Vaccine 16 1998 346 352
33. K. Makino, T. Mogi, N. Ohtake, M. Yoshida, S. Ando, T. Nakajima, and et al. Pulsatile drug release from poly (lactide-coglycolide) microspheres: how does the composition of the polymer matrices affect the time interval between the initial burst and the pulsatile release of drugs? Colloids Surf. B: Biointerfaces 19 2000 173 179
34. L. Lu, S.J. Peter, M.D. Lyman, H.L. Lai, S.M. Leite, J.A. Tamada, and et al. In vitro and in vivo degradation of porous poly(dl-lactic-co-glycolic acid) foams Biomaterials 21 2000 1837 1845
35. J.R. Garon, and W.A. Orenstein Understanding the host-pathogen interaction saves lives: lessons from vaccines and vaccinations Curr. Opin. Immunol. 36 2015 8 13
36. W.S. Shalaby Development of oral vaccines to stimulate mucosal and systemic immunity: barriers and novel strategies Clin. Immunol. Immunopathol. 74 1995 127 134
37. G. Boehm, M. Peyre, D. Sesardic, R.J. Huskisson, F. Mawas, A. Douglas, and et al. On technological and immunological benefits of multivalent single-injection microsphere vaccines Pharm. Res. 19 2002 1330 1336
38. J.M. Kemp, M. Kajihara, S. Nagahara, A. Sano, M. Brandon, and S. Lofthouse Continuous antigen delivery from controlled release implants induces significant and anamnestic immune responses Vaccine 20 2002 1089 1098
39. R.K. Gupta, M. Singh, and D.T. O'Hagan Poly(lactide-co-glycolide) microparticles for the development of single-dose controlled-release vaccines Adv. Drug Deliv. Rev. 32 1998 225 246
40. W. Jiang, R.K. Gupta, M.C. Deshpande, and S.P. Schwendeman Biodegradable poly(lactic-co-glycolic acid) microparticles for injectable delivery of vaccine antigens Adv. Drug Deliv. Rev. 57 2005 391 410
41. G.E. Visscher, R.L. Robison, H.V. Maulding, J.W. Fong, J.E. Pearson, and G.J. Argentieri Biodegradation of and tissue reaction to 50:50 poly(dl-lactide-co-glycolide) microcapsules J. Biomed. Mater. Res. 19 1985 349 365
42. J.A. Cadee, L.A. Brouwer, W. den Otter, W.E. Hennink, and M.J. van Luyn A comparative biocompatibility study of microspheres based on crosslinked dextran or poly(lactic-co-glycolic)acid after subcutaneous injection in rats J. Biomed. Mater. Res. 56 2001 600 609
43. K.L.S. Smith, M.E. Schimpf, and K.E. Thompson Bioerodible polymers for delivery of macromolecules Adv. Drug Deliv. Rev. 4 1990 343 357
44. J.H. Eldridge, J.K. Staas, J.A. Meulbroek, T.R. Tice, and R.M. Gilley Biodegradable and biocompatible poly(dl-lactide co-glycolide) microspheres as an adjuvant for staphylococcal enterotoxin B toxoid which enhances the level of toxin-neutralizing antibodies Infect. Immun. 59 1991 2978 2986
45. S.P. Schwendeman, M. Cardamone, A. Klibanov, and R. Langer Stability of proteins and their delivery from biodegradable polymer microspheres, In: S. Cohenand, H. Bernstein, (Eds.), Microparticulate systems for the delivery of proteins and vaccines 1996 Marcel Dekker New York 1 49
46. L.R. Beck, D.R. Cowsar, and D.H. Lewis Systemic and local delivery of contraceptive steroids using biodegradable microspheres E.S.E. Hafez, W.A.A. Van Os, Biodegradables and Delivery Systems for Contraception 1980 MTP Press Lancaster, England 63 82
47. N. Samadi, A. Abbadessa, A. Di Stefano, C.F. van Nostrum, T. Vermonden, S. Rahimian, and et al. The effect of lauryl capping group on protein release and degradation of poly(d, l-lactic-co-glycolic acid) particles J. Control. Release 172 2013 436 443
48. H.K. Makadia, and S.J. Siegel Poly lactic-co-glycolic acid (PLGA) as biodegradable controlled drug delivery carrier Polymers (Basel) 3 2011 1377 1397
49. A.C. Richards Grayson, I.S. Choi, B.M. Tyler, P.P. Wang, H. Brem, M.J. Cima, and R. Langer Multi-pulse drug delivery from a resorbable polymeric microchip device Nat. Mater. 2 2003 767 772
50. P. Gentile, V. Chiono, I. Carmagnola, and P.V. Hatton An overview of poly(lactic-co-glycolic) acid (PLGA)-based biomaterials for bone tissue engineering Int. J. Mol. Sci. 15 2014 3640 3659
51. Y. Li, Y. Pei, X. Zhang, Z. Gu, Z. Zhou, W. Yuan, and et al. PEGylated PLGA nanoparticles as protein carriers: synthesis, preparation and biodistribution in rats J. Control. Release 71 2001 203 211
52. J.K. Kim, H.J. Kim, J.Y. Chung, J.H. Lee, S.B. Young, and Y.H. Kim Natural and synthetic biomaterials for controlled drug delivery Arch. Pharm. Res. 37 2014 60 68
53. X. Li, X. Kong, S. Shi, X. Zheng, G. Guo, Y. Wei, and et al. Preparation of alginate coated chitosan microparticles for vaccine delivery BMC Biotechnol. 8 2008 89
54. A.A. Lugade, D.J. Bharali, V. Pradhan, G. Elkin, S.A. Mousa, and Y. Thanavala Single low-dose un-adjuvanted HBsAg nanoparticle vaccine elicits robust, durable immunity Nanomedicine 9 2013 923 934
55. B. Sayin, S. Somavarapu, X.W. Li, M. Thanou, D. Sesardic, H.O. Alpar, and et al. Mono-N-carboxymethyl chitosan (MCC) and N-trimethyl chitosan (TMC) nanoparticles for non-invasive vaccine delivery Int. J. Pharm. 363 2008 139 148
56. X. Zheng, Y. Huang, C. Zheng, S. Dong, and W. Liang Alginate-chitosan-PLGA composite microspheres enabling single-shot hepatitis B vaccination AAPS J. 12 2010 519 524
57. T.L. Bowersock, H. HogenEsch, M. Suckow, P. Guimond, S. Martin, D. Borie, and et al. Oral vaccination of animals with antigens encapsulated in alginate microspheres Vaccine 17 1999 1804 1811
58. B. Kim, T. Bowersock, P. Griebel, A. Kidane, L.A. Babiuk, M. Sanchez, and et al. Mucosal immune responses following oral immunization with rotavirus antigens encapsulated in alginate microspheres J. Control. Release 85 2002 191 202
59. F. Sarei, N.M. Dounighi, H. Zolfagharian, P. Khaki, and S.M. Bidhendi Alginate nanoparticles as a promising adjuvant and vaccine delivery system Indian J. Pharm. Sci. 75 2013 442 449
60. M. Higaki, Y. Azechi, T. Takase, R. Igarashi, S. Nagahara, A. Sano, and et al. Collagen minipellet as a controlled release delivery system for tetanus and diphtheria toxoid Vaccine 19 2001 3091 3096
61. S. Lofthouse, S. Nagahara, B. Sedgmen, G. Barcham, M. Brandon, and A. Sano The application of biodegradable collagen minipellets as vaccine delivery vehicles in mice and sheep Vaccine 19 2001 4318 4327
62. J.M. Pachence, M.P. Bohrer, and J. Kohn Biodegradable Polymers 3rd ed. 2007 Elsevier Academic Press Boston
63. M.I. Sabir, X. Xu, and L. Li A review on biodegradable polymeric materials for bone tissue engineering applications J. Mater. Sci. 44 2009 5713 5724
64. Y.Y. Yang, T.S. Chung, and N.P. Ng Morphology, drug distribution, and in vitro release profiles of biodegradable polymeric microspheres containing protein fabricated by double-emulsion solvent extraction/evaporation method Biomaterials 22 2001 231 241
65. Y. Tabata, S. Gutta, and R. Langer Controlled delivery systems for proteins using polyanhydride microspheres Pharm. Res. 10 1993 487 496
66. Y. Tabata, and R. Langer Polyanhydride microspheres that display near-constant release of water-soluble model drug compounds Pharm. Res. 10 1993 391 399
67. A.S. Determan, B.G. Trewyn, V.S. Lin, M. Nilsen-Hamilton, and B. Narasimhan Encapsulation, stabilization, and release of BSA-FITC from polyanhydride microspheres J. Control. Release 100 2004 97 109
68. A.S. Determan, J.H. Wilson, M.J. Kipper, M.J. Wannemuehler, and B. Narasimhan Protein stability in the presence of polymer degradation products: consequences for controlled release formulations Biomaterials 27 2006 3312 3320
69. M.P. Torres, A.S. Determan, G.L. Anderson, S.K. Mallapragada, and B. Narasimhan Amphiphilic polyanhydrides for protein stabilization and release Biomaterials 28 2007 108 116
70. L.K. Petersen, Y. Phanse, A.E. Ramer-Tait, M.J. Wannemuehler, and B. Narasimhan Amphiphilic polyanhydride nanoparticles stabilize Bacillus anthracis protective antigen Mol. Pharm. 9 2012 874 882
71. P.N. Wuthrich, S.Y., B.K. Fritzinger, K.V. Roskos, and J. Heller Pulsatile and delayed release of lysozyme from ointment-like poly(ortho esters) J. Control. Release 21 1992 191 200
72. J.R. Heller, A.F. Rime, S.S. Rao, B.K. Fritzinger, and S.Y. Ng Poly(ortho esters) for the Pulsed and Continuous Delivery of Peptides and Proteins 1995 Harwood Academic Publishers Chur, Switzerland
73. C. Wang, Q. Ge, D. Ting, D. Nguyen, H.R. Shen, J. Chen, and et al. Molecularly engineered poly(ortho ester) microspheres for enhanced delivery of DNA vaccines Nat. Mater. 3 2004 190 196
74. D.N. Nguyen, S.S. Raghavan, L.M. Tashima, E.C. Lin, S.J. Fredette, R.S. Langer, and et al. Enhancement of poly(orthoester) microspheres for DNA vaccine delivery by blending with poly(ethylenimine) Biomaterials 29 2008 2783 2793
75. S. Ohtake, D. Lechuga-Ballesteros, V. Truong-Le, and E.J. Patzer Strategies for Heat-stable Vaccines 1 ed. 2015 John Wiley & Sons Hoboken, NJ
76. A. Galazaka, J. Milstien, and M. Zaffran Thermostability of Vaccines: Global Programme for Vaccines and Immunization 1998 WHO Geneva
77. M. Peyre, D. Sesardic, H.P. Merkle, B. Gander, and P. Johansen An experimental divalent vaccine based on biodegradable microspheres induces protective immunity against tetanus and diphtheria J. Pharm. Sci. 92 2003 957 966
78. M.J. Alonso, S. Cohen, T.G. Park, R.K. Gupta, G.R. Siber, and R. Langer Determinants of release rate of tetanus vaccine from polyester microspheres Pharm. Res. 10 1993 945 953
79. M.J. Alonso, R.K. Gupta, C. Min, G.R. Siber, and R. Langer Biodegradable microspheres as controlled-release tetanus toxoid delivery systems Vaccine 12 1994 299 306
80. R.K. Gupta, J. Alroy, M.J. Alonso, R. Langer, and G.R. Siber Chronic local tissue reactions, long-term immunogenicity and immunologic priming of mice and guinea pigs to tetanus toxoid encapsulated in biodegradable polymer microspheres composed of poly lactide-co-glycolide polymers Vaccine 15 1997 1716 1723
81. A.C. Chang, and R.K. Gupta Stabilization of tetanus toxoid in poly(dl-lactic-co-glycolic acid) microspheres for the controlled release of antigen J. Pharm. Sci. 85 1996 129 132
82. M. Tobio, S.P. Schwendeman, Y. Guo, J. McIver, R. Langer, and M.J. Alonso Improved immunogenicity of a core-coated tetanus toxoid delivery system Vaccine 18 1999 618 622
83. S.P. Schwendeman, H.R. Costantino, R.K. Gupta, G.R. Siber, A.M. Klibanov, and R. Langer Stabilization of tetanus and diphtheria toxoids against moisture-induced aggregation Proc. Natl. Acad. Sci. U. S. A. 92 1995 11234 11238
84. L. Shi, M.J. Caulfield, R.T. Chern, R.A. Wilson, G. Sanyal, and D.B. Volkin Pharmaceutical and immunological evaluation of a single-shot hepatitis B vaccine formulated with PLGA microspheres J. Pharm. Sci. 91 2002 1019 1035
85. M. Singh, X.M. Li, J.P. McGee, T. Zamb, W. Koff, C.Y. Wang, and et al. Controlled release microparticles as a single dose hepatitis B vaccine: evaluation of immunogenicity in mice Vaccine 15 1997 475 481
86. M. Singh, A. Singh, and G.P. Talwar Controlled delivery of diphtheria toxoid using biodegradable poly(d, l-lactide) microcapsules Pharm. Res. 8 1991 958 961
87. M.S.O. Singh, A. Singh, and G.P. Talwar Immunogenicity studies on diphtheria toxoid loaded biodegradable microspheres Int. J. Pharm. 85 1992 R5 R8
88. K.M. Reddin, T.J. Easterbrook, S.M. Eley, P. Russell, V.A. Mobsby, D.H. Jones, and et al. Comparison of the immunological and protective responses elicited by microencapsulated formulations of the F1 antigen from Yersinia pestis Vaccine 16 1998 761 767
89. S.J. Elvin, J.E. Eyles, K.A. Howard, E. Ravichandran, S. Somavarappu, H.O. Alpar, and et al. Protection against bubonic and pneumonic plague with a single dose microencapsulated sub-unit vaccine Vaccine 24 2006 4433 4439
90. N. Kofler, C. Ruedl, J. Klima, H. Recheis, G. Bock, G. Wick, and et al. Preparation and characterization of poly-(d, l lactide-co-glycolide) and poly-(L-lactic acid) microspheres with entrapped pneumotropic bacterial antigens J. Immunol. Methods 192 1996 25 35
91. C. Arigita, J. van den Berg, K. Wensink, M. van Steenbergen, W.E. Hennink, D.J. Crommelin, and et al. Immunogenicity of meningococcal PorA formulations encapsulated in biodegradable microspheres Eur. J. Pharm. Sci. 21 2004 131 141
92. N. Dhiman, and G.K. Khuller Protective efficacy of mycobacterial 71-kDa cell wall associated protein using poly (dl-lactide-co-glycolide) microparticles as carrier vehicles FEMS Immunol. Med. Microbiol. 21 1998 19 28
93. A.M. Arenas-Gamboa, T.A. Ficht, D.S. Davis, P.H. Elzer, A. Wong-Gonzalez, and A.C. Rice-Ficht Enhanced immune response of red deer (Cervus elaphus) to live rb51 vaccine strain using composite microspheres J. Wildl. Dis. 45 2009 165 173
94. D. Chen, and D. Kristensen Opportunities and challenges of developing thermostable vaccines Expert Rev. Vaccines 8 2009 547 557
95. C. B'Hymer Residual solvent testing: a review of gas-chromatographic and alternative techniques Pharm. Res. 20 2003 337 344
96. J.M. Anderson, A. Rodriguez, and D.T. Chang Foreign body reaction to biomaterials Semin. Immunol. 20 2008 86 100
97. R.A. Goldsby, T.J. Kindt, and B.A. Osborne Leukocyte Migration and Inflammation 2000 W H Freeman & Co New York
98. D.W. Scheifele, S.A. Halperin, and A.C. Ferguson Assessment of injection site reactions to an acellular pertussis-based combination vaccine, including novel use of skin tests with vaccine antigens Vaccine 19 2001 4720 4726
99. F. Madani, M. Bessodes, A. Lakrouf, C. Vauthier, D. Scherman, and J.C. Chaumeil PEGylation of microspheres for therapeutic embolization: preparation, characterization and biological performance evaluation Biomaterials 28 2007 1198 1208
100. D.W. Dresser, and G. Gowland Immunological paralysis induced in adult rabbits by small amounts of a protein antigen Nature 203 1964 733 736
101. F.J. Dixon, and P.H. Mauer Immunologic unresponsiveness induced by protein antigens J. Exp. Med. 101 1955 245 257
102. N.A. Mitchison Induction of immunological paralysis in two zones of dosage Proc. R. Soc. Lond. B Biol. Sci. 161 1964 275 292
103. S. Lofthouse Immunological aspects of controlled antigen delivery Adv. Drug Deliv. Rev. 54 2002 863 870
104. J.L. Cleland, M.F. Powell, and S.J. Shire The development of stable protein formulations: a close look at protein aggregation, deamidation, and oxidation Crit. Rev. Ther. Drug Carrier Syst. 10 1993 307 377
105. D.F. Chu, X.Q. Fu, W.H. Liu, K. Liu, and Y.X. Li Pharmacokinetics and in vitro and in vivo correlation of huperzine A loaded poly(lactic-co-glycolic acid) microspheres in dogs Int. J. Pharm. 325 2006 116 123
106. J.M.R. Ramstack, M.G.I., S.E. Zale, J.M. Hotz, O.L. Johnson, Preparation of injectable suspensions having improved injectability. US Patent Office 2008, US6495164.
107. H. Zhang, Y. Gao, W. Lv, C. Jiao, M. Duan, H. Liu, and et al. Preparation of bleomycin A2-PLGA microspheres and related in vitro and in vivo studies J. Pharm. Sci. 100 2011 2790 2800
108. F. Lu, I. Boutselis, R.F. Borch, and H. Hogenesch Control of antigen-binding to aluminum adjuvants and the immune response with a novel phosphonate linker Vaccine 31 2013 4362 4367
109. L. Frost, P. Johansen, S. Pedersen, N. Veien, P.A. Ostergaard, and M.H. Nielsen Persistent subcutaneous nodules in children hyposensitized with aluminium-containing allergen extracts Allergy 40 1985 368 372
110. P.R. Pittman Aluminum-containing vaccine associated adverse events: role of route of administration and gender Vaccine 20 Suppl. 3 2002 S48 S50
111. T. Jefferson, M. Rudin, and C. Di Pietrantonj Adverse events after immunisation with aluminium-containing DTP vaccines: systematic review of the evidence Lancet Infect. Dis. 4 2004 84 90
112. A.T. Glenny, C.G. Pope, H. Waddington, and U. Wallace Immunological notes XVII-XXIV J. Pathol. Bacteriol. 29 1926 31 40
113. M.A. Aprile, and A.C. Wardlaw Aluminium compounds as adjuvants for vaccines and toxoids in man: a review Can. J. Public Health 57 1966 343 360
114. S. Shirodkar, R.L. Hutchinson, D.L. Perry, J.L. White, and S.L. Hem Aluminum compounds used as adjuvants in vaccines Pharm. Res. 7 1990 1282 1288
115. R. Gluck, R. Mischler, B. Finkel, J.U. Que, B. Scarpa, and S.J. Cryz Jr. Immunogenicity of new virosome influenza vaccine in elderly people Lancet 344 1994 160 163
116. A. Podda The adjuvanted influenza vaccines with novel adjuvants: experience with the MF59-adjuvanted vaccine Vaccine 19 2001 2673 2680
117. V.K. Sondak, and J.A. Sosman Results of clinical trials with an allogenic melanoma tumor cell lysate vaccine: Melacine Semin. Cancer Biol. 13 2003 409 415
118. H. Takada, and S. Kotani Structural requirements of lipid A for endotoxicity and other biological activities Crit. Rev. Microbiol. 16 1989 477 523
119. K.G. Desai, and S.P. Schwendeman Active self-healing encapsulation of vaccine antigens in PLGA microspheres J. Control. Release 165 2013 62 74
120. S. Pandit, E. Cevher, M.G. Zariwala, S. Somavarapu, and H.O. Alpar Enhancement of immune response of HBsAg loaded poly (L-lactic acid) microspheres against hepatitis B through incorporation of alum and chitosan J. Microencapsul. 24 2007 539 552
121. I. Esparza, and T. Kissel Parameters affecting the immunogenicity of microencapsulated tetanus toxoid Vaccine 10 1992 714 720
122. A.M. Hafner, B. Corthesy, and H.P. Merkle Particulate formulations for the delivery of poly(I:C) as vaccine adjuvant Adv. Drug Deliv. Rev. 65 2013 1386 1399
123. D.T. O'Hagan, and N.M. Valiante Recent advances in the discovery and delivery of vaccine adjuvants Nat. Rev. Drug Discov. 2 2003 727 735
124. D.T. O'Hagan, H. Jeffery, and S.S. Davis Long-term antibody responses in mice following subcutaneous immunization with ovalbumin entrapped in biodegradable microparticles Vaccine 11 1993 965 969
125. K.D. Newman, P. Elamanchili, G.S. Kwon, and J. Samuel Uptake of poly(d, l-lactic-co-glycolic acid) microspheres by antigen-presenting cells in vivo J. Biomed. Mater. Res. 60 2002 480 486
126. M. Peyre, R. Fleck, D. Hockley, B. Gander, and D. Sesardic In vivo uptake of an experimental microencapsulated diphtheria vaccine following sub-cutaneous immunisation Vaccine 22 2004 2430 2437
127. K.J. Maloy, I. Erdmann, V. Basch, S. Sierro, T.A. Kramps, R.M. Zinkernagel, and et al. Intralymphatic immunization enhances DNA vaccination Proc. Natl. Acad. Sci. U. S. A. 98 2001 3299 3303
128. P. Johansen, A.C. Haffner, F. Koch, K. Zepter, I. Erdmann, K. Maloy, and et al. Direct intralymphatic injection of peptide vaccines enhances immunogenicity Eur. J. Immunol. 35 2005 568 574
129. C.M. Jewell, S.C. Lopez, and D.J. Irvine In situ engineering of the lymph node microenvironment via intranodal injection of adjuvant-releasing polymer particles Proc. Natl. Acad. Sci. U. S. A. 108 2011 15745 15750
130. J.I. Andorko, L.H. Tostanoski, E. Solano, M. Mukhamedova, and C.M. Jewell Intra-lymph node injection of biodegradable polymer particles J. Vis. Exp. 2014 e50984
131. L. Thiele, H.P. Merkle, and E. Walter Phagocytosis and phagosomal fate of surface-modified microparticles in dendritic cells and macrophages Pharm. Res. 20 2003 221 228
132. A. Gamvrellis, D. Leong, J.C. Hanley, S.D. Xiang, P. Mottram, and M. Plebanski Vaccines that facilitate antigen entry into dendritic cells Immunol. Cell Biol. 82 2004 506 516
133. N. Brandhonneur, F. Chevanne, V. Vie, B. Frisch, R. Primault, M.F. Le Potier, and et al. Specific and non-specific phagocytosis of ligand-grafted PLGA microspheres by macrophages Eur. J. Pharm. Sci. 36 2009 474 485
134. R. Nakaoka, Y. Tabata, and Y. Ikada Adjuvant effect of biodegradable poly(dl-lactic acid) granules capable for antigen release following intraperitoneal injection Vaccine 14 1996 1671 1676
135. K. Izutsu Stabilization of therapeutic proteins by chemical and physical methods Methods Mol. Biol. 308 2005 287 292
136. H. Sah Protein behavior at the water/methylene chloride interface J. Pharm. Sci. 88 1999 1320 1325
137. W. Lu, and T.G. Park Protein release from poly(lactic-co-glycolic acid) microspheres: protein stability problems PDA J. Pharm. Sci. Technol. 49 1995 13 19
138. M. Morlock, H. Koll, G. Winter, and T. Kissel Microencapsulation of rh-erythropoietin using biodegradable poly(C, L-lactide-co-glycolide): protein stability and the effects of stabilizing excipients Eur. J. Pharm. Biopharm. 43 1997 29 36
139. M.F. Zambaux, F. Bonneaux, R. Gref, E. Dellacherie, and C. Vigneron Preparation and characterization of protein C-loaded PLA nanoparticles J. Control. Release 60 1999 179 188
140. K.S. Suslick, D.A. Hammerton, and R.D. Cline The sonochemical hot spot J. Am. Chem. Soc. 108 1986 5641 5642
141. H. Rafati, E.C. Lavelle, A.G. Coombes, S. Stolnik, J. Holland, and S.S. Davis The immune response to a model antigen associated with PLG microparticles prepared using different surfactants Vaccine 15 1997 1888 1897
142. H. Sah Protein instability toward organic solvent/water emulsification: implications for protein microencapsulation into microspheres PDA J. Pharm. Sci. Technol. 53 1999 3 10
143. H. Sah Stabilization of proteins against methylene chloride/water interface-induced denaturation and aggregation J. Control. Release 58 1999 143 151
144. J.L. Cleland, and A.J. Jones Stable formulations of recombinant human growth hormone and interferon-gamma for microencapsulation in biodegradable microspheres Pharm. Res. 13 1996 1464 1475
145. H. Kraan, P. van Herpen, G. Kersten, and J.P. Amorij Development of thermostable lyophilized inactivated polio vaccine Pharm. Res. 31 2014 2618 2629
146. J. Giri, W.J. Li, R.S. Tuan, and M.T. Cicerone Stabilization of proteins by nanoencapsulation in sugar-glass for tissue engineering and drug delivery applications Adv. Mater. 23 2011 4861 4867
147. R. Alcock, M.G. Cottingham, C.S. Rollier, J. Furze, S.D. De Costa, M. Hanlon, and et al. Long-term thermostabilization of live poxviral and adenoviral vaccine vectors at supraphysiological temperatures in carbohydrate glass Sci. Transl. Med. 2 2010 19ra2
148. S. Singh, A. Singh, M.A. Aziz, S.M. Waheed, R. Bhat, and R. Bhatnagar Thermal inactivation of protective antigen of Bacillus anthracis and its prevention by polyol osmolytes Biochem. Biophys. Res. Commun. 322 2004 1029 1037
149. M. Sola-Penna, and J.R. Meyer-Fernandes Stabilization against thermal inactivation promoted by sugars on enzyme structure and function: why is trehalose more effective than other sugars? Arch. Biochem. Biophys. 360 1998 10 14
150. R. Politi, and D. Harries Enthalpically driven peptide stabilization by protective osmolytes Chem. Commun. (Camb.) 46 2010 6449 6451
151. R. Gilman-Politi, and D. Harries Unraveling the molecular mechanism of enthalpy driven peptide folding by polyol osmolytes J. Chem. Theory Comput. 7 2011 3816 3828
152. F. Wan, M.J. Maltesen, S.K. Andersen, S. Bjerregaard, C. Foged, J. Rantanen, and et al. One-step production of protein-loaded PLGA microparticles via spray drying using 3-fluid nozzle Pharm. Res. 31 2014 1967 1977
153. O.L. Johnson, J.L. Cleland, H.J. Lee, M. Charnis, E. Duenas, W. Jaworowicz, and et al. A month-long effect from a single injection of microencapsulated human growth hormone Nat. Med. 2 1996 795 799
154. I.G. Loscertales, A. Barrero, I. Guerrero, R. Cortijo, M. Marquez, and A.M. Ganan-Calvo Micro/nano encapsulation via electrified coaxial liquid jets Science 295 2002 1695 1698
155. O.H. Franssen, and W.E. Hennink A novel preparation method for polymeric microparticles without the use of organic solvents Int. J. Pharm. 168 1998 1 7
156. R.J. Stenekes, O. Franssen, E.M. van Bommel, D.J. Crommelin, and W.E. Hennink The preparation of dextran microspheres in an all-aqueous system: effect of the formulation parameters on particle characteristics Pharm. Res. 15 1998 557 561
157. S.E. Reinhold, K.G. Desai, L. Zhang, K.F. Olsen, and S.P. Schwendeman Self-healing microencapsulation of biomacromolecules without organic solvents Angew. Chem. Int. Ed. Engl. 51 2012 10800 10803
158. R. Edelman, R.G. Russell, G. Losonsky, B.D. Tall, C.O. Tacket, M.M. Levine, and et al. Immunization of rabbits with enterotoxigenic E. coli colonization factor antigen (CFA/I) encapsulated in biodegradable microspheres of poly (lactide-co-glycolide) Vaccine 11 1993 155 158
159. J.B. Milstien, S.M. Lemon, and P.F. Wright Development of a more thermostable poliovirus vaccine J. Infect. Dis. 175 Suppl. 1 1997 S247 S253
160. H.R. Constantino Excipients for Use in Lyophilized Pharmaceutical Peptide, Protein, and Other Bioproducts 2004 AAPS Press Arlington, VA
161. J.F. Carpenter, M.J. Pikal, B.S. Chang, and T.W. Randolph Rational design of stable lyophilized protein formulations: some practical advice Pharm. Res. 14 1997 969 975
162. N. Guo, I. Puhlev, D.R. Brown, J. Mansbridge, and F. Levine Trehalose expression confers desiccation tolerance on human cells Nat. Biotechnol. 18 2000 168 171
163. J.K. Kaushik, and R. Bhat Why is trehalose an exceptional protein stabilizer? An analysis of the thermal stability of proteins in the presence of the compatible osmolyte trehalose J. Biol. Chem. 278 2003 26458 26465
164. N.K. Jain, and I. Roy Effect of trehalose on protein structure Protein Sci. 18 2009 24 36
165. P. Johansen, Y. Men, R. Audran, G. Corradin, H.P. Merkle, and B. Gander Improving stability and release kinetics of microencapsulated tetanus toxoid by co-encapsulation of additives Pharm. Res. 15 1998 1103 1110
166. S. Pisal, G. Wawde, S. Salvankar, S. Lade, and S. Kadam Vacuum foam drying for preservation of LaSota virus: effect of additives AAPS PharmSciTech 7 2006 60
167. G. Zhu, S.R. Mallery, and S.P. Schwendeman Stabilization of proteins encapsulated in injectable poly (lactide-coglycolide) Nat. Biotechnol. 18 2000 52 57
168. W.R. Liu, R. Langer, and A.M. Klibanov Moisture-induced aggregation of lyophilized proteins in the solid state Biotechnol. Bioeng. 37 1991 177 184
169. A. Shenderova, T.G. Burke, and S.P. Schwendeman The acidic microclimate in poly(lactide-co-glycolide) microspheres stabilizes camptothecins Pharm. Res. 16 1999 241 248
170. K. Fu, D.W. Pack, A.M. Klibanov, and R. Langer Visual evidence of acidic environment within degrading poly(lactic-co-glycolic acid) (PLGA) microspheres Pharm. Res. 17 2000 100 106
171. P.G. Shao, and L.C. Bailey Stabilization of pH-induced degradation of porcine insulin in biodegradable polyester microspheres Pharm. Dev. Technol. 4 1999 633 642
172. M.J. Blanco-Prieto, E. Leo, F. Delie, A. Gulik, P. Couvreur, and E. Fattal Study of the influence of several stabilizing agents on the entrapment and in vitro release of pBC 264 from poly(lactide-co-glycolide) microspheres prepared by a W/O/W solvent evaporation method Pharm. Res. 13 1996 1127 1129
173. S.P. Apte, and S.O. Ugwu Effect of buffers and stabilizers on vaccine stability and efficacy M. Singh, I.K. Srivastava, Development of Vaccines: From Discovery to Clinical Testing 2011 John Wiley & Sons Hoboken, NJ
174. S.O. Ugwu, and S.P. Apte The effect of buffers on protein conformational stability Pharm. Technol. 28 2004 86 113
175. B. Rombaut, B. Verheyden, K. Andries, and A. Boeye Thermal inactivation of oral polio vaccine: contribution of RNA and protein inactivation J. Virol. 68 1994 6454 6457
176. K.S. Jaganathan, P. Singh, D. Prabakaran, V. Mishra, and S.P. Vyas Development of a single-dose stabilized poly(d, l-lactic-co-glycolic acid) microspheres-based vaccine against hepatitis B J. Pharm. Pharmacol. 56 2004 1243 1250
177. N.K. Varde, and D.W. Pack Influence of particle size and antacid on release and stability of plasmid DNA from uniform PLGA microspheres J. Control. Release 124 2007 172 180
178. M.L. Houchin, S.A. Neuenswander, and E.M. Topp Effect of excipients on PLGA film degradation and the stability of an incorporated peptide J. Control. Release 117 2007 413 420
179. T. Kissel, R. Koneberg, A.K. Hilbert, and K.D. Hungerer Microencapsulation of antigens using biodegradable polyesters: facts and phantasies Behring Inst. Mitt. 172-83 1997
180. M. Shapiro-Shelef, and K. Calame Regulation of plasma-cell development Nat. Rev. Immunol. 5 2005 230 242
181. M.S. Shive, and J.M. Anderson Biodegradation and biocompatibility of PLA and PLGA microspheres Adv. Drug Deliv. Rev. 28 1997 5 24
182. P. Johansen, T. Storni, L. Rettig, Z. Qiu, A. Der-Sarkissian, K.A. Smith, and et al. Antigen kinetics determines immune reactivity Proc. Natl. Acad. Sci. U. S. A. 105 2008 5189 5194
183. L.D. MacDonald, A. Fuentes-Ortega, L. Sammatur, and M. Mansour Efficacy of a single dose hepatitis B depot vaccine Vaccine 28 2010 7143 7145
184. X.M. Deng, X.H. Li, M.L. Yuan, C.D. Xiong, Z.T. Huang, W.X. Jia, and et al. Optimization of preparative conditions for poly-dl-lactide-polyethylene glycol microspheres with entrapped Vibrio cholera antigens J. Control. Release 58 1999 123 131
185. H. Ahman, H. Kayhty, A. Vuorela, O. Leroy, and J. Eskola Dose dependency of antibody response in infants and children to pneumococcal polysaccharides conjugated to tetanus toxoid Vaccine 17 1999 2726 2732
186. J.A. Tamada, and R. Langer Erosion kinetics of hydrolytically degradable polymers Proc. Natl. Acad. Sci. USA 90 1993 552 556
187. J. Siepmann, K. Elkharraz, F. Siepmann, and D. Klose How autocatalysis accelerates drug release from PLGA-based microparticles: a quantitative treatment Biomacromolecules 6 2005 2312 2319
188. A. Schadlich, S. Kempe, and K. Mader Non-invasive in vivo characterization of microclimate pH inside in situ forming PLGA implants using multispectral fluorescence imaging J. Control. Release 179 2014 52 62
189. M.A. Tracy, K.L. Ward, L. Firouzabadian, Y. Wang, N. Dong, R. Qian, and et al. Factors affecting the degradation rate of poly(lactide-co-glycolide) microspheres in vivo and in vitro Biomaterials 20 1999 1057 1062
190. P. Menei, V. Daniel, C. Montero-Menei, M. Brouillard, A. Pouplard-Barthelaix, and J.P. Benoit Biodegradation and brain tissue reaction to poly(d, l-lactide-co-glycolide) microspheres Biomaterials 14 1993 470 478
191. Q. Wang, M.T. Tan, B.P. Keegan, M.A. Barry, and M.J. Heffernan Time course study of the antigen-specific immune response to a PLGA microparticle vaccine formulation Biomaterials 35 2014 8385 8393
192. M.T. Lubet, and J.R. Kettman Regulation of the primary immune response to ovalbumin in mice: activation of T cells mediating delayed-type hypersensitivity, nonspecific help, and specific help, and their sensitivity to radiation J. Immunol. 123 1979 426 433
193. T. Uchida, and S. Goto Oral delivery of poly(lactide-co-glycolide) microspheres containing ovalbumin as vaccine formulation: particle size study Biol. Pharm. Bull. 17 1994 1272 1276
194. R.K. Kumar, C. Herbert, and P.S. Foster The "classical" ovalbumin challenge model of asthma in mice Curr. Drug Targets 9 2008 485 494
195. B.R. Sloat, M.A. Sandoval, A.M. Hau, Y. He, and Z. Cui Strong antibody responses induced by protein antigens conjugated onto the surface of lecithin-based nanoparticles J. Control. Release 141 2010 93 100
196. G. Crotts, and T.G. Park Protein delivery from poly(lactic-co-glycolic acid) biodegradable microspheres: release kinetics and stability issues J. Microencapsul. 15 1998 699 713
197. R.C. Mehta, R. Jeyanthi, S. Calis, B.C. Thanoo, K.W. Burton, and P.P. DeLuca Biodegradable microspheres as depot systems for parenteral delivery of peptide drugs J. Control. Release 29 1994 375 384
198. I. Grizzi, H. Garreau, S. Li, and M. Vert Hydrolytic degradation of devices based on poly(dl-lactic acid) size-dependence Biomaterials 16 1995 305 311
199. Y.K. Katare, and A.K. Panda Influences of excipients on in vitro release and in vivo performance of tetanus toxoid loaded polymer particles Eur. J. Pharm. Sci. 28 2006 179 188
200. P. Johansen, L. Moon, H. Tamber, H.P. Merkle, B. Gander, and D. Sesardic Immunogenicity of single-dose diphtheria vaccines based on PLA/PLGA microspheres in guinea pigs Vaccine 18 2000 209 215