Development of thermostable vaccine adjuvants

References

• Karp CL, Lans D, Esparza J, et al., Evaluating the value proposition for improving vaccine thermostability to increase vaccine impact in low and middle-income countries. Vaccine. 2015;33(30): 3471–3479.
   PubMed Web of Science ®Google Scholar
• Lee BY, Wedlock PT, Haidari LA, et al. Economic impact of thermostable vaccines. Vaccine. 2017;35(23):3135–3142.
   PubMed Web of Science ®Google Scholar
• Kristensen DD, Lorenson T, Bartholomew K, et al. Can thermostable vaccines help address cold-chain challenges? Results from stakeholder interviews in six low- and middle-income countries. Vaccine. 2016;34(7):899–904.
   PubMed Web of Science ®Google Scholar
• Kristensen D, Chen D. Stabilization of vaccines: lessons learned. Hum Vaccines. 2010;6(3):227–231.
   PubMed Web of Science ®Google Scholar
• Kumru OS, Joshi SB, Smith DE, et al. Vaccine instability in the cold chain: mechanisms, analysis and formulation strategies. Biologicals. 2014;42(5):237–259.
   PubMed Web of Science ®Google Scholar
• McKee AS, Munks MW, Marrack P. How do adjuvants work? Important considerations for new generation adjuvants. Immunity. 2007;27(5):687–690.
   PubMed Web of Science ®Google Scholar
• Reed SG, Orr MT, Fox CB. Key roles of adjuvants in modern vaccines. Nat Med. 2013;19(12):1597–1608.
   PubMed Web of Science ®Google Scholar
• Campbell JD. Development of the CpG Adjuvant 1018: a case study. In: Fox CB, editor. Vaccine adjuvants: methods and protocols. New York: Springer New York; 2017. p. 15–27.
   Google Scholar
• Fox CB, Haensler J. An update on safety and immunogenicity of vaccines containing emulsion-based adjuvants. Expert Rev Vaccines. 2013;12(7):747–758.
   PubMed Web of Science ®Google Scholar
• HogenEsch H, O’Hagan DT, Fox CB. Optimizing the utilization of aluminum adjuvants in vaccines: you might just get what you want. Npj Vaccines. 2018;3(1):51.
   PubMed Web of Science ®Google Scholar
• Singh M, O’Hagan D. Advances in vaccine adjuvants. Nat Biotechnol. 1999;17(11):1075–1081.
   PubMed Web of Science ®Google Scholar
• Didierlaurent AM, Collignon C, Bourguignon P, et al. Enhancement of adaptive immunity by the human vaccine adjuvant as01 depends on activated dendritic cells. J Immunol. 2014;193(4):1920–1930.
   PubMed Web of Science ®Google Scholar
• Hanson CM, George AM, Sawadogo A, et al. Is freezing in the vaccine cold chain an ongoing issue? A literature review. Vaccine. 2017;35(17):2127–2133.
   PubMed Web of Science ®Google Scholar
• Das MK, Arora NK, Mathew T, et al. Temperature integrity and exposure of vaccines to suboptimal temperatures in cold chain devices at different levels in three states of India. Trop Dis Travel Med Vaccines. 2020; 6:8.
   PubMedGoogle Scholar
• Zipursky S, Djingarey MH, Lodjo JC, et al. Benefits of using vaccines out of the cold chain: delivering meningitis A vaccine in a controlled temperature chain during the mass immunization campaign in Benin. Vaccine. 2014;32(13):1431–1435.
   PubMed Web of Science ®Google Scholar
• Lydon P, Zipursky S, Tevi-Benissan C, et al. Economic benefits of keeping vaccines at ambient temperature during mass vaccination: the case of meningitis A vaccine in Chad. Bull World Health Organ. 2014;92(2):86–92.
   PubMed Web of Science ®Google Scholar
• World Health Organization. Controlled temperature chain: strategic roadmap for priority vaccines 2017-2020. WHO/IVB/17.20, (2017).
   Google Scholar
• World Health Organization. Temperature sensitivity of vaccines. WHO/IVB/06.10, (2006).
   Google Scholar
• World Health Organization. PQS performance specification. WHO/PQS/E006/IN05.4, (2020).
   Google Scholar
• Dolgin E. COVID-19 vaccines poised for launch, but impact on pandemic unclear. Nat Biotechnol. 2020 Nov 25. doi: 10.1038/d41587-020-00022-y. Epub ahead of print. PMID: 33239758.
   Google Scholar
• Kaiser J. Temperature concerns could slow the rollout of new coronavirus vaccines. Science, 2020 [Cited 2020 Nov 30]. https://www.sciencemag.org/news/2020/11/temperature-concerns-could-slow-rollout-new-coronavirus-vaccines
   Google Scholar
• Lowe D. Cold chain (and colder chain) distribution. In the pipeline, Science Translational Medicine, 2020 [Cited 2020 Nov 30]. https://blogs.sciencemag.org/pipeline/archives/2020/08/31/cold-chain-and-colder-chain-distribution
   Google Scholar
• Pfizer Inc., Pfizer and BioNTech submit COVID-19 vaccine stability data at standard freezer temperature to the U.S. FDA, 2021 [Cited 2021 Feb 21]. https://www.pfizer.com/news/press-release/press-release-detail/pfizer-and-biontech-submit-covid-19-vaccine-stability-data
   Google Scholar
• Marcandalli J, Fiala B, Ols S, et al. Induction of potent neutralizing antibody responses by a designed protein nanoparticle vaccine for respiratory syncytial virus. Cell. 2019;176(6):1420–1431.e1417.
   PubMed Web of Science ®Google Scholar
• Atmar RL, Bernstein DI, Harro CD, et al. Norovirus vaccine against experimental human Norwalk Virus illness. N Engl J Med. 2011;365(23):2178–2187.
   PubMed Web of Science ®Google Scholar
• Foged C. Thermostable subunit vaccines for pulmonary delivery: how close are we? Curr Pharm Des. 2016;22(17):2561–2576.
   PubMed Web of Science ®Google Scholar
• Kanojia G, Have R, Soema PC, et al. Developments in the formulation and delivery of spray dried vaccines. Hum Vaccines Immunother. 2017;13(10):2364–2378.
   PubMed Web of Science ®Google Scholar
• Gomez M, Archer M, Barona D, et al. Microparticle encapsulation of a tuberculosis subunit vaccine candidate containing a nanoemulsion adjuvant via spray drying. Eur J Pharm Biopharm. 2021; 163: 23–37.
   PubMed Web of Science ®Google Scholar
• Chan MY, Dutill TS, Kramer RM. Lyophilization of adjuvanted vaccines: methods for formulation of a thermostable freeze-dried product. Methods Mol Biol. 2017;1494:215–226.
   Google Scholar
• PATH, Summary of stability data for licensed vaccines, 2012 [Cited 2020 Nov 30]. https://path.azureedge.net/media/documents/TS_vaccine_stability_table.pdf
   Google Scholar
• Walters RH, Bhatnagar B, Tchessalov S, et al. Next generation drying technologies for pharmaceutical applications. J Pharm Sci. 2014;103(9):2673–2695.
   PubMed Web of Science ®Google Scholar
• Alzhrani RF, Xu H, Moon C, et al. Thin-film freeze-drying is a viable method to convert vaccines containing aluminum salts from liquid to dry powder. In: Pfeifer BA, Hill A, editors. Vaccine delivery technology: methods and protocols. New York, NY: Springer US; 2021. p. 489–498.
   Google Scholar
• Gomez M, McCollum J, Wang H, et al. Development of a formulation platform for a spray-dried, inhalable tuberculosis vaccine candidate. Int J Pharm. 2021;593:120121.
   PubMed Web of Science ®Google Scholar
• Ziaee A, Albadarin AB, Padrela L, et al. Spray drying of pharmaceuticals and biopharmaceuticals: critical parameters and experimental process optimization approaches. Eur J Pharm Sci. 2019;127:300–318.
   PubMed Web of Science ®Google Scholar
• Siew A. Exploring the use of aseptic spray drying in the manufacture of biopharmaceutical injectables. Pharm Technol. 2016;40(7):24–27.
   Google Scholar
• Emami F, Vatanara A, Park EJ, et al. Drying technologies for the stability and bioavailability of biopharmaceuticals. Pharmaceutics. 2018;10(3):131.
   PubMed Web of Science ®Google Scholar
• Chouvenc P, Francon A, Process for stabilizing an adjuvant containing vaccine composition, PCT/EP2009/052460, September 11, 2009.
   Google Scholar
• Clénet D, Imbert F, Probeck P, et al. Advanced kinetic analysis as a tool for formulation development and prediction of vaccine stability. J Pharm Sci. 2014;103(10):3055–3064.
   PubMed Web of Science ®Google Scholar
• World Health Organization. Guidelines on stability evaluation of vaccines. WHO/BS/06.2049 (2006).
   Google Scholar
• Clapp T, Siebert P, Chen D, et al. Vaccines with aluminum-containing adjuvants: optimizing vaccine efficacy and thermal stability. J Pharm Sci. 2011;100(2):388–401.
   PubMed Web of Science ®Google Scholar
• Fortpied J, Wauters F, Rochart C, et al. Stability of an aluminum salt-adjuvanted protein D-conjugated pneumococcal vaccine after exposure to subzero temperatures. Hum Vaccin Immunother. 2018;14(5):1243–1250.
   PubMed Web of Science ®Google Scholar
• Li X, Thakkar SG, Ruwona TB, et al. A method of lyophilizing vaccines containing aluminum salts into a dry powder without causing particle aggregation or decreasing the immunogenicity following reconstitution. J Control Release. 2015;204:38–50.
   PubMed Web of Science ®Google Scholar
• Braun LJ, Tyagi A, Perkins S, et al. Development of a freeze-stable formulation for vaccines containing aluminum salt adjuvants. Vaccine. 2009;27(1):72–79.
   PubMed Web of Science ®Google Scholar
• Maa YF, Shu C, Ameri M, et al. Optimization of an alum-adsorbed vaccine powder formulation for epidermal powder immunization. Pharm Res. 2003;20:969–977.
   PubMed Web of Science ®Google Scholar
• Jezek J, Chen D, Watson L, et al. A heat-stable hepatitis B vaccine formulation. Hum Vaccin. 2009;5(8):529–535.
   PubMed Web of Science ®Google Scholar
• Braun LJ, Jezek J, Peterson S, et al., Characterization of a thermostable hepatitis B vaccine formulation. Vaccine. 2009;27(34): 4609–4614.
   PubMed Web of Science ®Google Scholar
• Xue H, Yang B, Kristensen DD, et al. A freeze-stable formulation for DTwP and DTaP vaccines. Hum Vaccin Immunother. 2014;10(12):3607–3610.
   PubMed Web of Science ®Google Scholar
• Orr MT, Khandhar AP, Seydoux E, et al. Reprogramming the adjuvant properties of aluminum oxyhydroxide with nanoparticle technology. NPJ Vaccines. 2019;4(1–1). 10.1038/s41541-018-0094-0
   Web of Science ®Google Scholar
• Wang T, Zhen Y, Ma X, et al. Aluminum nanoparticles as an effective vaccine adjuvant-delivery system. ACS Appl Mater Interfaces. 2015;7(12):6391–6396.
   PubMed Web of Science ®Google Scholar
• Li X, Aldayel AM, Cui Z. Aluminum hydroxide nanoparticles show a stronger vaccine adjuvant activity than traditional aluminum hydroxide microparticles. J Control Release. 2014;173(148–157):148–157.
   PubMed Web of Science ®Google Scholar
• Yin X, Wang X, Zhang Z, et al. Demonstration of real-time and accelerated stability of hepatitis E vaccine with a combination of different physicochemical and immunochemical methods. J Pharm Biomed Anal. 2020;177:112880.
   Web of Science ®Google Scholar
• Shen Z, Rao Y, Tao S, et al. Unimpaired immunogenicity of yeast-expressed hepatitis B surface antigen stored at elevated temperatures. Acta Biochim Biophys Sin (Shanghai). 2016;48(12):1094–1100.
   PubMed Web of Science ®Google Scholar
• Lakatos K, McAdams D, White JA, et al. Formulation and preclinical studies with a trivalent rotavirus P2-VP8 subunit vaccine. Hum Vaccin Immunother. 2020;16(8):1957–1968.
   PubMed Web of Science ®Google Scholar
• Groome MJ, Fairlie L, Morrison J, et al. Safety and immunogenicity of a parenteral trivalent P2-VP8 subunit rotavirus vaccine: a multisite, randomised, double-blind, placebo-controlled trial. Lancet Infect Dis. 2020;20(7):851–863.
   PubMed Web of Science ®Google Scholar
• Roy CJ, Brey RN, Mantis NJ, et al. Thermostable ricin vaccine protects rhesus macaques against aerosolized ricin: epitope-specific neutralizing antibodies correlate with protection. Proc Natl Acad Sci U S A. 2015;112(12):3782–3787.
   PubMed Web of Science ®Google Scholar
• Hassett KJ, Cousins MC, Rabia LA, et al., Stabilization of a recombinant ricin toxin A subunit vaccine through lyophilization. Eur J Pharm Biopharm. 2013;85(2): 279–286.
   PubMed Web of Science ®Google Scholar
• Westfall J, Yates JL, Van Slyke G, et al., Thermal stability and epitope integrity of a lyophilized ricin toxin subunit vaccine. Vaccine. 2018;36(40): 5967–5976.
   PubMed Web of Science ®Google Scholar
• Hassett KJ, Meinerz NM, Semmelmann F, et al. Development of a highly thermostable, adjuvanted human papillomavirus vaccine. Eur J Pharm Biopharm. 2015;94:220–228.
   PubMed Web of Science ®Google Scholar
• Hassett KJ, Vance DJ, Jain NK, et al. Glassy-State Stabilization of a dominant negative inhibitor anthrax vaccine containing aluminum hydroxide and glycopyranoside lipid a adjuvants. J Pharm Sci. 2015;104(2):627–639.
   PubMed Web of Science ®Google Scholar
• Chisholm CF, Kang TJ, Dong M, et al. Thermostable Ebola virus vaccine formulations lyophilized in the presence of aluminum hydroxide. Eur J Pharm Biopharm. 2019;136:213–220.
   PubMed Web of Science ®Google Scholar
• Autumn Smiley M, Sanford DC, Triplett CA, et al. Comparative immunogenicity and efficacy of thermostable (lyophilized) and liquid formulation of anthrax vaccine candidate AV7909. Vaccine. 2019;37(43):6356–6361.
   PubMed Web of Science ®Google Scholar
• clinicaltrials.gov. Anthrax AV7909 liquid vs lyophilized. NCT04660201, (2021).
   Google Scholar
• Thakkar SG, Ruwona TB, Williams RO 3rd, et al. The immunogenicity of thin-film freeze-dried, aluminum salt-adjuvanted vaccine when exposed to different temperatures. Hum Vaccin Immunother. 2017;13(4):936–946.
   PubMed Web of Science ®Google Scholar
• Chen D, Kapre S, Goel A, et al., Thermostable formulations of a hepatitis B vaccine and a meningitis A polysaccharide conjugate vaccine produced by a spray drying method. Vaccine. 2010;28(31): 5093–5099.
   PubMed Web of Science ®Google Scholar
• Sievers RE, Quinn BP, Cape SP, et al. Near-critical fluid micronization of stabilized vaccines, antibiotics and anti-virals. J Supercrit Fluids. 2007;42(3):385–391.
   Web of Science ®Google Scholar
• Corbett HJ, Fernando GJ, Chen X, et al. Skin vaccination against cervical cancer associated human papillomavirus with a novel micro-projection array in a mouse model. PLoS One. 2010;5(10):e13460.
   PubMed Web of Science ®Google Scholar
• Garcea RL, Meinerz NM, Dong M, et al. Single-administration, thermostable human papillomavirus vaccines prepared with atomic layer deposition technology. Npj Vaccines. 2020;5(1):45.
   PubMed Web of Science ®Google Scholar
• Wang G, Cao R-Y, Chen R, et al. Rational design of thermostable vaccines by engineered peptide-induced virus self-biomineralization under physiological conditions. Proc Nat Acad Sci. 2013;110(19):7619–7624.
   PubMed Web of Science ®Google Scholar
• Du P, Liu R, Sun S, et al. Biomineralization improves the thermostability of foot-and-mouth disease virus-like particles and the protective immune response induced. Nanoscale. 2019;11(47):22748–22761.
   PubMed Web of Science ®Google Scholar
• Makidon PE, Bielinska AU, Nigavekar SS, et al. Pre-clinical evaluation of a novel nanoemulsion-based hepatitis B mucosal vaccine. PLoS One. 2008;3(8):e2954.
   PubMed Web of Science ®Google Scholar
• Stanberry LR, Simon JK, Johnson C, et al. Safety and immunogenicity of a novel nanoemulsion mucosal adjuvant W805EC combined with approved seasonal influenza antigens. Vaccine. 2012;30(2):307–316.
   PubMed Web of Science ®Google Scholar
• clinicaltrials.gov. A safety and immunogenicity of intranasal nanoemulsion adjuvanted recombinant anthrax vaccine in healthy adults (IN NE-rPA). NCT04148118, (2020).
   Google Scholar
• clinicaltrials.gov. Safety and immunogenicity study of inactivated nasal influenza vaccine NB-1008 administered by sprayer. NCT01354379, (2020).
   Google Scholar
• Iyer V, Cayatte C, Marshall JD, et al. Feasibility of freeze-drying oil-in-water emulsion adjuvants and subunit proteins to enable single-vial vaccine drug products. J Pharm Sci. 2017;106(6):1490–1498.
   PubMed Web of Science ®Google Scholar
• Ivins B, Fellows P, Pitt L, et al. Experimental anthrax vaccines: efficacy of adjuvants combined with protective antigen against an aerosol Bacillus anthracis spore challenge in guinea pigs. Vaccine. 1995;13(18):1779–1784.
   PubMed Web of Science ®Google Scholar
• Orr MT, Kramer RM, Barnes VL, et al., Elimination of the cold-chain dependence of a nanoemulsion adjuvanted vaccine against tuberculosis by lyophilization. J Control Release. 2014;177(0): 20–26.
   PubMed Web of Science ®Google Scholar
• Kramer RM, Archer MC, Orr MT, et al. Development of a thermostable nanoemulsion adjuvanted vaccine against tuberculosis using a design-of-experiments approach. Int J Nanomedicine. 2018;13:3689–3711.
   PubMed Web of Science ®Google Scholar
• Barnes VL, Fedor DM, Williams S, et al. Lyophilization of an adjuvanted mycobacterium tuberculosis vaccine in a single-chamber pharmaceutical cartridge. AAPS PharmSciTech. 2017;18(6):2077–2084.
   PubMed Web of Science ®Google Scholar
• clinicaltrials.gov. Phase 1 clinical trial of single-vial ID93 + GLA-SE in healthy adults. NCT03722472, (2020).
   Google Scholar
• Sprott GD, Dicaire CJ, Fleming LP, et al. Stability of liposomes prepared from archaeobacterical lipids and phosphatidylcholine mixtures. Cells Mater. 1996;6(1):16.
   Google Scholar
• Choquet CG, Patel GB, Beveridge TJ, et al. Stability of pressure-extruded liposomes made from archaeobacterial ether lipids. Appl Microbiol Biotechnol. 1994;42(2–3):375–384.
   PubMed Web of Science ®Google Scholar
• Krishnan L, Sprott GD. Archaeosome adjuvants: immunological capabilities and mechanism(s) of action. Vaccine. 2008;26(17):2043–2055.
   PubMed Web of Science ®Google Scholar
• Jia Y, Chandan V, Akache B, et al. Assessment of stability of sulphated lactosyl archaeol archaeosomes for use as a vaccine adjuvant. J Liposome Res. 2020;1–9. 10.1080/08982104.2020.1786115
   PubMed Web of Science ®Google Scholar
• Krishnan L, Sprott GD. Archaeosomes as self-adjuvanting delivery systems for cancer vaccines. J Drug Target. 2003;11(11):515–524.
   PubMed Web of Science ®Google Scholar
• Krishnan L, Sad S, Patel GB, et al. Archaeosomes induce enhanced cytotoxic T lymphocyte responses to entrapped soluble protein in the absence of interleukin 12 and protect against tumor challenge. Cancer Res. 2003;63(10):2526–2534.
   PubMed Web of Science ®Google Scholar
• Higa LH, Corral RS, Morilla MJ, et al. Archaeosomes display immunoadjuvant potential for a vaccine against Chagas disease. Hum Vaccin Immunother. 2013;9(2):409–412.
   PubMed Web of Science ®Google Scholar
• Higa LH, Schilrreff P, Perez AP, et al. Ultradeformable archaeosomes as new topical adjuvants. Nanomedicine. 2012;8(8):1319–1328.
   PubMed Web of Science ®Google Scholar
• Crowe JH, Crowe LM, Carpenter JF, et al. Stabilization of dry phospholipid bilayers and proteins by sugars. Biochem J. 1987;242(1):1–10.
   PubMed Web of Science ®Google Scholar
• Ingvarsson PT, Yang M, Nielsen HM, et al. Stabilization of liposomes during drying. Expert Opin Drug Deliv. 2011;8(3):375–388.
   PubMed Web of Science ®Google Scholar
• Sun WQ, Leopold AC, Crowe LM, et al. Stability of dry liposomes in sugar glasses. Biophys. J. 1996;70(4):1769–1776.
   Web of Science ®Google Scholar
• Christensen D, Foged C, Rosenkrands I, et al. Trehalose preserves DDA/TDB liposomes and their adjuvant effect during freeze-drying. Biochim Biophys Acta Biomembr. 2007;1768(9):2120–2129.
   Web of Science ®Google Scholar
• Yusuf H, Ali AA, Orr N, et al. Novel freeze-dried DDA and TPGS liposomes are suitable for nasal delivery of vaccine. Int J Pharm. 2017;533(1):179–186.
   PubMed Web of Science ®Google Scholar
• Mabrouk MT, Huang WC, Deng B, et al. Lyophilized, antigen-bound liposomes with reduced MPLA and enhanced thermostability. Int J Pharm. 2020;589:119843.
   PubMed Web of Science ®Google Scholar
• Wang N, Wang T. Preparation of multifunctional liposomes as a stable vaccine delivery-adjuvant system by procedure of emulsification-lyophilization. Methods Mol Biol. 2016;1404:635–649.
   PubMedGoogle Scholar
• Wang N, Wang T, Zhang M, et al. Using procedure of emulsification-lyophilization to form lipid A-incorporating cochleates as an effective oral mucosal vaccine adjuvant-delivery system (VADS). Int J Pharm. 2014;468(1–2):39–49.
   PubMed Web of Science ®Google Scholar
• Wang N, Wang T, Zhang M, et al. Mannose derivative and lipid A dually decorated cationic liposomes as an effective cold chain free oral mucosal vaccine adjuvant-delivery system. Eur J Pharm Biopharm. 2014;88(1):194–206.
   PubMed Web of Science ®Google Scholar
• Ebensen T, Paukner S, Link C, et al. Bacterial ghosts are an efficient delivery system for DNA vaccines. J Immunol. 2004;172(11):6858–6865.
   PubMed Web of Science ®Google Scholar
• Mayr UB, Walcher P, Azimpour C, et al. Bacterial ghosts as antigen delivery vehicles. Adv Drug Deliv Rev. 2005;57(9):1381–1391.
   PubMed Web of Science ®Google Scholar
• Eko FO, Schukovskaya T, Lotzmanova EY, et al. Evaluation of the protective efficacy of Vibrio cholerae ghost (VCG) candidate vaccines in rabbits. Vaccine. 2003;21(25–26):3663–3674.
   Google Scholar
• Eko FO, Lubitz W, McMillan L, et al. Recombinant Vibrio cholerae ghosts as a delivery vehicle for vaccinating against Chlamydia trachomatis. Vaccine. 2003;21(15):1694–1703.
   PubMed Web of Science ®Google Scholar
• Lacaille-Dubois M-A. Updated insights into the mechanism of action and clinical profile of the immunoadjuvant QS-21: a review. Phytomedicine. 2019;60:152905.
   PubMed Web of Science ®Google Scholar
• Fortpied J, Collignon S, Moniotte N, et al. The thermostability of the RTS,S/AS01 malaria vaccine can be increased by co-lyophilizing RTS,S and AS01. Malar J. 2020;19(1):202.
   PubMed Web of Science ®Google Scholar
• Ingvarsson PT, Schmidt ST, Christensen D, et al. Designing CAF-adjuvanted dry powder vaccines: spray drying preserves the adjuvant activity of CAF01. J Control Release. 2013;167(3):256–264.
   PubMed Web of Science ®Google Scholar
• Thakur A, Ingvarsson PT, Schmidt ST, et al. Immunological and physical evaluation of the multistage tuberculosis subunit vaccine candidate H56/CAF01 formulated as a spray-dried powder. Vaccine. 2018;36(23):3331–3339.
   PubMed Web of Science ®Google Scholar
• Mody K, Mahony D, Mahony TJ, et al. Freeze-drying of protein-loaded nanoparticles for vaccine delivery. Drug Deliv Lett. 2012;2(2):83–91
   Google Scholar
• Phan HT, Haes AJ. What does nanoparticle stability mean? J Phys Chem C. 2019;123(27):16495–16507.
   PubMed Web of Science ®Google Scholar
• Canali E, Bolchi A, Spagnoli G, et al. A high-performance thioredoxin-based scaffold for peptide immunogen construction: proof-of-concept testing with a human papillomavirus epitope. Sci Rep. 2014;4:4729.
   PubMed Web of Science ®Google Scholar
• Spagnoli G, Pouyanfard S, Cavazzini D, et al. Broadly neutralizing antiviral responses induced by a single-molecule HPV vaccine based on thermostable thioredoxin-L2 multiepitope nanoparticles. Sci Rep. 2017;7:18000.
   PubMed Web of Science ®Google Scholar
• Marcandalli J, Fiala B, Ols S, et al. Induction of potent neutralizing antibody responses by a designed protein nanoparticle vaccine for respiratory syncytial virus. Cell. 2019;176(6):1420–1431.e1417.
   PubMed Web of Science ®Google Scholar
• Cruz-Reséndiz A, Zepeda-Cervantes J, Sampieri A, et al. A self-aggregating peptide: implications for the development of thermostable vaccine candidates. BMC Biotechnol. 2020;20(1). 10.1186/s12896-019-0592-9
   PubMed Web of Science ®Google Scholar
• Crecente-Campo J, Lorenzo-Abalde S, Mora A, et al. Bilayer polymeric nanocapsules: a formulation approach for a thermostable and adjuvanted E. coliantigen vaccine. J Control Release. 2018;286:20–32.
   PubMed Web of Science ®Google Scholar
• González-Aramundiz JV, Peleteiro M, Á G-F, et al. Protamine nanocapsules for the development of thermostable adjuvanted nanovaccines. Mol Pharm. 2018;15(12):5653–5664.
   PubMed Web of Science ®Google Scholar
• Sloat BR, Sandoval MA, Cui Z. Towards preserving the immunogenicity of protein antigens carried by nanoparticles while avoiding the cold chain. Int J Pharm. 2010;393(1–2):197–202.
   PubMed Web of Science ®Google Scholar
• Tang F, Li L, Chen D. Mesoporous silica nanoparticles: synthesis, biocompatibility and drug delivery. Adv Mater. 2012;24(12):1504–1534.
   PubMed Web of Science ®Google Scholar
• Mody KT, Popat A, Mahony D, et al. Mesoporous silica nanoparticles as antigen carriers and adjuvants for vaccine delivery. Nanoscale. 2013;5(12):5167–5179.
   PubMed Web of Science ®Google Scholar
• Mody KT, Mahony D, Cavallaro AS, et al. Silica vesicle nanovaccine formulations stimulate long-term immune responses to the bovine viral diarrhoea virus E2 protein. PLoS One. 2015;10(12):e0143507.
   PubMed Web of Science ®Google Scholar
• D’Souza B, Shastri PN, Hammons G, et al. Immune-potentiation of pneumococcal capsular polysaccharide antigen using albumin microparticles. J. Pharmacovigil. 2018;6(3):261.
   Google Scholar
• Gala RP, D’Souza M, Zughaier SM. Evaluation of various adjuvant nanoparticulate formulations for meningococcal capsular polysaccharide-based vaccine. Vaccine. 2016;34(28):3260–3267.
   PubMed Web of Science ®Google Scholar
• Ubale RV, D’souza MJ, Infield DT, et al. Formulation of meningococcal capsular polysaccharide vaccine-loaded microparticles with robust innate immune recognition. J Microencapsul. 2013;30(1):28–41.
   PubMed Web of Science ®Google Scholar
• Tumban E, Peabody J, Peabody DS, et al. A universal virus-like particle-based vaccine for human papillomavirus: longevity of protection and role of endogenous and exogenous adjuvants. Vaccine. 2013;31(41):4647–4654.
   PubMed Web of Science ®Google Scholar
• Saboo S, Tumban E, Peabody J, et al., Optimized formulation of a thermostable spray-dried virus-like particle vaccine against human papillomavirus. Mol Pharm. 2016;13(5): 1646–1655.
   PubMed Web of Science ®Google Scholar
• Belyakov IM, Ahlers JD. What role does the route of immunization play in the generation of protective immunity against mucosal pathogens? J Immunol. 2009;183(11):6883–6892.
   PubMed Web of Science ®Google Scholar
• Boddupalli BM, Mohammed ZNK, Nath RA, et al. Mucoadhesive drug delivery system: an overview. J Adv Pharm Technol Res. 2010;1(4):381–387.
   PubMedGoogle Scholar
• Serradell MC, Rupil LL, Martino RA, et al. Efficient oral vaccination by bioengineering virus-like particles with protozoan surface proteins. Nat Commun. 2019;10(1):361.
   PubMed Web of Science ®Google Scholar
• Jelinek T, Kollaritsch H. Vaccination with Dukoral against travelers’ diarrhea (ETEC) and cholera. Expert Rev Vaccines. 2008;7(5):561–567.
   PubMed Web of Science ®Google Scholar
• Holmgren J, Lycke N, Czerkinsky C. Cholera toxin and cholera B subunit as oral-mucosal adjuvant and antigen vector systems. Vaccine. 1993;11(12):1179–1184.
   PubMed Web of Science ®Google Scholar
• Stratmann T. Cholera toxin subunit B as adjuvant––an accelerator in protective immunity and a break in autoimmunity. Vaccine. 2015;3(3):579–596.
   Google Scholar
• European Medicines Agency, Dukoral product information, [Cited 2021 Jan 24] https://www.ema.europa.eu/en/documents/product-information/dukoral-epar-product-information_en.pdf
   Google Scholar
• Odevall L, Hong D, Digilio L, et al. The Euvichol story – Development and licensure of a safe, effective and affordable oral cholera vaccine through global public private partnerships. Vaccine. 2018;36(45):6606–6614.
   PubMed Web of Science ®Google Scholar
• Katinger A, Lubitz W, Szostak MP, et al. Pigs aerogenously immunized with genetically inactivated (ghosts) or irradiated Actinobacillus pleuropneumoniae are protected against a homologous aerosol challenge despite differing in pulmonary cellular and antibody responses. J Biotechnol. 1999;73(2–3):251–260.
   PubMed Web of Science ®Google Scholar
• Summerton NA, Welch RW, Bondoc L, 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):1404–1411.
   PubMed Web of Science ®Google Scholar
• Akker FVD, Feil IK, Roach C, et al. Crystal structure of heat‐labile enterotoxin from Escherichia coli with increased thermostability introduced by an engineered disulfide bond in the A subunit. Protein Sci. 2008;6(12):2644–2649.
   Google Scholar
• Amacker M, Smardon C, Mason L, et al. New GMP manufacturing processes to obtain thermostable HIV-1 gp41 virosomes under solid forms for various mucosal vaccination routes. NPJ Vaccines. 2020; 5(41): 10.1038/s41541-020-0190-9
   Web of Science ®Google Scholar
• Shakya AK, Chowdhury MYE, Tao W, et al. Mucosal vaccine delivery: current state and a pediatric perspective. J Control Release. 2016;240:394–413.
   PubMed Web of Science ®Google Scholar
• Saengkrit N, Saesoo S, Woramongkolchai N, et al. Dry formulations enhanced mucoadhesive properties and reduced cold chain handing of influenza vaccines. AAPSPharmSciTech. 2018;19(8):3763–3769.
   Google Scholar
• El-Kamary SS, Pasetti MF, Mendelman PM, et al. Adjuvanted intranasal Norwalk virus-like particle vaccine elicits antibodies and antibody-secreting cells that express homing receptors for mucosal and peripheral lymphoid tissues. J Infect Dis. 2010;202(11):1649–1658.
   PubMed Web of Science ®Google Scholar
• Tyne A S, Jgy C, Shanahan E R, et al. TLR2-targeted secreted proteins from Mycobacterium tuberculosis are protective as powdered pulmonary vaccines. Vaccine. 2013;31(40):4322–4329.
   PubMed Web of Science ®Google Scholar
• Wang SH, Kirwan SM, Abraham SN, et al. Stable dry powder formulation for nasal delivery of anthrax vaccine. J Pharm Sci. 2012;101(1):31–47.
   PubMed Web of Science ®Google Scholar
• Longet S, Aversa V, O’Donnell D, et al., Thermostability of the coating, antigen and immunostimulator in an adjuvanted oral capsule vaccine formulation. Int J Pharm. 2017;534(1–2): 60–70.
   PubMed Web of Science ®Google Scholar
• Kim YC, Jarrahian C, Zehrung D, et al. Delivery systems for intradermal vaccination. Curr Top Microbiol Immunol. 2012;351:77–112.
   PubMed Web of Science ®Google Scholar
• Larrañeta E, Lutton REM, Woolfson AD, et al. Microneedle arrays as transdermal and intradermal drug delivery systems: materials science, manufacture and commercial development. Mater. Sci. Eng. R Rep. 2016;104:1–32.
   Web of Science ®Google Scholar
• Ellison TJ, Talbott GC, Henderson DR. VaxiPatch™, a novel vaccination system comprised of subunit antigens, adjuvants and microneedle skin delivery: an application to influenza B/Colorado/06/2017. Vaccine. 2020;38(43):6839–6848.
   PubMed Web of Science ®Google Scholar
• Stinson JA, Raja WK, Lee S, et al. Silk fibroin microneedles for transdermal vaccine delivery. ACS Biomater. Sci. Eng. 2017;3(3):360–369.
   PubMed Web of Science ®Google Scholar
• Poirier D, Renaud F, Dewar V, et al. Hepatitis B surface antigen incorporated in dissolvable microneedle array patch is antigenic and thermostable. Biomaterials. 2017;145(:256–265.
   PubMed Web of Science ®Google Scholar
• Weissmueller NT, Schiffter HA, Pollard AJ. Intradermal powder immunization with protein-containing vaccines. Expert Rev Vaccines. 2013;12(6):687–702.
   PubMed Web of Science ®Google Scholar
• Osorio JE, Zuleger CL, Burger M, et al. Immune responses to hepatitis B surface antigen following epidermal powder immunization. Immunol Cell Biol. 2003;81(1):52–58.
   PubMed Web of Science ®Google Scholar
• Chen D, Endres CAERL, Periwal SB, et al. Adjuvantation of epidermal powder immunization. Vaccine. 2001;19(20–22):2908–2917.
   PubMed Web of Science ®Google Scholar
• Chen D, Periwal SB, Larrivee K, et al. Serum and mucosal immune responses to an inactivated influenza virus vaccine induced by epidermal powder immunization. J Virol. 2001;75(17):7956–7965.
   PubMed Web of Science ®Google Scholar
• Chen D, Endres RL, Erickson CA, et al. Epidermal powder immunization using non-toxic bacterial enterotoxin adjuvants with influenza vaccine augments protective immunity. Vaccine. 2002;20(21–22):2671–2679.
   PubMed Web of Science ®Google Scholar
• Adali MB, Barresi AA, Boccardo G, et al. Spray freeze-drying as a solution to continuous manufacturing of pharmaceutical products in bulk. Processes. 2020;8(6):709.
   Web of Science ®Google Scholar
• Maa Y-F, Zhao L, Payne LG, et al. Stabilization of alum-adjuvanted vaccine dry powder formulations: mechanism and application. J Pharm Sci. 2003;92(2):319–332.
   PubMed Web of Science ®Google Scholar
• Hickey DK, Aldwell FE, Tan ZY, et al. Transcutaneous immunization with novel lipid-based adjuvants induces protection against gastric Helicobacter pylori infection. Vaccine. 2009;27(50):6983–6990.
   PubMed Web of Science ®Google Scholar
• Hung IF, Yap DY, Yip TP, et al. A double-blind randomized phase 2 controlled trial of intradermal hepatitis B vaccination with a topical Toll-like receptor 7 agonist imiquimod, in patients on dialysis. Clin Infect Dis. 2020;ciaa804
   Google Scholar
• Hung IF, Zhang AJ, To KK, et al. Immunogenicity of intradermal trivalent influenza vaccine with topical imiquimod, a double blind randomized controlled trial. Clinl Infect Dis. 2014;59(9):1246–1255.
   PubMed Web of Science ®Google Scholar
• Hung IF-N, Zhang AJ, To KK-W, et al. Topical imiquimod before intradermal trivalent influenza vaccine for protection against heterologous non-vaccine and antigenically drifted viruses: a single-centre, double-blind, randomised, controlled phase 2b/3 trial. Lancet Infect Dis. 2016;16(2):209–218.
   PubMed Web of Science ®Google Scholar
• Tebas P, Kraynyak KA, Patel A, et al. Intradermal Syncon® Ebola GP DNA vaccine is temperature stable and safely demonstrates cellular and humoral immunogenicity advantages in healthy volunteers. J Infect Dis. 2019;220(3):400–410.
   PubMed Web of Science ®Google Scholar
• Doekhie A, Dattani R, Chen YC, et al. Ensilicated tetanus antigen retains immunogenicity: in vivo study and time-resolved SAXS characterization. Sci Rep. 2020;10:9243.
   PubMed Web of Science ®Google Scholar
• Aaw AA, Doekhie A, Sartbaeva A, et al. Ensilication improves the thermal stability of the tuberculosis antigen Ag85b and an Sbi-Ag85b vaccine conjugate. Sci Rep. 2019;9(1):11409.
   PubMed Web of Science ®Google Scholar
• Stinson JA, Palmer CR, Miller DP, et al. Thin silk fibroin films as a dried format for temperature stabilization of inactivated polio vaccine. Vaccine. 2020;38:1652–1660.
   PubMed Web of Science ®Google Scholar
• Kashiwagi S. Laser adjuvant for vaccination. FASEB J. 2020;34(3):3485–3500.
   PubMed Web of Science ®Google Scholar
• Markarian J. Accelerating technology adoption to track the cold chain. BioPharm Int. 2021;34(1):38–40.
   Web of Science ®Google Scholar
• Crommelin DJA, Anchordoquy TJ, Volkin DB, et al. Addressing the cold reality of mRNA vaccine stability. J Pharm Sci. 2021;110(3):997–1001.
   Web of Science ®Google Scholar
• Zhao P, Hou X, Yan J, et al. Long-term storage of lipid-like nanoparticles for mRNA delivery. Bioact Mater. 2020;5(2):358–363.
   PubMed Web of Science ®Google Scholar
• Ball RL, Bajaj P, Whitehead KA. Achieving long-term stability of lipid nanoparticles: examining the effect of pH, temperature, and lyophilization. Int J Nanomedicine. 2017;12:305–315.
   PubMed Web of Science ®Google Scholar
• Gerhardt A, Voigt E, Archer M, Reed S, Larson E, Van Hoeven N, Kramer R, Fox C, Casper C. A thermostable, flexible RNA vaccine delivery platform for pandemic response. bioRxiv. 2021.02.01.429283
   Google Scholar