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Technology – Review

Current and next-generation formulation strategies for inactivated polio vaccines to lower costs, increase coverage, and facilitate polio eradication

, , , &
Article: 2154100 | Received 08 Sep 2022, Accepted 29 Nov 2022, Published online: 28 Dec 2022

References

  • CDC. History of polio. Global immunization. 2021 [accessed 2022 Mar 4]. https://www.cdc.gov/polio/what-is-polio/index.htm#:~:text=Polio%2C%20or%20poliomyelitis%2C%20is%20a,move%20parts%20of%20the%20body.
  • Racaniello VR. One hundred years of poliovirus pathogenesis. Virology. 2006;344(1):9–24. doi:10.1016/j.virol.2005.09.015.
  • Minor P. The polio endgame. Hum Vaccin Immunother. 2014;10(7):2106–08. doi:10.4161/21645515.2014.981115.
  • Hart CW. Franklin Delano Roosevelt: a famous patient. J Relig Health. 2014;53(4):1102–11. doi:10.1007/s10943-014-9886-3.
  • Minor PD. Poliovirus biology. Structure. 1996;4(7):775–78. doi:10.1016/s0969-2126(96)00084-6.
  • Le Bouvier GL. Poliovirus D and C antigens: their differentiation and measurement by precipitation in agar. Br J Exp Pathol. 1959;40:452–63.
  • Le Bouvier GL. The D to C change in poliovirus particles. Br J Exp Pathol. 1959;40:605–20.
  • Ferguson M, Wood DJ, Minor PD. Antigenic structure of poliovirus in inactivated vaccines. J Gen Virol. 1993;73:685–90. doi:10.1099/0022-1317-74-4-685.
  • CDC. Our progress against polio. 2021. [accessed 2022 Mar 8]. https://www.cdc.gov/polio/progress/index.htm.
  • Polio Golbal Eradication Initiative. [accessed 2022 Mar 11]. https://polioeradication.org/polio-today/history-of-polio/.
  • Dattani S, Spooner F, Ochmann S, Polio RM. Our world in data. 2022 [accessed 2022 Jul 25]. https://ourworldindata.org/polio.
  • Khullar D The preventable tragedy of polio in New York. The New Yorker. 2022 [accessed 2022 Sept 1]. https://www.newyorker.com/news/daily-comment/the-preventable-tragedy-of-polio-in-new-york.
  • Bandyopadhyay AS, Garon J, Seib K, Orenstein WA. Polio vaccination: past, present and future. Future Microbiol. 2015;10(5):791–808. doi:10.2217/fmb.15.19.
  • Modlin JF, Bandyopadhyay AS, Sutter R. Immunization against poliomyelitis and the challenges to worldwide poliomyelitis eradication. J Infect Dis. 2021;224(12 Suppl 2):S398–404. doi:10.1093/infdis/jiaa622.
  • WHO. Eupolio Inj. [accessed 2022 Mar 3]. https://extranet.who.int/pqweb/content/eupolio-inj.
  • Konopka-Anstadt JL, Campagnoli R, Vincent A, Shaw J, Wei L, Wynn NT, Smithee SE, Bujaki E, Te Yeh M, Laassri M, et al. Development of a new oral poliovirus vaccine for the eradication end game using codon deoptimization. NPJ Vaccines. 2020;5(1):26. doi:10.1038/s41541-020-0176-7.
  • Vidor E. Poliovirus Vaccine–Inactivated. In: Plotkin SA, Orenstein WA, Offit, PA, Edwards, KM, editors. Plotkin’s Vaccines. 7th Edition. United States of America: Elsevier 9780323393010; 2018.
  • Offit PA. The cutter incident, 50 years later. N Engl J Med. 2005;352(14):1411–12. doi:10.1056/NEJMp048180.
  • Fitzpatrick M. The cutter incident: how america’s first polio vaccine led to a growing vaccine crisis. J R Soc Med. 2006;99(3):156. doi:10.1177/014107680609900320.
  • Connor RI, Brickley EB, Wieland-Alter WF, Ackerman ME, Weiner JA, Modlin JF, Bandyopadhyay AS, Wright PF. Mucosal immunity to poliovirus. Mucosal Immunity. 2022;15:1–9. doi:10.1038/s41385-021-00428-0.
  • Hird TR, Grassly NC. Systematic review of mucosal immunity induced by oral and inactivated poliovirus vaccines against virus shedding following oral poliovirus challenge. PLoS Pathog. 2012;8(4):e1002599. doi:10.1371/journal.ppat.1002599.
  • Yuhong Xiao HD, Daniell H. Long-term evaluation of mucosal and systemic immunity and protection conferred by different polio booster vaccines. Vaccine. 2017;35:5418–25. doi:10.1016/2Fj.vaccine.2016.12.061.
  • Bandyopadhyay AS, Orenstein WA. Evolution of inactivated poliovirus vaccine use for the endgame and beyond. J Infect Dis. 2020;221(6):861–63. doi:10.1093/infdis/jiz300.
  • Marita Zimmermann BH, Lyons H. Projection of costs of polio eradication compared to permanent control. J Infect Dis. 2020;561–65. doi:10.1093/infdis/jiz488.
  • Bakker WA, Thomassen YE, van’t Oever AG, Westdijk J, van Oijen MG, Sundermann LC, van’t Veld P, Sleeman E, van Nimwegen FW, Hamidi A, et al. Inactivated polio vaccine development for technology transfer using attenuated Sabin poliovirus strains to shift from Salk-IPV to Sabin-IPV. Vaccine. 2011;29(41):7188–96. doi:10.1016/j.vaccine.2011.05.079.
  • Bandyopadhyay AS, Singh H, Fournier-Caruana J, Modlin JF, Wenger J, Partridge J, Sutter RW, Zaffran MJ. Facility-associated release of polioviruses into communities—risks for the posteradication era. Emerg Infect Dis. 2019;25(7):1363–69. doi:10.3201/2Feid2507.181703.
  • WHO. Containment verification of large-scale polio vaccine production and quality control facilities following the interruption of endemic poliomyelitis transmission. 2003 [accessed 2022 Mar 8]. https://cdn.who.int/media/docs/default-source/biologicals/vaccine-quality/polio-vaccine-containment-meeting-reportf0e0079f-4e5f-4fcb-b9df-2867937cec1d.pdf?sfvrsn=837d3772_1&download=true#:~:text=Currently%20Sabin%20strains%20used%20for,(BSL%2D1)%20conditions.
  • Wan Y, Hickey JM, Bird C, Witham K, Fahey P, Forster A, Joshi SB, Volkin DB. Development of stabilizing formulations of a trivalent inactivated poliovirus vaccine in a dried state for delivery in the nanopatch microprojection array. J Pharm Sci. 2018;107(6):1540–51. doi:10.1016/j.xphs.2018.01.027.
  • Shimizu H. Development and introduction of inactivated poliovirus vaccines derived from Sabin strains in Japan. Vaccine. 2016;34(16):1975–85. doi:10.1016/j.vaccine.2014.11.015.
  • Burke CJ, Hsu TA, Volkin DB. Formulation, stability, and delivery of live attenuated vaccines for human use. Crit Rev Ther Drug Carrier Syst. 1999;16(1):1–83. doi:10.1615/CritRevTherDrugCarrierSyst.v16.i1.10.
  • Verheyden B, Andries K, Rombaut B. Capsid and RNA stabilisation of the oral polio vaccine. Vaccine. 2001;19(15):1899–905. doi:10.1016/S0264-410X(00)00442-4.
  • Chen CH, Wu R, Roth LG, Guillot S, Crainic R. Elucidating mechanisms of thermostabilization of poliovirus by D2O and MgCl2. Arch Biochem Biophys. 1997;342(1):108–16. doi:10.1006/abbi.1997.0111.
  • Newman JF, Tirrell S, Ullman C, Piatti PG, Brown F. Stabilising oral polio vaccine at high ambient temperatures. Vaccine. 1995;13(15):1431–35. doi:10.1016/0264-410X(95)00070-H.
  • Wilton T, Dunn G, Eastwood D, Minor PD, Martin J. Effect of formaldehyde inactivation on poliovirus. J Virol. 2014;88(20):11955–64. doi:10.1128/JVI.01809-14.
  • Wilton T. Methods for the quality control of inactivated poliovirus vaccines. Methods Mol Biol. 2016;1387:279–97. doi:10.1007/978-1-4939-3292-4_15.
  • Kersten G, Hazendonk T, Beuvery C. Antigenic and immunogenic properties of inactivated polio vaccine made from Sabin strains. Vaccine. 1999;17(15–16):2059–66. doi:10.1016/s0264-410x(98)00409-5.
  • Arita M, Iwai-Itamochi M. High-throughput analysis of anti-poliovirus neutralization antibody titre in human serum by the pseudovirus neutralization test. Sci Rep. 2022;12(1):16074. doi:10.1038/s41598-022-20544-6.
  • Wood DJ, Health AB, Sawyer LA. A WHO collaborative study on assays of the antigenic content of inactivated poliovirus vaccines. Biologicals. 1995;23:83–94. doi:10.1016/1045-1056(95)90017-9.
  • Wood DJ, Heath AB. A WHO collaborative study of immunogenicity assays of inactivated poliovirus vaccines. Biologicals. 1995;23:301–11. doi:10.1006/biol.1995.0049.
  • Murakami K, Fujii Y, Someya Y. Effects of the thermal denaturation of Sabin-derived inactivated polio vaccines on the D-antigenicity and the immunogenicity in rats. Vaccine. 2020;38(17):3295–99. doi:10.1016/j.vaccine.2020.03.027.
  • White JA, Estrada M, Weldon WC, Chumakov K, Kouiavskaia D, Fournier-Caruana J, Stevens E, Gary HE Jr., Maes EF, Oberste MS, et al. Assessing the potency and immunogenicity of inactivated poliovirus vaccine after exposure to freezing temperatures. Biologicals. 2018;53:30–38. doi:10.1016/j.biologicals.2018.03.002.
  • Hasija M, Li L, Rahman N, Ausar SF. Forced degradation studies: an essential tool for the formulation development of vaccines. Vaccine Dev Ther. 2013;3:11–33. doi:10.2147/VDT.S41998.
  • Markova N, Cairns S, Jankevics-Jones H, Kaszuba M, Caputo F, Parot J. Biophysical characterization of viral and lipid-based vectors for vaccines and therapeutics with light scattering and calorimetric techniques. Vaccines. 2021;10:49. doi:10.3390/vaccines10010049.
  • Krell T, Manin C, Nicolaï MC, Pierre-Justin C, Bérard Y, Brass O, Gérentes L, Leung-Tack P, Chevalier M. Characterization of different strains of poliovirus and influenza virus by differential scanning calorimetry. Biotechnol Appl Biochem. 2005;41(Pt 3):241–46. doi:10.1042/ba20040113.
  • Qi W, Zeng Y, Orgel S, Francon A, Kim JH, Randolph TW, Carpenter JF, Middaugh CR. Preformulation study of highly purified inactivated polio vaccine, serotype 3. J Pharm Sci. 2014;103(1):140–51. doi:10.1002/jps.23801.
  • Torisu T, Shikama S, Nakamura K, Enomoto K, Maruno T, Mori A, Uchiyama S, Satou T. Physicochemical characterization of sabin inactivated poliovirus vaccine for process development. J Pharm Sci. 2021;110(5):2121–29. doi:10.1016/j.xphs.2020.12.012.
  • Huijuan Y, Xiaohu D, Ze L, Wei C, Jian Z, Lei M, Shaohui S, Weidong L, Guoyang L. Role of phenol red in the stabilization of the Sabin type 2 inactivated polio vaccine at various pH values. J Med Virol. 2019;91(1):22–30. doi:10.1002/jmv.25289.
  • Cai W, Ping L, Shen W, Liu J, Zhang M, Zhou J, Peng J, Wang M, Zhu Y, Ji G, et al. Potency of the Sabin inactivated poliovirus vaccine (sIPV) after exposure to freezing temperatures in cold chains. Hum Vaccines Immunother. 2020;16(8):1866–74. doi:10.1080/21645515.2019.1709352.
  • Westdijk J, Kogelman A, van der Put R, Eksteen Z, Suarez D, Kersten GFA, Metz B, Danial M. Immunochemical and biophysical characterization of inactivated Sabin poliovirus products: insights into rapid quality assessment tools. J Pharm Sci. 2022;111(4):1058–69. doi:10.1016/j.xphs.2022.01.031.
  • WHO. List of prequalified vaccines. [accessed 2022 Jul 25]. https://extranet.who.int/pqweb/vaccines/list-prequalified-vaccines.
  • PATH. Summary of stability data for licensed vaccines. [accessed 2022 Jul 25]. https://media.path.org/documents/TS_vaccine_stability_table.pdf?_gl=1*i2rxs2*_ga*MTIwMjY1MjY4MS4xNjU4Nzg1NzM4*_ga_YBSE7ZKDQM*MTY1ODc4NTczNy4xLjAuMTY1ODc4NTczOS4w.
  • US-FDA. Vaccines licensed for use in the United States. [accessed 2022 Jul 25]. https://www.fda.gov/vaccines-blood-biologics/vaccines/vaccines-licensed-use-united-states.
  • WHO. Picovax. 2021 [accessed 2022 Sept 5]. https://extranet.who.int/pqweb/content/picovax.
  • Jerajani K, Wan Y, Kumru OS, Pllagurla SP, Kumar P, Sharma N, Ogun O, Mapari S, Brendle S, Christensen ND, et al. Multi-dose formulation development for a quadrivalent human papillomavirus virus-like particle-based vaccine: part I- screening of preservative combinations. J Pharm Sci. 2022;111(11):2983–97. doi:10.1016/j.xphs.2022.07.019.
  • Moynihan M, Petersen I. The durability of inactivated poliovirus vaccine: studies on the stability of potency in vivo and in vitro. J Biol Stand. 1982;10(3):261–68. doi:10.1016/s0092-1157(82)80027-9.
  • Kristensen D Summary of stability data for licensed vaccines. PATH. [accessed 2012 Mar 11]. https://path.azureedge.net/media/documents/TS_vaccine_stability_table.pdf.
  • Hamidi A, Bakker WAM. Innovative IPV from attenuated Sabin poliovirus or newly designed alternative seed strains. Pharm Pat Anal. 2012;5:589–99. doi:10.4155/ppa.12.70.
  • Plotkin S, Robinson JM, Cunningham G, Iqbal R, Larsen S. The complexity and cost of vaccine manufacturing – an overview. Vaccine. 2017;35(33):4064–71. doi:10.1016/j.vaccine.2017.06.003.
  • Lee BY, Norman BA, Assi TM, Chen SI, Bailey RR, Rajgopal J, Brown ST, Wiringa AE, Burke DS. Single versus multi-dose vaccine vials: an economic computational model. Vaccine. 2010;28(32):5292–300. doi:10.1016/j.vaccine.2010.05.048.
  • Thomassen YE, van ‘T Oever AG, van Oijen MG, Wijffels RH, van der Pol LA, Bakker WA. Next generation inactivated polio vaccine manufacturing to support post polio-eradication biosafety goals. PLoS One. 2013;8(12):e83374. doi:10.1371/journal.pone.0083374.
  • WHO. WHO policy statement: Multi-Dose Vial Policy (MDVP). 2014 [accessed 2022 Sept 1]. https://apps.who.int/iris/bitstream/handle/10665/135972/WHO_IVB_14.07_eng.pdf.
  • Sawyer LA, McInnis J, Patel A, Horne AD, Albrecht P. Deleterious effect of thimerosal on the potency of inactivated poliovirus vaccine. Vaccine. 1994;12(9):851–56. doi:10.1016/0264-410x(94)90296-8.
  • Davisson EO, Powell HM, Macfarlane JO, Hodgson R, Stone RL, Culbertson CG. The preservation of poliomyelitis vaccine with stabilized merthiolate. J Lab Clin Med. 1956;47:8–19.
  • Kraan H, ten Have R, van der Maas L, Kersten G, Amorij J-P. Incompatibility of lyophilized inactivated polio vaccine with liquid pentavalent whole-cell-pertussis-containing vaccine. Vaccine. 2016;34(38):4572–78. doi:10.1016/j.vaccine.2016.07.030.
  • Alghounaim M, Alsaffar Z, Alfraij A, Bin-Hasan S, Hussain E. Whole-cell and acellular pertussis vaccine: reflections on efficacy. Med Princ Pract. 2022;31(4):313–21. doi:10.1159/000525468.
  • Sawant N, Kaur K, Holland DA, Hickey JM, Agarwal S, Brady JR, Dalvie NC, Tracey MK, Velez-Suberbie ML, Morris SA, et al. Rapid Developability assessments to formulate recombinant protein antigens as stable, low-cost, multi-dose vaccine candidates: case-study with Non-Replicating Rotavirus (NRRV) vaccine antigens. J Pharm Sci. 2021;110:1042–53. doi:10.1016/j.xphs.2020.11.039.
  • Kaur K, Xiong J, Sawant N, Agarwal S, Hickey JM, Holland DA, Mukhopadhyay TK, Brady JR, Dalvie NC, Tracey MK, et al. Mechanism of thimerosal-induced structural destabilization of a recombinant rotavirus P[4] protein antigen formulated as a multi-dose vaccine. J Pharm Sci. 2021;110:1054–66. doi:10.1016/j.xphs.2020.11.033.
  • EasySix, Panacea Biotec. Package insert. [ accessed 2022 Mar 19]. https://media.panaceabiotec.com/documents/2019/7/24/Easysix-PMPIS05903.pdf.
  • Kumar R, Sharma IJ, Vyankatrao SA, Manohar D, Sharma HJ; An immunogenic composition having improved stability, enhanced immunogenicity and reduced reactogenicity and process for preparation there of. PCT/IB2018/055180. 2019. https://patentscope.wipo.int/search/en/detail.jsf?docId=WO2019016654.
  • Young CS, Ae NY, Ji KE; Combination vaccine composition for multiple-dosage. PCT/KR2016/010313. 2017. https://patentscope.wipo.int/search/en/detail.jsf?docId=WO2017048038.
  • Mangarule S, Palkar S, Mitra M, Ravi MD, Dubey AP, Moureau A, Jayanth MV, Patel DM, Ravinuthala S, Jagga SR, et al. Safety and immunogenicity of a hexavalent DTwP-IPV-HB-PRP~ T vaccine versus separate DTwP-HB-PRP~ T and IPV vaccines in healthy infants in India. Vaccine. 2022;X:10. doi:10.1016/j.jvacx.2021.100137.
  • Kumru OS, Joshi SB, Smith DE, Middaugh CR, Prusik T, Volkin DB. Vaccine instability in the cold chain: mechanisms, analysis and formulation strategies. Biologicals. 2014;42(5):237–59. doi:10.1016/j.biologicals.2014.05.007.
  • Shin WJ, Hara D, Gbormittah F, Chang H, Chang BS, Jung JU. Development of thermostable lyophilized sabin inactivated poliovirus vaccine. mBio. 2018;9(6). doi:10.1128/mBio.02287-18.
  • Qi W, Orgel S, Francon A, Randolph TW, Carpenter JF. Urea improves stability of inactivated polio vaccine serotype 3 during lyophilization and storage in dried formulations. J Pharm Sci. 2018;107(8):2070–78. doi:10.1016/j.xphs.2018.04.019.
  • Kraan H, van Herpen P, Kersten G, Amorij J-P. Development of thermostable lyophilized inactivated polio vaccine. Pharm Res. 2014;31(10):2618–29. doi:10.1007/s11095-014-1359-6.
  • Preston KB, Randolph TW. Stability of lyophilized and spray dried vaccine formulations. Adv Drug Deliv Rev. 2021;171:50–61. doi:10.1016/j.addr.2021.01.016.
  • 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;3:51. doi:10.1038/s41541-018-0089-x.
  • 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. doi:10.1016/j.vaccine.2012.12.076.
  • Andreasen LV, Hansen LB, Andersen P, Agger EM, Dietrich J. Aluminium hydroxide potentiates a protective Th1 biased immune response against polio virus that allows for dose sparing in mice and rats. Vaccine. 2015;33:1873–79. doi:10.1016/j.vaccine.2015.02.011.
  • Bravo LC, Carlos JC, Gatchalian SR, Montellano MEB, Tabora C, Thierry-Carstensen B, Tingskov PN, Sorensen C, Wachmann H, Bandyopadhyay AS, et al. Immunogenicity and safety of an adjuvanted inactivated polio vaccine, IPV-Al, compared to standard IPV: a phase 3 observer-blinded, randomised, controlled trial in infants vaccinated at 6, 10, 14 weeks and 9 months of age. Vaccine. 2020;38(3):530–38. doi:10.1016/j.vaccine.2019.10.064.
  • Saez-Llorens X, Thierry-Carstensen B, Stoey LS, Sorensen C, Wachmann H, Bandyopadhyay AS, Nielsen PI, Kusk MV. Immunogenicity and safety of an adjuvanted inactivated polio vaccine, IPV-Al, following vaccination in children at 2, 4, 6 and at 15-18 months. Vaccine. 2020;38(21):3780–89. doi:10.1016/j.vaccine.2020.02.066.
  • Wallis C, Melnick JL, Ferry GD, Wimberly IL. An aluminum marker for the differentiation and separation of virulent and attenuated polioviruses. J Exp Med. 1962;115:763–75. doi:10.1084/jem.115.4.763.
  • Van Ramshorst JD. The concentration of poliovirus antigens for D-antigen determination. Bull World Health Organ. 1967;36:209–18.
  • Hawken J, Troy SB. Adjuvants and inactivated polio vaccine: a systematic review. Vaccine. 2012;30(49):6971–79. doi:10.1016/j.vaccine.2012.09.059.
  • Baldwin SL, Fox CB, Pallansch MA, Coler RN, Reed SG, Friede M. Increased potency of an inactivated trivalent polio vaccine with oil-in-water emulsions. Vaccine. 2011;29(4):644–49. doi:10.1016/j.vaccine.2010.11.043.
  • Dietrich J, Andreasen LV, Andersen P, Agger EM. Inducing dose sparing with inactivated polio virus formulated in adjuvant CAF01. PLoS One. 2014;9(6):e100879. doi:10.1371/journal.pone.0100879.
  • Steil BP, Jorquera P, Westdijk J, Bakker WAM, Johnston RE, Barro M. A mucosal adjuvant for the inactivated poliovirus vaccine. Vaccine. 2014;32(5):558–63. doi:10.1016/j.vaccine.2013.11.101.
  • Norton EB, Bauer DL, Weldon WC, Oberste MS, Lawson LB, Clements JD. The novel adjuvant dmLT promotes dose sparing, mucosal immunity and longevity of antibody responses to the inactivated polio vaccine in a murine model. Vaccine. 2015;33(16):1909–15. doi:10.1016/j.vaccine.2015.02.069.
  • White JA, Blum JS, Hosken NA, Marshak JO, Duncan L, Zhu CC, Norton EB, Clements JD, Koelle DM, Chen DX, et al. Serum and mucosal antibody responses to inactivated polio vaccine after sublingual immunization using a thermoresponsive gel delivery system. Hum Vaccines Immunother. 2014;10(12):3611–21. doi:10.4161/hv.32253.
  • Yang CT, Shi HY, Zhou J, Liang YW, Xu HL. CpG oligodeoxynucleotides are a potent adjuvant for an inactivated polio vaccine produced from Sabin strains of poliovirus. Vaccine. 2009;27(47):6558–63. doi:10.1016/j.vaccine.2009.08.047.
  • Ghendon Y, Markushin S, Akopova I, Koptiaeva I, Krivtsov G. Chitosan as an adjuvant for poliovaccine. J Med Virol. 2011;83(5):847–52. doi:10.1002/jmv.22030.
  • Ivanov AP, Dragunsky EM, Chumakov KM. 1,25-Dihydroxyvitamin D3 enhances systemic and mucosal immune responses to inactivated poliovirus vaccine in mice. J Infect Dis. 2006;193(4):598–600. doi:10.1086/499970.
  • de Costa F, Yendo ACA, Cibulski SP, Fleck JD, Roehe PM, Spilki FR, Gosmann G, Fett-Neto AG. Alternative inactivated poliovirus vaccines adjuvanted with quillaja brasiliensis or quil-a saponins are equally effective in inducing specific immune responses. PLoS One. 2014;9(8):e105374. doi:10.1371/journal.pone.0105374.
  • Kraan H, van der Stel W, Kersten G, Amorij JP. Alternative administration routes and delivery technologies for polio vaccines. Expert Rev Vaccines. 2016;15(8):1029–40. doi:10.1586/14760584.2016.1158650.
  • Tzeng SY, Guarecuco R, McHugh KJ, Rose S, Rosenberg EM, Zeng YY, Langer R, Jaklenec A. Thermostabilization of inactivated polio vaccine in PLGA-based microspheres for pulsatile release. J Control Release. 2016;233:101–13. doi:10.1016/j.jconrel.2016.05.012.
  • Tzeng SY, McHugh KJ, Behrens AM, Rose S, Sugarman JL, Ferber S, Langer R, Jaklenec A. Stabilized single-injection inactivated polio vaccine elicits a strong neutralizing immune response. Proc Natl Acad Sci U S A. 2018;115(23):E5269–78. doi:10.1073/pnas.1720970115.
  • Kraan H, Soema P, Amorij JP, Kersten G. Intranasal and sublingual delivery of inactivated polio vaccine. Vaccine. 2017;35(20):2647–53. doi:10.1016/j.vaccine.2017.03.090.
  • Kraan H, Ploemen I, van de Wijdeven G, Que I, Löwik C, Kersten G, Amorij J-P. Alternative delivery of a thermostable inactivated polio vaccine. Vaccine. 2015;33(17):2030–37. doi:http://dx.doi.org/10.1016/j.vaccine.2015.03.011.
  • WHO. Intradermal delivery of vaccines. 2009 [accessed 2022 Mar 20]. https://www.who.int/immunization/programmes_systems/supply_chain/optimize/Intradermal-delivery-vaccines_report_2009-Sept.pdf.
  • Okayasu H, Sein C, Chang Blanc D, Gonzalez AR, Zehrung D, Jarrahian C, Macklin G, Sutter RW. Intradermal administration of fractional doses of inactivated poliovirus vaccine: a dose-sparing option for polio immunization. J Infect Dis. 2017;216(suppl_1):S161–67. doi:10.1093/infdis/jix038.
  • Cadorna-Carlos J, Vidor E, Bonnet MC. Randomized controlled study of fractional doses of inactivated poliovirus vaccine administered intradermally with a needle in the Philippines. Int J Infect Dis. 2012;16(2):e110–6. doi:10.1016/j.ijid.2011.10.002.
  • Anand A, Molodecky NA, Pallansch MA, Sutter RW. Immunogenicity to poliovirus type 2 following two doses of fractional intradermal inactivated poliovirus vaccine: a novel dose sparing immunization schedule. Vaccine. 2017;35(22):2993–98. doi:10.1016/j.vaccine.2017.03.008.
  • Bandyopadhyay AS, Gast C, Rivera L, Saez-Llorens X, Oberste MS, Weldon WC, Modlin J, Clemens R, Costa Clemens SA, Jimeno J, et al. Safety and immunogenicity of inactivated poliovirus vaccine schedules for the post-eradication era: a randomised open-label, multicentre, phase 3, non-inferiority trial. Lancet Infect Dis. 2021;21(4):559–68. doi:10.1016/S1473-3099(20)30555-7.
  • Yu C, Walter M. CADTH Rapid Response Report: Summary with Critical Appraisal. Needleless injectors for the administration of vaccines: areview of clinical effectiveness. Canada: Ottawa (ON): Canadian Agency for Drugs and Technologies in Health; 2020. 33296154. https://pubmed.ncbi.nlm.nih.gov/33296154/
  • Jaiswal N, Singh S, Agarwal A, Chauhan A, Thumburu KK, Kaur H, Singh M. Equivalent schedules of intradermal fractional dose versus intramuscular full dose of inactivated polio vaccine for prevention of poliomyelitis. Cochrane Database Syst Rev. 2019;12:CD011780. doi:10.1002/14651858.CD011780.pub2.
  • Hoffman PN, Abuknesha RA, Andrews NJ, Samuel D, Lloyd JS. A model to assess the infection potential of jet injectors used in mass immunisation. Vaccine. 2001;19(28–29):4020–27. doi:10.1016/S0264-410X(01)00106-2.
  • Sweat JM, Abdy M, Weniger BG, Harrington R, Coyle B, Abuknesha RA, Gibbs EP. Safety testing of needle free, jet injection devices to detect contamination with blood and other tissue fluids. Ann N Y Acad Sci. 2000;916:681–82. doi:10.1111/j.1749-6632.2000.tb05361.x.
  • Resik S, Tejeda A, Lago PM, Diaz M, Carmenates A, Sarmiento L, Alemani N, Galindo B, Burton A, Friede M, et al. Randomized controlled clinical trial of fractional doses of inactivated poliovirus vaccine administered intradermally by needle-free device in Cuba. J Infect Dis. 2010;201(9):1344–52. doi:10.1086/651611.
  • Mohammed AJ, AlAwaidy S, Bawikar S, Kurup PJ, Elamir E, Shaban MM, Sharif SM, van der Avoort HG, Pallansch MA, Malankar P, et al. Fractional doses of inactivated poliovirus vaccine in Oman. N Engl J Med. 2010;362(25):2351–59. doi:10.1056/NEJMoa0909383.
  • Estivariz CF, Jafari H, Sutter RW, John TJ, Jain V, Agarwal A, Verma H, Pallansch MA, Singh AP, Guirguis S, et al. Immunogenicity of supplemental doses of poliovirus vaccine for children aged 6-9 months in Moradabad, India: a community-based, randomised controlled trial. Lancet Infect Dis. 2012;12(2):128–35. doi:10.1016/S1473-3099(11)70190-6.
  • Moon SS, Richter-Roche M, Resch TK, Wang Y, Foytich KR, Wang H, Mainou BA, Pewin W, Lee J, Henry S, et al. Microneedle patch as a new platform to effectively deliver inactivated polio vaccine and inactivated rotavirus vaccine. NPJ Vaccines. 2022;7(1):26. doi:10.1038/s41541-022-00443-7.
  • Wei JCJ, Haridass IN, Crichton ML, Mohammed YH, Meliga SC, Sanchez WY, Grice JE, Benson HAE, Roberts MS, Kendall MAF. Space- and time-resolved investigation on diffusion kinetics of human skin following macromolecule delivery by microneedle arrays. Sci Rep. 2018;8(1):17759. doi:10.1038/s41598-018-36009-8.
  • Edens C, Dybdahl-Sissoko NC, Weldon WC, Oberste MS, Prausnitz MR. Inactivated polio vaccination using a microneedle patch is immunogenic in the rhesus macaque. Vaccine. 2015;33(37):4683–90. doi:10.1016/j.vaccine.2015.01.089.
  • Jeong SY, Park JH, Lee YS, Kim YS, Park JY, Kim SY. The current status of clinical research involving microneedles: a systematic review. Pharmaceutics. 2020;12(11). doi:10.3390/pharmaceutics12111113.
  • Adhikari BB, Goodson JL, Chu SY, Rota PA, Meltzer MI. Assessing the potential cost-effectiveness of microneedle patches in childhood measles vaccination programs: the case for further research and development. Drugs RS. 2016;16(4):327–38. doi:10.1007/s40268-016-0144-x.
  • Kolluru C, Gomaa Y, Prausnitz MR. Development of a thermostable microneedle patch for polio vaccination. Drug Deliv Transl Res. 2019;9(1):192–203. doi:10.1007/s13346-018-00608-9.
  • Muller DA, Pearson FE, Fernando GJ, Agyei-Yeboah C, Owens NS, Corrie SR, Crichton ML, Wei JC, Weldon WC, Oberste MS, et al. Inactivated poliovirus type 2 vaccine delivered to rat skin via high density microprojection array elicits potent neutralising antibody responses. Sci Rep. 2016;6:22094. doi:10.1038/srep22094.
  • Fernando GJ, Zhang J, Ng HI, Haigh OL, Yukiko SR, Kendall MA. Influenza nucleoprotein DNA vaccination by a skin targeted, dry coated, densely packed microprojection array (Nanopatch) induces potent antibody and CD8(þ) T cell responses. J Control Release. 2016;237:35–41. doi:10.1016/j.jconrel.2016.06.045.
  • Pearson FE, McNeilly CL, Crichton ML, Primiero CA, Yukiko SR, Fernando GJ, Chen X, Gilbert SC, Hill AV, Kendall MA. Dry-coated live viral vector vaccines delivered by nanopatch microprojections retain long-term thermostability and induce transgene-specific T cell responses in mice. PLoS One. 2013;8(7):e67888. doi:10.1371/journal.pone.0067888.
  • Prow TW, Chen X, Prow NA, Fernando GJ, Tan CS, Raphael AP, Chang D, Ruutu MP, Jenkins DW, Pyke A, et al. Nanopatch-targeted skin vaccination against west Nile virus and chikungunya virus in mice. Small. 2010;6(16):1776–84. doi:10.1002/smll.201000331.
  • Pearson FE, Muller DA, Roalfe L, Zancolli M, Goldblatt D, Kendall MA. Functional anti-polysaccharide IgG titres induced by unadjuvanted pneumococcal-conjugate vaccine when delivered by microprojection-based skin patch. Vaccine. 2015;33(48):6675–83. doi:10.1016/j.vaccine.2015.10.081.
  • Crichton ML, Muller DA, Depelsenaire ACI, Pearson FE, Wei J, Coffey J, Zhang J, Fernando GJP, Kendall MAF. The changing shape of vaccination: improving immune responses through geometrical variations of a microdevice for immunization. Sci Rep. 2016;6:27217. doi:10.1038/srep27217.
  • Crichton ML, Archer-Jones C, Meliga S, Edwards G, Martin D, Huang H, Kendall MA. Characterising the material properties at the interface between skin and a skin vaccination microprojection device. Acta Biomater. 2016;36:186–94. doi:10.1016/j.actbio.2016.02.039.
  • McNeilly CL, Crichton ML, Primiero CA, Frazer IH, Roberts MS, Kendall MA. Microprojection arrays to immunise at mucosal surfaces. J Control Release. 2014;196:252–60. doi:10.1016/j.jconrel.2014.09.028.
  • Raphael AP, Prow TW, Crichton ML, Chen X, Fernando GJ, Kendall MA. Targeted, needle-free vaccinations in skin using multilayered, densely-packed dissolving microprojection arrays. Small. 2010;6(16):1785–93. doi:10.1002/smll.201000326.
  • Raphael AP, Crichton ML, Falconer RJ, Meliga S, Chen X, Fernando GJ, Huang H, Kendall MA. Formulations for microprojection/microneedle vaccine delivery: structure, strength and release profiles. J Control Release. 2016;225:40–52. doi:10.1016/j.jconrel.2016.01.027.
  • Jenkins D, Corrie S, Flaim C, Kendall M. High density and high aspect ratio solid micro-nanoprojection arrays for targeted skin vaccine delivery and specific antibody extraction. RSC Adv. 2012;2(8):3490–95. doi:10.1039/C2RA20153D.
  • Meyer BK, Kendall MAF, Williams DM, Bett AJ, Dubey S, Gentzel RC, Casimiro D, Forster A, Corbett H, Crichton M, et al. Immune response and reactogenicity of an unadjuvanted intradermally delivered human papillomavirus vaccine using a first generation Nanopatch™ in rhesus macaques: an exploratory, pre-clinical feasibility assessment. vaccine X. 2019;2(2):100030. doi:10.1016/j.jvacx.2019.100030.
  • Westdijk J, Brugmans D, Martin J, van’t Oever A, Bakker WAM, Levels L, Kersten G. Characterization and standardization of Sabin based inactivated polio vaccine: proposal for a new antigen unit for inactivated polio vaccines. Vaccine. 2011;29(18):3390–97. doi:10.1016/j.vaccine.2011.02.085.
  • Crichton ML, Ansaldo A, Chen XF, Prow TW, Fernando GJP, Kendall MAF. The effect of strain rate on the precision of penetration of short densely-packed microprojection array patches coated with vaccine. Biomaterials. 2010;31(16):4562–72. doi:10.1016/j.biomaterials.2010.02.022.
  • Depelsenaire ACI, Meliga SC, McNeilly CL, Pearson FE, Coffey JW, Haigh OL, Flaim CJ, Frazer IH, Kendall MAF. Colocalization of cell death with antigen deposition in skin enhances vaccine immunogenicity. J Invest Dermatol. 2014;134(9):2361–70. doi:10.1038/jid.2014.174.
  • Wan Y, Gupta V, Bird C, Pullagurla SR, Fahey P, Forster A, Volkin DB, Joshi SB. Formulation development and improved stability of a combination measles and rubella live-viral vaccine dried for use in the nanopatch(TM) microneedle delivery system. Hum Vaccin Immunother. 2021;17(8):2501–16. doi:10.1080/21645515.2021.1887692.
  • Kumar P, Shukla RS, Patel A, Pullagurla SR, Bird C, Ogun O, Kumru OS, Hamidi A, Hoeksema F, Yallop C, et al. Formulation development of a live attenuated human rotavirus (RV3-BB) vaccine candidate for use in low- and middle-income countries. Hum Vaccin Immunother. 2021;17(7):2298–310. doi:10.1080/21645515.2021.1885279.
  • Kumar P, Pullagurla SR, Patel A, Shukla RS, Bird C, Kumru OS, Hamidi A, Hoeksema F, Yallop C, Bines JE, et al. Effect of formulation variables on the stability of a live, rotavirus (RV3-BB) vaccine candidate using in vitro gastric digestion models to mimic oral delivery. J Pharm Sci. 2021;110(2):760–70. doi:10.1016/j.xphs.2020.09.047.
  • McAdams D, Estrada M, Holland D, Singh J, Sawant N, Hickey JM, Kumar P, Plikaytis B, Joshi SB, Volkin DB, et al. Concordance of in vitro and in vivo measures of non-replicating rotavirus vaccine potency. Vaccine. 2022;40(34):5069–78. doi:https://doi.org/10.1016/j.vaccine.2022.07.017.
  • Hamidi A, Hoeksema F, Velthof P, Lemckert A, Gillissen G, Luitjens A, Bines JE, Pullagurla SR, Kumar P, Volkin DB, et al. Developing a manufacturing process to deliver a cost effective and stable liquid human rotavirus vaccine. Vaccine. 2021;39(15):2048–59. doi:10.1016/j.vaccine.2021.03.033.
  • Falcaro M, Castanon A, Ndlela B, Checchi M, Soldan K, Lopez-Bernal J, Elliss-Brookes L, Sasieni P. The effects of the national HPV vaccination programme in England, UK, on cervical cancer and grade 3 cervical intraepithelial neoplasia incidence: a register-based observational study. Lancet. 2021;398(10316):2084–92. doi:10.1016/S0140-6736(21)02178-4.
  • Lei J, Ploner A, Elfstrom KM, Wang J, Roth A, Fang F, Sundstrom K, Dillner J, Sparen P. HPV vaccination and the risk of invasive cervical cancer. N Engl J Med. 2020;383(14):1340–48. doi:10.1056/NEJMoa1917338.
  • WHO. Human papillomavirus (HPV) and cervical cancer. 2022 [accessed 2022 Sept 5]. https://www.who.int/news-room/fact-sheets/detail/cervical-cancer.
  • Parashar UD, Johnson H, Steele AD, Tate JE. Health impact of rotavirus vaccination in developing countries: progress and way forward. Clin Infect Dis. 2016;62 Suppl 2:S91–5. doi:10.1093/cid/civ1015.
  • Tate JE, Burton AH, Boschi-Pinto C, Parashar UD, World Health Organization-Coordinated Global Rotavirus Surveillance N. Global, regional, and national estimates of rotavirus mortality in children <5 years of age, 2000-2013. Clin Infect Dis. 2016;62(Suppl 2):S96–105. doi:10.1093/cid/civ1013.
  • Drain PK, Nelson CM, Lloyd JS. Single-dose versus multi-dose vaccine vials for immunization programmes in developing countries. Bull World Health Organ. 2003;81:726–31.
  • Jerajani K, Wan Y, Hickey JM, Kumru OS, Sharma N, Pullagurla SR, Ogun O, Mapari S, Whitaker N, Brendle S, et al. Analytical and preformulation characterization studies of human papillomavirus virus-like particles to enable quadrivalent multi-dose vaccine formulation development. J Pharm Sci. 2022. doi:10.1016/j.xphs.2022.07.019.
  • Sharma N, Jerajani K, Wan Y, Kumru OS, Pullagurla SR, Ogun O, Mapari S, Brendle SA, Christensen ND, Batwal S, et al. Multi-dose formulation development for a quadrivalent human papillomavirus virus-like particle-based vaccine: part II- accelerated and real-time stability studies. 2022. doi:10.1016/j.xphs.2022.11.021.
  • Kirkwood CD, Ma L-F, Carey ME, Steele AD. The rotavirus vaccine development pipeline. vaccine. 2019;37(50):7328–35. doi:https://dx.doi.org/10.1016/j.vaccine.2017.03.076.
  • Witte D, Handley A, Jere KC, Bogandovic-Sakran N, Mpakiza A, Turner A, Pavlic D, Boniface K, Mandolo J, Ong DS, et al. Neonatal rotavirus vaccine (RV3-BB) immunogenicity and safety in a neonatal and infant administration schedule in Malawi: a randomised, double-blind, four-arm parallel group dose-ranging study. Lancet Infect Dis. 2022;22(5):668–78. doi:10.1016/S1473-3099(21)00473-4.
  • Pullagurla SR, Kumar P, Ogun O, Kumru OS, Hamidi A, Hoeksema F, Yallop C, Bines JE, Volkin DB, Joshi SB. Modeling the long-term 2-8 degrees C stability profiles of a live, rotavirus vaccine candidate (RV3-BB) in various liquid formulations via extrapolations of real-time and accelerated stability data. Biologicals. 2022;75:21–28. doi:10.1016/j.biologicals.2021.12.001.
  • Cates JE, JE T, Parashar U. Rotavirus vaccines: progress and new developments. Expert Opin Biol Ther. 2021. doi:10.1080/14712598.2021.1977279.
  • Debellut F, Pecenka C, Hausdorff WP, Clark A. Potential impact and cost-effectiveness of injectable next-generation rotavirus vaccines in 137 LMICs: a modelling study. Hum Vaccin Immunother. 2022;18(1):2040329. doi:10.1080/21645515.2022.2040329.
  • Kyle Lakatos DM, White JA, White JA, Chen D. Dexiang Chen, Formulation and preclinical studies with a trivalent rotavirus P2-VP8 subunit vaccine. Hum Vaccin Immunother. 2020;16(8):1957–68. doi:10.1080/21645515.2019.1710412.
  • Forman R, Shah S, Jeurissen P, Jit M, Mossialos E. COVID-19 vaccine challenges: what have we learned so far and what remains to be done? Health Policy (New York). 2021;125(5):553–67. doi:10.1016/j.healthpol.2021.03.013.
  • Bajoria S, Kaur K, Kumru OS, Van Slyke G, Doering J, Novak H, Rodriguez Aponte SA, Dalvie NC, Naranjo CA, Johnston RS, et al. Antigen-adjuvant interactions, stability, and immunogenicity profiles of a SARS-CoV-2 receptor-binding domain (RBD) antigen formulated with aluminum salt and CpG adjuvants. Hum Vaccin Immunother. 2022;18(5):2079346. doi:10.1080/21645515.2022.2079346.