Microneedles for vaccine delivery: challenges and future perspectives

References

• 1 Unicef. Why are children dying? (2016). www.unicef.org/immunization/index_why.html.Google Scholar
• 2 The END Fund. NTD overview: what are neglected tropical diseases? (2017). www.end.org/whatwedo/ntdoverview.Google Scholar
• 3 World Health Organization. Neglected tropical diseases (2016). www.who.int/neglected_diseases/diseases/en/.Google Scholar
• 4 Walkinshaw E. Mandatory vaccinations: the international landscape. Can. Med. Assoc. J. 183(16), (2011).Google Scholar
• 5 Stern AM, Markel H. The history of vaccines and immunization: familiar patterns, new challenges. Health Aff. 24(3), 611–621 (2005).Crossref, Google Scholar
• 6 Suh H, Shin J, Kim Y-C. Microneedle patches for vaccine delivery. Clin. Exp. Vaccine. Res. 3(1), 42–49 (2014).Crossref, Medline, CAS, Google Scholar
• 7 Mitragotri S. Immunization without needles. Nat. Rev. Immunol. 5(12), 905–916 (2005).Crossref, Medline, CAS, Google Scholar
• 8 Canadian Paediatric Society. Needle stick injuries. Paed Child Healt. 13(3), (2008).Google Scholar
• 9 Nir Y, Paz A, Sabo E, Potasman I. Fear of injections in young adults: prevalence and associations. Am. J. Trop. Med. Hyg. 68(3), 341–344 (2003).Crossref, Medline, Google Scholar
• 10 Taddio A, Ipp M, Thivakaran S et al. Survey of the prevalence of immunization non-compliance due to needle fears in children and adults. Vaccine 30(32), 4807–4812 (2012).Crossref, Medline, Google Scholar
• 11 Desai SN, Cravioto A, Sur D, Kanungo S. Maximizing protection from use of oral cholera vaccines in developing country settings: an immunological review of oral cholera vaccines. Hum. Vaccin. Immunother. 10(6), 1457–1465 (2014).Crossref, Medline, Google Scholar
• 12 Glass RI, Parashar UD. Rotavirus vaccines – balancing intus susception risks and health benefits. N. Engl. J. Med. 370, 568–570 (2014).Crossref, Medline, CAS, Google Scholar
• 13 Haque R, Snider C, Liu Y et al. Oral polio vaccine response in breast fed infants with malnutrition and diarrhea. Vaccine 32(4), 478–482 (2014).Crossref, Medline, Google Scholar
• 14 Choi H-J, Ebersbacher CF, Kim M-C, Kang S-M, Montemagno CD. A mechanistic study on the destabilization of whole inactivated influenza virus vaccine in gastric environment. PLoS ONE 8(6), e66316 (2013).Crossref, Medline, CAS, Google Scholar
• 15 Moon C, Oh E. Rationale and strategies for formulation development of oral fixed dose combination drug products. J. Pharm. Investig. 46, 615 (2016).Crossref, CAS, Google Scholar
• 16 Des Rieux A, Fievez V, Garinot M, Schneider Y-J, Préat V. Nanoparticles as potential oral delivery systems of proteins and vaccines: a mechanistic approach. J. Control. Rel. 116(1), 1–27 (2006).Crossref, Medline, CAS, Google Scholar
• 17 Hutchinson E. Vaccination: oral vaccine induces genitorectal immunity. Nat. Rev. Immunol. 12(9), 619–619 (2012).Crossref, Medline, CAS, Google Scholar
• 18 Kim YC, Park JH, Prausnitz MR. Microneedles for drug and vaccine delivery. Adv. Drug. Deliv. Rev. 64(14), 1547–1568 (2012).Crossref, Medline, CAS, Google Scholar
• 19 Rejinold NS, Shin J-H, Seok HY, Kim Y-C. Biomedical applications of microneedles in therapeutics: recent advancements and implications in drug delivery. Expert. Opin. Drug. Del. 13(1), 109–131 (2016).Crossref, Medline, CAS, Google Scholar
• 20 Kim Y-C, Prausnitz MR. Enabling skin vaccination using new delivery technologies. Drug. Deliv. Transl. Res. 1(1), 7–12 (2011).Crossref, Medline, Google Scholar
• 21 Laurent A, Mistretta F, Bottigioli D et al. Echographic measurement of skin thickness in adults by high frequency ultrasound to assess the appropriate microneedle length for intradermal delivery of vaccines. Vaccine 25(34), 6423–6430 (2007).Crossref, Medline, Google Scholar
• 22 Kim Y-C, Jarrahian C, Zehrung D, Mitragotri S, Prausnitz M. Delivery systems for intradermal vaccination. Curr. Top. Microbiol. Immunol. 351, 77–112 (2011).Google Scholar
• 23 Merad M, Ginhoux F, Collin M. Origin, homeostasis and function of Langerhans cells and other langerin-expressing dendritic cells. Nat. Rev. Immunol. 8(12), 935–947 (2008).Crossref, Medline, CAS, Google Scholar
• 24 Prausnitz MR, Mikszta JA, Cormier M, Andrianov AK. Microneedle-based vaccines. In: Vaccines for Pandemic Influenza. Richard W. Compans, Walter A. Orenstein (Eds). Springer, Berlin Heidelberg, 369–393 (2009).Crossref, Google Scholar
• 25 Cheung K, Das DB. Microneedles for drug delivery: trends and progress. Drug. Deliv. 23(7), 2338–2354 (2016).Crossref, Medline, CAS, Google Scholar
• 26 Takahashi H, Heo YJ, Arakawa N et al. Scalable fabrication of microneedle arrays via spatially controlled UV exposure. Microsyst. Nanoeng. 2, 16049 (2016).Crossref, Medline, CAS, Google Scholar
• 27 Lee G-H, Park YE, Cho M, Park H, Park JY. Magnetic force-assisted self-locking metallic bead array for fabrication of diverse concave microwell geometries. Lab. Chip. 16(18), 3565–3575 (2016).Crossref, Medline, CAS, Google Scholar
• 28 Heo YJ, Arakawa N, Yoshizawa S, Takahashi H, Kawano R. Microneedle array fabrication using inclined/rotated UV lithography. 19th International Conference on Miniaturized Systems for Chemistry and Life Sciences. Gyeongju, Korea, October 25–29, (2015).Google Scholar
• 29 Le Thanh H, Ta BQ, Le The H, Nguyen V, Wang K, Karlsen F. Low-cost fabrication of hollow microneedle arrays using CNC machining and UV lithography. J. Microelectromech. S. 24(5), 1583–1593 (2015).Crossref, Google Scholar
• 30 Ling Z, Lian K. SU-8 3D microoptic components fabricated by inclined UV lithography in water. Microsyst. Technol. 13(3–4), 245–251 (2007).Crossref, CAS, Google Scholar
• 31 Kang W-J, Rabe E, Kopetz S, Neyer A. Novel exposure methods based on reflection and refraction effects in the field of SU-8 lithography. J. Micromech. microeng. 16(4), 821 (2006).Crossref, CAS, Google Scholar
• 32 Hung K-Y, Hu H-T, Tseng F-G. Application of 3D glycerol-compensated inclined-exposure technology to an integrated optical pick-up head. J. Micromech. microeng. 14(7), 975 (2004).Crossref, Google Scholar
• 33 Miyamatsu T, Wang Y, Shima M et al. Material design for immersion lithography with high refractive index fluid (HIF). Presented at: Microlithography 2005. San Jose, CA, USA, February 27, (2005).Crossref, Google Scholar
• 34 Jiang G, Baig S, Wang MR. Prism-assisted inclined UV lithography for 3D microstructure fabrication. J. Micromech. microeng. 22(8), 085022 (2012).Crossref, Google Scholar
• 35 Jin CY, Han MH, Lee SS, Choi YH. Mass producible and biocompatible microneedle patch and functional verification of its usefulness for transdermal drug delivery. Biomed. Microdevices. 11(6), 1195 (2009).Crossref, Medline, CAS, Google Scholar
• 36 Broers AN. High resolution lithography systems: a review of the current status. Physik. Blätt. 34(12), 704–712 (1978).Crossref, CAS, Google Scholar
• 37 Ito T, Okazaki S. Pushing the limits of lithography. Nature 406(6799), 1027–1031 (2000).Crossref, Medline, CAS, Google Scholar
• 38 Khumpuang S, Horade M, Fujioka K, Sugiyama S. Microneedle fabrication using the plane pattern to cross-section transfer method. Smart. Mater. Struct. 15(2), 600 (2006).Crossref, Google Scholar
• 39 Matsuzuka N, Hirai Y, Tabata O. A novel fabrication process of 3D microstructures by double exposure in deep x-ray lithography (D2XRL). J. Micromech. microeng. 15(11), 2056 (2005).Crossref, CAS, Google Scholar
• 40 Moon SJ, Lee SS. A novel fabrication method of a microneedle array using inclined deep x-ray exposure. J. Micromech. microeng. 15(5), 903 (2005).Crossref, CAS, Google Scholar
• 41 Khumpuang S, Horade M, Fujioka K, Sugiyama S. Geometrical strengthening and tip-sharpening of a microneedle array fabricated by X-ray lithography. Microsyst. Technol. 13(3–4), 209–214 (2007).Crossref, CAS, Google Scholar
• 42 Lee K, Jung H. Drawing lithography for microneedles: a review of fundamentals and biomedical applications. Biomaterials 33(30), 7309–7326 (2012).Crossref, Medline, CAS, Google Scholar
• 43 Lee K, Lee HC, Lee DS, Jung H. Drawing lithography: three-dimensional fabrication of an ultrahigh-aspect-ratio microneedle. Adv. Mater. 22(4), 483–486 (2010).Crossref, Medline, CAS, Google Scholar
• 44 Li CG, Lee CY, Lee K, Jung H. An optimized hollow microneedle for minimally invasive blood extraction. Biomed. Microdevices. 15(1), 17–25 (2013).Crossref, Medline, Google Scholar
• 45 Lee CY, Lee K, You YS, Lee SH, Jung H. Tower microneedle via reverse drawing lithography for innocuous intravitreal drug delivery. Adv. Healthc. Mater. 2(6), 812–816 (2013).Crossref, Medline, CAS, Google Scholar
• 46 You YS, Lee CY, Li C, Lee SH, Kim K, Jung H. An arched micro-injector (ARCMI) for innocuous subretinal injection. PLoS ONE 9(8), e104145 (2014).Crossref, Medline, Google Scholar
• 47 Jung Dong Kim J-HB, Hong Kee Kim, Do Hyeon Jeong. Droplet-born air blowing (DAB) technology for the industrialization of dissolving microneedle. Proceedings of the World Congress on Recent Advances in Nanotechnology. Prague, Czech Republic doi:10.11159/nddte16.122 April 1–2, (2016).Google Scholar
• 48 Incyto. Hollow micro needle (2010). www.incyto.com/product/product10_index.php.Google Scholar
• 49 Lee JB, Choi K-H, Yoo K. Innovative SU-8 lithography techniques and their applications. Micromachines 6(1), 1–18 (2014).Crossref, Google Scholar
• 50 Van Der Maaden K, Jiskoot W, Bouwstra J. Microneedle technologies for (trans) dermal drug and vaccine delivery. J. Control. Rel. 161(2), 645–655 (2012).Crossref, Medline, CAS, Google Scholar
• 51 Zahn JD, Talbot NH, Liepmann D, Pisano AP. Microfabricated polysilicon microneedles for minimally invasive biomedical devices. Biomed. Microdevices. 2(4), 295–303 (2000).Crossref, Google Scholar
• 52 Mcallister DV, Wang PM, Davis SP et al. Microfabricated needles for transdermal delivery of macromolecules and nanoparticles: fabrication methods and transport studies. Proc. Natl Acad. Sci. USA 100(24), 13755–13760 (2003).Crossref, Medline, CAS, Google Scholar
• 53 Bediz B, Korkmaz E, Khilwani R et al. Dissolvable microneedle arrays for intradermal delivery of biologics: fabrication and application. Pharm. Res. 31(1), 117–135 (2014).Crossref, Medline, CAS, Google Scholar
• 54 Lee JW, Park JH, Prausnitz MR. Dissolving microneedles for transdermal drug delivery. Biomaterials 29(13), 2113–2124 (2008).Crossref, Medline, CAS, Google Scholar
• 55 Park JH, Allen MG, Prausnitz MR. Biodegradable polymer microneedles: fabrication, mechanics and transdermal drug delivery. J. Control. Rel. 104(1), 51–66 (2005).Crossref, Medline, CAS, Google Scholar
• 56 Kolli CS, Banga AK. Characterization of solid maltose microneedles and their use for transdermal delivery. Pharm. Res. 25(1), 104–113 (2008).Crossref, Medline, CAS, Google Scholar
• 57 Yan G, Warner KS, Zhang J, Sharma S, Gale BK. Evaluation needle length and density of microneedle arrays in the pretreatment of skin for transdermal drug delivery. Int. J. Pharm. 391(1), 7–12 (2010).Crossref, Medline, CAS, Google Scholar
• 58 Davidson A, Al-Qallaf B, Das DB. Transdermal drug delivery by coated microneedles: geometry effects on effective skin thickness and drug permeability. Chem. Eng. Res. Des. 86(11), 1196–1206 (2008).Crossref, CAS, Google Scholar
• 59 Gill HS, Denson DD, Burris BA, Prausnitz MR. Effect of microneedle design on pain in human subjects. Clin. J. Pain 24(7), 585 (2008).Crossref, Medline, Google Scholar
• 60 Davis SP, Landis BJ, Adams ZH, Allen MG, Prausnitz MR. Insertion of microneedles into skin: measurement and prediction of insertion force and needle fracture force. J. Biomech. 37(8), 1155–1163 (2004).Crossref, Medline, Google Scholar
• 61 Nissha Printing Co. Ltd. MicroCure microneedle patches for cosmetics (2017). www.nissha.com/english/company/crd/needle.html.Google Scholar
• 62 Yang S, Feng Y, Zhang L, Chen N, Yuan W, Jin T. A scalable fabrication process of polymer microneedles. Int. J. Nanomed. 7, 1415–1422 (2012).Medline, CAS, Google Scholar
• 63 Nestle FO, Di Meglio P, Qin J-Z, Nickoloff BJ. Skin immune sentinels in health and disease. Nat. Rev. Immunol. 9(10), 679–691 (2009).Crossref, Medline, CAS, Google Scholar
• 64 Gill HS, Prausnitz MR. Coating formulations for microneedles. Pharm. Res. 24(7), 1369–1380 (2007).Crossref, Medline, CAS, Google Scholar
• 65 Lee JW, Choi SO, Felner EI, Prausnitz MR. Dissolving microneedle patch for transdermal delivery of human growth hormone. Small 7(4), 531–539 (2011).Crossref, Medline, CAS, Google Scholar
• 66 Liu S, Jin M-N, Quan Y-S et al. Transdermal delivery of relatively high molecular weight drugs using novel self-dissolving microneedle arrays fabricated from hyaluronic acid and their characteristics and safety after application to the skin. Eur. J. Pharm. Biopharm. 86(2), 267–276 (2014).Crossref, Medline, CAS, Google Scholar
• 67 Wang PM, Cornwell M, Hill J, Prausnitz MR. Precise microinjection into skin using hollow microneedles. J. Invest. Dermatol. 126(5), 1080–1087 (2006).Crossref, Medline, CAS, Google Scholar
• 68 Edens C, Collins ML, Ayers J, Rota PA, Prausnitz MR. Measles vaccination using a microneedle patch. Vaccine 31(34), 3403–3409 (2013).Crossref, Medline, CAS, Google Scholar
• 69 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 33(37), 4683–4690 (2015).Crossref, Medline, CAS, Google Scholar
• 70 Kommareddy S, Baudner B, Bonificio A et al. Influenza subunit vaccine coated microneedle patches elicit comparable immune responses to intramuscular injection in guinea pigs. Vaccine 31(34), 3435–3441 (2013).Crossref, Medline, CAS, Google Scholar
• 71 Dean CH, Alarcon JB, Waterston AM et al. Cutaneous delivery of a live, attenuated chimeric flavivirus vaccines against Japanese encephalitis (ChimeriVaxTM-JE) in non-human primates. Hum. Vaccines. 1(3), 106–111 (2005).Crossref, Medline, CAS, Google Scholar
• 72 Beals CR, Railkar RA, Schaeffer AK et al. Immune response and reactogenicity of intradermal administration versus subcutaneous administration of varicella-zoster virus vaccine: an exploratory, randomised, partly blinded trial. Lancet Infect. Dis. 16(8), 915–922 (2016).Crossref, Medline, CAS, Google Scholar
• 73 Kim Y-C, Quan F-S, Yoo D-G, Compans RW, Kang S-M, Prausnitz MR. Enhanced memory responses to seasonal H1N1 influenza vaccination of the skin with the use of vaccine-coated microneedles. J. Infect. Dis. 201(2), 190–198 (2010).Crossref, Medline, CAS, Google Scholar
• 74 Kim Y-C, Quan F-S, Compans RW, Kang S-M, Prausnitz MR. Formulation and coating of microneedles with inactivated influenza virus to improve vaccine stability and immunogenicity. J. Control. Rel. 142(2), 187–195 (2010).Crossref, Medline, CAS, Google Scholar
• 75 Moon S, Wang Y, Edens C, Gentsch JR, Prausnitz MR, Jiang B. Dose sparing and enhanced immunogenicity of inactivated rotavirus vaccine administered by skin vaccination using a microneedle patch. Vaccine 31(34), 3396–3402 (2013).Crossref, Medline, CAS, Google Scholar
• 76 Laurent PE, Bourhy H, Fantino M, Alchas P, Mikszta JA. Safety and efficacy of novel dermal and epidermal microneedle delivery systems for rabies vaccination in healthy adults. Vaccine 28(36), 5850–5856 (2010).Crossref, Medline, Google Scholar
• 77 Kim E, Erdos G, Huang S, Kenniston T, Falo LD, Gambotto A. Preventative vaccines for Zika virus outbreak: preliminary evaluation. EBioMedicine 13, 315–320 (2016).Crossref, Medline, Google Scholar
• 78 Pearton M, Kang S-M, Song J-M et al. Influenza virus-like particles coated onto microneedles can elicit stimulatory effects on Langerhans cells in human skin. Vaccine 28(37), 6104–6113 (2010).Crossref, Medline, CAS, Google Scholar
• 79 Quan F-S, Kim Y-C, Vunnava A et al. Intradermal vaccination with influenza virus-like particles by using microneedles induces protection superior to that with intramuscular immunization. J. Virol. 84(15), 7760–7769 (2010).Crossref, Medline, CAS, Google Scholar
• 80 Sanders B, Koldijk M, Schuitemaker H. Inactivated viral vaccines. In: Vaccine Analysis: Strategies, Principles, and Control. Brian K. Nunnally, Vincent E. Turula, Robert D. Sitrin. Springer, Berlin, Heidelberg, 45–80 (2015).Crossref, Google Scholar
• 81 Hansen L, Daoussi R, Vervaet C, Remon J-P, De Beer T. Freeze-drying of live virus vaccines: a review. Vaccine 33(42), 5507–5519 (2015).Crossref, Medline, CAS, Google Scholar
• 82 Edens C, Collins ML, Goodson JL, Rota PA, Prausnitz MR. A microneedle patch containing measles vaccine is immunogenic in non-human primates. Vaccine 33(37), 4712–4718 (2015).Crossref, Medline, CAS, Google Scholar
• 83 Lohmann V, Körner F, Koch J-O, Herian U, Theilmann L, Bartenschlager R. Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 285(5424), 110–113 (1999).Crossref, Medline, CAS, Google Scholar
• 84 Pawar SD, Murtadak VB, Kale SD, Shinde PV, Parkhi SS. Evaluation of different inactivation methods for high and low pathogenic avian influenza viruses in egg-fluids for antigen preparation. J. Virol. Methods 222, 28–33 (2015).Crossref, Medline, CAS, Google Scholar
• 85 Cromeans T, Park GW, Costantini V et al. Comprehensive comparison of cultivable norovirus surrogates in response to different inactivation and disinfection treatments. Appl. Environ. Microbiol. 80(18), 5743–5751 (2014).Crossref, Medline, Google Scholar
• 86 Pfaender S, Brinkmann J, Todt D et al. Mechanisms of methods for hepatitis C virus inactivation. Appl. Environ. Microbiol. 81(5), 1616–1621 (2015).Crossref, Medline, CAS, Google Scholar
• 87 Predmore A, Sanglay GC, Dicaprio E, Li J, Uribe R, Lee K. Electron beam inactivation of Tulane virus on fresh produce, and mechanism of inactivation of human norovirus surrogates by electron beam irradiation. Int. J. Food Microbiol. 198, 28–36 (2015).Crossref, Medline, Google Scholar
• 88 Kew OM, Sutter RW, De Gourville EM, Dowdle WR, Pallansch MA. Vaccine-derived polioviruses and the endgame strategy for global polio eradication. Annu. Rev. Microbiol. 59, 587–635 (2005).Crossref, Medline, CAS, Google Scholar
• 89 Chu LY, Ye L, Dong K, Compans RW, Yang C, Prausnitz MR. Enhanced stability of inactivated influenza vaccine encapsulated in dissolving microneedle patches. Pharm. Res. 33(4), 868–878 (2016).Crossref, Medline, CAS, Google Scholar
• 90 Kim YC, Lee SH, Choi WH et al. Microneedle delivery of trivalent influenza vaccine to the skin induces long-term cross-protection. J. Drug Target. 24(10), 943–951 (2016).Crossref, Medline, CAS, Google Scholar
• 91 Schipper P, Van Der Maaden K, Romeijn S et al. Repeated fractional intradermal dosing of an inactivated polio vaccine by a single hollow microneedle leads to superior immune responses. J. Control. Rel. 242, 141–147 (2016).Crossref, Medline, CAS, Google Scholar
• 92 Koutsonanos DG, Esser ES, Mcmaster SR et al. Enhanced immune responses by skin vaccination with influenza subunit vaccine in young hosts. Vaccine 33(37), 4675–4682 (2015).Crossref, Medline, CAS, Google Scholar
• 93 Frey SE, Harrison C, Pass RF et al. Effects of antigen dose and immunization regimens on antibody responses to a cytomegalovirus glycoprotein B subunit vaccine. J. Infect. Dis. 180(5), 1700–1703 (1999).Crossref, Medline, CAS, Google Scholar
• 94 Mistilis MJ, Bommarius AS, Prausnitz MR. Development of a thermostable microneedle patch for influenza vaccination. J. Pharm. Sci. 104(2), 740–749 (2015).Crossref, Medline, CAS, Google Scholar
• 95 Weldon WC, Zarnitsyn VG, Esser ES et al. Effect of adjuvants on responses to skin immunization by microneedles coated with influenza subunit vaccine. PLoS ONE 7(7), e41501 (2012).Crossref, Medline, CAS, Google Scholar
• 96 Quan F-S, Kim Y-C, Compans RW, Prausnitz MR, Kang S-M. Dose sparing enabled by skin immunization with influenza virus-like particle vaccine using microneedles. J. Control. Rel. 147(3), 326–332 (2010).Crossref, Medline, CAS, Google Scholar
• 97 Song J-M, Kim Y-C, Barlow PG et al. Improved protection against avian influenza H5N1 virus by a single vaccination with virus-like particles in skin using microneedles. Antiviral Res. 88(2), 244–247 (2010).Crossref, Medline, CAS, Google Scholar
• 98 Kim Y-C, Quan F-S, Compans RW, Kang S-M, Prausnitz MR. Formulation of microneedles coated with influenza virus-like particle vaccine. AAPS PharmSciTech 11(3), 1193–1201 (2010).Crossref, Medline, CAS, Google Scholar
• 99 Quan F-S, Kim Y-C, Song J-M et al. Long-term protective immunity from an influenza virus-like particle vaccine administered with a microneedle patch. Clin. Vaccine Immunol. 20(9), 1433–1439 (2013).Crossref, Medline, CAS, Google Scholar
• 100 Kim MC, Lee JW, Choi HJ et al. Microneedle patch delivery to the skin of virus-like particles containing heterologous M2e extracellular domains of influenza virus induces broad heterosubtypic cross-protection. J. Control. Rel. 210, 208–216 (2015).Crossref, Medline, CAS, Google Scholar
• 101 Wang B-Z, Gill HS, He C et al. Microneedle delivery of an M2e-TLR5 ligand fusion protein to skin confers broadly cross-protective influenza immunity. J. Control. Rel. 178, 1–7 (2014).Crossref, Medline, CAS, Google Scholar
• 102 Medicago Inc. Medicago and IDRI reports positive results for its Phase I clinical trial for an H5N1 vaccine (2013). http://www.prnewswire.com/news-releases/medicago-and-idri-reports-positive-results-for-its-phase-i-clinical-trial-for-an-h5n1-vaccine-203445681.html.Google Scholar
• 103 Rybicki EP. Plant-based vaccines against viruses. Virol J. 11(1), 205 (2014).Crossref, Medline, Google Scholar
• 104 Kutzler MA, Weiner DB. DNA vaccines: ready for prime time? Nat. Rev. Genet. 9(10), 776–788 (2008).Crossref, Medline, CAS, Google Scholar
• 105 Corr M, Lee DJ, Carson DA, Tighe H. Gene vaccination with naked plasmid DNA: mechanism of CTL priming. J. Exp. Med. 184(4), 1555–1560 (1996).Crossref, Medline, CAS, Google Scholar
• 106 Prather KJ, Sagar S, Murphy J, Chartrain M. Industrial scale production of plasmid DNA for vaccine and gene therapy: plasmid design, production, and purification. Enzyme Microb. Technol. 33(7), 865–883 (2003).Crossref, CAS, Google Scholar
• 107 Watts AM, Kennedy RC. DNA vaccination strategies against infectious diseases. Int. J. Parasitol. 29(8), 1149–1163 (1999).Crossref, Medline, CAS, Google Scholar
• 108 Gurunathan S, Klinman DM, Seder RA. DNA vaccines: immunology, application, and optimization. Annu. Rev. Immunol. 18(1), 927–974 (2000).Crossref, Medline, CAS, Google Scholar
• 109 Kutzler MA, Weiner DB. Developing DNA vaccines that call to dendritic cells. J. Clin. Invest. 114(9), 1241–1244 (2004).Crossref, Medline, CAS, Google Scholar
• 110 Dynavax Technologies. Third Phase 3 trial shows HEPLISAV-B vaccine safe, effective against HBV (2016). http://www.healio.com/infectious-disease/vaccine-preventable-diseases/news/online/%7Bac90c05c-0e64-4cb6-adc1-18cd7fdb343b%7D/third-phase-3-trial-shows-heplisav-b-vaccine-safe-effective-against-hbv.Google Scholar
• 111 Kim Y-C, Song J-M, Lipatov AS et al. Increased immunogenicity of avian influenza DNA vaccine delivered to the skin using a microneedle patch. Eur. J. Pharm. Biopharm. 81(2), 239–247 (2012).Crossref, Medline, CAS, Google Scholar
• 112 Song J-M, Kim Y-C, Eunju O, Compans RW, Prausnitz MR, Kang S-M. DNA vaccination in the skin using microneedles improves protection against influenza. Mol. Ther. 20(7), 1472–1480 (2012).Crossref, Medline, CAS, Google Scholar
• 113 Hu Y, Xu B, Xu J et al. Microneedle-assisted dendritic cell-targeted nanoparticles for transcutaneous DNA immunization. Polym. Chem. 6(3), 373–379 (2015).Crossref, CAS, Google Scholar
• 114 Kim NW, Lee MS, Kim KR et al. Polyplex-releasing microneedles for enhanced cutaneous delivery of DNA vaccine. J. Control. Rel. 179, 11–17 (2014).Crossref, Medline, CAS, Google Scholar
• 115 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(+) T cell responses. J. Control. Rel. 237, 35–41 (2016).Crossref, Medline, CAS, Google Scholar
• 116 Arya JM, Dewitt K, Scott-Garrard M, Chiang YW, Prausnitz MR. Rabies vaccination in dogs using a dissolving microneedle patch. J. Control. Rel. 239, 19–26 (2016).Crossref, Medline, CAS, Google Scholar
• 117 Yang HW, Ye L, Guo XD, Yang C, Compans RW, Prausnitz MR. Ebola vaccination using a DNA vaccine coated on PLGA-PLL/gammaPGA nanoparticles administered using a microneedle patch. Adv. Healthc. Mater. 6(1), (2017).Crossref, Google Scholar
• 118 Curtiss R. Bacterial infectious disease control by vaccine development. J. Clin. Invest. 110(8), 1061–1066 (2002).Crossref, Medline, CAS, Google Scholar
• 119 Koch R. An address on bacteriological research. Br. Med. J. 2(1546), 380 (1890).Crossref, Medline, CAS, Google Scholar
• 120 Haesebrouck F, Pasmans F, Chiers K, Maes D, Ducatelle R, Decostere A. Efficacy of vaccines against bacterial diseases in swine: what can we expect? Vet. Microbiol. 100(3–4), 255–268 (2004).Crossref, Medline, CAS, Google Scholar
• 121 Hiraishi Y, Nandakumar S, Choi S-O et al. Bacillus Calmette-Guerin vaccination using a microneedle patch. Vaccine 29(14), 2626–2636 (2011).Crossref, Medline, CAS, Google Scholar
• 122 Thwaites CL, Beeching NJ, Newton CR. Maternal and neonatal tetanus. Lancet 385(9965), 362–370 (2015).Crossref, Medline, Google Scholar
• 123 Esser ES, Romanyuk A, Vassilieva EV et al. Tetanus vaccination with a dissolving microneedle patch confers protective immune responses in pregnancy. J. Control. Rel. 236, 47–56 (2016).Crossref, Medline, CAS, Google Scholar
• 124 Siddhapura K, Harde H, Jain S. Immunostimulatory effect of tetanus toxoid loaded chitosan nanoparticles following microneedles assisted immunization. Nanomedicine 12(1), 213–222 (2016).Crossref, Medline, CAS, Google Scholar
• 125 Ding Z, Bal SM, Romeijn S, Kersten GF, Jiskoot W, Bouwstra JA. Transcutaneous immunization studies in mice using diphtheria toxoid-loaded vesicle formulations and a microneedle array. Pharm. Res. 28(1), 145–158 (2011).Crossref, Medline, CAS, Google Scholar
• 126 Chen X, Kositratna G, Zhou C, Manstein D, Wu MX. Micro-fractional epidermal powder delivery for improved skin vaccination. J. Control. Rel. 192, 310–316 (2014).Crossref, Medline, CAS, Google Scholar
• 127 Larrañeta E, Lutton RE, Woolfson AD, Donnelly RF. Microneedle arrays as transdermal and intradermal drug delivery systems: materials science, manufacture and commercial development. Mat. Sci. Eng. R. 104, 1–32 (2016).Crossref, Google Scholar
• 128 Donnelly R, Douroumis D. Microneedles for drug and vaccine delivery and patient monitoring. Drug Deliv Transl Res. 5(4), 311–312 (2015).Crossref, Medline, Google Scholar
• 129 Kaddar M. World Health Organization Presentation Global vaccine market features and trends (2014).Google Scholar
• 130 Arya J, Prausnitz MR. Microneedle patches for vaccination in developing countries. J. Control. Rel. 240, 135–141 (2016).Crossref, Medline, CAS, Google Scholar
• 131 Jamil RK, Taqavian M, Sadigh Z-A et al. Evaluation of the thermal stability of a novel strain of live-attenuated mumps vaccine (RS-12 strain) lyophilized in different stabilizers. J. Virol. Methods 199, 35–38 (2014).Crossref, Medline, CAS, Google Scholar
• 132 Kristensen D, Chen D, Cummings R. Vaccine stabilization: research, commercialization, and potential impact. Vaccine 29(41), 7122–7124 (2011).Crossref, Medline, CAS, Google Scholar
• 133 Reed SG, Orr MT, Fox CB. Key roles of adjuvants in modern vaccines. Nat. Med. 19(12), 1597–1608 (2013).Crossref, Medline, CAS, Google Scholar
• 134 Who U, World Bank. State of the world's vaccines and immunization (2009). www.who.int/immunization/sowvi/en/.Google Scholar
• 135 Patel SR, Prausnitz MR. Targeted drug delivery within the eye through the suprachoroidal space. J. Ocul. Pharmacol. Ther. 32(10), 640–641 (2016).Crossref, Medline, CAS, Google Scholar
• 136 Gilger BC, Abarca EM, Salmon JH, Patel S. Treatment of acute posterior uveitis in a porcine model by injection of triamcinolone acetonide into the suprachoroidal space using microneedles triamcinolone in the suprachoroidal space. Invest. Ophthalmol. Vis. Sci. 54(4), 2483–2492 (2013).Crossref, Medline, CAS, Google Scholar
• 137 Ma Y, Tao W, Krebs SJ, Sutton WF, Haigwood NL, Gill HS. Vaccine delivery to the oral cavity using coated microneedles induces systemic and mucosal immunity. Pharm. Res. 31(9), 2393–2403 (2014).Crossref, Medline, CAS, Google Scholar
• 138 Van Damme P, Oosterhuis-Kafeja F, Van Der Wielen M, Almagor Y, Sharon O, Levin Y. Safety and efficacy of a novel microneedle device for dose sparing intradermal influenza vaccination in healthy adults. Vaccine 27(3), 454–459 (2009).Crossref, Medline, Google Scholar
• 139 Hirobe S, Azukizawa H, Hanafusa T et al. Clinical study and stability assessment of a novel transcutaneous influenza vaccination using a dissolving microneedle patch. Biomaterials 57, 50–58 (2015).Crossref, Medline, CAS, Google Scholar
• 140 Daddona PE, Matriano JA, Mandema J, Maa Y-F. Parathyroid hormone (1–34)-coated microneedle patch system: clinical pharmacokinetics and pharmacodynamics for treatment of osteoporosis. Pharm. Res. 28(1), 159–165 (2011).Crossref, Medline, CAS, Google Scholar
• 141 Arnou R, Icardi G, De Decker M et al. Intradermal influenza vaccine for older adults: a randomized controlled multicenter Phase III study. Vaccine 27(52), 7304–7312 (2009).Crossref, Medline, CAS, Google Scholar