Effect of vaccine administration modality on immunogenicity and efficacy

References

• Baxby D. Edward Jenner’s Inquiry; a bicentenary analysis. Vaccine 1999;17(4):301-7
   PubMed Web of Science ®Google Scholar
• Vaccine Recommendations of the ACIP. Available from: www.cdc.gov/vaccines/hcp/acip-recs/index.html
   Google Scholar
• Public health then and now :celebrating 50 years of MMWR at CDC. US. Department of Health and Human Services, Centers for Disease Control and Prevention, Atlanta, GA, 2011
   Google Scholar
• Blundell TL, Sibanda BL, Sternberg MJ, Thornton JM. Knowledge-based prediction of protein structures and the design of novel molecules. Nature 1987;326(6111):347-52
   PubMed Web of Science ®Google Scholar
• Richie TL, Saul A. Progress and challenges for malaria vaccines. Nature 2002;415(6872):694-701
   PubMed Web of Science ®Google Scholar
• Scanlan CN, Offer J, Zitzmann N, Dwek RA. Exploiting the defensive sugars of HIV-1 for drug and vaccine design. Nature 2007;446(7139):1038-45
   PubMed Web of Science ®Google Scholar
• Hilleman MR. A simplified vaccinologists’ vaccinology and the pursuit of a vaccine against AIDS. Vaccine 1998;16(8):778-93
   PubMed Web of Science ®Google Scholar
• Ellis RW. The new generation of recombinant viral subunit vaccines. Curr Opin Biotechnol 1996;7(6):646-52
   PubMed Web of Science ®Google Scholar
• Whalen RG, Leclerc C, Deriaud E, et al. DNA-mediated immunization to the hepatitis B surface antigen. Activation and entrainment of the immune response. Ann N Y Acad Sci 1995;772:64-76
   PubMed Web of Science ®Google Scholar
• Boog CJ. Principles of vaccination and possible development strategies for rational design. Immunol Lett 2009;122(2):104-7
   PubMed Web of Science ®Google Scholar
• Ludwig C, Wagner R. Virus-like particles-universal molecular toolboxes. Curr Opin Biotechnol 2007;18(6):537-45
   PubMed Web of Science ®Google Scholar
• Lu S, Grimes SJM, Wang S. Polyvalent AIDS vaccines. Curr HIV Res 2010;8(8):622-9
   PubMed Web of Science ®Google Scholar
• Lu S. Heterologous prime-boost vaccination. Curr Opin Immunol 2009;21(3):346-51
   PubMed Web of Science ®Google Scholar
• Pulendran B. Systems vaccinology: probing humanity’s diverse immune systems with vaccines. Proc Natl Acad Sci USA 2014;111(34):12300-6
   PubMed Web of Science ®Google Scholar
• Pulendran B, Oh JZ, Nakaya HI, et al. Immunity to viruses: learning from successful human vaccines. Immunol Rev 2013;255(1):243-55
   PubMed Web of Science ®Google Scholar
• Nakaya HI, Pulendran B. Systems vaccinology: its promise and challenge for HIV vaccine development. Curr Opin HIV AIDS 2012;7(1):24-31
   PubMed Web of Science ®Google Scholar
• Immunization schedules. Available from: www.cdc.gov/vaccines/schedules/
   Google Scholar
• Patel SM, Atmar RL, El SHM, et al. A phase I evaluation of inactivated influenza A/H5N1 vaccine administered by the intradermal or the intramuscular route. Vaccine 2010;28(17):3025-9
   PubMed Web of Science ®Google Scholar
• Park DE, Johnson TS, Nonyane BA, et al. The differential impact of coadministered vaccines, geographic region, vaccine product and other covariates on pneumococcal conjugate vaccine immunogenicity. Pediatr Infect Dis J 2014;33(Suppl 2):S130-9
   PubMed Web of Science ®Google Scholar
• Arguedas A, Soley C, Abdelnour A, et al. Assessment of the safety, tolerability and kinetics of the immune response to A/H1N1v vaccine formulations with and without adjuvant in healthy pediatric subjects from 3 through 17 years of age. Hum Vaccin 2011;7(1):58-66
   PubMed Web of Science ®Google Scholar
• Charest AF, McDougall J, Goldstein MB. A randomized comparison of intradermal and intramuscular vaccination against hepatitis B virus in incident chronic hemodialysis patients. Am J Kidney Dis 2000;36(5):976-82
   PubMed Web of Science ®Google Scholar
• Barraclough KA, Wiggins KJ, Hawley CM, et al. Intradermal versus intramuscular hepatitis B vaccination in hemodialysis patients: a prospective open-label randomized controlled trial in nonresponders to primary vaccination. Am J Kidney Dis 2009;54(1):95-103
   PubMed Web of Science ®Google Scholar
• Schwarz TF, Horacek T, Knuf M, et al. Single dose vaccination with AS03-adjuvanted H5N1 vaccines in a randomized trial induces strong and broad immune responsiveness to booster vaccination in adults. Vaccine 2009;27(45):6284-90
   PubMed Web of Science ®Google Scholar
• Rumke HC, Loch HP, Hoppenbrouwers K, et al. Immunogenicity and safety of a measles-mumps-rubella-varicella vaccine following a 4-week or a 12-month interval between two doses. Vaccine 2011;29(22):3842-9
   PubMed Web of Science ®Google Scholar
• Ledgerwood JE, Zephir K, Hu Z, et al. Prime-boost interval matters: a randomized phase 1 study to identify the minimum interval necessary to observe the H5 DNA influenza vaccine priming effect. J Infect Dis 2013;208(3):418-22
   PubMed Web of Science ®Google Scholar
• Beran J, Abdel-Messih IA, Raupachova J, et al. A phase III, randomized, open-label study to assess the tolerability and immunogenicity of an H5N1 influenza vaccine administered to healthy adults with a 1-, 2-, 3-, or 6-week interval between first and second doses. Clin Ther 2010;32(13):2186-97
   PubMed Web of Science ®Google Scholar
• Lodolce AE. Shortened interval between tetanus vaccines. Ann Pharmacother 2012;46(6):884-8
   PubMed Web of Science ®Google Scholar
• Ikeno D, Kimachi K, Kudo Y, et al. A prime-boost vaccination of mice with heterologous H5N1 strains. Vaccine 2009;27(23):3121-5
   PubMed Web of Science ®Google Scholar
• Zhang W, Ahmad G, Torben W, Siddiqui AA. Schistosoma mansoni antigen Sm-p80: Prophylactic efficacy of a vaccine formulated in human approved plasmid vector and adjuvant (VR 1020 and alum). Acta Trop 2011;118(2):142-51
   PubMed Web of Science ®Google Scholar
• Wang S, Parker C, Taaffe J, et al. Heterologous HA DNA vaccine prime–inactivated influenza vaccine boost is more effective than using DNA or inactivated vaccine alone in eliciting antibody responses against H1 or H3 serotype influenza viruses. Vaccine 2008;26(29-30):3626-33
   PubMed Web of Science ®Google Scholar
• Wang S, Arthos J, Lawrence JM, et al. Enhanced immunogenicity of gp120 protein when combined with recombinant DNA priming to generate antibodies that neutralize the JR-FL primary isolate of human immunodeficiency virus type 1. J Virol 2005;79(12):7933-7
   PubMed Web of Science ®Google Scholar
• Wang S, Pal R, Mascola JR, et al. Polyvalent HIV-1 Env vaccine formulations delivered by the DNA priming plus protein boosting approach are effective in generating neutralizing antibodies against primary human immunodeficiency virus type 1 isolates from subtypes A, B, C, D and E. Virology 2006;350(1):34-47
   PubMed Web of Science ®Google Scholar
• Vaine M, Wang S, Hackett A, et al. Antibody responses elicited through homologous or heterologous prime-boost DNA and protein vaccinations differ in functional activity and avidity. Vaccine 2010;28(17):2999-3007
   PubMed Web of Science ®Google Scholar
• Ishizaki H, Song GY, Srivastava T, et al. Heterologous prime/boost immunization with p53-based vaccines combined with toll-like receptor stimulation enhances tumor regression. J Immunother 2010;33(6):609-17
   PubMed Web of Science ®Google Scholar
• Jain S, Patrick AJ, Rosenthal KL. Multiple tandem copies of conserved gp41 epitopes incorporated in gag virus-like particles elicit systemic and mucosal antibodies in an optimized heterologous vector delivery regimen. Vaccine 2010;28(43):7070-80
   PubMed Web of Science ®Google Scholar
• McKay PF, Cope AV, Mann JF, et al. Glucopyranosyl lipid A adjuvant significantly enhances HIV specific T and B cell responses elicited by a DNA-MVA-protein vaccine regimen. PLoS One 2014;9(1):e84707
   PubMed Web of Science ®Google Scholar
• Tomai MA. TLR Agonists as Vaccine Adjuvants. In: Bascghieri S, editor. Innovation in Vaccinology. Springer ScienceBerlin, Germany; 2012. p. 205-28
   Google Scholar
• Garland SM. Imiquimod. Curr Opin Infect Dis 2003;16(2):85-9
   PubMed Web of Science ®Google Scholar
• Zhang AJ, Li C, To KK, et al. Toll-like receptor 7 agonist imiquimod in combination with influenza vaccine expedites and augments humoral immune responses against influenza A(H1N1)pdm09 virus infection in BALB/c mice. Clin Vaccine Immunol 2014;21(4):570-9
   PubMed Web of Science ®Google Scholar
• Johnston D, Bystryn JC. Topical imiquimod is a potent adjuvant to a weakly-immunogenic protein prototype vaccine. Vaccine 2006;24(11):1958-65
   PubMed Web of Science ®Google Scholar
• Chuang CM, Monie A, Hung CF, Wu TC. Treatment with imiquimod enhances antitumor immunity induced by therapeutic HPV DNA vaccination. J Biomed Sci 2010;17:32
   PubMed Web of Science ®Google Scholar
• Demaria S, Vanpouille-Box C, Formenti SC, Adams S. The TLR7 agonist imiquimod as an adjuvant for radiotherapy-elicited in situ vaccination against breast cancer. Oncoimmunology 2013;2(10):e25997
   PubMed Web of Science ®Google Scholar
• Xiong Z, Ohlfest JR. Topical imiquimod has therapeutic and immunomodulatory effects against intracranial tumors. J Immunother 2011;34(3):264-9
   PubMed Web of Science ®Google Scholar
• Roukens AH, Vossen AC, Boland GJ, et al. Intradermal hepatitis B vaccination in non-responders after topical application of imiquimod (Aldara). Vaccine 2010;28(26):4288-93
   PubMed Web of Science ®Google Scholar
• Firbas C, Boehm T, Buerger V, et al. Immunogenicity and safety of different injection routes and schedules of IC41, a Hepatitis C virus (HCV) peptide vaccine. Vaccine 2010;28(12):2397-407
   PubMed Web of Science ®Google Scholar
• Nierkens S, den Brok MH, Garcia Z, et al. Immune adjuvant efficacy of CpG oligonucleotide in cancer treatment is founded specifically upon TLR9 function in plasmacytoid dendritic cells. Cancer Res 2011;71(20):6428-37
   PubMed Web of Science ®Google Scholar
• Vollmer J, Krieg AM. Immunotherapeutic applications of CpG oligodeoxynucleotide TLR9 agonists. Adv Drug Deliv Rev 2009;61(3):195-204
   PubMed Web of Science ®Google Scholar
• Zent CS, Smith BJ, Ballas ZK, et al. Phase I clinical trial of CpG oligonucleotide 7909 (PF-03512676) in patients with previously treated chronic lymphocytic leukemia. Leuk Lymphoma 2012;53(2):211-17
   PubMed Web of Science ®Google Scholar
• Carpentier A, Metellus P, Ursu R, et al. Intracerebral administration of CpG oligonucleotide for patients with recurrent glioblastoma: a phase II study. Neuro Oncol 2010;12(4):401-8
   PubMed Web of Science ®Google Scholar
• Veenstra JJ, Gibson HM, Littrup PJ, et al. Cryotherapy with Concurrent CpG Oligonucleotide Treatment Controls Local Tumor Recurrence and Modulates HER2/neu Immunity. Cancer Res 2014;74(19):5409-20
   PubMed Web of Science ®Google Scholar
• Scheiermann J, Klinman DM. Clinical evaluation of CpG oligonucleotides as adjuvants for vaccines targeting infectious diseases and cancer. Vaccine 2014;32(48):6377-89
   Google Scholar
• Todoroff J, Lemaire MM, Fillee C, et al. Mucosal and systemic immune responses to Mycobacterium tuberculosis antigen 85A following its co-delivery with CpG, MPLA or LTB to the lungs in mice. PLoS One 2013;8(5):e63344
   PubMed Web of Science ®Google Scholar
• Mansourian M, Badiee A, Jalali SA, et al. Effective induction of anti-tumor immunity using p5 HER-2/neu derived peptide encapsulated in fusogenic DOTAP cationic liposomes co-administrated with CpG-ODN. Immunol Lett 2014;162(1 Pt A):87-93
   Google Scholar
• Evans JT, Cluff CW, Johnson DA, et al. Enhancement of antigen-specific immunity via the TLR4 ligands MPL adjuvant and Ribi.529. Expert Rev Vaccines 2003;2(2):219-29
   PubMedGoogle Scholar
• Brito LA, Malyala P, O’Hagan DT. Vaccine adjuvant formulations: a pharmaceutical perspective. Semin Immunol 2013;25(2):130-45
   PubMed Web of Science ®Google Scholar
• Tagliabue A, Rappuoli R. Vaccine adjuvants: the dream becomes real. Hum Vaccin 2008;4(5):347-9
   PubMed Web of Science ®Google Scholar
• Gasparini R, Pozzi T, Montomoli E, et al. Increased immunogenicity of the MF59-adjuvanted influenza vaccine compared to a conventional subunit vaccine in elderly subjects. Eur J Epidemiol 2001;17(2):135-40
   PubMed Web of Science ®Google Scholar
• Frey S, Poland G, Percell S, Podda A. Comparison of the safety, tolerability, and immunogenicity of a MF59-adjuvanted influenza vaccine and a non-adjuvanted influenza vaccine in non-elderly adults. Vaccine 2003;21(27-30):4234-7
   PubMed Web of Science ®Google Scholar
• Del Giudice G, Hilbert AK, Bugarini R, et al. An MF59-adjuvanted inactivated influenza vaccine containing A/Panama/1999 (H3N2) induced broader serological protection against heterovariant influenza virus strain A/Fujian/2002 than a subunit and a split influenza vaccine. Vaccine 2006;24(16):3063-5
   PubMed Web of Science ®Google Scholar
• Einstein MH, Levin MJ, Chatterjee A, et al. Comparative humoral and cellular immunogenicity and safety of human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine and HPV-6/11/16/18 vaccine in healthy women aged 18-45 years: follow-up through Month 48 in a Phase III randomized study. Hum Vaccin Immunother 2014;10(12):3455-65
   PubMed Web of Science ®Google Scholar
• Hazebrouck S, Przybylski-Nicaise L, Ah-Leung S, et al. Influence of the route of administration on immunomodulatory properties of bovine beta-lactoglobulin-producing Lactobacillus casei. Vaccine 2009;27(42):5800-5
   PubMed Web of Science ®Google Scholar
• Tang DC, Nguyen HH. The Yin-Yang arms of vaccines: disease-fighting power versus tissue-destructive inflammation. Expert Rev Vaccines 2014;13(3):417-27
   PubMed Web of Science ®Google Scholar
• Stevceva L, Ferrari MG. Mucosal adjuvants. Curr Pharm Des 2005;11(6):801-11
   PubMed Web of Science ®Google Scholar
• Vajdy M, Singh M. The role of adjuvants in the development of mucosal vaccines. Expert Opin Biol Ther 2005;5(7):953-65
   PubMed Web of Science ®Google Scholar
• Asanuma H, Hirokawa K, Uchiyama M, et al. Immune responses and protection in different strains of aged mice immunized intranasally with an adjuvant-combined influenza vaccine. Vaccine 2001;19(28-29):3981-9
   PubMed Web of Science ®Google Scholar
• Bumann D, Behre C, Behre K, et al. Systemic, nasal and oral live vaccines against Pseudomonas aeruginosa: a clinical trial of immunogenicity in lower airways of human volunteers. Vaccine 2010;28(3):707-13
   PubMed Web of Science ®Google Scholar
• Hickey DK, Aldwell FE, Beagley KW. Oral immunization with a novel lipid-based adjuvant protects against genital Chlamydia infection. Vaccine 2010;28(7):1668-72
   PubMed Web of Science ®Google Scholar
• Kende M, Del GG, Rivera N, Hewetson J. Enhancement of intranasal vaccination in mice with deglycosylated chain A ricin by LTR72, a novel mucosal adjuvant. Vaccine 2006;24(12):2213-21
   PubMed Web of Science ®Google Scholar
• Enioutina EY, Visic D, Daynes RA. The induction of systemic and mucosal immune responses to antigen-adjuvant compositions administered into the skin: alterations in the migratory properties of dendritic cells appears to be important for stimulating mucosal immunity. Vaccine 2000;18(24):2753-67
   PubMed Web of Science ®Google Scholar
• Mann JF, Shakir E, Carter KC, et al. Lipid vesicle size of an oral influenza vaccine delivery vehicle influences the Th1/Th2 bias in the immune response and protection against infection. Vaccine 2009;27(27):3643-9
   PubMed Web of Science ®Google Scholar
• Joo HM, He Y, Sundararajan A, et al. Quantitative analysis of influenza virus-specific B cell memory generated by different routes of inactivated virus vaccination. Vaccine 2010;28(10):2186-94
   PubMed Web of Science ®Google Scholar
• Gallorini S, Taccone M, Bonci A, et al. Sublingual immunization with a subunit influenza vaccine elicits comparable systemic immune response as intramuscular immunization, but also induces local IgA and TH17 responses. Vaccine 2014;32(20):2382-8
   PubMed Web of Science ®Google Scholar
• Huang J, Mikszta JA, Ferriter MS, et al. Intranasal administration of dry powder anthrax vaccine provides protection against lethal aerosol spore challenge. Hum Vaccin 2007;3(3):90-3
   PubMed Web of Science ®Google Scholar
• Ichinohe T, Ainai A, Tashiro M, et al. PolyI:polyC12U adjuvant-combined intranasal vaccine protects mice against highly pathogenic H5N1 influenza virus variants. Vaccine 2009;27(45):6276-9
   PubMed Web of Science ®Google Scholar
• Roy CJ, Ault A, Sivasubramani SK, et al. Aerosolized adenovirus-vectored vaccine as an alternative vaccine delivery method. Respir Res 2011;12:153
   PubMed Web of Science ®Google Scholar
• Wong-Chew RM, Islas-Romero R, Garcia-Garcia Mde L, et al. Immunogenicity of aerosol measles vaccine given as the primary measles immunization to nine-month-old Mexican children. Vaccine 2006;24(5):683-90
   PubMed Web of Science ®Google Scholar
• Bennett JV, Fernandez de Castro J, Valdespino-Gomez JL, et al. Aerosolized measles and measles-rubella vaccines induce better measles antibody booster responses than injected vaccines: randomized trials in Mexican schoolchildren. Bull World Health Organ 2002;80(10):806-12
   PubMed Web of Science ®Google Scholar
• Choi JH, Schafer SC, Zhang L, et al. A single sublingual dose of an adenovirus-based vaccine protects against lethal Ebola challenge in mice and guinea pigs. Mol Pharm 2012;9(1):156-67
   PubMed Web of Science ®Google Scholar
• Hunter Z, Smyth HD, Durfee P, Chackerian B. Induction of mucosal and systemic antibody responses against the HIV coreceptor CCR5 upon intramuscular immunization and aerosol delivery of a virus-like particle based vaccine. Vaccine 2009;28(2):403-14
   PubMed Web of Science ®Google Scholar
• Kapusta J, Modelska A, Figlerowicz M, et al. A plant-derived edible vaccine against hepatitis B virus. Faseb J 1999;13(13):1796-9
   PubMed Web of Science ®Google Scholar
• Alvarez ML, Cardineau GA. Prevention of bubonic and pneumonic plague using plant-derived vaccines. Biotechnol Adv 2010;28(1):184-96
   PubMed Web of Science ®Google Scholar
• Matoba N, Kajiura H, Cherni I, et al. Biochemical and immunological characterization of the plant-derived candidate human immunodeficiency virus type 1 mucosal vaccine CTB-MPR. Plant Biotechnol J 2009;7(2):129-45
   PubMed Web of Science ®Google Scholar
• Liang W, Huang Y, Yang X, et al. Oral immunization of mice with plant-derived fimbrial adhesin FaeG induces systemic and mucosal K88ad enterotoxigenic Escherichia coli-specific immune responses. FEMS Immunol Med Microbiol 2006;46(3):393-9
   PubMed Web of Science ®Google Scholar
• Tirabassi RS, Ace CI, Levchenko T, et al. A mucosal vaccination approach for herpes simplex virus type 2. Vaccine 2011;29(5):1090-8
   PubMed Web of Science ®Google Scholar
• Cho HJ, Kim JY, Lee Y, et al. Enhanced humoral and cellular immune responses after sublingual immunization against human papillomavirus 16 L1 protein with adjuvants. Vaccine 2010;28(14):2598-606
   PubMed Web of Science ®Google Scholar
• Lu YJ, Yadav P, Clements JD, et al. Options for inactivation, adjuvant, and route of topical administration of a killed, unencapsulated pneumococcal whole-cell vaccine. Clin Vaccine Immunol 2010;17(6):1005-12
   PubMed Web of Science ®Google Scholar
• Schellekens H. Immunogenicity of therapeutic proteins: clinical implications and future prospects. Clin Ther 2002;24(11):1720-40; discussion 19
   PubMed Web of Science ®Google Scholar
• Schellekens H. Immunogenicity of therapeutic proteins. Nephrol Dial Transplant 2003;18(7):1257-9
   PubMed Web of Science ®Google Scholar
• Ramsay JD, Williams CL, Simko E. Fatal adverse pulmonary reaction in calves after inadvertent intravenous vaccination. Vet Pathol 2005;42(4):492-5
   PubMed Web of Science ®Google Scholar
• Frosner G, Steffen R, Herzog C. Virosomal hepatitis a vaccine: comparing intradermal and subcutaneous with intramuscular administration. J Travel Med 2009;16(6):413-19
   PubMed Web of Science ®Google Scholar
• Davis HL. Novel vaccines and adjuvant systems: the utility of animal models for predicting immunogenicity in humans. Hum Vaccin 2008;4(3):246-50
   PubMed Web of Science ®Google Scholar
• Bonnotte B, Gough M, Phan V, et al. Intradermal injection, as opposed to subcutaneous injection, enhances immunogenicity and suppresses tumorigenicity of tumor cells. Cancer Res 2003;63(9):2145-9
   PubMed Web of Science ®Google Scholar
• Zehrung D, Jarrahian C, Wales A. Intradermal delivery for vaccine dose sparing: overview of current issues. Vaccine 2013;31(34):3392-5
   PubMed Web of Science ®Google Scholar
• Enama ME, Ledgerwood JE, Novik L, et al. Phase I randomized clinical trial of VRC DNA and rAd5 HIV-1 vaccine delivery by intramuscular (i.m.), subcutaneous (s.c.) and intradermal (i.d.) administration (VRC 011). PLoS One 2014;9(3):e91366
   PubMed Web of Science ®Google Scholar
• Ikeno D, Kimachi K, Kino Y, et al. Immunogenicity of an inactivated adjuvanted whole-virion influenza A (H5N1, NIBRG-14) vaccine administered by intramuscular or subcutaneous injection. Microbiol Immunol 2010;54(2):81-8
   PubMed Web of Science ®Google Scholar
• Mark A, Carlsson RM, Granstrom M. Subcutaneous versus intramuscular injection for booster DT vaccination of adolescents. Vaccine 1999;17(15-16):2067-72
   PubMed Web of Science ®Google Scholar
• Knuf M, Zepp F, Meyer CU, et al. Safety, immunogenicity and immediate pain of intramuscular versus subcutaneous administration of a measles-mumps-rubella-varicella vaccine to children aged 11-21 months. Eur J Pediatr 2010;169(8):925-33
   PubMed Web of Science ®Google Scholar
• Leung AK, Chiu AS, Siu TO. Subcutaneous versus intramuscular administration of Haemophilus influenzae type b vaccine. J R Soc Health 1989;109(2):71-3
   PubMedGoogle Scholar
• Malik B, Rath G, Goyal AK. Are the anatomical sites for vaccine administration selected judiciously? Int Immunopharmacol 2014;19(1):17-26
   PubMed Web of Science ®Google Scholar
• Tapiainen T, Cherry JD, Heininger U. Effect of injection site on reactogenicity and immunogenicity of acellular and whole-cell pertussis component diphtheria-tetanus-pertussis vaccines in infants. Vaccine 2005;23(43):5106-12
   PubMed Web of Science ®Google Scholar
• de Lalla F, Rinaldi E, Santoro D, Pravettoni G. Immune response to hepatitis B vaccine given at different injection sites and by different routes: a controlled randomized study. Eur J Epidemiol 1988;4(2):256-8
   PubMed Web of Science ®Google Scholar
• Shaw FEJr, Guess HA, Roets JM, et al. Effect of anatomic injection site, age and smoking on the immune response to hepatitis B vaccination. Vaccine 1989;7(5):425-30
   PubMed Web of Science ®Google Scholar
• Ohlfest JR, Andersen BM, Litterman AJ, et al. Vaccine injection site matters: qualitative and quantitative defects in CD8 T cells primed as a function of proximity to the tumor in a murine glioma model. J Immunol 2013;190(2):613-20
   PubMed Web of Science ®Google Scholar
• Diggle L, Deeks J. Effect of needle length on incidence of local reactions to routine immunisation in infants aged 4 months: randomised controlled trial. BMJ 2000;321(7266):931-3
   PubMed Web of Science ®Google Scholar
• Ipp MM, Gold R, Goldbach M, et al. Adverse reactions to diphtheria, tetanus, pertussis-polio vaccination at 18 months of age: effect of injection site and needle length. Pediatrics 1989;83(5):679-82
   PubMed Web of Science ®Google Scholar
• Jackson LA, Starkovich P, Dunstan M, et al. Prospective assessment of the effect of needle length and injection site on the risk of local reactions to the fifth diphtheria-tetanus-acellular pertussis vaccination. Pediatrics 2008;121(3):e646-52
   PubMed Web of Science ®Google Scholar
• Cook IF, Murtagh J. Needle length required for intramuscular vaccination of infants and toddlers. An ultrasonographic study. Aust Fam Physician 2002;31(3):295-7
   PubMedGoogle Scholar
• Donnelly RF, Woolfson AD. Patient safety and beyond: what should we expect from microneedle arrays in the transdermal delivery arena? Ther Deliv 2014;5(6):653-62
   PubMedGoogle Scholar
• Pettis RJ, Harvey AJ. Microneedle delivery: clinical studies and emerging medical applications. Ther Deliv 2012;3(3):357-71
   PubMedGoogle Scholar
• van der Maaden K, Jiskoot W, Bouwstra J. Microneedle technologies for (trans)dermal drug and vaccine delivery. J Control Release 2012;161(2):645-55
   PubMed Web of Science ®Google Scholar
• Koutsonanos DG, Compans RW, Skountzou I. Targeting the skin for microneedle delivery of influenza vaccine. Adv Exp Med Biol 2013;785:121-32
   PubMed Web of Science ®Google Scholar
• Donnelly RF, Mooney K, Caffarel-Salvador E, et al. Microneedle-mediated minimally invasive patient monitoring. Ther Drug Monit 2014;36(1):10-17
   PubMed Web of Science ®Google Scholar
• Seok HY, Suh H, Baek S, Kim YC. Microneedle applications for DNA vaccine delivery to the skin. Methods Mol Biol 2014;1143:141-58
   PubMedGoogle Scholar
• Suh H, Shin J, Kim YC. Microneedle patches for vaccine delivery. Clin Exp Vaccine Res 2014;3(1):42-9
   PubMedGoogle Scholar
• McGrath MG, Vucen S, Vrdoljak A, et al. Production of dissolvable microneedles using an atomised spray process: effect of microneedle composition on skin penetration. Eur J Pharm Biopharm 2014;86(2):200-11
   PubMed Web of Science ®Google Scholar
• Wang BZ, 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 Release 2014;178:1-7
   PubMed Web of Science ®Google Scholar
• van der Maaden K, Trietsch SJ, Kraan H, et al. Novel hollow microneedle technology for depth-controlled microinjection-mediated dermal vaccination: a study with polio vaccine in rats. Pharm Res 2014;31(7):1846-54
   PubMed Web of Science ®Google Scholar
• Carey JB, Vrdoljak A, O’Mahony C, et al. Microneedle-mediated immunization of an adenovirus-based malaria vaccine enhances antigen-specific antibody immunity and reduces anti-vector responses compared to the intradermal route. Sci Rep 2014;4:6154
   PubMed Web of Science ®Google Scholar
• Edens C, Collins ML, Ayers J, et al. Measles vaccination using a microneedle patch. Vaccine 2013;31(34):3403-9
   PubMed Web of Science ®Google Scholar
• Kim SH, Kim KS, Lee SR, et al. Structural modifications of outer membrane vesicles to refine them as vaccine delivery vehicles. Biochim Biophys Acta 2009;1788(10):2150-9
   PubMed Web of Science ®Google Scholar
• Van Damme P, Oosterhuis-Kafeja F, Van der Wielen M, et al. Safety and efficacy of a novel microneedle device for dose sparing intradermal influenza vaccination in healthy adults. Vaccine 2009;27(3):454-9
   PubMed Web of Science ®Google Scholar
• Mikszta JA, Dekker JPR, Harvey NG, et al. Microneedle-based intradermal delivery of the anthrax recombinant protective antigen vaccine. Infect Immun 2006;74(12):6806-10
   PubMed Web of Science ®Google Scholar
• Moon S, Wang Y, Edens C, et al. Dose sparing and enhanced immunogenicity of inactivated rotavirus vaccine administered by skin vaccination using a microneedle patch. Vaccine 2013;31(34):3396-402
   PubMed Web of Science ®Google Scholar
• Yin D, Liang W, Xing S, et al. Hepatitis B DNA vaccine-polycation nano-complexes enhancing immune response by percutaneous administration with microneedle. Biol Pharm Bull 2013;36(8):1283-91
   PubMed Web of Science ®Google Scholar
• Norman JJ, Arya JM, McClain MA, et al. Microneedle patches: usability and acceptability for self-vaccination against influenza. Vaccine 2014;32(16):1856-62
   PubMed Web of Science ®Google Scholar
• Kis EE, Winter G, Myschik J. Devices for intradermal vaccination. Vaccine 2012;30(3):523-38
   PubMed Web of Science ®Google Scholar
• Giudice EL, Campbell JD. Needle-free vaccine delivery. Adv Drug Deliv Rev 2006;58(1):68-89
   PubMed Web of Science ®Google Scholar
• Logomasini MA, Stout RR, Marcinkoski R. Jet injection devices for the needle-free administration of compounds, vaccines, and other agents. Int J Pharm Compd 2013;17(4):270-80
   PubMedGoogle Scholar
• Liu Y, Kendall MA. Optimization of a jet-propelled particle injection system for the uniform transdermal delivery of drug/vaccine. Biotechnol Bioeng 2007;97(5):1300-8
   PubMed Web of Science ®Google Scholar
• Liu J, Hogan NC, Hunter IW. Intradermal needle-free powdered drug injection by a helium-powered device. Conf Proc IEEE Eng Med Biol Soc 2012;2012:2068-71
   PubMedGoogle Scholar
• Millar JD, Roberto RR, Wulff H, et al. Smallpox vaccination by intradermal jet injection. I. Introduction, background and results of pilot studies. Bull World Health Organ 1969;41(6):749-60
   PubMed Web of Science ®Google Scholar
• Millar JD, Morris L, Macedo FA, et al. The introduction of jet injection mass vaccination into the national smallpox eradication program of Brazil. Trop Geogr Med 1971;23(1):89-101
   PubMedGoogle Scholar
• O’Hagan DT, Rappuoli R. Novel approaches to vaccine delivery. Pharm Res 2004;21(9):1519-30
   PubMed Web of Science ®Google Scholar
• Williams J, Fox-Leyva L, Christensen C, et al. Hepatitis A vaccine administration: comparison between jet-injector and needle injection. Vaccine 2000;18(18):1939-43
   PubMed Web of Science ®Google Scholar
• Fisch A, Cadilhac P, Vidor E, et al. Immunogenicity and safety of a new inactivated hepatitis A vaccine: a clinical trial with comparison of administration route. Vaccine 1996;14(12):1132-6
   PubMed Web of Science ®Google Scholar
• Jackson LA, Austin G, Chen RT, et al. Safety and immunogenicity of varying dosages of trivalent inactivated influenza vaccine administered by needle-free jet injectors. Vaccine 2001;19(32):4703-9
   PubMed Web of Science ®Google Scholar
• Aguiar JC, Hedstrom RC, Rogers WO, et al. Enhancement of the immune response in rabbits to a malaria DNA vaccine by immunization with a needle-free jet device. Vaccine 2001;20(1-2):275-80
   PubMed Web of Science ®Google Scholar
• Graham BS, Enama ME, Nason MC, et al. DNA vaccine delivered by a needle-free injection device improves potency of priming for antibody and CD8+ T-cell responses after rAd5 boost in a randomized clinical trial. PLoS One 2013;8(4):e59340
   PubMed Web of Science ®Google Scholar
• McAllister L, Anderson J, Werth K, et al. Needle-free jet injection for administration of influenza vaccine: a randomised non-inferiority trial. Lancet 2014;384(9944):674-81
   PubMed Web of Science ®Google Scholar
• Wesley RD, Lager KM. Evaluation of a recombinant human adenovirus-5 vaccine administered via needle-free device and intramuscular injection for vaccination of pigs against swine influenza virus. Am J Vet Res 2005;66(11):1943-7
   PubMed Web of Science ®Google Scholar
• Wang S, Zhang C, Zhang L, et al. The relative immunogenicity of DNA vaccines delivered by the intramuscular needle injection, electroporation and gene gun methods. Vaccine 2008;26(17):2100-10
   PubMed Web of Science ®Google Scholar
• Drape RJ, Macklin MD, Barr LJ, et al. Epidermal DNA vaccine for influenza is immunogenic in humans. Vaccine 2006;24(21):4475-81
   PubMed Web of Science ®Google Scholar
• Roy MJ, Wu MS, Barr LJ, et al. Induction of antigen-specific CD8+ T cells, T helper cells, and protective levels of antibody in humans by particle-mediated administration of a hepatitis B virus DNA vaccine. Vaccine 2000;19(7-8):764-78
   PubMed Web of Science ®Google Scholar
• Hogan ME, Kikuta A, Taddio A. A systematic review of measures for reducing injection pain during adult immunization. Vaccine 2010;28(6):1514-21
   PubMed Web of Science ®Google Scholar
• Epstein JE, Gorak EJ, Charoenvit Y, et al. Safety, tolerability, and lack of antibody responses after administration of a PfCSP DNA malaria vaccine via needle or needle-free jet injection, and comparison of intramuscular and combination intramuscular/intradermal routes. Hum Gene Ther 2002;13(13):1551-60
   PubMed Web of Science ®Google Scholar
• Naito S, Maeyama J, Mizukami T, et al. Transcutaneous immunization by merely prolonging the duration of antigen presence on the skin of mice induces a potent antigen-specific antibody response even in the absence of an adjuvant. Vaccine 2007;25(52):8762-70
   PubMed Web of Science ®Google Scholar
• Lee MY, Shin MC, Yang VC. Transcutaneous antigen delivery system. BMB Rep 2013;46(1):17-24
   PubMed Web of Science ®Google Scholar
• Matsuo K, Hirobe S, Okada N, Nakagawa S. Frontiers of transcutaneous vaccination systems: novel technologies and devices for vaccine delivery. Vaccine 2013;31(19):2403-15
   PubMed Web of Science ®Google Scholar
• Mittal A, Raber AS, Lehr CM, Hansen S. Particle based vaccine formulations for transcutaneous immunization. Hum Vaccin Immunother 2013;9(9):1950-5
   PubMed Web of Science ®Google Scholar
• Frolov VG, Seid RCJr, Odutayo O, et al. Transcutaneous delivery and thermostability of a dry trivalent inactivated influenza vaccine patch. Influenza Other Respir Viruses 2008;2(2):53-60
   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):6983-90
   PubMed Web of Science ®Google Scholar
• Ledet G, Pamujula S, Walker V, et al. Development and in vitro evaluation of a nanoemulsion for transcutaneous delivery. Drug Dev Ind Pharm 2014;40(3):370-9
   PubMed Web of Science ®Google Scholar
• Seid RCJr, Look JL, Ruiz C, et al. Transcutaneous immunization with Intercell’s vaccine delivery system. Vaccine 2012;30(29):4349-54
   PubMed Web of Science ®Google Scholar
• Sahdev P, Podaralla S, Kaushik RS, Perumal O. Calcium phosphate nanoparticles for transcutaneous vaccine delivery. J Biomed Nanotechnol 2013;9(1):132-41
   PubMed Web of Science ®Google Scholar
• Weiss R, Hessenberger M, Kitzmuller S, et al. Transcutaneous vaccination via laser microporation. J Control Release 2012;162(2):391-9
   PubMed Web of Science ®Google Scholar
• Unga J, Hashida M. Ultrasound induced cancer immunotherapy. Adv Drug Deliv Rev 2014;72:144-53
   PubMed Web of Science ®Google Scholar
• Tezel A, Paliwal S, Shen Z, Mitragotri S. Low-frequency ultrasound as a transcutaneous immunization adjuvant. Vaccine 2005;23(29):3800-7
   PubMed Web of Science ®Google Scholar
• Anandhakumar S, Raichur AM. Polyelectrolyte/silver nanocomposite multilayer films as multifunctional thin film platforms for remote activated protein and drug delivery. Acta Biomater 2013;9(11):8864-74
   PubMed Web of Science ®Google Scholar
• Un K, Kawakami S, Suzuki R, et al. Development of an ultrasound-responsive and mannose-modified gene carrier for DNA vaccine therapy. Biomaterials 2010;31(30):7813-26
   PubMed Web of Science ®Google Scholar
• Wahl M, Hermodsson S. Intradermal, subcutaneous or intramuscular administration of hepatitis B vaccine: side effects and antibody response. Scand J Infect Dis 1987;19(6):617-21
   PubMed Web of Science ®Google Scholar
• Heijtink RA, Knol RM, Schalm SW. Low-dose (2 micrograms) hepatitis B vaccination in medical students: comparable immunogenicity for intramuscular and intradermal routes. J Med Virol 1989;27(2):151-4
   PubMed Web of Science ®Google Scholar
• Fabrizi F, Dixit V, Magnini M, et al. Meta-analysis: intradermal vs. intramuscular vaccination against hepatitis B virus in patients with chronic kidney disease. Aliment Pharmacol Ther 2006;24(3):497-506
   PubMed Web of Science ®Google Scholar
• Ghabouli MJ, Sabouri AH, Shoeibi N, et al. High seroprotection rate induced by intradermal administration of a recombinant hepatitis B vaccine in young healthy adults: comparison with standard intramuscular vaccination. Eur J Epidemiol 2004;19(9):871-5
   PubMed Web of Science ®Google Scholar
• Rahman F, Dahmen A, Herzog-Hauff S, et al. Cellular and humoral immune responses induced by intradermal or intramuscular vaccination with the major hepatitis B surface antigen. Hepatology 2000;31(2):521-7
   PubMed Web of Science ®Google Scholar
• Nolwenn N, Bisceglia H, Rozieres A, et al. Nine microg intradermal influenza vaccine and 15 microg intramuscular influenza vaccine induce similar cellular and humoral immune responses in adults. Hum Vaccin Immunother 2014;10(9
   Google Scholar
• Song JY, Cheong HJ, Noh JY, et al. Long-term immunogenicity of the influenza vaccine at reduced intradermal and full intramuscular doses among healthy young adults. Clin Exp Vaccine Res 2013;2(2):115-19
   PubMedGoogle Scholar
• Chiu SS, Chan KH, Tu W, et al. Immunogenicity and safety of intradermal versus intramuscular route of influenza immunization in infants less than 6 months of age: a randomized controlled trial. Vaccine 2009;27(35):4834-9
   PubMed Web of Science ®Google Scholar
• Ansaldi F, Valle L, de Florentiis D, et al. Phase 4 randomized trial of intradermal low-antigen-content inactivated influenza vaccine versus standard-dose intramuscular vaccine in HIV-1-infected adults. Hum Vaccin Immunother 2012;8(8):1048-52
   PubMed Web of Science ®Google Scholar
• Kunzi V, Klap JM, Seiberling MK, et al. Immunogenicity and safety of low dose virosomal adjuvanted influenza vaccine administered intradermally compared to intramuscular full dose administration. Vaccine 2009;27(27):3561-7
   PubMed Web of Science ®Google Scholar
• Nelson EA, Lam HS, Choi KC, et al. A pilot randomized study to assess immunogenicity, reactogenicity, safety and tolerability of two human papillomavirus vaccines administered intramuscularly and intradermally to females aged 18-26 years. Vaccine 2013;31(34):3452-60
   PubMed Web of Science ®Google Scholar
• Kulkarni PS, Sapru A, D’Costa PM, et al. Safety and immunogenicity of a new purified vero cell rabies vaccine (PVRV) administered by intramuscular and intradermal routes in healthy volunteers. Vaccine 2013;31(24):2719-22
   PubMed Web of Science ®Google Scholar
• Laurent PE, Bourhy H, Fantino M, et al. Safety and efficacy of novel dermal and epidermal microneedle delivery systems for rabies vaccination in healthy adults. Vaccine 2010;28(36):5850-6
   PubMed Web of Science ®Google Scholar
• Cook IF, Barr I, Hartel G, et al. Reactogenicity and immunogenicity of an inactivated influenza vaccine administered by intramuscular or subcutaneous injection in elderly adults. Vaccine 2006;24(13):2395-402
   PubMed Web of Science ®Google Scholar
• Golekoh MC, Hu S, Norman AM, et al. Comparison of the immunogenicity of intramuscular versus subcutaneous administration of trivalent inactivated influenza vaccine in individuals with neuromuscular diseases. J Child Neurol 2013;28(5):596-601
   PubMed Web of Science ®Google Scholar
• Gillet Y, Habermehl P, Thomas S, et al. Immunogenicity and safety of concomitant administration of a measles, mumps and rubella vaccine (M-M-RvaxPro) and a varicella vaccine (VARIVAX) by intramuscular or subcutaneous routes at separate injection sites: a randomised clinical trial. BMC Med 2009;7:16
   PubMed Web of Science ®Google Scholar
• Ruben FL, Froeschle JE, Meschievitz C, et al. Choosing a route of administration for quadrivalent meningococcal polysaccharide vaccine: intramuscular versus subcutaneous. Clin Infect Dis 2001;32(1):170-2
   PubMed Web of Science ®Google Scholar
• Ozdemir R, Canpolat FE, Yurttutan S, et al. Effect of needle length for response to hepatitis B vaccine in macrosomic neonates: a prospective randomized study. Vaccine 2012;30(21):3155-8
   PubMed Web of Science ®Google Scholar
• Middleman AB, Anding R, Tung C. Effect of needle length when immunizing obese adolescents with hepatitis B vaccine. Pediatrics 2010;125(3):e508-12
   PubMed Web of Science ®Google Scholar