{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,17]],"date-time":"2026-01-17T23:40:01Z","timestamp":1768693201611,"version":"3.49.0"},"reference-count":62,"publisher":"Public Library of Science (PLoS)","issue":"8","license":[{"start":{"date-parts":[[2017,8,24]],"date-time":"2017-08-24T00:00:00Z","timestamp":1503532800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004211","name":"Oxford Martin School, University of Oxford","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100004211","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"DOI":"10.1371\/journal.pone.0183427","type":"journal-article","created":{"date-parts":[[2017,8,24]],"date-time":"2017-08-24T17:38:36Z","timestamp":1503596316000},"page":"e0183427","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":9,"title":["Alternative vaccine administration by powder injection: Needle-free dermal delivery of the glycoconjugate meningococcal group Y vaccine"],"prefix":"10.1371","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-4589-9286","authenticated-orcid":true,"given":"Nikolas T.","family":"Weissmueller","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Leanne","family":"Marsay","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Heiko A.","family":"Schiffter","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Robert C.","family":"Carlisle","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Christine S.","family":"Rollier","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Robert K.","family":"Prud\u2019homme","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Andrew J.","family":"Pollard","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2017,8,24]]},"reference":[{"key":"ref1","article-title":"Safety of Injections: Global Facts&Figures","year":"2004"},{"issue":"4","key":"ref2","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1179\/oeh.2004.10.4.451","article-title":"Preventing needlestick injuries among healthcare workers: A WHO-ICN collaboration","volume":"10","author":"SQ Wilburn","year":"2004","journal-title":"International Journal of Occupational and Environmental Health"},{"issue":"1","key":"ref3","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1038\/nm0103-99","article-title":"Can needle-free administration of vaccines become the norm in global immunization?","volume":"9","author":"MM Levine","year":"2003","journal-title":"Nature Medicine"},{"issue":"23","key":"ref4","doi-asserted-by":"crossref","first-page":"2697","DOI":"10.1016\/j.vaccine.2015.03.084","article-title":"Estimating the costs of the vaccine supply chain and service delivery for selected districts in Kenya and Tanzania","volume":"33","author":"M Mvundura","year":"2015","journal-title":"Vaccine"},{"issue":"7","key":"ref5","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1038\/nri3694","article-title":"From empiricism to rational design: a personal perspective of the evolution of vaccine development","volume":"14","author":"E De Gregorio","year":"2014","journal-title":"Nat Rev Immunol"},{"issue":"5","key":"ref6","doi-asserted-by":"crossref","first-page":"673","DOI":"10.1586\/erv.11.14","article-title":"Long-term protection after immunization with protein-polysaccharide conjugate vaccines in infancy","volume":"10","author":"G Blanchard-Rohner","year":"2011","journal-title":"Expert Rev Vaccines"},{"issue":"2","key":"ref7","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1111\/j.1365-2567.2004.01971.x","article-title":"Haemophilus influenzae type b conjugate vaccines","volume":"113","author":"DF Kelly","year":"2004","journal-title":"Immunology"},{"issue":"3","key":"ref8","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1038\/nri2494","article-title":"Maintaining protection against invasive bacteria with protein- polysaccharide conjugate vaccines","volume":"9","author":"AJ Pollard","year":"2009","journal-title":"Nature Reviews Immunology"},{"issue":"1","key":"ref9","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1186\/1478-7954-11-17","article-title":"Global epidemiology of invasive meningococcal disease","volume":"11","author":"RZ Jafri","year":"2013","journal-title":"Popul Health Metr"},{"issue":"2","key":"ref10","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1016\/j.ijpharm.2008.08.032","article-title":"Micro-scale devices for transdermal drug delivery","volume":"364","author":"A Arora","year":"2008","journal-title":"International Journal of Pharmaceutics"},{"issue":"2","key":"ref11","doi-asserted-by":"crossref","first-page":"192","DOI":"10.1038\/nbt928","article-title":"Discovery of transdermal penetration enhancers by high-throughput screening","volume":"22","author":"P Karande","year":"2004","journal-title":"Nat Biotechnol"},{"issue":"12","key":"ref12","doi-asserted-by":"crossref","first-page":"905","DOI":"10.1038\/nri1728","article-title":"Immunization without needles","volume":"5","author":"S Mitragotri","year":"2005","journal-title":"Nature Reviews Immunology"},{"issue":"10","key":"ref13","doi-asserted-by":"crossref","first-page":"1218","DOI":"10.1016\/j.addr.2008.03.006","article-title":"Low-frequency sonophoresis: current status and future prospects","volume":"60","author":"M Ogura","year":"2008","journal-title":"Adv Drug Deliv Rev"},{"issue":"7","key":"ref14","doi-asserted-by":"crossref","first-page":"1912","DOI":"10.1002\/jps.20104","article-title":"Influenza vaccine powder formulation development: Spray-freeze-drying and stability evaluation","volume":"93","author":"YF Maa","year":"2004","journal-title":"Journal of Pharmaceutical Sciences"},{"issue":"10","key":"ref15","doi-asserted-by":"crossref","first-page":"2122","DOI":"10.1002\/jps.10204","article-title":"Spray-freeze-drying for protein powder preparation: Particle characterization and a case study with trypsinogen stability","volume":"91","author":"C Sonner","year":"2002","journal-title":"Journal of Pharmaceutical Sciences"},{"issue":"4","key":"ref16","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1615\/CritRevTherDrugCarrierSyst.v16.i4.10","article-title":"Transdermal and transmucosal powdered drug delivery","volume":"16","author":"TL Burkoth","year":"1999","journal-title":"Critical Reviews in Therapeutic Drug Carrier Systems"},{"issue":"10","key":"ref17","doi-asserted-by":"crossref","first-page":"1187","DOI":"10.1038\/80538","article-title":"Epidermal immunization by a needle-free powder delivery technology: Immunogenicity of influenza vaccine and protection in mice","volume":"6","author":"D Chen","year":"2000","journal-title":"Nature Medicine"},{"issue":"11","key":"ref18","doi-asserted-by":"crossref","first-page":"1733","DOI":"10.1016\/j.jbiomech.2004.01.032","article-title":"Intradermal ballistic delivery of micro-particles into excised human skin for pharmaceutical applications","volume":"37","author":"M Kendall","year":"2004","journal-title":"Journal of Biomechanics"},{"issue":"3","key":"ref19","doi-asserted-by":"crossref","first-page":"390","DOI":"10.1016\/j.medengphy.2006.05.015","article-title":"Utilization of the venturi effect to introduce micro-particles for epidermal vaccination","volume":"29","author":"Y Liu","year":"2007","journal-title":"Medical Engineering and Physics"},{"issue":"1","key":"ref20","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1007\/s001930200126","article-title":"The delivery of particulate vaccines and drugs to human skin with a practical, hand-held shock tube-based system","volume":"12","author":"MA Kendall","year":"2002","journal-title":"Shock Waves"},{"issue":"5\u20136","key":"ref21","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1016\/S0147-9571(03)00021-3","article-title":"Powder and particle-mediated approaches for delivery of DNA and protein vaccines into the epidermis","volume":"26","author":"HJ Dean","year":"2003","journal-title":"Comparative Immunology, Microbiology and Infectious Diseases"},{"issue":"3","key":"ref22","doi-asserted-by":"crossref","first-page":"266","DOI":"10.1016\/j.jconrel.2010.09.018","article-title":"Advances in transcutaneous vaccine delivery: Do all ways lead to Rome?","volume":"148","author":"SM Bal","year":"2010","journal-title":"Journal of Controlled Release"},{"issue":"3","key":"ref23","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1038\/nri1310","article-title":"Immune surveillance in the skin: Mechanisms and clinical consequences","volume":"4","author":"TS Kupper","year":"2004","journal-title":"Nature Reviews Immunology"},{"issue":"6","key":"ref24","doi-asserted-by":"crossref","first-page":"687","DOI":"10.1586\/erv.13.48","article-title":"Intradermal powder immunization with protein-containing vaccines","volume":"12","author":"NT Weissmueller","year":"2013","journal-title":"Expert Rev Vaccines"},{"key":"ref25","first-page":"281","article-title":"Development and Manufacture of Protein Pharmaceuticals","author":"SL Nail","year":"2002"},{"key":"ref26","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1016\/j.ejpb.2004.10.002","article-title":"Effects of process variables on the powder yield of spray-dried trehalose on a laboratory spray-dryer","volume":"59","author":"M Maury","year":"2005","journal-title":"Euro J Pharm Biopharm"},{"issue":"SUPPL. 4","key":"ref27","doi-asserted-by":"crossref","first-page":"S483","DOI":"10.1098\/rsif.2010.0114.focus","article-title":"Spray-freeze-drying of nanosuspensions: The manufacture of insulin particles for needle-free ballistic powder delivery","volume":"7","author":"H Schiffter","year":"2010","journal-title":"Journal of the Royal Society Interface"},{"issue":"2","key":"ref28","doi-asserted-by":"crossref","first-page":"388","DOI":"10.1002\/jps.10059","article-title":"Protein spray freeze drying. 2. Effect of formulation variables on particle size and stability","volume":"91","author":"HR Costantino","year":"2002","journal-title":"Journal of Pharmaceutical Sciences"},{"issue":"11","key":"ref29","doi-asserted-by":"crossref","first-page":"1374","DOI":"10.1023\/A:1007570030368","article-title":"Protein spray-freeze drying. Effect of atomization conditions on particle size and stability","volume":"17","author":"HR Costantino","year":"2000","journal-title":"Pharmaceutical Research"},{"key":"ref30","first-page":"67","article-title":"Spray-freeze-drying in the manufacture of pharmaceuticals","volume":"12","author":"H Schiffter","year":"2007","journal-title":"Eur Pharm Rev"},{"issue":"9","key":"ref31","doi-asserted-by":"crossref","first-page":"2296","DOI":"10.1002\/jps.20861","article-title":"Dextran or hydroxyethyl starch in spray-freeze-dried trehalose\/mannitol microparticles intended as ballistic particulate carriers for proteins","volume":"96","author":"C Rochelle","year":"2007","journal-title":"J Pharm Sci"},{"issue":"1\u20132","key":"ref32","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1016\/j.virusres.2004.02.027","article-title":"Epidermal powder immunization: Cellular and molecular mechanisms for enhancing vaccine immunogenicity","volume":"103","author":"D Chen","year":"2004","journal-title":"Virus Research"},{"issue":"3","key":"ref33","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1586\/14760584.1.3.265","article-title":"Needle-free epidermal powder immunization","volume":"1","author":"D Chen","year":"2002","journal-title":"Expert Review of Vaccines"},{"issue":"3","key":"ref34","doi-asserted-by":"crossref","first-page":"739","DOI":"10.1111\/j.0022-202X.2004.22320.x","article-title":"Effects of relative humidity and ambient temperature on the ballistic delivery of micro-particles to excised porcine skin","volume":"122","author":"M Kendall","year":"2004","journal-title":"Journal of Investigative Dermatology"},{"issue":"7","key":"ref35","doi-asserted-by":"crossref","first-page":"969","DOI":"10.1023\/A:1024493719236","article-title":"Optimization of an alum-adsorbed vaccine powder formulation for epidermal powder immunization","volume":"20","author":"YF Maa","year":"2003","journal-title":"Pharmaceutical Research"},{"issue":"5","key":"ref36","doi-asserted-by":"crossref","first-page":"586","DOI":"10.1128\/CVI.00121-15","article-title":"Needle-Free Dermal Delivery of a Diphtheria Toxin CRM197 Mutant on Potassium-Doped Hydroxyapatite Microparticles","volume":"22","author":"NT Weissmueller","year":"2015","journal-title":"Clin Vaccine Immunol"},{"issue":"21\u201322","key":"ref37","doi-asserted-by":"crossref","first-page":"2830","DOI":"10.1016\/S0264-410X(03)00175-0","article-title":"Epidermal powder immunization of mice and monkeys with an influenza vaccine","volume":"21","author":"D Chen","year":"2003","journal-title":"Vaccine"},{"issue":"5","key":"ref38","doi-asserted-by":"crossref","first-page":"681","DOI":"10.1016\/j.vaccine.2004.06.041","article-title":"Epidermal powder immunization against influenza","volume":"23","author":"HJ Dean","year":"2004","journal-title":"Vaccine"},{"issue":"1","key":"ref39","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/S0169-409X(97)00506-1","article-title":"Preparation of peptide and protein powders for inhalation","volume":"26","author":"KA Johnson","year":"1997","journal-title":"Advanced Drug Delivery Reviews"},{"issue":"6","key":"ref40","doi-asserted-by":"crossref","first-page":"1475","DOI":"10.1128\/JCM.32.6.1475-1482.1994","article-title":"Multicenter comparison of Neisseria meningitidis serogroup C anti-capsular polysaccharide antibody levels measured by a standardized enzyme-linked immunosorbent assay","volume":"32","author":"LL Gheesling","year":"1994","journal-title":"J Clin Microbiol"},{"issue":"24","key":"ref41","doi-asserted-by":"crossref","first-page":"5093","DOI":"10.1016\/j.vaccine.2006.03.091","article-title":"Neisseria meningitidis group B correlates of protection and assay standardization\u2014international meeting report Emory University, Atlanta, Georgia, United States, 16\u201317 March 2005","volume":"24","author":"R Borrow","year":"2006","journal-title":"Vaccine"},{"issue":"2","key":"ref42","doi-asserted-by":"crossref","first-page":"99","DOI":"10.3109\/1547691X.2013.821564","article-title":"Immunogenicity of therapeutic proteins: influence of aggregation","volume":"11","author":"KD Ratanji","year":"2014","journal-title":"J Immunotoxicol"},{"issue":"1","key":"ref43","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/S0006-3495(04)74078-3","article-title":"Water accessibility, aggregation, and motional features of polysaccharide-protein conjugate vaccines","volume":"86","author":"F Berti","year":"2004","journal-title":"Biophys J"},{"key":"ref44","doi-asserted-by":"crossref","first-page":"20488","DOI":"10.1038\/srep20488","article-title":"Cross Reactive Material 197 glycoconjugate vaccines contain privileged conjugation sites","volume":"6","author":"U Moginger","year":"2016","journal-title":"Sci Rep"},{"issue":"7","key":"ref45","first-page":"1808","article-title":"Factors contributing to the immunogenicity of meningococcal conjugate vaccines","volume":"12","author":"M Broker","year":"2016","journal-title":"Hum Vaccin Immunother"},{"issue":"1\u20132","key":"ref46","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0378-5173(00)00423-3","article-title":"Lyophilization and development of solid protein pharmaceuticals","volume":"203","author":"W Wang","year":"2000","journal-title":"International Journal of Pharmaceutics"},{"issue":"1\u20132","key":"ref47","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.ijpharm.2004.11.014","article-title":"Protein aggregation and its inhibition in biopharmaceutics","volume":"289","author":"W Wang","year":"2005","journal-title":"International Journal of Pharmaceutics"},{"issue":"2","key":"ref48","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1021\/js970308x","article-title":"Spray-drying of air-liquid interface sensitive recombinant human growth hormone","volume":"87","author":"YF Maa","year":"1998","journal-title":"J Pharm Sci"},{"issue":"1","key":"ref49","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1021\/js9601896","article-title":"Characteristics and significance of the amorphous state in pharmaceutical systems","volume":"86","author":"BC Hancock","year":"1997","journal-title":"J Pharm Sci"},{"issue":"2","key":"ref50","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1023\/B:PHAM.0000016234.73023.75","article-title":"Design of freeze-drying processes for pharmaceuticals: practical advice","volume":"21","author":"X Tang","year":"2004","journal-title":"Pharm Res"},{"issue":"2","key":"ref51","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1016\/0963-9969(95)90798-F","article-title":"Volumetric shrinkage (collapse) in freeze-dried carbohydrates above their glass transition temperature","volume":"28","author":"G Levi","year":"1995","journal-title":"Food Research International"},{"issue":"7\u20138","key":"ref52","first-page":"716","article-title":"Assessment of the stability and immunogenicity of meningococcal oligosaccharide C-CRM197 conjugate vaccines","volume":"19","author":"MM Ho","year":"2000","journal-title":"Vaccine"},{"issue":"3","key":"ref53","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1097\/INF.0b013e31818e037d","article-title":"Immunogenicity and immune memory of a nonadjuvanted quadrivalent meningococcal glycoconjugate vaccine in infants","volume":"28","author":"KP Perrett","year":"2009","journal-title":"Pediatr Infect Dis J"},{"issue":"2","key":"ref54","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1001\/jama.2007.29-c","article-title":"Immunogenicity of a tetravalent meningococcal glycoconjugate vaccine in infants: a randomized controlled trial","volume":"299","author":"MD Snape","year":"2008","journal-title":"JAMA"},{"issue":"1","key":"ref55","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1111\/j.1574-695X.2000.tb01460.x","article-title":"Meningococcal serogroup C-specific IgG antibody responses and serum bactericidal titres in children following vaccination with a meningococcal A\/C polysaccharide vaccine","volume":"28","author":"R Borrow","year":"2000","journal-title":"FEMS Immunol Med Microbiol"},{"issue":"19","key":"ref56","doi-asserted-by":"crossref","first-page":"1499","DOI":"10.1001\/jama.1996.03530430043037","article-title":"Safety and immunogenicity of a serogroups A\/C Neisseria meningitidis oligosaccharide-protein conjugate vaccine in young children. A randomized controlled trial","volume":"275","author":"JM Lieberman","year":"1996","journal-title":"JAMA"},{"issue":"4","key":"ref57","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1128\/CDLI.5.4.479-485.1998","article-title":"A modified enzyme-linked immunosorbent assay for measurement of antibody responses to meningococcal C polysaccharide that correlate with bactericidal responses","volume":"5","author":"DM Granoff","year":"1998","journal-title":"Clin Diagn Lab Immunol"},{"issue":"36","key":"ref58","doi-asserted-by":"crossref","first-page":"4414","DOI":"10.1016\/j.vaccine.2015.07.019","article-title":"Serum bactericidal antibody assays\u2013The role of complement in infection and immunity","volume":"33","author":"E McIntosh","year":"2015","journal-title":"Vaccine"},{"issue":"11","key":"ref59","doi-asserted-by":"crossref","first-page":"5450","DOI":"10.1128\/IAI.66.11.5450-5456.1998","article-title":"Murine immune responses to Neisseria meningitidis group C capsular polysaccharide and a thymus-dependent toxoid conjugate vaccine","volume":"66","author":"LJ Rubinstein","year":"1998","journal-title":"Infect Immun"},{"issue":"35","key":"ref60","doi-asserted-by":"crossref","first-page":"4834","DOI":"10.1016\/j.vaccine.2009.05.066","article-title":"Immunogenicity and safety of intradermal versus intramuscular route of influenza immunization in infants less than 6 months of age: a randomized controlled trial","volume":"27","author":"SS Chiu","year":"2009","journal-title":"Vaccine"},{"issue":"6","key":"ref61","doi-asserted-by":"crossref","first-page":"617","DOI":"10.3109\/00365548709117195","article-title":"Intradermal, subcutaneous or intramuscular administration of hepatitis B vaccine: side effects and antibody response","volume":"19","author":"M Wahl","year":"1987","journal-title":"Scand J Infect Dis"},{"key":"ref62","first-page":"1","article-title":"Effect of vaccine administration modality on immunogenicity and efficacy","author":"L Zhang","year":"2015","journal-title":"Expert Rev Vaccines"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pone.0183427","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,10,16]],"date-time":"2020-10-16T06:06:03Z","timestamp":1602828363000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0183427"}},"subtitle":[],"editor":[{"given":"Eliane N.","family":"Miyaji","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2017,8,24]]},"references-count":62,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2017,8,24]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0183427","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,8,24]]}}}