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Human Vaccines & Immunotherapeutics Volume 12, 2016 - Issue 7
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Review

Factors contributing to the immunogenicity of meningococcal conjugate vaccines

Michael BrökerGSK Vaccines GmbH, Marburg, GermanyCorrespondence[email protected]
,
Francesco BertiGSK Vaccines, Siena, Italy
&
Paolo CostantinoGSK Vaccines, Siena, Italy
Pages 1808-1824 | Received 03 Dec 2015, Accepted 08 Feb 2016, Published online: 26 Apr 2016

References

  • Rosenstein NE, Perkins BA, Stephens DS, Popovic T, Hughes JM. Meningococcal disease. N Engl J Med 2001; 344:1378-88; PMID:11333996; http://dx.doi.org/10.1056/NEJM200105033441807
  • Harrison OB, Claus H, Jiang Y, Bennett JS, Bratcher HB, Jolley KA, Corton C, Care R, Poolman JT, Zollinger WD, et al. Description and nomenclature of Neisseria meningitidis capsule locus. Emerg Infect Dis 2013; 19:566-73; PMID:23628376; http://dx.doi.org/10.3201/eid1904.111799
  • Schneerson R, Barrera O, Sutton A, Robbins JB. Preparation, characterization, and immunogenicity of Haemophilus influenzae type b polysaccharide-protein conjugates. J Exp Med 1980; 152:361-76; PMID:6967514; http://dx.doi.org/10.1084/jem.152.2.361
  • Vella M, Pace D. Glycoconjugate vaccines: an update. Expert Opin Biol Ther 2015; 15:529-46; PMID:25496172; http://dx.doi.org/10.1517/14712598.2015.993375
  • Shinefield HR. Overview of the development and current use of CRM197 conjugate vaccines for pediatric use. Vaccine 2010; 28:4335-9; PMID:20452430; http://dx.doi.org/10.1016/j.vaccine.2010.04.072
  • Giannini G, Rappuoli R, Ratti G. The amino-acid sequence of 2 non-toxic mutants of diphtheria toxin: CRM45 and CRM197. Nucleic Acids Res 1984; 12:4063-9; PMID:6427753; http://dx.doi.org/10.1093/nar/12.10.4063
  • Bröker M, Costantino P, DeTora L, McIntosh ED, Rappuoli R. Biochemical and biological characteristics of cross-reacting material 197 (CRM197), a non-toxic mutant of diphtheria toxin: use as a conjugation protein in vaccines and other potential clinical applications. Biologicals 2011, 39:195-204; PMID:21715186; http://dx.doi.org/10.1016/j.biologicals.2011.05.004
  • Malito E, Bursulaya B, Chen C, Lo Surdo P, Picchianti M, Balducci E, Biancucci M, Brock A, Berti F, Bottomley MJ, et al. Structural basis for lack of toxicity of the diphtheria toxin mutant CRM197. Proc Natl Acad Sci USA 2013; 109:5229-34; PMID:22431623; http://dx.doi.org/10.1073/pnas.1201964109
  • Rappuoli R. New generation vaccines. Edited by Woodrow GC and Levine MM. New York: Marcel Dekker, Inc., 1990. New and improved vaccines against diphtheria and tetanus toxin; p. 251-68
  • Snape MD, Pollard AJ. Meningococcal polysaccharide-protein conjugate vaccines. Lancet Infect Dis 2005; 5:21-30; PMID:15620558; http://dx.doi.org/10.1016/S1473-3099(04)01251-4
  • Trotter CL, Maiden MC. Meningococcal vaccines and herd immunity: lessons learned from serogroup C conjugate vaccination programs. Expert Rev Vaccines 2009; 8:851-61; PMID:19538112; http://dx.doi.org/10.1586/erv.09.48
  • Costantino P, Viti S, Podda A, Velmonte MA, Nencioni L, Rappuoli R. Development and a phase 1 clinical testing of a conjugate vaccine against meningococcus A and C. Vaccine 1992; 10:691-8; PMID:1523880; http://dx.doi.org/10.1016/0264-410X(92)90091-W
  • Twumasi PA Jr, Kumah S, Leach A, O'Dempsey TJ, Ceesay SJ, Todd J, Broome CV, Carlone GM, Pais LB, Holder PK, et al. A trial of a group A plus group C meningococcal polysaccharide-protein conjugate vaccine in African infants. J Infect Dis 1995; 171:632-8; PMID:7876610; http://dx.doi.org/10.1093/infdis/171.3.632
  • Campagne G, Garba A, Fabre P, Schuchat A, Ryall R, Boulanger D, Bybel M, Carlone G, Briantais P, Ivanoff B, et al. Safety and immunogenicity of three doses of a Neisseria meningitidis A + C diphtheria conjugate vaccine in infants from Niger. Pediatr Infect Dis J 2000; 19:144-50; PMID:10694002; http://dx.doi.org/10.1097/00006454-200002000-00013
  • Chippaux JP, Garba A, Ethevenaux C, Campagne G, de Chabalier F, Djibo S, Nicolas P, Ali H, Charrondière M, Ryall R, et al. Immunogenicity, safety, and memory of different schedules of Neisseria meningitidis A/C-diphtheria toxoid conjugate vaccine in infants in Niger. Vaccine 2004; 22:3303-11; PMID:15308353; http://dx.doi.org/10.1016/j.vaccine.2004.02.028
  • Wu LJ, Zhao J, Han JJ, Sun FF, Jia Z, Sun JZ, Xiao ZR, Dong JC, Zhang P. Preparation of groups A and C meningococcal conjugate vaccine. Chin J Biologicals 2012; 11:1405-9
  • Li QM, Ma ZJ, Zhang J, Jin YQ, Chen S, Zhang XF, Liu MY. The immunological effect of group A and C meningococcal conjugate vaccine with double protein carriers. Chin J Microbiol Immunol 2011; 2:146-9
  • McVernon J, Nolan T, Richmond P, Reynolds G, Nissen M, Lambert SB, Marshall H, Papa T, Rehm C. A randomized trial to assess safety and immunogenicity of alternative formulations of a quadrivalent meningococcal (A, C, Y, and W-135) tetanus protein conjugate vaccine in toddlers. Pediatr Infect Dis J 2012; 31: e15-23; PMID:22094636; http://dx.doi.org/10.1097/INF.0b013e31823e1e34
  • Micoli F, Romano MR, Tontoni M, Cappelletti E, Gavini M, Proietti D, Rondini S. Swennen E, Santini L, Filippini S, et al. Development of a glycoconjugate vaccine to prevent meningitis in Africa caused by meningococcal serogroup X. Proc Natl Acad Sci USA 2013; 110:19077-82; PMID:24191022; http://dx.doi.org/10.1073/pnas.1314476110
  • Chilukuri SR, Reddy P, Avalaskar N, Mallya A, Pisal S, Dhere RM. Process development and immunogenicity studies on a serogroup “X” Meningococcal polysaccharide conjugate vaccine. Biologicals 2014; 42:160-8; PMID:24411634; http://dx.doi.org/10.1016/j.biologicals.2013.12.001
  • LaForce FM. (PATH, Washington, DC). Meningococcal vaccine and other product development. Project 1 Nov 2010-31 Mar 2015. London: Department for International Development. Research and Evidence Division (Human Development Team). DFID Research4Development Project Record. Available from: http://r4d.dfid.gov.uk/Project/60879/. [Accessed 21 July 2015]
  • Wang C, Ye Q, Li FX. Expression of nontoxic diphtheria toxin mutant CRM197 as a carrier protein. Chin J Biologicals 2008; 8:687-91
  • Lockyer K, Gao F, Derrick JP, Bolgiano B. Structural correlates of carrier protein recognition in tetanus toxoid-conjugated bacterial polysaccharide vaccines. Vaccine 2015; 33:1345-52; PMID:25640334; http://dx.doi.org/10.1016/j.vaccine.2015.01.046
  • Frech C, Hilbert AK, Hartmann G, Mayer K, Sauer T, Bolgiano B. Physicochemical analysis of purified diphtheria toxoids: is toxoided then purified the same as purified then toxoided? Dev Biol (Basel) 2000; 103:205-15; PMID:11214238
  • United States Pharmacopeia and National Formulary (USP 38-NF 33). Vol. One. Rockville, MD: United States Pharmacopeia Convention, 2015. Vaccines for Human Use – Polysaccharide and Glycoconjugate Vaccines; p. 1518-34
  • Knuf M, Kieninger-Baum D, Habermehl P, Muttonen P, Maurer H, Vink P, Poolman J, Boutriau D. A dose-range study assessing immunogenicity and safety of one dose of a new candidate meningococcal serogroups A, C, W-135, Y tetanus toxoid conjugate (MenACWY-TT) vaccine administered in the second year of life and in young children. Vaccine 2010; 28:744-53; PMID:19887137; http://dx.doi.org/10.1016/j.vaccine.2009.10.064
  • Steens A, Mollema L, Berbeers GAM, van Gageldonk PG, van der Klis FR, de Melker HE. High tetanus antitoxin antibody concentrations in the Netherlands: a seroepidemiological study. Vaccine 2010; 28:7803-9; PMID:20875496; http://dx.doi.org/10.1016/j.vaccine.2010.09.036
  • Burrage M, Robinson A, Borrow R, Andrews N, Southern J, Findlow J, Martin S, Thornton C, Goldblatt D, Corbel M, et al. Effect of vaccination with carrier protein on response to meningococcal C conjugate vaccines and value of different immunoassays as predictors of protection. Infect Immun 2002; 70:4946-54; PMID:12183540; http://dx.doi.org/10.1128/IAI.70.9.4946-4954.2002
  • Gasparini R, Johnston W, Conversano M, Garscadden A, Alexanderian D, Giglioli N, Percell S, Han L, Smolenov I. Immunogenicity and safety of combined tetanus, reduced diphtheria, acellular pertussis vaccine when co-administered with quadrivalent meningococcal conjugate and human papillomavirus vaccines in healthy adolescents. J Vaccines Vaccin 2014; 5:3
  • Dbaibo G, El-Ayoubi N, Ghanem S, Hajar F, Bianco V, Miller JM, Mesaros N. Immunogenicity and safety of a quadrivalent meningococcal serogroups A, C, W-135 and Y tetanus toxoid conjugate vaccine (MenACWY-TT) administered to adults aged 56 Years and older: result of an open-label, randomized, controlled trial. Drugs Aging 2013; 30:309-19; PMID:23494214; http://dx.doi.org/10.1007/s40266-013-0065-0
  • Dagan R, Poolman J, Siegrist CA. Glycoconjugate vaccines and immune interference: A review. Vaccine 2010; 28:5513-23; PMID:20600514; http://dx.doi.org/10.1016/j.vaccine.2010.06.026
  • Basta NE, Ng S, Berthe A, Bai X, Findlow H, Almond R, Borrow R, Sow S. Meningococcal serogroup A and tetanus immunity two years after MenAfriVac™ introduction in Mali. Int J Infect Dis 2014; 21(Suppl 1):435; http://dx.doi.org/10.1016/j.ijid.2014.03.1317
  • Borrow R, Tang Y, Yakubu A, Kulkarni PS, LaForce FM. MenAfriVac as an antitetanus vaccine. Clin Infect Dis 2015; 61 Suppl 5: S570-7; PMID:26553690; http://dx.doi.org/10.1093/cid/civ512
  • Bröker M. Potential protective immunogenicity of tetanus toxoid, diphtheria toxoid and Cross Reacting Material 197 (CRM197) when used as carrier proteins in glycoconjugates. Hum Vaccin Immunother 2016;12(3):664-67; PMID:26327602; http://dx.doi.org/10.1080/21645515.2015.1086048.
  • Wu Y, Gao Y, Zhu B, Zhou H, Shi Z, Wang J, Wang H, Shao Z. Antitoxins for diphtheria and tetanus decline more slowly after vaccination with DTwP than with DTaP: a study in a Chinese population. Vaccine 2014; 32:2570-3; PMID:24681275; http://dx.doi.org/10.1016/j.vaccine.2014.03.052
  • Pobre K, Tashani M, Ridda I, Rashid H, Wong M, Booy R. Carrier priming or suppression: understanding carrier priming enhancement of anti-polysaccharide antibody response to conjugate vaccines. Vaccine 2014; 32:1423-30.; PMID:24492014; http://dx.doi.org/10.1016/j.vaccine.2014.01.047
  • Peeters JM, Hazendonk TG, Beuvery EC, Tesser GI. Comparison of four bifunctional reagents for coupling peptides to proteins and the effect of the three moieties on the immunogenicity of the conjugates. J Immunol Methods 1989; 120:133-43; PMID:2499636; http://dx.doi.org/10.1016/0022-1759(89)90298-6
  • Phalipon A, Tanguy M, Grandjean C, Guerreiro C, Cohen D, Sansonetti P, Mulard LA. A synthetic carbohydrate-protein conjugate vaccine candidate against Shigella flexneri 2a infection. J Immunol 2009;182:2241-7; PMID:19201878; http://dx.doi.org/10.4049/jimmunol.0803141
  • Buskas T, Li Y, Boons GJ. The immunogenicity of the tumor-associated antigen Lewisy may be suppressed by a bifunctional cross-linker required for coupling to a carrier protein. Chemistry 2004; 10:3517-24; PMID:15252797; http://dx.doi.org/10.1002/chem.200400074
  • Ryall RP, inventor; Sanofi Pasteur, Inc., assignee. Multivalent meningococcal polysaccharide-protein conjugate vaccine. US8741314 B2. 2014 Jun 3
  • Huang Q, Li D, Kang A, An W, Fan B, Ma X, Su Z, Hu T. PEG as a spacer arm markedly increases the immunogenicity of meningococcal group Y polysaccharide conjugate vaccine. J Control Release 2013; 172:382-9; PMID:23511718; http://dx.doi.org/10.1016/j.jconrel.2013.03.008
  • Østergaard L, Lebacq E, Poolman J, Maechler G, Boutriau D. Immunogenicity, reactogenicity and persistence of meningococcal A, C, W-135 and Y-tetanus toxoid candidate conjugate (MenACWY-TT) vaccine formulations in adolescents age 15-25 years. Vaccine 2009; 27:161-8; PMID:18834910; http://dx.doi.org/10.1016/j.vaccine.2008.08.075
  • Lee CH, Kuo WC, Beri S, Kapre S, Joshi JS, Bouveret N, LaForce FM, Frasch CE. Preparation and characterization of an immunogenic meningococcal group A conjugate vaccine for use in Africa. Vaccine 2009; 27:726-32; PMID:19063929; http://dx.doi.org/10.1016/j.vaccine.2008.11.065
  • Frasch CE, Preziosi MP, LaForce FM. Development of a group A meningococcal conjugate vaccine, MenAfriVac™. Hum Vaccin Immunother 2012; 8:715-24; PMID:22495119; http://dx.doi.org/10.4161/hv.19619
  • Fiebig T, Berti F, Freiberger F, Pinto V, Claus H, Romano MR, Proietti D, Brogioni B, Stummeyer K, Berger M, et al. Functional expression of the capsule polymerase of Neisseria meningitidis serogroup X: a new perspective for vaccine development. Glycobiology 2014; 24:150-8; PMID:24259400; http://dx.doi.org/10.1093/glycob/cwt102
  • Egan W, Schneerson R, Werner KE, Zon G. Structural studies and chemistry of bacterial capsular polysaccharides. Investigations of phosphodiester-linked capsular polysaccharides isolated from Haemophilus influenzae types a, b, c, and f: NMR spectroscopic identification and chemical modification of end groups and the nature of base-catalyzed hydrolytic depolymerization. J Am Chem Soc 1982; 104:2898-910; http://dx.doi.org/10.1021/ja00374a033
  • Sturgess AW, Rush K, Charbonneau RJ, Lee JI, West DJ, Sitrin RD, Hennessy JP Jr. Haemophilus influenzae type b conjugate vaccine stability: catalytic depolymerization of PRP in the presence of aluminum hydroxide. Vaccine 1999; 17:1169-78; PMID:10195629; http://dx.doi.org/10.1016/S0264-410X(98)00337-5
  • Foschiatti M, Hearshaw M, Cescutti P, Ravenscroft N, Rizzo R. Conformational studies of the capsular polysaccharide produced by Neisseria meningitidis group A. Carbohydr Res 2009; 344:940-3; PMID:19306991; http://dx.doi.org/10.1016/j.carres.2009.02.027
  • Jódar L, Griffiths E, Feavers I. Scientific challenges for the quality control and production of group C meningococcal conjugate vaccines. Vaccine 2004; 22:1047-53; PMID:15161082; http://dx.doi.org/10.1016/j.vaccine.2003.08.040
  • Rana R, Dalal J, Singh D, Kumar N, Hanif S, Joshi N, Chhikara MK. Development and characterization of Haemophilus influenzae type b conjugate vaccine prepared using different polysaccharide chain lengths. Vaccine 2015; 33:2646-54; PMID:25907408; http://dx.doi.org/10.1016/j.vaccine.2015.04.031
  • Wang CH, Li ST, Lin TL, Cheng YY, Sun TH, Wang JT, Cheng TJ, Mong KK, Wong CH, Wu CY. Synthesis of Neisseria meningitidis serogroup W-135 capsular oligosaccharides for immunogenicity comparison and vaccine development. Angew Chem Int Ed Engl 2013; 52:9157-61; PMID:23843313; http://dx.doi.org/10.1002/anie.201302540
  • Liao G, Zhou Z, Guo Z. Synthesis and immunological study of α-2,9-oligosialic acid conjugates as anti-group C meningitis vaccines. Chem Commun (Camb) 2015; 51:9647-50; PMID:25973942; http://dx.doi.org/10.1039/C5CC01794G
  • Morelli l, Cancogni D, Tontini M, Nilo A, Filippini S, Costantino P, Romano MR, Berti F, Adamo R, Lay L. Synthesis and immunological evaluation of protein conjugates of Neisseria meningitidis X capsular polysaccharide fragments. Beilstein J Org Chem 2014; 10:2367-76; PMID:25383107; http://dx.doi.org/10.3762/bjoc.10.247
  • Cai X, Lei QP, Lamb DH, Shannon A, Jacoby J, Kruk J, Kensinger RD, Ryall R, Zablackis E, Cash P. LC/MS characterization of meningococcal depolymerized polysaccharide group C reducing endgroup and internal repeating unit. Anal Chem 2004; 76:7387-90; PMID:15595884; http://dx.doi.org/10.1021/ac0491760
  • Anderson PW, Pichichero ME, Stein EC, Porcelli S, Betts RF, Connuck DM, Korones D, Insel RA, Zahradnik JM, Eby R. Effect of oligosaccharide chain length, exposed terminal group, and hapten loading on the antibody response of human adults and infants to vaccines consisting of Haemophilus influenzae type b capsular antigen uniterminally coupled to the diphtheria protein CRM197. J Immunol 1989; 142:2464-8; PMID:2784464
  • Bröker M, Dull PM, Rappuoli R, Costantino P. Chemistry of a new investigational quadrivalent meningococcal conjugate vaccine that is immunogenic at all ages. Vaccine 2009; 27:5574-80; PMID:19619500; http://dx.doi.org/10.1016/j.vaccine.2009.07.036
  • Frasch CE. Preparation of bacterial polysaccharide-protein conjugates: analytical and manufacturing challenges. Vaccine 2009; 27:6468-70; PMID:19555714; http://dx.doi.org/10.1016/j.vaccine.2009.06.013
  • Frasch CE, Kapre SV, Lee CH, Préaud JM. Technical development of a new meningococcal vaccine. Clin Infect Dis 2015; 61 Suppl 5: S404-9; PMID:26553667; http://dx.doi.org/10.1093/cid/civ595
  • Claus H, Borrow R, Achtman M, Morelli G, Kantelberg C, Longworth E, Frosch M, Vogel U. Genetics of capsule O-acetylation in serogroup C, W-135 and Y meningococci. Mol Microbiol 2004; 51:227-39; PMID:14651624; http://dx.doi.org/10.1046/j.1365-2958.2003.03819.x
  • Borrow R, Longworth E, Gray SJ, Kaczmarski EB. Prevalence of de-O-acetylated serogroup C meningococci before the introduction of meningococcal serogroup C conjugate vaccines in the United Kingdom. FEMS Immunol Med Microbiol 2000; 28:189-91; PMID:10865169; http://dx.doi.org/10.1111/j.1574-695X.2000.tb01475.x
  • Michon F, Huang CH, Farley EK, Hronowski L, Di J, Fusco PC. Structure activity studies on group C meningococcal polysaccharide-protein conjugate vaccines: effect of O-acetylation on the nature of the protective epitope. Dev Biol (Basel) 2000; 103:151-160
  • Berry DS, Lynn F, Lee CH, Frasch CE, Bash MC. Effect of O acetylation of Neisseria meningitidis serogroup A capsular polysaccharide on development of functional immune responses. Infect Immun 2002; 70:3707-13; PMID:12065513; http://dx.doi.org/10.1128/IAI.70.7.3707-3713.2002
  • Lupisan S, Limkittikul K, Sosa N, Chanthavanich P, Bianco V, Baine Y, Van der Wielen M, Miller JM. Meningococcal polysaccharide A O-acetylation levels do not impact the immunogenicity of the quadrivalent meningococcal tetanus toxoid conjugate vaccine: results from a randomized, controlled phase III study of healthy adults aged 18 to 25 years. Clin Vaccine Immunol 2013; 20:1499-507; PMID:23885033; http://dx.doi.org/10.1128/CVI.00162-13
  • Longworth E, Fernsten P, Mininni TL, Vogel U, Claus H, Gray S, Kaczmarski E, Borrow R. O-Acetylation status of the capsular polysaccharides of serogroup Y and W meningococci isolated in the UK. FEMS Immunol Med Microbiol 2002; 32:119-23; PMID:11821233; http://dx.doi.org/10.1111/j.1574-695X.2002.tb00543.x
  • Taha MK, Achtman M, Alonso JM, Greenwood B, Ramsey M, Fox A, Gray S, Kaczmarski E. Serogroup W135 meningococcal disease in Hajj pilgrims. Lancet 2000; 356:2159; PMID:11191548; http://dx.doi.org/10.1016/S0140-6736(00)03502-9
  • Fusco PC, Farley EK, Huang CH, Moore S, Michon F. Protective meningococcal capsular polysaccharide epitopes and the role of O-acetylation. Clin Vaccine Immunol 2007; 14:577-84; PMID:17376859; http://dx.doi.org/10.1128/CVI.00009-07
  • Giardini PC, Longworth E, Evans-Johnson RE, Bessette ML, Zhang H, Borrow R, Madore D, Fernsten P. Analysis of human serum immunoglobulin G against O-acetyl-positive and O-acetyl-negative serogroup W135 meningococcal capsular polysaccharide. Clin Diagn Lab Immunol 2005; 12:586-92; PMID:15879019
  • Jin Z, Bohach GA, Shiloach J, Norris Se, Freedberg DI, Deobald C, Coxon B, Robbins JB, Schneerson R. Conjugates of group A and W135 capsular polysaccharides of Neisseria meningitidis bound to recombinant Staphylococcus aureus enterotoxin C1: preparation, physicochemical characterization, and immunological properties in mice. Infect Immun 2005; 73:7887-93; PMID:16299279; http://dx.doi.org/10.1128/IAI.73.12.7887-7893.2005
  • Gudlavalleti SK, Lee CH, Norris SE, Paul-Satyaseela M, Vann WF, Frasch CE. Comparison of Neisseria meningitidis serogroup W135 polysaccharide-tetanus toxoid conjugate vaccines made by periodate activation of O-acetylated, non-O-acetylated and chemically de-O-acetylated polysaccharide. Vaccine 2007; 46:7972-80; PMID:17936445; http://dx.doi.org/10.1016/j.vaccine.2007.06.018
  • Reed SG, Orr MT, Fox CB. Key roles of adjuvants in modern vaccines. Nat Med 2013, 19:1597-608; PMID: 24309663; http://dx.doi.org/10.1038/nm.3409
  • Ho MM, Bolgiano B, Corbel MJ. Assessment of the stability and immunogenicity of meningococcal oligosaccharide C-CRM197 conjugate vaccines. Vaccine 2000; 19:716-25; PMID:11115692; http://dx.doi.org/10.1016/S0264-410X(00)00261-9
  • Otto RBD, Burkin K, Erum Amir S, Crane DT, Bolgiano B. Patterns of binding of aluminium-containing adjuvants to Haemophilus influenzae type b and meningococcal group C conjugate vaccines and components. Biological 2015; PMID:26194164; http://dx.doi.org/10.1016/j.biologicals2015.06.008
  • Schlegl R, Weber M, Wruss J, Low D, Queen K, Stilwell S, Lindblad EB, Möhlen M. Influence of elemental impurities in aluminium hydroxide adjuvant on the stability of inactivated Japanese Encephalitis vaccine, IXIARO®. Vaccine 2015; 33:5989-96; PMID: 26095510; http://dx.doi.org/10.1016/j.vaccine.2015.05.103.
  • Jackson LA, Jacobson RM, Reisinger KS, Anemona A, Danzig LE, Dull PM. A randomized trial to determine the tolerability and immunogenicity of a quadrivalent meningococcal glycoconjugate vaccine in healthy adolescents. Pediatr Infect Dis J 2009; 28:86-91; PMID:19116603; http://dx.doi.org/10.1097/INF.0b013e31818a0237
  • O'Hagan DT, Rappuoli R, De Gregorio E, Tsai T, Del Giudice G. MF59 adjuvant: the best insurance against influenza strain diversity. Expert Rev Vaccines 2011; 10:447-62; PMID:21506643; http://dx.doi.org/10.1586/erv.11.23
  • Granoff DM, McHugh YE, Raff HV, Mokatrin AS, Van Nest GA. MF59 adjuvant enhances antibody responses of infant baboons immunized with Haemophilus influenzae type b and Neisseria meningitidis group C oligosaccharide-CRM197 conjugate vaccine. Infect Immun 1997; 65:1710-15; PMID:9125551
  • Qiao W, Ji S, Zhao Y, Hu T. Conjugation of β-glucan markedly increase the immunogenicity of meningococcal group Y polysaccharide conjugate vaccine. Vaccine 2015; 33:2066-72; PMID:25728319; http://dx.doi.org/10.1016/j.vaccine.2015.02.045
  • Ugozzoli M, Mariani M, Del Giudice G, Soenawan E, O'Hagan DT. Combinations of protein polysaccharide conjugate vaccines for intranasal immunization. J Infect Dis 2002; 186:1358-61; PMID:12402209; http://dx.doi.org/10.1086/344320
  • Baudner BC, Morandi M, Giuliani MM, Verhoef JC, Junginger HE, Costantino P, Rappuoli R, Del Giudice G. Modulation of immune response to group C meningococcal conjugate vaccine given intranasally to mice together with the LTK63 mucosal adjuvant and the trimethyl chitosan delivery system. J Infect Dis 2004; 189:828-32; PMID:14976599; http://dx.doi.org/10.1086/381708
  • Brynjolfsson SF, Bjarnarson SP, Mori E, Del Giudice G, Jonsdottir I. Concomitant administration of Mycobacterium bovis BCG with the meningococcal C conjugate vaccine to neonatal mice enhances antibody response and protective efficacy. Clin Vaccine Immunol 2011; 18:1936-42; PMID:21900528; http://dx.doi.org/10.1128/CVI.05247-11
  • Lee SM, Donaldson C. Formulation studies of an adsorbed conjugate vaccine. How a thorough formulation study ensured the development of a stable and effective vaccine. BioPharm International 2008; 21(Suppl 10):31-5. Available from: http://www.biopharminternational.com/formulation-studies-adsorbed-conjugate-vaccine
  • Geier DA, King PG, Hooker BS, Dórea JG, Kern JK, Sykes LK, Geier MR. Thimerosal: clinical, epidemiologic and biochemical studies. Clin Chim Acta 2015; 444:212-20; PMID:25708367; http://dx.doi.org/10.1016/j.cca.2015.02.030
  • Agrawal A, Kaushal P, Agrawal S, Gollapudi S, Gupta S. Thimerosal induces TH2 responses via influencing cytokine secretion by human dendritic cells. J Leukoc Biol 2007; 81:474-82. doi:10.1189/jlb.0706467; PMID:17079650; http://dx.doi.org/10.1189/jlb.0706467
  • Sawyer LA, McInnis J, Patel A, Horne AD, Albrecht P. Deleterious effect of thimerosal on the potency of inactivated poliovirus vaccine. Vaccine 1994; 12:851-6; PMID:7526574; http://dx.doi.org/10.1016/0264-410X(94)90296-8
  • Harmsen MM, Fijten HP, Westra DF, Coco-Martin JM. Effect of thiomersal on dissociation of intact (146S) foot-and-mouth disease virions into 12S particles as assessed by novel ELISAs specific for either 146S or 12S particles. Vaccine 2011; 29:2682-90; PMID:21316500; http://dx.doi.org/10.1016/j.vaccine.2011.01.069
  • Borrow R, Findlow J. Prevention of meningococcal serogroup C disease by NeisVac-C. Expert Rev Vaccines 2009; 8:265-79; PMID:19249967; http://dx.doi.org/10.1586/14760584.8.3.265
  • Findlow H, Borrow R, Andrews N, Waight P, Sheasby E, Matheson M, England A, Goldblatt D, Ashton L, Findlow J, Miller E. Immunogenicity of a single dose of meningococcal group C conjugate vaccine given at 3 months of age to healthy infants in the United Kingdom. Pediatr Infect Dis J 2012; 31:616-22; PMID:22333698; http://dx.doi.org/10.1097/INF.0b013e31824f34e6
  • JCVI statement on the use of meningococcal C vaccines in the routine childhood immunization programme, 29 January 2012. Available from: http://webarchive.nationalarchives.gov.uk/20130107105354/http:/www.dh.gov.uk/prod_consum_dh/groups/dh_digitalassets/@dh/@ab/documents/digitalasset/dh_132443.pdf. [Accessed 6 July 2015]
  • Knuf M, Romain O, Kindler K, Walther U, Tran PM, Pankow-Culot H, Fischbach T, Kieninger-Baum D, Bianco V, Baine Y, et al. Immunogenicity and safety of the quadrivalent meningococcal serogroups A, C, W-135 and Y tetanus toxoid conjugate vaccine (MenACWY-TT) in 2-10-year-old children: results of an open, randomised, controlled study. Eur J Pediatr 2013; 172:601-12; PMID:23307281; http://dx.doi.org/10.1007/s00431-012-1924-0
  • Rennels M, King J Jr, Ryall R, Papa T, Froeschle J. Dosage escalation, safety and immunogenicity study of four dosages of a tetravalent meningococcal polysaccharide diphtheria toxoid conjugate vaccine in infants. Pediatr infect Dis J 2004; 23:429-35; PMID:15131466; http://dx.doi.org/10.1097/01.inf.0000126297.28952.f8

Literature of carrier priming at preclinical level

  • Pobre K, Tashani M, Ridda I, Rashid H, Wong M, Booy R. Carrier priming or suppression: understanding carrier priming enhancement of anti-polysaccharide antibody response to conjugate vaccines. Vaccine 2014; 32: 1423-30; PMID:24492014; http://dx.doi.org/10.1016/j.vaccine.2014.01.047
  • Peeters CC, Tenbergen-Meekes AM, Poolman JT, Beurret M, Zegers BJ, Rijkers GT. Effect of carrier priming on immunogenicity of saccharide-protein conjugate vaccines. Infect Immun 1991; 59: 3504–10; PMID:1894357
  • Herzenberg LA, Tokuhisa T. Epitope-specific regulation. I. Carrier-specific induction of suppression for IgG anti-hapten antibody responses. J Exp Med 1982; 155: 1730–40; PMID:6176665
  • Herzenberg LA, Tokuhisa T, Parks DR, Herzenberg LA. Epitope-specific regulation. II. A bistable, Igh-restricted regulatory mechanism central to immunologic memory. J Exp Med 1982; 155: 1741–53; PMID:6176666
  • Schutze MP, Deriaud E, Przewlocki G, LeClerc C. Carrier-induced epitopic suppression is initiated through clonal dominance. J Immunol 1989; 142: 2635–40; PMID:2467933
  • Del Giudice G. New carriers and adjuvants in the development of vaccines. Curr Opin Immunol 1992; 4: 454–9; PMID:1388847
  • LeClerc C, Schutze MP, Deriaud E, Przewlocki G. The in vivo elimination of CD4+ T cells prevents the induction but not the expression of carrier-induced epitopic suppression. J Immunol 1990; 145: 1343–9; PMID:1696595
  • Tontini M, Berti F, Romano MR, Proietti D, Zambonelli C, Bottomley MJ, De Gregorio E, Del Giudice G, Rappuoli R, Costantino P, et al. Comparison of CRM197, diphtheria toxoid and tetanus toxoid as protein carriers for meningococcal glycoconjugate vaccines. Vaccine 2013; 31: 4827–33; PMID:23965218; http://dx.doi.org/10.1016/j.vaccine.2013.07.078
  • Pecetta S, Lo Surdo P, Tontini M, Proietti D, Zambonelli C, Bottomley MJ, Biagini M, Berti F, Costantino P, Romano MR, Study Group. Carrier priming with CRM197 or diphtheria toxoid has a different impact on the immunogenicity of the respective glycoconjugates: biophysical and immunochemical interpretation. Vaccine 2015; 33: 314–320; PMID:25448110; http://dx.doi.org/10.1016/j.vaccine.2014.11.026

Literature on carrier interference at clinical level

  • Burrage M, Robinson A, Borrow R, Andrews N, Southern J, Findlow J, Martin S, Thornton C, Goldblatt D, Corbel M, et al. Effect of vaccination with carrier protein on response to meningococcal C conjugate vaccines and value of different immunoassays as predictors of protection. Infect Immun 2002; 70: 4946-54; PMID:12183540
  • Dagan R, Poolman J, Siegrist CA. Glycoconjugate vaccines and immune interference: A review. Vaccine 2010; 28: 5513-23; PMID:20600514; http://dx.doi.org/10.1016/j.vaccine.2010.06.026
  • Pobre K, Tashani M, Ridda I, Rashid H, Wong M, Booy R. Carrier priming or suppression: understanding carrier priming enhancement of anti-polysaccharide antibody response to conjugate vaccines. Vaccine 2014; 32: 1423-30; PMID:24492014; http://dx.doi.org/10.1016/j.vaccine.2014.01.047
  • Granoff DM, Holmes SJ, Belshe RB, Osterholm MT, McHugh JE, Anderson EL. Effect of carrier protein priming on antibody responses to Haemophilus influenzae type b conjugate vaccines in infants. JAMA 1994; 272: 1116–21; PMID:7933324
  • Granoff DM, Rathore MH, Holmes SJ, Granoff PD, Lucas AH. Effect of immunity to the carrier protein on antibody responses to Haemophilus influenzae type b conjugate vaccines. Vaccine 1993;11 Suppl 1: S46–51; PMID:8447176
  • Shelly MA, Pichichero ME, Treanor JJ. Low baseline antibody level to diphtheria is associated with poor response to conjugated pneumococcal vaccines in adults. Scand J Infect Dis 2001; 33: 542–4; PMID:11515767
  • Barington T, Skettrup M, Juul L, Heilmann C. Non-epitope-specific suppression of the antibody response to Haemophilus influenzae type b conjugate vaccines by preimmunization with vaccine components. Infect Immun 1993; 61: 432–8; PMID:7678586
  • Lee LH, Blake MS. Effect of increased CRM197 carrier protein dose on meningococcal C bactericidal antibody response. Clin Vaccine Immunol 2012; 19: 551–6; PMID:22336285; http://dx.doi.org/10.1128/CVI.05438-11
  • Dagan R, Goldblatt D, Maleckar JR, Yaïch M, Eskola J. Reduction of antibody response to an 11-valent pneumococcal vaccine coadministered with a vaccine containing acellular pertussis components. Infect Immun 2004; 72: 5383–91; PMID:15322036
  • Knuf M, Kowalzik F, Kieninger D. Comparative effects of carrier proteins on vaccine-induced immune response. Vaccine 2011; 29: 4881–90; PMID:21549783; http://dx.doi.org/10.1016/j.vaccine.2011.04.053
  • Borrow R, Dagan R, Zepp F, Hallander H, Poolman J. Glycoconjugate vaccines and immune interactions, and implications for vaccination schedules. Expert Rev Vaccines 2011; 10: 1621–31; PMID:22043960; http://dx.doi.org/10.1586/erv.11.142
  • Usonis V, Bakasenas V, Lockhart S, Baker S, Gruber W, Laudat F. A clinical trial examining the effect of increased total CRM197 carrier protein dose on the antibody response to Haemophilus influenzae type b CRM197 conjugate vaccine. Vaccine 2008; 26: 4602–7; PMID:18577410; http://dx.doi.org/10.1016/j.vaccine.2008.05.087
  • Ruiz-Palacios GM, Huang LM, Lin TY, Hernandez L, Guerrero ML, Villalobos AL, Van der Wielen M, Moreira M, Fissette L, Borys D, et al. Immunogenicity and safety of a booster dose of the 10-valent pneumococcal Haemophilus influenzae protein D conjugate vaccine coadministered with the tetravalent meningococcal serogroups A, C, W-135 and Y tetanus toxoid conjugate vaccine in toddlers: a randomized trial. Pediatric Infect Dis J 2013; 32: 62–71; PMID:23076383; http://dx.doi.org/10.1097/INF.0b013e3182784143
  • Dagan R, Eskola J, Leclerc C, Leroy O. Reduced response to multiple vaccines sharing common protein epitopes that are administered simultaneously to infants. Infect Immun 1998; 66: 2093–8; PMID:9573094
  • Prymula R, Schuerman L. 10-valent pneumococcal nontypeable Haemophilus influenzae PD conjugate vaccine: Synflorix. Expert Rev Vaccines 2009; 8: 1479–500; PMID:19863240; http://dx.doi.org/10.1586/erv.09.113

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