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Advances in Preventive Medicine
Volume 2011, Article ID 846756, 17 pages
http://dx.doi.org/10.4061/2011/846756
Review Article

Conjugate Meningococcal Vaccines Development: GSK Biologicals Experience

1GlaxoSmithKline Biologicals, 2301 Renaissance Boulevard, King of Prussia, PA 19406, USA
2GlaxoSmithKline Biologicals, Avenue Fleming 20 (W23), 1300 Wavre, Belgium

Received 30 November 2010; Accepted 19 April 2011

Academic Editor: Jodie McVernon

Copyright © 2011 Jacqueline M. Miller et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. S. Stephens, “Conquering the meningococcus,” FEMS Microbiology Reviews, vol. 31, no. 1, pp. 3–14, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  2. A. Khatami and A. J. Pollard, “The epidemiology of meningococcal disease and the impact of vaccines,” Expert Review of Vaccines, vol. 9, no. 3, pp. 285–298, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  3. M. P. Girard, M. P. Preziosi, M. T. Aguado, and M. P. Kieny, “A review of vaccine research and development: meningococcal disease,” Vaccine, vol. 24, no. 22, pp. 4692–4700, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  4. R. Brooks, C. W. Woods, D. K. Benjamin, and N. E. Rosenstein, “Increased case-fatality rate associated with outbreaks of Neisseria meningitidis infection, compared with sporadic meningococcal disease, in the United States, 1994-2002,” Clinical Infectious Diseases, vol. 43, no. 1, pp. 49–54, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  5. J. A. D. Leake, M. L. Kone, A. A. Yada et al., “Early detection and response to meningococcal disease epidemics in sub-Saharan Africa: appraisal of the WHO strategy,” Bulletin of the World Health Organization, vol. 80, no. 5, pp. 342–349, 2002. View at Google Scholar · View at Scopus
  6. World Health Organization, Control of Epidemic Meningococcal Disease. WHO Practical Guidelines, WHO/EMC/BAC/98.3, 2nd edition, 1998.
  7. J. A. Al-Tawfiq, T. A. Clark, and Z. A. Memish, “Meningococcal disease: the organism, clinical presentation, and worldwide epidemiology,” Journal of Travel Medicine, vol. 17, supplement 3–8, 2010. View at Publisher · View at Google Scholar · View at PubMed
  8. Z. A. Memish, “Meningococcal disease and travel,” Clinical Infectious Diseases, vol. 34, no. 1, pp. 84–90, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  9. C. Jones, “Vaccines based on the cell surface carbohydrates of pathogenic bacteria,” Anais da Academia Brasileira de Ciencias, vol. 77, no. 2, pp. 293–324, 2005. View at Google Scholar · View at Scopus
  10. A. C. Cohn, J. R. MacNeil, L. H. Harrison et al., “Changes in Neisseria meningitidis disease epidemiology in the United States, 1998–2007: implications for prevention of meningococcal disease,” Clinical Infectious Diseases, vol. 50, no. 2, pp. 184–191, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  11. C. M. Healy, K. M. Butler, E. O. B. Smith et al., “Influence of serogroup on the presentation, course, and outcome of invasive meningococcal disease in children in the Republic of Ireland, 1995–2000,” Clinical Infectious Diseases, vol. 34, no. 10, pp. 1323–1330, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  12. N. E. Rosenstein, B. A. Perkins, D. S. Stephens et al., “The changing epidemiology of meningococcal disease in the United States, 1992–1996,” Journal of Infectious Diseases, vol. 180, no. 6, pp. 1894–1901, 1999. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  13. M. S. Edwards and C. J. Baker, “Complications and sequelae of meningococcal infections in children,” Journal of Pediatrics, vol. 99, no. 4, pp. 540–545, 1981. View at Google Scholar · View at Scopus
  14. N. E. Rosenstein, B. A. Perkins, D. S. Stephens, T. Popovic, and J. M. Hughes, “Meningococcal disease,” New England Journal of Medicine, vol. 344, no. 18, pp. 1378–1388, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  15. L. H. Harrison, M. A. Pass, A. B. Mendelsohn et al., “Invasive meningococcal disease in adolescents and young adults,” Journal of the American Medical Association, vol. 286, no. 6, pp. 694–699, 2001. View at Google Scholar · View at Scopus
  16. M. van Deuren, P. Brandtzaeg, and J. W. van der Meer, “Update on meningococcal disease with emphasis on pathogenesis and clinical management,” Clinical Microbiology Reviews, vol. 13, no. 1, pp. 144–166, 2000. View at Google Scholar · View at Scopus
  17. L. H. Harrison, “Epidemiological profile of meningococcal disease in the United States,” Clinical Infectious Diseases, vol. 50, no. 2, pp. S37–S44, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  18. W. P. Hausdorff, R. Hajjeh, A. Al-Mazrou, A. Shibl, and M. Soriano-Gabarro, “The epidemiology of pneumococcal, meningococcal, and Haemophilus disease in the Middle East and North Africa (MENA) region–current status and needs,” Vaccine, vol. 25, no. 11, pp. 1935–1944, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  19. L. H. Harrison, C. L. Trotter, and M. E. Ramsay, “Global epidemiology of meningococcal disease,” Vaccine, vol. 27, supplement 2, pp. B51–B63, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  20. B. Greenwood, “Manson lecture. Meningococcal meningitis in Africa,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 93, no. 4, pp. 341–353, 1999. View at Publisher · View at Google Scholar · View at Scopus
  21. B. Greenwood, “Editorial: 100 Years of epidemic meningitis in West Africa—has anything changed?” Tropical Medicine and International Health, vol. 11, no. 6, pp. 773–780, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  22. J. R. Lingappa, A. M. Al-Rabeah, R. Hajjeh et al., “Serogroup W-135 meningococcal disease during the Hajj, 2000,” Emerging Infectious Diseases, vol. 9, no. 6, pp. 665–671, 2003. View at Google Scholar · View at Scopus
  23. Y. Traoré, B. M. Njanpop-Lafourcade, K. L. S. Adjogble et al., “The rise and fall of epidemic Neisseria meningitidis serogroup W135 meningitis in Burkina Faso, 2002-2005,” Clinical Infectious Diseases, vol. 43, no. 7, pp. 817–822, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  24. P. Boisier, P. Nicolas, S. Djibo et al., “Meningococcal meningitis: unprecedented incidence of serogroup X-related cases in 2006 in Niger,” Clinical Infectious Diseases, vol. 44, no. 5, pp. 657–663, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  25. S. P. Gagneux, A. Hodgson, T. A. Smith et al., “Prospective study of a serogroup X Neisseria meningitidis outbreak in northern Ghana,” Journal of Infectious Diseases, vol. 185, no. 5, pp. 618–626, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  26. D. M. Mutonga, G. Pimentel, J. Muindi et al., “Epidemiology and risk factors for serogroup x meningococcal meningitis during an outbreak in western Kenya, 2005-2006,” American Journal of Tropical Medicine and Hygiene, vol. 80, no. 4, pp. 619–624, 2009. View at Google Scholar · View at Scopus
  27. M. Connolly and N. Noah, “Is group C meningococcal disease increasing in Europe? A report of surveillance of meningococcal infection in Europe 1993-6. European meningitis surveillance group,” Epidemiol Infect, vol. 122, pp. 41–49, 1999. View at Google Scholar
  28. L. Jódar, I. M. Feavers, D. Salisbury, and D. M. Granoff, “Development of vaccines against meningococcal disease,” Lancet, vol. 359, no. 9316, pp. 1499–1508, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  29. World Health Organization, “Meningococcal disease,” 2010, http://www.ecdc.europa.eu/en/activities/surveillance/EU_IBD/Pages/index.aspx. View at Google Scholar
  30. World Health Organization, “The immunological basis for immunization series, module 15: meningococcal disease,” Tech. Rep., WHO Press, Geneva, Switzerland.
  31. H. Peltola, “Meningococcal vaccines. Current status and future possibilities,” Drugs, vol. 55, no. 3, pp. 347–366, 1998. View at Google Scholar
  32. O. O. Bilukha and N. Rosenstein, “Prevention and control of meningococcal disease: recommendations of the advisory committee on immunization practices (ACIP),” Morbidity and Mortality Weekly Report. Recommendations and Reports, vol. 54, no. 7, pp. 1–21, 2005. View at Google Scholar · View at Scopus
  33. P. L. Shao, L. Y. Chang, S. M. Hsieh et al., “Safety and immunogenicity of a tetravalent polysaccharide vaccine against meningococcal disease,” Journal of the Formosan Medical Association, vol. 108, no. 7, pp. 539–547, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. World Health Organization, “Meningococcal vaccines: polysaccharide and polysaccharide conjugate vaccines,” Wkly Epidemiol Rec, vol. 77, no. 7, pp. 331–339, 2002. View at Google Scholar
  35. R. Gold, M. L. Lepow, I. Goldschneider, T. L. Draper, and E. C. Gotschlich, “Clinical evaluation of group A and group C meningococcal polysaccharide vaccines in infants,” Journal of Clinical Investigation, vol. 56, no. 6, pp. 1536–1547, 1975. View at Google Scholar · View at Scopus
  36. S. I. Pelton and G. P. Gilmet, “Expanding prevention of invasive meningococcal disease,” Expert Review of Vaccines, vol. 8, no. 6, pp. 717–727, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  37. P. Richmond, ED. Kaczmarski, R. Borrow et al., “Meningococcal C polysaccharide vaccine induces immunologic hyporesponsiveness in adults that is overcome by meningococcal C conjugate vaccine,” Journal of Infectious Diseases, vol. 181, no. 2, pp. 761–764, 2000. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  38. L. H. Harrison, “Prospects for vaccine prevention of meningococcal infection,” Clinical Microbiology Reviews, vol. 19, no. 1, pp. 142–164, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  39. D. M. Granoff, R. K. Gupta, R. B. Belshe, and E. L. Andersen, “Induction of immunologic refractoriness in adults by meningococcal C polysaccharide vaccination,” Journal of Infectious Diseases, vol. 178, no. 3, pp. 870–874, 1998. View at Google Scholar · View at Scopus
  40. M. Bröker and K. Veitch, “Quadrivalent meningococcal vaccines: hyporesponsiveness as an important consideration when choosing between the use of conjugate vaccine or polysaccharide vaccine,” Travel Medicine and Infectious Disease, vol. 8, no. 1, pp. 47–50, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  41. G. B. Lesinski and M. A. J. Westerink, “Novel vaccine strategies to T-independent antigens,” Journal of Microbiological Methods, vol. 47, no. 2, pp. 135–149, 2001. View at Publisher · View at Google Scholar · View at Scopus
  42. M. C. J. Maiden, A. B. Ibarz-Pavón, R. Urwin et al., “Impact of meningococcal serogroup C conjugate vaccines on carriage and herd immunity,” Journal of Infectious Diseases, vol. 197, no. 5, pp. 737–743, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  43. E. Miller, D. Salisbury, and M. Ramsay, “Planning, registration, and implementation of an immunisation campaign against meningococcal serogroup C disease in the UK: a success story,” Vaccine, vol. 20, supplement 1, pp. S58–S67, 2001. View at Publisher · View at Google Scholar · View at Scopus
  44. M. E. Ramsay, N. J. Andrews, C. L. Trotter, E. B. Kaczmarski, and E. Miller, “Herd immunity from meningococcal serogroup C conjugate vaccination in England: database analysis,” British Medical Journal, vol. 326, no. 7385, pp. 365–366, 2003. View at Google Scholar · View at Scopus
  45. R. M. de Voer, L. Mollema, R. M. Schepp et al., “Immunity against Neisseria meningitidis serogroup C in the Dutch population before and after introduction of the meningococcal C conjugate vaccine,” PLoS One, vol. 5, no. 8, Article ID e12144, 2010. View at Google Scholar
  46. P. De Wals, V. H. Nguyen, L. J. Erickson, M. Guay, J. Drapeau, and J. St-Laurent, “Cost-effectiveness of immunization strategies for the control of serogroup C meningococcal disease,” Vaccine, vol. 22, no. 9-10, pp. 1233–1240, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  47. A. Larrauri, R. Cano, M. García, and S. Mateo, “Impact and effectiveness of meningococcal C conjugate vaccine following its introduction in Spain,” Vaccine, vol. 23, no. 32, pp. 4097–4100, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  48. X. Bai and R. Borrow, “Genetic shifts of Neisseria meningitidis serogroup B antigens and the quest for a broadly cross-protective vaccine,” Expert Review of Vaccines, vol. 9, pp. 1203–1217, 2010. View at Google Scholar
  49. D. M. Granoff, “Review of meningococcal group B vaccines,” Clinical Infectious Diseases, vol. 50, supplement 2, pp. S54–S65, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  50. L. Jodar, K. Cartwright, and I. M. Feavers, “Standardisation and validation of serological assays for the evaluation of immune responses to Neisseria meningitidis serogroup A and C vaccines,” Biologicals, vol. 28, no. 3, pp. 193–197, 2000. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  51. I. Goldschneider, E. C. Gotschlich, and M. S. Artenstein, “Human immunity to the meningococcus,” Journal of Experimental Medicine, vol. 129, no. 6, pp. 1307–1326, 1969. View at Google Scholar · View at Scopus
  52. C. L. Trotter, N. J. Andrews, E. B. Kaczmarski, E. Miller, and M. E. Ramsay, “Effectiveness of meningococcal serogroup C conjugate vaccine 4 years after introduction,” Lancet, vol. 364, no. 9431, pp. 365–367, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  53. N. Andrews, R. Borrow, and E. Miller, “Validation of serological correlate of protection for meningococcal C conjugate vaccine by using efficacy estimates from postlicensure surveillance in England,” Clinical and Diagnostic Laboratory Immunology, vol. 10, no. 5, pp. 780–786, 2003. View at Publisher · View at Google Scholar · View at Scopus
  54. S. E. Maslanka, J. W. Tappero, B. D. Plikaytis et al., “Age-dependent Neisseria meningitidis serogroup C class-specific antibody concentrations and bactericidal titers in sera from young children from montana immunized with a licensed polysaccharide vaccine,” Infection and Immunity, vol. 66, no. 6, pp. 2453–2459, 1998. View at Google Scholar · View at Scopus
  55. World Health Organization, The Immunological Basis for Immunization Series. Module 15: Meningococcal Disease, Immunization, Vaccines and Biologicals, 2010.
  56. World Health Organization, “Enhanced surveillance of epidemic meningococcal meningitis in Africa: a three year experience,” Wkly Epidemiol Rec, vol. 80, pp. 313–320, 2005. View at Google Scholar
  57. S. Vergnano and P. Heath, “Neisseria meningitidis serogroup A vaccines: an overview,” Expert Review of Vaccines, vol. 2, no. 4, pp. 571–582, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  58. World Health Organization, “Group A and C meningococcal vaccines,” Wkly Epidemiol Rec, vol. 74, pp. 297–304, 1999. View at Google Scholar
  59. S. Gatchalian, E. Palestroque, I. De Vleeschauwer et al., “The development of a new heptavalent diphtheria-tetanus-whole cell pertussis-hepatitis B-Haemophilus influenzae type b-Neisseria meningitidis serogroups A and C vaccine: a randomized dose-ranging trial of the conjugate vaccine components,” International Journal of Infectious Diseases, vol. 12, no. 3, pp. 278–288, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  60. A. Hodgson, A. A. Forgor, D. Chandramohan et al., “A phase II, randomized study on an investigational DTPw-HBV/Hib-MenAC conjugate vaccine administered to infants in Northern Ghana,” PLoS One, vol. 3, no. 5, Article ID e2159, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  61. A. Kerdpanich, B. Warachit, P. Kosuwon et al., “Primary vaccination with a new heptavalent DTPw-HBV/Hib-Neisseria meningitidis serogroups A and C combined vaccine is well tolerated,” International Journal of Infectious Diseases, vol. 12, no. 1, pp. 88–97, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  62. J. C. Tejedor, M. Moro, J. Ruiz-Contreras et al., “Immunogenicity and reactogenicity of primary immunization with a novel combined Haemophilus influenzae type b and Neisseria meningitidis serogroup C-tetanus toxoid conjugate vaccine coadministered with a diphtheria-tetanus- acellular pertussis-hepatitis B-inactivated poliovirus vaccine at 2, 4 and 6 months,” Pediatric Infectious Disease Journal, vol. 26, no. 1, pp. 1–7, 2007. View at Google Scholar
  63. E. T. Luman, L. E. Barker, M. M. McCauley, and C. Drews-Botsch, “Timeliness of childhood immunizations: a state-specific analysis,” American Journal of Public Health, vol. 95, no. 8, pp. 1367–1374, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  64. G. S. Marshall, L. E. Happe, O. E. Lunacsek et al., “Use of combination vaccines is associated with improved coverage rates,” Pediatric Infectious Disease Journal, vol. 26, no. 6, pp. 496–500, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  65. C. Auckland, S. Gray, R. Borrow et al., “Clinical and immunologic risk factors for meningococcal C conjugate vaccine failure in the United Kingdom,” Journal of Infectious Diseases, vol. 194, no. 12, pp. 1745–1752, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  66. M. E. Ramsay, J. McVernon, N. J. Andrews, P. T. Heath, and M. P. Slack, “Estimating Haemophilus influenzae type b vaccine effectiveness in England and Wales by use of the screening method,” Journal of Infectious Diseases, vol. 188, no. 4, pp. 481–485, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  67. J. Eskola, J. Ward, R. Dagan, D. Goldblatt, F. Zepp, and C. A. Siegrist, “Combined vaccination of Haemophilus influenzae type b conjugate and diphtheria-tetanus-pertussis containing acellular pertussis,” Lancet, vol. 354, no. 9195, pp. 2063–2068, 1999. View at Publisher · View at Google Scholar · View at Scopus
  68. P. Habermehl, G. Leroux-Roels, R. Sanger, G. Machler, and D. Boutriau, “Combined Haemophilus influenzae type b and Neisseria meningitidis serogroup C (HibMenC) or serogroup C and Y-tetanus toxoid conjugate (and HibMenCY) vaccines are well-tolerated and immunogenic when administered according to the 2, 3, 4 months schedule with a fourth dose at 12-18 months of age,” Human Vaccines, vol. 6, no. 8, pp. 1–13, 2010. View at Google Scholar
  69. D. Pace, M. Snape, S. Westcar et al., “A new combination Haemophilus influenzae type B and Neisseria meningitidis serogroup C-tetanus toxoid conjugate vaccine for primary immunization of infants,” Pediatric Infectious Disease Journal, vol. 26, no. 11, pp. 1057–1059, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  70. H. J. Schmitt, G. Maechler, P. Habermehl et al., “Immunogenicity, reactogenicity, and immune memory after primary vaccination with a novel Haemophilus influenzae-Neisseria meningitidis serogroup C conjugate vaccine,” Clinical and Diagnostic Laboratory Immunology, vol. 14, no. 4, pp. 426–434, 2007. View at Google Scholar
  71. M. Knuf, L. Szenborn, M. Moro et al., “Immunogenicity of routinely used childhood vaccines when coadministered with the 10-valent pneumococcal non-typeable Haemophilus influenzae protein D conjugate vaccine (PHiD-CV),” Pediatric Infectious Disease Journal, vol. 28, no. 4, pp. S97–S108, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  72. R. Booy, P. Richmond, T. Nolan et al., “Immediate and longer term immunogenicity of a single dose of the combined Haemophilus influenzae type b-Neisseria meningitidis serogroup C-tetanus toxoid conjugate vaccine in primed toddlers 12 to 18 months of age,” Pediatric Infectious Disease Journal, vol. 30, no. 4, pp. 340–342, 2011. View at Google Scholar
  73. D. Pace, M. Snape, S. Westcar et al., “A novel combined Hib-MenC-TT glycoconjugate vaccine as a booster dose for toddlers: a phase 3 open randomised controlled trial,” Archives of Disease in Childhood, vol. 93, no. 11, pp. 963–970, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  74. J. C. Tejedor, M. Moro, J. M. Merino et al., “Immunogenicity and reactogenicity of a booster dose of a novel combined Haemophilus influenzae type b-Neisseria meningitidis serogroup C-tetanus toxoid conjugate vaccine given to toddlers of 13-14 months of age with antibody persistence Up to 31 months of age,” Pediatric Infectious Disease Journal, vol. 27, no. 7, pp. 579–588, 2008. View at Google Scholar
  75. A. Carmona, M. Miranda, F. Barrio et al., “Reactogenicity and immunogenicity of combined Haemophilus influenzae type B-meningococcal serogroup C conjugate vaccine booster dose coadministered with measles, mumps, and rubella vaccine,” Pediatric Infectious Disease Journal, vol. 29, no. 3, pp. 269–271, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  76. A. Khatami, M. D. Snape, T. John et al., “Persistence of immunity following a booster dose of Haemophilus influenzae type B-meningococcal serogroup C glycoconjugate vaccine: follow-up of a randomized controlled trial,” Pediatric Infectious Disease Journal, vol. 30, no. 3, pp. 197–202, 2011. View at Google Scholar
  77. K. P. Perrett, A. P. Winter, E. Kibwana et al., “Antibody persistence after serogroup C meningococcal conjugate immunization of United Kingdom primary-school children in 1999-2000 and response to a booster: a phase 4 clinical trial,” Clinical Infectious Diseases, vol. 50, no. 12, pp. 1601–1610, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  78. R. Borrow, N. Andrews, H. Findlow et al., “Kinetics of antibody persistence following administration of a combination meningococcal serogroup C and Haemophilus influenzae type b conjugate vaccine in healthy infants in the United Kingdom primed with a monovalent meningococcal serogroup C vaccine,” Clinical and Vaccine Immunology, vol. 17, no. 1, pp. 154–159, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  79. J. Díez-Domingo, M. V. Planelles Cantarino, J. M. Baldó Torrentí et al., “A randomized, multicenter, open-label clinical trial to assess the immunogenicity of a meningococcal C vaccine booster dose administered to children aged 14 to 18 months,” Pediatric Infectious Disease Journal, vol. 29, no. 2, pp. 148–152, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  80. J. Wysocki, J. C. Tejedor, D. Grunert et al., “Immunogenicity of the 10-valent pneumococcal non-typeable Haemophilus influenzae protein D conjugate vaccine (PHiD-CV) when coadministered with different Neisseria meningitidis serogroup C conjugate vaccines,” Pediatric Infectious Disease Journal, vol. 28, no. 4, pp. S77–S88, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  81. T. Nolan, S. Lambert, D. Roberton et al., “A novel combined Haemophilus influenzae type b-Neisseria meningitidis serogroups C and Y-tetanus-toxoid conjugate vaccine is immunogenic and induces immune memory when co-administered with DTPa-HBV-IPV and conjugate pneumococcal vaccines in infants,” Vaccine, vol. 25, no. 51, pp. 8487–8499, 2007. View at Publisher · View at Google Scholar · View at PubMed
  82. C. D. Marchant, J. M. Miller, G. S. Marshall et al., “Randomized trial to assess immunogenicity and safety of Haemophilus influenzae type B and Neisseria meningitidis serogroups C and Y-tetanus toxoid conjugate vaccine in infants,” Pediatric Infectious Disease Journal, vol. 29, no. 1, pp. 48–52, 2010. View at Publisher · View at Google Scholar · View at PubMed
  83. G. S. Marshall, C. D. Marchant, M. Blatter et al., “Immune response and one-year antibody persistence after a fourth dose of a novel Haemophilus influenzae type b and Neisseria meningitidis serogroups C and Y-tetanus toxoid conjugate vaccine (hibmency) at 12 to 15 months of age,” Pediatric Infectious Disease Journal, vol. 29, no. 5, pp. 469–471, 2010. View at Publisher · View at Google Scholar · View at PubMed
  84. T. Nolan, P. Richmond, H. Marshall et al., “Immunogenicity and safety of an investigational combined Haemophilus influenzae type b-Neisseria meningitidis serogroups C and Y- tetanus toxoid conjugate vaccine,” Pediatric Infectious Disease Journal, vol. 30, pp. 190–196, 2011. View at Google Scholar
  85. K. A. Bryant, G. S. Marshall, C. D. Marchant et al., “Immunogenicity and safety of H. influenzae type b-N. meningitidis C/Y conjugate vaccine in infants,” Pediatrics, vol. 127, no. 6, pp. 1375–1385, 2011. View at Google Scholar
  86. L. Østergaard, E. Lebacq, J. Poolman, G. Maechler, and D. Boutriau, “Immunogenicity, reactogenicity and persistence of meningococcal A, C, W-135 and Y-tetanus toxoid candidate conjugate (MenACWY-TT) vaccine formulations in adolescents aged 15-25 years,” Vaccine, vol. 27, no. 1, pp. 161–168, 2009. View at Publisher · View at Google Scholar · View at PubMed
  87. M. Knuf, D. Kieninger-Baum, P. Habermehl et al., “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, vol. 28, no. 3, pp. 744–753, 2010. View at Publisher · View at Google Scholar · View at PubMed
  88. N. Bermal, L.-M. Huang, A. P. Dubey et al., “Safety and immunogenicity of a tetravalent meningococcal serogroups A, C, W-135 and Y conjugate vaccine in adolescents and adults,” Human vaccines, vol. 7, no. 2, pp. 239–247, 2011. View at Google Scholar
  89. R. Baxter, Y. Baine, K. Ensor, V. Bianco, L. R. Friedland, and J. M. Miller, “Immunogenicity and safety of an investigational quadrivalent meningococcal ACWY tetanus toxoid conjugate vaccine in healthy adolescents and young adults 10-25 years of age,” Pediatric Infectious Disease Journal, vol. 30, pp. e41–e48, 2011. View at Google Scholar
  90. T. Vesikari, A. Karvonen, V. Bianco, M. Van der Wielen, and J. Miller, “Tetravalent meningococcal serogroups A, C, W-135 and Y conjugate vaccine is well tolerated and immunogenic when co-administered with measles-mumps-rubella-varicella vaccine during the second year of life: an open, randomised controlled trial,” Vaccine, vol. 29, no. 25, pp. 4274–4284, 2011. View at Google Scholar
  91. M. Knuf, A. Pantazi-Chatzikonstantinou, U. Pfletschinger et al., “An investigational tetravalent meningococcal serogroups A, C, W-135 and Y-tetanus toxoid conjugate vaccine co-administered with InfanrixTm hexa is immunogenic, with an acceptable safety profile in 12-23 month old children,” Vaccine, vol. 29, no. 25, pp. 4264–4273, 2011. View at Google Scholar
  92. J. R. Lingappa, N. Rosenstein, E. R. Zell, K. A. Shutt, A. Schuchat, and B. A. Perkins, “Surveillance for meningococcal disease and strategies for use of conjugate meningococcal vaccines in the United States,” Vaccine, vol. 19, no. 31, pp. 4566–4575, 2001. View at Publisher · View at Google Scholar
  93. J. Diez-Domingo, M. V. Planelles Cantarino, M. V. Úbeda Sansano et al., “Immune response and antibody persistence data after a conjugate MenC booster vaccination,” in Proceedings of the 27th Annual Meeting of the European Society for Paediatric Infectious Diseases, Brussels, Belgium, June 2009.
  94. H. Keyserling, T. Papa, K. Koranyi et al., “Safety, immunogenicity, and immune memory of a novel meningococcal (groups A, C, Y, and W-135) polysaccharide diphtheria toxoid conjugate vaccine (MCV-4) in healthy adolescents,” Archives of Pediatrics and Adolescent Medicine, vol. 159, no. 10, pp. 907–913, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  95. S. Black, N. P. Klein, J. Shah, L. Bedell, A. Karsten, and P. M. Dull, “Immunogenicity and tolerability of a quadrivalent meningococcal glycoconjugate vaccine in children 2-10 years of age,” Vaccine, vol. 28, no. 3, pp. 657–663, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus