Long-term protection after immunization with protein-polysaccharide conjugate vaccines in infancy

Expert Review of Vaccines

Volumn 10, Issue 5, 2011, Pages 673-684

  Blanchard Rohner, Geraldine ^a,b   Pollard, Andrew J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b GENEVA UNIVERSITY HOSPITALS   (Switzerland)

Author keywords

antibody; B cells; encapsulated bacteria; long term immunity; protein polysaccharide conjugate vaccines

Indexed keywords

B LYMPHOCYTE ANTIBODY; B LYMPHOCYTE RECEPTOR; BACTERIAL POLYSACCHARIDE; CAPSULAR ANTIBODY; CD19 ANTIGEN; COMPLEMENT COMPONENT C3D RECEPTOR; EPITOPE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; POLYSACCHARIDE VACCINE; PROTEIN POLYSACCHARIDE CONJUGATE VACCINE; T LYMPHOCYTE ANTIGEN; UNCLASSIFIED DRUG; VACCINE;

ANTIBODY RESPONSE; ANTIBODY TITER; B LYMPHOCYTE; CELL FUNCTION; DRUG EFFICACY; DRUG MECHANISM; DRUG PROTEIN BINDING; HAEMOPHILUS INFLUENZAE TYPE B; HELPER CELL; HUMAN; IMMUNIZATION; IMMUNOLOGICAL MEMORY; INFANCY; INFANT; MEMORY CELL; NEISSERIA MENINGITIDIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SPLEEN; STREPTOCOCCUS PNEUMONIAE; SURVIVAL RATE;

ANTIBODIES, BACTERIAL; BACTERIAL PROTEINS; BACTERIAL VACCINES; HAEMOPHILUS INFECTIONS; HAEMOPHILUS INFLUENZAE; HUMANS; IMMUNITY, HERD; IMMUNOLOGIC MEMORY; INFANT; MENINGOCOCCAL INFECTIONS; NEISSERIA MENINGITIDIS; PNEUMOCOCCAL INFECTIONS; POLYSACCHARIDES, BACTERIAL; STREPTOCOCCUS PNEUMONIAE; TIME FACTORS; VACCINATION; VACCINES, CONJUGATE;

EID: 79957604981     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/erv.11.14     Document Type: Review

References (90)

1. Watt JP, Wolfson LJ, O'Brien KL et al. Burden of disease caused by Haemophilus influenzae type b in children younger than5 years: global estimates. Lancet 374(9693), 903-911 (2009).
2. O'Brien KL, Wolfson LJ, Watt JP et al. Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates. Lancet 374(9693), 893-902 (2009).
3. Pollard AJ, Frasch C. Development of natural immunity to Neisseria meningitidis. Vaccine 19(11-12), 1327-1346 (2001). (Pubitemid 32332716)
4. Goldschneider I, Gotschlich EC, Artenstein MS. Human immunity to the meningococcus. I. The role of humoral antibodies. J. Exp. Med. 129(6), 1307-1326 (1969).
5. Troncoso G, Sanchez S, Moreda M, Criado MT, Ferreiros CM. Antigenic cross-reactivity between outer membrane proteins of Neisseria meningitidis and commensal Neisseria species. FEMS Immunol. Med. Microbiol. 27(2), 103-109 (2000). (Pubitemid 30047087)
6. Lesinski GB, Westerink MA. Novel vaccine strategies to T-independent antigens. J. Microbiol. Methods 47(2), 135-149 (2001). (Pubitemid 32910271)
7. Martin F, Kearney JF. B1 cells: similarities and differences with other B cell subsets. Curr. Opin. Immunol. 13(2), 195-201 (2001). (Pubitemid 32176039)
8. Boes M. Role of natural and immune IgM antibodies in immune responses. Mol. Immunol. 37(18), 1141-1149 (2000).
9. Baumgarth N, Tung JW, Herzenberg LA. Inherent specificities in natural antibodies: a key to immune defense against pathogen invasion. Springer Semin. Immunopathol. 26(4), 347-362 (2005).
10. Pillai S, Cariappa A, Moran ST. Marginal zone B cells. Annu. Rev. Immunol. 23, 161-196 (2005). (Pubitemid 40563168)
11. Weller S, Braun MC, Tan BK et al. Human blood IgM "memory" B cells are circulating splenic marginal zone B cells harboring a prediversified immunoglobulin repertoire. Blood 104(12), 3647-3654 (2004). (Pubitemid 39564441)
12. Kruetzmann S, Rosado MM, Weber H et al. Human immunoglobulin M memory B cells controlling Streptococcus pneumoniae infections are generated in the spleen. J. Exp. Med. 197(7), 939-945 (2003). (Pubitemid 36437871)
13. Kruschinski C, Zidan M, Debertin AS, von Horsten S, Pabst R. Age-dependent development of the splenic marginal zone in human infants is associated with different causes of death. Hum. Pathol. 35(1), 113-121 (2004). (Pubitemid 38133931)
14. Fearon DT, Carroll MC. Regulation of B lymphocyte responses to foreign and self-antigens by the CD19/CD21 complex. Annu. Rev. Immunol. 18, 393-422 (2000). (Pubitemid 30365386)
15. Iwasaki A, Medzhitov R. Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 5(10), 987-995 (2004). (Pubitemid 41057715)
16. Rijkers GT, Sanders EA, Breukels MA, Zegers BJ. Infant B cell responses to polysaccharide determinants. Vaccine 16(14-15), 1396-1400 (1998). (Pubitemid 28364674)
17. Tzianabos A, Wang JY, Kasper DL. Biological chemistry of immunomodulation by zwitterionic polysaccharides. Carbohydr. Res. 338(23), 2531-2538 (2003). (Pubitemid 37509952)
18. Cobb BA, Kasper DL. Zwitterionic capsular polysaccharides: the new MHCII-dependent antigens. Cell. Microbiol. 7(10), 1398-1403 (2005). (Pubitemid 41335244)
19. Jokhdar H, Borrow R, Sultan A et al. Immunologic hyporesponsiveness to serogroup C but not serogroup A following repeated meningococcal A/C polysaccharide vaccination in Saudi Arabia. Clin. Diagn. Lab. Immunol. 11(1), 83-88 (2004). (Pubitemid 38090656)
20. Peltola H, Makela H, Kayhty H et al. Clinical efficacy of meningococcus group A capsular polysaccharide vaccine in children three months to five years of age. N. Engl. J. Med. 297(13), 686-691 (1977). (Pubitemid 8208235)
21. Lucas AH, Apicella MA, Taylor CE. Carbohydrate moieties as vaccine candidates. Clin. Infect. Dis. 41(5), 705-712 (2005). (Pubitemid 41174585)
22. Lepow ML, Goldschneider I, Gold R, Randolph M, Gotschlich EC. Persistence of antibody following immunization of children with groups A and C meningococcal polysaccharide vaccines. Pediatrics 60(5), 673-680 (1977). (Pubitemid 8242421)
23. Peltola H, Kayhty H, Virtanen M, Makela PH. Prevention of Hemophilus influenzae type b bacteremic infections with the capsular polysaccharide vaccine. N. Engl. J. Med. 310(24), 1561-1566 (1984). (Pubitemid 14117336)
24. Conaty S, Watson L, Dinnes J, Waugh N. The effectiveness of pneumococcal polysaccharide vaccines in adults: a systematic review of observational studies and comparison with results from randomised controlled trials. Vaccine 22(23-24), 3214-3224 (2004). (Pubitemid 39037227)
25. Granoff DM, Pollard AJ. Reconsideration of the use of meningococcal polysaccharide vaccine. Pediatr. Infect. Dis. J. 26(8), 716-722 (2007). (Pubitemid 47424642)
26. Makela PH, Kayhty H. Evolution of conjugate vaccines. Expert Rev. Vaccines 1(3), 399-410 (2002). (Pubitemid 36559874)
27. MacLennan IC. Germinal centers. Annu. Rev. Immunol. 12, 117-139 (1994). (Pubitemid 24140411)
28. Lai Z, Schreiber JR. Antigen processing of glycoconjugate vaccines; the polysaccharide portion of the pneumococcal CRM197 conjugate vaccine co-localizes with MHC II on the antigen processing cell surface. Vaccine 27(24), 3137-3144 (2009).
29. Borrow R, Andrews N, Findlow H 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. Clin. Vaccine Immunol. 17(1), 154-159 (2010).
30. Ramsay ME, McVernon J, Andrews NJ, Heath PT, Slack MP. Estimating Haemophilus influenzae type b vaccine effectiveness in England and Wales by use of the screening method. J. Infect. Dis. 188(4), 481-485 (2003). (Pubitemid 37011798)
31. Haddy RI, Perry K, Chacko CE et al. Comparison of incidence of invasive Streptococcus pneumoniae disease among children before and after introduction of conjugated pneumococcal vaccine. Pediatr. Infect. Dis. J. 24(4), 320-323 (2005). (Pubitemid 40525339)
32. Heath PT, McVernon J. The UK Hib vaccine experience. Arch. Dis. Child. 86(6), 396-399 (2002). (Pubitemid 34596646)
33. Ramsay ME, Andrews NJ, Trotter CL, Kaczmarski EB, Miller E. Herd immunity from meningococcal serogroup C conjugate vaccination in England: database analysis. BMJ (Clin. Res. Ed.) 326(7385), 365-366 (2003). (Pubitemid 36241472)
34. Borrow R, Goldblatt D, Finn A et al. Immunogenicity of, and immunologic memory to, a reduced primary schedule of meningococcal C-tetanus toxoid conjugate vaccine in infants in the United kingdom. Infect. Immun. 71(10), 5549-5555 (2003). (Pubitemid 37205605)
35. Trotter CL, Andrews NJ, Kaczmarski EB, Miller E, Ramsay ME. Effectiveness of meningococcal serogroup C conjugate vaccine 4 years after introduction. Lancet 364(9431), 365-367 (2004). (Pubitemid 38970013)
36. Snape MD, Kelly DF, Salt P et al. Serogroup C meningococcal glycoconjugate vaccine in adolescents: persistence of bactericidal antibodies and kinetics of the immune response to a booster vaccine more than 3 years after immunization. Clin. Infect. Dis. 43(11), 1387-1394 (2006). (Pubitemid 44845637)
37. Snape MD, Kelly DF, Lewis S et al. Seroprotection against serogroup C meningococcal disease in adolescents in the United Kingdom: observational study. BMJ (Clin. Res. Ed.) 336(7659), 1487-1491 (2008). (Pubitemid 351977021)
38. Khatami A, Snape MD, John T 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. Pediatr. Infect. Dis. J. 30(3), 197-202 (2011).
39. Siber GR, Chang I, Baker S et al. Estimating the protective concentration of anti-pneumococcal capsular polysaccharide antibodies. Vaccine 25(19), 3816-3826 (2007). (Pubitemid 46589754)
40. Plotkin SA. Correlates of protection induced by vaccination. Clin. Vaccine Immunol. 17(7), 1055-1065 (2010).
41. Vernacchio L, Romero-Steiner S, Martinez JE et al. Comparison of an opsonophagocytic assay and IgG ELISA to assess responses to pneumococcal polysaccharide and pneumococcal conjugate vaccines in children and young adults with sickle cell disease. J. Infect. Dis. 181(3), 1162-1166 (2000). (Pubitemid 30194508)
42. WHO. Recommendations to assure the quality, safety and efficacy of pneumococcal conjugate vaccines. In: WHO Technical Report Series. WHO, Geneva, Switzerland, 927 (2009).
43. Borrow R, Andrews N, Goldblatt D, Miller E. Serological basis for use of meningococcal serogroup C conjugate vaccines in the United Kingdom: reevaluation of correlates of protection. Infect. Immun. 69(3), 1568-1573 (2001). (Pubitemid 32187610)
44. Maslanka SE, Tappero JW, Plikaytis BD 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. Infect. Immun. 66(6), 2453-2459 (1998). (Pubitemid 28261738)
45. Kayhty H, Peltola H, Karanko V, Makela PH. The protective level of serum antibodies to the capsular polysaccharide of Haemophilus influenzae type b. J. Infect. Dis. 147(6), 1100 (1983). (Pubitemid 13068358)
46. Lee LH, Frasch CE, Falk LA, Klein DL, Deal CD. Correlates of immunity for pneumococcal conjugate vaccines. Vaccine 21(17-18), 2190-2196 (2003).
47. Kayhty H. Difficulties in establishing a serological correlate of protection after immunization with Haemophilus influenzae conjugate vaccines. Biologicals 22(4), 397-402 (1994).
48. Snape MD, Kelly DF, Green B, Moxon ER, Borrow R, Pollard AJ. Lack of serum bactericidal activity in preschool children two years after a single dose of serogroup C meningococcal polysaccharide-protein conjugate vaccine. Pediatr. Infect. Dis. J. 24(2), 128-131 (2005). (Pubitemid 40250770)
49. Auckland C, Gray S, Borrow R et al. Clinical and immunologic risk factors for meningococcal C conjugate vaccine failure in the United Kingdom. J. Infect. Dis. 194(12), 1745-1752 (2006). (Pubitemid 44902007)
50. McVernon J, Johnson PD, Pollard AJ, Slack MP, Moxon ER. Immunologic memory in Haemophilus influenzae type b conjugate vaccine failure. Arch. Dis. Child. 88(5), 379-383 (2003). (Pubitemid 36566716)
51. Blanchard Rohner G, Snape MD, Kelly DF et al. The magnitude of the antibody and memory B cell responses during priming with a protein- polysaccharide conjugate vaccine in human infants is associated with the persistence of antibody and the intensity of booster response. J. Immunol. 180(4), 2165-2173 (2008).
52. Edwards EA, Devine LF, Sengbusch GH, Ward HW. Immunological investigations of meningococcal disease. III. Brevity of group C acquisition prior to disease occurrence. Scand. J. Infect. Dis. 9(2), 105-110 (1977). (Pubitemid 8103945)
53. John TJ, Samuel R. Herd immunity and herd effect: new insights and definitions. Eur. J. Epidemiol. 16(7), 601-606 (2000).
54. Lexau CA, Lynfield R, Danila R et al. Changing epidemiology of invasive pneumococcal disease among older adults in the era of pediatric pneumococcal conjugate vaccine. JAMA 294(16), 2043-2051 (2005). (Pubitemid 41539937)
55. Jacob J, Kassir R, Kelsoe G. In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. I. The architecture and dynamics of responding cell populations. J. Exp. Med. 173(5), 1165-1175 (1991).
56. Nossal GJ, Makela O. Autoradiographic studies on the immune response. I. The kinetics of plasma cell proliferation. J. Exp. Med. 115, 209-230 (1962).
57. Klein U, Rajewsky K, Kuppers R. Human immunoglobulin (Ig)M+IgD+ peripheral blood B cells expressing the CD27 cell surface antigen carry somatically mutated variable region genes: CD27 as a general marker for somatically mutated (memory) B cells. J. Exp. Med. 188(9), 1679-1689 (1998). (Pubitemid 28516113)
58. Smith KG, Light A, Nossal GJ, Tarlinton DM. The extent of affinity maturation differs between the memory and antibody-forming cell compartments in the primary immune response. EMBO J. 16(11), 2996-3006 (1997). (Pubitemid 27234939)
59. Vieira P, Rajewsky K. The half-lives of serum immunoglobulins in adult mice. Eur. J. Immunol. 18(2), 313-316 (1988). (Pubitemid 18078861)
60. Crotty S, Ahmed R. Immunological memory in humans. Semin. Immun. 16(3), 197-203 (2004). (Pubitemid 38569900)
61. Manz RA, Hauser AE, Hiepe F, Radbruch A. Maintenance of serum antibody levels. Annu. Rev. Immunol. 23, 367-386 (2005). (Pubitemid 40563174)
62. Slifka MK, Antia R, Whitmire JK, Ahmed R. Humoral immunity due to long-lived plasma cells. Immunity 8(3), 363-372 (1998). (Pubitemid 28188896)
63. DiLillo DJ, Hamaguchi Y, Ueda Y et al. Maintenance of long-lived plasma cells and serological memory despite mature and memory B cell depletion during CD20 immunotherapy in mice. J. Immunol. 180(1), 361-371 (2008).
64. Fairfax KA, Kallies A, Nutt SL, Tarlinton DM. Plasma cell development: from B-cell subsets to long-term survival niches. Semin. Immun. 20(1), 49-58 (2008).
65. Edwards JC, Szczepanski L, Szechinski J et al. Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N. Engl. J. Med. 350(25), 2572-2581 (2004). (Pubitemid 38758544)
66. Crotty S, Felgner P, Davies H, Glidewell J, Villarreal L, Ahmed R. Cutting edge: long-term B cell memory in humans after smallpox vaccination. J. Immunol. 171(10), 4969-4973 (2003). (Pubitemid 37432774)
67. Maruyama M, Lam KP, Rajewsky K. Memory B-cell persistence is independent of persisting immunizing antigen. Nature 407(6804), 636-642 (2000).
68. Ochsenbein AF, Pinschewer DD, Sierro S, Horvath E, Hengartner H, Zinkernagel RM. Protective long-term antibody memory by antigen-driven and T help-dependent differentiation of long-lived memory B cells to short-lived plasma cells independent of secondary lymphoid organs. Proc. Natl Acad. Sci. USA 97(24), 13263-13268 (2000).
69. Bernasconi NL, Traggiai E, Lanzavecchia A. Maintenance of serological memory by polyclonal activation of human memory B cells. Science 298(5601), 2199-2202 (2002). (Pubitemid 35471246)
70. Kelly DF, Snape MD, Perrett KP et al. Plasma and memory B-cell kinetics in infants following a primary schedule of CRM 197-conjugated serogroup C meningococcal polysaccharide vaccine. Immunology 127(1), 134-143 (2009).
71. Kelly DF, Snape M, Clutterbuck EC et al. CRM197-conjugated serogroup C meningococcal capsular polysaccharide, but not the native polysaccharide, induces persistent antigen specific memory B cells. Blood 108(8), 2642-2647 (2006).
72. Clutterbuck EA, Oh S, Hamaluba M, Westcar S, Beverley PC, Pollard AJ. Serotype-specific and age-dependent generation of pneumococcal polysaccharide-specific memory B-cell and antibody responses to immunization with a pneumococcal conjugate vaccine. Clin. Vaccine Immunol. 15(2), 182-193 (2008). (Pubitemid 352025528)
73. Siegrist CA, Aspinall R. B-cell responses to vaccination at the extremes of age. Nat. Rev. 9(3), 185-194 (2009).
74. Griffioen AW, Franklin SW, Zegers BJ, Rijkers GT. Expression and functional characteristics of the complement receptor type 2 on adult and neonatal B lymphocytes. Clin. Immunol. Immunopathol. 69(1), 1-8 (1993). (Pubitemid 23303569)
75. Pedraz C, Lorente F, Pedraz MJ, Salazar Villalobos V. Development of the serum levels of complement during the first year of life. An. Esp. Pediatr. 13(7), 571-576 (1980). (Pubitemid 11234709)
76. Pihlgren M, Tougne C, Bozzotti P et al. Unresponsiveness to lymphoid-mediated signals at the neonatal follicular dendritic cell precursor level contributes to delayed germinal center induction and limitations of neonatal antibody responses to T-dependent antigens. J. Immunol. 170(6), 2824-2832 (2003). (Pubitemid 36302152)
77. Siegrist CA. Mechanisms by which maternal antibodies influence infant vaccine responses: review of hypotheses and definition of main determinants. Vaccine 21(24), 3406-3412 (2003).
78. Bryant VL, Ma CS, Avery DT et al. Cytokine-mediated regulation of human B cell differentiation into Ig-secreting cells: predominant role of IL-21 produced by CXCR5+ T follicular helper cells. J. Immunol. 179(12), 8180-8190 (2007).
79. Pihlgren M, Schallert N, Tougne C et al. Delayed and deficient establishment of the long-term bone marrow plasma cell pool during early life. Eur J. Immunol. 31(3), 939-946 (2001). (Pubitemid 32237130)
80. Pihlgren M, Friedli M, Tougne C, Rochat AF, Lambert PH, Siegrist CA. Reduced ability of neonatal and early-life bone marrow stromal cells to support plasmablast survival. J. Immunol. 176(1), 165-172 (2006). (Pubitemid 43023260)
81. Parsons HK, Dockrell DH. The burden of invasive pneumococcal disease and the potential for reduction by immunisation. Int. J. Antimicrob. Agents 19(2), 85-93 (2002). (Pubitemid 34168175)
82. Policy statement - Recommended childhood and adolescent immunization schedules - United States, 2010. Pediatrics 125(1), 195-196 (2010).
83. Snape MD, Perrett KP, Ford KJ et al. Immunogenicity of a tetravalent meningococcal glycoconjugate vaccine in infants: a randomized controlled trial. JAMA 299(2), 173-184 (2008).
84. Rodenburg GD, van Gils EJ, Veenhoven RH et al. Comparability of antibody response to a booster dose of 7-valent pneumococcal conjugate vaccine in infants primed with either 2 or 3 doses. Vaccine 28(5), 1391-1396 (2010).
85. Pace D, Snape M, Westcar S et al. A novel combined Hib-MenC-TT glycoconjugate vaccine as a booster dose for toddlers: a Phase 3 open randomised controlled trial. Arch. Dis. Child. 93(11), 963-970 (2008).
86. Heath PT, Booy R, Azzopardi HJ et al. Antibody concentration and clinical protection after Hib conjugate vaccination in the United Kingdom. JAMA 284(18), 2334-2340 (2000).
87. Southern J, McVernon J, Gelb D et al. Immunogenicity of a fourth dose of Haemophilus influenzae type b (Hib) conjugate vaccine and antibody persistence in young children from the United Kingdom who were primed with acellular or whole-cell pertussis component-containing Hib combinations in infancy. Clin. Vaccine Immunol. 14(10), 1328-1333 (2007). (Pubitemid 350012976)
88. Tsai TF, Borrow R, Gnehm HE et al. Early appearance of bactericidal antibodies after polysaccharide challenge of toddlers primed with a group C meningococcal conjugate vaccine: what is its role in the maintenance of protection? Clin. Vaccine Immunol. 13(8), 854-861 (2006). (Pubitemid 44409623)
89. Richmond P, Borrow R, Goldblatt D et al. Ability of 3 different meningococcal C conjugate vaccines to induce immunologic memory after a single dose in UK toddlers. J. Infect. Dis. 183(1), 160-163 (2001). (Pubitemid 32043057)
90. McVernon J, Maclennan J, Buttery J, Oster P, Danzig L, Moxon ER. Safety and immunogenicity of meningococcus serogroup C conjugate vaccine administered as a primary or booster vaccination to healthy four-year-old children. Pediatr. Infect. Dis. J. 21(8), 747-753 (2002).