Toward a new vaccine for pertussis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 9, 2014, Pages 3213-3216

  Robbins, John B ^a   Schneerson, Rachel ^a   Kubler Kielb, Joanna ^a   Keith, Jerry M ^a   Trollfors, Birger ^b   Vinogradov, Evgeny ^c   Shiloach, Joseph ^d  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b SAHLGRENSKA UNIVERSITY HOSPITAL   (Sweden)

^c NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^d NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

Lipooligosaccharide conjugate; New pertussis vaccine

Indexed keywords

BACTERIUM ANTIBODY; CARRIER PROTEIN; NEUTRALIZING ANTIBODY; OLIGOSACCHARIDE; PERTUSSIS VACCINE; TRISACCHARIDE;

ANTIBACTERIAL ACTIVITY; BORDETELLA BRONCHISEPTICA; BORDETELLA PARAPERTUSSIS; BORDETELLA PERTUSSIS; CONJUGATE; HUMAN; NONHUMAN; PERTUSSIS; PRIORITY JOURNAL; REVIEW;

LIPOOLIGOSACCHARIDE CONJUGATE; NEW PERTUSSIS VACCINE;

ANIMALS; ANTIBODIES, BACTERIAL; BACTERIAL VACCINES; BORDETELLA BRONCHISEPTICA; BORDETELLA PERTUSSIS; DRUG DESIGN; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; MICE; OLIGOSACCHARIDES; SERUM ALBUMIN, BOVINE; VACCINES, CONJUGATE; WHOOPING COUGH;

EID: 84895793675     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1324149111     Document Type: Review

References (87)

1. Bordet J, Gengou O (1906) Le microbe de la coqueluche. Ann Inst Pasteur (Paris) 20:731-741.
2. Centers for Disease Control and Prevention (CDC) (2008) Licensure of a diphtheria and tetanus toxoids and acellular pertussis adsorbed, inactivated poliovirus, and haemophilus B conjugate vaccine and guidance for use in infants and children. MMWR Morb Mortal Wkly Rep 57(39):1079-1080.
3. Centers for Disease Control and Prevention (CDC) (2012) Updated recommendations for use of tetanus toxoid, reduced diphtheria toxoid, and acellular pertussis (Tdap) vaccine in adults aged 65 years and older-Advisory Committee on Immunization Practices (ACIP), 2012. MMWR Morb Mortal Wkly Rep 61(25):468-470.
4. Fishman DN, et al. (2011) Jamieson F. Pertussis resurgence in Toronto, Canada: A population-based study including test-incidence feedback modeling. BMC Public Health 11:1-10.
5. Celentano LP, Massari M, Paramatti D, Salmaso S, Tozzi AE; EUVAC-NET Group (2005) Resurgence of pertussis in Europe. Pediatr Infect Dis J 24(9):761-765.
6. Zepp F, et al. (2011) Rationale for pertussis booster vaccination throughout life in Europe. Lancet Infect Dis 11(7):557-570.
7. Cherry JD (2012) Epidemic pertussis in 2012-The resurgence of a vaccine-preventable disease. N Engl J Med 367(9):785-787.
8. Winter K, et al. (2012) California pertussis epidemic, 2010. J Pediatr 161(6):1091-1096.
9. Pittman M (1991) History of the development of pertussis vaccine. Dev Biol Stand 73:13-29.
10. Centers for Disease Control and Prevention (CDC) (2002) Pertussis-United States, 1997-2000. MMWR Morb Mortal Wkly Rep 51(4):73-76.
11. Madsen T (1933) Vaccination against whooping cough. JAMA 101:1878-188.
12. Sauer LW (1930) Whooping cough: Results of a seven year study. J Pediatr 1930:740-749.
13. Kendrick PL, Eldering G, Dixon MK, Misner J (1947) Mouse protection tests in the study of pertussis vaccine. Am J Public Health 37(9):803-810.
14. Pittman M, Lieberman JE (1948) An analysis of the Wilson-Worcester method for determining the median effective dose of pertussis vaccine. Am J Public Health Nations Health 38(1 Pt 1): 15-21.
15. Pittman M (1956) Pertussis and pertussis vaccine control. J Wash Acad Sci 46:234-242.
16. Centers for Disease Control (CDC) (1984) Pertussis-United States, 1982 and 1983. MMWR Morb Mortal Wkly Rep 33(40): 573-575.
17. Linneman CC, Jr., Ramundo N, Perlstein PH, Minton D, Englander GS (1977) Use of pertussis vaccine in an epidemic involving hospital staff. Lancet 2:540-543.
18. Stewart GT (1977) Vaccination against whooping-cough. Efficacy versus risks. Lancet 1(8005):234-237.
19. Cherry JD (1990) 'Pertussis vaccine encephalopathy': It is time to recognize it as the myth that it is. JAMA 263(12):1679-1680.
20. Iida T, Kusano N, Yamamoto A, Konosu M (1966) An immunofluorescence study of the action of antibody in experimental intracerebral infection of mice with Bordetella pertussis. J Pathol Bacteriol 92(2):359-367.
21. Sato H, Sato Y, Ohishi I (1991) Comparison of pertussis toxin (PT)-neutralizing activities and mouse-protective activities of anti-PT mouse monoclonal antibodies. Infect Immun 59(10):3832-3835.
22. Watanabe M, et al. (2002) Efficacy of pertussis components in an acellular vaccine, as assessed in a murine model of respiratory infection and a murine intracerebral challenge model. Vaccine 20(9-10):1429-1434.
23. Robbins JB, Schneerson R, Trollfors B, Taranger J, Lagergard T (1998) Standardization of acellular pertussis vaccine by assay of serum neutralizing antibodies to pertussis toxin (antitoxin): Analogy with diphtheria toxoid. Dev Biol Stand 95:155-158.
24. Pittman M (1979) Pertussis toxin: The cause of the harmful effects and prolonged immunity of whooping cough. A hypothesis. Rev Infect Dis 1(3):401-412.
25. Locht C, Keith JM (1986) Pertussis toxin gene: Nucleotide sequence and genetic organization. Science 232(4755):1258-1264.
26. Nicosia A, et al. (1986) Cloning and sequencing of the pertussis toxin genes: Operon structure and gene duplication. Proc Natl Acad Sci USA 83(13):4631-4635.
27. Burnette WN, Cieplak W, Mar VL, Kaljot KT, Sato H, Keith JM (1988) Pertussis toxin S1 mutant with reduced enzyme activity and a conserved protective epitope. Science 242(4875):72-74.
28. Nencioni L, et al. (1990) Characterization of genetically inactivated pertussis toxin mutants: Candidates for a new vaccine against whooping cough. Infect Immun 58(5):1308-1315.
29. Sato Y, Kimura M, Fukumi H (1984) Development of a pertussis component vaccine in Japan. Lancet 1(8369):122-126.
30. Olin P, Rasmussen F, Gustafsson L, Hallander HO, Heijbel H; Ad Hoc Group for the Study of Pertussis Vaccines (1997) Randomised controlled trial of two-component, three-component, and fivecomponent acellular pertussis vaccines compared with whole-cell pertussis vaccine. Lancet 350(9091):1569-1577.
31. Liese JG, et al.; Munich Vaccine Study Group (2001) Safety and immunogenicity of Biken acellular pertussis vaccine in combination with diphtheria and tetanus toxoid as a fifth dose at four to six years of age. Pediatr Infect Dis J 20(10):981-988.
32. Halperin SA, et al. (2003) Nature, evolution, and appraisal of adverse events and antibody response associated with the fifth consecutive dose of a five-component acellular pertussis-based combination vaccine. Vaccine 21(19-20):2298-2306.
33. Dagan R, et al. (1999) Reactogenicity and immunogenicity of reduced antigen content diphtheria-tetanus-acellular pertussis vaccines as a booster in 4-7-year-old children primed with diphtheriatetanus-whole cell pertussis vaccine before 2 years of age. Vaccine 17(20-21):2620-2627.
34. Knuf M, et al. (2006) Immunogenicity of a single dose of reduced-antigen acellular pertussis vaccine in a non-vaccinated adolescent population. Vaccine 24(12):2043-2048.
35. Klein NP, Bartlett J, Rowhani-Rahbar A, Fireman B, Baxter R (2012) Waning protection after fifth dose of acellular pertussis vaccine in children. N Engl J Med 367(11):1012-1019.
36. Yeh SH (2003) Pertussis: Persistent pathogen, imperfect vaccines. Expert Rev Vaccines 2(1):113-127.
37. Robbins JB, et al. (2009) Pertussis vaccine: A critique. Pediatr Infect Dis J 28(3):237-241.
38. Storsaeter J, Hallander HO, Gustafsson L, Olin P (2003) Low levels of antipertussis antibodies plus lack of history of pertussis correlate with susceptibility after household exposure to Bordetella pertussis. Vaccine 21(25-26):3542-3549.
39. Trollfors B, et al. (1995) A placebo-controlled trial of a pertussistoxoid vaccine. N Engl J Med 333(16):1045-1050.
40. Hviid A, Stellfeld M, Andersen PH, Wohlfahrt J, Melbye M (2004) Impact of routine vaccination with a pertussis toxoid vaccine in Denmark. Vaccine 22(27-28):3530-3534.
41. Thierry-Cartensen B, et al. (2013) Experience with monocomponent acellular pertussis combination vaccines for infants, children, adolescents and adults-A review of safety, immunogenicity, efficacy and effectiveness studies and 15 years of field experience. Vaccine 31(45):5178-5191.
42. de Melker HE, et al. (2000) Specificity and sensitivity of high levels of immunoglobulin G antibodies against pertussis toxin in a single serum sample for diagnosis of infection with Bordetella pertussis. J Clin Microbiol 38(2):800-806.
43. Taranger J, Trollfors B, Lagergard T, Zackrisson G (1994). Parapertussis infection followed by pertussis infection. Lancet 334(8938):1703.
44. Bergfors E, et al. (1999) Parapertussis and pertussis: Differences and similarities in incidence, clinical course, and antibody responses. Int J Infect Dis 3(3):140-146.
45. Edwards K, et al. (1995) Comparison of 13 acellular pertussis vaccines: Overview and serologic response. Pediatrics 96(3 Pt 2): 548-557.
46. Heininger U, et al.; Pertussis Vaccine Study Group (1998) Comparative efficacy of the Lederle/Takeda acellular pertussis component DTP (DTaP) vaccine and Lederle whole-cell component DTP vaccine in German children after household exposure. Pediatrics 102(3 Pt 1):546-553.
47. Blackwelder WC, Storsaeter J, Olin P, Hallander HO (1991) Acellular pertussis vaccines. Efficacy and evaluation of clinical case definitions. Am J Dis Child 145(11):1285-1289.
48. Cherry JD, Gornbein J, Heininger U, Stehr K (1998) A search for serologic correlates of immunity to Bordetella pertussis cough illnesses. Vaccine 16(20):1901-1906.
49. Charles I, et al. (1993) Expression of P.69/pertactin from Bordetella pertussis in a baculovirus/insect cell expression system: Protective properties of the recombinant protein. Res Microbiol 144(9):681-690.
50. Shahin RD, Brennan MJ, Li ZM, Meade BD, Manclark CR (1990) Characterization of the protective capacity and immunogenicity of the 69-kD outer membrane protein of Bordetella pertussis. J Exp Med 171(1):63-73.
51. Isacson J, Trollfors B, Taranger J, Lagergard T (1995) Acquisition of IgG serum antibodies against two Bordetella antigens (filamentous hemagglutinin and pertactin) in children with no symptoms of pertussis. Pediatr Infect Dis J 14(6):517-521.
52. Kuno-Sakai H, Kimura M, Watanabe H (2004) Verification of components of acellular pertussis vaccines that have been distributed solely, been in routine use for the last two decades and contributed greatly to control of pertussis in Japan. Biologicals 32(1):29-35.
53. Otsuka N, et al. (2012) Prevalence and genetic characterization of pertactin-deficient Bordetella pertussis in Japan. PLoS ONE 7(2): e31985.
54. Queenan AM, Cassiday PK, Evangelista A (2013) Pertactinnegative variants of Bordetella pertussis in the United States. N Engl J Med 368(6):583-584.
55. Bodilis H, Guiso N (2013) Virulence of pertactin-negative Bordetella pertussis isolates from infants, France. Emerg Infect Dis 19(3):471-474.
56. Crossley K, Irvine P, Warren JB, Lee BK, Mead K (1979) Tetanus and diphtheria immunity in urban Minnesota adults. JAMA 242(21): 2298-2300.
57. Jenkinson D (1988) Duration of effectiveness of pertussis vaccine: Evidence from a 10 year community study. Br Med J (Clin Res Ed) 296(6622):612-614.
58. Gordon YC, et al. (2006) Effect of different forms of adenylate cyclase toxin on Bordetella pertussis on protection afforded by an acellular pertussis vaccine in a murine model. Infect Immun 74:6799-6805.
59. Roberts R, et al. (2008) Outer membrane vesicles as acellular vaccine against pertussis. Vaccine 26(36):4639-4646.
60. Meade BD, Kind PD, Ewell JB, McGrath PP, Manclark CR (1984) In vitro inhibition of murine macrophage migration by Bordetella pertussis lymphocytosis-promoting factor. Infect Immun 45(3): 718-725.
61. Schneerson R, Robbins JB, Taranger J, Lagergard T, Trollfors B (1996) A toxoid vaccine for pertussis as well as for diphtheria? Lancet 348(9037):1289-1292.
62. Trollfors B, et al. (1998) Immunization of children with pertussis toxoid decreases spread of pertussis within the family. Pediatr Infect Dis J 17(3):196-199.
63. Rappuoli R (1999) The vaccine containing recombinant pertussis toxin induces early and long-lasting immunity. Biologicals 27(2): 98-102.
64. Robbins JB, et al. (2007) The rise in pertussis cases urges replacement of chemically-inactivated with genetically-inactivated toxoid for DTP. Vaccine 25(15):2811-2816.
65. Taranger J, et al. (2001) Mass vaccination of children with pertussis toxoid-decreased incidence in both vaccinated and nonvaccinated persons. Clin Infect Dis 33(7):1004-1010.
66. Le T, et al.; APERT Study (2004) Immune responses and antibody decay after immunization of adolescents and adults with an acellular pertussis vaccine: The APERT Study. J Infect Dis 190(3):535-544.
67. Trollfors B, Dotevall L, Sundh V, Welinder-Olsson C (2011) Pertussis after end of a mass vaccination project-End of the "vaccination honey-moon" Vaccine 29(13):2444-2450.
68. Heininger U, Cherry JD, Stehr K (2004) Serologic response and antibody-titer decay in adults with pertussis. Clin Infect Dis 38(4): 591-594.
69. Weiss AA, et al. (2004) Acellular pertussis vaccines and complement killing of Bordetella pertussis. Infect Immun 72(12): 7346-7351.
70. Watson DC, Robbins JB, Szu SC (1992) Protection of mice against Salmonella typhimurium with an O-specific polysaccharide-protein conjugate vaccine. Infect Immun 60(11):4679-4686.
71. Cohen D, et al. (1997) Double-blind vaccine-controlled randomised efficacy trial of an investigational Shigella sonnei conjugate vaccine in young adults. Lancet 349(9046):155-159.
72. Passwell JH, et al.; Israeli Shigella Study Group (2010) Age-related efficacy of Shigella O-specific polysaccharide conjugates in 1-4-yearold Israeli children. Vaccine 28(10):2231-2235.
73. Claesson BA, et al. (2005) Antibodies against Haemophilus influenzae type b capsular polysaccharide and tetanus toxoid before and after a booster dose of the carrier protein nine years after primary vaccination with a protein conjugate vaccine. Pediatr Infect Dis J 24(5):463-464.
74. Myerowitz RL, Gordon RE, Robbins JB (1973) Polysaccharides of the genus Bacillus cross-reactive with the capsular polysaccharides of Diplococcus pneumoniae type 3, Haemophilus influenzae type b, and Neisseria meningitidis group A. Infect Immun 8(6):896-900.
75. Caroff M, et al. (2001) Structural variability and originality of the Bordetella endotoxins. J Endotoxin Res 7(1):63-68.
76. Peppler MS (1984) Two physically and serologically distinct lipopolysaccharide profiles in strains of Bordetella pertussis and their phenotype variants. Infect Immun 43(1):224-232.
77. Preston A, et al. (2006) Complete structures of Bordetella bronchiseptica and Bordetella parapertussis lipopolysaccharides. J Biol Chem 281(26):18135-18144.
78. Trollfors B, et al. (2001) Serum immunoglobulin G antibody responses to Bordetella pertussis lipooligosaccharide and B. parapertussis lipopolysaccharide in children with pertussis and parapertussis. Clin Diagn Lab Immunol 8(5):1015-1017.
79. Weingart CL, Keitel WA, Edwards KM, Weiss AA (2000) Characterization of bactericidal immune responses following vaccination with acellular pertussis vaccines in adults. Infect Immun 68(12):7175-7179.
80. Mountzouros KT, Kimura A, Cowell JL (1992) A bactericidal monoclonal antibody specific for the lipooligosaccharide of Bordetella pertussis reduces colonization of the respiratory tract of mice after aerosol infection with B. pertussis. Infect Immun 60(12): 5316-5318.
81. Archambault D, Rondeau P, Martin D, Broudeur BR (1991) Characterization and comparative bactericidal activity of monoclonal antibodies to Bordetella pertussis lipooligosaccharide A. J Gen Micro 137(4):905-911.
82. Shahin RD, Hamel J, Leef MF, Brodeur BR (1994) Analysis of protective and nonprotective monoclonal antibodies specific for Bordetella pertussis lipooligosaccharide. Infect Immun 62(2): 722-725.
83. Weiss AA, Mobberley PS, Fernandez RC, Mink CM (1999) Characterization of human bactericidal antibodies to Bordetella pertussis. Infect Immun 67(3):1424-1431.
84. Kubler-Kielb J, Pozsgay V (2005) A new method for conjugation of carbohydrates to proteins using an aminooxy-thiol heterobifunctional linker. J Org Chem 70(17):6987-6990.
85. Kubler-Kielb J, et al. (2008) Saccharide/protein conjugate vaccines for Bordetella species: Preparation of saccharide, development of new conjugation procedures, and physico-chemical and immunological characterization of the conjugates. Vaccine 26(29-30):3587-3593.
86. Kubler-Kielb J, et al. (2011) Oligosaccharide conjugates of Bordetella pertussis and bronchiseptica induce bactericidal antibodies, an addition to pertussis vaccine. Proc Natl Acad Sci USA 108(10):4087-4092.
87. Schneerson R, et al. (1992) Synthesis of a conjugate vaccine composed of pneumococcus type 14 capsular polysaccharide bound to pertussis toxin. Infect Immun 60(9):3528-3532.