Are vaccination programs and isolate polymorphism linked to pertussis re-emergence?

Expert Review of Vaccines

Volumn 4, Issue 5, 2005, Pages 757-778

  Godfroid, Fabrice ^b   Denoël, Philippe ^b   Poolman, Jan ^a,b  

^a SmithKline Beecham Biologicals   (Belgium)

^b GLAXOSMITHKLINE BIOLOGICALS   (Belgium)

Author keywords

Bordetella pertussis; Changes in epidemiology; DTPa; DTPw; Isolates polymorphism; Re emergence; Vaccine; Waning immunity

Indexed keywords

FIMBRIA PROTEIN; FIMBRIAE2 PROTEIN; FIMBRIAE3 PROTEIN; PERTACTIN; PERTUSSIS TOXIN; PERTUSSIS VACCINE; T CELL FACTOR PROTEIN; UNCLASSIFIED DRUG;

ALLELE; BACTERIAL STRAIN; BACTERIAL TRANSMISSION; BORDETELLA PERTUSSIS; CANADA; DNA FINGERPRINTING; DNA POLYMORPHISM; FIMBRIA; FINLAND; FRANCE; GENETIC VARIABILITY; GERMANY; HUMAN; IMMUNITY; ITALY; JAPAN; NETHERLANDS; NEUROLOGIC DISEASE; PERTUSSIS; POLAND; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PULSED FIELD GEL ELECTROPHORESIS; REVIEW; RUSSIAN FEDERATION; SWEDEN; TANDEM REPEAT; UNITED KINGDOM; UNITED STATES; VACCINATION;

EID: 27444442408     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/14760584.4.5.757     Document Type: Review

References (94)

1. Jefferson T, Rudin M, DiPietrantonj C. Systematic review of the effects of pertussis vaccines in children. Vaccine 21(17-18), 2003-2014 (2003). Systematic review of studies assessing the efficacy and safety of diptheria-tetanus-pertussis (DTP) vaccines.
2. de Melker HE, Schellekens JFP, Neppelenbroek SE, Mooi FR, Rümke HC, Conyn-van Spaendonck MAE. Reemergence of pertussis in the highly vaccinated population of the Netherlands: observations on surveillance data. Emerg. Infect. Dis. 6(4), 348-357 (2000).
3. Guris D, Strebel PM, Bardenheier B et al. Changing epidemiology of pertussis in the United States: increasing reported incidence among adolescents and adults, 1990-1996. Clin. Infect. Dis. 28(6), 1230-1237 (1999).
4. Mooi FR, van Loo IHM, King AJ. Adaptation of Bordetella pertussis to vaccination: A cause for its reemergence? Emerg. Infect. Dis. 7(Suppl. 3), 526-528 (2001).
5. Bass JW, Wittier RR. Return of epidemic pertussis in the United States. Pediatr. Infect. Dis. J. 13(5), 343-345 (1994).
6. Bentsi-Enchill AD, Halperin SA, Scott J, MacIsaac K, Duclos P. Estimates of the effectiveness of a whole-cell pertussis vaccine from an outbreak in an immunized population. Vaccine 15(3), 301-306 (1997).
7. DeSerres G, Boulianne N, Duval B et al. Effectiveness of a whole cell pertussis vaccine in child-care centers and schools. Pediatr. Infect. Dis. J. 15(6), 519-524 (1996).
8. Halperin SA, Bortolussi R, MacLean D, Chisholm N. Persistence of pertussis in an immunized population: results of the Nova Scotia Enhanced Pertussis Surveillance Program. J. Pediatr. 115(5 Pt. 1), 686-693 (1989).
9. Baron S, Njamkepo E, Grimprel E et al. Epidemiology of pertussis in French hospitals in 1993 and 1994: thirty years after a routine use of vaccination. Pediatr. Infect. Dis. J. 17(5), 412-418 (1998).
10. Van Buynder PG, Owen D, Vurdien JE, Andrews NJ, Matthews RC, Miller E. Bordetella pertussis surveillance in England and Wales: 1995-7. Epidemiol. Infect. 123(3), 403-411 (1999).
11. Wirsing von König CH, Halperin S, Riffelmann M, Guiso N. Pertussis of adults and infants. Lancet Infect. Dis. 2(12), 744-750 (2002). Review on current epidemiology of pertussis.
12. Gilberg S, Njamkepo E, Parent du Chatelet I et al. Evidence of Bordetella pertussis infection in adults presenting with persistent cough in a French area with very high whole-cell vaccine coverage. J. Infect. Dis. 186(3), 415-418 (2002).
13. Skowronski DM, De Serres G, MacDonald D et al. The changing age and seasonal profile of pertussis in Canada. J. Infect. Dis. 185(10), 1448-1453 (2002).
14. Groseclose SL, Brathwaite WS, Hall PA et al. Summary of notifiable diseases - United States, 2002. Morb. Mortal. Wkly Rep. 51(53), 1-84 (2004).
15. Mooi FR, van Oirschot H, Heuvelman K, van der Heide HGJ, Gaastra W, Willems RJL. Polymorphism in the Bordetella pertussis virulence factors P.69/pertactin and pertussis toxin in The Netherlands: temporal trends and evidence for vaccine-driven evolution. Infect. Immun. 66(2), 670-675 (1998).
16. Mooi FR, Hallander H, Wirsing von König CH, Hoet B, Guiso N. Epidemiological typing of Bordetella pertussis isolates: recommendations for a standard methodology. Eur. J. Clin. Microbiol. Infect. Dis. 19(3), 174-181 (2000).
17. Schouls LM, van der Heide HGJ, Vauterin L, Vauterin P, Mooi FR. Multiple-locus variable-number tandem repeat analysis of Dutch Bordetella pertussis strains reveals rapid genetic changes with clonal expansion during the late 1990s. J. Bacteriol. 186(16), 5496-5505 (2004).
18. King AJ, Berbers G, van Oirschot LM, Hoogerhout P, Knipping K, Mooi FR. Role of the polymorphic region 1 of the Bordetella pertussis protein pertactin in immunity. Microbiology 147(Pt. 11), 2885-2895 (2001).
19. van Loo IHM, Heuvelman KJ, King AJ, Mooi FR. Multilocus sequence typing of Bordetella pertussis based on surface protein genes. J. Clin. Microbiol. 40(6), 1994-2001 (2002).
20. Van Amersfoorth SCM, Schouls LM, van der Heide HGJ et al. Analysis of Bordetella pertussis populations in European countries with different vaccination policies. J. Clin. Microbiol. 43(6), 2837-2843 (2005). Recent evaluation of Bordetella pertussis polymorphism in different European countries.
21. Packard ER, Parton R, Coote JG, Fry NK. Sequence variation and conservation in virulence-related genes of Bordetella pertussis isolates from the UK. J. Med. Microbiol. 53(Pt. 5), 355-365 (2004).
22. Tsang RSW, Lau AKH, Sill ML et al. Polymorphisms of the fimbria fim3 gene of Bordetella pertussis strains isolated in Canada. J. Clin. Microbiol. 42(11), 5364-5367 (2004).
23. Caro V, Njamkepo E, Van Amersfoorth SCM et al. Pulsed-field gel electrophoresis analysis of Bordetella pertussis populations in various European countries with different vaccine policies. Microb. Infect. 7(7-8), 976-982 (2005). Recent evaluation of B. pertussis polymorphism in different European countries.
24. Carbonetti NH, Artamonova GV, Mays RM, Worthington ZEV. Pertussis toxin plays an early role in respiratory tract colonization by Bordetella pertussis. Infect. Immun. 71(11), 6358-6366 (2003).
25. Katada T, Tamura M, Ui M. The A protomer of islet-activating protein, pertussis toxin, as an active peptide catalyzing ADP-ribosylation of a membrane protein. Arch. Biochem. Biophys. 224(1), 290-298 (1983).
26. Moss J, Stanley SJ, Burns DL et al. Activation by thiol of the latent NAD glycohydrolase and ADP-ribosyltransferase activities of Bordetella pertussis toxin (islet-activating protein). J. Biol. Chem. 258(19), 11879-11882 (1983).
27. Brennan MJ, Li ZM, Cowell JL et al. Identification of a 69-kilodalton nonfimbrial protein as an agglutinogen of Bordetella pertussis. Infect. Immun. 56(12), 3189-3195 (1988).
28. Witvliet MH, Burns DL, Brennan MJ, Poolman JT, Manclark CR. Binding of pertussis toxin to eucaryotic cells and glycoproteins. Infect. Immun. 57(11), 3324-3330 (1989).
29. Hausman SZ, Burns DL. Use of pertussis toxin encoded by ptx genes from Bordetella bronchiseptica to model the effects of antigenic drift of pertussis toxin on antibody neutralization. Infect. Immun. 68(6), 3763-3767 (2000).
30. Charles IG, Dougan G, Pickard D et al. Molecular cloning and characterization of protective outer membrane protein P.69 from Bordetella pertussis. Proc. Natl Acad. Sci. USA 86(10), 3554-3558 (1989).
31. Leininger E, Roberts M, Kenimer JG et al. Pertactin, an Arg-Gly-Asp-containing Bordetella pertussis surface protein that promotes adherence of mammalian cells. Proc. Natl Acad. Sci. USA 88(2), 345-349 (1991).
32. Leininger E, Ewanowich CA, Bhargava A, Peppler MS, Kenimer JG, Brennan MJ. Comparative roles of the Arg-Gly-Asp sequence present in the Bordetella pertussis adhesins pertactin and filamentous hemagglutinin. Infect. Immun. 60(6), 2380-2385 (1992).
33. Bassinet L, Gueirard P, Maitre B, Housset B, Gounon P, Guiso N. Role of adhesins and toxins in invasion of human tracheal epithelial cells by Bordetella pertussis. Infect. Immun. 68(4), 1934-1941 (2000).
34. Emsley P, Charles IG, Fairweather NF, Isaacs NW. Structure of Bordetella pertussis virulence factor P.69 pertactin. Nature 381(6577), 90-92 (1996).
35. Muyldermans G, Pierard D, Hoebrekx N et al. Simple algorithm for identification of Bordetella pertussis pertactin gene variants. J. Clin. Microbiol. 42(4), 1614-1619 (2004).
36. Boursaux-Eude C, Guiso N. Polymorphism of repeated regions of pertactin in Bordetella pertussis, Bordetella parapertussis, and Bordetella bronchiseptica. Infect. Immun. 68(8), 4815-4817 (2000).
37. Register KB. Novel genetic and phenotypic heterogeneity in Bordetella bronchiseptica pertactin. Infect. Immun. 69(3), 1917-1921 (2001).
38. Hijnen M, Mooi FR, van Gageldonk PGM, Hoogerhout P, King AJ, Berbers GAM. Epitope structure of the Bordetella pertussis protein P.69 pertactin, a major vaccine component and protective antigen. Infect. Immun. 72(7), 3716-3723 (2004).
39. Geuijen CAW, Willems RJL, Mooi FR. The major fimbrial subunit of Bordetella pertussis binds to sulfated sugars. Infect. Immun. 64(7), 2657-2665 (1996).
40. Hazenbos WL, Geuijen CA, van den Berg BM, Mooi FR, van Furth R. Bordetella pertussis fimbriae bind to human monocytes via the minor fimbrial subunit FimD. J. Infect. Dis. 171(4), 924-929 (1995).
41. Steven AC, Bisher ME, Trus BL, Thomas D, Zhang JM, Cowell JL. Helical structure of Bordetella pertussis fimbriae. J. Bacteriol. 167(3), 968-974 (1986).
42. Geuijen CAW, Willems RJL, Bongaerts M, Top J, Gielen H, Mooi FR. Role of the Bordetella pertussis minor fimbrial subunit, FimD, in colonization of the mouse respiratory tract. Infect. Immun. 65(10), 4222-4228 (1997).
43. Ashworth LAE, Irons LI, Dowsett AB. Antigenic relationship between serotype-specific agglutinogen and fimbriae of Bordetella pertussis. Infect. Immun. 37(3), 1278-1281 (1982).
44. Livey I, Duggleby CJ, Robinson A. Cloning and nucleotide sequence analysis of the serotype 2 fimbrial subunit gene of Bordetella pertussis. Mol. Microbiol. 1(2), 203-209 (1987).
45. Mooi FR, ter Avest A, van der Heide HGJ. Structure of the Bordetella pertussis gene coding for the serotype 3 fimbrial subunit. FEMS Microbiol Lett. 66(1-3), 327-331 (1990).
46. Njamkepo E, Rimlinger F, Thiberge S, Guiso N. Thirty-five years' experience with the whole-cell pertussis vaccine in France: vaccine strains analysis and immunogenicity. Vaccine 20(9-10), 1290-1294 (2002). Link between consistent vaccine effectiveness and lack of epidemics in France.
47. Grimprel E, Bégué P, Anjak I, Njamkepo E, François P, Guiso N. Long-term human serum antibody responses after immunization with whole-cell pertussis vaccine in France. Clin. Diagn. Lab. Immunol. 3(1), 93-97 (1996).
48. Weber C, Boursaux-Eude C, Coralie G, Caro V, Guiso N. Polymorphism of Bordetella pertussis isolates circulating for the last 10 years in France, where a single effective whole-cell vaccine has been used for more than 30 years. J. Clin. Microbiol. 39(12), 4396-4403 (2001).
49. Cohen HH. Development of pertussis vaccine production and control in the National Institute of Public Health in the Netherlands during the years 1950-1962. Antonie Van Leeuwenhoek 29, 183-201 (1963).
50. de Melker HE, Conyn-van Spaendonck MAE, Rumke HC, van Wijngaarden JK, Mooi FR, Schellekens JFP. Pertussis in the Netherlands: an outbreak despite high levels of immunization with whole-cell vaccine. Emerg. Infect. Dis. 3(2), 175-178 (1997).
51. van Loo IHM, van der Heide HGJ, Nagelkerke NJD, Verhoef J, Mooi FR. Temporal trends in the population structure of Bordetella pertussis during 1949-1996 in a highly vaccinated population. J. Infect. Dis. 179(4), 915-923 (1999).
52. van Der Zee A, Vernooij S, Peeters M, van Embden J, Mooi FR. Dynamics of the population structure of Bordetella pertussis as measured by IS1002-associated RFLP: comparison of pre- and post- vaccination strains and global distribution. Microbiology 142(Pt. 12), 3479-3485 (1996).
53. van Loo IHM, Mooi FR. Changes in the Dutch Bordetella pertussis population in the first 20 years after the introduction of whole-cell vaccines. Microbiology 148(Pt. 7), 2011-2018 (2002).
54. Gustafsson L, Hallander HO, Olin P, Reizenstein E, Storsaeter J. A controlled trial of a two-component acellular, a five-component acellular, and a whole-cell pertussis vaccine. N. Engl. J. Med. 334(6), 349-355 (1996).
55. de Moissac YR, Ronald SL, Peppler MS. Use of pulsed-field gel electrophoresis for epidemiological study of Bordetella pertussis in a whooping cough outbreak. J. Clin. Microbiol. 32(2), 398-402 (1994).
56. Peppler MS, Kuny S, Nevesinjac A et al. Strain variation among Bordetella pertussis isolates from Quéec and Alberta provinces of Canada from 1985 to 1994. J. Clin. Microbiol. 41(7), 3344-3347 (2003).
57. De Serres G, Shadmani R, Boulianne N et al. Effectiveness of a single dose of acellular pertussis vaccine to prevent pertussis in children primed with pertussis whole cell vaccine. Vaccine 19(20-22), 3004-3008 (2001).
58. Hopkins RS, Jajosky RA, Hall PA et al. Summary of notifiable diseases - United States, 2003. Morb. Mortal Wkly Rep. 52(54), 1-85 (2005).
59. Brennan M, Strebel P, George H et al. Evidence for transmission of pertussis in schools, Massachusetts, 1996: epidemiologic data supported by pulsed-field gel electrophoresis studies. J. Infect. Dis. 181(1), 210-215 (2000).
60. Bisgard KM, Christie CDC, Reising SF et al. Molecular epidemiology of Bordetella pertussis by pulsed-field gel electrophoresis profile: Cincinnati, 1989-1996. J. Infect. Dis. 183(9), 1360-1367 (2001).
61. Hardwick TH, Cassiday P, Weyant RS, Bisgard KM, Sanden GN. Changes in predominance and diversity of genomic subtypes of Bordetella pertussis isolated in the United States, 1935 to 1999. Emerg. Infect. Dis. 8(1), 44-49 (2002).
62. Cassiday P, Sanden G, Heuvelman K, Mooi F, Bisgard KM, Popovic T. Polymorphism in Bordetella pertussis pertactin and pertussis toxin virulence factors in the United States, 1935-1999. J. Infect. Dis. 182(5), 1402-1408 (2000).
63. Cherry JD, Grimprel E, Guiso N, Heininger U, Mertsola J. Defining pertussis epidemiology: clinical, microbiologic and serologic perspectives. Pediatr. Infect. Dis. J. 24(Suppl. 5), S25-S34 (2005). Recent view of pertussis epidemiology and potential impact of booster dose introduction.
64. Therre H, Baron S. Pertussis immunisation in Europe - the situation in late 1999. Euro. Surveill. 5(1), 6-10 (2000).
65. Fine PE, Clarkson JA. Distribution of immunity to pertussis in the population of England and Wales. J. Hyg. 92(1), 21-36 (1984).
66. Fry NK, Neal S, Harrison TG, Miller E, Matthews R, George RC. Genotypic variation in the Bordetella pertussis virulence factors pertactin and pertussis toxin in historical and recent clinical isolates in the United Kingdom. Infect. Immun. 69(9), 5520-5528 (2001).
67. Preston NW, Carter EJ. Serotype specificity of vaccine-induced immunity to pertussis. Commun. Dis. Rep. Rev. 2(13), R155-R156 (1992).
68. Gzyl A, Augustynowicz E, Rabczenko D, Gniadek G, Slusarczyk J. Pertussis in Poland. Int. J. Epidemiol. 33(2), 358-365 (2004).
69. Gzyl A, Augustynowicz E, van Loo I, Slusarczyk J. Temporal nucleotide changes in pertactin and pertussis toxin genes in Bordetella pertussis strains isolated from clinical cases in Poland. Vaccine 20(3-4), 299-303 (2001).
70. Gzyl A, Augustynowicz E, Gniadek G, Rabczenko D, Dulny G, Slusarczyk J. Sequence variation in pertussis S1 subunit toxin and pertussis genes in Bordetella pertussis strains used for the whole-cell pertussis vaccine produced in Poland since 1960L. Efficiency of the DTwP vaccine-induced immunity against currently circulating B. pertussis isolates. Vaccine 22(17-18), 2122-2128 (2004).
71. Kourova N, Caro V, Weber C et al. Comparison of the Bordetella pertussis and Bordetella parapertussis isolates circulating in Saint Petersburg between 1998 and 2000 with Russian vaccine strains. J. Clin. Microbiol. 41(8), 3706-3711 (2003).
72. Sato Y, Kimura M, Fukumi H. Development of a pertussis component vaccine in Japan. Lancet (8369), 122-126 (1984).
73. Kato T. Pertussis vaccine in Japan. J. Infect. Chemother. 5(4), 185-189 (1999).
74. Kuno-Sakai H, Kimura M. Safety and efficacy of acellular pertussis vaccine in Japan, evaluated by 23 years of its use for routine immunization. Pediatr. Int. 46(6), 650-655 (2004).
75. Guiso N, Boursaux-Eude C, Weber C et al. Analysis of Bordetella pertussis isolates collected in Japan before and after introduction of acellular pertussis vaccines. Vaccine 19(23-24), 3248-3252 (2001).
76. Kodama A, Kamachi K, Horiuchi Y, Konda T, Arakawa Y. Antigenic divergence suggested by correlation between antigenic variation and pulsed-field gel electrophoresis profiles of Bordetella pertussis isolates in Japan. J. Clin. Microbiol. 42(12), 5453-5457 (2004).
77. Liese JG, Renner C, Stojanov S, Belohradsky BH. Clinical and epidemiological picture of B. pertussis and B. parapertussis infections after introduction of acellular pertussis vaccines. Arch. Dis. Child 88(8), 684-687 (2003).
78. Heininger U, Frei R, Cherry JD, Stehr K. Comparison of pulsed field gel electrophoresis patterns of Bordetella pertussis isolates from unvaccinated children with severe or mild pertussis. Pediatr. Infect. Dis. J. 23(3), 211-217 (2004).
79. Olin P, Gustafsson L, Barreto L et al. Declining pertussis incidence in Sweden following the introduction of acellular pertussis vaccine. Vaccine 21(17-18), 2015-2021 (2003).
80. Hallander HO, Advani A, Donnelly D, Gustafsson L, Carlson RM. Shifts of Bordetella pertussis variants in Sweden from 1970 to 2003, during three periods marked by different vaccination programs. J. Clin. Microbiol. 43(6), 2856-2865 (2005).
81. Greco D, Salmaso S, Mastrantonio P et al. A controlled trial of two acellular vaccines and one whole-cell vaccine against pertussis. Progetto Pertosse Working Group. N. Engl. J. Med. 334(6), 341-348 (1996).
82. Mastrantonio P, Spigaglia P, van Oirschot H et al. Antigenic variants in Bordetella pertussis strains isolated from vaccinated and unvaccinated children. Microbiology 145(Pt 8), 2069-2075 (1999).
83. Stefanelli P, De Marzi L, Robino L et al. Characterization of Bordetella pertussis strains of recent isolation. New Microbiol. 22(3), 187-194 (1999).
84. Lévy-Bruhl D, Pebody R, Veldhuijzen I, Valenciano M, Osborne K. ESEN: a comparison of vaccination programmes - part two: pertussis. Euro. Surveillance 3(11), 107-110 (1998).
85. Mooi FR, He Q, van Oirschot H, Mertsola J. Variation in the Bordetella pertussis virulence factors pertussis toxin and pertactin in vaccine strains and clinical isolates in Finland. Infect. Immun. 67(6), 3133-3134 (1999).
86. Lee YS, Yang CY, Lu CH, Tseng YH. Molecular epidemiology of Bordetella pertussis isolated in Taiwan, 1992-1997. Microbiol. Immunol. 47(12), 903-909 (2003).
87. Boursaux-Eude C, Thiberge S, Carletti G, Guiso N. Intranasal murine model of Bordetella pertussis infection: II. Sequence variation and protection induced by a tricomponent acellular vaccine. Vaccine 17(20-21), 2651-2660 (1999).
88. Denoël P, Godfroid F, Guiso N, Hallander H, Poolman J. Comparison of acellular pertussis vaccines-induced immunity against infection due to Bordetella pertussis variant isolates in a mouse model. Vaccine (In Press) (2005).
89. Wendelboe AM, Van Rie A, Salmaso S, Englund JA. Duration of immunity against pertussis after natural infection or vaccination. Pediatr. Infect. Dis. J. 24(5), S58-S61 (2005).
90. Taranger J, Trollfors B, Bergfors E et al. Mass vaccination of children with pertussis toxoid-decreased incidence in both vaccinated and nonvaccinated persons. Clin. Infect. Dis. 33(7), 1004-1010 (2001).
91. Forsyth KD, Campins-Marti M, Caro J et al. New pertussis vaccination strategies beyond infancy: recommendations by the Global Pertussis Initiative. Clin. Infect. Dis. 39(12), 1802-1809 (2004). Recommendation of the introduction of booster immunization.
92. De Schutter I, Malfroot A, Dab I et al. Molecular typing of Bordetella pertussis isolates recovered from Belgian children and their household members. Clin. Infect. Dis. 36(11), 1391-1396 (2003).
93. Muyldermans G, Hoebrekx N, Soetens O et al. Polymorphism of Belgian Bordetella pertussis isolates. J. Microbiol. Methods 47(1), 108 (2001).
94. Wang J, Yang Y, Li J et al. Infantile pertussis rediscovered in China. Emerg. Infect. Dis. 8(8), 859-861 (2002).