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Antigenic variability of Bordetella pertussis strains isolated in 1967–2010 in the Czech Republic – possible explanation for the rise in cases of pertussis?


Authors: J. Zavadilová 1;  D. Lžičařová 1;  M. Musílek 1;  P. Křížová 1;  K. Fabiánová 1,2
Authors‘ workplace: Centrum epidemiologie a mikrobiologie, Státní zdravotní ústav, Praha 1;  Ústav epidemiologie, 3. LF UK, Praha 2
Published in: Epidemiol. Mikrobiol. Imunol. 64, 2015, č. 3, s. 130-138
Category: Original Papers

Overview

Objective:
Comparison of antigenic structures of Bordetella pertussis (B. pertussis) strains isolated from 1967 to 2010 in the Czech Republic.

Material and methods:
Seventy strains of B. pertussis were referred to the National Reference Laboratory (NRL) for Pertussis and Diphtheria within the surveillance of pertussis from all over the Czech Republic (CR) between 1967 and 2010. To study the strains, the analysis was performed of the genome sequences encoding the surface immunogenic structures – the pertussis toxin S1 subunit gene (ptxA), pertactin gene region 1 (prnA), type 3 fimbriae gene (fim3) – and pertussis toxin promoter (ptxP) responsible for the regulation of the production of pertussis toxin.

Results:
For the study set of B. pertussis strains, the sequencing analysis revealed changes in all genomic regions studied. The isolates from three periods differ in the allelic profile. In period I (1967−1978) with the use of whole cell pertussis vaccine (wP), the following two profiles were the most common: ptxP(1), ptxA(2), prnA(1), fim3(1) and ptxP(1), ptxA(1), prnA(3), fim3(1). In period 2 (1990−2007) with the switch to acellular pertussis vaccine (aP), the most common profile was: ptxP(3), ptxA(1), prnA(2), fim3(2). Period 3 (2008−2010) with the use of aP was characterized by the predominance of the following two profiles which had never been found in period 1: ptxP(3), ptxA(1), prnA(2), fim3(2) and ptxP(3) ptxA(1), prnA(2), fim3(1).

Conclusions:
Sequencing of the genomic regions ptxP, ptxA, prnA, and fim3 of B. pertussis strains isolated in the CR between 1967 and 2010 confirmed changes in the allelic variants of these regions. The incidence of strains carrying the new allelic variants was increasing after 1995 at the expense of those carrying the original variants. The study results can be interpreted as a partial genetic escape of pathogenic strains of B. pertussis beyond the reach of the pertussis vaccines.

Keywords:
Bordetella pertussis strain – isolate – sequencing – epidemiology – vaccine


Sources

1. Resurgence of pertussis – United States, 1993, Morb Mortal Wkly Rep, 1993;42(49):952–953.

2. Milord F. Resurgence of pertussis in Montérégie, Quebec – 1990–1994. Can Commun Dis Rep, 1995;21(5):40–44.

3. Poynten M, McIntyre PB, Mooi FR, et al. Temporal trends in circulating Bordetella pertussis strains in Australia. Epidemiol Infect, 2004;132(2):185–193.

4. Celentano LP, Massari M, Paramatti D, et al. Resurgence of pertussis in Europe. Pediatr Infect Dis J, 2005;24(9):761–765.

5. Gonçalves G, Machado E, Gouveia E, et al. Resurgence of pertussis in northern Portugal: two severe cases in very young children. Euro Surveill, 2005;10(25):pii=2731 [online]. [cit. 2014–11–14]. Dostupný na www: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=2731.

6. Grilc E, Pirnat N. Pertussis outbreak in recently vaccinated children in a kindergarten in Ljubljana during a resurgence in pertussis incidence. Euro Surveill, 2005;10(33):pii=2779 [online]. [cit. 2010–08–05]. Dostupný na www: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=2779.

7. de Melker HE, Conyn-van Spaendock MA, Rümke HC, et al. Pertussis in The Netherlands: an outbreak despite high levels of immunization with whole-cell vaccine. Emerg Infect Dis, 1997;3(2):175–178.

8. Gzyl A, Augustynowicz E, Rabczenko D, et al. Pertussis in Poland. Int J Epidemiol, 2004;33(2):358–365.

9. Gustafsson L, Hessel L, Storsaeter J, et al. Long-term follow-up of Swedish children vaccinated with acellular pertussis vaccines at 3, 5, and 12 months of age indicates the need for a booster dose at 5 to 7 years of age. Pediatrics, 2006;118(3):978–984.

10. Dlhý J. Administrativní kontrola proočkovanosti v České republice k datu 31. 12. 2010. Zprávy Centra epidemiologie a mikrobiologie, SZÚ, Praha, 2012; 21(3):92–97.

11. Bass JW, Stephenson SR. The return of pertussis. Pediatr Infect Dis J, 1987;6(2):141–44.

12. Lam C, Octavia S, Bahrame Z, et al. Selection and emergence of pertussis toxin promoter ptxP3 allele in the evolution of Bordetella pertussis. Infect Genet Evol, 2012;12(2):492–495.

13. Mattoo S, Cherry JD. Molecular pathogenesis, epidemiology, and clinical manifestations of respiratoty infections due to Bordetella pertussis and other Bordetella subspecies. Clin Microbiol Rev, 2005;18(2):326–382.

14. Melvin JA, Scheller EV, Miller JF, et al. Bordetella pertussis pathogenesis: current and future challenges. Nat Rev Microbiol, 2014;12(4):274–288.

15. Mooi FR. Bordetella pertussis and vaccination: the persistence of a genetically monomorphic pathogen. Infect Genet Evol, 2010;10(1):36–49.

16. Mooi FR, van Loo IH, van Gent M, et al. Bordetella pertussis strains with increased toxin production associated with pertussis resurgence. Emerg Infect Dis, 2009;15(8):1206–1213.

17. van Gent M, Bart MJ, van der Heide HG, et al. Small mutations in Bordetella pertussis are associated with selective sweeps. PLoS One, 2012;7(9):e46407 [online]. [cit. 2014–09–21]. Dostupný na www: http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0046407.

18. De Magistris MT, Di Tommaso A, Domenighini M et al. Interaction of the pertussis toxin peptide containing residues 30 – 42 with DRI and the T-cell receptors of 12 human T-cell clones. Proc Natl Acad Sci USA, 1992;89(7):2990–2994.

19. van Loo IHM, Heuvelman KJ, King AJ, et al. Multilocus Sequence Typing of Bordetella pertussis based on surface protein genes. J Clin Microbiol, 2002;40(6):1994–2001.

20. Cherry JD, Paddock CD. Pathogenesis and histopathology of pertussis: Implications for vaccination. Expert Rev Vaccines, 2014; 13(9):1115–1123.

21. Paddock CD, Sanden GN, Cherry JD, et al. Pathology and pathogenesis of fatal Bordetella pertussis infection in infants. Clin Infect Dis, 2008;47(3):328–338.

22. Mooi FR, Hallander H, Wirsing von König CH, et al. Epidemiological typing of Bordetella pertussis isolates: recommendations for a standard methodology. Eur J Clin Microbiol Infect Dis, 2000;19(3):174–181.

23. He Q, Mäkinen J, Berbers G, et al. Bordetella pertussis protein pertactin induces type-specific antibodies: one possible explanation for the emergence of antigenic variants? J Infect Dis, 2003;187(8):1200–1205.

24. King AJ, Berbers G, van Oirschot, et al. Role of the polymorphic region 1 of the Bordetella pertussis protein pertactin in immunity. Microbiology, 2001;147(11):2885–2895.

25. van Gent M, de Greef SC, van der Heide HG, et al. An investigation into the cause of the 1983 whooping cough epidemic in the Netherlands. Vaccine, 2009;27(13):1898–1903.

26. Litt DJ, Neal SE, Fry NK. Changes in genetic diversity of the Bordetella pertussis population in the United Kingdom between 1920 and 2006 reflect vaccination coverage and emergence of a single dominant clonal type. J Clin Microbiol, 2009;47(3):680–688.

27. Van Loo IH, Mooi FR. Changes in the Dutch Bordetella pertussis population in the first 20 years after the introduction of whole-cell vaccines. Microbiology, 2002;148(7):2011–218.

28. Bouchez V, Brun D, Cantinelli T, et al. First report and detailed characterization of B. pertussis isolates not expressing Pertussis Toxin or Pertactin. Vaccine, 2009;27(43):6034–6041.

29. Lam C, Octavia S., Rifacort L, et al. Rapid increase in pertactin-deficient Bordetella pertussis isolates, Australia. Emerg Infect Dis, 2014;20(4):626–633.

30. Otsuka N, Han HJ, Toyoizumi–Ajisaka H, et al. Prevalence and genetic characterization of pertactin – deficient Bordetella pertussis in Japan. PLoS One, 2012;7(2):e31985 [online]. [cit. 2012–02–14]. Dostupný na www: http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0031985.

31. Kallonen T, He Q. Bordetella pertussis strain variation and evolution postvaccination. Expert Rev Vaccines, 2009;8(7):863–875.

32. King Aj, van der Lee S, Mohangoo A, et al. Genome-wide gene expression analysis of Bordetella pertussis isolates associated with a resurgence in pertussis: elucidation of factors involved in the increased fitness of epidemic strains. PLoS One, 2013;8(6):e66150 [online]. [cit. 2013–06–11]. Dostupný na www: http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0066150.

33. Sealey KL, Harris SR, Fry NK, et al. Genomic analysis of isolates from the United Kingdom 2012 pertussis outbreak reveals that vaccine antigen genes are unusually fast evolving. J Infect Dis, 2014; pii: jiu665 [online]. [cit. 2014–12–08]. Dostupný na www: http://jid.oxfordjournals.org/content/early/2015/01/06/infdis.jiu665.long.

34. Berbers GA, de Greeff S, Mooi FR. Improving pertussis vaccination. Hum Vaccin, 2009;5(7):497–503.

35. Mooi FR, van Oirschot H, Heuvelman K, et al. 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, 1998;66(2):670–675.

36. Mooi FR, He Q, van Oirschot H, et al. Variation in the Bordetella pertussis virulence factors pertussis toxin and pertactin in vaccine strains and clinical isolates in Finland. Infect Immun, 1999;67(6):3133–3134.

37. Fry NK, Neal S, Harrison TG, et al. Genotypic variation in the Bordetella pertussis virulence factors pertactin and pertussis toxin in historical and recent clinical isolates in the United Kingdom. Infect Immun, 2001;69(9):5520–5528.

38. Hallander HO, Advani A, Donelly D, et al. Shifts of Bordetella pertussis variants in Sweden from 1970 to 2003, during three periods marked by different vaccination programs. J Clin Microbiol, 2005;43(6):2856–2865.

39. Bottero D, Gaillard ME, Fingermann M, et al. Pulsed-field gel electrophoresis, pertactin, pertussis toxin S1 subunit polymorphisms, and surfaceome analysis of vaccine and clinical Bordetella pertussis strains. Clin Vaccine Immunol, 2007;14(11):1490–1498.

40. Gzyl A, Augustynowicz E, van Loo I, et al. Temporal nucleotide changes in pertactin and pertussis toxin genes in Bordetella pertussis strains isolated from clinical cases in Poland. Vaccine, 2001;20(3–4):299–303.

41. Packard ER, Parton R, Coote JG, et al. Sequence variation and conservation in virulence-related genes of Bordetella pertussis isolates from the UK. J Med Microbiol, 2004;53(5):355–365.

42. Borisova O, Kombarova SY, Zakharova NS, et al. Antigenic divergence between Bordetella pertussis clinical isolates from Moscow, Russia, and vaccine strains. Clin Vaccine Immunol, 2007;14(3):234–238.

43. Cherry JD, Gornbein J, Heininger U, et al. A search for serologic correlates of immunity to Bordetella pertussis cough illnesses. Vaccine, 1998;16(20):1901–1906.

44. Taranger J, Trollfors B, Lagergård T, et al. Correlation between pertussis toxin IgG antibodies in postvaccination sera and subsequent protection against pertussis. J Infect Dis, 2000;181(3):1010–1013.

45. Advani A, Van der Heide HG, Hallander HO, et al. Analysis of Swedish Bordetella pertussis isolates with three typing methods: characterization of an epidemic lineage. J Microbiol Methods, 2009;78(3):297–301.

46. Diavatopoulos DA, Cummings CA, Schouls LM et al. Bordetella pertussis, the causative agent of whooping cough, evolved from a distinct, human-associated lineage of B. bronchiseptica. PLoS Pathog, 2005;1(4):e45 [online]. [cit. 2014–10–02]. Dostupný na www: http://journals.plos.org/plospathogens/article?id=10.1371/journal.ppat.0010045.

47. Bart MJ, Harris SR, Advani A, et al. Global population structure and evolution of Bordetella pertussis and their relationship with vaccination. Mbio, 2014;5(2):e01074 [online]. [cit. 2014–12–20]. Dostupný na www: http://mbio.asm.org/content/5/2/e01074-14.full.pdf+html.

48. Weber C, Boursaux-Eude C, Coralie G, et al. 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, 2001;39(12):4396–4403.

49. van Amersfoorth SC, Schouls LM, van der Heide HG et al. Analysis of Bordetella pertussis populations in European countries with different vaccination policies. J Clin Microbiol, 2005;43(6):2837–2843.

50. Octavia S, Maharjan RP, Sintchenko V, et al. Insight into evolution of Bordetella pertussis from comparative genomic analysis: evidence of vaccine-driven selection. Mol Biol Evol, 2011;28(1):707–715.

51. Tsang RS, Lau AK, Sill ML, et al. Polymorphisms of the fimbria fim3 gene of Bordetella pertussis strains isolated in Canada. J Clin Microbiol, 2004;42(11):5364–5367.

52. King AJ, van Gorkom T, Pennings JL, et al. Comparative genomic profiling of Dutch clinical Bordetella pertussis isolates using DNA microarrays: identification of genes absent from epidemic strains. BMC Genomics, 2008;9:311 [online]. [cit. 2012–03–25]. Dostupný na www: http://www.biomedcentral.com/1471-2164/9/311.

53. King AJ, van Gorkom T, van der Heide HG, et al. Changes in the genomic content of circulating Bordetella pertussis strains isolated from the Netherlands, Sweden, Japan and Australia: adaptive evolution or drift? BMC Genomics, 2010;11:64 [online]. [cit. 2012–03–25]. Dostupný na www: http://www.biomedcentral.com/1471-2164/11/64.

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