1887

Abstract

Purpose. Despite the long history of pertussis vaccination and high vaccination coverage in Poland and many other developed countries, pertussis incidence rates have increased substantially, making whooping cough one of the most prevalent vaccine-preventable diseases. Among the factors potentially involved in pertussis resurgence, the adaptation of the Bordetella pertussis population to country-specific vaccine-induced immunity through selection of non-vaccine-type strains still needs detailed studies.

Methodology. Multi-locus variable-number tandem repeat analysis (MLVA), also linked to MLST and PFGE profiling, was applied to trace the genetic changes in the B. pertussis population circulating in Poland in the period 1959–2013 versus country-specific vaccine strains.

Results. Generally, among 174 B. pertussis isolates, 31 MLVA types were detected, of which 11 were not described previously. The predominant MLVA types of recent isolates in Poland were different from those of the typical isolates circulating in other European countries. The MT27 type, currently predominant in Europe, was rarely seen and detected in only five isolates among all studied. The features of the vaccine strains used for production of the pertussis component of a national whole-cell diphtheria-tetanus-pertussis (DTP) vaccine, as studied by MLVA and MLST tools, were found to not match those observed in the currently circulating B. pertussis isolates in Poland.

Conclusions. Differences traced by MLVA in relation to the MLST and PFGE profiling confirmed that the B. pertussis strain types currently observed elsewhere in Europe, even if appearing in Poland, were not able to successfully disseminate within a human population in Poland that has been vaccinated with a whole-cell pertussis vaccine not used in other countries.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.000408
2017-06-09
2019-10-20
Loading full text...

Full text loading...

/deliver/fulltext/jmm/66/6/753.html?itemId=/content/journal/jmm/10.1099/jmm.0.000408&mimeType=html&fmt=ahah

References

  1. He Q, Mertsola J. Factors contributing to pertussis resurgence. Future Microbiol 2008;3:329–339 [CrossRef][PubMed]
    [Google Scholar]
  2. Mooi FR. Bordetella pertussis and vaccination: the persistence of a genetically monomorphic pathogen. Infect Genet Evol 2010;10:36–49 [CrossRef][PubMed]
    [Google Scholar]
  3. Mooi FR, van der Maas NA, de Melker HE. Pertussis resurgence: waning immunity and pathogen adaptation - two sides of the same coin. Epidemiol Infect 2014;142:1–10 [CrossRef][PubMed]
    [Google Scholar]
  4. Tan T, Dalby T, Forsyth K, Halperin SA, Heininger U et al. Pertussis across the globe: recent epidemiologic trends from 2000 to 2013. Pediatr Infect Dis J 2015;34:e222232 [CrossRef][PubMed]
    [Google Scholar]
  5. Mosiej E, Augustynowicz E, Zawadka M, Dabrowski W, Lutyńska A. Strain variation among Bordetella pertussis isolates circulating in Poland after 50 years of whole-cell pertussis vaccine use. J Clin Microbiol 2011;49:1452–1457 [CrossRef][PubMed]
    [Google Scholar]
  6. Gzyl A, Augustynowicz E, Rabczenko D, Gniadek G, Slusarczyk J. Pertussis in Poland. Int J Epidemiol 2004;33:358–365 [CrossRef][PubMed]
    [Google Scholar]
  7. Paradowska-Stankiewicz I, Rudowska J. Pertussis in Poland in 2013. Przegl Epidemiol 2015;69:745–747 885–887[PubMed]
    [Google Scholar]
  8. Zakład Epidemiologii NIZP-PZH Departament Zapobiegania oraz Zwalczania Zakażeń i Chorób Zakaźnych u Ludzi GIS. Zachorowania na wybrane choroby zakaźne w Polsce od 1 stycznia do 31 grudnia 2010 r. oraz w porównywalnym okresie 2009 r. http://wwwold.pzh.gov.pl/oldpage/epimeld/2010/INF_10_12B.pdf
  9. Sealey KL, Belcher T, Preston A. Bordetella pertussis epidemiology and evolution in the light of pertussis resurgence. Infect Genet Evol 2016;40:136–143 [CrossRef][PubMed]
    [Google Scholar]
  10. Sheridan SL, Ware RS, Grimwood K, Lambert SB. Number and order of whole cell pertussis vaccines in infancy and disease protection. JAMA 2012;308:454 [CrossRef][PubMed]
    [Google Scholar]
  11. Witt MA, Arias L, Katz PH, Truong ET, Witt DJ. Reduced risk of pertussis among persons ever vaccinated with whole cell pertussis vaccine compared to recipients of acellular pertussis vaccines in a large US cohort. Clin Infect Dis 2013;56:1248–1254 [CrossRef][PubMed]
    [Google Scholar]
  12. Lam C, Octavia S, Ricafort L, Sintchenko V, Gilbert GL et al. Rapid increase in pertactin-deficient Bordetella pertussis isolates, Australia. Emerg Infect Dis 2014;20: [CrossRef][PubMed]
    [Google Scholar]
  13. Pawloski LC, Queenan AM, Cassiday PK, Lynch AS, Harrison MJ et al. Prevalence and molecular characterization of pertactin-deficient Bordetella pertussis in the United States. Clin Vaccine Immunol 2014;21:119–125 [CrossRef][PubMed]
    [Google Scholar]
  14. Zeddeman A, van Gent M, Heuvelman CJ, van der Heide HG, Bart MJ et al. Investigations into the emergence of pertactin-deficient Bordetella pertussis isolates in six European countries, 1996 to 2012. Euro Surveill 2014;19:20881 [CrossRef][PubMed]
    [Google Scholar]
  15. He Q. Evolution of Bordetella pertussis. Pediatr Infect Dis J 2016;35:915–917 [CrossRef][PubMed]
    [Google Scholar]
  16. Cherry JD. Epidemic pertussis in 2012—the resurgence of a vaccine-preventable disease. N Engl J Med 2012;367:785–787 [CrossRef][PubMed]
    [Google Scholar]
  17. Cherry JD. Pertussis: challenges today and for the future. PLoS Pathog 2013;9:e1003418 [CrossRef][PubMed]
    [Google Scholar]
  18. Advani A, van der Heide HG, Hallander HO, Mooi FR. Analysis of Swedish Bordetella pertussis isolates with three typing methods: characterization of an epidemic lineage. J Microbiol Methods 2009;78:297–301 [CrossRef][PubMed]
    [Google Scholar]
  19. Advani A, Hallander HO, Dalby T, Krogfelt KA, Guiso N et al. Pulsed-field gel electrophoresis analysis of Bordetella pertussis isolates circulating in Europe from 1998 to 2009. J Clin Microbiol 2013;51:422–428 [CrossRef][PubMed]
    [Google Scholar]
  20. Hallander H, Advani A, Riffelmann M, von König CH, Caro V et al. Bordetella pertussis strains circulating in Europe in 1999 to 2004 as determined by pulsed-field gel electrophoresis. J Clin Microbiol 2007;45:3257–3262 [CrossRef][PubMed]
    [Google Scholar]
  21. Kallonen T, Gröndahl-Yli-Hannuksela K, Elomaa A, Lutyńska A, Fry NK et al. Differences in the genomic content of Bordetella pertussis isolates before and after introduction of pertussis vaccines in four European countries. Infect Genet Evol 2011;11:2034–2042 [CrossRef][PubMed]
    [Google Scholar]
  22. Octavia S, Maharjan RP, Sintchenko V, Stevenson G, Reeves PR et al. Insight into evolution of Bordetella pertussis from comparative genomic analysis: evidence of vaccine-driven selection. Mol Biol Evol 2011;28:707–715 [CrossRef][PubMed]
    [Google Scholar]
  23. Schmidtke AJ, Boney KO, Martin SW, Skoff TH, Tondella ML et al. Population diversity among Bordetella pertussis isolates, United States, 1935–2009. Emerg Infect Dis 2012;18:1248–1255 [CrossRef][PubMed]
    [Google Scholar]
  24. Shuel M, Jamieson FB, Tang P, Brown S, Farrell D et al. Genetic analysis of Bordetella pertussis in Ontario, Canada reveals one predominant clone. Int J Infect Dis 2013;17:e413e417 [CrossRef][PubMed]
    [Google Scholar]
  25. Hegerle N, Guiso N. Bordetella pertussis and pertactin-deficient clinical isolates: lessons for pertussis vaccines. Expert Rev Vaccines 2014;13:1135–1146 [CrossRef][PubMed]
    [Google Scholar]
  26. Mosiej E, Zawadka M, Krysztopa-Grzybowska K, Polak M, Augustynowicz E et al. Sequence variation in virulence-related genes of Bordetella pertussis isolates from Poland in the period 1959–2013. Eur J Clin Microbiol Infect Dis 2015;34:147–152 [CrossRef][PubMed]
    [Google Scholar]
  27. Schouls LM, van der Heide HG, 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 2004;186:5496–5505 [CrossRef][PubMed]
    [Google Scholar]
  28. Hunter PR, Gaston MA. Numerical index of the discriminatory ability of typing systems: an application of Simpson's index of diversity. J Clin Microbiol 1988;26:2465–2466[PubMed]
    [Google Scholar]
  29. Petersen RF, Dalby T, Dragsted DM, Mooi F, Lambertsen L. Temporal trends in Bordetella pertussis populations, Denmark, 1949–2010. Emerg Infect Dis 2012;18:767–774 [CrossRef][PubMed]
    [Google Scholar]
  30. van Gent M, de Greeff SC, van der Heide HG, Mooi FR. An investigation into the cause of the 1983 whooping cough epidemic in the Netherlands. Vaccine 2009;27:1898–1903 [CrossRef][PubMed]
    [Google Scholar]
  31. King AJ, van Gorkom T, Pennings JL, van der Heide HG, He Q 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 [CrossRef][PubMed]
    [Google Scholar]
  32. van Gent M, Heuvelman CJ, van der Heide HG, Hallander HO, Advani A et al. Analysis of Bordetella pertussis clinical isolates circulating in European countries during the period 1998–2012. Eur J Clin Microbiol Infect Dis 2015;34:821–830 [CrossRef][PubMed]
    [Google Scholar]
  33. 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;47:680–688 [CrossRef][PubMed]
    [Google Scholar]
  34. Kurniawan J, Maharjan RP, Chan WF, Reeves PR, Sintchenko V et al. Bordetella pertussis clones identified by multilocus variable-number tandem-repeat analysis. Emerg Infect Dis 2010;16:297–300 [CrossRef][PubMed]
    [Google Scholar]
  35. Miyaji Y, Otsuka N, Toyoizumi-Ajisaka H, Shibayama K, Kamachi K. Genetic analysis of Bordetella pertussis isolates from the 2008–2010 pertussis epidemic in Japan. PLoS One 2013;8:e77165 [CrossRef][PubMed]
    [Google Scholar]
  36. Wagner B, Melzer H, Freymüller G, Stumvoll S, Rendi-Wagner P et al. Genetic variation of Bordetella pertussis in Austria. Mokrousov I, editor. Plos One 2015;10:e0132623
    [Google Scholar]
  37. Galit SR, Otsuka N, Furuse Y, Almonia DJ, Sombrero LT et al. Molecular epidemiology of Bordetella pertussis in the Philippines in 2012–2014. Int J Infect Dis 2015;35:24–26 [CrossRef]
    [Google Scholar]
  38. Xu Y, Zhang L, Tan Y, Wang L, Zhang S et al. Genetic diversity and population dynamics of Bordetella pertussis in China between 1950–2007. Vaccine 2015;33:6327–6331 [CrossRef][PubMed]
    [Google Scholar]
  39. Bart MJ, Harris SR, Advani A, Arakawa Y, Bottero D et al. Global population structure and evolution of Bordetella pertussis and their relationship with vaccination. MBio 2014;5:e01074-14 [CrossRef][PubMed]
    [Google Scholar]
  40. Bouchez V, Hegerle N, Strati F, Njamkepo E, Guiso N. New data on vaccine antigen deficient Bordetella pertussis isolates. Vaccines 2015;3:751–770 [CrossRef][PubMed]
    [Google Scholar]
  41. Hegerle N, Guiso N. Epidemiology of whooping cough & typing of Bordetella pertussis. Future Microbiol 2013;8:1391–1403 [CrossRef][PubMed]
    [Google Scholar]
  42. Xu Y, Liu B, Gröndahl-Yli-Hannuksila K, Tan Y, Feng L et al. Whole-genome sequencing reveals the effect of vaccination on the evolution of Bordetella pertussis. Sci Rep 2015;5:12888 [CrossRef][PubMed]
    [Google Scholar]
  43. Bottero D, Gaillard ME, Basile LA, Fritz M, Hozbor DF. Genotypic and phenotypic characterization of Bordetella pertussis strains used in different vaccine formulations in Latin America. J Appl Microbiol 2012;112:1266–1276[CrossRef]
    [Google Scholar]
  44. Hegerle N, Paris AS, Brun D, Dore G, Njamkepo E et al. Evolution of french Bordetella pertussis and Bordetella parapertussis isolates: increase of Bordetellae not expressing pertactin. Clin Microbiol Infect 2012;18:E340E346 [CrossRef][PubMed]
    [Google Scholar]
  45. Bowden KE, Williams MM, Cassiday PK, Milton A, Pawloski L et al. Molecular epidemiology of the pertussis epidemic in Washington State in 2012. J Clin Microbiol 2014;52:3549–3557 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.000408
Loading
/content/journal/jmm/10.1099/jmm.0.000408
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error