Multiple-locus variable number tandem repeat analysis of Bordetella pertussis strains collected in the Czech Republic in 1967–2015: spread of a variant adapted to the population with a high vaccination coverage
Authors:
D. Lžičařová 1,2; J. Zavadilová 1; M. Musílek 1; Z. Jandová 1; P. Křížová 1; K. Fabiánová 1,3
Authors‘ workplace:
Centrum epidemiologie a mikrobiologie, Státní zdravotní ústav, Praha
1; Ústav lékařské mikrobiologie 2. LF UK a FN Motol
2; Ústav epidemiologie, 3. LF UK, Praha
3
Published in:
Epidemiol. Mikrobiol. Imunol. 65, 2016, č. 2, s. 102-111
Category:
Original Papers
Overview
Aim:
To perform multiple-locus variable number tandem repeat analysis (MLVA) of B. pertussis strains from the collection of the National Reference Laboratory for Diphtheria and Pertussis (NRL/DIPE), National Institute of Public Health (NIPH), Prague. The study strains were isolated from clinical specimens collected mostly in the Czech Republic over a nearly 50-year period from 1967 to 2015 (June). The isolates from three periods characterized by different vaccination strategies and trends in pertussis are compared for genetic diversity and distribution of MLVA types (MT). Based on the results obtained, the suitability for use of MLVA in the analysis of epidemic outbreaks of B. pertussis in the Czech Republic is considered.
Material and methods:
DNA samples extracted from B. pertussis strains included in the present study were examined by MLVA using the standard protocol. Data were processed by means of the eBURST algorithm and the calculation of the Simpson diversity index (DI) was used for the statistical analysis. Data were analyzed as a whole and also separately for strains from the three periods: 1967–1980, 1990–2007, and 2008–2015 (June).
Results:
Fourteen different MT were detected in the study strains, with three of them not being reported before. The most common MTs were MT27 and MT29. MT29 was predominant in 1967–1980 while MT27 was the most prevalent in 1990–2007 and 2008–2015 (June). The DI was the lowest (0.49) in 2008–2015 (June), and comparably higher DIs were calculated for the two previous periods (i.e. 0.667 for 1967–1980 and 0.654 for 1990–2007).
Conclusion:
MLVA revealed a decrease in genetic diversity and shifts in MT distribution of B. pertussis strains isolated from clinical specimens in the Czech Republic from 1967 to 2015 (June). These shifts in the Czech Republic can be characterized as a progressive increase in global MTs at the expense of the locally unique ones. The most common MT, similarly to other geographical areas with long-term high vaccination coverage, is MT27. The results of MLVA of 136 B. pertussis strains can provide a background for using this method in molecular epidemiological analysis of smaller groups of strains.
KEYWORDS:
Bordetella pertusis – MLVA – population – diversity – adaptation
Sources
1. Kříž B, Fabiánová K, Maixnerová M, et al. Pertusse – navracející se infekce? Epidemiol Mikrobiol Imunol, 2007;56(2):51–65.
2. Fabiánová K, Beneš Č, Kříž B. Stálý nárůst incidence pertuse v České republice od 90. let. Epidemiol Mikrobiol Imunol, 2010;59(1):25–33.
3. Fabiánová K, Zavadilová J, Šebestová H, et al. Syndrom dávivého kašle. Pertuse a parapertuse v České republice v roce 2014 – rozbor epidemiologické situace. Zprávy CEM, 2015;24(5):172–176.
4. Tan T, Dalby T, Forsyth K, et al. Pertussis Across the Globe: Recent Epidemiologic Trends From 2000 to 2013. Pediatr Infect Dis J, 2015;34(9):e222–232.
5. Rohani P, Drake JM. The decline and resurgence of pertussis in the US. Epidemics, 2011;3(3–4):183–188.
6. Celentano LP, Massari M, Paramatti D, et al. Resurgence of pertussis in Europe. Pediatr Infect Dis J, 2005;24(9):761–765.
7. Clark T. Changing pertussis epidemiology: Everything old is new again. J Infect Dis, 2014:20(9):978–981.
8. de Melker HE, Schellekens JF, Neppelenbroek SE, et al. Reemergence of pertussis in the highly vaccinated population of the Netherlands: observations on surveillance data. Emerg Infect Dis, 2000;6(4):348–357.
9. Althouse BM, Scarpino SV. Asymptomatic transmission and the resurgence of Bordetella pertussis. BMC Med, 2015;13:146.
10. Bouchez V, Guiso N. Bordetella pertussis, B. parapertussis, vaccines and cycles of whooping cough. Pathog Dis, 2015;73(7). pii: ftv055.
11. Tartof SY, Lewis M, Kenyon C, et al. Waning immunity to pertussis following 5 doses of DTaP. Pediatrics, 2013;131(4):e1047–1052.
12. Lavine J, Bjornstad O, Freiesleben de Blasio B, et al. Short-lived immunity against pertussis, age-specific routes of transmission, and the utility of a teenage booster vaccine. Vaccine, 2012;30(3):544–551.
13. 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(4):685–694.
14. Smits K, Pottier G, Smet J, et al. Different T cell memory in preadolescents after whole-cell or acellular pertussis vaccination. Vaccine, 2013;32(1):111–118.
15. Edwards KM, Berbers GAM. Immune responses to pertussis vaccines and disease. J Infect Dis, 2014;209(S1):S10–15.
16. Cherry JD. Why do pertussis vaccines fail? Pediatrics, 2012;129(5):968–970.
17. Guiso N. Bordetella pertussis: why is it still circulating? J Infect, 2014;Suppl 1:S119–124.
18. Mooi FR, van Loo IHM, van Gent M, et al. Bordetella pertussis strain with increased toxin production associated with pertussis resurgence. Emerg Infect Dis, 2009;15(8):1206–1213.
19. de Gouw D, Hermans PW, Bootsma HJ, et al. Differentially expressed genes in Bordetella pertussis strains belonging to a lineage which recently spread globally. PLoS One, 2014;9(1):e84523.
20. Aguas R, Goncalves G, Gomes MG. Pertussis: increasing disease as a consequence of reducing transmission. Lancet Infect Dis, 2006;6(2):112–117.
21. Rohani P, Zhong X, King AA. Contact network structure explains the changing epidemiology of pertussis. Science, 2010;330(6006):982–985.
22. Jenkinson D. Increase in pertussis may be due to increased recognition and diagnosis. BMJ, 2012;345:e5463.
23. Paddock CJ, Sander GN, Cherry JD, et al. Pathology and pathogenesis of fatal Bordetella pertussis infection in infants. Clin Infect Dis, 2008;47:328–338.
24. Mattoo S, Cherry JD. Molecular Pathogenesis, Epidemiology, and Clinical Manifestations of Respiratory Infections Due to Bordetella pertussis and Other Bordetella Subspecies. Clin Microbiol Rev, 2005;18(2):326–382.
25. Cherry JD. Adult pertussis in the pre- and post-vaccine eras; lifelong vaccine-induced immunity? Expert Rev Vaccines, 2014;13(9):1073–1080.
26. Parkhill J, Sebaihia M, Preston A, et al. Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nature Genet, 2003;35(1):32–40.
27. Mooi FR. Bordetella pertussis and vaccination: The persistence of a genetically monomorphic pathogen. Infect Genet Evol, 2010;10(1):36–49.
28. Bouchez V, Caro V, Levillain E, et al. Genomic content of Bordetella pertussis clinical isolates circulating in areas of intensive children vaccination. PLoS ONE, 2008;3(6):e2437.
29. Brinig MM, Cummings CA, Sanden GN, et al. Significant gene order and expression differences in Bordetella pertussis despite limited gene content variation. J Bacteriol, 2006;188(7):2375–2382.
30. Spratt BG, Maiden MCJ. Bacterial population genetics, evolution and epidemiology. Philos Trans R Soc Lond B Biol Sci, 1999;354(1384):701–710.
31. 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.
32. 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.
33. Kallonen T, He Q. Bordetella pertussis strain variation and evolution postvaccination. Expert Rev Vaccines, 2009;8(7):863–875.
34. 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.
35. 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):e01074–14.
36. 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(Pt5):355–365.
37. 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.
38. Zavadilová J, Lžičařová D, Musílek M, et al. Antigenní variabilita kmenů Bordetella pertussis izolovaných v letech 1967–2010 v České republice – možné vysvětlení vzestupu nemocnosti pertusí? Epidemiol Mikrobiol Imunol, 2015;64(3):130–138.
39. Mooi FR, van Loo IH, King AJ. Adaptation of Bordetella pertussis to vaccination: a cause for its reemergence? Emerg Infect Dis, 2001;7(3 Suppl):526–528.
40. 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.
41. 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.
42. Lam C, Octavia S, Ricafort L, et al. Rapid increase in pertactin-deficient Bordetella pertussis isolates, Australia. Emerg Infect Dis, 2014;20(4):626–633.
43. Pawloski LC, Queenan AM, Cassiday PK, et al. Prevalence and molecular characterization of pertactin-deficient Bordetella pertussis in the United states. Clin Vacc Immunol, 2014;21(2):119–125.
44. van Belkum A, Scherer S, van Alphen L, et al. Short-sequence DNA repeats in prokaryotic genomes. Mic Mol Biol Rev, 1998;62(2):275–293.
45. van Gent M, Pierard D, Lauwers S, et al. Characterization of Bordetella pertussis clinical isolates that do not express the tracheal colonization factor. FEMS, 2007;51(1):149–154.
46. Schouls LM, van der Heide HGJ, Vauterin L, et al. 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(16):5496–5505.
47. King AJ, van Gorkom T, Pennings JLA, et al. Comparative genomic profiling of Dutch clinical Bordetella pertussis isolates using DNA microarrays: identificaton of genes absent from epidemic strains. BMC Genomics, 2008;9:311.
48. Karami N, Helldal H, Welinder-Olsson C, et al. Sub-typing of extended-spectrum-β-lactamase-producing isolates from a nosocomial outbreak: application of 10-loci generic Escherichia coli multi-locus variable number tandem repeat analysis. PLoS ONE, 2013;8(12):e83030.
49. Bowden KE, Williams MM, Cassiday PK, et al. Molecular epidemiology of the pertussis epidemic in Washington state in 2012. J Clin Microbiol, 2014;52(10):3549–3557.
50. Galit SRL, Otsuka N, Furuse Y, et al. Molecular epidemiology of Bordetella pertussis in the Philippines in 2012–2014. Int J Infect Dis, 2015;35:24–26.
51. Miyaji Y, Otsuka N, Toyoizumi-Ajisaka H, et al. Genetic analysis of Bordetella pertussis isolates from the 2008–2010 epidemic in Japan. PLoS ONE, 2013;8(10):e77165.
52. Lindsted BA, Torpdahl M, Verqnaud G, et al. Use of multilocus variable-number tandem repeat analysis (MLVA) in eight European countries, 2012. Euro Surveill, 2013;18(4):20385.
53. van Gent M, Heuvelman CJ, van der Heide HG, 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(4):821–830.
54. 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.
55. Schmidtke AJ, Boney KO, Martin SW, et al. Population diversity among Bordetella pertussis isolates, United States, 1935–2009. Emerg Infect Dis, 2012;18(8):1248–1255.
56. Kurniawan J, Maharjan RP, Chan WF, et al. Bordetella pertussis clones identified by multilocus variable-number tandem-repeat analysis. Emerg Infect Dis, 2010;16(2):297–300.
57. Multiple-Locus Variable number tandem repeat Analysis. Dostupné na www: www.mlva.net
58. van Belkum A, Tassios PT, Dijkshoorn L, et al. Guidelines for the validation and application of typing methods for use in bacterial epidemiology. Clin Microb Infect Dis, 2007;13(Suppl. 3):1–46.
59. Spratt BG, Hanage WP, Li B, et al. Displaying the relatedness among isolates of bacterial species - the eBURST approach. FEMS Microbiol Lett, 2004;241(2):129–134.
60. Hunter PR, Gaston MA. Numerical index of the discriminatory ability of typing systems: an application of Simpson´s idex of diversity. J Clin Microbiol, 1988;26(11):2465–2466.
61. Grundmann H, Hori S, Tanner G. Determining confidence intervals when measuring genetic diversity and the discriminatory abilities of typing methods for microorganisms. J Clin Microbiol, 2001;39(11):4190–4192.
62. Online tool for quantitative assessment of classification agreement. Dostupné na www: www.comparingpartitions.info
63. Musílek M. Osobní sdělení. Nepublikovaná data.
64. 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, 2005;43(6):2837–2843.
65. Mooi FR, van Loo IHM, van Gent M, et al. Bordetella pertussis strains with increased toxin production associated with pertussis resurgence. Emerg Infect Dis, 2009;15(8):1206–1213.
66. 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.
67. King AJ, van der Lee S, Mohangoo A, et al. Genome-wide 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.
68. van Gent M, Bart MJ, van der Heide HGJ, et al. SNP-based typing: a useful tool to study Bordetella pertussis populations. PLoS ONE, 2011;6(5):e20340.
69. van Belkum A, Struelens M, de Visser A, et al. Role of genomic typing in taxonomy, evolutionary genetics, and microbial epidemiology. Clin Microbiol Rev, 2001;14(3):547–560.
70. Advani A, van der Heide HGJ, 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.
71. Wagner B, Melzer H, Freymuller G, et al. Genetic variation of Bordetella pertussis in Austria. PLoS ONE, 2015;10(7):e0132623.
72. Litt DJ, Jauneikaite E, Tchipeva D, et al. Direct molecular typing of Bordetella pertussis from clinical specimens submitted for diagnostic quantitative (real-time) PCR. J Med Microbiol, 2012;61(Pt 12):1662–1668.
73. Vestrheim DF, Steinbakk M, Bjornstad M, et al. Recovery of Bordetella pertussis from PCR-positive nasopharyngeal sample sis dependent on bacterial load. J Clin Microbiol, 2012;50(12):4114–4115.
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