Multiple-locus variable-number tandem repeat analysis of Dutch Bordetella pertussis strains reveals rapid genetic changes with clonal expansion during the late 1990s

Journal of Bacteriology

Volumn 186, Issue 16, 2004, Pages 5496-5505

  Schouls, Leo M ^a   Van Der Heide, Han G J ^a   Vauterin, Luc ^b   Vauterin, Paul ^b   Mooi, Frits R ^a  

^a NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^b Applied Maths ^*  (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ALLELE; ARTICLE; BACTERIAL GENETICS; BACTERIUM IDENTIFICATION; BORDETELLA PERTUSSIS; CLONAL EXPANSION; CLONE; EPIDEMIC; GENETIC VARIABILITY; GENOTYPE; MINIMUM SPANNING TREE; MOLECULAR BIOLOGY; MULTIPLE ANTIGEN SEQUENCE TYPING; MULTIPLE LOCUS VARIABLE NUMBER OF TANDEM REPEAT; NETHERLANDS; NONHUMAN; PERTUSSIS; PHYLOGENETIC TREE; PRIORITY JOURNAL; STRAIN DIFFERENCE; VACCINATION; VARIABLE NUMBER OF TANDEM REPEAT;

ALLELES; ANTIGENS, BACTERIAL; BACTERIAL TYPING TECHNIQUES; BORDETELLA PERTUSSIS; DNA FINGERPRINTING; DNA, BACTERIAL; ENDEMIC DISEASES; EPIDEMIOLOGY, MOLECULAR; GENES, BACTERIAL; GENOTYPE; HUMANS; MINISATELLITE REPEATS; NETHERLANDS; PHYLOGENY; SEQUENCE ANALYSIS, DNA; VARIATION (GENETICS); WHOOPING COUGH;

ANIMALIA; BACTERIA (MICROORGANISMS); BORDETELLA; BORDETELLA PERTUSSIS; INSERTION SEQUENCES; NEGIBACTERIA; PROKARYOTA; TRANSPOSONS;

EID: 3843099223     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.186.16.5496-5505.2004     Document Type: Article

References (37)

1. Benson, G. 1999. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27:573-580.
2. Bisgard, K. M., C. D. Christie, S. F. Reising, G. N. Sanden, P. K. Cassiday, C. Gomersall, W. A. Wattigney, N. E. Roberts, and P. M. Strebel. 2001. Molecular epidemiology of Bordetella pertussis by pulsed-field gel electrophoresis profile: Cincinnati, 1989-1996. J. Infect. Dis. 183:1360-1367.
3. Cassiday, P., G. Sanden, K. Heuvelman, F. Mooi, K. M. Bisgard, and T. Popovic. 2000. Polymorphism in Bordetella pertussis pertactin and pertussis toxin virulence factors in the United States, 1935-1999. J. Infect. Dis. 182:1402-1408.
4. Coletta-Filho, H. D., M. A. Takita, A. A. de Souza, C. I. Aguilar-Vildoso, and M. A. Machado. 2001. Differentiation of strains of Xylella fastidiosa by a variable number of tandem repeat analysis. Appl. Environ. Microbiol. 67:4091-4095.
5. Crowcroft, N. S., and J. Britto. 2002. Whooping cough-a continuing problem. Br. Med. J. 324:1537-1538.
6. de Melker, H. E., J. F. Schellekens, S. E. Neppelenbroek, F. R. Mooi, H. C. Rumke, and M. A. Conyn-van Spaendonck. 2000. Reemergence of pertussis in the highly vaccinated population of the Netherlands: observations on surveillance data. Emerg. Infect. Dis. 6:348-357.
7. Dingle, K. E., F. M. Colles, D. R. A. Wareing, R. Ure, A. J. Fox, F. E. Bolton, H. J. Bootsma, R. J. L. Willems, R. Urwin, and M. C. J. Maiden. 2001. Multilocus sequence typing system for Campylobacterjejuni. J. Clin. Microbiol. 39:14-23.
8. Enright, M. C., N. P. J. Day, C. E. Davies, S. J. Peacock, and B. G. Spratt. 2000. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J. Clin. Microbiol. 38:1008-1015.
9. Enright, M. C., and B. G. Spratt. 1998. A multilocus sequence typing scheme for Streptococcuspneumoniae: identification of clones associated with serious invasive disease. Microbiology 144:3049-3060.
10. Farlow, J., D. Postic, K. L. Smith, Z. Jay, G. Baranton, and P. Keim. 2002. Strain typing of Borrelia burgdorferi, Borrelia afzelii, and Borrelia garinii by using multiple-locus variable-number tandem repeat analysis. J. Clin. Microbiol. 40:4612-4618.
11. Farlow, J., K. L. Smith, J. Wong, M. Abrams, M. Lytle, and P. Keim. 2001. Francisella tularensis strain typing using multiple-locus, variable-number tandem repeat analysis. J. Clin. Microbiol. 39:3186-3192.
12. Frothingham, R., and W. A. Meeker-O'Connell. 1998. Genetic diversity in the Mycobacterium tuberculosis complex based on variable numbers of tandem DNA repeats. Microbiology 144:1189-1196.
13. Fry, N. K., S. Neal, T. G. Harrison, E. Miller, R. Matthews, and R. C. George. 2001. Genotypic variation in the Bordetella pertussis virulence factors pertactin and pertussis toxin in historical and recent clinical isolates in the United Kingdom. Infect. Immun. 69:5520-5528.
14. Guris, D., P. M. Strebel, B. Bardenheier, M. Brennan, P. Tachdjian, E. Finch, M. Wharton, and J. P. Livengood. 1999. Changing epidemiology of pertussis in the United States: increasing reported incidence among adolescents and adults, 1990-1996. Clin. Infect. Dis. 28:1230-1237.
15. He, Q., J. Makinen, G. Berbers, F. R. Mooi, M. K. Viljanen, H. Arvilommi, and J. Mertsola. 2003. Bordetella pertussis protein pertactin induces type-specific antibodies: one possible explanation for the emergence of antigenic variants? J. Infect. Dis. 187:1200-1205.
16. Keim, P., A. M. Klevytska, L. B. Price, J. M. Schupp, G. Zinser, K. L. Smith, M. E. Hugh-Jones, R. Okinaka, K. K. Hill, and P. J. Jackson. 1999. Molecular diversity in Bacillus anthracis. J. Appl. Microbiol. 87:215-217.
17. King, A. J., G. Berbers, H. F. van Oirschot, P. Hoogerhout, K. Knipping, and F. R. Mooi. 2001. Role of the polymorphic region 1 of the Bordetella pertussis protein pertactin in immunity. Microbiology 147:2885-2895.
18. Klevytska, A. M., L. B. Price, J. M. Schupp, P. L. Worsham, J. Wong, and P. Keim. 2001. Identification and characterization of variable-number tandem repeats in the Yersinia pestis genome. J. Clin. Microbiol. 39:3179-3185.
19. Liu, Y., M.-A. Lee, E.-E. Ooi, Y. Mavis, A.-L. Tan, and H.-H. Quek. 2003. Molecular typing of Salmonella enterica serovar Typhi isolates from various countries in Asia by a multiplex PCR assay on variable-number tandem repeats. J. Clin. Microbiol. 41:4388-4394.
20. Maiden, M. C. J., J. A. Bygraves, E. Feil, G. Morelli, J. E. Russell, R. Urwin, Q. Zhang, J. J. Zhou, K. Zurth, D. A. Caugant, I. M. Feavers, M. Achtman, and B. G. Spratt. 1998. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc. Natl. Acad. Sci. USA 95:3140-3145.
21. Margalef, R. 1958. Information theory in ecology. Gen. Syst. 3:36-71.
22. Mastrantonio, P., P. Spigaglia, H. van Oirschot, H. G. van der Heide, K. Heuvelman, P. Stefanelli, and F. R. Mooi. 1999. Antigenic variants in Bordetella pertussis strains isolated from vaccinated and unvaccinated children. Microbiology 145:2069-2075.
23. Mooi, F. R., Q. He, H. van Oirschot, and J. Mertsola. 1999. Variation in the Bordetella pertussis virulence factors pertussis toxin and pertactin in vaccine strains and clinical isolates in Finland. Infect. Immun. 67:3133-3134.
24. Mooi, F. R., I. H. van Loo, and A. J. King. 2001. Adaptation of Bordetella pertussis to vaccination: a cause for its reemergence? Emerg, Infect. Dis. 7:526-528.
25. Mooi, F. R., H. van Oirschot, K. Heuvelman, H. G. van der Heide, W. Gaastra, and R. J. L. Willems. 1998. 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. 66:670-675.
26. O'Rourke, J. 1998. Computational geometry in C, 2nd ed. Cambridge University Press, Cambridge, England.
27. Pourcel, C., Y. Vidgop, F. Ramisse, G. Vergnaud, and C. Tram. 2003. Characterization of a tandem repeat polymorphism in Legionella pneumophila and its use for genotyping. J. Clin. Microbiol. 41:1819-1826.
28. Sabat, A., J. Krzyszton-Russjan, W. Strzalka, R. Filipek, K. Kosowska, W. Hryniewicz, J. Travis, and J. Potempa. 2003. New method for typing Staphylococcus aureus strains: multiple-locus variable-number tandem repeat analysis of polymorphism and genetic relationships of clinical isolates. J. Clin. Microbiol. 41:1801-1804.
29. Senzilet, L. D., S. A. Halperin, J. S. Spika, M. Alagaratnam, A. Morris, and B. Smith. 2001. Pertussis is a frequent cause of prolonged cough illness in adults and adolescents. Clin. Infect. Dis. 32:1691-1697.
30. Syedabubakar, S. N., R. C. Matthews, N. W. Preston, D. Owen, and V. Hillier. 1995. Application of pulsed field gel electrophoresis to the 1993 epidemic of whooping cough in the United Kingdom. Epidemiol. Infect. 115:101-113.
31. van Belkum, A., S. Scherer, W. van Leeuwen, D. Willemse, L. van Alphen, and H. Verbrugh. 1997. Variable number of tandem repeats in clinical strains of Haemophilus influenzae. Infect. Immun. 65:5017-5027.
32. van Boven, M., H. E. de Melker, J. F. Schellekens, and M. Kretzschmar. 2000. Waning immunity and sub-clinical infection in an epidemic model: implications for pertussis in The Netherlands. Math. Biosci. 164:161-182.
33. van der Zee, A., C. Agterberg, M. Peeters, J. Schellekens, and F. R. Mooi. 1993. Polymerase chain reaction assay for pertussis: simultaneous detection and discrimination of Bordetella pertussis and Bordetella parapertussis. J. Clin. Microbiol. 31:2134-2140.
34. van der Zee, A., H. Groenendijk, M. Peeters, and F. R. Mooi. 1996. The differentiation of Bordetella parapertussis and Bordetella bronchiseptica from humans and animals as determined by DNA polymorphism mediated by two different insertion sequence elements suggests their phylogenetic relationship. Int. J. Syst. Bacteriol. 46:640-647.
35. van der Zee, A., S. Vernooij, M. Peeters, J. van Embden, and F. R. Mooi. 1996. 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 142:3479-3485.
36. van Loo, I. H., K. J. Heuvelman, A. J. King, and F. R. Mooi. 2002. Multilocus sequence typing of Bordetella pertussis based on surface protein genes. J. Clin. Microbiol. 40:1994-2001.
37. van Loo, I. H., H. G. van der Heide, N. J. Nagelkerke, J. Verhoef, and F. R. Mooi 1999. Temporal trends in the population structure of Bordetella pertussis during 1949-1996 in a highly vaccinated population. J. Infect. Dis. 179:915-923.