1887

Abstract

Human-adapted is one of the causative agents of whooping cough; however, there are currently no genotyping systems with high discriminatory power for this bacterial pathogen. We therefore aimed to develop a multilocus variable-number tandem repeat analysis (MLVA) for human-adapted .

Four highly polymorphic variable number tandem repeat (VNTR) loci in the genome were selected and amplified by multiplex PCR. MLVA was performed based on the number of tandem repeats at VNTR loci. The discriminatory power of MLVA was evaluated with three laboratory reference strains and 50 human isolates of .

Multiplex PCR-based MLVA characterized 53 reference strains and isolates into 25 MLVA types and the Simpson diversity index was 0.91 (95 % confidence interval, 0.86–0.97). The three reference strains exhibited different MLVA types. Thirty-one Japanese isolates, ten French isolates and three Taiwanese isolates belonged to fourteen, nine and three MLVA types, respectively. In contrast, all five Australian isolates belonged to the same type. Two Japanese isolates collected from patients with known epidemiological links had the same type.

Our novel MLVA method has high discriminatory power for genotyping human . Regarding this organism, this genotyping system is a promising tool for epidemiological surveillance and investigating outbreaks.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001095
2019-11-01
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/jmm/68/11/1671.html?itemId=/content/journal/jmm/10.1099/jmm.0.001095&mimeType=html&fmt=ahah

References

  1. Libster R, Edwards KM. Re-emergence of pertussis: what are the solutions?. Expert Rev Vaccines 2012; 11:1331–1346 [View Article]
    [Google Scholar]
  2. Watanabe M, Nagai M. Whooping cough due to Bordetella parapertussis: an unresolved problem. Expert Rev Anti Infect Ther 2004; 2:447–454 [View Article]
    [Google Scholar]
  3. 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; 18:326–382 [View Article]
    [Google Scholar]
  4. Grogan JA, Logan C, O'Leary J, Rush R, O'Sullivan N. Real-time PCR-based detection of Bordetella pertussis and Bordetella parapertussis in an Irish paediatric population. J Med Microbiol 2011; 60:722–729 [View Article]
    [Google Scholar]
  5. Zouari A, Smaoui H, Brun D, Njamkepo E, Sghaier S et al. Prevalence of Bordetella pertussis and Bordetella parapertussis infections in Tunisian hospitalized infants: results of a 4-year prospective study. Diagn Microbiol Infect Dis 2012; 72:303–317 [View Article]
    [Google Scholar]
  6. Jõgi P, Oona M, Kaart T, Toompere K, Maskina T et al. Pertussis and parapertussis in children and adults with a persistent cough: an observational study. Infection 2018; 46:83–91 [View Article]
    [Google Scholar]
  7. Kamachi K, Yoshino S, Katsukawa C, Otsuka N, Hiramatsu Y et al. Laboratory-based surveillance of pertussis using multitarget real-time PCR in Japan: evidence for Bordetella pertussis infection in preteens and teens. New Microbes New Infect 2015; 8:70–74 [View Article]
    [Google Scholar]
  8. Zhang Q, Yin Z, Li Y, Luo H, Shao Z et al. Prevalence of asymptomatic Bordetella pertussis and Bordetella parapertussis infections among school children in China as determined by pooled real-time PCR: a cross-sectional study. Scand J Infect Dis 2014; 46:280–287 [View Article]
    [Google Scholar]
  9. Javed S, Said F, Eqani SA, Bokhari H. Bordetella parapertussis outbreak in Bisham, Pakistan in 2009-2010: fallout of the 9/11 syndrome. Epidemiol Infect 2015; 143:2619–2623 [View Article]
    [Google Scholar]
  10. Karalius VP, Rucinski SL, Mandrekar JN, Patel R. Bordetella parapertussis outbreak in Southeastern Minnesota and the United States, 2014. Medicine 2017; 96:e6730 [View Article]
    [Google Scholar]
  11. Koepke R, Bartholomew ML, Eickhoff JC, Ayele RA, Rodd D et al. Widespread Bordetella parapertussis infections-Wisconsin, 2011-2012: clinical and epidemiologic features and antibiotic use for treatment and prevention. Clin Infect Dis 2015; 61:1421–1431 [View Article]
    [Google Scholar]
  12. Spicer KB, Salamon D, Cummins C, Leber A, Rodgers LE et al. Occurrence of 3 Bordetella species during an outbreak of cough illness in Ohio: epidemiology, clinical features, laboratory findings and antimicrobial susceptibility. Pediatr Infect Dis J 2014; 33:e162–167 [View Article]
    [Google Scholar]
  13. He Q, Viljanen MK, Arvilommi H, Aittanen B, Mertsola J. Whooping cough caused by Bordetella pertussis and Bordetella parapertussis in an immunized population. JAMA 1998; 280:635–637 [View Article]
    [Google Scholar]
  14. Cherry JD, Seaton BL. Patterns of Bordetella parapertussis respiratory illnesses: 2008-2010. Clin Infect Dis 2012; 54:534–537 [View Article]
    [Google Scholar]
  15. Brinig MM, Register KB, Ackermann MR, Relman DA. Genomic features of Bordetella parapertussis clades with distinct host species specificity. Genome Biol 2006; 7:R81 [View Article]
    [Google Scholar]
  16. Porter JF, Connor K, Donachie W. Differentiation between human and ovine isolates of Bordetella parapertussis using pulsed-field gel electrophoresis. FEMS Microbiol Lett 1996; 135:131–135 [View Article]
    [Google Scholar]
  17. van der Zee A, Mooi F, Van Embden J, Musser J. Molecular evolution and host adaptation of Bordetella spp.: phylogenetic analysis using multilocus enzyme electrophoresis and typing with three insertion sequences. J Bacteriol 1997; 179:6609–6617 [View Article]
    [Google Scholar]
  18. van der Zee A, Groenendijk H, Peeters M, Mooi FR. 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 1996; 46:640–647 [View Article]
    [Google Scholar]
  19. Yuk MH, Heininger U, Martínez de Tejada G, Miller JF. Human but not ovine isolates of Bordetella parapertussis are highly clonal as determined by PCR-based RAPD fingerprinting. Infection 1998; 26:270–273 [View Article]
    [Google Scholar]
  20. Zawadka M, Polak M, Rabczenko D, Mosiej E, Augustynowicz E et al. Effectiveness of the whole-cell pertussis vaccine produced in poland against different Bordetella parapertussis isolates in the mouse intranasal challenge model. Vaccine 2011; 29:5488–5494 [View Article]
    [Google Scholar]
  21. Bouchez V, Brun D, Dore G, Njamkepo E, Guiso N. Bordetella parapertussis isolates not expressing pertactin circulating in France. Clin Microbiol Infect 2011; 17:675–682 [View Article]
    [Google Scholar]
  22. Bokhari H, Said F, Syed MA, Mughal A, Kazi YF et al. Molecular typing of Bordetella parapertussis isolates circulating in Pakistan. FEMS Immunol Med Microbiol 2011; 63:373–380 [View Article]
    [Google Scholar]
  23. Letowska I, Hryniewicz W. Epidemiology and characterization of Bordetella parapertussis strains isolated between 1995 and 2002 in and around Warsaw, Poland. Eur J Clin Microbiol Infect Dis 2004; 23:499–501 [View Article]
    [Google Scholar]
  24. Mäkinen J, Mertsola J, Soini H, Arvilommi H, Viljanen MK et al. PFGE and pertactin gene sequencing suggest limited genetic variability within the Finnish Bordetella parapertussis population. J Med Microbiol 2003; 52:1059–1063 [View Article]
    [Google Scholar]
  25. Diavatopoulos DA, Cummings CA, Schouls LM, Brinig MM, Relman DA et al. Bordetella pertussis, the causative agent of whooping cough, evolved from a distinct, human-associated lineage of B. bronchiseptica . PLoS Pathog 2005; 1:e45 [View Article]
    [Google Scholar]
  26. Toubiana J, Azarnoush S, Bouchez V, Landier A, Guillot S et al. Bordetella parapertussis bacteremia: clinical expression and bacterial genomics. Open Forum Infect Dis 2019; 6:ofz122 [View Article]
    [Google Scholar]
  27. 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 2004; 186:5496–5505 [View Article]
    [Google Scholar]
  28. 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 [View Article]
    [Google Scholar]
  29. Aoyama T, Murase Y, Iwata T, Imaizumi A, Suzuki Y et al. Comparison of blood-free medium (cyclodextrin solid medium) with Bordet-Gengou medium for clinical isolation of Bordetella pertussis . J Clin Microbiol 1986; 23:1046–1048
    [Google Scholar]
  30. Benson G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 1999; 27:573–580 [View Article]
    [Google Scholar]
  31. Nadon CA, Trees E, Ng LK, Møller Nielsen E, Reimer A et al. Development and application of MLVA methods as a tool for inter-laboratory surveillance. Euro Surveill 2013; 18:20565 [View Article]
    [Google Scholar]
  32. 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
    [Google Scholar]
  33. Lam C, Octavia S, Reeves PR, Lan R. Multi-locus variable number tandem repeat analysis of 7th pandemic Vibrio cholerae . BMC Microbiol 2012; 12:82 [View Article]
    [Google Scholar]
  34. Feil EJ, Li BC, Aanensen DM, Hanage WP, Spratt BG. eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J Bacteriol 2004; 186:1518–1530 [View Article]
    [Google Scholar]
  35. Chalmers G, Martin SW, Prescott JF, Boerlin P. Typing of Clostridium perfringens by multiple-locus variable number of tandem repeats analysis. Vet Microbiol 2008; 128:126–135 [View Article]
    [Google Scholar]
  36. Schouls LM, Spalburg EC, van Luit M, Huijsdens XW, Pluister GN et al. Multiple-locus variable number tandem repeat analysis of Staphylococcus aureus: comparison with pulsed-field gel electrophoresis and spa-typing. PLoS One 2009; 4:e5082 [View Article]
    [Google Scholar]
  37. Bergamini F, Iori A, Massi P, Pongolini S. Multilocus variable-number of tandem-repeats analysis of Salmonella enterica serotype gallinarum and comparison with pulsed-field gel electrophoresis genotyping. Vet Microbiol 2011; 149:430–436 [View Article]
    [Google Scholar]
  38. Dahyot S, Lebeurre J, Argemi X, François P, Lemée L et al. Multiple-locus variable number tandem repeat analysis (MLVA) and tandem repeat sequence typing (TRST), helpful tools for subtyping Staphylococcus lugdunensis . Sci Rep 2018; 8:11669 [View Article]
    [Google Scholar]
  39. Kurova N, Njamkepo E, Brun D, Tseneva G, Guiso N. Monitoring of Bordetella isolates circulating in Saint Petersburg, Russia between 2001 and 2009. Res Microbiol 2010; 161:810–815 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.001095
Loading
/content/journal/jmm/10.1099/jmm.0.001095
Loading

Data & Media loading...

Supplements

Supplementary material 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