1887

Abstract

The aims of the present study were to implement a microbead-based ‘spoligotyping’ technique and to evaluate improvements by the addition of a panel of 25 extra spacers that we expected to provide an increased resolution on principal genetic group 1 (PGG 1) strains. We confirmed the high sensitivity and reproducibility of the classical technique using the 43 spacer panel and we obtained perfect agreement between the membrane-based and the microbead-based techniques. We further demonstrated an increase in the discriminative power of an extended 68 spacer format for differentiation of PGG 1 clinical isolates, in particular for the East African–Indian clade. Finally, we define a limited yet highly informative reduced 10 spacer panel set which could offer a more cost-effective option for implementation in resource-limited countries and that could decrease the need for additional VNTR (variable number of tandem repeats) genotyping work in molecular epidemiological studies. We also present an economic analysis comparing membrane-based and microbead-based techniques.

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2010-03-01
2024-12-02
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References

  1. Ahmed N., Leblebicioglu H. 2006; India's ‘gold mine' of ancestral bacilli and the looming TB-HIV pandemic. Ann Clin Microbiol Antimicrob 5:31 [CrossRef]
    [Google Scholar]
  2. Alland D., Kalkut G. E., Moss A. R., Adam R. A. M., Hahn J. A., Bosworth W., Drucker E., Bloom B. R. 1994; Transmission of tuberculosis in New York City: an analysis by DNA fingerprinting and conventional epidemiologic methods. N Engl J Med 330:1710–1716 [CrossRef]
    [Google Scholar]
  3. Asiimwe B. B., Koivula T., Kallenius G., Huard R. C., Ghebremichael S., Asiimwe J., Joloba M. L. 2008; Mycobacterium tuberculosis Uganda genotype is the predominant cause of TB in Kampala, Uganda. Int J Tuberc Lung Dis 12:386–391
    [Google Scholar]
  4. Baker L., Brown T., Maiden M. C., Drobniewski F. 2004; Silent nucleotide polymorphisms and a phylogeny for Mycobacterium tuberculosis . Emerg Infect Dis 10:1568–1577 [CrossRef]
    [Google Scholar]
  5. Baums I. B., Goodwin K. D., Kiesling T., Wanless D., Diaz M. R., Fell J. W. 2007; Luminex detection of fecal indicators in river samples, marine recreational water, and beach sand. Mar Pollut Bull 54:521–536 [CrossRef]
    [Google Scholar]
  6. Beggs M. L., Cave M. D., Marlowe C., Cloney L., Duck P., Eisenach K. D. 1996; Characterization of Mycobacterium tuberculosis complex direct repeat sequence for use in cycling probe reaction. J Clin Microbiol 34:2985–2989
    [Google Scholar]
  7. Bergval I. L., Vijzelaar R. N., Dalla Costa E. R., Schuitema A. R., Oskam L., Kritski A. L., Klatser P. R., Anthony R. M. 2008; Development of multiplex assay for rapid characterization of Mycobacterium tuberculosis . J Clin Microbiol 46:689–699 [CrossRef]
    [Google Scholar]
  8. Brudey K., Gutierrez M. C., Vincent V., Parsons L. M., Salfinger M., Rastogi N., Sola C. 2004; Mycobacterium africanum genotyping using novel spacer oligonucleotides in the direct repeat locus. J Clin Microbiol 42:5053–5057 [CrossRef]
    [Google Scholar]
  9. Brudey K., Driscoll J., Rigouts L., Prodinger W. M., Gori A., Al-Hajoj S. A. M., Allix C., Aristimuno L., Arora J. other authors 2006; Mycobacterium tuberculosis complex genetic diversity: mining the fourth international spoligotyping database (SpolDB4) for classification, population genetics, and epidemiology. BMC Microbiol 6:23 [CrossRef]
    [Google Scholar]
  10. Cowan L. S., Diem L., Brake M. C., Crawford J. T. 2004; Transfer of a Mycobacterium tuberculosis genotyping method, spoligotyping, from a reverse line-blot hybridization, membrane-based assay to the Luminex multianalyte profiling system. J Clin Microbiol 42:474–477 [CrossRef]
    [Google Scholar]
  11. Dos Vultos T., Mestre O., Rauzier J., Golec M., Rastogi N., Rasolofo V., Tonjum T., Sola C., Matic I. other authors 2008; Evolution and diversity of clonal bacteria: the paradigm of Mycobacterium tuberculosis . PLoS One 3:e1538 [CrossRef]
    [Google Scholar]
  12. Drobniewski F. A., Caws M., Gibson A., Young D. 2003; Modern laboratory diagnosis of tuberculosis. Lancet Infect Dis 3:141–147 [CrossRef]
    [Google Scholar]
  13. Dunbar S. A. 2006; Applications of Luminex xMAP technology for rapid, high-throughput multiplexed nucleic acid detection. Clin Chim Acta 363:71–82 [CrossRef]
    [Google Scholar]
  14. Dunbar S. A., Vander Zee C. A., Oliver K. G., Karem K. L., Jacobson J. W. 2003; Quantitative, multiplexed detection of bacterial pathogens: DNA and protein applications of the Luminex LabMAP system. J Microbiol Methods 53:245–252 [CrossRef]
    [Google Scholar]
  15. Dye C., Williams B. G. 2008; Eliminating human tuberculosis in the twenty-first century. J R Soc Interface 5:653–662 [CrossRef]
    [Google Scholar]
  16. Filliol I., Motiwala A. S., Cavatore M., Qi W., Hernando Hazbon M., Bobadilla Del Valle M., Fyfe J., Garcia-Garcia L., Rastogi N. other authors 2006; Global phylogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol 188:759–772 [CrossRef]
    [Google Scholar]
  17. Gagneux S., Small P. M. 2007; Global phylogeography of Mycobacterium tuberculosis and implications for tuberculosis product development. Lancet Infect Dis 7:328–337 [CrossRef]
    [Google Scholar]
  18. Goguet de la Salmoniere Y. O., Kim C. C., Tsolaki A. G., Pym A. S., Siegrist M. S., Small P. M. 2004; High-throughput method for detecting genomic-deletion polymorphisms. J Clin Microbiol 42:2913–2918 [CrossRef]
    [Google Scholar]
  19. Groenen P. M., Bunschoten A. E., van Soolingen D., van Embden J. D. 1993; Nature of DNA polymorphism in the direct repeat cluster of Mycobacterium tuberculosis ; application for strain differentiation by a novel typing method. Mol Microbiol 10:1057–1065 [CrossRef]
    [Google Scholar]
  20. Gutacker M. M., Mathema B., Soini H., Shashkina E., Kreiswirth B. N., Graviss E. A., Musser J. M. 2006; Single-nucleotide polymorphism-based population genetic analysis of Mycobacterium tuberculosis strains from 4 geographic sites. J Infect Dis 193:121–128 [CrossRef]
    [Google Scholar]
  21. Hanekom M., van der Spuy G. D., Gey van Pittius N. C., McEvoy C. R. E., Hoek K. G. P., Ndabambi S. L., Jordan A. M., Victor T. C., van Helden P. D., Warren R. M. 2008; Discordance between mycobacterial interspersed repetitive-unit–variable-number tandem-repeat typing and IS 6110 restriction fragment length polymorphism genotyping for analysis of Mycobacterium tuberculosis Beijing strains in a setting of high incidence of tuberculosis. J Clin Microbiol 46:3338–3345 [CrossRef]
    [Google Scholar]
  22. Hardenbol P., Baner J., Jain M., Nilsson M., Namsaraev E. A., Karlin-Neumann G. A., Fakhrai-Rad H., Ronaghi M., Willis T. D. other authors 2003; Multiplexed genotyping with sequence-tagged molecular inversion probes. Nat Biotechnol 21:673–678 [CrossRef]
    [Google Scholar]
  23. Hunter P. R., Gaston M. A. 1988; Numerical index of the discriminatory ability of typing systems: an application of Simpson's index of diversity. J Clin Microbiol 26:2465–2466
    [Google Scholar]
  24. Jansen R., van Embden J. D. A., Gaastra W., Schouls L. M. 2002; Identification of a novel family of sequence repeats among prokaryotes. OMICS 6:23–33 [CrossRef]
    [Google Scholar]
  25. Javed M. T., Aranaz A., de Juan L., Bezos J., Romero B., Alvarez J., Lozano C., Mateos A., Dominguez L. 2007; Improvement of spoligotyping with additional spacer sequences for characterization of Mycobacterium bovis and M. caprae isolates from Spain. Tuberculosis (Edinb 87:437–445 [CrossRef]
    [Google Scholar]
  26. Jiang H. L., Zhu H. H., Zhou L. F., Chen F., Chen Z. 2006; Genotyping of human papillomavirus in cervical lesions by L1 consensus PCR and the Luminex xMAP system. J Med Microbiol 55:715–720 [CrossRef]
    [Google Scholar]
  27. Kamerbeek J., Schouls L., Kolk A., van Agterveld M., van Soolingen D., Kuijper S., Bunschoten A., Molhuizen H., Shaw R. other authors 1997; Simultaneous detection and strain differentiation of Mycobacterium tuberculosis for diagnosis and epidemiology. J Clin Microbiol 35:907–914
    [Google Scholar]
  28. Kaufhold A., Podbielski A., Baumgarten G., Blokpoel M., Top J., Schouls L. 1994; Rapid typing of group A streptococci by the use of DNA amplification and non-radioactive allele-specific oligonucleotide probes. FEMS Microbiol Lett 119:19–26 [CrossRef]
    [Google Scholar]
  29. Kremer K., van Soolingen D., Frothingham R., Haas W. H., Hermans P. W., Martin C., Palittapongarnpim P., Plikaytis B. B., Riley L. W. other authors 1999; Comparison of methods based on different molecular epidemiological markers for typing of Mycobacterium tuberculosis complex strains: interlaboratory study of discriminatory power and reproducibility. J Clin Microbiol 37:2607–2618
    [Google Scholar]
  30. Manissero D., Fernandez de la Hoz K. 2006; Surveillance methods and case definition for extensively drug resistant TB (XDR-TB) and relevance to Europe: summary update. Euro Surveill 11:E061103
    [Google Scholar]
  31. Mokrousov I., Limeschenko E., Vyazovaya A., Narvskaya O. 2007; Corynebacterium diphtheriae spoligotyping based on combined use of two CRISPR loci. Biotechnol J 2:901–906 [CrossRef]
    [Google Scholar]
  32. Nakajima H. 1993; Tuberculosis: a global emergency. World Health Forum 14:438
    [Google Scholar]
  33. Rastogi N., Legrand E., Sola C. 2001; The mycobacteria: an introduction to nomenclature and pathogenesis. Rev Sci Tech 20:21–54
    [Google Scholar]
  34. Sebban M., Mokrousov I., Rastogi N., Sola C. 2002; A data-mining approach to spacer oligonucleotide typing of Mycobacterium tuberculosis . Bioinformatics 18:235–243 [CrossRef]
    [Google Scholar]
  35. Smith N. H., Kremer K., Inwald J., Dale J., Driscoll J. R., Gordon S. V., van Soolingen D., Glyn Hewinson R., Maynard Smith J. 2006; Ecotypes of the Mycobacterium tuberculosis complex. J Theor Biol 239:220–225 [CrossRef]
    [Google Scholar]
  36. Soini H., Pan X., Amin A., Graviss E. A., Siddiqui A., Musser J. M. 2000; Characterization of Mycobacterium tuberculosis isolates from patients in Houston, Texas, by spoligotyping. J Clin Microbiol 38:669–676
    [Google Scholar]
  37. Sola C., Filliol I., Legrand E., Mokrousov I., Rastogi N. 2001; Mycobacterium tuberculosis phylogeny reconstruction based on combined numerical analysis with IS 1081 , IS 6110 , VNTR and DR-based spoligotyping suggests the existence of two new phylogeographical clades. J Mol Evol 53:680–689 [CrossRef]
    [Google Scholar]
  38. Sola C., Filliol I., Legrand E., Lesjean S., Locht C., Supply P., Rastogi N. 2003; Genotyping of the Mycobacterium tuberculosis complex using MIRUs: association with VNTR and spoligotyping for molecular epidemiology and evolutionary genetics. Infect Genet Evol 3:125–133 [CrossRef]
    [Google Scholar]
  39. Song E. J., Jeong H. J., Lee S. M., Kim C. M., Song E. S., Park Y. K., Bai G. H., Lee E. Y., Chang C. L. 2007; A DNA chip-based spoligotyping method for the strain identification of Mycobacterium tuberculosis isolates. J Microbiol Methods 68:430–433 [CrossRef]
    [Google Scholar]
  40. Sorek R., Kunin V., Hugenholtz P. 2008; CRISPR – a widespread system that provides acquired resistance against phages in bacteria and archaea. Nat Rev Microbiol 6:181–186 [CrossRef]
    [Google Scholar]
  41. Sreevatsan S., Pan X., Stockbauer K. E., Connell N. D., Kreiswirth B. N., Whittam T. S., Musser J. M. 1997; Restricted structural gene polymorphism in the Mycobacterium tuberculosis complex indicates evolutionarily recent global dissemination. Proc Natl Acad Sci U S A 94:9869–9874 [CrossRef]
    [Google Scholar]
  42. Supply P., Allix C., Lesjean S., Cardoso-Oelemann M., Rusch-Gerdes S., Willery E., Savine E., de Haas P., van Deutekom H. other authors 2006; Proposal for standardization of optimized mycobacterial interspersed repetitive unit-variable-number tandem repeat typing of Mycobacterium tuberculosis . J Clin Microbiol 44:4498–4510 [CrossRef]
    [Google Scholar]
  43. Tafaj S., Zhang J., Hauck Y., Pourcel C., Hafizi H., Zoraqi G., Sola C. 2009; First insight into genetic diversity of the Mycobacterium tuberculosis complex in Albania obtained by multilocus variable-number tandem-repeat analysis and spoligotyping reveals the presence of Beijing multidrug-resistant isolates. J Clin Microbiol 47:1581–1584 [CrossRef]
    [Google Scholar]
  44. Tanaka M. M., Francis A. R. 2006; Detecting emerging strains of tuberculosis by using spoligotypes. Proc Natl Acad Sci U S A 103:15266–15271 [CrossRef]
    [Google Scholar]
  45. Uplekar M., Lonnroth K. 2007; MDR and XDR – the price of delaying engagement with all care providers for control of TB and TB/HIV. Trop Med Int Health 12:473–474 [CrossRef]
    [Google Scholar]
  46. Valcheva V., Mokrousov I., Rastogi N., Narvskaya O., Markova N. 2008; Molecular characterization of Mycobacterium tuberculosis isolates from different regions of Bulgaria. J Clin Microbiol 46:1014–1018 [CrossRef]
    [Google Scholar]
  47. van der Zanden A. G., Kremer K., Schouls L. M., Caimi K., Cataldi A., Hulleman A., Nagelkerke N. J., van Soolingen D. 2002; Improvement of differentiation and interpretability of spoligotyping for Mycobacterium tuberculosis complex isolates by introduction of new spacer oligonucleotides. J Clin Microbiol 40:4628–4639 [CrossRef]
    [Google Scholar]
  48. van Embden J. D., Cave M. D., Crawford J. T., Dale J. W., Eisenach K. D., Gicquel B., Hermans P., Martin C., McAdam R. other authors 1993; Strain identification of Mycobacterium tuberculosis by DNA fingerprinting: recommendations for a standardized methodology. J Clin Microbiol 31:406–409
    [Google Scholar]
  49. van Embden J. D. A., van Gorkom T., Kremer K., Jansen R., van der Zeijst B. A. M., Schouls L. M. 2000; Genetic variation and evolutionary origin of the direct repeat locus of Mycobacterium tuberculosis complex bacteria. J Bacteriol 182:2393–2401 [CrossRef]
    [Google Scholar]
  50. van Soolingen D. 2001; Molecular epidemiology of tuberculosis and other mycobacterial infections: main methodologies and achievements. J Intern Med 249:1–26
    [Google Scholar]
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