Comparison of methods based on different molecular epidemiological markers for typing of Mycobacterium tuberculosis complex strains: Interlaboratory study of discriminatory power and reproducibility

Journal of Clinical Microbiology

Volumn 37, Issue 8, 1999, Pages 2607-2618

  Kremer, K ^a   Van Soolingen, D ^a   Frothingham, R ^d   Haas, W H ^c   Hermans, P W M ^b   Martin C ⁱ   Palittapongarnpim, P ^j   Plikaytis, B B ^e   Riley, L W ^g   Yakrus, M A ^f   Musser, J M ^h   Van Embden, J D A ^a  

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

^b ERASMUS UNIVERSITY ROTTERDAM   (Netherlands)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d DURHAM VA MEDICAL CENTER   (United States)

^e NATL CENTER FOR INFECTIOUS DISEASES   (United States)

^f CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h BAYLOR COLLEGE OF MEDICINE   (United States)

ⁱ UNIVERSITY OF ZARAGOZA   (Spain)

^j MAHIDOL UNIVERSITY   (Thailand)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIUM IDENTIFICATION; DNA FINGERPRINTING; GENETIC MARKER; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RELIABILITY; REPRODUCIBILITY; RESTRICTION FRAGMENT LENGTH POLYMORPHISM;

ACTINOBACTERIA (CLASS); BACTERIA (MICROORGANISMS); MYCOBACTERIUM; MYCOBACTERIUM TUBERCULOSIS; UNCULTURED ACTINOMYCETE;

EID: 0032802792     PISSN: 00951137     EISSN: None     Source Type: Journal    
DOI: 10.1128/jcm.37.8.2607-2618.1999     Document Type: Article

References (62)

1. Alland, D., G. E. Kakut, A. R. Moss, R. A. McAdam, J. A. Hahn, W. Bosworth, E. Drucker, and B. R. Bloom. 1994. Transmission of tuberculosis in New York City. An analysis by DNA fingerprinting and conventional epidemiologic methods. N. Engl. J. Med. 330:1710-1716.
2. Beck-Sagué, C., S. W. Dooley, M. D. Hutton, J. Otten, A. Breeden, J. T. Crawford, A. E. Pitchenik, C. Woodley, G. Cauthen, and W. R. Jarvis. 1992. Hospital outbreak of multidrug-resistant Mycobacterium tuberculosis infections. Factors in transmission to staff and HIV-infected patients. JAMA 268:1280-1286.
3. Bergmans, A. M. C., J. Groothedde, J. F. P. Schellekens, J. D. A. van Embden, J. M. Ossewaarde, and L. M. Schouls. 1995. A comparative study on the etiology of cat scratch disease: PCR detection of Bartonella (formerly Rochalimaea) and Afipia felis DNA, serology and skin testing. J. Infect. Dis. 171:916-923.
4. Cole, S. T., R. Brosch, J. Parkhill, T. Garnier, C. Churcher, D. Harris, S. V. Gordon, K. Eiglmeier, S. Gas, C. E. Barry III, F. Tekaia, K. Badcock, D. Basham, D. Brown, T. Chillingworth, R. Connor, R. Davies, K. Devlin, T. Feltwell, S. Gentles, N. Hamlin, S. Holroyd, T. Hornsby, K. Jagels, A. Krogh, J. McClean, S. Moule, L. Murphy, K. Oliver, J. Osborne, M. A. Quail, M. A. Rajandream, J. Rogers, S. Rutter, K. Seeger, J. Skelton, R. Squares, S. Squares, J. E. Sulston, K. Taylor, S. Whitehead, and B. G. Barrell. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537-544.
5. Collins, D. M., and G. W. de Lisle. 1984. DNA restriction endonuclease analysis of Mycobacterium tuberculosis and Mycobacterium bovis BGC. J. Gen. Microbiol. 130:1019-1021.
6. Collins, D. M., and D. M. Stephens. 1991. Identification of insertion sequence, IS1081, in Mycobacterium bovis. FEMS Lett. 83:11-16.
7. Coronado, V. G., C. M. Beck-Sagué, M. D. Hutton, B. J. Davis, P. Nicholas, C. Villareal, C. L. Woodley, J. O. Kilburn, J. T. Crawford, T. R. Frieden, R. L. Sinkowitz, and W. R. Jarvis. 1993. Transmission of multidrug-resistant Mycobacterium tuberculosis among persons with human immunodeficiency virus infection in an urban hospital: epidemiologic and restriction fragment length polymorphism analysis. J. Infect. Dis. 168:1052-1055.
8. Cousins, D. V., S. N. Williams, B. C. Ross, and T. M. Ellis. 1993. Use of a repetitive element isolated from Mycobacterium tuberculosis in hybridization studies with Mycobacterium bovis: a new tool for epidemiological studies of bovine tuberculosis. Vet. Microbiol. 37:1-17.
9. Del Portillo, P., L. A. Murillo, and M. E. Patarroyo. 1991. Amplification of a species-specific DNA fragment of Mycobacterium tuberculosis and its possible use in diagnosis. J. Clin. Microbiol. 29:2163-2168.
10. Edlin, B. R., J. I. Tokars, M. H. Grieco, J. T. Crawford, J. Williams, E. M. Sordillo, K. R. Ong, J. O. Kilburn, S. W. Dooley, K. G. Castro, W. R. Jarvis, and S. D. Holmberg. 1992. An outbreak of multidrug-resistant tuberculosis among hospitalized patients with the acquired immunodeficiency syndrome. N. Engl. J. Med. 326:1514-1521.
11. Eisenach, K. D., J. T. Crawford, and J. H. Bates. 1986. Genetic relatedness among strains of the Mycobacterium tuberculosis complex: analysis of restriction fragment heterogeneity using cloned DNA probes. Am. Rev. Respir. Dis. 133:1065-1068.
12. Fang, Z., N. Morrison, B. Watt, C. Doig, and K. J. Forbes. 1998. IS6110 transposition and evolutionary scenario of the direct repeat locus in a group of closely related Mycobacterium tuberculosis strains. J. Bacteriol. 180:2102-2109.
13. Feizabadi, M. M., I. D. Robertson, D. V. Cousins, and D. J. Hampson. 1996. Genomic analysis of Mycobacterium bovis and other members of the Mycobacterium tuberculosis complex by isoenzyme analysis and pulsed-field gel electrophoresis. J. Clin. Microbiol. 34:1136-1142.
14. Friedman, C. R., M. Y. Stoeckle, W. D. Johnson, Jr., and L. W. Riley. 1995. Double repetitive element PCR method for subtyping Mycobacterium tuberculosis clinical isolates. J. Clin. Microbiol. 33:1064-1069.
15. Frothingham, R., H. G. Hills, and K. H. Wilson. 1994. Extensive DNA sequence conservation throughout the Mycobacterium tuberculosis complex. J. Clin. Microbiol. 32:1639-1643.
16. 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.
17. Gordon, S. V., B. Heym, J. Parkhill, B. Barrell, and S. T. Cole. 1999. New insertion sequences and a novel repeated sequence in the genome of Mycobacterium tuberculosis H37Rv. Microbiology 145:881-892.
18. Goyal, M., D. Young, Z. Zhang, P. A. Jenkins, and R. J. Shaw. 1994. PCR amplification of variable sequence upstream of katG gene to subdivide strains of Mycobacterium tuberculosis complex. J. Clin. Microbiol. 32:3070-3071.
19. Greifinger, R., J. Grabau, A. Quinlan, A. Loeder, G. DiFerdinando, Jr., and D. L. Morse. 1992. Transmission of multidrug-resistant tuberculosis among immunocompromised persons in a correctional system - New York, 1991. Morbid. Mortal. Weekly Rep. 41:507-509.
20. Haas, W. H., W. R. Butler, C. L. Woodley, and J. T. Crawford. 1993. Mixed-linker polymerase chain reaction: a new method for rapid fingerprinting of isolates of the Mycobacterium tuberculosis complex. J. Clin. Microbiol. 31:1293-1298.
21. Harris, M. H., and D. A. Hopkinson. 1976. Handbook of enzyme electrophoresis in human genetics. Elsevier Science Publishing, Inc., New York, N.Y.
22. Heersma, H. F., K. Kremer, and J. D. A. van Embden. 1998. Computer analysis of IS6110 RFLP patterns of Mycobacterium tuberculosis, p. 395-122. In T. Parish and N. G. Stoker (ed.), Methods in molecular biology, vol. 101. Mycobacteria protocols. Humana Press, Inc., Totowa, N.J.
23. Hermans, P. W. M., M. Shuijter, T. Hogeboezem, H. Heersma, A. van Belkum, and R. de Groot. 1995. Comparative study of five different DNA fingerprint techniques for molecular typing of Streptococcus pneumonia strains. J. Clin. Microbiol. 33:1606-1612.
24. Hermans, P. W. M., D. van Soolingen, E. M. Bik, P. E. W. de Haas, J. W. Dale, and J. D. A. van Embden. 1991. The insertion element IS987 from Mycobacterium bovis BCG is located in a hot spot integration region for insertion elements in Mycobacterium tuberculosis complex strains. Infect. Immun. 59:2695-2705.
25. Hermans, P. W. M., D. van Soolingen, and J. D. A. van Embden. 1992. Characterization of a major polymorphic tandem repeat in Mycobacterium tuberculosis and its potential use in the epidemiology of Mycobacterium kansasii and Mycobacterium gordonae. J. Bacteriol. 174:4157-4165.
26. Imeada, T. 1985. Deoxyribonucleic acid relatedness among selected strains of Mycobacterium tuberculosis, Mycobacterium bovis, Mycobacterium bovis BCG, Mycobacterium microti, and Mycobacterium africanum. Int. J. Syst. Bacteriol. 35:147-150.
27. Kamerbeek, J., L. Schouls, A. Kolk, M. van Agterveld, D. van Soolingen, S. Kuijper, A. Bunschoten, H. Molhuizen, R. Shaw, M. Goyal, and J. van Embden. 1997. Rapid detection and simultaneous strain differentiation of Mycobacterium tuberculosis for diagnosis and tuberculosis control. J. Clin. Microbiol. 35:907-914.
28. Kapur, V., T. S. Whittam, and J. M. Musser. 1994. Is Mycobacterium tuberculosis 15,000 years old? J. Infect. Dis. 170:1348-1349.
29. Kent, L., T. D. McHugh, O. Billington, J. W. Dale, and S. H. Gillespie. 1995. Demonstration of homology between IS6110 of Mycobacterium tuberculosis and DNAs of other Mycobacterium spp. J. Clin. Microbiol. 33:2290-2293.
30. Kirschner, P., B. Springer, U. Vogel, A. Meier, A. Wrede, M. Kiekenbeck, F.-C. Bange, and E. C. Böttger. 1993. Genotypic identification of mycobacteria by nucleic acid sequence determination: report of a 2-year experience in a clinical laboratory. J. Clin. Microbiol. 31:2882-2889.
31. Kremer, K. Personal communication.
32. Kurepina, N. E., S. Sreevatsan, B. B. Plikaytis, P. J. Bifani, N. D. Connell, R. J. Donnelly, D. van Soolingen, J. M. Musser, and B. N. Kreiswirth. 1998. Characterization of the phylogenic distribution and chromosomal insertion sites of five IS6110 elements in Mycobacterium tuberculosis: non-random integration in the dnaA-dnaN region. Tuber. Lung Dis. 79:31-42.
33. Li, H., J. C. Ultrup, T. O. Jonassen, K. Melby, S. Nagai, and M. Harboe. 1993. Evidence for absence of the MPB64 gene in some substrains of Mycobacterium bovis BCG. Infect. Immun. 61:1730-1734.
34. Liébana, E., A. Aranaz, B. Francis, and D. Cousins. 1996. Assessment of genetic markers for differentiation within the Mycobacterium tuberculosis complex. J. Clin. Microbiol. 34:933-938.
35. Mariani, F., E. Piccolella, V. Colizzi, R. Rappuoli, and R. Gross. 1993. Characterization of an IS-like element from Mycobacterium tuberculosis. J. Gen. Microbiol. 139:1767-1772.
36. McHugh, T. D., L. E. Newport, and S. H. Gillespie. 1997. IS6110 homologs are present in multiple copies in mycobacteria other than tuberculosis-causing mycobacteria. J. Clin. Microbiol. 35:1769-1771.
37. Otal, I., S. Samper, M. P. Asensio, M. A. Victoria, M. C. Rubio, R. Gómez-Lus, and C. Martín. 1997. Use of a PCR method based on IS6110 polymorphism for typing Mycobacterium tuberculosis strains from BACTEC cultures. J. Clin. Microbiol. 35:273-277.
38. Palittapongarnpim, P., S. Chomyc, A. Fanning, and D. Kunimoto. 1993. DNA fragment length polymorphism analysis of Mycobacterium tuberculosis isolates by arbitrarily primed polymerase chain reaction. J. Infect. Dis. 16:975-978.
39. Plikaytis, B. B. Personal communication.
40. Plikaytis, B. B., J. T. Crawford, C. L. Woodley, W. R. Butler, K. D. Eisenach, M. D. Cave, and T. M. Shinnick. 1993. Rapid, amplification-based fingerprinting of Mycobacterium tuberculosis. J. Gen. Microbiol. 139:1537-1542.
41. Ross, B. C., K. Raios, K. Jackson, and B. Dwyer. 1992. Molecular cloning of a highly repeated DNA element from Mycobacterium tuberculosis and its use as an epidemiological tool. J. Clin. Microbiol. 30:942-946.
42. Sahadevan, R., S. Narayanan, C. N. Paramasivan, R. Prabhakar, and P. R. Narayanan. 1995. Restriction fragment length polymorphism typing of clinical isolates of Mycobacterium tuberculosis from patients with pulmonary tuberculosis in Madras, India, by use of direct-repeat probe. J. Clin. Microbiol. 33:3037-3039.
43. Selander, R. K., D. A. Caugant, H. Ochman, J. M. Musser, M. N. Gilmour, and T. S. Whittan. 1986. Methods of multilocus enzyme electrophoresis for bacterial population genetics and systematics. Appl. Environ. Microbiol. 51:873-884.
44. Small, P. M., P. C. Hopewell, S. P. Singh, A. Paz, J. Parsonnet, D. C. Ruston, G. F. Schecter, C. L. Daley, and G. K. Schoolnik. 1994. The epidemiology of tuberculosis in San Francisco. A population-based study using conventional and molecular methods. N. Engl. J. Med. 330:1703-1709.
45. Sreevatsan, S., X. Pan, K. E. Stockbauer, N. D. Connell, B. N. Kreiswirth, T. S. Whittam, and J. M. Musser. 1997. Restricted structural gene polymorphism in the Mycobacterium tuberculosis complex indicates evolutionarily recent global dissemination. Proc. Natl. Acad. Sci. USA 94:9869-9874.
46. Steenken, W., Jr., and L. U. Gardner. 1946. History of H37 strain of tubercle bacillus. Am. Rev. Tuberc. Pulm. Dis. 54:62-66.
47. Thierry, D., A. Brisson-Noël, V. Vincent-Lévy-Frébault, S. Nguyen, J. Guesdon, and B. Gicquel. 1990. Characterization of a Mycobacterium tuberculosis insertion sequence, IS6110, and its application in diagnosis. J. Clin. Microbiol. 28:2668-2673.
48. van Embden, J. D. A., J. T. Crawford, J. W. Dale, B. Gicquel, P. Hermans, R. McAdam, T. Shinnick, and P. M. Small. 1993. Strain identification of Mycobacterium tuberculosis by DNA fingerprinting: recommendations for a standardized methodology. J. Clin. Microbiol. 31:406-409.
49. van Embden, J. D. A., L. M. Schouls, and D. van Soolingen. 1995. Molecular techniques: applications in epidemiologic studies, p. 15-27. In C. O. Thoen and J. H. Steele (ed.), Mycobacterium bovis infection in animals and humans. Iowa State University Press, Ames, Iowa.
50. van Soolingen, D., P. E. W. de Haas, R. M. Blumenthal, K. Kremer, M. Shuijter, J. E. M. Pijnenburg, L. M. Schouls, J. E. R. Thole, M. W. G. Dessens-Kroon, J. D. A. van Embden, and P. W. M. Hermans. 1996. Host-mediated modification of PvuII restriction in Mycobacterium tuberculosis. J. Bacteriol. 178:78-84.
51. van Soolingen, D., P. E. W. de Haas, J. Haagsma, T. Eger, P. W. M. Hermans, V. Ritacco, A. Alito, and J. D. A. Van Embden. 1994. Use of various genetic markers in differentiation of Mycobacterium bovis strains from animals and humans and for studying epidemiology of bovine tuberculosis. J. Clin. Microbiol. 32:2425-2433.
52. van Soolingen, D., P. E. W. de Haas, P. W. M. Hermans, P. Groenen, and J. D. A. van Embden. 1993. Comparison of various repetitive DNA elements as genetic markers for strain differentiation and epidemiology of Mycobacterium tuberculosis. J. Clin. Microbiol. 31:1987-1995.
53. van Soolingen, D., P. E. W. de Haas, P. W. M. Hermans, and J. D. A. van Embden. 1994. DNA fingerprinting of Mycobacterium tuberculosis. Methods Enzymol. 235:196-205.
54. van Soolingen, D., P. W. M. Hermans, P. E. W. de Haas, and J. D. A. van Embden. 1992. Insertion element IS1081-associated restriction fragment length polymorphism in Mycobacterium tuberculosis complex species: a reliable tool to recognize Mycobacterium bovis BCG. J. Clin. Microbiol. 30:1772-1777.
55. van Soolingen D., T. Hoogenboezem, P. E. W. de Haas, P. W. M. Hermans, M. A. Koedam, K. S. Teppema, P. J. Brennan, G. S. Besra, F. Portaels, J. Top, L. M. Schouls, and J. D. A. van Embden. 1997. A novel pathogenic taxon of the Mycobacterium tuberculosis complex, canettii: characterization of an exceptional isolate from Africa. Int. J. Syst. Bacteriol. 47:1236-1245.
56. van Soolingen, D., L. Qian, P. E. W. de Haas, J. T. Douglas, H. Traore, F. Portaels, H. Z. Qing, D. Enkhasaikan, P. Nymadawa, and J. D. A. van Embden. 1995. Predominance of a single genotype of Mycobacterium tuberculosis in countries of East Asia. J. Clin. Microbiol. 33:3234-3238.
57. van Soolingen, D., A. G. M. van der Zanden, P. E. W. de Haas, G. T. Noordhoek, A. Kiers, N. A. Foudraine, F. Portaels, A. H. J. Kolk, K. Kremer, and J. D. A. van Embden. 1998. Disclosure of Mycobacterium microti infections among humans using novel genetic markers. J. Clin. Microbiol. 36:1840-1845.
58. van Steenbergen, T. J. M., S. D. Colloms, P. W. M. Hermans, J. de Graaff, and R. H. A. Plasterk. 1995. Genomic DNA fingerprinting by restriction fragment end labeling (RFEL). Proc. Natl. Acad. Sci. USA 92:3234-3238.
59. Vera-Cabrera, L., S. T. Howard, A. Laszlo, and W. M. Johnson. 1997. Analysis of genetic polymorphism in the phospholipase region of Mycobacterium tuberculosis. J. Clin. Microbiol. 35:1190-1195.
60. 5 as a marker for Mycobacterium tuberculosis strain identification. J. Clin. Microbiol. 32:1318-1321.
61. Yang, Z. H., P. E. W. de Haas, C. H. Wachman, D. van Soolingen, J. D. A. van Embden, and Å. B. Andersen. 1995. Molecular epidemiology of tuberculosis in Denmark in 1992. J. Clin. Microbiol. 33:2077-2081.
62. Zhang, Y., B. Heym, B. Allen, D. Young, and S. Cole. 1992. The catalaseperoxidase gene and isoniazid resistance of Mycobacterium tuberculosis. Nature 358:591-593.