This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by van Soolingen, D.
Right arrow Articles by Garcia, M. J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by van Soolingen, D.
Right arrow Articles by Garcia, M. J.

 Previous Article  |  Next Article 

Journal of Clinical Microbiology, October 1998, p. 3051-3054, Vol. 36, No. 10
0095-1137/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

IS1245 Restriction Fragment Length Polymorphism Typing of Mycobacterium avium Isolates: Proposal for Standardization

Dick van Soolingen,1,* Jeanett Bauer,2 Viviana Ritacco,3 Sylvia Cardoso Leão,4 Ivo Pavlik,5 Veronique Vincent,6 Nalin Rastogi,7 Andrea Gori,8 Thomas Bodmer,9 Carlo Garzelli,10 and Maria J. Garcia11

Diagnostic Laboratory of Infectious Diseases and Perinatal Screening, National Institute of Public Health and the Environment, 3720 BA Bilthoven, The Netherlands1; Department of Mycobacteriology, Division of Diagnostics, Statens Serum Institut, 2300 Copenhagen S, Denmark2; Pan American Institute for Food Protection and Zoonoses, Martinez 1640, Argentina3; Departamento de Microbiologia, Imunologia e Parasitologia, Universidade Federal de São Paulo, 862.3, Andar, São Paulo, Brazil4; Veterinary Research Institute, Hudcova 70, 621 32 Brno, Czech Republic5; Laboratoire de Référence des Mycobactéries, Institut Pasteur, 75724 Paris Cedex 15, France6; Unité de la Tuberculose et des Mycobactéries, Institut Pasteur, 97165 Pointe-à-Pitre Cedex, Guadeloupe, French West Indies7; Clinic of Infectious Diseases, Luigi Sacco Hospital, University of Milan, 20157 Milan,8 and Department of Biomedicine, University of Pisa, 56127 Pisa,10 Italy; Institute for Medical Microbiology, University of Berne, Berne, Switzerland9; and Departmento de M. Preventiva, Facultad de Medicina, Universidad Autonoma, 28029 Madrid, Spain11

Received 13 April 1998/Returned for modification 6 June 1998/Accepted 4 July 1998

    ABSTRACT
Top
Abstract
Text
References

Mycobacterium avium has become a major human pathogen, primarily due to the emergence of the AIDS epidemic. Restriction fragment length polymorphism (RFLP) typing, using insertion sequence IS1245 as a probe, provides a powerful tool in the molecular epidemiology of M. avium-related infections and will facilitate well-founded studies into the sources of M. avium infections in animal and environmental reservoirs. The standardization of this technique allows computerization of IS1245 RFLP patterns for comparison on a local level and the establishment of M. avium DNA fingerprint databases for interlaboratory comparison. Moreover, by combining international DNA typing results of M. avium complex isolates from a broad spectrum of sources, long-lasting questions on the epidemiology of this major agent of mycobacterial infections will be answered.

    TEXT
Top
Abstract
Text
References

The Mycobacterium avium complex (MAC) comprises opportunistic and obligate pathogens of animals and humans as well as less-defined (sub)species (12, 22, 29). Previously, on the basis of the production of similar polar glycolipid surface antigens which could be used in agglutination tests of bacterial cells, Mycobacterium avium, Mycobacterium intracellulare, and Mycobacterium scrophulaceum were assigned to the MAC (29). Later, Thorel et al. proposed dividing the MAC into the species M. avium, Mycobacterium silvaticum, and Mycobacterium paratuberculosis because of differences in genotypic and growth characteristics, pathogenicity, and host range (22).

Several classical and novel techniques are available to identify and type MAC isolates for taxonomic or epidemiological purposes. Until a few years ago, most laboratories favored serotyping (1, 10), and extensive interlaboratory studies have been conducted to standardize this technique (28). More recently, other techniques have become available; these techniques include multilocus enzyme electrophoresis (28) and DNA-based methodologies, such as pulsed-field gel electrophoresis (14, 20), PCR-based typing (17, 21), and restriction fragment length polymorphism (RFLP) typing. For the latter technique, insertion sequences such as IS900 (6), IS901 (13), IS902 (15), IS1110 (9), IS1141 (26), IS1245 (7), and IS1311 (19) have been proposed as possible epidemiological tools to type and distinguish isolates of the different groupings within the MAC. On the basis of RFLP typing, Guerrero et al. (7) and Bono et al. (2) determined the host range of IS1245 to be limited to M. avium, while M. intracellulare appeared to be devoid of this genomic element. Devallois and Rastogi (3) showed that the highly similar IS1245 and IS1311 possess a similar discriminatory potential for M. avium isolates.

Highly polymorphic multibanded IS1245 RFLP patterns were almost invariably found among M. avium isolates from humans (2, 7, 16, 18, 19). A significant part of the IS1245 DNA fingerprints of M. avium isolates from pigs shared a high degree of similarity with the human isolates (2, 18). In contrast, isolates from a wide variety of bird species were found to possess identical three-band patterns (2, 18). The three-band pattern found in birds was also found in a small fraction of the pig isolates. As this pattern was only rarely encountered among human isolates, birds were found not to be an important source of M. avium infections in humans (18).

Other possible reservoirs for M. avium infection in humans have been reported to be tap water (27), hard cheese (11), and cigarettes (4). Extensive RFLP typing studies of M. avium isolates from these and other reservoirs are needed to investigate the epidemiological relatedness with human infections. This will also provide more insight into the taxonomy and evolutionary divergence within the MAC. To fully explore the possibilities of RFLP typing, international standardization of this method is required. This would facilitate the establishment of databases of M. avium DNA fingerprints and help to trace true sources of infection of this emerging potential pathogen. A previous international standardization of IS6110 RFLP typing of Mycobacterium tuberculosis has resulted in an international database of fingerprints.

Proposal for standardization. Standardization of IS1245 RFLP typing involves the following issues: the choice of the restriction enzyme, the electrophoresis conditions, the preparation of the probe (primers and target), the hybridization stringency, and the use of molecular size marker DNA.

M. avium is a slow-growing microorganism, and the amount of bacterial culture obtained from a Löwenstein slant is often limited. Furthermore, the quantity of DNA extracted from M. avium bacteria is often less than that from M. tuberculosis complex cells. When insufficient growth is obtained on Löwenstein medium, an excellent way to obtain high yields of M. avium cells in the log phase can be achieved by inoculating bacteria from a viable culture in 5 ml of Middlebrook 7H9 liquid medium containing Tween 80 and albumin-glucose (20, 24). After 7 days, the culture is transferred into a volume of 50 ml and incubated (while being agitated) for an additional 10 days (optical density at 600 nm of 0.8 to 1.2). The cells are concentrated by centrifugation and resuspended in a total volume of 400 µl of Tris EDTA buffer for the DNA extraction. Cell lysis and DNA extraction should be performed as described previously (24).

The choice of the restriction enzyme is strongly dependent on the range of sizes of DNA fragments obtained after cleavage of genomic DNA from M. avium strains. Several restriction enzymes provide a wide range of DNA fragments and are capable of defining distinct banding patterns and clusters of identical or highly related isolates, and at least one enzyme, NruI, has been proposed as appropriate for IS1245-based RFLP analysis (5). However, in most previous M. avium RFLP studies (2, 3, 7, 18, 19), the restriction enzyme PvuII was used and PvuII-based RFLP pattern databases have been established. We therefore recommend using PvuII as the restriction enzyme. The use of this restriction enzyme yields restriction fragments ranging from 0.5 to 20 kb. The disadvantage of the use of this enzyme is the appearance of faint bands in the RFLP patterns (5, 18). This can largely be overcome by using a probe for hybridization prepared by PCR amplification on an IS1245 DNA-containing plasmid and higher-stringency washing conditions after hybridization.

Except for the strains with the three-band pattern of birds, IS1245 RFLP patterns of M. avium isolates consist of a high average number of bands, approximately 20 (18). In order to facilitate accurate computer-assisted analysis of these multibanded DNA fingerprints, it is necessary to have a high electrophoresis resolution. The use of relatively long agarose gels (minimum of 24 cm) and electrophoresis at a low voltage (0.5 V/cm) for 20 h can achieve this. The electrophoresis should be continued until the 872-bp fragment of an external DNA size marker, for example, HaeIII-digested phi X174 DNA, has reached a distance of 19 cm from the slots of the gel.

The probe used for the detection of IS1245-containing PvuII restriction fragments in the hybridization procedure can be prepared by PCR with the primer set described by Guerrero et al. (7). The two primers P1 (5'-GCCGCCGAAACGATCTAC) and P2 (5'-AGGTGGCGTCGAGGAAGAC) amplify the region of IS1245 sequence from positions 197 to 623 (accession no. L33879), resulting in a PCR product of 427 bp. The required PCR treatment consists of 30 cycles, with 1 cycle being 1 min at 94°C, 1 min at 65°C, and 1 min at 72°C, followed by one final extension step of 10 min at 72°C (7).

The high degree of similarity between the DNA sequences of IS1245 and IS1311 (19) may result in variable PCR products if DNAs from different strains are used as targets for PCR probe amplification. Furthermore, there may be more, yet unknown, IS elements in M. avium strains representing the same type of insertion sequence family. Therefore, to obtain a standardized and pure IS1245 probe, the use of plasmid pMA12 (Fig. 1), containing the IS1245 DNA sequence as an insert, is highly recommended as a target for probe amplification. This pUC-derived plasmid contains the NruI/SphI restriction fragment of IS1245 between the SphI and SmaI sites. Since both NruI and SmaI are blunt-end cleavers, after ligation both restriction sites are lost. However, the IS1245 insert can be removed by using restriction enzymes SphI and EcoRI. In PCR, 10 to 20 ng of undigested plasmid DNA is sufficient to ensure an optimal DNA target concentration.


View larger version (12K):
[in this window]
[in a new window]
  		FIG. 1.   Physical map of plasmid pMA12 containing an IS1245 insert, which can be used as a target in PCR amplification resulting in a standardized IS1245 probe.

The accurate determination of the sizes of IS1245-containing PvuII restriction fragments requires the use of reference DNA size markers. Either internal or external size markers could be used. However, the use of internal size markers provides much more accurate band position determinations. We recommend using the same internal size markers as those used in the standardized method for RFLP typing of M. tuberculosis isolates (23). In short, each digested M. avium DNA sample is mixed with a reference DNA mix consisting of PvuII-digested supercoiled DNA ladder and HaeIII-digested phi X174 DNA (23). The use of a mix of two internal size markers is necessary to obtain reference DNA fragments of the right size range. After electrophoresis and Southern blotting, the first hybridization enables detection of IS1245-containing PvuII restriction fragments. An additional hybridization on the same membrane is performed by using a mix of PvuII-digested supercoiled DNA ladder and HaeIII-digested phi X174 marker DNA as a probe to visualize the marker bands of known sizes (Fig. 2). During the computer-assisted analyses, both hybridization patterns are superimposed and the sizes of IS1245 bands can be accurately determined.


View larger version (83K):
[in this window]
[in a new window]
  		FIG. 2.   IS1245 RFLP patterns (B) and internal size marker patterns (A) prepared by the proposed standard method. The internal marker bands are PvuII-digested supercoiled DNA ladder fragments with molecular sizes of 16.2, 14.2, 12.1, 10.1, 8.1, 7.0, 6.0, 5.0, 4.0, and 2.9 kb and HaeIII-digested phi X174 ladder fragments with molecular sizes of 1.4, 1.1, and 0.9 kb. Note that the bands indicated by the two arrows represent supercoiled DNA ladder fragments that were not well digested and that should be excluded from the computer analyses. The smallest fragment of the internal marker patterns is 0.9 kb. In standard DNA fingerprinting of M. tuberculosis isolates, the 0.6-kb band of the HaeII-digested phi X176 DNA marker is also used for computer-assisted analysis (24). For typing of M. avium, this band is not required. The outermost IS1245 RFLP patterns in panel B represent the external control strains R13 (leftmost lane) and IWGMT49 (rightmost lane).

It is also possible to use an external size marker with the right range of DNA fragments on at least three different parts of the gel. To facilitate the best achievable intralaboratory comparison of IS1245 RFLP patterns with external size markers, we propose to use reference strain IWGMT49. The computer-assisted analysis based on three external markers will be less accurate than analysis based on internal size markers but will be sufficiently accurate to compare DNA patterns within an accuracy of 1.5% band position deviation.

The final hybridization patterns are strongly dependent on the choice of the stringency conditions during the hybridization and posthybridization washes. The ECL direct system (Amersham International plc) for labeling and detection of probes can be applied with the following modifications. It is recommended that after hybridization more stringent conditions are used than those suggested by the manufacturer in order to obtain IS1245-specific hybridization patterns. This is achieved by washing the Southern blot twice for 10 min each time at 55°C with a 6 M urea primary wash buffer (supplemented with 0.1× SSC-0.4% SDS [1× SSC is 0.15 M NaCl plus 0.015 M sodium citrate, and SDS is sodium dodecyl sulfate]), followed by a secondary wash for 5 min each time at 65°C with 2× SSC-0.1% SDS. Rinsing twice for 5 min at room temperature with 1× SSC completes the washing procedure.

Interlaboratory exchange of computerized IS1245 RFLP patterns requires the standardization of the computer program and settings. The Gelcompar software (Applied Maths, Kortrijk, Belgium) has been successfully used before in both M. avium and M. tuberculosis epidemiology (8, 18, 25), but other DNA fingerprint analysis computer programs can be used (3). Due to the use of the 24-cm-long agarose gels and the on average high-copy-number of IS1245, a track resolution of 1,000 positions is recommended. The standard positions of the bands of the internal marker for normalization are 38, 48, 64, 88, 128, 157, 197, 253, 330, and 446 for the PvuII-digested supercoiled DNA ladder and 784, 875, 957 for the three largest bands of HaeIII-digested phi X174 DNA. The external marker strains should be applied to each gel, one to the second slot and one to the penultimate slot. One of these control strains should provide a wide range of IS1245-containing PvuII restriction fragments, and for this purpose, we recommend the use of strain IWGMT49 (band positions 62, 254, 447, 459, 481, 754, 840, and 934). For a second control strain, we recommend R13, representing the three-band IS1245 RFLP pattern typical of birds (band positions 110, 416, and 452). The use of two external marker strains offers the possibility of controlling the superimposing of the IS1245 and size marker patterns. The band position deviation between the DNA patterns of the control strains in different gels should not exceed 0.8%. The entire procedure for RFLP typing and computer-assisted analysis of mycobacteria has been described in detail in a laboratory manual (24).

    ACKNOWLEDGMENTS

We thank Petra de Haas, Remco van den Hoek, and Kristin Kremer (all at RIVM, Bilthoven, The Netherlands), M. C. Menendez (Universidad Autonoma, Madrid, Spain), M. Picardeau (Institute Pasteur, Paris, France), and Lenka Bejckova (VUVEL, Brno, Czech Republic) for excellent technical assistance and useful discussions. We thank A. Telenti for kindly providing plasmid pDDIR1218, from which pMA12 was prepared.

This study was financially supported in part by grants FIS-97/0042-02 and AC-07/042/96 from the institutions of the Spanish government.

    FOOTNOTES

* Corresponding author. Mailing address: Mycobacteria Department, National Institute of Public Health and the Environment (RIVM), P.O. Box 1, 3720 BA Bilthoven, The Netherlands. Phone: 31 30 2742363. Fax: 31 30 2744418. E-mail: D.van.Soolingen{at}rivm.nl.

    REFERENCES
Top
Abstract
Text
References

1. Askgaard, D., S. B. Giese, S. Thybo, A. Lerche, and J. Bennedsen. 1994. Serovars of Mycobacterium avium complex isolated from patients in Denmark. J. Clin. Microbiol. 32:2880-2882[Abstract/Free Full Text].
2. Bono, M., T. Jemmi, C. Bernasconi, D. Burki, A. Telenti, and T. Bodmer. 1995. Genotypic characterization of Mycobacterium avium strains recovered from animals and their comparison to human strains. Appl. Environ. Microbiol. 61:371-373[Abstract].
3. Devallois, A., and N. Rastogi. 1997. Computer-assisted analysis of Mycobacterium avium fingerprints using insertion elements IS1245 and IS1311 in a Caribbean setting. Res. Microbiol. 148:703-713[Medline].
4. Eaton, T., J. O. Falkingham, and C. F. von Reyn. 1995. Recovery of Mycobacterium avium from cigarettes. J. Clin. Microbiol. 33:2757-2758[Abstract].
5. Garzelli, C., N. Lari, B. Nguon, M. Cavallini, M. Pistello, and G. Falcone. 1997. Comparison of three restriction endonucleases in IS1245-based RFLP typing of Mycobacterium avium. J. Med. Microbiol. 46:933-939[Abstract/Free Full Text].
6. Green, E. P., M. L. V. Tizard, M. T. Moss, J. Thompson, D. J. Winterbourne, J. J. McFadden, and J. Hermon-Taylor. 1989. Sequence and characteristics of IS900, an insertion element identified in a human Crohn's disease isolate of Mycobacterium paratuberculosis. Nucleic Acids Res. 17:9063-9073[Abstract/Free Full Text].
7. Guerrero, C., C. Bernasconi, D. Burki, T. Bodmer, and A. Telenti. 1995. A novel insertion element from Mycobacterium avium, IS1245, is a specific target for analysis of strain relatedness. J. Clin. Microbiol. 33:304-307[Abstract].
8. Hermans, P. W. M., F. Massadi, H. Guebrexabher, D. van Soolingen, P. E. W. de Haas, H. Heersma, H. de Neeling, A. Ayoub, F. Portaels, D. Frommel, M. Zribi, and J. D. A. van Embden. 1995. Analysis of the population structure of Mycobacterium tuberculosis in Ethiopia, Tunisia, and the Netherlands: usefulness of DNA typing for global tuberculosis epidemiology. J. Infect. Dis. 171:1504-1513[Medline].
9. Hernandez Perez, M., N. G. Fomukong, T. Hellyer, I. N. Brown, and J. W. Dale. 1994. Characterisation of IS1110, a highly mobile genetic element from Mycobacterium avium. Mol. Microbiol. 12:717-724[Medline].
10. Hoffner, S. E., G. Kallenius, B. Petrini, P. J. Brennan, and A. Y. Tsang. 1990. Serovar of Mycobacterium avium complex isolated from patients in Sweden. J. Clin. Microbiol. 28:1105-1107[Abstract/Free Full Text].
11. Horsburgh, C. R., Jr., D. P. Chin, D. M. Yajko, P. C. Hopewell, P. S. Nassos, E. P. Elkin, W. K. Hadley, E. N. Stone, E. M. Simon, P. Gonzalez, S. Ostroff, and A. L. Reingold. 1994. Environmental risk factors for acquisition of Mycobacterium avium complex in persons with human immunodeficiency virus infection. J. Infect. Dis. 170:362-367[Medline].
12. Inderlied, C. B., C. A. Kemper, and L. E. M. Bermudez. 1993. The Mycobacterium avium complex. Clin. Microbiol. Rev. 6:266-310[Abstract/Free Full Text].
13. Kunze, Z. M., S. Wall, R. Wallenberg, M. T. Silva, F. Portaels, and J. J. McFadden. 1992. IS901, a member of a widespread class of atypical insertion sequences, is associated with pathogenicity in Mycobacterium avium. Mol. Microbiol. 5:2265-2272.
14. Mazurek, G. H., S. Hartman, Y. Zhang, B. A. Brown, J. S. R. Hector, D. Murphy, and R. J. Wallace, Jr. 1993. Large DNA selection fragment polymorphism in the Mycobacterium avium-M. intracellulare complex: a potential epidemiological tool. J. Clin. Microbiol. 31:390-394[Abstract/Free Full Text].
15. Moss, M. T., Z. P. Malik, M. L. V. Tizard, E. P. Green, J. D. Sanderson, and J. Hermon-Taylor. 1992. IS902, an insertion element of the chronic-enteritis-causing Mycobacterium avium subsp. silvaticum. J. Gen. Microbiol. 138:139-145[Abstract/Free Full Text].
16. Picardeau, M., A. Varnerot, T. Lecompte, E. Brel, T. May, and V. Vincent. 1997. Use of different molecular typing techniques for bacteriological follow-up in a clinical trial with AIDS patients with Mycobacterium avium bacteriemia. J. Clin. Microbiol. 35:2503-2510[Abstract].
17. Picardeau, M., and V. Vincent. 1996. Typing of Mycobacterium avium isolates by PCR. J. Clin. Microbiol. 34:389-392[Abstract].
18. Ritacco, V., K. Kremer, T. van der Laan, J. E. M. Pijnenburg, P. E. W. de Haas, and D. van Soolingen. 1998. Use of IS901 and IS1245 in RFLP typing of Mycobacterium avium complex: relatedness among serovar reference strains, human and animal isolates. Int. J. Tubercle Lung Dis. 2:242-251.
19. Roiz, M. P., E. Palenque, C. Guerrero, and M. J. Garcia. 1995. Use of restriction fragment length polymorphism as a genetic marker for typing Mycobacterium avium strains. J. Clin. Microbiol. 33:1389-1391[Abstract].
20. Slutsky, A. M., R. D. Arbeit, T. W. Barber, J. Rich, C. Fordham von Reyn, W. Pieciak, M. A. Barlow, and J. N. Marlow. 1994. Polyclonal infections due to Mycobacterium avium complex in patients with AIDS detected by pulsed-field gel electrophoresis of sequential clinical isolates. J. Clin. Microbiol. 32:1773-1778[Abstract/Free Full Text].
21. Sola, C., A. Devallois, K. S. Gob, E. Legrand, and N. Rastogi. 1996. Molecular characterization of Mycobacterium avium complex isolates from Caribbean patients by DT1/DT6 - PCR, nonradioactive Southern hybridization and the Accuprobe system. Curr. Microbiol. 33:352-358[Medline].
22. Thorel, M. F., M. Kriechevsky, and V. V. Levi-Frebault. 1990. Numerical taxonomy of mycobactin-dependent mycobacteria, emended description of Mycobacterium avium, and description of Mycobacterium avium subsp. avium subsp. nov., Mycobacterium avium subsp. paratuberculosis subsp. nov., and Mycobacterium avium subsp. silvaticum subsp. nov. Int. J. Syst. Bacteriol. 40:254-260[Abstract/Free Full Text].
23. Van Embden, J. D. A., M. D. Cave, J. T. Crawford, J. W. Dale, K. D. Eisenach, B. Gicquel, P. Hermans, C. Martin, R. McAdam, T. M. 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[Abstract/Free Full Text].
24. 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[Medline].
25. Van Soolingen, D., L. Qian, P. E. W. de Haas, J. T. Douglas, H. Traore, F. Portaels, H. Z. Qing, D. Enkhsaikan, 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[Abstract].
26. Via, L. E., and J. O. Falkingham III. 1993. Genbank accession no. L10239.
27. Von Reyn, C. F., J. N. Maslow, T. W. Barber, J. O. Falkingham III, and R. D. Arbeit. 1994. Persistent colonisation of potable water as a source of Mycobacterium avium infection in AIDS. Lancet 343:1137-1141[Medline].
28. Wasem, C. H., C. M. McCarthy, and L. W. Murray. 1991. Multilocus enzyme electrophoresis analysis of the Mycobacterium avium complex and other mycobacteria. J. Clin. Microbiol. 29:264-271[Abstract/Free Full Text].
29. Wayne, L. G., R. C. Good, A. Tsang, R. Butler, D. Dawson, D. Groothuis, W. Gross, J. Hawkins, J. Kilburn, M. Kubin, K. H. Schroder, V. A. Silcox, C. Smith, M. F. Thorel, C. Woodley, and M. A. Yakrus. 1993. Serovar determination and molecular taxonomic correlation in Mycobacterium avium, Mycobacterium intracellulare, and Mycobacterium scrofulaceum: a cooperative study of the International Working Group on Mycobacterial Taxonomy. Int. J. Syst. Bacteriol. 43:482-489[Abstract/Free Full Text].

Journal of Clinical Microbiology, October 1998, p. 3051-3054, Vol. 36, No. 10
0095-1137/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Inagaki, T., Nishimori, K., Yagi, T., Ichikawa, K., Moriyama, M., Nakagawa, T., Shibayama, T., Uchiya, K.-i., Nikai, T., Ogawa, K. (2009). Comparison of a Variable-Number Tandem-Repeat (VNTR) Method for Typing Mycobacterium avium with Mycobacterial Interspersed Repetitive-Unit-VNTR and IS1245 Restriction Fragment Length Polymorphism Typing. J. Clin. Microbiol. 47: 2156-2164 [Abstract] [Full Text]  
  • Domingos, M., Amado, A., Botelho, A. (2009). IS1245 RFLP analysis of strains of Mycobacterium avium subspecies hominissuis isolated from pigs with tuberculosis lymphadenitis in Portugal. Vet Rec. 164: 116-120 [Abstract] [Full Text]  
  • Alvarez, J., Garcia, I. G., Aranaz, A., Bezos, J., Romero, B., de Juan, L., Mateos, A., Gomez-Mampaso, E., Dominguez, L. (2008). Genetic Diversity of Mycobacterium avium Isolates Recovered from Clinical Samples and from the Environment: Molecular Characterization for Diagnostic Purposes. J. Clin. Microbiol. 46: 1246-1251 [Abstract] [Full Text]  
  • Turenne, C. Y., Wallace, R. Jr., Behr, M. A. (2007). Mycobacterium avium in the Postgenomic Era. Clin. Microbiol. Rev. 20: 205-229 [Abstract] [Full Text]  
  • Elias, J., Vogel, U. (2007). IS1301 Fingerprint Analysis of Neisseria meningitidis Strains Belonging to the ET-15 Clone. J. Clin. Microbiol. 45: 159-167 [Abstract] [Full Text]  
  • Glawischnig, W., Steineck, T., Spergser, J. (2006). INFECTIONS CAUSED BY MYCOBACTERIUM AVIUM SUBSPECIES AVIUM, HOMINISSUIS, AND PARATUBERCULOSIS IN FREE-RANGING RED DEER (CERVUS ELAPHUS HIPPELAPHUS) IN AUSTRIA, 2001-2004. J Wildl Dis 42: 724-731 [Abstract] [Full Text]  
  • Murcia, M. I., Tortoli, E., Menendez, M. C., Palenque, E., Garcia, M. J. (2006). Mycobacterium colombiense sp. nov., a novel member of the Mycobacterium avium complex and description of MAC-X as a new ITS genetic variant.. Int. J. Syst. Evol. Microbiol. 56: 2049-2054 [Abstract] [Full Text]  
  • Semret, M., Turenne, C. Y., de Haas, P., Collins, D. M., Behr, M. A. (2006). Differentiating Host-Associated Variants of Mycobacterium avium by PCR for Detection of Large Sequence Polymorphisms.. J. Clin. Microbiol. 44: 881-887 [Abstract] [Full Text]  
  • Semret, M., Turenne, C. Y., Behr, M. A. (2006). Insertion Sequence IS900 Revisited.. J. Clin. Microbiol. 44: 1081-1083 [Abstract] [Full Text]  
  • Turenne, C. Y., Semret, M., Cousins, D. V., Collins, D. M., Behr, M. A. (2006). Sequencing of hsp65 Distinguishes among Subsets of the Mycobacterium avium Complex. J. Clin. Microbiol. 44: 433-440 [Abstract] [Full Text]  
  • Johansen, T. B., Djonne, B., Jensen, M. R., Olsen, I. (2005). Distribution of IS1311 and IS1245 in Mycobacterium avium Subspecies Revisited. J. Clin. Microbiol. 43: 2500-2502 [Abstract] [Full Text]  
  • Matlova, L., Dvorska, L., Ayele, W. Y., Bartos, M., Amemori, T., Pavlik, I. (2005). Distribution of Mycobacterium avium Complex Isolates in Tissue Samples of Pigs Fed Peat Naturally Contaminated with Mycobacteria as a Supplement. J. Clin. Microbiol. 43: 1261-1268 [Abstract] [Full Text]  
  • Tortoli, E., Rindi, L., Garcia, M. J., Chiaradonna, P., Dei, R., Garzelli, C., Kroppenstedt, R. M., Lari, N., Mattei, R., Mariottini, A., Mazzarelli, G., Murcia, M. I., Nanetti, A., Piccoli, P., Scarparo, C. (2004). Proposal to elevate the genetic variant MAC-A, included in the Mycobacterium avium complex, to species rank as Mycobacterium chimaera sp. nov.. Int. J. Syst. Evol. Microbiol. 54: 1277-1285 [Abstract] [Full Text]  
  • Cangelosi, G. A., Freeman, R. J., Lewis, K. N., Livingston-Rosanoff, D., Shah, K. S., Milan, S. J., Goldberg, S. V. (2004). Evaluation of a High-Throughput Repetitive-Sequence-Based PCR System for DNA Fingerprinting of Mycobacterium tuberculosis and Mycobacterium avium Complex Strains. J. Clin. Microbiol. 42: 2685-2693 [Abstract] [Full Text]  
  • Krzywinska, E., Krzywinski, J., Schorey, J. S. (2004). Phylogeny of Mycobacterium avium strains inferred from glycopeptidolipid biosynthesis pathway genes. Microbiology 150: 1699-1706 [Abstract] [Full Text]  
  • Motiwala, A. S., Strother, M., Amonsin, A., Byrum, B., Naser, S. A., Stabel, J. R., Shulaw, W. P., Bannantine, J. P., Kapur, V., Sreevatsan, S. (2003). Molecular Epidemiology of Mycobacterium avium subsp. paratuberculosis: Evidence for Limited Strain Diversity, Strain Sharing, and Identification of Unique Targets for Diagnosis. J. Clin. Microbiol. 41: 2015-2026 [Abstract] [Full Text]  
  • Oliveira, R. S., Sircili, M. P., Oliveira, E. M. D., Balian, S. C., Ferreira-Neto, J. S., Leao, S. C. (2003). Identification of Mycobacterium avium Genotypes with Distinctive Traits by Combination of IS1245-Based Restriction Fragment Length Polymorphism and Restriction Analysis of hsp65. J. Clin. Microbiol. 41: 44-49 [Abstract] [Full Text]  
  • Gazouli, M., Ikonomopoulos, J., Trigidou, R., Foteinou, M., Kittas, C., Gorgoulis, V. (2002). Assessment of Mycobacterial, Propionibacterial, and Human Herpesvirus 8 DNA in Tissues of Greek Patients with Sarcoidosis. J. Clin. Microbiol. 40: 3060-3063 [Abstract] [Full Text]  
  • Keller, A. P., Beggs, M. L., Amthor, B., Bruns, F., Meissner, P., Haas, W. H. (2002). Evidence of the Presence of IS1245 and IS1311 or Closely Related Insertion Elements in Nontuberculous Mycobacteria outside of the Mycobacterium avium Complex. J. Clin. Microbiol. 40: 1869-1872 [Abstract] [Full Text]  
  • Menendez, M. C., Palenque, E., Navarro, M. C., Nunez, M. C., Rebollo, M. J., Garcia, M. J. (2001). Characterization of a Mycobacterium intracellulare Variant Strain by Molecular Techniques. J. Clin. Microbiol. 39: 4241-4246 [Abstract] [Full Text]  
  • Oliveira, R. S., Sircili, M. P., Ueki, S. Y. M., Telles, M. A. S., Schnabel, B., Briones, M. R. S., Leão, S. C. (2000). PCR-Restriction Enzyme Analysis of a Bone Marrow Isolate from a Human Immunodeficiency Virus-Positive Patient Discloses Polyclonal Infection with Two Mycobacterium avium Strains. J. Clin. Microbiol. 38: 4643-4645 [Abstract] [Full Text]  
  • NOVI, C., RINDI, L., LARI, N., GARZELLI, C. (2000). Molecular typing of Mycobacterium avium isolates by sequencing of the 16S-23S rDNA internal transcribed spacer and comparison with IS1245-based fingerprinting. J Med Microbiol 49: 1091-1095 [Abstract] [Full Text]  
  • Coetsier, C., Vannuffel, P., Blondeel, N., Denef, J.-F., Cocito, C., Gala, J.-L. (2000). Duplex PCR for Differential Identification of Mycobacterium bovis, M. avium, and M. avium subsp. paratuberculosis in Formalin- Fixed Paraffin-Embedded Tissues from Cattle. J. Clin. Microbiol. 38: 3048-3054 [Abstract] [Full Text]  
  • Komijn, R. E., de Haas, P. E. W., Schneider, M. M. E., Eger, T., Nieuwenhuijs, J. H. M., van den Hoek, R. J., Bakker, D., van Zijd Erveld, F. G., van Soolingen, D. (1999). Prevalence of Mycobacterium avium in Slaughter Pigs in The Netherlands and Comparison of IS1245 Restriction Fragment Length Polymorphism Patterns of Porcine and Human Isolates. J. Clin. Microbiol. 37: 1254-1259 [Abstract] [Full Text]  
  • Bauer, J., Andersen, A. B., Askgaard, D., Giese, S. B., Larsen, B. (1999). Typing of Clinical Mycobacterium avium Complex Strains Cultured during a 2-Year Period in Denmark by Using IS1245. J. Clin. Microbiol. 37: 600-605 [Abstract] [Full Text]  
  • Bauer, J., Andersen, A. B. (1999). Stability of Insertion Sequence IS1245, a Marker for Differentiation of Mycobacterium avium Strains. J. Clin. Microbiol. 37: 442-444 [Abstract] [Full Text]  

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by van Soolingen, D.
Right arrow Articles by Garcia, M. J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by van Soolingen, D.
Right arrow Articles by Garcia, M. J.

Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»