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Mycobacteriology and Aerobic Actinomycetes

Mycobacterium africanum Subtype II Is Associated with Two Distinct Genotypes and Is a Major Cause of Human Tuberculosis in Kampala, Uganda

S. Niemann, S. Rüsch-Gerdes, M. L. Joloba, C. C. Whalen, D. Guwatudde, J. J. Ellner, K. Eisenach, N. Fumokong, J. L. Johnson, T. Aisu, R. D. Mugerwa, A. Okwera, S. K. Schwander
S. Niemann
1National Reference Center for Mycobacteria, Research Center Borstel, Borstel, Germany
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  • For correspondence: sniemann@fz-borstel.de
S. Rüsch-Gerdes
1National Reference Center for Mycobacteria, Research Center Borstel, Borstel, Germany
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M. L. Joloba
2Departments of Medicine and Medical Microbiology, Makerere University, Kampala, Uganda
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C. C. Whalen
3Departments of Epidemiology and Biostatistics and of Medicine, Case Western Reserve University School of Medicine, Cleveland, Ohio 44106
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D. Guwatudde
2Departments of Medicine and Medical Microbiology, Makerere University, Kampala, Uganda
3Departments of Epidemiology and Biostatistics and of Medicine, Case Western Reserve University School of Medicine, Cleveland, Ohio 44106
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J. J. Ellner
4Department of Medicine and Ruy V. Lourenco Center for the Study of Emerging and Reemerging Pathogens, University of Medicine and Dentistry-New Jersey Medical School, Newark, New Jersey 07103
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K. Eisenach
5Departments of Pathology and Immunology, University of Arkansas for Medical Sciences, Little Rock, Arkansas 72205
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N. Fumokong
5Departments of Pathology and Immunology, University of Arkansas for Medical Sciences, Little Rock, Arkansas 72205
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J. L. Johnson
3Departments of Epidemiology and Biostatistics and of Medicine, Case Western Reserve University School of Medicine, Cleveland, Ohio 44106
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T. Aisu
2Departments of Medicine and Medical Microbiology, Makerere University, Kampala, Uganda
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R. D. Mugerwa
2Departments of Medicine and Medical Microbiology, Makerere University, Kampala, Uganda
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A. Okwera
2Departments of Medicine and Medical Microbiology, Makerere University, Kampala, Uganda
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S. K. Schwander
4Department of Medicine and Ruy V. Lourenco Center for the Study of Emerging and Reemerging Pathogens, University of Medicine and Dentistry-New Jersey Medical School, Newark, New Jersey 07103
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DOI: 10.1128/JCM.40.9.3398-3405.2002
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  • FIG. 1.
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    FIG. 1.

    Spoligotype patterns of the 233 M. tuberculosis (darker shading) and M. africanum subtype II (lighter shading) strains. Banding patterns are ordered by similarity in a dendrogram. The position of each spoligotyping hybridization spot is normalized so that banding patterns of all strains are mutually comparable. The scale depicts similarity of patterns calculated with the Dice coefficient and the UPGMA method.

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    FIG. 2.

    Spoligotype (a) and IS6110 RFLP (b) patterns of four pairs of M. tuberculosis and M. africanum subtype II strains. M. tuberculosis and M. africanum subtype II strains had very similar spoligotype patterns but were clearly separated by IS6110 RFLP typing.

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    FIG. 3.

    IS6110 DNA fingerprint patterns of the 233 M. tuberculosis (darker shading) and M. africanum subtype II (lighter shading) strains. Banding patterns are ordered by similarity in a dendrogram. M. africanum subtype II strains were clustered in two closely related strain families (genotypes Uganda I and II) and were clearly separated from the M. tuberculosis strains.

  • FIG. 4.
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    FIG. 4.

    Representative spoligotype patterns of M. africanum subtype II strains of genotypes Uganda I and II (C and D) compared to spoligotype patterns of type strains M. tuberculosis H37 (ATCC 27294), M. bovis (ATCC 19210), M. bovis BCG (ATCC 27289), M. africanum (ATCC 25420), and a collection of M. africanum subtype I (A) and M. africanum subtype II (B) isolates from our previous work (15). In contrast to M. bovis, all M. africanum strains showed hybridization to several of the spacers 39 to 43 which were derived from the direct repeat (DR) region of M. tuberculosis H37. In the case of M. africanum subtype II, no hybridization was observed to the M. bovis BCG-derived spacers 33 to 36, whereas M. africanum subtype I isolates as well as the M. africanum type strain (ATCC 25420) showed hybridization to at least two of these spacers. All M. africanum subtype II strains showed a characteristic lack of hybridization to spacer 40. Strains of genotype Uganda I lack spacer 43 in addition (arrows). In contrast, M. africanum subtype I strains lack spacer 39.

Tables

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  • TABLE 1.

    Biochemical characteristics of type strains M. tuberculosis H37 (ATCC 27294), M. bovis (ATCC 19210), and M. africanum (ATCC 25420) and the strains analyzeda

    Organism and group (no. of strains)Test result (% of isolates)
    Niacin accumulationNitrate reductionGrowth in presence of:Colony morphologyChange of color of bromocresol mediumGrowth on Lebek mediumMean catalase activityb ± SD
    TCHPZA
    M. tuberculosis H37 (ATCC 27294)+++−Eugonic+Aerophilic6.0
    M. bovis (ATCC 19210)−−−+Dysgonic−Microaerophilic0.1
    M. africanum (ATCC 25420)−±−−Dysgonic−Microaerophilic0.2
    M. tuberculosis (76)+ (100)+ (100)+ (100)− (97), + (3)cEugonic (100)+ (100)Aerophilic (100)3.0 ± 1.2
    M. bovis (1)−−−+Dysgonic−Mircroaerophilic0.1
    M. africanum subtype II Uganda I (55)+ (7), ± (87), − (6)+ (100)+ (100)− (100)Dysgonic (100)− (100)Microaerophilic (100)0.5 ± 0.2
    M. africanum subtype II Uganda II (102)+ (5), ± (91), − (4)+ (100)+ (100)− (100)Dysgonic (100)− (100)Mircroaerophilic (100)0.5 ± 0.2
    • ↵ a Abbreviations and symbols: +, positive test result; −, negative test result; ±, weakly positive; PZA, pyrazinamide. One M. tuberculosis isolate, three M. africanum subtype II Uganda I, and two Uganda II isolates were resistant to isoniazid and cross-resistant to TCH.

    • ↵ b Centimeters of foam production at room temperature.

    • ↵ c Strains were resistant to isoniazid, streptomycin, and pyrazinamide.

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Mycobacterium africanum Subtype II Is Associated with Two Distinct Genotypes and Is a Major Cause of Human Tuberculosis in Kampala, Uganda
S. Niemann, S. Rüsch-Gerdes, M. L. Joloba, C. C. Whalen, D. Guwatudde, J. J. Ellner, K. Eisenach, N. Fumokong, J. L. Johnson, T. Aisu, R. D. Mugerwa, A. Okwera, S. K. Schwander
Journal of Clinical Microbiology Sep 2002, 40 (9) 3398-3405; DOI: 10.1128/JCM.40.9.3398-3405.2002

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Mycobacterium africanum Subtype II Is Associated with Two Distinct Genotypes and Is a Major Cause of Human Tuberculosis in Kampala, Uganda
S. Niemann, S. Rüsch-Gerdes, M. L. Joloba, C. C. Whalen, D. Guwatudde, J. J. Ellner, K. Eisenach, N. Fumokong, J. L. Johnson, T. Aisu, R. D. Mugerwa, A. Okwera, S. K. Schwander
Journal of Clinical Microbiology Sep 2002, 40 (9) 3398-3405; DOI: 10.1128/JCM.40.9.3398-3405.2002
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KEYWORDS

Bacterial Typing Techniques
mycobacterium
Oligonucleotides
Polymorphism, Restriction Fragment Length
Tuberculosis, Pulmonary

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