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, 40 (9), 3398-405

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

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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 et al. J Clin Microbiol.

Abstract

The population structure of 234 Mycobacterium tuberculosis complex strains obtained during 1995 and 1997 from tuberculosis patients living in Kampala, Uganda (East Africa), was analyzed by routine laboratory procedures, spoligotyping, and IS6110 restriction fragment length polymorphism (RFLP) typing. According to biochemical test results, 157 isolates (67%) were classified as M. africanum subtype II (resistant to thiophen-2-carboxylic acid hydrazide), 76 isolates (32%) were classified as M. tuberculosis, and 1 isolate was classified as classical M. bovis. Spoligotyping did not lead to clear differentiation of M. tuberculosis and M. africanum, but all M. africanum subtype II isolates lacked spacers 33 to 36, differentiating them from M. africanum subtype I. Moreover, spoligotyping was not sufficient for differentiation of isolates on the strain level, since 193 (82%) were grouped into clusters. In contrast, in the IS6110-based dendrogram, M. africanum strains were clustered into two closely related strain families (Uganda I and II) and clearly separated from the M. tuberculosis isolates. A further characteristic of both M. africanum subtype II families was the absence of spoligotype spacer 40. All strains of family I also lacked spacer 43. The clustering rate obtained by the combination of spoligotyping and RFLP IS6110 analysis was similar for M. africanum and M. tuberculosis, as 46% and 49% of the respective isolates were grouped into clusters. The results presented demonstrate that M. africanum subtype II isolates from Kampala, Uganda, belong to two closely related genotypes, which may represent unique phylogenetic branches within the M. tuberculosis complex. We conclude that M. africanum subtype II is the main cause of human tuberculosis in Kampala, Uganda.

Figures

FIG. 1.
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.
FIG. 2.
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.
FIG. 3.
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.
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.

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