Mycobacterium africanum--review of an important cause of human tuberculosis in West Africa

Bouke C de Jong, Martin Antonio, Sebastien Gagneux, Bouke C de Jong, Martin Antonio, Sebastien Gagneux

Abstract

Mycobacterium africanum consists of two phylogenetically distinct lineages within the Mycobacterium tuberculosis complex, known as M. africanum West African 1 and M. africanum West African 2. These lineages are restricted to West Africa, where they cause up to half of human pulmonary tuberculosis. In this review we discuss the definition of M. africanum, describe the prevalence and restricted geographical distribution of M. africanum West African 1 and 2, review the occurrence of M. africanum in animals, and summarize the phenotypic differences described thus far between M. africanum and M. tuberculosis sensu stricto.

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Figure 1. Nomenclature of M. africanum as…
Figure 1. Nomenclature of M. africanum as related to its biochemical and molecular classification.
Biochemical classification is reviewed in Table 1. LSPs, large sequence polymorphisms . Spoligotype signatures are reviewed in .
Figure 2. The position of M. africanum…
Figure 2. The position of M. africanum in the global phylogeny of the M. tuberculosis complex (MTBC) as originally published by Hershberg et al..
This phylogeny is based on over 65 kb of DNA sequence data (89 concatenated gene sequences) in each of 108 strains of the MTBC and was inferred using maximum parsimony, which resulted in a single tree with negligable homoplasy . Analysis by the neighbor-joining method resulted in an identical tree topology with high statistical support for all main branches . This phylogeny has been referred to as the most robust and most detailed phylogeny of the MTBC to date, and thus should be considered as the new gold standard for classification of the MTBC . The six main MTBC lineages adapted to humans and the animal strains are indicated in different colors. The human MTBC lineages include four M. tuberculosis lineages and the two M. africanum type I lineages. The “Uganda” genotype (formally referred to as M. africanum type II), which is a sub-lineage within M. tuberculosis lineage 4 (also known as the Euro-American lineage), is also shown. These lineages are completely congruent to previous classifications based on LSPs , , . Black arrows indicate genomic regions or regions of difference (RDs) that are deleted in all descendent strains belonging to a particular lineage or sub-lineage. The scale indicates the genetic distance as number of SNPs (adapted from Figure 1 in with additional data from [5]).
Figure 3. M. africanum prevalence in Western…
Figure 3. M. africanum prevalence in Western African countries.
Prevalence figures were derived from the most recently published studies from Table 2 and unpublished data from Tunisia, Senegal, Cote d'Ivoire, Cameroon, and the Central African Republic extracted from the SITVIT2 proprietary database of Institut Pasteur de la Guadeloupe. If studies did not list the prevalence of MAF1 and/or MAF2, the estimates were based on interpretation of the spoligotype patterns. Areas with MAF1 are shaded in brown and areas with MAF2 are shaded in green, with striped shading if prevalence of MAF1 and MAF2 exceeds 5% each. Map courtesy of http://www.theodora.com/maps/, used with permission.

References

    1. Kallenius G, Koivula T, Ghebremichael S, Hoffner SE, Norberg R, et al. Evolution and clonal traits of Mycobacterium tuberculosis complex in Guinea-Bissau. J Clin Microbiol. 1999;37:3872–3878.
    1. de Jong BC, Antonio M, Awine T, Ogungbemi K, de Jong YP, et al. Use of spoligotyping and large-sequence polymorphisms to study the population structure of the Mycobacterium tuberculosis complex in a cohort study of consecutive smear positive tuberculosis cases in the Gambia. J Clin Microbiol 2009
    1. Castets M, Boisvert H, Grumbach F, Brunel M, Rist N. [Tuberculosis bacilli of the African type: preliminary note]. Rev Tuberc Pneumol (Paris) 1968;32:179–184.
    1. Mostowy S, Onipede A, Gagneux S, Niemann S, Kremer K, et al. Genomic analysis distinguishes Mycobacterium africanum. J Clin Microbiol. 2004;42:3594–3599.
    1. Gagneux S, DeRiemer K, Van T, Kato-Maeda M, de Jong BC, et al. Variable host-pathogen compatibility in Mycobacterium tuberculosis. Proc Natl Acad Sci U S A. 2006;103:2869–2873.
    1. Castets M. [Mycobacterium africanum (author's transl)]. Med Trop (Mars) 1979;39:145–148.
    1. Onipede AO, de Jong BC, Adegbola RA. Mycobacterium africanum- a review. African Journal of Clinical and Experimental Microbiology. 2005;6:167–175.
    1. Pattyn SR, Portaels F, Spanoghe L, Magos J. Further studies on African strains of Mycobacterium tuberculosis: comparison with M. bovis and M. microti. Ann Soc Belges Med Trop Parasitol Mycol. 1970;50:211–227.
    1. Meissner G, Schroder K. [The so-called African mycobacteria strains from the tropical West Africa]. Zentralbl Bakteriol Orig. 1969;211:69–81.
    1. Grosset J, Decroix G, Sors C. [Tuberculosis due to Mycobacterium africanum in African negroes in the Paris area]. Rev Tuberc Pneumol (Paris) 1971;35:430–436.
    1. Grosset J, Sangare S, Rist N, Meyer L. Cultural and Biochemical Characteristics of Tubercle Bacilli Isolated From 230 Cases of Tuberculosis in Mali. Bull Int Union Tuberc. 1974;49:177–187.
    1. Van Der Groen G, Pattyn SR. Comparison of Mycobacterium africanum, M. tuberculosis and M. bovis by their utilization of carbon and nitrogen sources. Ann Soc Belg Med Trop. 1975;55:647–651.
    1. Toure IM. [The status of Mycobacterium africanum in West Africa]. Bull Int Union Tuberc. 1982;57:241–249.
    1. David HL, Jahan MT, Jumin A, Grandry J, Lehman HE. Numerical Taxonomy Analysis of Mycobacterium africanum. International Journal of Systematic Bacteriology. 1978;28:467–472.
    1. Comas I, Homolka S, Niemann S, Gagneux S. Genotyping of genetically monomorphic bacteria: DNA sequencing in mycobacterium tuberculosis highlights the limitations of current methodologies. PLoS ONE. 2009;4:e7815. doi: .
    1. Streicher EM, Victor TC, van der Spuy G, Sola C, Rastogi N, et al. Spoligotype signatures in the Mycobacterium tuberculosis complex. J Clin Microbiol. 2007;45:237–240.
    1. Frothingham R, Strickland PL, Bretzel G, Ramaswamy S, Musser JM, et al. Phenotypic and genotypic characterization of Mycobacterium africanum isolates from West Africa. J Clin Microbiol. 1999;37:1921–1926.
    1. Viana-Niero C, Gutierrez C, Sola C, Filliol I, Boulahbal F, et al. Genetic diversity of Mycobacterium africanum clinical isolates based on IS6110-restriction fragment length polymorphism analysis, spoligotyping, and variable number of tandem DNA repeats. J Clin Microbiol. 2001;39:57–65.
    1. Tsolaki AG, Hirsh AE, DeRiemer K, Enciso JA, Wong MZ, et al. Functional and evolutionary genomics of Mycobacterium tuberculosis: insights from genomic deletions in 100 strains. Proc Natl Acad Sci U S A. 2004;101:4865–4870.
    1. Gagneux S, Small PM. Global phylogeography of Mycobacterium tuberculosis and implications for tuberculosis product development. Lancet Infect Dis. 2007;7:328–337.
    1. Brosch R, Gordon SV, Marmiesse M, Brodin P, Buchrieser C, et al. A new evolutionary scenario for the Mycobacterium tuberculosis complex. Proc Natl Acad Sci U S A. 2002;99:3684–3689.
    1. Mostowy S, Cousins D, Brinkman J, Aranaz A, Behr MA. Genomic deletions suggest a phylogeny for the Mycobacterium tuberculosis complex. J Infect Dis. 2002;186:74–80.
    1. Hershberg R, Lipatov M, Small PM, Sheffer H, Niemann S, et al. High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography. PLoS Biol. 2008;6:e311. doi: .
    1. Huard RC, Fabre M, de Haas P, Lazzarini LC, van Soolingen D, et al. Novel genetic polymorphisms that further delineate the phylogeny of the Mycobacterium tuberculosis complex. J Bacteriol. 2006;188:4271–4287.
    1. Goncalves Vasconcellos SE, Huard RC, Niemann S, Kremer K, Santos AR, et al. Distinct genotypic profiles of the two major clades of Mycobacterium africanum. BMC Infect Dis. 2010;10:80.
    1. Nerlich AG, Losch S. Paleopathology of human tuberculosis and the potential role of climate. Interdiscip Perspect Infect Dis. 2009;2009:437187.
    1. Zink AR, Sola C, Reischl U, Grabner W, Rastogi N, et al. Characterization of Mycobacterium tuberculosis complex DNAs from Egyptian mummies by spoligotyping. J Clin Microbiol. 2003;41:359–367.
    1. Pattyn SR, Keterew W, Hadgu AG, Van Den Breen L. Identification and drug sensitivity of tubercle bacilli from Addis Ababa, Ethiopia. Ann Soc Belg Med Trop. 1978;58:59–62.
    1. Demers AM, Mostowy S, Coetzee D, Warren R, van Helden P, et al. Mycobacterium africanum is not a major cause of human tuberculosis in Cape Town, South Africa. Tuberculosis (Edinb) 2010
    1. Diop S, de Medeiros D, de Medeiros G, Baylet R, Sankale M. [Incidence and geographic distribution of Mycobacterium africanum in Senegal]. Bull Soc Med Afr Noire Lang Fr. 1976;21:50–56.
    1. Huet M, Rist N, Boube G, Potier D. [Bacteriological study of tuberculosis in Cameroon]. Rev Tuberc Pneumol (Paris) 1971;35:413–426.
    1. Niobe-Eyangoh SN, Kuaban C, Sorlin P, Cunin P, Thonnon J, et al. Genetic biodiversity of Mycobacterium tuberculosis complex strains from patients with pulmonary tuberculosis in Cameroon. J Clin Microbiol. 2003;41:2547–2553.
    1. Goyal M, Lawn S, Afful B, Acheampong JW, Griffin G, et al. Spoligotyping in molecular epidemiology of tuberculosis in Ghana. J Infect. 1999;38:171–175.
    1. Affolabi D, Anyo G, Faihun F, Sanoussi N, Shamputa IC, et al. First molecular epidemiological study of tuberculosis in Benin. Int J Tuberc Lung Dis. 2009;13:317–322.
    1. Jungbluth H, Fink H, Reusch F. [Tuberculous infection caused by Myco. africanum in black africans resident in the German Federal Republic (author's transl)]. Prax Klin Pneumol. 1978;32:306–309.
    1. Schroder KH. [Occurence of M. africanum in the Federal Republic of Germany (author's transl)]. Zentralbl Bakteriol Mikrobiol Hyg [A] 1982;251:341–344.
    1. Grange JM, Yates MD. Incidence and nature of human tuberculosis due to Mycobacterium africanum in South-East England: 1977-87. Epidemiol Infect. 1989;103:127–132.
    1. Desmond E, Ahmed AT, Probert WS, Ely J, Jang Y, et al. Mycobacterium africanum cases, California. Emerg Infect Dis. 2004;10:921–923.
    1. Frottier J, Eliaszewicz M, Arlet V, Gaudillat C. [Infections caused by Mycobacterium africanum]. Bull Acad Natl Med. 1990;174:29–33; discussion 34–25.
    1. Perez-de Pedro I, Bermudez P, Artero I, Jimenez MS. [Orchiepididymitis due to Mycobacterium africanum]. Enferm Infecc Microbiol Clin. 2008;26:600–602.
    1. Reparaz J, Olivan AS, Pinillos MA, Uriz J, Lopez-Unzu MJ, et al. [Disseminated Mycobacterium africanum infection]. Rev Med Univ Navarra. 1987;31:103–105.
    1. Baril L, Caumes E, Truffot-Pernot C, Bricaire F, Grosset J, et al. Tuberculosis caused by Mycobacterium africanum associated with involvement of the upper and lower respiratory tract, skin, and mucosa. Clin Infect Dis. 1995;21:653–655.
    1. Remacha Esteras MA, Parra Parra I, Blanco Mercade MD. [Disseminated tuberculosis due to Mycobacterium africanum]. Arch Bronconeumol. 2003;39:376.
    1. Aldea MJ, Lezcano MA, Esteban A, Bello S, Vila M, et al. [Pleuropulmonary tuberculosis caused by Mycobacterium africanum in a white male]. Enferm Infecc Microbiol Clin. 1990;8:64–65.
    1. Petit JC, Lesage D, et al. Bone tuberculosis due to Mycobacterium africanum- 2 cases. Nouvelle Presse Medicale. 1980;9:2845.
    1. Bhanot N, Badem O, Mathew L, Haran M. Mycobacterium africanum Presenting as a Brain Mass. Infect Dis Clin Pract. 2008;16:327–329.
    1. Janier M, Wagner L, et al. Ulcerative tuberculosis of the anal canal due to Mycobacterium africanum. Annales De Dermatologie Et De Venereologie. 1987;114:1395–1397.
    1. Brudey K, Driscoll JR, Rigouts L, Prodinger WM, Gori A, et al. Mycobacterium tuberculosis complex genetic diversity: mining the fourth international spoligotyping database (SpolDB4) for classification, population genetics and epidemiology. BMC Microbiol. 2006;6:23.
    1. Meyer CG, Scarisbrick G, Niemann S, Browne EN, Chinbuah MA, et al. Pulmonary tuberculosis: virulence of Mycobacterium africanum and relevance in HIV co-infection. Tuberculosis (Edinb) 2008;88:482–489.
    1. Bercion R, Kuaban C. Initial resistance to antituberculosis drugs in Yaounde, Cameroon in 1995. Int J Tuberc Lung Dis. 1997;1:110–114.
    1. Abate G, Koivula T, Hoffner SE. In vitro activity of thiacetazone on mycobacterial species belonging to the Mycobacterium tuberculosis complex. Int J Tuberc Lung Dis. 2002;6:933–935.
    1. Rey JL, Villon A, Menard M, Le Mao G, Albert JP. [Present state of resistance to antibiotics by tuberculous bacilli in Africa (author's transl)]. Med Trop (Mars) 1979;39:149–154.
    1. Nunn P, Kibuga D, Gathua S, Brindle R, Imalingat A, et al. Cutaneous hypersensitivity reactions due to thiacetazone in HIV-1 seropositive patients treated for tuberculosis. Lancet. 1991;337:627–630.
    1. Diarra B, Tounkara A, Traore B, Maiga M, Diallo S, et al. Keystone Conference: Overcoming the Crisis of TB and AIDS (T2) Arusha, Tanzania: 2009. Molecular Identification of Drug Resistant Mycobacteria Species in Bamako, Mali.
    1. Unger F, Münstermann S, Goumou A, Apia CN, Konte M. Banjul: ITC (International Trypanotolerance Centre); 2003. Risk associated with Mycobacterium bovis infections detected in selected study herds and slaughter cattle in 4 countries of West Africa. pp. 1–25.
    1. Goossens B, Osaer S, Kora S, Chandler KJ, Petrie L, et al. Abattoir survey of sheep and goats in The Gambia. Vet Rec. 1998;142:277–281.
    1. Thorel MF. Isolation of Mycobacterium africanum from monkeys. Tubercle. 1980;61:101–104.
    1. Thorel MF. [Mycobacteria identified in a centre for veterinary research between 1973 and 1979 (author's transl)]. Ann Microbiol (Paris) 1980;131:61–69.
    1. Rahim Z, Mollers M, te Koppele-Vije A, de Beer J, Zaman K, et al. Characterization of Mycobacterium africanum subtype I among cows in a dairy farm in Bangladesh using spoligotyping. Southeast Asian J Trop Med Public Health. 2007;38:706–713.
    1. Cadmus S, Palmer S, Okker M, Dale J, Gover K, et al. Molecular analysis of human and bovine tubercle bacilli from a local setting in Nigeria. J Clin Microbiol. 2006;44:29–34.
    1. Cadmus SI, Yakubu MK, Magaji AA, Jenkins AO, van Soolingen D. Mycobacterium bovis, but also M. africanum present in raw milk of pastoral cattle in north-central Nigeria. Trop Anim Health Prod 2010
    1. de Kantor IN, Pereira J, Miquet J, Rovere R. Pouvoir pathogene experimental de Mycobacterium africanum pour les bovins. Bull Acad Vet de France. 1979;52:499–503.
    1. de Jong BC, Hill PC, Brookes RH, Gagneux S, Jeffries DJ, et al. Mycobacterium africanum Elicits an Attenuated T Cell Response to Early Secreted Antigenic Target, 6 kDa, in Patients with Tuberculosis and Their Household Contacts. J Infect Dis. 2006;193:1279–1286.
    1. Castets M, Sarrat H. [Experimental study of the virulence of Mycobacterium africanum (preliminary note)]. Bull Soc Med Afr Noire Lang Fr. 1969;14:693–696.
    1. Korsak T, Millet M. [Observations on 200 strains of mycobacteria collected in Central Africa]. Acta Tuberc Pneumol Belg. 1970;61:388–398.
    1. de Kantor IN, Barcat JA, Cetrangolo A. [M. africanum: experimental virulence and sensitizing capacity to different tuberculin PPDs (proceedings)]. Bull Int Union Tuberc. 1979;54:173–174.
    1. de Medeiros D, Diop S, de Medeiros G, Baylet R, Sankale M. [Comparative allergological study of Mycobacterium tuberculosis of the classical type and Mycobacterium tuberculosis var. Africanum (apropos of 400 intradermoreactions)]. Bull Soc Med Afr Noire Lang Fr. 1974;19:96–104.
    1. de Jong BC, Hill PC, Brookes RH, Otu JK, Peterson KL, et al. Mycobacterium africanum: a new opportunistic pathogen in HIV infection? AIDS. 2005;19:1714–1715.
    1. de Jong BC, Hill PC, Aiken A, Jeffries DJ, Onipede A, et al. Clinical presentation and outcome of tuberculosis patients infected by M. africanum versus M. tuberculosis. Int J Tuberc Lung Dis. 2007;11:450–456.
    1. de Jong BC, Adetifa I, Walther B, Hill PC, Antonio M, et al. FEMS Immunol Med Microbiol in press; 2009. Differences between TB cases infected with M. africanum, West-African type 2, relative to Euro-American M. tuberculosis- an update.
    1. de Jong BC, Hill PC, Aiken A, Awine T, Antonio M, et al. Progression to Active Tuberculosis, but Not Transmission, Varies by Mycobacterium tuberculosis Lineage in The Gambia. J Infect Dis. 2008;198:1037–1043.
    1. Gao LY, Guo S, McLaughlin B, Morisaki H, Engel JN, et al. A mycobacterial virulence gene cluster extending RD1 is required for cytolysis, bacterial spreading and ESAT-6 secretion. Mol Microbiol. 2004;53:1677–1693.
    1. Pym AS, Brodin P, Majlessi L, Brosch R, Demangel C, et al. Recombinant BCG exporting ESAT-6 confers enhanced protection against tuberculosis. Nat Med. 2003;9:533–539.
    1. Inwald J, Jahans K, Hewinson RG, Gordon SV. Inactivation of the Mycobacterium bovis homologue of the polymorphic RD1 gene Rv3879c (Mb3909c) does not affect virulence. Tuberculosis (Edinb) 2003;83:387–393.
    1. Intemann CD, Thye T, Niemann S, Browne EN, Amanua Chinbuah M, et al. Autophagy gene variant IRGM -261T contributes to protection from tuberculosis caused by Mycobacterium tuberculosis but not by M. africanum strains. PLoS Pathog. 2009;5:e1000577. doi: .
    1. de Jong BC, Hammond A, Otu JK, Antonio M, Adegbola RA, et al. Immunogenicity of antigens from the TbD1 region present in M. africanum and missing from “modern” M. tuberculosis: a cross- sectional study. BMC Infect Dis. 2010;10:11.
    1. Parkhill J. 2010. Mycobacterium genomes. Wellcome Trust Sanger Institute. Available:
    1. Comas I, Gagneux S. The past and future of tuberculosis research. PLoS Pathog. 2009;5:e1000600. doi: .
    1. Ledru S, Cauchoix B, Yameogo M, Zoubga A, Lamande-Chiron J, et al. Impact of short-course therapy on tuberculosis drug resistance in South-West Burkina Faso. Tuber Lung Dis. 1996;77:429–436.
    1. Godreuil S, Torrea G, Terru D, Chevenet F, Diagbouga S, et al. First molecular epidemiology study of Mycobacterium tuberculosis in Burkina Faso. J Clin Microbiol. 2007;45:921–927.
    1. van der Werf TS, Groothuis DG, van Klingeren B. High initial drug resistance in pulmonary tuberculosis in Ghana. Tubercle. 1989;70:249–255.
    1. Addo K, Owusu-Darko K, Yeboah-Manu D, Caulley P, Minamikawa M, et al. Mycobacterial species causing pulmonary tuberculosis at the korle bu teaching hospital, accra, ghana. Ghana Med J. 2007;41:52–57.
    1. Niang MN, de la Salmoniere YG, Samb A, Hane AA, Cisse MF, et al. Characterization of M. tuberculosis strains from west African patients by spoligotyping. Microbes Infect. 1999;1:1189–1192.
    1. Haas WH, Bretzel G, Amthor B, Schilke K, Krommes G, et al. Comparison of DNA fingerprint patterns of isolates of Mycobacterium africanum from east and west Africa. J Clin Microbiol. 1997;35:663–666.
    1. Homolka S, Post E, Oberhauser B, George AG, Westman L, et al. High genetic diversity among Mycobacterium tuberculosis complex strains from Sierra Leone. BMC Microbiol. 2008;8:103.
    1. de Jong BC, Adetifa I, Walther B, Hill PC, Antonio M, et al. Differences between tuberculosis cases infected with Mycobacterium africanum, West African type 2, relative to Euro-American Mycobacterium tuberculosis: an update. FEMS Immunol Med Microbiol. 2010;58:102–105.
    1. Smith NH, Hewinson RG, Kremer K, Brosch R, Gordon SV. Myths and misconceptions: the origin and evolution of Mycobacterium tuberculosis. Nat Rev Microbiol. 2009;7:537–544.

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