The Mycobacterium tuberculosis Complex in Africa

  • Sven D. C. ParsonsEmail author
  • Michele A. Miller
  • Paul D. van Helden


The Mycobacterium tuberculosis complex (MTC) comprises distinct lineages of clonally evolving organisms and includes a number of genotypically and phenotypically defined species, many of which are associated with specific animal hosts. Mycobacterium bovis is the most common cause of tuberculosis (TB) in animals in Africa, and it appears to have been introduced onto the continent with the movement of humans and their domestic livestock. However, a lesser known cause of animal TB is a lineage of the MTC that had its early origins in West Africa. This lineage is represented by a number of species including the chimpanzee bacillus, isolated from a chimpanzee (Pan troglodytes) in Côte d’Ivoire; the dassie bacillus, which causes TB in rock hyraxes (Procavia capensis); M. mungi, which infects banded mongooses (Mungos mungo); and M. suricattae, which has been isolated from meerkats (Suricata suricatta). These members of the MTC as well as other rare causes of TB in animals in Africa are reviewed, namely, M. africanum and M. orygis. The value of careful genotyping of mycobacterial pathogens is discussed.


Africa Wildlife Chimpanzee bacillus Mycobacterium microti-like dassie bacillus Dassie bacillus Genotyping Mongoose Meerkats Procavia capensis Mycobacterium tuberculosis complex Mycobacterium mungi Mycobacterium suricattae Mycobacterium africanum Mycobacterium orygis 


  1. Alexander KA, Pleydell E, Williams MC et al (2002) Mycobacterium tuberculosis: an emerging disease of free-ranging wildlife. Emerg Infect Dis 8:598–601. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Alexander KA, Laver PN, Michel AL et al (2010) Novel Mycobacterium tuberculosis complex pathogen, M. mungi. Emerg Infect Dis 16:1296–1299. CrossRefPubMedPubMedCentralGoogle Scholar
  3. Alexander KA, Sanderson CE, Laver PN (2015) Novel Mycobacterium tuberculosis complex spp. in group-living African mammals. In: Tuberculosis, leprosy and mycobacterial diseases of man and animals: The many hosts of mycobacteria. CABI, pp 386–401Google Scholar
  4. Alexander KA, Larsen MH, Robbe-Austerman S et al (2016a) Draft genome sequence of the Mycobacterium tuberculosis complex pathogen M. mungi, identified in a banded mongoose (Mungos mungo) in northern Botswana. Genome Announc 4:e00471–e00416. CrossRefPubMedPubMedCentralGoogle Scholar
  5. Alexander KA, Sanderson CE, Larsen MH et al (2016b) Emerging tuberculosis pathogen hijacks social communication behavior in the group-living banded mongoose (Mungos mungo). mBio 7:e00281-16. CrossRefPubMedPubMedCentralGoogle Scholar
  6. Aranaz A (2003) Elevation of Mycobacterium tuberculosis subsp. caprae Aranaz et al. 1999 to species rank as Mycobacterium caprae comb. nov., sp. nov. Int J Syst Evol Microbiol 53:1785–1789. CrossRefPubMedGoogle Scholar
  7. Asante-Poku A, Aning KG, Boi-Kikimoto B et al (2014) Prevalence of bovine tuberculosis in a dairy cattle farm and a research farm in Ghana. Onderstepoort J Vet Res 81:E1–E6CrossRefGoogle Scholar
  8. Barry RE, Chiweshe N, Mundy PJ (2015) Fluctuations in bush and rock hyrax (Hyracoidea: Procaviidae) abundances over a 13-year period in the Matopos, Zimbabwe. Afr J Wildl Res 45:17–27. CrossRefGoogle Scholar
  9. Bentley SD, Comas I, Bryant JM et al (2012) The Genome of Mycobacterium africanum West African 2 reveals a lineage-specific locus and genome erosion common to the M. tuberculosis complex. PLoS Negl Trop Dis 6:e1552. CrossRefPubMedPubMedCentralGoogle Scholar
  10. Brosch R, Gordon SV, Marmiesse M et al (2002) A new evolutionary scenario for the Mycobacterium tuberculosis complex. Proc Natl Acad Sci USA 99:3684–3689CrossRefGoogle Scholar
  11. Cadmus S, Palmer S, Okker M et al (2006) Molecular analysis of human and bovine tubercle bacilli from a local setting in Nigeria. J Clin Microbiol 44:29–34. CrossRefPubMedPubMedCentralGoogle Scholar
  12. Cadmus SIB, Yakubu MK, Magaji AA et al (2010) Mycobacterium bovis, but also M. africanum present in raw milk of pastoral cattle in north-central Nigeria. Trop Anim Health Prod 42:1047–1048. CrossRefPubMedGoogle Scholar
  13. Cavanagh R, Begon M, Bennett M et al (2002) Mycobacterium microti infection (vole tuberculosis) in wild rodent populations. J Clin Microbiol 40:3281–3285. CrossRefPubMedPubMedCentralGoogle Scholar
  14. Clarke C, van Helden PD, Miller MA et al (2016) Animal-adapted members of the Mycobacterium tuberculosis complex endemic to the Southern African sub region. J SA Vet Assoc 87(1):a1322. CrossRefGoogle Scholar
  15. Clarke C, Patterson SJ, Drewe JA et al (2017) Development and evaluation of a diagnostic cytokine-release assay for Mycobacterium suricattae infection in meerkats (Suricata suricatta). BMC Vet Res 13:2. CrossRefPubMedPubMedCentralGoogle Scholar
  16. Comas I, Coscolla M, Luo T et al (2013) Out-of-Africa migration and neolithic coexpansion of Mycobacterium tuberculosis with modern humans. Nat Genet 45:1176–1182. CrossRefPubMedPubMedCentralGoogle Scholar
  17. Coscolla M, Lewin A, Metzger S et al (2013) Novel Mycobacterium tuberculosis complex isolate from a wild chimpanzee. Emerg Infect Dis 19:969–976. CrossRefPubMedPubMedCentralGoogle Scholar
  18. Cousins DV (2003) Tuberculosis in seals caused by a novel member of the Mycobacterium tuberculosis complex: Mycobacterium pinnipedii sp. nov. Int J Syst Evol Microbiol 53:1305–1314. CrossRefPubMedGoogle Scholar
  19. Cousins DV, Peet RL, Gaynor WT et al (1994) Tuberculosis in imported hyrax (Procavia capensis) caused by an unusual variant belonging to the Mycobacterium tuberculosis complex. Vet Microbiol 42:135–145. CrossRefPubMedGoogle Scholar
  20. Dannenberg AM Jr, Collins FM (2001) Progressive pulmonary tuberculosis is not due to increasing numbers of viable bacilli in rabbits, mice and guinea pigs, but is due to a continuous host response to mycobacterial products. Tuberculosis 81:229–242. CrossRefPubMedGoogle Scholar
  21. de Jong BC, Hill PC, Aiken A et al (2008) Progression to active tuberculosis, but not transmission, varies by M. tuberculosis lineage in The Gambia. J Infect Dis 198:1037–1043. CrossRefPubMedPubMedCentralGoogle Scholar
  22. de Jong BC, Antonio M, Awine T et al (2009) 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 47:994–1001. CrossRefPubMedPubMedCentralGoogle Scholar
  23. de Jong BC, Antonio M, Gagneux S (2010) Mycobacterium africanum—review of an important cause of human tuberculosis in West Africa. PLoS Negl Trop Dis 4:e744. CrossRefPubMedPubMedCentralGoogle Scholar
  24. Dippenaar A, Parsons SDC, Sampson SL et al (2015) Whole genome sequence analysis of Mycobacterium suricattae. Tuberculosis 95(6):682–688CrossRefGoogle Scholar
  25. Drewe JA (2010) Who infects whom? Social networks and tuberculosis transmission in wild meerkats. Proc R Soc Lond B Biol Sci 277:633–642. CrossRefGoogle Scholar
  26. Drewe JA, Foote AK, Sutcliffe RL et al (2009a) Pathology of Mycobacterium bovis infection in wild meerkats (Suricata suricatta). J Comp Pathol 140:12–24. CrossRefPubMedGoogle Scholar
  27. Drewe JA, Dean GS, Michel AL et al (2009b) Accuracy of three diagnostic tests for determining Mycobacterium bovis infection status in live-sampled wild meerkats (Suricata Suricatta). J Vet Diagn Invest 21:31–39. CrossRefPubMedGoogle Scholar
  28. Drewe JA, Eames KTD, Madden JR et al (2011) Integrating contact network structure into tuberculosis epidemiology in meerkats in South Africa: Implications for control. Prev Vet Med 101:113–120. CrossRefPubMedGoogle Scholar
  29. Durnez L, Suykerbuyk P, Nicolas V et al (2010) Terrestrial small mammals as reservoirs of Mycobacterium ulcerans in Benin. Appl Environ Microbiol 76:4574–4577. CrossRefPubMedPubMedCentralGoogle Scholar
  30. Flint BF, Hawley DM, Alexander KA (2016) Do not feed the wildlife: associations between garbage use, aggression, and disease in banded mongooses (Mungos mungo). Ecol Evol 6:5932–5939. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Gehre F, Otu J, DeRiemer K et al (2013) Deciphering the growth behaviour of Mycobacterium africanum. PLoS Neg Trop Dis 7(5):e2220. CrossRefGoogle Scholar
  32. Gey van Pittius NC, Perrett KD, Michel AL et al (2012) Infection of African buffalo (Syncerus caffer) by oryx bacillus, a rare member of the antelope clade of the Mycobacterium tuberculosis complex. J Wildl Dis 48:849–857. CrossRefGoogle Scholar
  33. Hershberg R, Lipatov M, Small PM et al (2008) High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography. PLoS Biol 6:e311. CrossRefPubMedPubMedCentralGoogle Scholar
  34. Huard RC, Fabre M, de Haas P et al (2006) Novel genetic polymorphisms that further delineate the phylogeny of the Mycobacterium tuberculosis complex. J Bacteriol 188:4271–4287. CrossRefPubMedPubMedCentralGoogle Scholar
  35. Laver PN, Ganswindt A, Ganswindt SB et al (2012) Non-invasive monitoring of glucocorticoid metabolites in banded mongooses (Mungos mungo) in response to physiological and biological challenges. Gen Comp Endocrinol 179:178–183. CrossRefPubMedGoogle Scholar
  36. Loeffler SH, de Lisle GW, Neill MA et al (2014) The seal tuberculosis agent, Mycobacterium pinnipedii, infects domestic cattle in New Zealand: epidemiologic factors and DNA strain typing. J Wildl Dis 50:180–187. CrossRefPubMedGoogle Scholar
  37. Lutze-Wallace C, Turcotte C, Glover G et al (2006) Isolation of a Mycobacterium microti-like organism from a rock hyrax (Procavia capensis) in a Canadian zoo. Can Vet J 47:1011–1013PubMedPubMedCentralGoogle Scholar
  38. Mostowy S, Cousins D, Behr MA (2004) Genomic interrogation of the dassie bacillus reveals it as a unique RD1 mutant within the Mycobacterium tuberculosis complex. J Bacteriol 186:104–109CrossRefGoogle Scholar
  39. Mostowy S, Inwald J, Gordon S et al (2005) Revisiting the evolution of Mycobacterium bovis. J Bacteriol 187:6386–6395. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Oevermann A, Pfyffer GE, Zanolari P et al (2004) Generalized tuberculosis in llamas (Lama glama) due to Mycobacterium microti. J Clin Microbiol 42:1818–1821. CrossRefPubMedPubMedCentralGoogle Scholar
  41. Ofukwu RA, Oboegbulem SI, Akwuobu CA (2008) Zoonotic Mycobacterium species in fresh cow milk and fresh skimmed, unpasteurised market milk (nono) in Makurdi, Nigeria: implications for public health. J Anim Plant Sci 1:21–25Google Scholar
  42. Parsons S, Smith SGD, Martins Q et al (2008) Pulmonary infection due to the dassie bacillus (Mycobacterium tuberculosis complex sp.) in a free-living dassie (rock hyrax—Procavia capensis) from South Africa. Tuberculosis 88:80–83. CrossRefGoogle Scholar
  43. Parsons SDC, Drewe JA, Gey van Pittius NC et al (2013) Novel cause of tuberculosis in meerkats, South Africa. Emerg Infect Dis 19:2004–2007. CrossRefPubMedPubMedCentralGoogle Scholar
  44. Pepperell CS, Casto AM, Kitchen A et al (2013) The role of selection in shaping diversity of natural M. tuberculosis populations. PLoS Pathog 9:e1003543. CrossRefPubMedPubMedCentralGoogle Scholar
  45. Rahim Z, Möllers M, te Koppele-Vije A et al (2007) Characterization of Mycobacterium africanum subtype I among cows in a dairy farm in Bangladesh using spoligotyping. Southeast Asian J Trop Med Public Health 38:706–713PubMedGoogle Scholar
  46. Smith N (1965) Animal pathogenicity of the “dassie bacillus”. Tubercle 46:58–64CrossRefGoogle Scholar
  47. Smith NH, Kremer K, Inwald J et al (2006) Ecotypes of the Mycobacterium tuberculosis complex. J Theor Biol 239:220–225. CrossRefPubMedGoogle Scholar
  48. Thorel MF (1980) Isolation of Mycobacterium africanum from monkeys. Tubercle 61:101–104. CrossRefPubMedGoogle Scholar
  49. van Ingen J, Rahim Z, Mulder A et al (2012) Characterization of Mycobacterium orygis as M. tuberculosis complex subspecies. Emerg Infect Dis 18:653–655. CrossRefPubMedPubMedCentralGoogle Scholar
  50. van Soolingen D, de Haas PE, Haagsma J et al (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 32:2425–2433PubMedPubMedCentralGoogle Scholar
  51. van Soolingen D, van der Zanden AGM, de Haas PEW et al (1998) Diagnosis of Mycobacterium microti infections among humans by using novel genetic markers. J Clin Microbiol 36:1840–1845PubMedPubMedCentralGoogle Scholar
  52. Wagner JC, Bokkenheuser V (1961) The Mycobacterium isolated from the dassie Procavia capensis (Pallas). Tubercle 42:47–56CrossRefGoogle Scholar
  53. Wagner JC, Buchanan G, Bokkenheuser V et al (1958) An acid-fast bacillus isolated from the lungs of the cape hyrax, Procavia capensis (Pallas). Nature 181:284–285. CrossRefPubMedGoogle Scholar
  54. Warren RM, Gey van Pittius NC, Barnard M et al (2006) Differentiation of Mycobacterium tuberculosis complex by PCR amplification of genomic regions of difference. Int J Tuberc Lung Dis 10:818–822Google Scholar
  55. Wernery U, Kinne J, Jahans KL et al (2007) Tuberculosis outbreak in a dromedary racing herd and rapid serological detection of infected camels. Vet Microbiol 122:108–115. CrossRefPubMedGoogle Scholar
  56. Wirth T, Hildebrand F, Allix-Béguec C et al (2008) Origin, spread and demography of the Mycobacterium tuberculosis complex. PLoS Pathog 4:e1000160. CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Sven D. C. Parsons
    • 1
    • 2
    Email author
  • Michele A. Miller
    • 1
    • 2
  • Paul D. van Helden
    • 3
  1. 1.DST-NRF Centre of Excellence for Biomedical Tuberculosis Research, Division of Molecular Biology and Human Genetics, Faculty of Medicine and Health SciencesStellenbosch UniversityCape TownSouth Africa
  2. 2.SAMRC Centre for TB Research, Division of Molecular Biology and Human Genetics, Faculty of Medicine and Health SciencesStellenbosch UniversityCape TownSouth Africa
  3. 3.Division of Molecular Biology and Human Genetics, Faculty of Medicine and Health SciencesSouth African MRC Centre for TB Research, DST NRF Centre of Excellence for Biomedical Tuberculosis Research, Stellenbosch UniversityTygerbergSouth Africa

Personalised recommendations