Holes and Patches: An Account of Tuberculosis Caused by Mycobacterium bovis in Uganda

  • A. MuwongeEmail author
  • L. Nyakarahuka
  • W. Ssengooba
  • J. Oloya
  • F. Olea-Popelka
  • C. Kankya


Uganda, known as “the pearl of Africa,” is richly endowed by nature, but it comes at a cost. The fertile and attractive landscapes, abundant water, and optimal temperature not only sustain the Ugandan crop and livestock industries but also ensure a constant abundance of pathogens and parasites affecting humans and animals. These features cause a constant shift of environmental frontiers compounded by the explosive population growth experienced in the country and an increasingly porous human–animal interface. These shifts occur at such a tremendous pace that the holes created at this interface are becoming harder to patch. Pathogens like Mycobacterium bovis, the causative agent of bovine tuberculosis (BTB), exploit these constant changes and cross species barriers to establish new wildlife and domestic species disease reservoirs. Because of these events, M. bovis has now become a multi-host, endemic pathogen, and as zoonotic TB it became a serious public health threat in Uganda. The sustainable growth of an agriculture-based country like Uganda is dependent on the health of its people, crops, and animals, and it is imperative to deal with diseases that threaten this growth. It is critical to be able to diagnose and control TB caused by M. bovis in livestock, wildlife species, and humans and to understand the relevant risks and strategies required to control and eventually eradicate the infection. This chapter addresses these various issues.


Bovine tuberculosis Mycobacterium bovis Cattle movement networks Livestock husbandry Molecular epidemiology Non-tuberculous mycobacteria Uganda Zoonotic tuberculosis 


  1. Asiimwe BB, Asiimwe J, Kallenius G et al (2009) Molecular characterisation of Mycobacterium bovis isolates from cattle carcases at a city slaughterhouse in Uganda. Vet Rec 164:655–658CrossRefGoogle Scholar
  2. Bakama B (2010) A contemporary geography of Uganda, 1st edn. Mkuki na Nyota, Dar es SalaamGoogle Scholar
  3. Berg S, Garcia-Pelayo MC, Müller B et al (2011) African 2, a clonal complex of Mycobacterium bovis epidemiologically important in East Africa. J Bacteriol 193:670–678CrossRefGoogle Scholar
  4. Bernard F, Vincent C, Matthieu L et al (2005) Tuberculosis and brucellosis prevalence survey on dairy cattle in Mbarara milk basin (Uganda). Prev Vet Med 67:267–681CrossRefGoogle Scholar
  5. Boysen O, Matthews A (2012) The differentiated effects of food price spikes on poverty in Uganda. In: 123rd European Association of Agricultural Economists Seminar, Price volatility and farm income stabilization: modeling outcomes and assessing market and policy based responses, Dublin, Ireland, February, pp 23–24Google Scholar
  6. Bretzel G, Aziz M, Wendl-Richter U et al (1999) Anti-tuberculosis drug resistance surveillance in Uganda 1996–1997. Int J Tuberc Lung Dis 3:810–815PubMedGoogle Scholar
  7. Byarugaba F, Grimaud P, Godreuil S (2010) Risk assessment in zoonotic tuberculosis in Mbarara, the main milk basin of Uganda. Bull Anim Health Prod Afr 58:125–132Google Scholar
  8. Cosivi O, Grange JM, Daborn CJ et al (1998) Zoonotic tuberculosis due to Mycobacterium bovis in developing countries. Emerg Infect Dis 4:59–70CrossRefGoogle Scholar
  9. Daniel TM (1998) The early history of tuberculosis in Central East Africa: insights from the clinical records of the first twenty years of Mengo Hospital and review of relevant literature. Int J Tuberc Lung Dis 2:784–790PubMedGoogle Scholar
  10. Daniel TM (2006) The history of tuberculosis. Respir Med 100:1862–1870CrossRefGoogle Scholar
  11. Dickman KR, Nabyonga L, Kateete DP et al (2010) Detection of multiple strains of Mycobacterium tuberculosis using MIRU-VNTR in patients with pulmonary tuberculosis in Kampala, Uganda. BMC Infect Dis 10:349CrossRefGoogle Scholar
  12. Dürr S, Müller B, Alonso S et al (2013) Differences in primary sites of infection between zoonotic and human tuberculosis: results from a worldwide systematic review. PLoS Negl Trop Dis 7:e2399CrossRefGoogle Scholar
  13. Ebanyat P, de Ridder N, de Jager A et al (2010) Drivers of land use change and household determinants of sustainability in smallholder farming systems of eastern Uganda. Popul Environ 31:474–506CrossRefGoogle Scholar
  14. Enøe C, Christensen G, Andersen S et al (2003) The need for built-in validation of surveillance data so that changes in diagnostic performance of post-mortem meat inspection can be detected. Prev Vet Med 57:117–125CrossRefGoogle Scholar
  15. Everett CA, Davis JL, Worodria W et al (2010) Performance of LED fluorescence microscopy for the diagnosis of pulmonary tuberculosis: preliminary results from the Uganda National Reference Laboratory. Am J Respir Crit Care Med 181:A1769Google Scholar
  16. Falkinham JO (2009) Surrounded by mycobacteria: nontuberculous mycobacteria in the human environment. J Appl Microbiol 107:356–367CrossRefGoogle Scholar
  17. Farmer P (1996) Social inequalities and emerging infectious diseases. Emerg Inf Dis 2:256–269CrossRefGoogle Scholar
  18. Fèvre EM, Bronsvoort BMDC, Hamilton K et al (2006) Animal movements and the spread of infectious diseases. Trends Microbiol 14:125–131CrossRefGoogle Scholar
  19. Firdessa R, Tschopp R, Wubete A et al (2012) High prevalence of bovine tuberculosis in dairy cattle in Central Ethiopia: implications for the dairy industry and public health. PLoS One 7:e52851CrossRefGoogle Scholar
  20. Ford LB (2007) Civil conflict and sleeping sickness in Africa in general and Uganda in particular. Confl Heal 1:6CrossRefGoogle Scholar
  21. Government of Uganda (2000) Public Health Act, Uganda. pp 1–17
  22. Gray S, Sundal M, Wiebusch B et al (2003) Cattle raiding, cultural survival, and adaptability of east African pastoralists. Curr Anthropol 44(5 Suppl):S3–S30CrossRefGoogle Scholar
  23. Hovil L (2007) Self-settled refugees in Uganda: an alternative approach to displacement? J Refug Stud 20:599–620CrossRefGoogle Scholar
  24. Hudelson P (1996) Gender differentials in tuberculosis: the role of socio-economic and cultural factors. Tuber Lung Dis 77:391–400CrossRefGoogle Scholar
  25. Huxley PA (1965) Climate and agricultural production in Uganda. Exp Agric 1:81–97CrossRefGoogle Scholar
  26. Inangolet FO, Demelash B, Oloya J et al (2008) A cross-sectional study of bovine tuberculosis in the transhumant and agro-pastoral cattle herds in the border areas of Katakwi and Moroto districts, Uganda. Trop Anim Health Prod 40:501–508CrossRefGoogle Scholar
  27. Jabs L (2007) Where two elephants meet, the grass suffers: a case study of intractable conflict in Karamoja, Uganda. Am Behav Sci 50:1498–1519CrossRefGoogle Scholar
  28. Joloba ML, Whalen CC, Cave DM et al (2000) Determination of drug susceptibility and DNA fingerprint patterns of clinical isolates of Mycobacterium tuberculosis from Kampala, Uganda. East Afr Med J 77:111–115PubMedGoogle Scholar
  29. Kalema-Zikusoka G, Bengis RG, Michel AL et al (2005) A preliminary investigation of tuberculosis and other diseases in African buffalo (Syncerus caffer) in Queen Elizabeth National Park, Uganda. Onderstepoort J Vet Res 72:145–151CrossRefGoogle Scholar
  30. Kankya C, Muwonge A, Olet S et al (2010) Factors associated with pastoral community knowledge and occurrence of mycobacterial infections in human-animal interface areas of Nakasongola and Mubende districts, Uganda. BMC Public Health 10:471CrossRefGoogle Scholar
  31. Kankya C, Muwonge A, Djønne B et al (2011) Isolation of non-tuberculous mycobacteria from pastoral ecosystems of Uganda: public health significance. BMC Pub Health 11:320CrossRefGoogle Scholar
  32. Lukoye D, Katabazi FA, Musisi K et al (2014) The T2 Mycobacterium tuberculosis genotype, predominant in Kampala, Uganda, shows negative correlation with antituberculosis drug resistance. Antimicrob Agents Chemother 58:3853–3859CrossRefGoogle Scholar
  33. Mario R (2014) The end TB strategy. WHO/HTM/GTB/2015.09Google Scholar
  34. Ministry of Agriculture (2010) Agricultural sector development strategy and investment plan 2010–15. Ministry of agriculture report, pp 11–16Google Scholar
  35. Ministry of Health (1992) Manual of the national tuberculosis and leprosy program in Uganda for district TB/leprosy supervisors, 1st edn. Ministry of Health report, pp 1–9Google Scholar
  36. Müller B, Dürr S, Alonso S et al (2013) Zoonotic Mycobacterium bovis-induced tuberculosis in humans. Emerg Infect Dis 19:899–908CrossRefGoogle Scholar
  37. Murray G (1986) Ante-mortem and post-mortem meat inspection: an Australian inspection service perspective. Aust Vet J 63:211–215CrossRefGoogle Scholar
  38. Muwonge A (2012) Non tuberculous mycobacteria in swine: is it a public health problem? Mycobacteria Dis 20(2):e110. CrossRefGoogle Scholar
  39. Muwonge A, Johansen TB, Vigdis E et al (2012a) Mycobacterium bovis infections in slaughter pigs in Mubende district, Uganda: a public health concern. BMC Vet Res 8:168CrossRefGoogle Scholar
  40. Muwonge A, Kankya C, Johansen TB et al (2012b) Non-tuberculous mycobacteria isolated from slaughter pigs in Mubende district, Uganda. BMC Vet Res 8:52CrossRefGoogle Scholar
  41. Muwonge A, Oloya J, Kankya C et al (2014) Molecular characterization of Mycobacterium avium subspecies hominissuis isolated from humans, cattle and pigs in the Uganda cattle corridor using VNTR analysis. Infect Genet Evol 21:184–191CrossRefGoogle Scholar
  42. Mwinga A (2005) Challenges and hope for the diagnosis of tuberculosis in infants and young children. Lancet 365(9454):97–98CrossRefGoogle Scholar
  43. Nasaka J 2014 Occurence of bovine tuberculosis in slaughtered cattle. MSc Dissertation, Department of Environment and Natural Resources Management, Makerere University, UgandaGoogle Scholar
  44. Nielsen SS, Toft N, Gardner A (2011) Structured approach to design of diagnostic test evaluation studies for chronic progressive infections in animals. Vet Microbiol 150:115–125CrossRefGoogle Scholar
  45. Niemann S, Rüsch-Gerdes S, Joloba ML et al (2002) Mycobacterium africanum subtype II is associated with two distinct genotypes and is a major cause of human tuberculosis in Kampala, Uganda. J Clin Microbiol 40:3398–3405CrossRefGoogle Scholar
  46. Nyakahuma D, Kimezire M (1995) Uganda. In: Thoen C, Steel J (eds) M. bovis infection in animals and humans. Iowa State University Press, Ames, pp 303–330Google Scholar
  47. OIE (2009) Bovine tuberculosis: The OIE terrestrial manual.
  48. Oloya J, Opuda-Asibo J, Djønne B et al (2006) Responses to tuberculin among Zebu cattle in the transhumance regions of Karamoja and Nakasongola district of Uganda. Trop Anim Health Prod 38:275–283CrossRefGoogle Scholar
  49. Oloya J, Kazwala R, Lund A et al (2007a) Characterisation of mycobacteria isolated from slaughter cattle in pastoral regions of Uganda. BMC Microbiol 7:95CrossRefGoogle Scholar
  50. Oloya J, Muma JB, Opuda-Asibo J et al (2007b) Risk factors for herd-level bovine-tuberculosis seropositivity in transhumant cattle in Uganda. Prev Vet Med 80:318–329CrossRefGoogle Scholar
  51. Oloya J, Opuda-Asibo J, Kazwala R et al (2008) Mycobacteria causing human cervical lymphadenitis in pastoral communities in the Karamoja region of Uganda. Epidemiol Infect 136:636–643CrossRefGoogle Scholar
  52. Opuda-Asibo J (1995) Regional and country status reports, Uganda. In: Thoen C, Steel J (eds) Mycobacterium bovis infection in animals and humans. Iowa State University Press, Ames, pp 299–303Google Scholar
  53. Rodriguez-Campos S, Aranaz A, de Juan L et al (2011) Limitations of spoligotyping and variable-number tandem-repeat typing for molecular tracing of Mycobacterium bovis in a high-diversity setting. J Clin Microbiol 49:3361–3364CrossRefGoogle Scholar
  54. Sabat AJ, Budimir A, Nashev D et al (2013) Overview of molecular typing methods for outbreak detection and epidemiological surveillance. Euro Surveill 18(4):15. CrossRefGoogle Scholar
  55. Sharma SK, Mohan A, Sharma A (2012) Challenges in the diagnosis and treatment of miliary tuberculosis. Indian J Med Res 135:703–730CrossRefGoogle Scholar
  56. Shittu A, Clifton-Hadley RS, Ely ER et al (2013) Factors associated with bovine tuberculosis confirmation rates in suspect lesions found in cattle at routine slaughter in Great Britain, 2003–2008. Prev Vet Med 110:395–404CrossRefGoogle Scholar
  57. Ssali FN, Kamya MR, Wabwire-Mangen F et al (1998) A prospective study of community-acquired bloodstream infections among febrile adults admitted to Mulago Hospital in Kampala, Uganda. J Acquir Immune Defic Syndr 19:484–489CrossRefGoogle Scholar
  58. Ssengooba W, Gelderbloem SJ, Mboowa G et al (2015) Feasibility of establishing a biosafety level 3 tuberculosis culture laboratory of acceptable quality standards in a resource-limited setting: an experience from Uganda. Health Res Policy Syst 13:1–10CrossRefGoogle Scholar
  59. Strain SAJ, Mcnair J, Mcdowell SWJ (2011) Bovine tuberculosis: a review of diagnostic tests for M. bovis infection in badgers. Bacteriology Branch Veterinary Sciences Division Agri-Food and Biosciences Institute. p 45
  60. Thoen C, Lobue P, de Kantor I (2006) The importance of Mycobacterium bovis as a zoonosis. Vet Microbiol 112:339–345CrossRefGoogle Scholar
  61. WFO (2012) Re-greening the Ugandan Cattle Corridor. Water Food Organisation. Accessed 22 Jul 2015

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • A. Muwonge
    • 1
    Email author
  • L. Nyakarahuka
    • 2
  • W. Ssengooba
    • 3
  • J. Oloya
    • 4
  • F. Olea-Popelka
    • 5
  • C. Kankya
    • 3
  1. 1.The Roslin Institute, The Dick School of Veterinary Medicine, College of Medicine and Veterinary MedicineUniversity of Edinburgh, Easter BushEdinburghUK
  2. 2.Department of Public Health and Preventive Medicine, College of Veterinary Medicine, Animal Resources & BiosecurityMakerere UniversityKampalaUganda
  3. 3.Mycobacteriology Laboratory, Department of Medical MicrobiologyMakerere University College of Health SciencesKampalaUganda
  4. 4.Department of Epidemiology and Biostatistics/Population Health, College of Public Health, 132 Coverdell CenterUniversity of GeorgiaAthensUSA
  5. 5.Department of Clinical Sciences and Mycobacteria Research Laboratories (MRL), College of Veterinary Medicine and Biomedical SciencesColorado State UniversityFort CollinsUSA

Personalised recommendations