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Tuberculosis control in the era of HIV

Abstract

Without HIV, the tuberculosis (TB) epidemic would now be in decline almost everywhere. However, instead of looking forward to the demise of TB, countries that are badly affected by HIV are struggling against a rising tide of HIV-infected patients with TB. As a consequence, global TB control policies have had to be revised and control of TB now demands increased investment. This paper assesses what is being done to address the issue and what remains to be done.

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Figure 1: Map illustrating tuberculosis (TB) and HIV interactions.
Figure 2: Graph of rising estimated incidence rates in Africa and the rest of the world.
Figure 3: HIV prevalence in adults, and tuberculosis (TB) notification rates, for Kisumu, Kenya.

References

  1. Dubos, J. & Dubos, R. The White Plague (Rutgers Univ. Press, New Brunswick, 1987).

    Google Scholar 

  2. World Health Organization. Report of the Third Global TB/HIV Working Group meeting: 'Two diseases — one patient' (WHO, Geneva, 2003).

  3. World Health Organization. Global tuberculosis control: surveillance, planning, financing (WHO, Geneva, 2005).

  4. UNAIDS. AIDS epidemic update: December 2004 (UNAIDS, Geneva, 2004).

  5. Harries, A. D. et al. Deaths from tuberculosis in sub-Saharan African countries with a high prevalence of HIV-1. Lancet 357, 1519–1523 (2001).

    Article  CAS  Google Scholar 

  6. United Nations. Millenium development goals [online] <http://millenniumindicators.un.org/unsd/mi/mi_goals.asp> (2004).

  7. World Health Organization. Treating 3 million by 2005: making it happen (WHO, Geneva, 2003).

  8. Office of the US Government AIDS Coordinator. Bringing hope and saving lives: building sustainable HIV/AIDS treatment (US State Department, Washington DC, USA, 2004).

  9. The Global Fund to Fight AIDS, TB and Malaria. A force for change: the global fund at 30 months (GFATM, Geneva, 2004).

  10. World Health Organization. An expanded framework for effective tuberculosis control. Int. J. Tuberc. Lung Dis. 6, 378–388 (2002).

  11. World Health Organization. Scaling up antiretroviral therapy in resource-limited settings: treatment guidelines for a public health approach. 2003 revision (WHO, Geneva, 2003).

  12. Sachs, J. Report of the Commission on Macroeconomics and Health. ISBN 92-4-154550X (WHO, Geneva, 2001).

  13. Corbett, E. L. et al. The growing burden of tuberculosis: global trends and interactions with the HIV epidemic. Arch. Intern. Med. 163, 1009–1021 (2003).

    Article  Google Scholar 

  14. Raviglione, M. C. et al. in Harrison's Principles of Internal Medicine (ed. Fauci, A. S.) 1004–1014 (McGraw-Hill, New York, 1998).

    Google Scholar 

  15. DesPrez, R. M. & Heim, C. R. in Principles and Practice of Infectious Diseases (eds Mandell, G. L., Douglas, R. G. & Bennet, J. E.) 1877–1906 (Churchill Livingstone, New York, 1990).

    Google Scholar 

  16. Comstock, G. W. & Cauthen, G. M. in Tuberculosis. A Comprehensive International Approach Vol. 66 (eds Reichman, L. B. & Hershfield, E. S.) 23–48 (Marcel Dekker Inc., New York, 1993).

    Google Scholar 

  17. Selwyn, P. A. et al. A prospective study of the risk of tuberculosis among intravenous drug users with human immunodeficiency virus infection. N. Engl. J .Med. 320, 545–550 (1989).

    Article  CAS  Google Scholar 

  18. Antonucci G., Girardi E., Raviglione M. C. & Ippolito G. Risk factors for tuberculosis in HIV-infected persons. A prospective cohort study. The Gruppo Italiano di Studio Tubercolosi e AIDS (GISTA). JAMA 274, 143–148 (1995).

    Article  CAS  Google Scholar 

  19. Williams, B. G. & Dye, C. Antiretroviral drugs for tuberculosis control in the era of HIV/AIDS. Science 301, 1535–1537 (2003).

    Article  CAS  Google Scholar 

  20. Makubalo, L., Netshidzivhani, P., Mahlasela, L. & du Plessis, R. National HIV and syphilis antenatal sero-prevalence survey in South Africa 2003 (Department of Health, Pretoria, South Africa, 2004).

  21. Stoneburner, R. L. & Low-Beer, D. Population-level HIV declines and behavioral risk avoidance in Uganda. Science 304, 714–718 (2004).

    Article  CAS  Google Scholar 

  22. Fylkesnes, K. et al. Declining HIV prevalence and risk behaviours in Zambia: evidence from surveillance and population-based surveys. AIDS 15, 907–916 (2001).

    Article  CAS  Google Scholar 

  23. Glynn, J. R. et al. Trends in tuberculosis and the influence of HIV infection in northern Malawi, 1988–2001. AIDS 18, 1459–1463 (2004).

    Article  Google Scholar 

  24. Corbett, E. L. et al. Human immunodeficiency virus and the prevalence of undiagnosed tuberculosis in African gold miners. Am. J. Resp. Crit. Care Med. 170, 673–679 (2004).

    Article  Google Scholar 

  25. Brindle, R. J. et al. Quantitative bacillary response to treatment in HIV-associated pulmonary tuberculosis. Am. Rev. Resp. Dis. 147, 958–961 (1993).

    Article  CAS  Google Scholar 

  26. Corbett, E. L. et al. HIV infection and silicosis: the impact of two potent risk factors on the incidence of mycobacterial disease in South African miners. AIDS 14, 2759–2768 (2000).

    Article  CAS  Google Scholar 

  27. Sonnenberg, P. et al. HIV and pulmonary tuberculosis: the impact goes beyond those infected with HIV. AIDS 18, 657–662 (2004).

    Article  Google Scholar 

  28. Harries, A. D., Nyirenda, T., Banerjee, A., Salaniponi, F. M. & Boeree, M. J. Tuberculosis control in the face of the HIV epidemic. Trop. Doct. 28, 243–245 (1998).

    Article  CAS  Google Scholar 

  29. Harries, A. D., Nyirenda, T. E., Banerjee, A., Mundy, C. & Salaniponi, F. M. District sputum smear microscopy services in Malawi. Int. J. Tuberc. Lung Dis. 2, 914–918 (1998).

    CAS  PubMed  Google Scholar 

  30. Nunn, P. et al. The impact of HIV on resource utilization by patients with tuberculosis in a tertiary referral hospital, Nairobi, Kenya. Tuber. Lung Dis. 74, 273–279 (1993).

    Article  CAS  Google Scholar 

  31. Narasimhan, V. et al. Responding to the global human resources crisis. Lancet 363, 1469–1472 (2004).

    Article  Google Scholar 

  32. Chen, L. et al. Human resources for health: overcoming the crisis. Lancet 364, 1984–1990 (2004).

    Article  Google Scholar 

  33. Harries, A. D. et al. Human resources for control of tuberculosis and HIV-associated tuberculosis. Int. J. Tuberc. Lung Dis. 9, 128–137 (2005).

    CAS  PubMed  Google Scholar 

  34. Rigoli, F. & Dassault, G. The interface between health sector reform and human resources in health. Hum. Resour. Health. 1, 1–12 (2003).

    Article  Google Scholar 

  35. Wilkinson, D. & Gilks, C. F. Increasing frequency of tuberculosis among staff in a South African district hospital: impact of the HIV epidemic on the supply side of health care. Trans. R. Soc .Trop. Med. Hyg. 92, 500–502 (1998).

    Article  CAS  Google Scholar 

  36. Ministry of Health, Republic of Malawi. Human resources in the health sector: toward a solution (Ministry of Health, Lilongwe, 2004).

  37. Hongoro, C. & McPake, B. How to bridge the gap in human resources for health. Lancet 364, 1451–1456 (2004).

    Article  Google Scholar 

  38. Uplekar, M., Pathania, V. & Raviglione, M. Private practitioners and public health: weak links in tuberculosis control. Lancet 358, 912–916 (2001).

    Article  CAS  Google Scholar 

  39. World Health Organization. Community contribution to TB care: practice and policy. WHO/CDS/TB/2003.312 (WHO, Geneva, 2003).

  40. Cantwell, M. F. & Binkin, N. J. Impact of HIV on tuberculosis in sub-Saharan Africa: a regional perspective. Int. J. Tuberc. Lung Dis. 1, 205–214 (1997).

    CAS  PubMed  Google Scholar 

  41. Styblo, K. et al. Epidemiological and clinical study of tuberculosis in the district of Kolin, Czechoslovakia. Bull. World Health Organ. 37, 819–874 (1967).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. World Health Organization. WHO report on the tuberculosis epidemic, 1995: stop TB at the source (Tuberculosis Programme, Geneva, 1995).

  43. World Health Organization. An expanded DOTS framework for effective tuberculosis control, 1–20 (WHO, Geneva, 2002).

  44. World Health Organization. in 44th World Health Assembly Resolutions and Decisions (WHO, Geneva, 1991).

  45. Dye, C., Garnett, G. P., Sleeman, K. & Williams, B. G. Prospects for worldwide tuberculosis control under the WHO DOTS strategy. Lancet 352, 1886–1891 (1998).

    Article  CAS  Google Scholar 

  46. World Health Organization. Report on the meeting of the second ad hoc committee on the TB epidemic. WHO/HTM/STB/2004.28 (WHO, Geneva, 2004).

  47. Suarez, P. G. et al. The dynamics of tuberculosis in response to 10 years of intensive control effort in Peru. J. Infect. Dis. 184, 473–478 (2001).

    Article  CAS  Google Scholar 

  48. Dye, C., Zhao, F., Scheele, S. & Williams, B. G. Evaluating the impact of tuberculosis control: number of deaths prevented by short-course chemotherapy in China. Int. J. Epidemiol 29, 558–564 (2000).

    Article  CAS  Google Scholar 

  49. China Tuberculosis Control Collaboration. The effect of tuberculosis control in China. Lancet 364, 417–422 (2004).

  50. Styblo, K. Epidemiology of Tuberculosis, 1–136 (Royal Netherlands Tuberculosis Association, The Hague, 1991).

    Google Scholar 

  51. De Cock, K. M. & Chaisson, R. E. Will DOTS do it? A reappraisal of tuberculosis control in countries with high rates of HIV infection. Int. J. Tuberc. Lung Dis. 3, 457–465 (1999).

    CAS  PubMed  Google Scholar 

  52. Currie, C. S., Williams, B. G., Cheng, R. C. & Dye, C. Tuberculosis epidemics driven by HIV: is prevention better than cure? AIDS 17, 2501–2508 (2003).

    Article  Google Scholar 

  53. World Health Organization. Interim policy on collaborative TB/HIV activities. WHO/HTM/TB/2004.330, WHO/HTM/HIV/2004.1 (WHO, Geneva, 2004).

  54. World Health Organization. Guidelines for HIV surveillance among tuberculosis patients 2nd edn. WHO/HTM/TB/2004.339 (WHO, Geneva, 2004).

  55. World Health Organization A guide to monitoring and evaluation for collaborative TB/HIV activities: field test version. WHO/HTM/TB/2004.342, WHO/HIV/2004.09 (WHO, Geneva, 2004).

  56. Bucher, H. C. et al. Isoniazid prophylaxis for tuberculosis in HIV infection: a meta-analysis of randomized controlled trials. AIDS 13, 501–507 (1999).

    Article  CAS  Google Scholar 

  57. Bell, J. C., Rose, D. N. & Sacks, H. S. Tuberculosis preventive therapy for HIV-infected people in sub-Saharan Africa is cost-effective. AIDS 13, 1549–1556 (1999).

    Article  CAS  Google Scholar 

  58. Mwinga, A. et al. Twice weekly tuberculosis preventive therapy in HIV infection in Zambia. AIDS 12, 2447–2457 (1998).

    Article  CAS  Google Scholar 

  59. Pape, J. W., Jean, S. S., Ho, J. L., Hafner, A. & Johnson, W. D. Jr. Effect of isoniazid prophylaxis on incidence of active tuberculosis and progression of HIV infection. Lancet 342, 268–272 (1993).

    Article  CAS  Google Scholar 

  60. Whalen, C. C. et al. A trial of three regimens to prevent tuberculosis in Ugandan adults infected with the human immunodeficiency virus. Uganda–Case Western Reserve University Research Collaboration. N. Engl. J. Med. 337, 801–808 (1997).

    Article  CAS  Google Scholar 

  61. World Health Organization. Report of a 'Lessons Learnt' Workshop on the six ProTEST pilot projects in Malawi, South Africa and Zambia. WHO/HTM/TB/2004.336 (WHO, Geneva, 2004).

  62. World Health Organization. Guidelines for the prevention of tuberculosis in health care facilities in resource-limited settings. WHO/CDC/TB/99, 1–51 (1999).

  63. Wiktor, S. Z. et al. Efficacy of trimethoprim-sulphamethoxazole prophylaxis to decrease morbidity and mortality in HIV-q-infeted patients with tuberculosis in Abidjan, Côte d'Ivoire: a randomised controlled trial. Lancet 353, 1469–1475 (1999).

    Article  CAS  Google Scholar 

  64. Zachariah, R. et al. Voluntary counselling, HIV testing and adjunctive cotrimoxazole reduces mortality in tuberculosis patients in Thyolo, Malawi. AIDS 17, 1053–1061 (2003).

    Article  CAS  Google Scholar 

  65. Chimzizi, R. et al. Voluntary counselling, HIV testing and adjunctive cotrimoxazole are associated with improved TB treatment outcomes under routine conditions, Thyolo district, Malawi. Int. J. Tuberc. Lung Dis. 8, 579–585 (2004).

    CAS  PubMed  Google Scholar 

  66. Harries, A. D., Maher, D. & Graham, S. TB/HIV: A Clinical Manual, 1–210 (WHO, Geneva, 2004).

    Google Scholar 

  67. CASCADE Collaboration. Survival after introduction of HAART in people with known duration of HIV-1 infection. Lancet 355, 1158–1159 (2000).

  68. UNAIDS and World Health Organization. '3 by 5' progress report. December 2004. ISBN 92-4-1592753 (WHO, Geneva, 2004).

  69. Jones, J. L., Hanson, D. L., Dworkin, M. S. & DeCock, K. M. HIV-associated tuberculosis in the era of highly active antiretroviral therapy. The Adult/Adolescent Spectrum of HIV Disease Group. Int. J. Tuberc. Lung Dis. 4, 1026–1031 (2000).

    CAS  PubMed  Google Scholar 

  70. World Health Organization. Scaling up prevention and treatment for TB and HIV: report of the 4th Global TB/HIV Working Group Meeting (WHO, Geneva, 2004).

  71. Lopez-Cortes, L. F. et al. Pharmacokinetic interactions between efavirenz and rifampicin in HIV-infected patients with tuberculosis. Clin. Pharmacokinet. 41, 681–690 (2002).

    Article  CAS  Google Scholar 

  72. French, M. A., Price, P. & Stone, S. F. Immune restoration disease after antiretroviral therapy. AIDS 18, 1615–1627 (2004).

    Article  CAS  Google Scholar 

  73. Zachariah, R. et al. Can we get more HIV-positive tuberculosis patients on antiretroviral treatment in a rural district of Malawi? Int. J. Tuberc. Lung Dis. 9, 238–247 (2005).

    CAS  PubMed  Google Scholar 

  74. Harries, A. D., Nyangulu, D. S., Hargreaves, N. J., Kaluwa, O. & Salaniponi, F. M. Preventing antiretroviral anarchy in sub-Saharan Africa. Lancet 358, 410–414 (2001).

    Article  CAS  Google Scholar 

  75. Badri, M., Wilson, D. & Wood, R. Effect of highly active antiretroviral therapy on incidence of tuberculosis in South Africa: a cohort study. Lancet 359, 2059–2064 (2002).

    Article  Google Scholar 

  76. Schwartländer, B. et al. AIDS: Resource needs for HIV/AIDS. Science 292, 2434–2436 (2001).

    Article  Google Scholar 

  77. Floyd, K., Blanc, L., Raviglione, M. & Lee, J. W. Resources required for global tuberculosis control. Science 295, 2040–2041 (2002).

    Article  CAS  Google Scholar 

  78. The STOP TB Partnership. Global plan to stop TB: phase 1: 2001 to 2005, 190 (WHO, Geneva, 2002).

  79. Gutierrez, J. P. et al. Achieving the WHO/UNAIDS antiretroviral treatment 3-by-5 goal: what will it cost? Lancet 364, 63–64 (2004).

    Article  Google Scholar 

  80. Floyd, K., Kumaranayake, L., Getahun, H. & Nunn, P. in The XV International AIDS Conference, 2004 (Bangkok, Thailand, 2004).

    Google Scholar 

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Correspondence to Paul Nunn.

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Nunn, P., Williams, B., Floyd, K. et al. Tuberculosis control in the era of HIV. Nat Rev Immunol 5, 819–826 (2005). https://doi.org/10.1038/nri1704

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