© 2007 American Thoracic Society doi: 10.1164/rccm.200609-1376ED
Tuberculosis Fueled by HIV: Putting Out the FlamesStop TB Department, World Health Organization, Geneva, Switzerland The end of apartheid in the early 1990s in South Africa ended some of the more egregious labor practices that had driven the spread of tuberculosis in that country (1, 2), but coincided with a rapid increase in the number of HIV cases (3), which has further fueled the epidemic of tuberculosis (2). In the decade before 1995, case notification rates for all forms of tuberculosis in South Africa were fairly constant at about 200/100,000 population, but increased to 718/100,000 in 2004 (4), when 60% of patients with tuberculosis were infected with HIV and the incidence of tuberculosis was increasing at 8.5% per year (3). There are, however, substantial variations in both tuberculosis and HIV in different places and population groups. The annual case notification rate of pulmonary tuberculosis of 1,931/100,000 population in one selected South African population group, as reported by Wood and colleagues (5) in this issue of the Journal (pp. 87–93), is nearly three times the national average. The epidemiology of the interaction between HIV and tuberculosis is well known but not completely understood. Tuberculosis control in locations where up to one in three adults are HIV-positive is a matter of great concern. The conventional method of controlling tuberculosis (i.e., the directly observed therapy, short-course [DOTS] strategy) has emphasized the effective treatment of tuberculosis cases detected among symptomatic patients presenting to health facilities (6). It has been argued that "DOTS alone is unlikely to control tuberculosis in sub-Saharan Africa" (7), which raises two questions: first, what is meant by "control," and second, what would be needed to achieve this end? HIV infection increases the risk of tuberculosis by up to an order of magnitude, and in countries such as South Africa, it is not surprising that even full implementation of the DOTS strategy is unable to reduce the tuberculosis incidence more quickly than HIV drives it upwards. But it is more useful and more interesting to ask what a high tuberculosis incidence in HIV-positive people does to tuberculosis transmission. To address this question, Corbett and coworkers (8) showed that among South African gold miners, the incidence of tuberculosis in those who were not infected with HIV remained constant even as tuberculosis incidence doubled in those infected with HIV. This can be explained if the increased risk of tuberculosis infection among those with HIV is balanced by correspondingly fast tuberculosis disease progression, and hence reduced duration, of tuberculosis disease (4). To quantify this argument, Corbett and colleagues (4) define the tuberculosis disease duration as the time between developing disease and either dying or being cured, and showed that the disease duration ratio (i.e., the disease duration in HIV-positive patients with tuberculosis divided by the disease duration in HIV-negative patients with tuberculosis) was about 0.15 (0.00–0.73; ranges here and below give 95% bootstrap confidence limits) for those with sputum smear–positive tuberculosis and 0.33 (0.14–0.72) for those with all forms of tuberculosis. The study by Wood and coworkers (5) adds important new data from a different setting where about 13,000 black Africans live in shacks in the Western Cape and are not engaged in mining. From their data, the disease duration ratio is 1.19 (0.51–3.57) for those with sputum smear–positive tuberculosis and 1.34 (0.41–6.56) for those with all forms of tuberculosis. (Estimates of the disease duration and disease duration ratio from both studies are given and discussed briefly in the online supplement). Since both studies found few prevalent cases, the confidence intervals are correspondingly large and there is substantial overlap in the confidence bounds for both disease duration and disease duration ratio in the two studies. Which of the two more closely approximates the situation on the ground is a matter of great importance. The estimates of Corbett and colleagues suggest (1) that the DOTS strategy should continue to be effective for HIV-negative patients, while HIV-positive subjects must start antiretroviral therapy; and (2) that the very rapid progression of tuberculosis in HIV-positive individuals will limit the effectiveness of intensified tuberculosis case-finding. The estimates of Wood and coworkers (5) suggest (1) that the epidemic of tuberculosis in HIV-positive people also fuels tuberculosis in those who are HIV-negative; and (2) that the rather slower progression of tuberculosis in HIV-positive people means that intensified case-finding is an important addition to the DOTS strategy for tuberculosis control, even where the prevalence of HIV is high. Taken together, these two studies highlight the importance of the disease duration ratio for understanding the dynamics of the interaction between tuberculosis and HIV, but, more importantly, the need to obtain better data on the disease duration ratio in different settings. Although incidence and prevalence surveys are difficult to carry out, prevalence surveys have been performed in many countries and their importance for measuring the burden of tuberculosis is increasingly recognized. In several African countries, including Kenya and Malawi, HIV testing among patients with tuberculosis is becoming increasingly routine. Thus, a more immediate way of determining the impact of HIV and the efficacy of tuberculosis control efforts where HIV prevalence is high may be to assess tuberculosis trends in HIV-negative patients with tuberculosis. The study by Wood and colleagues (5) adds to the extensive literature documenting the extent to which HIV is fueling the tuberculosis epidemic in countries with high HIV prevalence (nearly all of which are in sub-Saharan Africa). For several years, WHO has promoted a public health approach to dealing with HIV-related tuberculosis based on both putting out the flames (by controlling tuberculosis more effectively) and starving the fire of its fuel (by controlling HIV) (9). Controlling tuberculosis in populations with high HIV prevalence requires interventions directly targeting tuberculosis (intensified case-finding, improved cure rates, and tuberculosis preventive treatment for those with HIV) and interventions targeting HIV and therefore indirectly targeting tuberculosis (including condom promotion, treatment of sexually transmitted infections, and the provision of antiretroviral therapy) (9). While the performance of the tuberculosis program in the population studied by Wood and coworkers (5) appears to be satisfactory, treatment success nationally remains low (3). Poor treatment increases the risk of drug-resistant tuberculosis which, in its extreme form, has recently generated considerable media attention (10). In South Africa, as throughout Africa, much remains to be done to strengthen tuberculosis programs (including intensifying case-finding to decrease the disease duration and extending the provision of tuberculosis preventive treatment). While Wood and colleagues (5) highlight the importance of good tuberculosis control in putting out the flames of the tuberculosis epidemic, tuberculosis control in Africa depends also on mitigating the impact of HIV, by reducing HIV prevalence, and ensuring wide coverage of antiretroviral therapy, and so decreasing the fuel on the fire (11). Acknowledgments The authors alone are responsible for the views expressed in this editorial, which do not necessarily represent the decisions, policy, or views of the World Health Organization. This editorial has an online supplement, which is accessible from this issue's table of contents at www.atsjournals.org FOOTNOTES Conflict of Interest Statement: Neither author has a financial relationship with a commercial entity that has an interest in the subject of this manuscript. REFERENCES
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