- Email: [email protected]
Assessment of worldwide tuberculosis control
THE LANCET
Assessment of worldwide tuberculosis control
Mario C Raviglione, Christopher Dye, Sonja Schmidt, Arata Kochi, for the WHO Global Surveillance and Monitoring Project*
Summary Background Because worldwide tuberculosis (TB) control had never been assessed, WHO set up a surveillance and monitoring project in 1995. The objectives were to assess the performance of national TB programmes; to assess the extent of implementation of the WHO strategy of TB control; and to attempt a comparison between regions that had adopted the WHO strategy and those that had not. Methods In June, 1996, we sent data-collection forms requesting information on national TB programmes’ control policies, 1995 case notifications, and 1994 treatment results to 216 countries, areas, and territories. We assessed the performance of national TB programmes by comparing case notifications with estimated incidence and by outcome of treatment in cohorts of patients. We also investigated worldwide treatment success and case detection among sputumsmear-positive patients. Findings 180 (83%) of the 216 countries, areas, and territories surveyed replied to WHO (98% of the worldwide population). In 1995, the WHO control strategy had been implemented in 75 countries, and in 39 of these implementation was countrywide. Up to 23% of the worldwide population lived in regions where the strategy was available. In 1995, 3 297 688 cases of TB (all types) were reported, of which 1 161 411 (35%) were sputum-smear positive. 54% of all reported cases in countries that used the WHO strategy were sputumsmear positive, compared with 30% in other countries. The worldwide case-detection rate of new sputum-smearpositive cases was 35%. 92% of cases registered for treatment in 1994 in regions that used WHO strategy were assessed for outcome and 76% were treated successfully, compared with 54% and 42%, respectively, in regions that had not implemented the WHO strategy. Among cases reported worldwide in 1994, the documented treatment-success rate was 43%. Interpretation National TB programmes that have adopted the WHO TB control strategy achieve higher cure rates, but their impact on TB is modest on a *Other participants listed at end of paper Global Tuberculosis Programme, World Health Organization, 20 Avenue Appia CH-1211, Geneva 27, Switzerland (M C Raviglione MD, C Dye DPhil, S Schmidt MPH, A Kochi MD) Correspondence to: Dr Mario C Raviglione (e-mail: [email protected])
624
worldwide scale. Wider continuous coverage with the WHO strategy is needed for effective worldwide TB control.
Lancet 1997; 350: 624–29
Introduction Tuberculosis (TB) has been neglected as a publichealth issue for many years by many countries and remains the major cause of death from a single infectious agent among adults in developing countries. There has been a resurgence of TB in industrialised countries.1 Several factors, most notably a lack of resources and government commitment, have prevented adequate implementation of control measures. In many countries of Africa and southeast Asia, infection with HIV has further increased TB morbidity and mortality.2–4 In several formerly socialist countries, TB morbidity and mortality continue to rise because of the deterioration of public-health systems.5 Finally, in many industrialised countries the recent increase of TB, which is due largely to cases among immigrants from other countries,6–8 is the direct consequence of worldwide neglect. In 1993, WHO declared TB to be a global emergency.1 The exact burden of disease, however, is not known and the worldwide achievements of national TB control programmes in terms of diagnosis and treatment results have not been analysed. The key to controlling TB is rapid detection and cure of infectious cases by TB control programmes. In 1991, the World Health Assembly recommended that national TB programmes should work towards two objectives by the year 2000: to treat successfully 85% and to detect 70% of smear-positive cases9 by the introduction of an effective approach to TB control. The WHO TB control strategy (directly observed treatment, short course) is defined by five elements: government commitment to TB control; case detection focusing on patients with symptoms self-reporting to health services and use of sputum-smear microscopy; administration of short-course chemotherapy in a standard way throughout the country with direct observation of treatment during, at least, the first 2 months of treatment; a regular supply of all essential antituberculosis drugs; and a standard recording and reporting system that allows assessment of treatment results.10 To assess the achievements of TB control, WHO set up a worldwide surveillance and monitoring project in 1995. We present the first results, focusing on the extent of implementation of the WHO strategy and the
Vol 350 • August 30, 1997
THE LANCET
Has the country reported to WHO on TB control activities?
No
Yes
Category 0
Does the country accept the WHO TB control strategy? Yes
<10% coverage
10–90% coverage
No >90% coverage
Is the country’s case-notification rate <10 per Category 2 Category 3 Category 4 100 000 population?
Yes
No
Category 5 Category 1 Categorisation of countries
performance of national TB programmes, and attempt to compare areas that have and have not adopted the WHO strategy.
Methods In early 1996, we developed two data-collection forms requesting information on TB-control policy, cases reported for 1995, and treatment outcomes among patients registered during 1994. The first form asked questions in the standard format proposed by WHO10 for countries or areas within countries where the WHO strategy was implemented. The second form was designed for countries and areas where the WHO strategy had not been implemented and did not request certain data—for example, re-treatment results. The apparent lack of synchronisation between case notification data for 1995 and treatment outcomes for 1994 reflects the fact that the figures reported were the latest available. Information from countries consisted of case notifications for 1995 compiled at the beginning of 1996, and treatment results for all patients registered in 1994, available only at the end of 1995 because treatment lasts for 6–8 months. We compared the performance of national TB programmes that did and did not follow the WHO recommendations. Not all countries had implemented WHO strategy countrywide, and we expected that they would return both forms. To assist countries in accurately completing these forms, we also sent detailed instructions and definitions with the questionnaires. In May, 1996, 216 countries, areas, and territories were sent forms via WHO’s regional offices. We used reports from WHO and other organisations involved in TB control and published data to cross-check data received from the national TB programmes. In addition, each staff member at WHO Headquarters and the regional offices World Bank regions
Number of countries
Number of countries reporting
CHI EME FSE IND LAC MEC OAI SSA Worldwide
1 27 19 1 45 32 44 47 216
1 (100%) 19 (70%) 19 (100%) 1 (100%) 34 (76%) 28 (88%) 34 (77%) 44 (94%) 180 (83%)
responsible for coordinating regional and country activities systematically analysed the data received. Any inconsistencies (such as incorrect calculations) were checked by the regional offices with the national TB programmes directly until information was satisfactory. We developed a database with Microsoft Access, version 2.0, to manage and analyse the data. Data from both forms were included. To check for data-entry errors, all database outputs for single countries were compared with the original data-collection forms. Countries were separated into those that had adopted the WHO strategy, classified by degree of implementation, and those that had not yet adopted the strategy, classified by notification rate. We included estimates of death rates for countries not reporting to WHO when appropriate. Countries or regions that had accepted the WHO strategy are referred to as “WHO areas” in this paper. A country was deemed to have adopted the WHO strategy if it had a technical policy for case finding and management consistent with WHO recommendations incorporated in a national TB control manual endorsed by WHO, and the national TB programme’s staff had led or attended a WHO standard training course on management of TB at district level within the previous 5 years or, at least, ensured that training or education consistent with WHO recommendations were available in the country, (eg, those provided by the International Union Against Tuberculosis and Lung Disease). The country categories are shown in the figure. We assessed national TB programmes at country, area, and worldwide levels by various performance indicators. For the regional assessment, although data were available for both WHO and World Bank regions, we aggregated the countries by World Bank regions (China, established market economies, formerly socialist economies of Europe, India, Latin America and the Caribbean, middle eastern crescent, other Asia and islands, and sub-Saharan Africa). 11 Based on the data provided in both forms, we assessed TB programmes separately by areas that had and had not implemented WHO strategy. For case detection, 1995 case notifications distinguished between all types of TB and sputum-smear-positive cases. Case notifications represent only some of the true number of cases in a country because of difficulties with health-service coverage, detection of suspect cases, diagnosis of cases, and their recording and reporting. Therefore, we had to estimate the true number of cases. The ratio of cases notified in a given year (as a proxy of those detected) to the estimated annual incidence is an indicator of the national TB programme’s detection efficiency (case-detection rate), expressed as a percentage. To calculate the case-detection rate we used an estimate of total TB incidence based on the annual risk of infection method12 and published in the World Bank’s World Development Report, 1993.11 Since country-specific estimates were made for 1990, when we applied them to 1995 populations we adjusted them if necessary according to information available at WHO from after 1990. Because the estimates include information on all cases of tuberculosis, we divided the figures by 2·2 to analyse only new smear-positive cases, based on the empirical evidence that for each one
Number of countries in categories Category 0
Category 1
Category 2
Category 3
Category 4
Category 5
.. 8 .. .. 11 4 10 3 36
.. 9 17 .. 16 15 13 14 84
.. .. .. 1 .. 1 4 1 7
1 .. .. .. 3 6 7 12 29
.. 2 2 .. 5 3 10 17 39
.. 8 .. .. 10 3 .. .. 21
CHI=China; EME=established market economies; FSE=formerly socialist economies of Europe; IND=India; LAC=Latin America and the Caribbean; MEC=middle eastern crescent; OAI=other Asia and island; SSA-sub-Saharan Africa.
Table 1: Status of tuberculosis control in countries reporting to WHO, 1995
Vol 350 • August 30, 1997
625
THE LANCET
Strategy*
% total population
Number of cases notified
Notified cases as % of total notified cases
Number of sputum-smearpositive cases
CHI WHO Non-WHO No report
50·0 50·0 0
157 935 199 894 ..
44·1 55·9 ..
90 554 43 934 ..
EME WHO Non-WHO No report
3·1 91·6 5·4
7196 114 337 ..
5·9 94·1 ..
2019 35 531 0
FSE WHO Non-WHO No report
4·6 95·4 0
3374 174 554 ..
1·9 98·1 ..
1275 73 771 ..
IND WHO Non-WHO No report
1·5 98·5 0
5047 1 209 829 ..
0·4 99·6 ..
1985 262 633 ..
LAC WHO Non-WHO No report
15·9 79·3 4·8
63 636 151 876 ..
29·5 70·5 ..
43 290 83 802 0
MEC WHO Non-WHO No report
18·8 73·5 7·7
58 116 146 048 ..
28·5 71·5 ..
25 086 47 948 0
OAI WHO Non-WHO No report
23·8 72·7 3·5
100 189 438 233 ..
18·6 81·4 ..
60 066 199 193 0
SSA WHO Non-WHO No report
48·2 51·7 0·1
304 286 163 138 ..
65·1 34·9 ..
153 191 37 133 0
Worldwide WHO Non-WHO No report
23·0 74·6 2·4
699 779 2 597 909 ..
21·2 78·8 ..
377 466 783 945 0
CHI EME FSE IND LAC MEC OAI SSA Worldwide
Case detection rate (%) Sputum-smear-positive cases
All cases
29 50 64 29 66 30 37 32 35
35 74 69 60 51 38 35 36 45
Region abbreviations as in table 1.
% may add up to more than 100% because of rounding. Region abbreviations as in table 1. *WHO=areas that have implemented WHO TB control strategy; non-WHO=areas that have not implemented WHO control strategy.
Table 2: Case notifications by World Bank region, 1995 sputum-smear positive case, 1·2 other (sputum-smear and extrapulmonary) cases occur.13 All countries, including those not reporting to WHO, were included for the incidence estimates. To assess the quality of treatment programmes for new infectious cases, we first calculated the proportion of registered cases being assessed for outcome to show the programmes’ performance in assessment of results. Second, we assessed six standard and mutually exclusive outcomes of treatment as percentages of all registered cases, so that the total of all the outcomes and the non-assessed cases came to 100. We defined the outcomes as follows. Cured patients were initially smear positive and had negative sputum-smear results after completion of treatment on at least two occasions during the continuation phase (4–6 months), including one at completion of treatment. Treatment completed patients were sputum-smear positive and had negative sputum-smear results at the end of the initial phase after completion of treatment, with no or only one negative sputum-smear result in the continuation phase and none at the end of treatment. Died was used for any death during treatment, irrespective of cause. Failed patients remained or became smear positive again at least 5 months after the start of treatment. Interrupted treatment (defaulted) was used for patients who did not collect drugs for 2 months or more at any time after registration. Transferred out was used for patients who were transferred to another reporting unit whose results were not known. In addition to these outcomes, documented treatment success was obtained by adding the percentage of cured cases to that of cases who completed treatment.
626
World Bank regions
Table 3: Case detection rates based on World Bank Development Report by World Bank region, 1995 To calculate the worldwide treatment-success rate, we added the number of cured and completed treatment cases in the WHO and non-WHO regions. We calculated the rate in terms of the number of sputum-smear-positive cases notified and the number of cases registered for treatment in 1994, worldwide. The number notified, which is not available for WHO and non-WHO areas separately, 14 is generally more than the number of cases registered.
Results By 1 July, 1997, WHO had received data from 180 countries, areas, and territories (83% of the 216 surveyed, 98% of the worldwide population). Of these, 84 (47%) areas had not yet accepted the WHO strategy, 75 (42%) had implemented the strategy (39 in >90% of the population), and 21 (12%) had a casenotification rate of less than ten per 100 000 population (table 1). 2% of the worldwide population lived in countries that did not report to WHO, 27% in countries where the WHO strategy was not implemented anywhere, 7% in countries that had a low incidence of TB, and 64% in countries that had adopted the WHO strategy. However, in these countries diagnostic and treatment services that follow the WHO strategy were available in only a few healthadministration units. Therefore, we estimated that the percentage of the worldwide population with access to these services was 23% (table 2). The 180 countries, areas, and territories reporting to WHO reported 3 297 688 cases of TB (59·1 per 100 000 population). Of these, 1 161 411 (35%) were sputum-smear positive. Of the total cases reported, 699 779 (21%) were from areas in which the WHO strategy was implemented and 2 597 909 (79%) were from other areas (table 2). 54% of all cases in areas where the WHO strategy was implemented were sputum-smear positive, compared with 30% in the other areas. Furthermore, 64% of new pulmonary cases in WHO areas were sputum-smear positive compared with 33% in other areas. Based on the World Bank’s World Development Report, estimated incidence rates adjusted for population growth since 1990 suggested that an estimated 3·32 million new smear-positive cases and 7.32 million cases of all TB occurred in 1995.11 Of these, 1·16 million and 3·30 million, respectively, were notified, which is a case-detection rate of 35% among new sputum-smear-positive cases and 45% among all cases (table 3). Based on reports to WHO collected in 1995, 977 679 new sputum-smear-positive cases were notified by 141 countries in 1994.14 Of these, 808 898 (83%) were registered for treatment according to the 1996
Vol 350 • August 30, 1997
THE LANCET
Strategy*
Number of cases registered
% cases not assessed
% cured
% completed treatment
% treatment interrupted
% failed
% died
% transferred out
Treatment success
CHI WHO Non-WHO
59 500 36 987
1 1
92 86
2 0
1 4
2 6
2 2
0 1
94 86
EME WHO Non-WHO
1924 2
26 0
28 0
32 100
5 0
2 0
4 0
2 0
60 100
FSE WHO Non-WHO
930 64 694
0 4
78 64
5 3
1 2
2 5
7 21
7 1
83 67
IND WHO Non-WHO
1026 226 543
0 100
82 ..
1
6 ..
2 ..
4 ..
5 ..
83 ..
LAC WHO Non-WHO
45 059 35 723
9 32
61 27
16 24
7 10
2 1
3 3
2 3
77 51
MEC WHO Non-WHO
18 091 35 386
1 21
74 34
8 21
7 8
1 3
2 6
7 7
82 55
OAI WHO Non-WHO
42 199 119 246
5 4
79 62
3 15
4 9
2 2
2 2
5 6
82 77
SSA WHO Non-WHO
78 652 42 936
18 10
47 27
11 41
11 12
1 2
6 5
6 3
58 68
Worldwide WHO Non-WHO
247 381 561 517
8 46
68 32
8 10
7 4
1 2
4 4
4 2
76 42
..
Region abbreviations as in table 1. *WHO=areas that have implemented WHO TB control strategy; non-WHO=areas that have not implemented WHO TB control strategy.
Table 4: Number of registered cases and treatment results for new smear-positive cases by World Bank region and treatment strategy, 1994
data-collection forms. In areas that have adopted the WHO strategy, 247 381 new sputum-smear-positive cases were registered for treatment (table 4), and the outcomes of 226 628 (92%) of them were assessed. The documented treatment-success rate among all registered sputum-smear-positive cases in the WHO areas was 76% (table 4). The highest treatment-success rate (94%) was reported from China. The outcome was uncertain in 19% of cases (not assessed, interrupted treatment, and transferred out). In areas where the WHO strategy was not implemented, 561 517 new sputum-smear-positive cases were registered for treatment. Of these, 304 562 (54%) were assessed for treatment results (table 4). The documented treatment-success rate among all registered cases was 42% (table 4). The outcome was uncertain in 52% of cases (not assessed, defaulted, and transferred out), which was due largely to the lack of assessment of treatment results in India. The weighted worldwide treatment-success average was 52%. This figure corresponds to 422 155 cases. However, this rate decreased to 43% when we used the number of cases notified for 1994 as the denominator (977 679, table 4).
Discussion The main purposes of this study were to assess the extent of implementation of the WHO strategy worldwide, the achievements of national TB programmes, and the progress towards the achievements of the two WHO targets set by the World Health Assembly in 1991.9 Of the 216 countries, areas, and territories surveyed, 83% replied to WHO. By the end of 1995, the WHO strategy had been accepted in 75 countries (35% of the 216 surveyed),
Vol 350 • August 30, 1997
but only 39 countries had implemented the strategy countrywide. The remaining countries had implemented the strategy in only part of their territory, or only as far as the first phase, or in pilot projects. Therefore, at the beginning of 1995, only 23% of the worldwide population was covered by control programmes that followed the WHO strategy. The information given on populations living in regions where the WHO strategy is implemented must, therefore, be treated with caution. However, of the high-incidence countries that have not accepted the WHO strategy, some, such as Oman, Myanmar, Kyrgyzstan, and Thailand, were in a preparatory phase in early 1996. Of the 3 297 688 cases notified for 1995, 21% were reported from areas in which the WHO strategy was implemented. This proportion should increase as more and more national TB programmes adopt WHO strategy. The limitations of our worldwide assessment must be acknowledged. First, interpretation of the performance indicators in areas that had not implemented the WHO strategy was difficult, since definitions were not standard. The reliability of these data is also variable. Furthermore, the success in WHO areas may also be influenced by factors other than the technical elements of the WHO strategy. For example, a country with a generally good health system may have been more likely to adopt the strategy than one with a poor system. We found a further limitation when we averaged performance indicators by region. A few countries with many TB cases may dominate regional averages, although the use of World Bank areas allowed at least a separate assessment of India and China. Despite these limitations, assessment of the national TB programmes’ performance is important. 627
THE LANCET
Bringing together the results from WHO and nonWHO areas gives an overview of the treatment-success rate worldwide. National TB programmes documented a treatment-success rate of only 43% among all notified cases. Many patients interrupt treatment (up to 12% in sub-Saharan Africa where the WHO strategy was not implemented). Some patients fail treatment and need to be re-treated at a later date. Some die of TB: at least 5–6% in sub-Saharan Africa, where the influence of HIV infection is greater than anywhere else, and as many as 21% in the formerly socialist economies of Europe, in which WHO strategy has not been implemented. These countries are mostly of the former Soviet Union, where national TB programmes are collapsing and drugs are in poor supply.5 Documented treatment-success rates help in the assessment of achievements of TB control programmes as recorded results. However, these results do not apply to cases that were not notified, not registered for treatment, not assessed, or recorded as treatment interrupted and transferred out. We therefore constructed two hypothetical models in an attempt to calculate the true worldwide cure rate. Given that TB spontaneously resolves in about a third of cases,15,16 the lower estimate of a favourable outcome is 37%. On the other hand, if we assume that in the best of circumstances treatment-success rates were the same for assessed and non-assessed cases, the true worldwide cure rate could be as high as 78%. In these aggregated results we found important differences in the treatment-success rates between WHO and non-WHO areas. First, in areas where the WHO strategy was implemented, 92% of the registered cases were assessed, compared with only 54% in the non-WHO areas. Therefore, the performance indicators of the non-WHO TB-control areas apply only to a small proportion of all cases in these areas. Second, the documented treatment-success rate among new sputum-smear-positive cases was 76% in those areas where the WHO strategy was implemented and only 42% in other areas, mostly because there are no outcome data from India. If we exclude India from the worldwide assessment, the treatment success in nonWHO areas was 70%. Conversely, the sum of unknown or unsuccessful outcomes was much higher in nonWHO areas (58% vs 24%). Although patients who die are less important for transmission of TB infection and perpetuation of the epidemic, patients who stop treatment, defaulters, and to a certain extent transferred-out cases constitute, together with cases registered for treatment and not assessed, an uncertainty index. One way of assessing the effectiveness of case-finding is based on calculation of the proportion of cases that were sputum-smear-positive. This proportion was expected to be between 50% and 66%, but was less than a third in developing countries in which the WHO strategy was not implemented. This small proportion shows a lack of emphasis on detection and giving priority to infectious TB cases or inappropriate diagnosis in the non-WHO areas, or both. Data from all 180 countries, areas, and territories that replied suggest that the percentage of new infectious cases notified in 1995 was only 35% of the estimated incidence and that it could be lower. The credibility of this indicator depends on the quality of 628
the information system. High case-detection rates are credible in countries that have adopted the WHO strategy and have sound methods of reporting and treating TB patients, such as Botswana (81%), Morocco (93%), Peru (94%), Tanzania (80%), and Vietnam (67%). Some countries that had not implemented the WHO strategy also seemed to have high case-detection rates of above 50%. However, we were suspicious about these rates because information gathering is generally poor in these countries. The rates suggest that too many cases are notified or that incidence estimates in the 1994 World Development Report11 are too low. Even with uncertainty about the estimate of 35%, detection of only about a third of new cases is unlikely to lead to TB elimination, since transmission of infection from undetected or untreated cases will be perpetuated. There is a great need to improve worldwide TB control. Many cases clearly remain undiagnosed and receive no treatment at all, many cases are diagnosed outside national TB programmes, and many receive inadequate treatment.17 Such patients commonly are persistently infectious, chronically ill, and more likely to die, and they carry drug-resistant strains.18 Implementation of a sound TB control strategy is clearly necessary in all countries to improve TB control worldwide. Initially proven to be effective in the national TB programmes assisted by the IUATLD,19,20 the preferred approach has been refined and promoted by WHO intensively in the past 6 years. Results have shown that the strategy is effective. For example, the treatment success documented in China21 and Tanzania20 and the increase in successes after years of decline in Malawi22 suggest that the strategy works well in different settings. More proof is provided by the national TB programmes in Morocco and Peru, which have both achieved consistently high cure rates for several years (data given to WHO from these programmes) and reductions in case notifications. Intensified technical and financial assistance to countries is, therefore, likely to result in increased case detection and treatment success, and, at the same time, an improved quality of information collected by the national TB programmes. Better information will, in turn, allow a better assessment of the achievements of national TB programmes, ultimately challenging countries to improve their control efforts. WHO Global Surveillance and Monitoring Project P Chaulet, M Grzemska, C Hanson, J Kumaresan, M Levy, F Luelmo, P P Nunn, S Spinaci, E Tayler, (Global Tuberculosis Programme, Geneva, Switzerland); E Nyarko, J-C Willame (WHO African Regional Office, Brazzaville, Congo); R R Cruz, D Weil (WHO American Regional Office, Washington DC, USA); Z Hallaj, A Seita (WHO Eastern Mediterranean Regional Office, Alexandria, Egypt); T-A Madaras (WHO European Regional Office, Copenhagen, Denmark); M V H Gunaratne (WHO South- East Asian Regional Office, Delhi, India); L Blanc, D I Ahn (WHO Western Pacific Regional Office, Manila, Philippines).
Contributors Mario Raviglione, Sergio Spinaci, and Arata Kochi were responsible for protocol design. Mario Raviglione, Sonja Schmidt, and Paul Nunn (GTB, Geneva) coordinated the study. Data were collected and verified by Sonja Schmidt, Pierre Chaulet, Malgorzata Grzemska, Christy Hanson, Jacob Kumaresan, Michael Levy, Fabio Luelmo, Sergio Spinaci, Elizabeth Tayler (GTB, Geneva); Eugene Nyarko, Jean-Claude Willame (WHO Arican Regional Office, Brazzaville, Congo); Rodolfo Rodriguez Cruz, Diana Weil (WHO American
Vol 350 • August 30, 1997
THE LANCET Regional Office, Washington DC, USA); Zoheir Hallaj, Akihiro Seita (WHO Eastern Mediterranean Regional Office, Alexandria, Egypt); Tünde-Agnes Madaras (WHO European Regional Office, Copenhagen, Denmark); Methsiri Gunaratne (WHO South-East Asian Regional Office, Delhi, India); Leopold Blanc, Dong Il Ahn (WHO Western Pacific Regional Office, Manila, Philippines). The data were analysed by Mario Raviglione and Christopher Dye. Mario Raviglione, Christopher Dye, and Sonja Schmidt wrote the paper.
Acknowledgments We thank all the National Tuberculosis Programme managers who provided their country data to WHO; WHO tuberculosis country advisors who collected and reviewed data from the national programmes; and H Rieder of the International Union Against Tuberculosis and Lung Disease for providing useful comments on the manuscript.
9
10
11 12
13
14
References 1
2
3 4
5
6
7
8
Raviglione MC, Snider DE Jr, Kochi A. Global epidemiology of tuberculosis: morbidity and mortality of a worldwide epidemic. JAMA 1995; 273: 220–26. Narain JP, Raviglione MC, Kochi A. HIV-associated tuberculosis in developing countries: epidemiology and strategies for prevention. Tuberc Lung Dis 1992; 73: 311–21. De Cock KM, Soro B, Coulibaly IM, Lucas SB. Tuberculosis and HIV infection in sub-Saharan Africa. JAMA 1992; 268: 1581–87. Yanai H, Uthaivoravit W, Panich V, et al. Rapid increase in HIV-related tuberculosis, Chiang Rai, Thailand, 1990–1994. AIDS 1996; 10: 527–31. Raviglione MC, Rieder HL, Styblo K, Khomenko AG, Esteves K, Kochi A. Tuberculosis trends in Eastern Europe and the former USSR. Tuberc Lung Dis 1994; 75: 400–16. Cantwell MF, Snider DE Jr, Cauthen GM, Onorato IM. Epidemiology of tuberculosis in the United States, 1985 through 1992. JAMA 1994; 272: 535–39. McKenna MT, McCray E, Onorato I. The epidemiology of tuberculosis among foreign-born persons in the United States, 1986 to 1993. N Engl J Med 1995; 332: 1071–76. Raviglione MC, Sudre P, Rieder HL, Spinaci S, Kochi A. Secular
Vol 350 • August 30, 1997
15
16 17 18 19 20
21
22
trends of tuberculosis in Western Europe. Bull World Health Organ 1993; 71: 297–306. World Health Organization. Forty-Fourth World Health Assembly, Geneva, 6-16 May 1991. Resolutions and decisions. Geneva, Switzerland: WHO 1991; WHA44/1991/REC/1. World Health Organization. WHO Tuberculosis Programme: framework for effective tuberculosis control. Geneva, Switzerland: WHO 1994; WHO/TB/94.179. The World Bank. World Development Report 1993: investing in health. New York: Oxford University Press, 1993; 1–225. Styblo K. The relationship between the risk of tuberculous infection and the risk of developing infectious tuberculosis. Bull Int Union Tuberc Lung Dis 1986; 60: 117–19. Murray CJL, Styblo K, Rouillon A. Tuberculosis in developing countries: burden, intervention and cost. Bull Int Union Tuberc Lung Dis 1990; 65: 6–24. World Health Organization. Global Tuberculosis Programme: global tuberculosis control. Geneva, Switzerland: WHO Report, 1997; WHO/TB/97.225. National Tuberculosis Institute, Bangalore. Tuberculosis in a rural population of south India: a five-year epidemiological study. Bull World Health Organ 1974; 51: 473–88. Springett VH. Ten-year results during the introduction of chemotherapy for tuberculosis. Tubercle 1971; 52: 73–87. Uplekar MW, Rangan S. Private doctors and tuberculosis control in India. Tuberc Lung Dis 1993; 74: 332–37. Jain NK. Drug resistance in India: a tragedy in the making. Ind J Tuberc 1992; 39: 145–48. Enarson D. Principles of IUATLD collaborative tuberculosis programmes. Bull Int Union Tuberc Lung Dis 1991; 66: 195–200. Styblo K. Overview and epidemiologic assessment of the current global tuberculosis situation with an emphasis on control in developing countries. Rev Infect Dis 1989; 11 (suppl 2): S339–46. China Tuberculosis Control Collaboration. Results of directly observed short-course chemotherapy in 112 842 Chinese patients with smear-positive tuberculosis. Lancet 1996; 347: 358–62. Harries AD, Nyong’Onya Mbewe L, Salaniponi FML, et al. Tuberculosis programme changes and treatment outcomes in patients with smear-positive pulmonary tuberculosis in Blantyre, Malawi. Lancet 1996, 347: 807–09.
629
Assessment of worldwide tuberculosis control
Mario C Raviglione, Christopher Dye, Sonja Schmidt, Arata Kochi, for the WHO Global Surveillance and Monitoring Project*
Summary Background Because worldwide tuberculosis (TB) control had never been assessed, WHO set up a surveillance and monitoring project in 1995. The objectives were to assess the performance of national TB programmes; to assess the extent of implementation of the WHO strategy of TB control; and to attempt a comparison between regions that had adopted the WHO strategy and those that had not. Methods In June, 1996, we sent data-collection forms requesting information on national TB programmes’ control policies, 1995 case notifications, and 1994 treatment results to 216 countries, areas, and territories. We assessed the performance of national TB programmes by comparing case notifications with estimated incidence and by outcome of treatment in cohorts of patients. We also investigated worldwide treatment success and case detection among sputumsmear-positive patients. Findings 180 (83%) of the 216 countries, areas, and territories surveyed replied to WHO (98% of the worldwide population). In 1995, the WHO control strategy had been implemented in 75 countries, and in 39 of these implementation was countrywide. Up to 23% of the worldwide population lived in regions where the strategy was available. In 1995, 3 297 688 cases of TB (all types) were reported, of which 1 161 411 (35%) were sputum-smear positive. 54% of all reported cases in countries that used the WHO strategy were sputumsmear positive, compared with 30% in other countries. The worldwide case-detection rate of new sputum-smearpositive cases was 35%. 92% of cases registered for treatment in 1994 in regions that used WHO strategy were assessed for outcome and 76% were treated successfully, compared with 54% and 42%, respectively, in regions that had not implemented the WHO strategy. Among cases reported worldwide in 1994, the documented treatment-success rate was 43%. Interpretation National TB programmes that have adopted the WHO TB control strategy achieve higher cure rates, but their impact on TB is modest on a *Other participants listed at end of paper Global Tuberculosis Programme, World Health Organization, 20 Avenue Appia CH-1211, Geneva 27, Switzerland (M C Raviglione MD, C Dye DPhil, S Schmidt MPH, A Kochi MD) Correspondence to: Dr Mario C Raviglione (e-mail: [email protected])
624
worldwide scale. Wider continuous coverage with the WHO strategy is needed for effective worldwide TB control.
Lancet 1997; 350: 624–29
Introduction Tuberculosis (TB) has been neglected as a publichealth issue for many years by many countries and remains the major cause of death from a single infectious agent among adults in developing countries. There has been a resurgence of TB in industrialised countries.1 Several factors, most notably a lack of resources and government commitment, have prevented adequate implementation of control measures. In many countries of Africa and southeast Asia, infection with HIV has further increased TB morbidity and mortality.2–4 In several formerly socialist countries, TB morbidity and mortality continue to rise because of the deterioration of public-health systems.5 Finally, in many industrialised countries the recent increase of TB, which is due largely to cases among immigrants from other countries,6–8 is the direct consequence of worldwide neglect. In 1993, WHO declared TB to be a global emergency.1 The exact burden of disease, however, is not known and the worldwide achievements of national TB control programmes in terms of diagnosis and treatment results have not been analysed. The key to controlling TB is rapid detection and cure of infectious cases by TB control programmes. In 1991, the World Health Assembly recommended that national TB programmes should work towards two objectives by the year 2000: to treat successfully 85% and to detect 70% of smear-positive cases9 by the introduction of an effective approach to TB control. The WHO TB control strategy (directly observed treatment, short course) is defined by five elements: government commitment to TB control; case detection focusing on patients with symptoms self-reporting to health services and use of sputum-smear microscopy; administration of short-course chemotherapy in a standard way throughout the country with direct observation of treatment during, at least, the first 2 months of treatment; a regular supply of all essential antituberculosis drugs; and a standard recording and reporting system that allows assessment of treatment results.10 To assess the achievements of TB control, WHO set up a worldwide surveillance and monitoring project in 1995. We present the first results, focusing on the extent of implementation of the WHO strategy and the
Vol 350 • August 30, 1997
THE LANCET
Has the country reported to WHO on TB control activities?
No
Yes
Category 0
Does the country accept the WHO TB control strategy? Yes
<10% coverage
10–90% coverage
No >90% coverage
Is the country’s case-notification rate <10 per Category 2 Category 3 Category 4 100 000 population?
Yes
No
Category 5 Category 1 Categorisation of countries
performance of national TB programmes, and attempt to compare areas that have and have not adopted the WHO strategy.
Methods In early 1996, we developed two data-collection forms requesting information on TB-control policy, cases reported for 1995, and treatment outcomes among patients registered during 1994. The first form asked questions in the standard format proposed by WHO10 for countries or areas within countries where the WHO strategy was implemented. The second form was designed for countries and areas where the WHO strategy had not been implemented and did not request certain data—for example, re-treatment results. The apparent lack of synchronisation between case notification data for 1995 and treatment outcomes for 1994 reflects the fact that the figures reported were the latest available. Information from countries consisted of case notifications for 1995 compiled at the beginning of 1996, and treatment results for all patients registered in 1994, available only at the end of 1995 because treatment lasts for 6–8 months. We compared the performance of national TB programmes that did and did not follow the WHO recommendations. Not all countries had implemented WHO strategy countrywide, and we expected that they would return both forms. To assist countries in accurately completing these forms, we also sent detailed instructions and definitions with the questionnaires. In May, 1996, 216 countries, areas, and territories were sent forms via WHO’s regional offices. We used reports from WHO and other organisations involved in TB control and published data to cross-check data received from the national TB programmes. In addition, each staff member at WHO Headquarters and the regional offices World Bank regions
Number of countries
Number of countries reporting
CHI EME FSE IND LAC MEC OAI SSA Worldwide
1 27 19 1 45 32 44 47 216
1 (100%) 19 (70%) 19 (100%) 1 (100%) 34 (76%) 28 (88%) 34 (77%) 44 (94%) 180 (83%)
responsible for coordinating regional and country activities systematically analysed the data received. Any inconsistencies (such as incorrect calculations) were checked by the regional offices with the national TB programmes directly until information was satisfactory. We developed a database with Microsoft Access, version 2.0, to manage and analyse the data. Data from both forms were included. To check for data-entry errors, all database outputs for single countries were compared with the original data-collection forms. Countries were separated into those that had adopted the WHO strategy, classified by degree of implementation, and those that had not yet adopted the strategy, classified by notification rate. We included estimates of death rates for countries not reporting to WHO when appropriate. Countries or regions that had accepted the WHO strategy are referred to as “WHO areas” in this paper. A country was deemed to have adopted the WHO strategy if it had a technical policy for case finding and management consistent with WHO recommendations incorporated in a national TB control manual endorsed by WHO, and the national TB programme’s staff had led or attended a WHO standard training course on management of TB at district level within the previous 5 years or, at least, ensured that training or education consistent with WHO recommendations were available in the country, (eg, those provided by the International Union Against Tuberculosis and Lung Disease). The country categories are shown in the figure. We assessed national TB programmes at country, area, and worldwide levels by various performance indicators. For the regional assessment, although data were available for both WHO and World Bank regions, we aggregated the countries by World Bank regions (China, established market economies, formerly socialist economies of Europe, India, Latin America and the Caribbean, middle eastern crescent, other Asia and islands, and sub-Saharan Africa). 11 Based on the data provided in both forms, we assessed TB programmes separately by areas that had and had not implemented WHO strategy. For case detection, 1995 case notifications distinguished between all types of TB and sputum-smear-positive cases. Case notifications represent only some of the true number of cases in a country because of difficulties with health-service coverage, detection of suspect cases, diagnosis of cases, and their recording and reporting. Therefore, we had to estimate the true number of cases. The ratio of cases notified in a given year (as a proxy of those detected) to the estimated annual incidence is an indicator of the national TB programme’s detection efficiency (case-detection rate), expressed as a percentage. To calculate the case-detection rate we used an estimate of total TB incidence based on the annual risk of infection method12 and published in the World Bank’s World Development Report, 1993.11 Since country-specific estimates were made for 1990, when we applied them to 1995 populations we adjusted them if necessary according to information available at WHO from after 1990. Because the estimates include information on all cases of tuberculosis, we divided the figures by 2·2 to analyse only new smear-positive cases, based on the empirical evidence that for each one
Number of countries in categories Category 0
Category 1
Category 2
Category 3
Category 4
Category 5
.. 8 .. .. 11 4 10 3 36
.. 9 17 .. 16 15 13 14 84
.. .. .. 1 .. 1 4 1 7
1 .. .. .. 3 6 7 12 29
.. 2 2 .. 5 3 10 17 39
.. 8 .. .. 10 3 .. .. 21
CHI=China; EME=established market economies; FSE=formerly socialist economies of Europe; IND=India; LAC=Latin America and the Caribbean; MEC=middle eastern crescent; OAI=other Asia and island; SSA-sub-Saharan Africa.
Table 1: Status of tuberculosis control in countries reporting to WHO, 1995
Vol 350 • August 30, 1997
625
THE LANCET
Strategy*
% total population
Number of cases notified
Notified cases as % of total notified cases
Number of sputum-smearpositive cases
CHI WHO Non-WHO No report
50·0 50·0 0
157 935 199 894 ..
44·1 55·9 ..
90 554 43 934 ..
EME WHO Non-WHO No report
3·1 91·6 5·4
7196 114 337 ..
5·9 94·1 ..
2019 35 531 0
FSE WHO Non-WHO No report
4·6 95·4 0
3374 174 554 ..
1·9 98·1 ..
1275 73 771 ..
IND WHO Non-WHO No report
1·5 98·5 0
5047 1 209 829 ..
0·4 99·6 ..
1985 262 633 ..
LAC WHO Non-WHO No report
15·9 79·3 4·8
63 636 151 876 ..
29·5 70·5 ..
43 290 83 802 0
MEC WHO Non-WHO No report
18·8 73·5 7·7
58 116 146 048 ..
28·5 71·5 ..
25 086 47 948 0
OAI WHO Non-WHO No report
23·8 72·7 3·5
100 189 438 233 ..
18·6 81·4 ..
60 066 199 193 0
SSA WHO Non-WHO No report
48·2 51·7 0·1
304 286 163 138 ..
65·1 34·9 ..
153 191 37 133 0
Worldwide WHO Non-WHO No report
23·0 74·6 2·4
699 779 2 597 909 ..
21·2 78·8 ..
377 466 783 945 0
CHI EME FSE IND LAC MEC OAI SSA Worldwide
Case detection rate (%) Sputum-smear-positive cases
All cases
29 50 64 29 66 30 37 32 35
35 74 69 60 51 38 35 36 45
Region abbreviations as in table 1.
% may add up to more than 100% because of rounding. Region abbreviations as in table 1. *WHO=areas that have implemented WHO TB control strategy; non-WHO=areas that have not implemented WHO control strategy.
Table 2: Case notifications by World Bank region, 1995 sputum-smear positive case, 1·2 other (sputum-smear and extrapulmonary) cases occur.13 All countries, including those not reporting to WHO, were included for the incidence estimates. To assess the quality of treatment programmes for new infectious cases, we first calculated the proportion of registered cases being assessed for outcome to show the programmes’ performance in assessment of results. Second, we assessed six standard and mutually exclusive outcomes of treatment as percentages of all registered cases, so that the total of all the outcomes and the non-assessed cases came to 100. We defined the outcomes as follows. Cured patients were initially smear positive and had negative sputum-smear results after completion of treatment on at least two occasions during the continuation phase (4–6 months), including one at completion of treatment. Treatment completed patients were sputum-smear positive and had negative sputum-smear results at the end of the initial phase after completion of treatment, with no or only one negative sputum-smear result in the continuation phase and none at the end of treatment. Died was used for any death during treatment, irrespective of cause. Failed patients remained or became smear positive again at least 5 months after the start of treatment. Interrupted treatment (defaulted) was used for patients who did not collect drugs for 2 months or more at any time after registration. Transferred out was used for patients who were transferred to another reporting unit whose results were not known. In addition to these outcomes, documented treatment success was obtained by adding the percentage of cured cases to that of cases who completed treatment.
626
World Bank regions
Table 3: Case detection rates based on World Bank Development Report by World Bank region, 1995 To calculate the worldwide treatment-success rate, we added the number of cured and completed treatment cases in the WHO and non-WHO regions. We calculated the rate in terms of the number of sputum-smear-positive cases notified and the number of cases registered for treatment in 1994, worldwide. The number notified, which is not available for WHO and non-WHO areas separately, 14 is generally more than the number of cases registered.
Results By 1 July, 1997, WHO had received data from 180 countries, areas, and territories (83% of the 216 surveyed, 98% of the worldwide population). Of these, 84 (47%) areas had not yet accepted the WHO strategy, 75 (42%) had implemented the strategy (39 in >90% of the population), and 21 (12%) had a casenotification rate of less than ten per 100 000 population (table 1). 2% of the worldwide population lived in countries that did not report to WHO, 27% in countries where the WHO strategy was not implemented anywhere, 7% in countries that had a low incidence of TB, and 64% in countries that had adopted the WHO strategy. However, in these countries diagnostic and treatment services that follow the WHO strategy were available in only a few healthadministration units. Therefore, we estimated that the percentage of the worldwide population with access to these services was 23% (table 2). The 180 countries, areas, and territories reporting to WHO reported 3 297 688 cases of TB (59·1 per 100 000 population). Of these, 1 161 411 (35%) were sputum-smear positive. Of the total cases reported, 699 779 (21%) were from areas in which the WHO strategy was implemented and 2 597 909 (79%) were from other areas (table 2). 54% of all cases in areas where the WHO strategy was implemented were sputum-smear positive, compared with 30% in the other areas. Furthermore, 64% of new pulmonary cases in WHO areas were sputum-smear positive compared with 33% in other areas. Based on the World Bank’s World Development Report, estimated incidence rates adjusted for population growth since 1990 suggested that an estimated 3·32 million new smear-positive cases and 7.32 million cases of all TB occurred in 1995.11 Of these, 1·16 million and 3·30 million, respectively, were notified, which is a case-detection rate of 35% among new sputum-smear-positive cases and 45% among all cases (table 3). Based on reports to WHO collected in 1995, 977 679 new sputum-smear-positive cases were notified by 141 countries in 1994.14 Of these, 808 898 (83%) were registered for treatment according to the 1996
Vol 350 • August 30, 1997
THE LANCET
Strategy*
Number of cases registered
% cases not assessed
% cured
% completed treatment
% treatment interrupted
% failed
% died
% transferred out
Treatment success
CHI WHO Non-WHO
59 500 36 987
1 1
92 86
2 0
1 4
2 6
2 2
0 1
94 86
EME WHO Non-WHO
1924 2
26 0
28 0
32 100
5 0
2 0
4 0
2 0
60 100
FSE WHO Non-WHO
930 64 694
0 4
78 64
5 3
1 2
2 5
7 21
7 1
83 67
IND WHO Non-WHO
1026 226 543
0 100
82 ..
1
6 ..
2 ..
4 ..
5 ..
83 ..
LAC WHO Non-WHO
45 059 35 723
9 32
61 27
16 24
7 10
2 1
3 3
2 3
77 51
MEC WHO Non-WHO
18 091 35 386
1 21
74 34
8 21
7 8
1 3
2 6
7 7
82 55
OAI WHO Non-WHO
42 199 119 246
5 4
79 62
3 15
4 9
2 2
2 2
5 6
82 77
SSA WHO Non-WHO
78 652 42 936
18 10
47 27
11 41
11 12
1 2
6 5
6 3
58 68
Worldwide WHO Non-WHO
247 381 561 517
8 46
68 32
8 10
7 4
1 2
4 4
4 2
76 42
..
Region abbreviations as in table 1. *WHO=areas that have implemented WHO TB control strategy; non-WHO=areas that have not implemented WHO TB control strategy.
Table 4: Number of registered cases and treatment results for new smear-positive cases by World Bank region and treatment strategy, 1994
data-collection forms. In areas that have adopted the WHO strategy, 247 381 new sputum-smear-positive cases were registered for treatment (table 4), and the outcomes of 226 628 (92%) of them were assessed. The documented treatment-success rate among all registered sputum-smear-positive cases in the WHO areas was 76% (table 4). The highest treatment-success rate (94%) was reported from China. The outcome was uncertain in 19% of cases (not assessed, interrupted treatment, and transferred out). In areas where the WHO strategy was not implemented, 561 517 new sputum-smear-positive cases were registered for treatment. Of these, 304 562 (54%) were assessed for treatment results (table 4). The documented treatment-success rate among all registered cases was 42% (table 4). The outcome was uncertain in 52% of cases (not assessed, defaulted, and transferred out), which was due largely to the lack of assessment of treatment results in India. The weighted worldwide treatment-success average was 52%. This figure corresponds to 422 155 cases. However, this rate decreased to 43% when we used the number of cases notified for 1994 as the denominator (977 679, table 4).
Discussion The main purposes of this study were to assess the extent of implementation of the WHO strategy worldwide, the achievements of national TB programmes, and the progress towards the achievements of the two WHO targets set by the World Health Assembly in 1991.9 Of the 216 countries, areas, and territories surveyed, 83% replied to WHO. By the end of 1995, the WHO strategy had been accepted in 75 countries (35% of the 216 surveyed),
Vol 350 • August 30, 1997
but only 39 countries had implemented the strategy countrywide. The remaining countries had implemented the strategy in only part of their territory, or only as far as the first phase, or in pilot projects. Therefore, at the beginning of 1995, only 23% of the worldwide population was covered by control programmes that followed the WHO strategy. The information given on populations living in regions where the WHO strategy is implemented must, therefore, be treated with caution. However, of the high-incidence countries that have not accepted the WHO strategy, some, such as Oman, Myanmar, Kyrgyzstan, and Thailand, were in a preparatory phase in early 1996. Of the 3 297 688 cases notified for 1995, 21% were reported from areas in which the WHO strategy was implemented. This proportion should increase as more and more national TB programmes adopt WHO strategy. The limitations of our worldwide assessment must be acknowledged. First, interpretation of the performance indicators in areas that had not implemented the WHO strategy was difficult, since definitions were not standard. The reliability of these data is also variable. Furthermore, the success in WHO areas may also be influenced by factors other than the technical elements of the WHO strategy. For example, a country with a generally good health system may have been more likely to adopt the strategy than one with a poor system. We found a further limitation when we averaged performance indicators by region. A few countries with many TB cases may dominate regional averages, although the use of World Bank areas allowed at least a separate assessment of India and China. Despite these limitations, assessment of the national TB programmes’ performance is important. 627
THE LANCET
Bringing together the results from WHO and nonWHO areas gives an overview of the treatment-success rate worldwide. National TB programmes documented a treatment-success rate of only 43% among all notified cases. Many patients interrupt treatment (up to 12% in sub-Saharan Africa where the WHO strategy was not implemented). Some patients fail treatment and need to be re-treated at a later date. Some die of TB: at least 5–6% in sub-Saharan Africa, where the influence of HIV infection is greater than anywhere else, and as many as 21% in the formerly socialist economies of Europe, in which WHO strategy has not been implemented. These countries are mostly of the former Soviet Union, where national TB programmes are collapsing and drugs are in poor supply.5 Documented treatment-success rates help in the assessment of achievements of TB control programmes as recorded results. However, these results do not apply to cases that were not notified, not registered for treatment, not assessed, or recorded as treatment interrupted and transferred out. We therefore constructed two hypothetical models in an attempt to calculate the true worldwide cure rate. Given that TB spontaneously resolves in about a third of cases,15,16 the lower estimate of a favourable outcome is 37%. On the other hand, if we assume that in the best of circumstances treatment-success rates were the same for assessed and non-assessed cases, the true worldwide cure rate could be as high as 78%. In these aggregated results we found important differences in the treatment-success rates between WHO and non-WHO areas. First, in areas where the WHO strategy was implemented, 92% of the registered cases were assessed, compared with only 54% in the non-WHO areas. Therefore, the performance indicators of the non-WHO TB-control areas apply only to a small proportion of all cases in these areas. Second, the documented treatment-success rate among new sputum-smear-positive cases was 76% in those areas where the WHO strategy was implemented and only 42% in other areas, mostly because there are no outcome data from India. If we exclude India from the worldwide assessment, the treatment success in nonWHO areas was 70%. Conversely, the sum of unknown or unsuccessful outcomes was much higher in nonWHO areas (58% vs 24%). Although patients who die are less important for transmission of TB infection and perpetuation of the epidemic, patients who stop treatment, defaulters, and to a certain extent transferred-out cases constitute, together with cases registered for treatment and not assessed, an uncertainty index. One way of assessing the effectiveness of case-finding is based on calculation of the proportion of cases that were sputum-smear-positive. This proportion was expected to be between 50% and 66%, but was less than a third in developing countries in which the WHO strategy was not implemented. This small proportion shows a lack of emphasis on detection and giving priority to infectious TB cases or inappropriate diagnosis in the non-WHO areas, or both. Data from all 180 countries, areas, and territories that replied suggest that the percentage of new infectious cases notified in 1995 was only 35% of the estimated incidence and that it could be lower. The credibility of this indicator depends on the quality of 628
the information system. High case-detection rates are credible in countries that have adopted the WHO strategy and have sound methods of reporting and treating TB patients, such as Botswana (81%), Morocco (93%), Peru (94%), Tanzania (80%), and Vietnam (67%). Some countries that had not implemented the WHO strategy also seemed to have high case-detection rates of above 50%. However, we were suspicious about these rates because information gathering is generally poor in these countries. The rates suggest that too many cases are notified or that incidence estimates in the 1994 World Development Report11 are too low. Even with uncertainty about the estimate of 35%, detection of only about a third of new cases is unlikely to lead to TB elimination, since transmission of infection from undetected or untreated cases will be perpetuated. There is a great need to improve worldwide TB control. Many cases clearly remain undiagnosed and receive no treatment at all, many cases are diagnosed outside national TB programmes, and many receive inadequate treatment.17 Such patients commonly are persistently infectious, chronically ill, and more likely to die, and they carry drug-resistant strains.18 Implementation of a sound TB control strategy is clearly necessary in all countries to improve TB control worldwide. Initially proven to be effective in the national TB programmes assisted by the IUATLD,19,20 the preferred approach has been refined and promoted by WHO intensively in the past 6 years. Results have shown that the strategy is effective. For example, the treatment success documented in China21 and Tanzania20 and the increase in successes after years of decline in Malawi22 suggest that the strategy works well in different settings. More proof is provided by the national TB programmes in Morocco and Peru, which have both achieved consistently high cure rates for several years (data given to WHO from these programmes) and reductions in case notifications. Intensified technical and financial assistance to countries is, therefore, likely to result in increased case detection and treatment success, and, at the same time, an improved quality of information collected by the national TB programmes. Better information will, in turn, allow a better assessment of the achievements of national TB programmes, ultimately challenging countries to improve their control efforts. WHO Global Surveillance and Monitoring Project P Chaulet, M Grzemska, C Hanson, J Kumaresan, M Levy, F Luelmo, P P Nunn, S Spinaci, E Tayler, (Global Tuberculosis Programme, Geneva, Switzerland); E Nyarko, J-C Willame (WHO African Regional Office, Brazzaville, Congo); R R Cruz, D Weil (WHO American Regional Office, Washington DC, USA); Z Hallaj, A Seita (WHO Eastern Mediterranean Regional Office, Alexandria, Egypt); T-A Madaras (WHO European Regional Office, Copenhagen, Denmark); M V H Gunaratne (WHO South- East Asian Regional Office, Delhi, India); L Blanc, D I Ahn (WHO Western Pacific Regional Office, Manila, Philippines).
Contributors Mario Raviglione, Sergio Spinaci, and Arata Kochi were responsible for protocol design. Mario Raviglione, Sonja Schmidt, and Paul Nunn (GTB, Geneva) coordinated the study. Data were collected and verified by Sonja Schmidt, Pierre Chaulet, Malgorzata Grzemska, Christy Hanson, Jacob Kumaresan, Michael Levy, Fabio Luelmo, Sergio Spinaci, Elizabeth Tayler (GTB, Geneva); Eugene Nyarko, Jean-Claude Willame (WHO Arican Regional Office, Brazzaville, Congo); Rodolfo Rodriguez Cruz, Diana Weil (WHO American
Vol 350 • August 30, 1997
THE LANCET Regional Office, Washington DC, USA); Zoheir Hallaj, Akihiro Seita (WHO Eastern Mediterranean Regional Office, Alexandria, Egypt); Tünde-Agnes Madaras (WHO European Regional Office, Copenhagen, Denmark); Methsiri Gunaratne (WHO South-East Asian Regional Office, Delhi, India); Leopold Blanc, Dong Il Ahn (WHO Western Pacific Regional Office, Manila, Philippines). The data were analysed by Mario Raviglione and Christopher Dye. Mario Raviglione, Christopher Dye, and Sonja Schmidt wrote the paper.
Acknowledgments We thank all the National Tuberculosis Programme managers who provided their country data to WHO; WHO tuberculosis country advisors who collected and reviewed data from the national programmes; and H Rieder of the International Union Against Tuberculosis and Lung Disease for providing useful comments on the manuscript.
9
10
11 12
13
14
References 1
2
3 4
5
6
7
8
Raviglione MC, Snider DE Jr, Kochi A. Global epidemiology of tuberculosis: morbidity and mortality of a worldwide epidemic. JAMA 1995; 273: 220–26. Narain JP, Raviglione MC, Kochi A. HIV-associated tuberculosis in developing countries: epidemiology and strategies for prevention. Tuberc Lung Dis 1992; 73: 311–21. De Cock KM, Soro B, Coulibaly IM, Lucas SB. Tuberculosis and HIV infection in sub-Saharan Africa. JAMA 1992; 268: 1581–87. Yanai H, Uthaivoravit W, Panich V, et al. Rapid increase in HIV-related tuberculosis, Chiang Rai, Thailand, 1990–1994. AIDS 1996; 10: 527–31. Raviglione MC, Rieder HL, Styblo K, Khomenko AG, Esteves K, Kochi A. Tuberculosis trends in Eastern Europe and the former USSR. Tuberc Lung Dis 1994; 75: 400–16. Cantwell MF, Snider DE Jr, Cauthen GM, Onorato IM. Epidemiology of tuberculosis in the United States, 1985 through 1992. JAMA 1994; 272: 535–39. McKenna MT, McCray E, Onorato I. The epidemiology of tuberculosis among foreign-born persons in the United States, 1986 to 1993. N Engl J Med 1995; 332: 1071–76. Raviglione MC, Sudre P, Rieder HL, Spinaci S, Kochi A. Secular
Vol 350 • August 30, 1997
15
16 17 18 19 20
21
22
trends of tuberculosis in Western Europe. Bull World Health Organ 1993; 71: 297–306. World Health Organization. Forty-Fourth World Health Assembly, Geneva, 6-16 May 1991. Resolutions and decisions. Geneva, Switzerland: WHO 1991; WHA44/1991/REC/1. World Health Organization. WHO Tuberculosis Programme: framework for effective tuberculosis control. Geneva, Switzerland: WHO 1994; WHO/TB/94.179. The World Bank. World Development Report 1993: investing in health. New York: Oxford University Press, 1993; 1–225. Styblo K. The relationship between the risk of tuberculous infection and the risk of developing infectious tuberculosis. Bull Int Union Tuberc Lung Dis 1986; 60: 117–19. Murray CJL, Styblo K, Rouillon A. Tuberculosis in developing countries: burden, intervention and cost. Bull Int Union Tuberc Lung Dis 1990; 65: 6–24. World Health Organization. Global Tuberculosis Programme: global tuberculosis control. Geneva, Switzerland: WHO Report, 1997; WHO/TB/97.225. National Tuberculosis Institute, Bangalore. Tuberculosis in a rural population of south India: a five-year epidemiological study. Bull World Health Organ 1974; 51: 473–88. Springett VH. Ten-year results during the introduction of chemotherapy for tuberculosis. Tubercle 1971; 52: 73–87. Uplekar MW, Rangan S. Private doctors and tuberculosis control in India. Tuberc Lung Dis 1993; 74: 332–37. Jain NK. Drug resistance in India: a tragedy in the making. Ind J Tuberc 1992; 39: 145–48. Enarson D. Principles of IUATLD collaborative tuberculosis programmes. Bull Int Union Tuberc Lung Dis 1991; 66: 195–200. Styblo K. Overview and epidemiologic assessment of the current global tuberculosis situation with an emphasis on control in developing countries. Rev Infect Dis 1989; 11 (suppl 2): S339–46. China Tuberculosis Control Collaboration. Results of directly observed short-course chemotherapy in 112 842 Chinese patients with smear-positive tuberculosis. Lancet 1996; 347: 358–62. Harries AD, Nyong’Onya Mbewe L, Salaniponi FML, et al. Tuberculosis programme changes and treatment outcomes in patients with smear-positive pulmonary tuberculosis in Blantyre, Malawi. Lancet 1996, 347: 807–09.
629