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Previous Volume 344:1294-1303 April 26, 2001 Number 17 Next

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ABSTRACT

Background Data on global trends in resistance to antituberculosis drugs are lacking.

Methods We expanded the survey conducted by the World Health Organization and the International Union against Tuberculosis and Lung Disease to assess trends in resistance to antituberculosis drugs in countries on six continents. We obtained data using standard protocols from ongoing surveillance or from surveys of representative samples of all patients with tuberculosis. The standard sampling techniques distinguished between new and previously treated patients, and laboratory performance was checked by means of an international program of quality assurance.

Results Between 1996 and 1999, patients in 58 geographic sites were surveyed; 28 sites provided data for at least two years. For patients with newly diagnosed tuberculosis, the frequency of resistance to at least one antituberculosis drug ranged from 1.7 percent in Uruguay to 36.9 percent in Estonia (median, 10.7 percent). The prevalence increased in Estonia, from 28.2 percent in 1994 to 36.9 percent in 1998 (P=0.01), and in Denmark, from 9.9 percent in 1995 to 13.1 percent in 1998 (P=0.04). The median prevalence of multidrug resistance among new cases of tuberculosis was only 1.0 percent, but the prevalence was much higher in Estonia (14.1 percent), Henan Province in China (10.8 percent), Latvia (9.0 percent), the Russian oblasts of Ivanovo (9.0 percent) and Tomsk (6.5 percent), Iran (5.0 percent), and Zhejiang Province in China (4.5 percent). There were significant decreases in multidrug resistance in France and the United States. In Estonia, the prevalence in all cases increased from 11.7 percent in 1994 to 18.1 percent in 1998 (P<0.001).

Conclusions Multidrug-resistant tuberculosis continues to be a serious problem, particularly among some countries of eastern Europe. Our survey also identified areas with a high prevalence of multidrug-resistant tuberculosis in such countries as China and Iran.

Methods

Methods previously described are summarized here,^1,2 and changes and new developments are described in detail. The new surveillance projects or surveys were conducted between 1996 and 1999. Data on temporal changes are from geographic sites that provided data for at least two time points between 1994 and 1999. Standard methods of surveillance were used.⁴ Surveillance of drug resistance adhered to three principles: the samples of patients with tuberculosis in each country or region (e.g., state or province) were representative of that geographic site; recommended microbiologic methods were used by national laboratories that were monitored by an international system of proficiency testing; and in almost all countries, new cases were distinguished from previously treated cases.

New cases of tuberculosis were defined as incident cases in patients who, in response to direct questioning, denied having had previous antituberculosis treatment or having been treated for one month or more and, in countries where adequate documentation was available, for whom there was no evidence of a history of such treatment. Drug resistance among new cases was defined as the presence of resistant strains of Mycobacterium tuberculosis in new cases of tuberculosis. Drug resistance among previously treated cases was defined as the absence of a response in patients with tuberculosis who had already received antituberculosis therapy for one month or more (as documented in the tuberculosis registry or in medical records or by the account of the patient) and who had begun a retreatment regimen. Previously treated patients included patients who had a relapse after having completed successful treatment in the past, patients in whom treatment failed, patients who returned to a health care provider after having discontinued treatment, and patients with chronic tuberculosis who had positive sputum smears after the completion of two fully supervised courses of treatment. These definitions are presented elsewhere.⁵ Multidrug resistance was defined as resistance to at least isoniazid and rifampin.

Interlaboratory monitoring of the proficiency of testing for susceptibility to isoniazid, rifampin, streptomycin, and ethambutol has been conducted annually since 1994 within a network of 23 supranational reference laboratories. The methods used by the participating laboratories to test drug susceptibility include the absolute-concentration method, the resistance-ratio method, and the proportion method and its variants, including the BACTEC 460 radiometric culture method.^1,6,7 Descriptions of the methods and the early results of this program of proficiency testing have been published elsewhere.⁷

For each survey, the target population consisted of all registered patients in the survey area with sputum-smear–positive cases of tuberculosis. All newly registered patients with such cases were eligible for inclusion. In most countries, the survey area was the entire country. The calculation of the required sample size for surveys followed standard guidelines for the surveillance of drug resistance in tuberculosis.⁴ The required sample size was calculated on the basis of the expected prevalence of resistance to rifampin among new cases of tuberculosis, which, in turn, was estimated on the basis of data from previous studies or from the national tuberculosis programs. In countries that were conducting surveillance of drug resistance, all registered patients with tuberculosis were enrolled for testing. Sites that provided data for two or more time points conducted their surveillance or surveys in similar populations of patients with new cases of tuberculosis and sampled them over time. Similar protocols, including similar sampling techniques and similar populations sampled between surveys, were used to ensure the comparability of populations.

Testing of drug susceptibility was performed by the national reference laboratory, which was linked to one supranational reference laboratory for the validation of data. The results for a subsample of all strains tested were validated and confirmed by the supranational laboratory.

Statistical Analysis

The software packages Epi Info (version 6.04, Centers for Disease Control and Prevention, Atlanta) and SPSS for Windows (version 7.5.2, SPSS, Chicago) were used for the analyses. Median values were calculated for the prevalence of drug resistance among new cases, among previously treated cases, for individual drugs, and for pertinent combinations. Data on prevalence are from the latest year of surveillance or survey in each participating site. The analysis of trends focused on drug resistance found in new cases and previously treated cases. The standard chi-square test and Fisher's exact test were used for the comparison of two data points (proportions), and the chi-square test for trends was used for the comparison of three or more data points. The coverage of the global project was estimated with the use of data on tuberculosis notification that were reported to the World Health Organization,^8,9,10,11,12 and the population figures used for 1997 were those estimated by the United Nations Population Division.¹³ In the case of geographic sites for which data on the prevalence in two or more years were reported, only the latest one was used in the calculation of coverage. When surveys were conducted in administrative units of large countries (states, provinces, or oblasts), only the tuberculosis cases and populations of these administrative units were used in the calculation of coverage.

Results

Prevalence

Between 1996 and 1999, patients were surveyed in 58 geographic sites, in 54 of which there was drug-resistant tuberculosis among new cases and in 48 of which there was drug-resistant tuberculosis among previously treated cases. Australia, Belgium, Canada, and Israel reported drug resistance but did not distinguish between new and previously treated cases. The surveillance and surveys conducted in this phase of the global project tested a total of 61,415 patients with tuberculosis (median per geographic site, 661; range, 41 [Northern Ireland] to 12,675 [United States]). These geographic sites accounted for approximately 610,000 of the 3.3 million cases of tuberculosis reported to the World Health Organization in 1997 (18 percent) and 1.5 billion of the world's 5.8 billion inhabitants (26 percent). Proficiency testing in 1998 by the supranational reference laboratories of susceptibility to the four drugs for which the national laboratories tested showed an overall sensitivity of 98 percent and an overall specificity of 95 percent.

Among new cases of tuberculosis, the prevalence of resistance to at least one drug ranged from 1.7 percent in Uruguay to 36.9 percent in Estonia (median, 10.7 percent) (Table 1). The prevalence of multidrug-resistant tuberculosis ranged from 0 percent in eight sites to 14.1 percent in Estonia (median, 1.0 percent). The prevalence of multidrug-resistant tuberculosis was also high in Henan Province, China (10.8 percent), Latvia (9.0 percent), the Russian oblasts of Ivanovo (9.0 percent) and Tomsk (6.5 percent), Iran (5.0 percent), and Zhejiang Province, China (4.5 percent). The prevalence of resistance to a single drug ranged from 1.3 percent in the Czech Republic to 17.9 percent in Sierra Leone (data not shown). Resistance to all four drugs for which testing was conducted ranged from 0 percent in 24 sites to 8.5 percent in Estonia (data not shown).

View this table: [in this window] [in a new window]   Table 1. Prevalence of Drug Resistance among New Cases of Tuberculosis, According to Geographic Site, 1996–1999.

 
Among previously treated cases of tuberculosis, the prevalence of resistance to at least one drug ranged from 0 percent in Finland to 93.8 percent in Uruguay (median, 23.3 percent) (Table 2). The prevalence of multidrug-resistant tuberculosis among previously treated cases ranged from 0 percent in four sites to 48.2 percent in Iran (median, 9.3 percent). The median prevalence of resistance to a single drug was 11.3 percent, and the median prevalence of resistance to all four drugs was 1.8 percent (data not shown).

View this table: [in this window] [in a new window]   Table 2. Prevalence of Drug Resistance among Previously Treated Cases of Tuberculosis, According to Geographic Site, 1996–1999.

 
Temporal Changes

Data from two or more years were available from 28 of the 58 geographic sites. Of these sites, 24 provided data on new cases of tuberculosis, 20 provided data on previously treated cases, and 4 did not distinguish between the two types of cases. Table 3 shows trends among new and previously treated cases. Among countries with data available for three or more years, there was a statistically significant upward trend in the prevalence of resistance to any drug among new cases in Estonia, from 28.2 percent in 1994 to 36.9 percent in 1998 (P=0.01 for the trend across three data points), and in Denmark, from 9.9 percent in 1995 to 13.1 percent in 1998 (P=0.04 for the trend across four data points). Of the sites with data available for two years, Peru, New Zealand, and Germany had significant increases in the proportions of drug-resistant tuberculosis among new cases, whereas Barcelona (Spain) and Switzerland had significant decreases. Although no significant increases occurred in Latvia, Estonia, and the Russian oblast of Ivanovo, a high prevalence of multidrug-resistant tuberculosis (9.0 percent or higher in all sites) was still found among new cases in the most recent year of surveillance. France and the United States reported significant decreases.

View this table: [in this window] [in a new window]   Table 3. Trends in Drug Resistance among New and Previously Treated Cases of Tuberculosis.

 
Among previously treated cases, there was no evidence of an increase in the prevalence of resistance to at least one drug. There were, in fact, statistically significant decreases in Cuba, England and Wales, Peru, and the Republic of Korea. In Estonia, the prevalence of multidrug-resistant tuberculosis among previously treated cases increased from 19.2 percent in 1994 to 37.8 percent in 1998 (P=0.04). The prevalence of multidrug-resistant tuberculosis among all cases increased in Estonia from 11.1 percent in 1994 to 18.1 percent in 1998 (P<0.001, data not shown).

Discussion

We attempted to quantify global trends in resistance to antituberculosis drugs by means of standard epidemiologic and microbiologic methods. Our findings indicate that multidrug-resistant tuberculosis continues to be a serious problem in countries of eastern Europe — especially Estonia, Latvia, and Russia. Such findings suggest the continued creation and increased circulation of drug-resistant strains due to poor tuberculosis control, which poses a threat to other countries. Trends in the Russian oblast of Ivanovo confirm that the situation is critical, and the high prevalence of drug resistance found in the newly surveyed oblast of Tomsk, in Siberia, shows that the problem exists in other parts of the country and may be widespread throughout Russia. There are newly identified areas with a high prevalence of multidrug-resistant tuberculosis in heavily populated countries such as China and Iran, which indicates that the creation of highly resistant strains of M. tuberculosis is not limited to one part of the world.

Since multidrug-resistant tuberculosis is associated with higher rates of failure and death than is drug-susceptible tuberculosis¹⁴ and is more difficult and expensive to treat,¹⁵ great pressure is being put on the health care systems of these countries. They should immediately adopt or expand programs of tuberculosis control by making use of proven and cost-effective interventions such as the directly-observed-treatment, short-course strategy of the World Health Organization.¹⁶ The use of second-line drugs to cure multidrug-resistant tuberculosis and to reduce further transmission should be considered, but only as part of well-structured programs of tuberculosis control. Trials to assess the feasibility and cost effectiveness of the use of second-line drugs in settings with limited resources are currently being conducted as part of a new international initiative to manage multidrug-resistant tuberculosis.¹⁷

There is, however, reassuring news from this phase of the global project. There were no significant increases in the prevalence of multidrug-resistant tuberculosis among new cases in Botswana, Chile, Cuba, Czech Republic, Denmark, England and Wales, Finland, France, Germany, Nepal, the Netherlands, New Zealand, Northern Ireland, the Republic of Korea, Peru, Scotland, Sierra Leone, Spain (Barcelona), Sweden, Switzerland, and the United States. Many of these areas have been able to maintain high cure rates for tuberculosis.^{18,19,20,21,22}

In the Americas, all the countries that were surveyed for the first time in this phase of the project — including Canada, Chile, Colombia, Mexico, Nicaragua, Uruguay, and Venezuela — showed no signs of a serious problem. Most African countries surveyed — even those with a high incidence of human immunodeficiency virus–related tuberculosis — were not seriously affected by multidrug-resistant tuberculosis.^23,24 This low prevalence could be the result of various factors, including the recent introduction of rifampin in these countries, the use of rifampin-free treatment regimens in the continuation phase of therapy, and the growing use of direct observation of treatment.^25,26 Lack of access to treatment may also contribute to the low prevalence of multidrug-resistant tuberculosis. Several countries in Africa with a very high incidence of tuberculosis — including the Democratic Republic of Congo, Ethiopia, and Nigeria — have not yet been surveyed.²⁷ Thus, more data are needed to produce a balanced picture of drug resistance in Africa.

In western Europe, multidrug-resistant tuberculosis is not a major public health problem. Among new cases in Denmark and Germany, there were increases in the prevalence of resistance to at least one drug. An increase in the transmission of strains resistant to streptomycin and isoniazid has been reported among persons in Denmark who are 25 to 54 years of age.²⁸ A higher prevalence of drug resistance among immigrants has also increased the overall prevalence in these countries.^28,29 The increase in the prevalence of multidrug-resistant tuberculosis in Australia could be due to a large influx of immigrants from neighboring countries where the prevalence is high.³⁰

The two most populous countries, China and India, account for an estimated 3.1 million of the world's estimated 8.0 million incident cases of tuberculosis (39 percent).³¹ It has been estimated that 75 percent of the cases worldwide occur in five countries in Asia. The spread of multidrug-resistant tuberculosis in Asia could seriously hamper global efforts to control tuberculosis. The high prevalence of drug-resistant tuberculosis in this region emphasizes the need for a rapid expansion of the directly-observed-treatment, short-course strategy, which is being used for only 44 percent of the population of this region.²⁷ Management of multidrug resistance will require the wise use of second-line drugs.

Our data have some limitations. First, more information on the magnitude of drug-resistant tuberculosis is needed from countries with the highest rates of incidence of the disease.³¹ Of the 22 countries with the highest incidence rates (which account for an estimated 80 percent of all new cases annually), only 11 have relevant data available. It is therefore necessary to continue expanding surveillance efforts in these countries. Second, selection bias and misclassification of previously treated cases as new cases cannot be completely ruled out in some of the participating sites. Third, for some sites, apparent decreases in the prevalence of multidrug-resistant tuberculosis among previously treated cases could be related to sampling bias between surveys. For surveys of drug resistance, the required sample size is normally calculated only for new cases, because the proportion of patients with previously treated cases is usually a small fraction of the total number of patients registered for treatment in the geographic site.

A paradox was observed in countries that have had good tuberculosis-control programs for many years. In countries such as Uruguay and Cuba, almost all previously treated patients had drug-resistant tuberculosis, but there were only small numbers of such patients. Therefore, a very small number of drug-resistant, previously treated cases should not be regarded as a sign of the failure of a control program.³² Finally, several sites provided data for only two time points, which can only suggest a trend.

Despite such limitations, we attempt to present follow-up data on the magnitude of drug resistance around the world. The 58 new sites recruited to the study represent a 65 percent increase in the number of countries that have been surveyed.¹ The follow-up data confirm that the prevalence of multidrug-resistant tuberculosis is still alarmingly high in some countries in eastern Europe. Newly surveyed areas with a high prevalence have also been identified, suggesting that drug resistance is not limited to eastern Europe.

Measures to manage multidrug-resistant tuberculosis are urgently needed, but these will be successful only if the management of drug-susceptible tuberculosis, which accounts for the large majority of cases, is also successful.³³ Thus, if proper case management of drug-susceptible tuberculosis with first-line treatment regimens cannot be guaranteed,^34,35,36 the use of second-line drugs should be discouraged. The undisciplined use of both first- and second-line drugs will lead to the further spread of untreatable disease.

Supported by a grant from the United States Agency for International Development.

We are indebted to the national authorities in the participating countries and the institutions that hosted the national and international laboratories; to Dr. Eduardo Netto for his help with the analysis; and to Corazon Dolores and Zahra Ali-Piazza for secretarial assistance.

^* Other members of the group are listed in the Appendix.

Source Information

From the Communicable Diseases Cluster, World Health Organization, Geneva (M.A.E., L.S., C.D., R.W., M.C.R.); the International Union against Tuberculosis and Lung Disease, Paris (A.L., H.L.R.); the Laboratory Centre for Disease Control, Ottawa, Ont., Canada (A.L.); the Institut Pasteur, Algiers, Algeria (F.B.); the Korean Institute of Tuberculosis, Seoul, Republic of Korea (S.J.K.); the Instituto Panamericano de Protección de Alimentos y Zoonosis, Buenos Aires, Argentina (A.R.); the Swedish Institute for Infectious Disease Control, Stockholm (S.H.); and the Division of Tuberculosis Elimination, Centers for Disease Control and Prevention, Atlanta (N.B.).

Address reprint requests to Dr. Espinal at Communicable Diseases Control, Prevention, and Eradication, World Health Organization, 20 Ave. Appia, 1211 Geneva, Switzerland, or at espinalm{at}who.int.

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The following members of the World Health Organization–International Union against Tuberculosis and Lung Disease Working Group on Anti-Tuberculosis Drug Resistance Surveillance also participated in the study:Australia — D. Dawson, W. Chew, F. Haverkort, R. Lumb, A. Sievers; Belgium — M. Fauville Dufaux, M. Wanlin, M. Uydebrouck, F. Portaels; Botswana — M. Mwasekaga, T. Kenyon, E. Talbot; Canada — H. Njoo, P. Nault; Central African Republic (Bangui) — E. Kassa-Kelembho; Chile — P. Valenzuela, S. Piffardi; China (Beijing) — D. Hong-jin, W. Sumin, Z. Ben; China (Guangdong Province) — Z. Qiu, Q. Ming, L. Hong-qiao; China (Henan Province) — W. Guobin, P. Vili, Z. Guolong, Z. Li; China (Shandong Province) — Z. Sheng, G. Xiang, Z. Guo; China (Zhejiang Province) — L.. Qun, W. Xiaomeng, H. Haibo; Colombia — C. Leon Franco, M. Irinirida, C. Sierra, N. Naranjo, M. Garzon; Cuba — J. Valdivia, E. Montoro, A. Marrero Figueroa; Czech Republic — M. Havelková, O. Oádal; Denmark — V. Thomsen, S. Glisman; Estonia — A. Krüüner, K. Vink, M. Danilovich; Finland — M. Viljanen, M. Kokki, P. Ruutu; France — J. Grosset, V. Vincent, B. Carbonnelle, J. Robert; Germany — M. Forßohm, S. Ruesch-Gerdes, K. Feldmann, G. Bretzel; Guinea — B. Mamadou Dian, O. Younoussa Sow, D. Aliomou; Hong Kong Special Administrative Region of China — M. Kai, M. Cheuk; India (Tamil Nadu State) — C. Paramasivan, K. Bhaskaran, P. Venkataraman, T. Frieden; Iran — M.-R. Masjedi, A.-A. Velayati, M. Bahadori, S. Javad Tabatabaii; Israel — D. Chemtob, O. Dreazen; Italy — G. Migliori, G. Besozzi, A. Cassone, G. Orefici, L. Fattorini, E. Iona; Japan — C. Abe; Latvia — J. Leimans, V. Leimane, D. Mihalovska; Malaysia — I. Kuppusamy, D. Padmini, S. Ramayah; Mexico — A. Santaella-Solis, S. Balandrano Campos, A. Flisser Steinbruch, R. Granich; Morocco — S.-E. Ottmani, J. Mahjour, P. Chaulet; Mozambique — A. MacArthur, P. Perdigao, S. Gloyd; Nepal — D. Singh Bam, P. Malla, I. Smith; the Netherlands — B. van Klingeren, C. Lambregts-van Weezenbeek, N. Kalisvaart; New Caledonia — P. Duval; New Zealand — M. Brett, R. Vaughan, M. Carr, C. Tocker; Nicaragua — L. Chacon, J. Cruz; Norway — E. Heldal, N. Brattås, P. Sandven; Oman — A. Ahmed Ba Omar, S. Al-Awan, S. Al-Busaidy, J. George; Peru — L. Vàsquez Campos, J. Portocarrero Céliz, P. Suarez; Poland — Z. Zwolska, K. Roszkowski; Puerto Rico — O. Joglar; Republic of Korea — G.-H. Bai; Russia (Ivanovo Oblast) — A. Khomenko (deceased), M. Stoyunin, N. Katulina, I. Danilova, V. Golyshevskaya; Russia (Tomsk Oblast) — A. Sloutsky, A. Goldfarb, T. Healing, M. Kimerling; Sierra Leone — L. Westman, A. George; Singapore — J. Yap, I. Snodgrass; Slovakia — M. Svejnochová, E. Rajecová, L. Chovan; Slovenia — M. olnir-Dov, J. Sorli, D. Eren; South Africa — K. Weyer; Spain (Barcelona) — N. Martin-Casabona; Sweden — G. Källenius, V. Romanus; Switzerland — P. Helbling, G. Pfyffer, J.-P. Zellweger; Thailand — V. Payanandana, D. Rienthong, S. Rienthong, L. Ratanavichit, H. Sawert; Uganda — F. Adatu, M. Aziz, H.-U. Wendl-Richter, T. Aisu; United Kingdom — J. Watson, F. Drobniewski, J. Herbert, P. Christie, B. Watt, B. Smyth, M. Crowe; United States — E. McCray, I. Onorato, B. Metchock, K. Laserson, A. Pablos-Méndez, D. Cohn, E. Brenner; Uruguay — V. Cuesta Aramburu, C. Rivas; Venezuela — R. Armengol, A. Guilarte, L. Albina Vázquez de Salas; World Health Organization — P. Nunn, R. Rodriguez, A. Seita, L. Blanc, D. Il Ahn.

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