Treatment outcomes of pulmonary tuberculosis in the past decade in the mainland of China: a meta-analysis

Abstract

Due to the implementation of directly observed treatment strategy (DOTS), China has made a significant achievement in tackling the tuberculosis (TB) epidemic in the 1990s. However, only half of regions in China met or exceeded the 85% rate of treatment success target. The aim of the present study is to summarize the treatment outcomes of smear-positive pulmonary TB in the mainland of China in the past decade using meta-analysis based on systematic review of published observational studies. A total of 50 eligible articles (58 studies) were identified and included in this study. The summarized treatment success rates were 93.9% (95% CI, 92.8%–94.7%) for new cases and 85.4% (95% CI, 83.0%–87.6%) for previously treated cases, and the summarized cured rate were 92.2% (95% CI, 90.9%–93.3%) and 81.2% (95% CI, 79.1%–83.1%), respectively. A remarkable increase of rates for treatment success and cure was observed in the 1990s. After 2000, the summarized treatment outcomes were tending towards stability. In addition, geographic areas, type of the data and administrative level of the hospital were also found to influence the estimates of the treatment outcomes. Results of the present study clearly show, in general, that the pulmonary TB treatment achieved significant success in the past decade in the mainland of China. However, it needs to be further strengthened in the central and west areas.

Keywords

tuberculosis / treatment / outcome / China / meta-analysis

Introduction

Tuberculosis (TB) is one of the most severe public health problems threatening human health. In 2010, there were about 8.8 million incident cases of TB around the world. [1]. Standardized short-course chemotherapy (SSCC), which is the cornerstone of modern TB control, can rapidly control illness and dramatically reduce the chance of death [2]. To improve the treatment outcomes and to prevent the emergence of drug resistance, directly observed treatment strategy (DOTS) based on SSCC was then suggested by the World Health Organization (WHO) and widespread in the world. Nowadays, DOTS is recognized as a highly efficient and cost-effective strategy for TB control. In 1991, assisted by a World Bank loan, DOTS was implemented in 12 provinces with a population of 573 million by the Government of China [3].

Therefore, China has made a significant achievement in tackling the TB epidemic in the 1990s. By 2000, free treatment was provided to 1.3 million smear-positive cases, and more than 90% of them were cured [3,4]. In 2000, China launched the project “TB Treatment and Control Planning of China (2001-2010)” to strengthen TB prevention and control in countywide. The WHO introduced surveillance of treatment outcomes since 1993 to evaluate the impact of TB control program. According to the recent report [1], only half of regions in China met or exceeded the global target for the treatment success rate as 85% [3]. To our knowledge, numbers of studies have been conducted to evaluate the treatment of TB in China. However, the results were heterogeneous and have not been systematically reviewed.

The objective of the present study is to summarize the best available evidence on the treatment outcomes of smear-positive pulmonary TB (PTB) in the mainland of China using meta-analysis based on systematic review of published articles. The relevant estimates were summarized and evaluated for new cases and previously treated cases, respectively.

Materials and methods

Literature search

All of the published articles addressing TB treatment in the mainland of China (1991-2011) were considered and searched in the databases including Chinese BioMedical Literature Database (1978-), PubMed (1946-), MEDLINE (1947-), EMBASE (1974-) and the Cochrane CENTRAL database (1972-). Different combination of keywords “tuberculosis,” “Koch’s Disease,” “Kochs Disease,” “Koch Disease,” “recovery rate,” “curative ratio,” “treatment outcome” and “mainland of China” was used for literature search.

Eligibility criteria

All the potentially relevant literatures were reviewed independently by two investigators. The criteria for inclusion in the meta-analyses include: (1) prospective or retrospective studies reporting the treatment outcomes of smear-positive PTB in the mainland of China between 1991 and 2001; (2) studies explicitly providing the information on diagnostic and cure criteria, chemotherapy regimen and treatment outcome; (3) articles in English or Chinese. If the study was reported in duplicate, the article published in English or published earlier in time was included.

Review articles, studies in languages other than English or Chinese, data from the regions of China other than the mainland, studies not implementing DOTS were excluded. To minimize the potential bias caused by too small sample size, articles with less than 100 patients were excluded.

Data extraction

The included studies were screened for the following information: first author and published year, study population and enrollment time, major characteristics of the study participants (age, sex, new cases or previously treated case, etc.), diagnostic and cure criteria. Data on chemotherapy regimen was extracted as well, the most widely used first-line anti-TB drugs include: soniazid (H), rifampicin (R), pyrazinamide (Z), ethambutol (E), streptomycin (S), rifapentine (L). All data were extracted independently by two investigators and discrepancies in data extraction were resolved by repeated manuscript review to reach consensus.

Definitions of treatment outcomes

The outcomes of TB treatment contain “successfully treated,” “cured,” “completed treatment,” “died,” “failed,” “defaulted,” and “not evaluated.” “Cured” means that an initially smear-positive patient was smear-negative in the last month of treatment. “Failed” means that an initially smear-positive patient remained smear-positive after 5 months of treatment. “Completed treatment” means that a patient completed treatment but did not meet the criteria for cure or failure. “Defaulted” means that the treatment was interrupted for 2 consecutive months or longer, also includes the cases that were lost to follow-up or transferred-out. “Not evaluated” means that the treatment outcome of a patient is not known. Additionally, “successfully treated” means that a patient was cured or completed treatment. Therefore, the cured rate can be calculated using the number of cured patients divided by the total number of evaluated patients. The treatment success rate is the value of the number of cured patients or patients who completed treatment divided by the total number of evaluated patients.

Statistical analysis

The summarized rates and corresponding 95% confidence intervals (CI) of TB treatment outcome were carried out using a random-effects model by Comprehensive Meta-Analysis (V2.0, Biostat, and Englewood, NJ, USA). Stratified analyses were subsequently performed with respect to the geographic areas, the end time of the enrollment period, and study base (the administrative levels of hospitals). Heterogeneity between included studies was assessed by calculating I² and Q estimates (P<0.05 was considered indicative of statistically significant publication bias) [4]. Publication bias was assessed with Begg rank correlation and Egger weighted regression methods [5]. Differences between the stratified analyses were assessed by chi-square tests.

Results

As shown in Fig. 1, a total of 1393 articles were identified by literature search using different combination of key terms from the databases. Of those, 420 were considered for full-text evaluation after exclusion based on title and abstract evaluation. Finally, 50 eligible articles (58 studies) were identified and included in the meta-analysis.

As shown in Table 1, 47 of the 50 included articles provided information of new cases with smear-positive PTB and 39 provided data of previously treated cases. All of the included studies launched the DOTS strategy. The studies were performed between 1992 and 2009, and the number of studied cases ranged from 115 to 19 501. In total 134 994 new cases and 23 412 previously treated cases from 17 provinces of the mainland of China were included in the analyses. More studies were conducted in East China [34] as compared to the Central [11] and the West [9] China. Six were prospective studies and used the WHO method of quarterly cohort reports, 23 were retrospective studies or surveys based on heath services data. Most studies confirmed TB by diagnosis standard recommended by the WHO. Twenty three studies reported detailed information of patients who had a conversion of sputum smear after 2 or 3 months of treatment.

The information on treatment outcomes and therapeutic regimen for the included studies were shown in Table 2. All of the included studies used short-course chemotherapy for treatment, 22 of them used SSCC and the remaining studies used therapeutic regimen similar to SSCC. Table 3 shows the meta-analysis of treatment outcomes for new cases and previously treated cases, 54 studies and 39 studies were included in the analysis respectively. The summarized success outcomes were 93.9% (95% CI, 92.8%–94.7%) for new cases and 85.4% (95% CI, 83.0%-87.6%) for previously treated cases. The summarized cured rates were 92.2% (95% CI, 90.9%-93.3%) and 81.2% (95%CI, 79.1%-83.1%), the estimate of the failed outcomes was 1.4% (95% CI, 1.1%-1.9%) and 4.9% (95% CI, 3.6%-6.5%), respectively. The summarized percentage of sputum smear conversion after 2 months of treatment was 88.5% in new cases and 78.0% in previously treated cases, which was 94.6% and 87.6% respectively after 3 months of treatment. The results were found to be heterogeneous between studies for newly diagnosed and previously treated cases (P for Q test<0.01). No evident publication bias was observed (P>0.05).

Table 4 shows the stratified analyses with respect to geographic areas, study base and administrative level of the hospital. Despite the heterogeneity between included studies, the summarized estimates of treatment success and cured rates were found to be significantly influenced by these variables (P<0.01). To investigate the time trend of treatment outcomes, the treatment success and cured rates were also summarized by year as shown in Fig. 2. A remarkable increase of treatment success and cure was found for both new cases and previously treated cases from 1992 to 2000. The summarized rates were then slightly decreased and tending toward stability after 2000. Please refer to Table 5 and Table 6 for more detailed information on the time trend analysis.

Discussion

To our knowledge, this is the first meta-analysis to systematically evaluate PTB treatment outcomes effect in the mainland of China. The included 58 eligible studies have nearly covered all of the provinces in the mainland of China. The summarized treatment success rates were 93.9% (95% CI, 92.8%-94.7%) for new cases and 85.4% (95% CI, 83.0%-87.6%) for previously treated cases, and the summarized cured rates were 92.2% (95% CI, 90.9%-93.3%) and 81.2% (95%CI, 79.1%-83.1%), respectively. A remarkable increased trend in treatment success and cured rate was observed between 1992 and 2000. After 2000, it was tending toward stability. In addition, geographic areas, type of the data and administrative level of the hospital were found to influence the estimates of the treatment outcomes as well.

The success and cured rate have long been used to evaluate the effect of TB control program [57]. In this study, the summarized treatment success rate (93.9%) exceeded the 85% threshold suggested by the WHO for new cases. The proposition of treatment success in previously treated patients (85.4%) was lower than in the new cases, which is consistent with the previous report [58]. As we previously studied, more than a quarter of the newly diagnosed TB cases (27.9%) and more than a half of previously treated cases (60.3%) were resistant to at least one drug[57]. Such a high prevalence of drug resistance might be a big challenge to achieve treatment success [57]. However, since the treatment regimen is a combination of drugs, resistant to one drug might not influence the clinical outcome based on the effect of other drugs in the regimen. Therefore, multidrug resistance (MDR) might be more relevant to influencing treatment effect. Consistently, as reported previously, the prevalence of multidrug resistance was found to be 5.3% and 27.4% in new cases and previously treated cases respectively [59].

The failed treatment in the new cases has been thought to be strongly correlated with occurrence of MDR [60]. In the present study, the summarized proportion of failed treatment in the mainland of China is 1.4% (95% CI, 1.1%-1.9%), and a decreasing trend was observed in the past decade from 4.4% in 1992 to 0.5% in 2007 (Table 5). The proportion of patients who showed a conversion of sputum smear after 2 or 3 mouths of treatment is known as a useful indicator of ideal TB treatment effect [61,62]. As shown in Table 5, consistently, the time trend of conversion of sputum smear is positively related to the trend of treatment success. However, Horne and colleagues performed a meta-analysis to estimate the accuracy of a positive sputum smear for predicting poor outcome in patients with pulmonary TB in 2010, and they found low sensitivity and moderate specificity for prediction of relapse or failure in all studies regardless of sputum examination or time of evaluation [63]. Therefore, the usefulness of a sputum specimen to predict poor outcome and decide on an extension of treatment is in debate and needs further studies to clarify. In addition, because most included articles did not provide the detail information on proportion of loss to follow-up and/or transfer-out, so their influence to the evaluation of treatment outcome was not assessed in the present study. High quality studies are needed to provide more valid estimates and standard definitions of treatment outcomes in the mainland of China.

Our stratified analysis suggested that the administrative levels of hospitals might influence treatment effect. In rural China, people usually seek health care at village health stations, private clinics or township health centers where the medical and public health resources are limited as compared to the cities. Previous studies have reported that in most instances the outcomes of population-based study and hospital-based study are different [3]. Our results suggest the treatment success was higher in hospital based studies than population based studies, which might be due to the higher level of treatment management and the better study quality in the hospital. In addition, in the stratified analyses on geographic areas, we found that most of the included studies came from the East China and achieved relatively improved higher success rates. It suggests that the higher social-economic status might contribute to the better treatment effect because the west and central areas are not as developed as the east areas in the mainland of China. Potential bias caused by the limited number of studies from areas with lower social-economic status could not be excluded.

In 1990, DOTS was introduced into China by the WHO and it has been popularized in countrywide by now [1]. Therefore, the summarized treatment success and cure rates among new cases and previously treated cases had been improved continuously up to 2000. In 2001, the China government launched the project “TB Treatment and Control Planning of China (2001-2010)” to strengthen TB prevention and control. The definition of TB diagnosis and treatment outcomes were further clarified and standardized. Probably for this reason, the summarized treatment success rate showed slightly decrease after 2000 but then tended toward stability as shown in Fig. 2. Probably because the DOTS has covered all provinces in China and the treatment outcomes are stable, the studies reporting treatment outcomes were relatively fewer since 2007. However, studies monitoring treatment effect are still needed especially for controlling drug resistance and exploring strategies to minimize the gap between geographic areas and between different levels of hospitals.

Limitations of this systematic review should be considered when interpreting the results. First, the potential impact of age, sex, ethnicity, economic level and life styles was not analyzed due to the limited information obtained from the original studies. Second, nearly three quarters of the included studies were conducted in the East China with better economic status. Therefore, stratified analyses with respect to geographic area were performed to minimize such potential selection bias. Third, although no evident publication bias was observed in the statistical analyses, potential bias still cannot be completely excluded as the present review was based only on published individual studies. Fourth, evident heterogeneity observed between the included studies should be kept in mind. As suggested by stratified analyses, it might be explained, at least in part, by various geographic areas, data sources and administrative levels of the hospital.

In conclusion, our results suggest that the treatment of PTB in the mainland of China achieved significant success in the past decade. But more constant attention is still needed and factors influencing the treatment outcomes should be noticed to improve the control and treatment of PTB. At the same time, high quality studies with large sample size to follow-up PTB treatment should be strengthened in the Central and the West China in the future.

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