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Tobacco Smoke, Indoor Air Pollution and Tuberculosis: a Systematic Review and Meta-Analysis

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Tobacco Smoke, Indoor Air Pollution and Tuberculosis: a Systematic Review and Meta-Analysis PLoS MEDICINE Tobacco Smoke, Indoor Air Pollution and Tuberculosis: A Systematic Review and Meta-Analysis Hsien-Ho Lin1, Majid Ezzati2, Megan Murray1,3,4* 1 Department of Epidemiology, Harvard School of Public Health, Boston, Massachusetts, United States of America, 2 Department of Population and International Health and Department of Environmental Health, Harvard School of Public Health, Boston, Massachusetts, United States of America, 3 Division of Social Medicine and Health Inequalities, Brigham and Women’s Hospital, Boston, Massachusetts, United States of America, 4 Infectious Disease Unit, Massachusetts General Hospital, Boston, Massachusetts, United States of America Funding: This review was supported by The International Union Against ABSTRACT Tuberculosis and Lung Disease through a grant from the World Bank. The funders had no role in Background study design, data collection and analysis, decision to publish, or Tobacco smoking, passive smoking, and indoor air pollution from biomass fuels have been preparation of the manuscript. implicated as risk factors for tuberculosis (TB) infection, disease, and death. Tobacco smoking Competing Interests: The authors and indoor air pollution are persistent or growing exposures in regions where TB poses a major have declared that no competing health risk. We undertook a systematic review and meta-analysis to quantitatively assess the interests exist. association between these exposures and the risk of infection, disease, and death from TB. Academic Editor: Thomas E. Novotny, Center for Tobacco Control Research and Education, United Methods and Findings States of America We conducted a systematic review and meta-analysis of observational studies reporting Citation: Lin HH, Ezzati M, Murray M effect estimates and 95% confidence intervals on how tobacco smoking, passive smoke (2007) Tobacco smoke, indoor air exposure, and indoor air pollution are associated with TB. We identified 33 papers on tobacco pollution and tuberculosis: A systematic review and meta-analysis. smoking and TB, five papers on passive smoking and TB, and five on indoor air pollution and PLoS Med 4(1): e20. doi:10.1371/ TB. We found substantial evidence that tobacco smoking is positively associated with TB, journal.pmed.0040020 regardless of the specific TB outcomes. Compared with people who do not smoke, smokers Received: July 27, 2006 have an increased risk of having a positive tuberculin skin test, of having active TB, and of dying Accepted: November 30, 2006 from TB. Although we also found evidence that passive smoking and indoor air pollution Published: January 16, 2007 increased the risk of TB disease, these associations are less strongly supported by the available Copyright: Ó 2007 Lin et al. This is evidence. an open-access article distributed under the terms of the Creative Commons Attribution License, which Conclusions permits unrestricted use, distribution, and reproduction in any There is consistent evidence that tobacco smoking is associated with an increased risk of TB. medium, provided the original author and source are credited. The finding that passive smoking and biomass fuel combustion also increase TB risk should be substantiated with larger studies in future. TB control programs might benefit from a focus on Abbreviations: AM, alveolar interventions aimed at reducing tobacco and indoor air pollution exposures, especially among macrophage; CI, confidence interval; IAP, indoor air pollution from those at high risk for exposure to TB. biomass fuels; OR, odds ratio; TB, tuberculosis; TST, tuberculin skin test The Editors’ Summary of this article follows the references. * To whom correspondence should be addressed. E-mail: mmurray@ hsph.harvard.edu PLoS Medicine | www.plosmedicine.org0173 January 2007 | Volume 4 | Issue 1 | e20 Tobacco and Biomass Smoke and TB Introduction Box 1. Search Strategy and Terms Used to Identify Studies on Smoking Tuberculosis (TB) causes an estimated 2 million deaths per and TB year, the majority of which occur in the developing world. MeSH term search Many studies conducted over the past 60 years have found an 1. ‘‘tuberculosis’’ association between tobacco smoking and TB, as manifested 2. ‘‘smoking’’ by a positive tuberculin skin test (TST) or as active disease 3. ‘‘air pollution, indoor’’ 4. ‘‘biomass’’ and its sequelae. A smaller number have found that indoor air 5. ‘‘fuel oils’’ pollution from biomass fuels (IAP) and passive smoking are 6. ‘‘(1) AND (2)’’ OR ‘‘(1) AND (3)’’ OR ‘‘(1) AND (4)’’ OR ‘‘(1) AND (5)’’ also risk factors for TB and its sequelae. Tobacco smoking has Direct keyword search: increased substantially in developing countries over the past three decades, with an estimated 930 million of the world’s 1.1 7. ‘‘tuberculosis’’ 8. ‘‘smoking’’ billion smokers currently living in the low-income and 9. ‘‘indoor air pollution’’ middle-income countries [1,2]. Approximately half of the 10. ‘‘cooking fuel’’ world’s population uses coal and biomass, in the form of 11. ‘‘biomass’’ 12. ‘‘(7) AND (8)’’ OR ‘‘(7) AND (9)’’ OR ‘‘(7) AND (10)’’ OR ‘‘(7) AND wood, animal dung, crop residues, and charcoal as cooking (11)’’ and heating fuels especially in Africa and Asia. Given the 13. (6) OR (12) persistent or growing exposure to both smoking and IAP in regions where TB poses a major health risk, it is essential to delineate the role of these environmental factors in the were available, we included only the one with the most etiology and epidemiology of TB. Previous reviews have detailed information for both outcome and exposure. addressed qualitatively the epidemiologic and biologic link between tobacco smoke and TB, but have not systematically Data Extraction and Quality Assessment reviewed the epidemiologic data on this association [3,4]. We For every eligible study, we collected detailed information therefore undertook to quantitatively assess the association on year and country of study, study design, study population, between smoking, passive smoking, and IAP, and the risk of sample size, choice of controls, definition and measurement infection, disease, and death from TB. We have considered of tobacco smoking or IAP, type of TB outcome, confounders smoking, passive smoking, and IAP together because these adjusted for, effect sizes and 95% confidence intervals (CIs), sources result in exposure to common set of respirable and dose-response relationships. Since TB disease and death pollutants, and because their effects are currently or are relatively rare events, even in high-incidence areas, we increasingly found in the developing countries. assumed that odds ratios (ORs), risk ratios, and rate ratios all provided an equivalent estimate of risk and therefore Methods reported them as ORs [5]. Although latent TB infection is not a rare event, each of the studies of latent TB infection Data Source estimated ORs and we therefore reported ORs for this We searched the PubMed via the NCBI Entrez system (1950 outcome as well. Data were extracted independently by two of to February 1, 2006) (http://www.ncbi.nlm.nih.gov/entrez/ the investigators (HL and MM), and differences were resolved query.fcgi) and the EMBASE via Ovid (1988 to 2003) (http:// by discussion with a third (ME). www.ovid.com) for studies of the association between smok- ing, passive smoking, and indoor air pollution and TB Data Synthesis infection, disease, and mortality. We also searched bibliog- We performed separate analyses for each exposure-out- raphies of identified reports for additional references. Our come association that had been studied. Within each search strategy is described in Box 1. subanalysis we further stratified on different study designs. When more than one study used a specific study design, we Study Selection assessed heterogeneity using the I2 statistic described by We limited our search to studies published in English, Higgins et al. [6]. Because of the significant heterogeneity and Russian, and Chinese. Studies were included if they involved different study designs within subgroups, we did not compute human participants with TB or at risk from TB. We included pooled effect measures [7]. Instead, we graphically presented studies if a quantitative effect estimate of the association each of the weighted point estimates and 95% CIs of effect between ever, former, or current tobacco smoking, passive estimates for individual studies within subanalyses. For the smoking, or IAP, and TST positivity, clinical TB disease, or TB subanalysis in which we found no significant heterogeneity, mortality was presented or could be estimated from the data effect estimates were given a weight equal to the inverse provided in the paper or through contact with the authors. variance of the study (fixed effects model). For those Studies were included in the review if they were full-length subanalyses in which we noted significant heterogeneity, we peer-reviewed reports of cohort studies, case-control studies, used a random effects model to assign the weight of each or cross-sectional studies, if they controlled for possible study according to the method described by DerSimonian confounding by age or age group, and if they screened for the and Laird [8]. In order to assess the effect of study quality on presence of TB among exposed and unexposed study the reported effect estimates, we conducted sensitivity participants in the same way. For analyses of the effect of analyses in which we compared pooled effect estimates for passive smoking on TB outcomes, we excluded studies if they subgroups stratified on quality-associated
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