Contribution of Smoking to Tuberculosis Incidence and Mortality in High-Tuberculosis-Burden Countries

Contribution of Smoking to Tuberculosis Incidence and Mortality in High-Tuberculosis-Burden... Abstract Globally, 10 million incident cases of tuberculosis (TB) are reported annually, and 95% of TB cases and 80% of tobacco users reside in low- and middle-income countries. Smoking approximately doubles the risk of TB disease and TB mortality. We estimated the proportion of annual incident TB cases and TB mortality attributable to tobacco smoking in 32 high-TB-burden countries. We obtained country-specific estimates of TB incidence, TB mortality, and smoking prevalence from the World Health Organization Global TB Report (2017), tobacco surveillance reports (2015), and the Tobacco Atlas. Risk ratios for the effect of smoking on TB incidence and TB mortality were obtained from published meta-analyses. An estimated 17.6% (95% confidence interval (CI): 8.4, 21.4) of TB cases and 15.2% (95% CI: 1.8, 31.9) of TB mortality were attributable to smoking. Among high-TB-burden countries, Russia had the highest proportion of smoking-attributable TB disease (31.6%, 95% CI: 15.9, 37.6) and deaths (28.1%, 95% CI: 3.8, 51.4). Men had a greater proportion of TB cases attributable to smoking (30.3%, 95% CI: 14.7, 36.6) than did women (4.3, 95% CI: 1.7, 5.7). Our findings highlight the need for tobacco control in high-TB-burden countries to combat TB incidence and TB mortality. population attributable fraction, tobacco, tuberculosis Tuberculosis (TB) remains a leading cause of morbidity and mortality worldwide. In 2016, 10.4 million people developed active TB, and 1.3 million died from the disease, accounting for more deaths than any other infectious disease (1, 2). The vast majority of TB disease (87%) occurs in 30 high-burden countries, and 95% of TB cases and deaths occur in low- and middle-income countries (LMIC) (1, 2). The convergence of TB with noncommunicable diseases and tobacco use in LMIC threatens the End TB Strategy and Sustainable Development goals and highlights the need to modify established epidemiologic approaches to TB control (3, 4). Compared with nonsmokers, those who smoke tobacco have twice the risk of TB disease, and patients with TB who smoke have twice the risk of death during TB treatment (5–9). Currently, there are more than 1 billion tobacco users, nearly 80% of whom live in LMIC (10, 11). Separately, active TB and tobacco-related diseases constitute a substantial portion of morbidity and mortality in LMIC, where limited health resources are available to manage these costly diseases (12). However, an improved understanding of the contribution of smoking to TB disease and TB mortality is needed to better characterize the joint impact of smoking and TB on health burdens in LMIC. Although tobacco use is declining in many high-income countries, it is increasing in LMIC (13) where tobacco control policies are not well established (13–15). The extent to which changes in smoking prevalence may affect current efforts to reduce global TB incidence is largely unknown. According to previous reports, an estimated 20% of adult TB cases are attributable to smoking, compared with 16% for human immunodeficiency virus and 15% for diabetes (16, 17). However, previous studies have not estimated the proportion of country-specific TB deaths attributable to smoking in high-TB-burden countries. Furthermore, previous estimates of the proportion of TB cases attributable to smoking were not age- and sex-adjusted and did not include sensitivity analyses to assess bias from smoking-prevalence measurement error. In this study, we provide reliable estimates of the proportion of latent TB infection (LTBI) and TB disease incidence due to tobacco smoking in 32 countries with a high burden of TB. We have also estimated the proportion of TB deaths due to tobacco use. METHODS Data and study population Data from adult male and female individuals aged 15 years or older who lived in 32 high-TB-burden countries were included in the analyses. Thirty high-TB-burden countries were defined by the 2016 World Health Organization (WHO) Global TB Report as the top 20 countries with the highest absolute number of TB cases and the top 10 countries with the highest incidence rates of TB, with at least 10,000 new cases per year (1, 18). We added Uganda and Afghanistan, which were not among the 2016 WHO high-TB-burden countries but were included in 2015 (2, 19). We used 6 population-based cross-sectional data sources for our analyses (Table 1). We obtained TB case notification and TB mortality data from the 2017 WHO Global TB Report (1). Tobacco use data was acquired from the: 1) Global Adult Tobacco Survey (20), 2) WHO Global Report on Trends in Prevalence of Tobacco Smoking 2015 (21), 3) Tobacco Free Initiative country profiles (22), and 4) Tobacco Atlas (23). We obtained population size data from the US Census Bureau (24). Table 1. Epidemiologic Data Sources for Population Attributable Risk Calculations for the Contribution of Smoking to Tuberculosis Incidence and Mortality in High-Tuberculosis-Burden Countries, 2009–2016 Dataa Data Sourcesb Countries Variables Measurement Smoking prevalence Global Adult Tobacco Survey Bangladesh, Brazil, China, India, Indonesia, Nigeria, Pakistan, Philippines, Russia, Thailand, Vietnam Current tobacco smoking Self-reported WHO Global Report on Trends in Prevalence of Tobacco Smoking 2015 Cambodia, Congo, Ethiopia, Kenya, Lesotho, Liberia, Mozambique, Myanmar, Namibia, Sierra Leone, South Africa, Tanzania, Uganda, Zambia, Zimbabwe Current tobacco smoking Self-reported WHO Tobacco Free Initiative North Korea, Papua New Guinea Current tobacco smoking Self-reported Tobacco Atlas Afghanistan, Angola, CAR, DRC Daily tobacco smoking Self-reported TB incidence and TB mortality WHO 2017 TB Report N/A Population United States Census Bureau N/A Dataa Data Sourcesb Countries Variables Measurement Smoking prevalence Global Adult Tobacco Survey Bangladesh, Brazil, China, India, Indonesia, Nigeria, Pakistan, Philippines, Russia, Thailand, Vietnam Current tobacco smoking Self-reported WHO Global Report on Trends in Prevalence of Tobacco Smoking 2015 Cambodia, Congo, Ethiopia, Kenya, Lesotho, Liberia, Mozambique, Myanmar, Namibia, Sierra Leone, South Africa, Tanzania, Uganda, Zambia, Zimbabwe Current tobacco smoking Self-reported WHO Tobacco Free Initiative North Korea, Papua New Guinea Current tobacco smoking Self-reported Tobacco Atlas Afghanistan, Angola, CAR, DRC Daily tobacco smoking Self-reported TB incidence and TB mortality WHO 2017 TB Report N/A Population United States Census Bureau N/A Abbreviations: CAR, Central African Republic; DRC, Democratic Republic of Congo ; N/A, not applicable; TB, tuberculosis; WHO, World Health Organization. a We obtained TB case notification and TB mortality data from the 2017 WHO Global TB Report (1). Tobacco use data was acquired from: 1) Global Adult Tobacco Survey (20), 2) WHO Global Report on Trends in Prevalence of Tobacco Smoking 2015 (21), 3) Tobacco Free Initiative country profiles (22), and 4) the Tobacco Atlas (23). We obtained age- and sex-specific population data from the US Census Bureau (24). b Data sources were chosen in order of priority from the first row to the fourth. Table 1. Epidemiologic Data Sources for Population Attributable Risk Calculations for the Contribution of Smoking to Tuberculosis Incidence and Mortality in High-Tuberculosis-Burden Countries, 2009–2016 Dataa Data Sourcesb Countries Variables Measurement Smoking prevalence Global Adult Tobacco Survey Bangladesh, Brazil, China, India, Indonesia, Nigeria, Pakistan, Philippines, Russia, Thailand, Vietnam Current tobacco smoking Self-reported WHO Global Report on Trends in Prevalence of Tobacco Smoking 2015 Cambodia, Congo, Ethiopia, Kenya, Lesotho, Liberia, Mozambique, Myanmar, Namibia, Sierra Leone, South Africa, Tanzania, Uganda, Zambia, Zimbabwe Current tobacco smoking Self-reported WHO Tobacco Free Initiative North Korea, Papua New Guinea Current tobacco smoking Self-reported Tobacco Atlas Afghanistan, Angola, CAR, DRC Daily tobacco smoking Self-reported TB incidence and TB mortality WHO 2017 TB Report N/A Population United States Census Bureau N/A Dataa Data Sourcesb Countries Variables Measurement Smoking prevalence Global Adult Tobacco Survey Bangladesh, Brazil, China, India, Indonesia, Nigeria, Pakistan, Philippines, Russia, Thailand, Vietnam Current tobacco smoking Self-reported WHO Global Report on Trends in Prevalence of Tobacco Smoking 2015 Cambodia, Congo, Ethiopia, Kenya, Lesotho, Liberia, Mozambique, Myanmar, Namibia, Sierra Leone, South Africa, Tanzania, Uganda, Zambia, Zimbabwe Current tobacco smoking Self-reported WHO Tobacco Free Initiative North Korea, Papua New Guinea Current tobacco smoking Self-reported Tobacco Atlas Afghanistan, Angola, CAR, DRC Daily tobacco smoking Self-reported TB incidence and TB mortality WHO 2017 TB Report N/A Population United States Census Bureau N/A Abbreviations: CAR, Central African Republic; DRC, Democratic Republic of Congo ; N/A, not applicable; TB, tuberculosis; WHO, World Health Organization. a We obtained TB case notification and TB mortality data from the 2017 WHO Global TB Report (1). Tobacco use data was acquired from: 1) Global Adult Tobacco Survey (20), 2) WHO Global Report on Trends in Prevalence of Tobacco Smoking 2015 (21), 3) Tobacco Free Initiative country profiles (22), and 4) the Tobacco Atlas (23). We obtained age- and sex-specific population data from the US Census Bureau (24). b Data sources were chosen in order of priority from the first row to the fourth. The WHO Global TB Report has provided epidemiologic TB surveillance at global and country levels annually since 1997 (2). The Global Adult Tobacco Survey is a household survey, developed in 2007 by the Global Tobacco Surveillance System, which collects nationally representative tobacco-use data among persons aged 15 years or older. The Global Adult Tobacco Survey includes 25 LMIC where tobacco burdens are high (22). The WHO Global Report on Trends in Prevalence of Tobacco Smoking 2015 includes estimated age-specific current tobacco smoking prevalence based on Bayesian hierarchical meta-regression modeling and projected tobacco smoking prevalence trends in WHO regions (21). The Tobacco Free Initiative provides country-specific tobacco surveillance data (22). Tuberculosis incidence and mortality To estimate country-specific TB incidence rates, we obtained TB notification data from the 2017 WHO Global TB Report for the 32 highest TB-burden countries (1). In the absence of directly measured, country-level TB incidence rates, TB case notification rates provide proxy estimates for TB incidence that include notified and undiagnosed TB cases (19). A TB notification indicates that TB has been diagnosed in a patient and reported within the national surveillance system to WHO (25). The TB notification rate comprises the number of new and relapsed TB cases notified in a given year per 100,000 population (25). In 2017, 201 countries reported TB incidence data to WHO (1). We used TB notification rates for our estimates of TB incidence, because it includes sex- and age-specific data. In 2016, notifications of newly diagnosed TB cases represented 61% of estimated incident cases worldwide (1). To determine country-specific rates of TB mortality, we used the reported number of TB deaths where treatment outcome was indicated as TB deaths. A TB death was defined as all-cause mortality during TB treatment (19). We extracted 2015 TB mortality data from the 2017 WHO Global TB Report for all countries except for Angola, for which only 2014 data was available (1). Relative risk for TB disease and TB mortality associated with smoking We obtained relative risk estimates for the associations between smoking and LTBI, between smoking and TB incidence, and between smoking and TB mortality from studies reported by Bates et al. (6), Slama et al. (5), and Lin et al. (26), all in 2007. The relative risk of TB disease in smokers versus nonsmokers was reported to be 2.3 (95% confidence interval (CI): 2.0, 2.8) (6), 2.3 (95% CI: 1.8, 3.0) (5), and 2.0 (95% CI: 1.6, 2.6) (26). The reported relative risk for TB mortality, comparing smokers with nonsmokers, was reported as 2.1 (95% CI: 1.4, 3.4) (6), 2.2 (95% CI: 1.3, 3.7) (5), and 2.0 (95% CI: 1.1, 3.5) (26). For LTBI, we used a relative risk of 1.7 (95% CI: 1.5, 2.0) from Bates et al. (6). We used a relative risk of 2.3 (95% CI: 1.5, 2.8) for smoking-TB disease as reported in 2 systematic reviews (5, 6). For TB mortality, we used a relative risk of 2.0 (95% CI: 1.1, 3.7), comparing smokers with nonsmokers (26). Smoking prevalence Smoking prevalence data were obtained from 4 previously described sources for 32 countries (Table 1). Age- and sex-specific smoking prevalence data were extracted from the Global Adult Tobacco Survey for 11 countries (age-bands (years) reported as 15–24, 25–44, 45–64, ≥65) (22), which was our primary data source, and from the WHO Global Report on Trends in Prevalence of Tobacco Smoking 2015 for 15 countries (age-band (years) reported as 15–24, 25–39, 40–54, 55–69, and ≥70) (21). When country data were unavailable in the primary source, we used the next available data source (Table 1). For countries without age-stratified data, we used Tobacco Free Initiative country profiles and the Tobacco Atlas to estimate smoking prevalence (22, 23). The smoking prevalence data used for this study was based on the definition of current tobacco use, except for Afghanistan, Angola, and the Central African Republic. For Afghanistan, Angola, and the Central African Republic, we used daily tobacco use. Current tobacco use included daily smoking and occasional smoking of any type of smoked tobacco (27, 28). Smoked tobacco included manufactured cigarettes, bidi, hookah (water pipes), hand-rolled cigarettes, pipes of tobacco, cigars, cheroots, cigarillos, dhaba (bamboo water pipes), and any other tobacco products (27). Population data The 2016 age- and sex-specific population data for the 32 highest TB-burden countries were extracted from the US Census Bureau (24). The US Census Bureau estimates the population size of countries by collecting demographic data from censuses, surveys, vital registration, and administrative records (24). Statistical calculations We estimated the proportions of LTBI, TB disease, and TB death due to smoking using standard population attributable proportion (PAP) formulas (29). We first calculated unadjusted estimates of PAP for LTBI, TB disease incidence, and TB mortality for the 32 countries (29). PAP calculations were made using age- and sex-specific smoking prevalence data. For each PAP calculation (LTBI, active TB incidence, and TB mortality) we used estimated country-specific smoking prevalence and respective relative risks comparing smokers with nonsmokers. We used 95% confidence intervals of the relative risks from published estimates (5, 6, 26) to calculate the upper and lower PAP estimates for each country. We estimated excess numbers of active TB cases attributable to smoking for each country in each age and sex stratum by multiplying age- and sex-specific PAPs by the corresponding country-specific reported TB cases from WHO. Numbers of TB deaths attributable to smoking were estimated by multiplying the PAP for each country by the number of reported TB deaths from corresponding countries. Formulas for PAP calculations were: LatentTBInfection=Prevalenceofsmoking(RR−1)/(1+Prevalenceofsmoking(RR−1))WhereRR=RelativeriskofLTBI(1.7,95%CI:1.5,2.0) TBIncidence=Prevalenceofsmoking(RR−1)/(1+Prevalenceofsmoking(RR−1))WhereRR=RelativeriskofTBdisease(2.3,95%CI:1.5,2.8) TBMortality=Prevalenceofsmoking(RR−1)/(1+Prevalenceofsmoking(RR−1))WhereRR=RelativeriskofTBmortality(2.0,95%CI:1.1,3.7) In secondary descriptive ecological analyses, we compared the 5-year change in smoking prevalence with the 5-year change in estimated TB incidence for the 26 countries where smoking prevalence data were available in the same data sets described above (21). We plotted the country-level changes in smoking prevalence and change in TB incidence rate for 2010 and 2015 using a scatter plot. To estimate the relationship between 5-year change in TB incidence and smoking prevalence from 2010 to 2015, we calculated the Pearson correlation coefficient and P value. Sensitivity analysis We used Monte Carlo simulation to measure the amount of systematic error due to uncertainty in the smoking prevalence and relative risk estimates (30). We simulated smoking prevalence for each country using a normal distribution with mean equal to the reported point estimates for each country according to the Global Adult Tobacco Survey and the WHO Global Report on Trends in Prevalence of Tobacco Smoking 2015 and standard deviation derived from the 95% confidence intervals. We reproduced the natural logarithms of the relative risks for TB disease and TB mortality using the normal distribution with corresponding mean of the relative risk and standard deviation derived from the 95% confidence interval around the relative risk (for TB disease, relative risk = 2.3, 95% confidence interval (CI): 1.5, 2.8; for TB mortality, relative risk = 2.0, 95% CI: 1.1, 3.7). The relationships between smoking prevalence and the relative risks were assumed to be independent. The estimated PAPs for TB disease and TB mortality were based on 1,000 Monte Carlo simulations. RESULTS In 2016, an estimated 3.4 billion people over the age of 15 years lived in 32 high-TB-burden countries; in those countries, the estimated number of TB cases and TB deaths that year were 8.3 million and 1.1 million, respectively,. The crude smoking prevalence in the 32 countries was 21.5% (95% CI: 20.2, 23.0), representing 722 million smokers (Web Figure 1A and 1B, available at https://academic.oup.com/aje). Smoking prevalence was higher among men (38.8%) than among women (3.9%). In adults aged 15 years or older, LTBI attributable to smoking was 13.2% (95% CI: 8.8, 17.7). The proportion of LTBI attributable to smoking ranged from 2.8% (95% CI: 1.8, 3.9) in Nigeria to 22.2% (95% CI: 15.2, 28.9) in Russia (Web Table 1). The crude proportion of TB disease incidence attributable to tobacco smoking was 19.6% (95% CI: 8.7, 24.5), and the age-adjusted PAP was 17.6% (95% CI: 8.4, 21.4), accounting for an estimated 1.3 million excess cases each year (Table 2). The country-specific proportion of TB disease attributable to tobacco smoking ranged from 4.7% (95% CI: 1.9, 6.3) in Nigeria to 31.6% (95% CI: 15.9, 37.6) in Russia (Table 2, Web Figure 1C). Smoking-attributable TB disease was higher among men (30.3%) than among women (4.3%) (Table 3). Among men, the proportion of TB disease attributable to smoking ranged from 8.7% in Nigeria to 46.6% in Indonesia. Among women, the proportion ranged from 0.0% in North Korea to 22.0% in Russia (Table 3). Table 2. Estimated Proportion of Tuberculosis Disease Attributable to Tobacco Smoking Among Adults in 32 High-Tuberculosis-Burden Countries, 2009–2016 Country Smoking Prevalencea Crudeb Age-Adjustedc No. of Excess TB Casesd PAP, % 95% CI PAP, % 95% CI Afghanistan 13.0e 14.4 6.1, 18.5 Angola 9.2e 10.7 4.4, 13.9 Bangladesh 23.0 23.0 10.3, 28.7 18.6 9.2, 22.3 59,130 Brazil 17.2 18.3 7.9, 23.1 18.1 7.9, 22.8 14,037 Cambodia 21.2 21.6 9.6, 27.1 18.7 9.0, 22.7 8,422 CAR 8.6e 10.0 4.1, 13.0 China 28.1 26.8 12.3, 33.0 22.4 11.4, 26.6 176,649 Congo 13.9 15.3 6.5, 19.6 13.4 6.1, 16.7 3,195 DRC 6.4 7.7 3.1, 10.1 Ethiopia 4.3 5.3 2.1, 7.0 4.8 2.0, 6.3 7,932 India 14.0 15.4 6.5, 19.7 14.3 6.5, 17.8 363,861 Indonesia 34.8 31.2 14.8, 37.9 24.9 13.2, 29.1 238,368 Kenya 13.5 14.9 6.3, 19.1 13.3 6.0, 16.6 15,758 Lesotho 22.6 22.7 10.2, 28.3 18.7 9.3, 22.3 2,554 Liberia 12.1 13.6 5.7, 17.5 12.6 5.5, 15.8 1,681 Mozambique 18.9 19.7 8.6, 24.9 16.6 7.6, 20.6 24,605 Myanmar 20.0 20.6 9.1, 26.0 20.8 9.7, 25.5 35,727 Namibia 21.6 21.9 9.8, 27.4 20.3 9.3, 25.2 2,622 Nigeria 3.9 4.8 1.9, 6.4 4.7 1.9, 6.3 34,819 North Korea 20.1 20.7 9.1, 26.0 Pakistan 12.4 13.9 5.8, 17.8 12.1 5.5, 15.0 55,900 PNG 26.3 25.5 11.6, 31.5 Philippines 28.3 26.9 12.4, 33.1 24.1 11.7, 29.1 120,731 Russia 39.1 33.7 16.4, 40.6 31.6 15.9, 37.6 26,678 Sierra Leone 31.9 29.3 13.8, 35.8 26.1 12.7, 31.7 5,367 South Africa 19.4 20.1 8.84, 25.4 19.5 8.9, 24.2 72,580 Tanzania 16.3 17.5 7.5, 22.2 10.9 4.8, 13.6 17,471 Thailand 24.0 23.8 10.7, 29.6 23.9 11.5, 29.7 26,345 Uganda 10.1 11.6 4.8, 15.0 10.2 4.4, 13.0 8,078 Vietnam 23.8 23.6 10.6, 29.4 19.7 9.9, 23.5 21,678 Zambia 14.6 16.0 6.8, 20.4 14.0 6.3, 17.5 9,563 Zimbabwe 14.6 16.0 6.8, 20.4 13.9 6.4, 17.2 4,486 Weighted average 21.5 19.6 8.7, 24.5 17.6 8.4, 21.4 1,358,237 Country Smoking Prevalencea Crudeb Age-Adjustedc No. of Excess TB Casesd PAP, % 95% CI PAP, % 95% CI Afghanistan 13.0e 14.4 6.1, 18.5 Angola 9.2e 10.7 4.4, 13.9 Bangladesh 23.0 23.0 10.3, 28.7 18.6 9.2, 22.3 59,130 Brazil 17.2 18.3 7.9, 23.1 18.1 7.9, 22.8 14,037 Cambodia 21.2 21.6 9.6, 27.1 18.7 9.0, 22.7 8,422 CAR 8.6e 10.0 4.1, 13.0 China 28.1 26.8 12.3, 33.0 22.4 11.4, 26.6 176,649 Congo 13.9 15.3 6.5, 19.6 13.4 6.1, 16.7 3,195 DRC 6.4 7.7 3.1, 10.1 Ethiopia 4.3 5.3 2.1, 7.0 4.8 2.0, 6.3 7,932 India 14.0 15.4 6.5, 19.7 14.3 6.5, 17.8 363,861 Indonesia 34.8 31.2 14.8, 37.9 24.9 13.2, 29.1 238,368 Kenya 13.5 14.9 6.3, 19.1 13.3 6.0, 16.6 15,758 Lesotho 22.6 22.7 10.2, 28.3 18.7 9.3, 22.3 2,554 Liberia 12.1 13.6 5.7, 17.5 12.6 5.5, 15.8 1,681 Mozambique 18.9 19.7 8.6, 24.9 16.6 7.6, 20.6 24,605 Myanmar 20.0 20.6 9.1, 26.0 20.8 9.7, 25.5 35,727 Namibia 21.6 21.9 9.8, 27.4 20.3 9.3, 25.2 2,622 Nigeria 3.9 4.8 1.9, 6.4 4.7 1.9, 6.3 34,819 North Korea 20.1 20.7 9.1, 26.0 Pakistan 12.4 13.9 5.8, 17.8 12.1 5.5, 15.0 55,900 PNG 26.3 25.5 11.6, 31.5 Philippines 28.3 26.9 12.4, 33.1 24.1 11.7, 29.1 120,731 Russia 39.1 33.7 16.4, 40.6 31.6 15.9, 37.6 26,678 Sierra Leone 31.9 29.3 13.8, 35.8 26.1 12.7, 31.7 5,367 South Africa 19.4 20.1 8.84, 25.4 19.5 8.9, 24.2 72,580 Tanzania 16.3 17.5 7.5, 22.2 10.9 4.8, 13.6 17,471 Thailand 24.0 23.8 10.7, 29.6 23.9 11.5, 29.7 26,345 Uganda 10.1 11.6 4.8, 15.0 10.2 4.4, 13.0 8,078 Vietnam 23.8 23.6 10.6, 29.4 19.7 9.9, 23.5 21,678 Zambia 14.6 16.0 6.8, 20.4 14.0 6.3, 17.5 9,563 Zimbabwe 14.6 16.0 6.8, 20.4 13.9 6.4, 17.2 4,486 Weighted average 21.5 19.6 8.7, 24.5 17.6 8.4, 21.4 1,358,237 Abbreviations: CAR, Central African Republic; CI, confidence interval; DRC, Democratic Republic of Congo; PAP, population attributable proportion; PNG, Papua New Guinea; TB, tuberculosis. a Current tobacco smoking prevalence. b TB disease incidence based on relative risk of 2.3 (95% CI: 1.5, 2.8) (crude). c TB disease incidence based on relative risk of 2.3 2.3 (95% CI: 1.5, 2.8) (age-adjusted); blank if no age-specific data. d Excess cases based on age-adjusted PAP except for countries with no age-specific data. e Daily smoking prevalence (percentage of population). Table 2. Estimated Proportion of Tuberculosis Disease Attributable to Tobacco Smoking Among Adults in 32 High-Tuberculosis-Burden Countries, 2009–2016 Country Smoking Prevalencea Crudeb Age-Adjustedc No. of Excess TB Casesd PAP, % 95% CI PAP, % 95% CI Afghanistan 13.0e 14.4 6.1, 18.5 Angola 9.2e 10.7 4.4, 13.9 Bangladesh 23.0 23.0 10.3, 28.7 18.6 9.2, 22.3 59,130 Brazil 17.2 18.3 7.9, 23.1 18.1 7.9, 22.8 14,037 Cambodia 21.2 21.6 9.6, 27.1 18.7 9.0, 22.7 8,422 CAR 8.6e 10.0 4.1, 13.0 China 28.1 26.8 12.3, 33.0 22.4 11.4, 26.6 176,649 Congo 13.9 15.3 6.5, 19.6 13.4 6.1, 16.7 3,195 DRC 6.4 7.7 3.1, 10.1 Ethiopia 4.3 5.3 2.1, 7.0 4.8 2.0, 6.3 7,932 India 14.0 15.4 6.5, 19.7 14.3 6.5, 17.8 363,861 Indonesia 34.8 31.2 14.8, 37.9 24.9 13.2, 29.1 238,368 Kenya 13.5 14.9 6.3, 19.1 13.3 6.0, 16.6 15,758 Lesotho 22.6 22.7 10.2, 28.3 18.7 9.3, 22.3 2,554 Liberia 12.1 13.6 5.7, 17.5 12.6 5.5, 15.8 1,681 Mozambique 18.9 19.7 8.6, 24.9 16.6 7.6, 20.6 24,605 Myanmar 20.0 20.6 9.1, 26.0 20.8 9.7, 25.5 35,727 Namibia 21.6 21.9 9.8, 27.4 20.3 9.3, 25.2 2,622 Nigeria 3.9 4.8 1.9, 6.4 4.7 1.9, 6.3 34,819 North Korea 20.1 20.7 9.1, 26.0 Pakistan 12.4 13.9 5.8, 17.8 12.1 5.5, 15.0 55,900 PNG 26.3 25.5 11.6, 31.5 Philippines 28.3 26.9 12.4, 33.1 24.1 11.7, 29.1 120,731 Russia 39.1 33.7 16.4, 40.6 31.6 15.9, 37.6 26,678 Sierra Leone 31.9 29.3 13.8, 35.8 26.1 12.7, 31.7 5,367 South Africa 19.4 20.1 8.84, 25.4 19.5 8.9, 24.2 72,580 Tanzania 16.3 17.5 7.5, 22.2 10.9 4.8, 13.6 17,471 Thailand 24.0 23.8 10.7, 29.6 23.9 11.5, 29.7 26,345 Uganda 10.1 11.6 4.8, 15.0 10.2 4.4, 13.0 8,078 Vietnam 23.8 23.6 10.6, 29.4 19.7 9.9, 23.5 21,678 Zambia 14.6 16.0 6.8, 20.4 14.0 6.3, 17.5 9,563 Zimbabwe 14.6 16.0 6.8, 20.4 13.9 6.4, 17.2 4,486 Weighted average 21.5 19.6 8.7, 24.5 17.6 8.4, 21.4 1,358,237 Country Smoking Prevalencea Crudeb Age-Adjustedc No. of Excess TB Casesd PAP, % 95% CI PAP, % 95% CI Afghanistan 13.0e 14.4 6.1, 18.5 Angola 9.2e 10.7 4.4, 13.9 Bangladesh 23.0 23.0 10.3, 28.7 18.6 9.2, 22.3 59,130 Brazil 17.2 18.3 7.9, 23.1 18.1 7.9, 22.8 14,037 Cambodia 21.2 21.6 9.6, 27.1 18.7 9.0, 22.7 8,422 CAR 8.6e 10.0 4.1, 13.0 China 28.1 26.8 12.3, 33.0 22.4 11.4, 26.6 176,649 Congo 13.9 15.3 6.5, 19.6 13.4 6.1, 16.7 3,195 DRC 6.4 7.7 3.1, 10.1 Ethiopia 4.3 5.3 2.1, 7.0 4.8 2.0, 6.3 7,932 India 14.0 15.4 6.5, 19.7 14.3 6.5, 17.8 363,861 Indonesia 34.8 31.2 14.8, 37.9 24.9 13.2, 29.1 238,368 Kenya 13.5 14.9 6.3, 19.1 13.3 6.0, 16.6 15,758 Lesotho 22.6 22.7 10.2, 28.3 18.7 9.3, 22.3 2,554 Liberia 12.1 13.6 5.7, 17.5 12.6 5.5, 15.8 1,681 Mozambique 18.9 19.7 8.6, 24.9 16.6 7.6, 20.6 24,605 Myanmar 20.0 20.6 9.1, 26.0 20.8 9.7, 25.5 35,727 Namibia 21.6 21.9 9.8, 27.4 20.3 9.3, 25.2 2,622 Nigeria 3.9 4.8 1.9, 6.4 4.7 1.9, 6.3 34,819 North Korea 20.1 20.7 9.1, 26.0 Pakistan 12.4 13.9 5.8, 17.8 12.1 5.5, 15.0 55,900 PNG 26.3 25.5 11.6, 31.5 Philippines 28.3 26.9 12.4, 33.1 24.1 11.7, 29.1 120,731 Russia 39.1 33.7 16.4, 40.6 31.6 15.9, 37.6 26,678 Sierra Leone 31.9 29.3 13.8, 35.8 26.1 12.7, 31.7 5,367 South Africa 19.4 20.1 8.84, 25.4 19.5 8.9, 24.2 72,580 Tanzania 16.3 17.5 7.5, 22.2 10.9 4.8, 13.6 17,471 Thailand 24.0 23.8 10.7, 29.6 23.9 11.5, 29.7 26,345 Uganda 10.1 11.6 4.8, 15.0 10.2 4.4, 13.0 8,078 Vietnam 23.8 23.6 10.6, 29.4 19.7 9.9, 23.5 21,678 Zambia 14.6 16.0 6.8, 20.4 14.0 6.3, 17.5 9,563 Zimbabwe 14.6 16.0 6.8, 20.4 13.9 6.4, 17.2 4,486 Weighted average 21.5 19.6 8.7, 24.5 17.6 8.4, 21.4 1,358,237 Abbreviations: CAR, Central African Republic; CI, confidence interval; DRC, Democratic Republic of Congo; PAP, population attributable proportion; PNG, Papua New Guinea; TB, tuberculosis. a Current tobacco smoking prevalence. b TB disease incidence based on relative risk of 2.3 (95% CI: 1.5, 2.8) (crude). c TB disease incidence based on relative risk of 2.3 2.3 (95% CI: 1.5, 2.8) (age-adjusted); blank if no age-specific data. d Excess cases based on age-adjusted PAP except for countries with no age-specific data. e Daily smoking prevalence (percentage of population). Table 3. Estimated Number and Proportion of Tuberculosis Disease Attributable to Tobacco Smoking According to Sex Among Adults in 32 High-Tuberculosis-Burden Countries, 2009–2016 Country Men Women No. of TB Casesa PAP, % 95% CIb No. of Excess TB Casesc No. of TB Casesa PAP, % 95% CIb No. of Excess TB Casesc Afghanistan 9,004 22.9 10.3, 28.6 2,066 14,519 3.5 1.4, 4.7 510 Angola 14,001 17.8 7.7, 22.6 2,497 9,317 2.0 0.8, 2.7 190 Bangladesh 125,646 36.8 18.3, 43.9 46,179 87,336 1.9 0.7, 2.6 1,670 Brazil 50,383 21.9 9.7, 27.4 11,046 22,537 14.6 6.1, 18.6 3,280 Cambodia 15,089 34.5 16.9, 41.5 5,213 13,171 4.5 1.8, 5.9 589 CAR 5,275 17.1 7.4, 21.8 904 3,574 1.9 0.7, 2.6 68 China 535,618 40.7 20.9, 48.1 218,252 238,185 3.0 1.2, 4.0 7,207 Congo 5,294 25.5 11.6, 31.5 1,349 4,037 2.2 0.8, 2.9 87 DRC 64,101 15.6 6.6, 19.9 9,989 48,684 1.5 0.6, 2.1 748 Ethiopia 61,198 9.5 3.9, 12.4 5,830 48,956 0.6 0.2, 0.9 316 India 1,107,520 24.0 10.8, 29.8 265,875 551,470 3.6 1.4, 4.8 20,035 Indonesia 192,516 46.6 25.1, 54.0 89,621 133,490 3.4 1.3, 4.5 4,527 Kenya 44,799 24.6 11.2, 30.5 11,022 24,865 2.7 1.0, 3.5 661 Lesotho 4,194 37.5 18.8, 44.7 1,574 2,536 0.6 0.2, 0.9 16 Liberia 4,293 23.3 10.5, 29.1 1,001 2,015 3.5 1.4, 4.7 71 Mozambique 33,255 30.0 14.2, 36.6 9,983 29,301 7.3 3.0, 9.6 2,153 Myanmar 67,911 32.9 15.9, 39.8 22,376 37,977 9.6 3.9, 12.5 3,658 Namibia 4,710 30.2 14.3, 36.8 1,423 3,306 12.5 5.2, 16.1 414 Nigeria 57,163 8.7 3.5, 11.3 4,955 34,872 0.5 0.2, 0.7 180 North Korea 61,102 36.3 18.0, 43.4 22,201 35,648 0.0 0.0 0 Pakistan 160,044 22.4 10.0, 28.0 35,844 154,588 2.7 1.0, 3.5 4,108 PNG 2,247 32.7 15.7, 39.5 734 2,095 15.7 6.7, 20.6 332 Philippines 188,226 38.3 19.3, 45.5 72,044 96,016 10.5 4.3, 13.6 10,057 Russia 62,462 43.9 23.1, 51.3 27,422 26,672 22.0 9.8, 27.5 5,869 Sierra Leone 7,195 39.3 20.0, 46.6 2,831 4,477 15.8 6.7, 20.1 706 South Africa 128,842 29.4 13.8, 35.9 37,852 87,642 9.2 3.8, 12.0 8,069 Tanzania 36,162 27.3 12.6, 33.6 9,876 21,973 4.7 1.9, 6.2 1,034 Thailand 46,870 37.7 18.9, 44.9 17,682 22,324 3.3 1.3, 4.4 730 Uganda 26,573 18.6 8.1, 23.5 4,948 12,927 3.4 1.3, 4.5 438 Vietnam 76,979 38.1 19.2, 45.3 29,349 23,275 1.8 0.7, 2.4 416 Zambia 23,197 24.7 11.2, 30.6 5,724 12,960 4.9 2.0, 6.5 641 Zimbabwe 15,436 26.7 12.3, 32.9 4,119 10,349 2.5 1.0, 3.4 262 Weighted averaged 3,237,305 30.3 14.7, 36.6 981,781 1,821,094 4.3 1.7, 5.7 79,042 Country Men Women No. of TB Casesa PAP, % 95% CIb No. of Excess TB Casesc No. of TB Casesa PAP, % 95% CIb No. of Excess TB Casesc Afghanistan 9,004 22.9 10.3, 28.6 2,066 14,519 3.5 1.4, 4.7 510 Angola 14,001 17.8 7.7, 22.6 2,497 9,317 2.0 0.8, 2.7 190 Bangladesh 125,646 36.8 18.3, 43.9 46,179 87,336 1.9 0.7, 2.6 1,670 Brazil 50,383 21.9 9.7, 27.4 11,046 22,537 14.6 6.1, 18.6 3,280 Cambodia 15,089 34.5 16.9, 41.5 5,213 13,171 4.5 1.8, 5.9 589 CAR 5,275 17.1 7.4, 21.8 904 3,574 1.9 0.7, 2.6 68 China 535,618 40.7 20.9, 48.1 218,252 238,185 3.0 1.2, 4.0 7,207 Congo 5,294 25.5 11.6, 31.5 1,349 4,037 2.2 0.8, 2.9 87 DRC 64,101 15.6 6.6, 19.9 9,989 48,684 1.5 0.6, 2.1 748 Ethiopia 61,198 9.5 3.9, 12.4 5,830 48,956 0.6 0.2, 0.9 316 India 1,107,520 24.0 10.8, 29.8 265,875 551,470 3.6 1.4, 4.8 20,035 Indonesia 192,516 46.6 25.1, 54.0 89,621 133,490 3.4 1.3, 4.5 4,527 Kenya 44,799 24.6 11.2, 30.5 11,022 24,865 2.7 1.0, 3.5 661 Lesotho 4,194 37.5 18.8, 44.7 1,574 2,536 0.6 0.2, 0.9 16 Liberia 4,293 23.3 10.5, 29.1 1,001 2,015 3.5 1.4, 4.7 71 Mozambique 33,255 30.0 14.2, 36.6 9,983 29,301 7.3 3.0, 9.6 2,153 Myanmar 67,911 32.9 15.9, 39.8 22,376 37,977 9.6 3.9, 12.5 3,658 Namibia 4,710 30.2 14.3, 36.8 1,423 3,306 12.5 5.2, 16.1 414 Nigeria 57,163 8.7 3.5, 11.3 4,955 34,872 0.5 0.2, 0.7 180 North Korea 61,102 36.3 18.0, 43.4 22,201 35,648 0.0 0.0 0 Pakistan 160,044 22.4 10.0, 28.0 35,844 154,588 2.7 1.0, 3.5 4,108 PNG 2,247 32.7 15.7, 39.5 734 2,095 15.7 6.7, 20.6 332 Philippines 188,226 38.3 19.3, 45.5 72,044 96,016 10.5 4.3, 13.6 10,057 Russia 62,462 43.9 23.1, 51.3 27,422 26,672 22.0 9.8, 27.5 5,869 Sierra Leone 7,195 39.3 20.0, 46.6 2,831 4,477 15.8 6.7, 20.1 706 South Africa 128,842 29.4 13.8, 35.9 37,852 87,642 9.2 3.8, 12.0 8,069 Tanzania 36,162 27.3 12.6, 33.6 9,876 21,973 4.7 1.9, 6.2 1,034 Thailand 46,870 37.7 18.9, 44.9 17,682 22,324 3.3 1.3, 4.4 730 Uganda 26,573 18.6 8.1, 23.5 4,948 12,927 3.4 1.3, 4.5 438 Vietnam 76,979 38.1 19.2, 45.3 29,349 23,275 1.8 0.7, 2.4 416 Zambia 23,197 24.7 11.2, 30.6 5,724 12,960 4.9 2.0, 6.5 641 Zimbabwe 15,436 26.7 12.3, 32.9 4,119 10,349 2.5 1.0, 3.4 262 Weighted averaged 3,237,305 30.3 14.7, 36.6 981,781 1,821,094 4.3 1.7, 5.7 79,042 Abbreviations: CAR, Central African Republic; CI, confidence interval; DRC, Democratic Republic of Congo; PAP, population attributable proportion; PNG, Papua New Guinea; TB, tuberculosis. a Number of TB cases reported in 2016 among men and women in each country. b Confidence interval calculated based on relative risk of 2.3 (95% CI: 1.5, 2.8). c Number of excess TB cases based on reported number of TB cases. d The weighted average calculated based on the number of TB cases. Table 3. Estimated Number and Proportion of Tuberculosis Disease Attributable to Tobacco Smoking According to Sex Among Adults in 32 High-Tuberculosis-Burden Countries, 2009–2016 Country Men Women No. of TB Casesa PAP, % 95% CIb No. of Excess TB Casesc No. of TB Casesa PAP, % 95% CIb No. of Excess TB Casesc Afghanistan 9,004 22.9 10.3, 28.6 2,066 14,519 3.5 1.4, 4.7 510 Angola 14,001 17.8 7.7, 22.6 2,497 9,317 2.0 0.8, 2.7 190 Bangladesh 125,646 36.8 18.3, 43.9 46,179 87,336 1.9 0.7, 2.6 1,670 Brazil 50,383 21.9 9.7, 27.4 11,046 22,537 14.6 6.1, 18.6 3,280 Cambodia 15,089 34.5 16.9, 41.5 5,213 13,171 4.5 1.8, 5.9 589 CAR 5,275 17.1 7.4, 21.8 904 3,574 1.9 0.7, 2.6 68 China 535,618 40.7 20.9, 48.1 218,252 238,185 3.0 1.2, 4.0 7,207 Congo 5,294 25.5 11.6, 31.5 1,349 4,037 2.2 0.8, 2.9 87 DRC 64,101 15.6 6.6, 19.9 9,989 48,684 1.5 0.6, 2.1 748 Ethiopia 61,198 9.5 3.9, 12.4 5,830 48,956 0.6 0.2, 0.9 316 India 1,107,520 24.0 10.8, 29.8 265,875 551,470 3.6 1.4, 4.8 20,035 Indonesia 192,516 46.6 25.1, 54.0 89,621 133,490 3.4 1.3, 4.5 4,527 Kenya 44,799 24.6 11.2, 30.5 11,022 24,865 2.7 1.0, 3.5 661 Lesotho 4,194 37.5 18.8, 44.7 1,574 2,536 0.6 0.2, 0.9 16 Liberia 4,293 23.3 10.5, 29.1 1,001 2,015 3.5 1.4, 4.7 71 Mozambique 33,255 30.0 14.2, 36.6 9,983 29,301 7.3 3.0, 9.6 2,153 Myanmar 67,911 32.9 15.9, 39.8 22,376 37,977 9.6 3.9, 12.5 3,658 Namibia 4,710 30.2 14.3, 36.8 1,423 3,306 12.5 5.2, 16.1 414 Nigeria 57,163 8.7 3.5, 11.3 4,955 34,872 0.5 0.2, 0.7 180 North Korea 61,102 36.3 18.0, 43.4 22,201 35,648 0.0 0.0 0 Pakistan 160,044 22.4 10.0, 28.0 35,844 154,588 2.7 1.0, 3.5 4,108 PNG 2,247 32.7 15.7, 39.5 734 2,095 15.7 6.7, 20.6 332 Philippines 188,226 38.3 19.3, 45.5 72,044 96,016 10.5 4.3, 13.6 10,057 Russia 62,462 43.9 23.1, 51.3 27,422 26,672 22.0 9.8, 27.5 5,869 Sierra Leone 7,195 39.3 20.0, 46.6 2,831 4,477 15.8 6.7, 20.1 706 South Africa 128,842 29.4 13.8, 35.9 37,852 87,642 9.2 3.8, 12.0 8,069 Tanzania 36,162 27.3 12.6, 33.6 9,876 21,973 4.7 1.9, 6.2 1,034 Thailand 46,870 37.7 18.9, 44.9 17,682 22,324 3.3 1.3, 4.4 730 Uganda 26,573 18.6 8.1, 23.5 4,948 12,927 3.4 1.3, 4.5 438 Vietnam 76,979 38.1 19.2, 45.3 29,349 23,275 1.8 0.7, 2.4 416 Zambia 23,197 24.7 11.2, 30.6 5,724 12,960 4.9 2.0, 6.5 641 Zimbabwe 15,436 26.7 12.3, 32.9 4,119 10,349 2.5 1.0, 3.4 262 Weighted averaged 3,237,305 30.3 14.7, 36.6 981,781 1,821,094 4.3 1.7, 5.7 79,042 Country Men Women No. of TB Casesa PAP, % 95% CIb No. of Excess TB Casesc No. of TB Casesa PAP, % 95% CIb No. of Excess TB Casesc Afghanistan 9,004 22.9 10.3, 28.6 2,066 14,519 3.5 1.4, 4.7 510 Angola 14,001 17.8 7.7, 22.6 2,497 9,317 2.0 0.8, 2.7 190 Bangladesh 125,646 36.8 18.3, 43.9 46,179 87,336 1.9 0.7, 2.6 1,670 Brazil 50,383 21.9 9.7, 27.4 11,046 22,537 14.6 6.1, 18.6 3,280 Cambodia 15,089 34.5 16.9, 41.5 5,213 13,171 4.5 1.8, 5.9 589 CAR 5,275 17.1 7.4, 21.8 904 3,574 1.9 0.7, 2.6 68 China 535,618 40.7 20.9, 48.1 218,252 238,185 3.0 1.2, 4.0 7,207 Congo 5,294 25.5 11.6, 31.5 1,349 4,037 2.2 0.8, 2.9 87 DRC 64,101 15.6 6.6, 19.9 9,989 48,684 1.5 0.6, 2.1 748 Ethiopia 61,198 9.5 3.9, 12.4 5,830 48,956 0.6 0.2, 0.9 316 India 1,107,520 24.0 10.8, 29.8 265,875 551,470 3.6 1.4, 4.8 20,035 Indonesia 192,516 46.6 25.1, 54.0 89,621 133,490 3.4 1.3, 4.5 4,527 Kenya 44,799 24.6 11.2, 30.5 11,022 24,865 2.7 1.0, 3.5 661 Lesotho 4,194 37.5 18.8, 44.7 1,574 2,536 0.6 0.2, 0.9 16 Liberia 4,293 23.3 10.5, 29.1 1,001 2,015 3.5 1.4, 4.7 71 Mozambique 33,255 30.0 14.2, 36.6 9,983 29,301 7.3 3.0, 9.6 2,153 Myanmar 67,911 32.9 15.9, 39.8 22,376 37,977 9.6 3.9, 12.5 3,658 Namibia 4,710 30.2 14.3, 36.8 1,423 3,306 12.5 5.2, 16.1 414 Nigeria 57,163 8.7 3.5, 11.3 4,955 34,872 0.5 0.2, 0.7 180 North Korea 61,102 36.3 18.0, 43.4 22,201 35,648 0.0 0.0 0 Pakistan 160,044 22.4 10.0, 28.0 35,844 154,588 2.7 1.0, 3.5 4,108 PNG 2,247 32.7 15.7, 39.5 734 2,095 15.7 6.7, 20.6 332 Philippines 188,226 38.3 19.3, 45.5 72,044 96,016 10.5 4.3, 13.6 10,057 Russia 62,462 43.9 23.1, 51.3 27,422 26,672 22.0 9.8, 27.5 5,869 Sierra Leone 7,195 39.3 20.0, 46.6 2,831 4,477 15.8 6.7, 20.1 706 South Africa 128,842 29.4 13.8, 35.9 37,852 87,642 9.2 3.8, 12.0 8,069 Tanzania 36,162 27.3 12.6, 33.6 9,876 21,973 4.7 1.9, 6.2 1,034 Thailand 46,870 37.7 18.9, 44.9 17,682 22,324 3.3 1.3, 4.4 730 Uganda 26,573 18.6 8.1, 23.5 4,948 12,927 3.4 1.3, 4.5 438 Vietnam 76,979 38.1 19.2, 45.3 29,349 23,275 1.8 0.7, 2.4 416 Zambia 23,197 24.7 11.2, 30.6 5,724 12,960 4.9 2.0, 6.5 641 Zimbabwe 15,436 26.7 12.3, 32.9 4,119 10,349 2.5 1.0, 3.4 262 Weighted averaged 3,237,305 30.3 14.7, 36.6 981,781 1,821,094 4.3 1.7, 5.7 79,042 Abbreviations: CAR, Central African Republic; CI, confidence interval; DRC, Democratic Republic of Congo; PAP, population attributable proportion; PNG, Papua New Guinea; TB, tuberculosis. a Number of TB cases reported in 2016 among men and women in each country. b Confidence interval calculated based on relative risk of 2.3 (95% CI: 1.5, 2.8). c Number of excess TB cases based on reported number of TB cases. d The weighted average calculated based on the number of TB cases. Overall, 15.2% (95% CI: 1.8, 31.9) of TB deaths in adults aged 15 years or older were attributable to tobacco smoking. The proportion of TB deaths attributed to smoking ranged from 3.8% (95% CI: 0.4, 9.5) in Nigeria to 28.1% (95% CI: 3.8, 51.4) in Russia. Russia (28.1%), Indonesia (25.8%), and Sierra Leone (24.2%) were the top 3 countries in terms of proportion of smoking-attributable TB deaths (Table 4). Although the proportions of TB cases (14.3%, 95% CI: 6.5, 17.8) and TB deaths (12.3%, 95% CI: 1.4, 27.4) attributable to tobacco smoking in India were low (ranked 19 and 22, respectively), the absolute number of TB cases and TB deaths were highest. Table 4. Estimated Proportion and Number of TB Deaths Attributable to Tobacco Smoking Among Adults in 32 High-Tuberculosis-Burden Countries, 2009–2016 Country Crude TB Mortalitya No. of Deaths Attributable to Smokingb No. of TB Deathsc Estimated No. of TB Casesd Estimated No. of TB Deathsd PAP, % 95% CI Afghanistan 11.5 1.3, 26.0 62 542 57,000 11,000 Angola 8.4 0.9, 19.9 119 1,417 95,000 18,000 Bangladesh 18.7 2.25, 38.3 1,460 7,806 324,000 66,000 Brazil 14.7 1.7, 31.7 891 6,069 77,000 5,400 Cambodia 17.5 2.1, 36.4 83 475 47,000 3,200 CAR 7.9 0.9, 18.8 17 212 15,900 2,700 China 21.9 2.7, 43.1 1,950 8,890 795,000 50,000 Congo 12.2 1.4, 27.3 16 129 23,100 3,100 DRC 6.0 0.6, 14.7 265 4,413 223,000 53,000 Ethiopia 4.12 0.4, 10.4 153 3,712 158,000 26,000 India 12.3 1.4, 27.4 7,061 57,494 2,557,000 423,000 Indonesia 25.8 3.4, 48.4 2,042 7,908 960,000 110,000 Kenya 11.9 1.3, 26.7 552 4,639 147,000 29,000 Lesotho 18.4 2.2, 38.0 201 1,093 13,600 1,100 Liberia 10.8 1.2, 24.6 31 283 12,600 2,800 Mozambique 15.9 1.9, 33.8 538 3,384 137,000 22,000 Myanmar 16.7 2.0, 35.1 1,087 6,523 169,000 25,000 Namibia 17.8 2.1, 36.8 129 728 13,000 750 Nigeria 3.8 0.4, 9.5 188 5,016 351,000 115,000 North Korea 16.7 2.0, 35.2 469 2,802 116,000 11,000 Pakistan 11.0 1.2, 25.1 488 4,425 467,000 44,000 PNG 20.8 2.6, 41.5 28 134 31,000 3,600 Philippines 22.1 2.8, 43.3 1,470 6,665 502,000 22,000 Russia 28.1 3.8, 51.4 2,259 8,035 84,000 12,000 Sierra Leone 24.2 3.1, 46.3 52 216 19,900 3,400 South Africa 16.3 1.9, 34.4 3,111 19,148 380,000 23,000 Tanzania 14.0 1.6, 30.6 495 3,531 151,000 28,000 Thailand 19.4 2.3, 39.3 918 4,743 110,000 8,600 Uganda 9.2 1.0, 21.4 281 3,058 75,000 11,000 Vietnam 19.2 2.3, 39.1 450 2,340 111,000 13,000 Zambia 12.7 1.4, 28.3 270 2,116 54,000 4,800 Zimbabwe 12.7 1.4, 28.3 328 2,571 31,000 1,200 Weighted averagee 15.2 1.8, 31.9 27,462 180,517 8,307,100 1,152,650 Country Crude TB Mortalitya No. of Deaths Attributable to Smokingb No. of TB Deathsc Estimated No. of TB Casesd Estimated No. of TB Deathsd PAP, % 95% CI Afghanistan 11.5 1.3, 26.0 62 542 57,000 11,000 Angola 8.4 0.9, 19.9 119 1,417 95,000 18,000 Bangladesh 18.7 2.25, 38.3 1,460 7,806 324,000 66,000 Brazil 14.7 1.7, 31.7 891 6,069 77,000 5,400 Cambodia 17.5 2.1, 36.4 83 475 47,000 3,200 CAR 7.9 0.9, 18.8 17 212 15,900 2,700 China 21.9 2.7, 43.1 1,950 8,890 795,000 50,000 Congo 12.2 1.4, 27.3 16 129 23,100 3,100 DRC 6.0 0.6, 14.7 265 4,413 223,000 53,000 Ethiopia 4.12 0.4, 10.4 153 3,712 158,000 26,000 India 12.3 1.4, 27.4 7,061 57,494 2,557,000 423,000 Indonesia 25.8 3.4, 48.4 2,042 7,908 960,000 110,000 Kenya 11.9 1.3, 26.7 552 4,639 147,000 29,000 Lesotho 18.4 2.2, 38.0 201 1,093 13,600 1,100 Liberia 10.8 1.2, 24.6 31 283 12,600 2,800 Mozambique 15.9 1.9, 33.8 538 3,384 137,000 22,000 Myanmar 16.7 2.0, 35.1 1,087 6,523 169,000 25,000 Namibia 17.8 2.1, 36.8 129 728 13,000 750 Nigeria 3.8 0.4, 9.5 188 5,016 351,000 115,000 North Korea 16.7 2.0, 35.2 469 2,802 116,000 11,000 Pakistan 11.0 1.2, 25.1 488 4,425 467,000 44,000 PNG 20.8 2.6, 41.5 28 134 31,000 3,600 Philippines 22.1 2.8, 43.3 1,470 6,665 502,000 22,000 Russia 28.1 3.8, 51.4 2,259 8,035 84,000 12,000 Sierra Leone 24.2 3.1, 46.3 52 216 19,900 3,400 South Africa 16.3 1.9, 34.4 3,111 19,148 380,000 23,000 Tanzania 14.0 1.6, 30.6 495 3,531 151,000 28,000 Thailand 19.4 2.3, 39.3 918 4,743 110,000 8,600 Uganda 9.2 1.0, 21.4 281 3,058 75,000 11,000 Vietnam 19.2 2.3, 39.1 450 2,340 111,000 13,000 Zambia 12.7 1.4, 28.3 270 2,116 54,000 4,800 Zimbabwe 12.7 1.4, 28.3 328 2,571 31,000 1,200 Weighted averagee 15.2 1.8, 31.9 27,462 180,517 8,307,100 1,152,650 Abbreviations: CAR, Central African Republic; CI, confidence interval; DRC, Democratic Republic of Congo; PAP, population attributable proportion; PNG, Papua New Guinea; TB, tuberculosis. a TB death attributable to smoking calculated based on relative risk of 2.0 (95% CI: 1.1, 3.7). b Excess TB death based on reported TB deaths. c Number of reported TB deaths in 2015. d Estimated number of TB cases (2016) and deaths (2015). e The weighted average calculated based on the number of TB deaths. Table 4. Estimated Proportion and Number of TB Deaths Attributable to Tobacco Smoking Among Adults in 32 High-Tuberculosis-Burden Countries, 2009–2016 Country Crude TB Mortalitya No. of Deaths Attributable to Smokingb No. of TB Deathsc Estimated No. of TB Casesd Estimated No. of TB Deathsd PAP, % 95% CI Afghanistan 11.5 1.3, 26.0 62 542 57,000 11,000 Angola 8.4 0.9, 19.9 119 1,417 95,000 18,000 Bangladesh 18.7 2.25, 38.3 1,460 7,806 324,000 66,000 Brazil 14.7 1.7, 31.7 891 6,069 77,000 5,400 Cambodia 17.5 2.1, 36.4 83 475 47,000 3,200 CAR 7.9 0.9, 18.8 17 212 15,900 2,700 China 21.9 2.7, 43.1 1,950 8,890 795,000 50,000 Congo 12.2 1.4, 27.3 16 129 23,100 3,100 DRC 6.0 0.6, 14.7 265 4,413 223,000 53,000 Ethiopia 4.12 0.4, 10.4 153 3,712 158,000 26,000 India 12.3 1.4, 27.4 7,061 57,494 2,557,000 423,000 Indonesia 25.8 3.4, 48.4 2,042 7,908 960,000 110,000 Kenya 11.9 1.3, 26.7 552 4,639 147,000 29,000 Lesotho 18.4 2.2, 38.0 201 1,093 13,600 1,100 Liberia 10.8 1.2, 24.6 31 283 12,600 2,800 Mozambique 15.9 1.9, 33.8 538 3,384 137,000 22,000 Myanmar 16.7 2.0, 35.1 1,087 6,523 169,000 25,000 Namibia 17.8 2.1, 36.8 129 728 13,000 750 Nigeria 3.8 0.4, 9.5 188 5,016 351,000 115,000 North Korea 16.7 2.0, 35.2 469 2,802 116,000 11,000 Pakistan 11.0 1.2, 25.1 488 4,425 467,000 44,000 PNG 20.8 2.6, 41.5 28 134 31,000 3,600 Philippines 22.1 2.8, 43.3 1,470 6,665 502,000 22,000 Russia 28.1 3.8, 51.4 2,259 8,035 84,000 12,000 Sierra Leone 24.2 3.1, 46.3 52 216 19,900 3,400 South Africa 16.3 1.9, 34.4 3,111 19,148 380,000 23,000 Tanzania 14.0 1.6, 30.6 495 3,531 151,000 28,000 Thailand 19.4 2.3, 39.3 918 4,743 110,000 8,600 Uganda 9.2 1.0, 21.4 281 3,058 75,000 11,000 Vietnam 19.2 2.3, 39.1 450 2,340 111,000 13,000 Zambia 12.7 1.4, 28.3 270 2,116 54,000 4,800 Zimbabwe 12.7 1.4, 28.3 328 2,571 31,000 1,200 Weighted averagee 15.2 1.8, 31.9 27,462 180,517 8,307,100 1,152,650 Country Crude TB Mortalitya No. of Deaths Attributable to Smokingb No. of TB Deathsc Estimated No. of TB Casesd Estimated No. of TB Deathsd PAP, % 95% CI Afghanistan 11.5 1.3, 26.0 62 542 57,000 11,000 Angola 8.4 0.9, 19.9 119 1,417 95,000 18,000 Bangladesh 18.7 2.25, 38.3 1,460 7,806 324,000 66,000 Brazil 14.7 1.7, 31.7 891 6,069 77,000 5,400 Cambodia 17.5 2.1, 36.4 83 475 47,000 3,200 CAR 7.9 0.9, 18.8 17 212 15,900 2,700 China 21.9 2.7, 43.1 1,950 8,890 795,000 50,000 Congo 12.2 1.4, 27.3 16 129 23,100 3,100 DRC 6.0 0.6, 14.7 265 4,413 223,000 53,000 Ethiopia 4.12 0.4, 10.4 153 3,712 158,000 26,000 India 12.3 1.4, 27.4 7,061 57,494 2,557,000 423,000 Indonesia 25.8 3.4, 48.4 2,042 7,908 960,000 110,000 Kenya 11.9 1.3, 26.7 552 4,639 147,000 29,000 Lesotho 18.4 2.2, 38.0 201 1,093 13,600 1,100 Liberia 10.8 1.2, 24.6 31 283 12,600 2,800 Mozambique 15.9 1.9, 33.8 538 3,384 137,000 22,000 Myanmar 16.7 2.0, 35.1 1,087 6,523 169,000 25,000 Namibia 17.8 2.1, 36.8 129 728 13,000 750 Nigeria 3.8 0.4, 9.5 188 5,016 351,000 115,000 North Korea 16.7 2.0, 35.2 469 2,802 116,000 11,000 Pakistan 11.0 1.2, 25.1 488 4,425 467,000 44,000 PNG 20.8 2.6, 41.5 28 134 31,000 3,600 Philippines 22.1 2.8, 43.3 1,470 6,665 502,000 22,000 Russia 28.1 3.8, 51.4 2,259 8,035 84,000 12,000 Sierra Leone 24.2 3.1, 46.3 52 216 19,900 3,400 South Africa 16.3 1.9, 34.4 3,111 19,148 380,000 23,000 Tanzania 14.0 1.6, 30.6 495 3,531 151,000 28,000 Thailand 19.4 2.3, 39.3 918 4,743 110,000 8,600 Uganda 9.2 1.0, 21.4 281 3,058 75,000 11,000 Vietnam 19.2 2.3, 39.1 450 2,340 111,000 13,000 Zambia 12.7 1.4, 28.3 270 2,116 54,000 4,800 Zimbabwe 12.7 1.4, 28.3 328 2,571 31,000 1,200 Weighted averagee 15.2 1.8, 31.9 27,462 180,517 8,307,100 1,152,650 Abbreviations: CAR, Central African Republic; CI, confidence interval; DRC, Democratic Republic of Congo; PAP, population attributable proportion; PNG, Papua New Guinea; TB, tuberculosis. a TB death attributable to smoking calculated based on relative risk of 2.0 (95% CI: 1.1, 3.7). b Excess TB death based on reported TB deaths. c Number of reported TB deaths in 2015. d Estimated number of TB cases (2016) and deaths (2015). e The weighted average calculated based on the number of TB deaths. In Monte Carlo simulation to estimate smoking prevalence misclassification and relative risk misspecification, the proportions of TB disease and TB death attributable to smoking were 17.7% (95% CI: 9.4, 27.0) and 17.9% (95% CI: 1.5, 35.7), respectively (Table 5). Table 5. Sensitivity Analysis for Proportion of TB Disease and Deaths, Among Adults in 32 High-Tuberculosis-Burden Countries, Attributable to Tobacco Smoking Based on Monte Carlo Analysis, 2009–2016 Country Smoking Prevalence TB Disease TB Mortality Point Estimate, %a 95% CIa PAP, % 95% CI PAP, % 95% CI Afghanistanb 13.0 10.0, 15.9 11.5 5.6, 18.7 11.9 1.0, 25.9 Angolab 9.2 6.2, 12.2 8.4 3.5, 14.4 8.7 0.5, 20.4 Bangladesh 23.0 21.9, 24.2 18.6 10.0, 28.3 18.9 1.6, 37.2 Brazil 17.2 16.7, 17.7 14.7 7.7, 22.4 15.0 1.2, 30.8 Cambodia 21.2 16.2, 27.3 17.5 9.2, 27.2 17.9 1.8, 36.2 CARb 8.6 5.6, 11.5 7.9 3.5, 13.7 8.2 0.6, 19.7 China 28.1 26.7, 29.7 21.8 11.9, 32.7 21.9 2.0, 42.4 Congo 13.9 9.9, 18.3 12.1 5.5, 19.8 12.5 1.0, 27.5 DRCb 6.4 3.5, 9.3 6.1 2.4, 11.3 6.3 0.4, 15.2 Ethiopia 4.3 3.0, 5.6 4.2 1.8, 7.3 4.4 0.3, 10.5 India 14.0 13.4, 14.6 12.3 6.4, 19.4 12.7 1.0, 27.2 Indonesia 34.8 33.2, 36.4 25.7 14.2, 37.3 25.8 3.1, 48.5 Kenya 13.5 9.9, 17.3 11.9 5.8, 19.6 12.3 1.0, 26.2 Lesotho 22.6 16.6, 29.4 18.3 9.2, 28.5 18.6 1.5, 38.0 Liberia 12.1 6.5, 20.8 10.7 3.6, 20.4 11.0 0.7, 26.2 Mozambique 18.9 12.2, 27.7 15.8 7.2, 26.6 16.0 1.5, 33.5 Myanmar 20.0 16.1, 29.6 16.6 8.1, 26.7 16.9 1.6, 35.5 Namibia 21.6 15.5, 28.8 17.6 8.8, 28.6 17.9 1.4, 36.9 Nigeria 3.9 3.3, 4.5 3.8 1.8, 6.5 4.0 0.3, 9.4 North Koreab 20.1 17.2, 23.0 16.7 8.8, 26.0 17.0 1.4, 34.3 Pakistan 12.4 11.2, 13.3 11.1 5.7, 17.6 11.5 0.8, 24.4 PNGb 26.3 23.4, 29.2 20.7 11.1, 32.8 20.9 1.9, 41.4 Philippines 28.3 27.0, 29.5 21.9 11.9, 32.8 22.1 2.0, 42.3 Russia 39.1 37.8, 40.5 27.9 15.9, 40.4 27.6 2.7, 50.1 Sierra Leone 31.9 22.0, 42.3 23.9 11.9, 37.0 23.9 2.6, 47.0 South Africa 19.4 15.5, 24.1 16.2 8.2, 25.7 16.5 1.5, 34.8 Tanzania 16.3 11.7, 21.3 13.9 6.5, 22.3 14.2 1.2, 30.9 Thailand 24.0 22.8, 25.1 19.3 10.2, 29.0 19.5 1.7, 38.3 Uganda 10.1 7.3, 13.6 9.3 4.3, 15.4 9.6 0.7, 21.4 Vietnam 23.8 22.7, 24.9 19.2 10.2, 29.4 19.4 1.7, 38.4 Zambia 14.6 10.0, 19.5 12.8 6.1, 21.5 13.2 0.9, 28.5 Zimbabwe 14.6 10.8, 18.5 12.6 6.1, 20.4 13.0 0.9, 28.9 Weighted average 21.5 20.2, 23.0 17.7 9.4, 27.0 17.9 1.5, 35.7 Country Smoking Prevalence TB Disease TB Mortality Point Estimate, %a 95% CIa PAP, % 95% CI PAP, % 95% CI Afghanistanb 13.0 10.0, 15.9 11.5 5.6, 18.7 11.9 1.0, 25.9 Angolab 9.2 6.2, 12.2 8.4 3.5, 14.4 8.7 0.5, 20.4 Bangladesh 23.0 21.9, 24.2 18.6 10.0, 28.3 18.9 1.6, 37.2 Brazil 17.2 16.7, 17.7 14.7 7.7, 22.4 15.0 1.2, 30.8 Cambodia 21.2 16.2, 27.3 17.5 9.2, 27.2 17.9 1.8, 36.2 CARb 8.6 5.6, 11.5 7.9 3.5, 13.7 8.2 0.6, 19.7 China 28.1 26.7, 29.7 21.8 11.9, 32.7 21.9 2.0, 42.4 Congo 13.9 9.9, 18.3 12.1 5.5, 19.8 12.5 1.0, 27.5 DRCb 6.4 3.5, 9.3 6.1 2.4, 11.3 6.3 0.4, 15.2 Ethiopia 4.3 3.0, 5.6 4.2 1.8, 7.3 4.4 0.3, 10.5 India 14.0 13.4, 14.6 12.3 6.4, 19.4 12.7 1.0, 27.2 Indonesia 34.8 33.2, 36.4 25.7 14.2, 37.3 25.8 3.1, 48.5 Kenya 13.5 9.9, 17.3 11.9 5.8, 19.6 12.3 1.0, 26.2 Lesotho 22.6 16.6, 29.4 18.3 9.2, 28.5 18.6 1.5, 38.0 Liberia 12.1 6.5, 20.8 10.7 3.6, 20.4 11.0 0.7, 26.2 Mozambique 18.9 12.2, 27.7 15.8 7.2, 26.6 16.0 1.5, 33.5 Myanmar 20.0 16.1, 29.6 16.6 8.1, 26.7 16.9 1.6, 35.5 Namibia 21.6 15.5, 28.8 17.6 8.8, 28.6 17.9 1.4, 36.9 Nigeria 3.9 3.3, 4.5 3.8 1.8, 6.5 4.0 0.3, 9.4 North Koreab 20.1 17.2, 23.0 16.7 8.8, 26.0 17.0 1.4, 34.3 Pakistan 12.4 11.2, 13.3 11.1 5.7, 17.6 11.5 0.8, 24.4 PNGb 26.3 23.4, 29.2 20.7 11.1, 32.8 20.9 1.9, 41.4 Philippines 28.3 27.0, 29.5 21.9 11.9, 32.8 22.1 2.0, 42.3 Russia 39.1 37.8, 40.5 27.9 15.9, 40.4 27.6 2.7, 50.1 Sierra Leone 31.9 22.0, 42.3 23.9 11.9, 37.0 23.9 2.6, 47.0 South Africa 19.4 15.5, 24.1 16.2 8.2, 25.7 16.5 1.5, 34.8 Tanzania 16.3 11.7, 21.3 13.9 6.5, 22.3 14.2 1.2, 30.9 Thailand 24.0 22.8, 25.1 19.3 10.2, 29.0 19.5 1.7, 38.3 Uganda 10.1 7.3, 13.6 9.3 4.3, 15.4 9.6 0.7, 21.4 Vietnam 23.8 22.7, 24.9 19.2 10.2, 29.4 19.4 1.7, 38.4 Zambia 14.6 10.0, 19.5 12.8 6.1, 21.5 13.2 0.9, 28.5 Zimbabwe 14.6 10.8, 18.5 12.6 6.1, 20.4 13.0 0.9, 28.9 Weighted average 21.5 20.2, 23.0 17.7 9.4, 27.0 17.9 1.5, 35.7 Abbreviations: CAR, Central African Republic; CI, confidence interval; DRC, Democratic Republic of Congo; PAP, population attributable proportion; PNG, Papua New Guinea; TB, tuberculosis. a Point estimate and 95% confidence interval for smoking prevalence from World Health Organization reports (20, 21). b 95% confidence intervals were calculated based on the average standard error from the 26 countries. Table 5. Sensitivity Analysis for Proportion of TB Disease and Deaths, Among Adults in 32 High-Tuberculosis-Burden Countries, Attributable to Tobacco Smoking Based on Monte Carlo Analysis, 2009–2016 Country Smoking Prevalence TB Disease TB Mortality Point Estimate, %a 95% CIa PAP, % 95% CI PAP, % 95% CI Afghanistanb 13.0 10.0, 15.9 11.5 5.6, 18.7 11.9 1.0, 25.9 Angolab 9.2 6.2, 12.2 8.4 3.5, 14.4 8.7 0.5, 20.4 Bangladesh 23.0 21.9, 24.2 18.6 10.0, 28.3 18.9 1.6, 37.2 Brazil 17.2 16.7, 17.7 14.7 7.7, 22.4 15.0 1.2, 30.8 Cambodia 21.2 16.2, 27.3 17.5 9.2, 27.2 17.9 1.8, 36.2 CARb 8.6 5.6, 11.5 7.9 3.5, 13.7 8.2 0.6, 19.7 China 28.1 26.7, 29.7 21.8 11.9, 32.7 21.9 2.0, 42.4 Congo 13.9 9.9, 18.3 12.1 5.5, 19.8 12.5 1.0, 27.5 DRCb 6.4 3.5, 9.3 6.1 2.4, 11.3 6.3 0.4, 15.2 Ethiopia 4.3 3.0, 5.6 4.2 1.8, 7.3 4.4 0.3, 10.5 India 14.0 13.4, 14.6 12.3 6.4, 19.4 12.7 1.0, 27.2 Indonesia 34.8 33.2, 36.4 25.7 14.2, 37.3 25.8 3.1, 48.5 Kenya 13.5 9.9, 17.3 11.9 5.8, 19.6 12.3 1.0, 26.2 Lesotho 22.6 16.6, 29.4 18.3 9.2, 28.5 18.6 1.5, 38.0 Liberia 12.1 6.5, 20.8 10.7 3.6, 20.4 11.0 0.7, 26.2 Mozambique 18.9 12.2, 27.7 15.8 7.2, 26.6 16.0 1.5, 33.5 Myanmar 20.0 16.1, 29.6 16.6 8.1, 26.7 16.9 1.6, 35.5 Namibia 21.6 15.5, 28.8 17.6 8.8, 28.6 17.9 1.4, 36.9 Nigeria 3.9 3.3, 4.5 3.8 1.8, 6.5 4.0 0.3, 9.4 North Koreab 20.1 17.2, 23.0 16.7 8.8, 26.0 17.0 1.4, 34.3 Pakistan 12.4 11.2, 13.3 11.1 5.7, 17.6 11.5 0.8, 24.4 PNGb 26.3 23.4, 29.2 20.7 11.1, 32.8 20.9 1.9, 41.4 Philippines 28.3 27.0, 29.5 21.9 11.9, 32.8 22.1 2.0, 42.3 Russia 39.1 37.8, 40.5 27.9 15.9, 40.4 27.6 2.7, 50.1 Sierra Leone 31.9 22.0, 42.3 23.9 11.9, 37.0 23.9 2.6, 47.0 South Africa 19.4 15.5, 24.1 16.2 8.2, 25.7 16.5 1.5, 34.8 Tanzania 16.3 11.7, 21.3 13.9 6.5, 22.3 14.2 1.2, 30.9 Thailand 24.0 22.8, 25.1 19.3 10.2, 29.0 19.5 1.7, 38.3 Uganda 10.1 7.3, 13.6 9.3 4.3, 15.4 9.6 0.7, 21.4 Vietnam 23.8 22.7, 24.9 19.2 10.2, 29.4 19.4 1.7, 38.4 Zambia 14.6 10.0, 19.5 12.8 6.1, 21.5 13.2 0.9, 28.5 Zimbabwe 14.6 10.8, 18.5 12.6 6.1, 20.4 13.0 0.9, 28.9 Weighted average 21.5 20.2, 23.0 17.7 9.4, 27.0 17.9 1.5, 35.7 Country Smoking Prevalence TB Disease TB Mortality Point Estimate, %a 95% CIa PAP, % 95% CI PAP, % 95% CI Afghanistanb 13.0 10.0, 15.9 11.5 5.6, 18.7 11.9 1.0, 25.9 Angolab 9.2 6.2, 12.2 8.4 3.5, 14.4 8.7 0.5, 20.4 Bangladesh 23.0 21.9, 24.2 18.6 10.0, 28.3 18.9 1.6, 37.2 Brazil 17.2 16.7, 17.7 14.7 7.7, 22.4 15.0 1.2, 30.8 Cambodia 21.2 16.2, 27.3 17.5 9.2, 27.2 17.9 1.8, 36.2 CARb 8.6 5.6, 11.5 7.9 3.5, 13.7 8.2 0.6, 19.7 China 28.1 26.7, 29.7 21.8 11.9, 32.7 21.9 2.0, 42.4 Congo 13.9 9.9, 18.3 12.1 5.5, 19.8 12.5 1.0, 27.5 DRCb 6.4 3.5, 9.3 6.1 2.4, 11.3 6.3 0.4, 15.2 Ethiopia 4.3 3.0, 5.6 4.2 1.8, 7.3 4.4 0.3, 10.5 India 14.0 13.4, 14.6 12.3 6.4, 19.4 12.7 1.0, 27.2 Indonesia 34.8 33.2, 36.4 25.7 14.2, 37.3 25.8 3.1, 48.5 Kenya 13.5 9.9, 17.3 11.9 5.8, 19.6 12.3 1.0, 26.2 Lesotho 22.6 16.6, 29.4 18.3 9.2, 28.5 18.6 1.5, 38.0 Liberia 12.1 6.5, 20.8 10.7 3.6, 20.4 11.0 0.7, 26.2 Mozambique 18.9 12.2, 27.7 15.8 7.2, 26.6 16.0 1.5, 33.5 Myanmar 20.0 16.1, 29.6 16.6 8.1, 26.7 16.9 1.6, 35.5 Namibia 21.6 15.5, 28.8 17.6 8.8, 28.6 17.9 1.4, 36.9 Nigeria 3.9 3.3, 4.5 3.8 1.8, 6.5 4.0 0.3, 9.4 North Koreab 20.1 17.2, 23.0 16.7 8.8, 26.0 17.0 1.4, 34.3 Pakistan 12.4 11.2, 13.3 11.1 5.7, 17.6 11.5 0.8, 24.4 PNGb 26.3 23.4, 29.2 20.7 11.1, 32.8 20.9 1.9, 41.4 Philippines 28.3 27.0, 29.5 21.9 11.9, 32.8 22.1 2.0, 42.3 Russia 39.1 37.8, 40.5 27.9 15.9, 40.4 27.6 2.7, 50.1 Sierra Leone 31.9 22.0, 42.3 23.9 11.9, 37.0 23.9 2.6, 47.0 South Africa 19.4 15.5, 24.1 16.2 8.2, 25.7 16.5 1.5, 34.8 Tanzania 16.3 11.7, 21.3 13.9 6.5, 22.3 14.2 1.2, 30.9 Thailand 24.0 22.8, 25.1 19.3 10.2, 29.0 19.5 1.7, 38.3 Uganda 10.1 7.3, 13.6 9.3 4.3, 15.4 9.6 0.7, 21.4 Vietnam 23.8 22.7, 24.9 19.2 10.2, 29.4 19.4 1.7, 38.4 Zambia 14.6 10.0, 19.5 12.8 6.1, 21.5 13.2 0.9, 28.5 Zimbabwe 14.6 10.8, 18.5 12.6 6.1, 20.4 13.0 0.9, 28.9 Weighted average 21.5 20.2, 23.0 17.7 9.4, 27.0 17.9 1.5, 35.7 Abbreviations: CAR, Central African Republic; CI, confidence interval; DRC, Democratic Republic of Congo; PAP, population attributable proportion; PNG, Papua New Guinea; TB, tuberculosis. a Point estimate and 95% confidence interval for smoking prevalence from World Health Organization reports (20, 21). b 95% confidence intervals were calculated based on the average standard error from the 26 countries. The scatterplot examining ecological trends in country-specific smoking prevalence and PAP for TB disease incidence did not suggest a relationship between 5-year change in smoking prevalence and 5-year change in TB incidence for 26 countries (Web Figure 2). The correlation between 5-year change in smoking prevalence with change in TB incidence was r = 0.05 (P = 0.81). DISCUSSION Overall, we estimated that tobacco smoking accounted for more than 1 of every 6 cases of incident TB disease in the 32 high-TB-burden countries. Similarly, we estimated that tobacco smoking accounted for more than 1 of every 7 TB deaths in these same countries. We estimated that the proportion of TB disease attributable to smoking was more than 6 times higher in men than in women, due to high smoking prevalence among men. Our PAP calculations demonstrate an enormously negative impact of smoking on TB disease and TB death. These findings highlight an urgent need to improve existing efforts to integrate tobacco control initiatives within TB control programs and vice versa. Previous studies from individual countries have estimated the proportion of TB incidence attributable to smoking and reported findings consistent with our results. For example, 17% of TB cases in Taiwan (31) and 14% of TB cases in India (32) were attributable to smoking. Our results aligned with those from a study from Hong Kong that reported that 33% of TB cases were attributable to smoking among men and 9% to smoking among women (8). In most countries, smoking prevalence among TB patients is higher than in the general population. For example, in 2008, 43% of men with active TB disease in Ethiopia were smokers while the population prevalence estimate of smoking among Ethiopian men was 8.1% (33). In South Africa during 2011, 56% of all TB patients were current smokers, and the population smoking prevalence was 19.4% (34). Our PAP estimate was lower than that reported in a 2010 study by Lönnroth et al. (16), who estimated that 21% of incident TB was attributable to smoking among 22 high-TB-burden countries. Our study’s inclusion of 10 more countries than Lönnroth et al. and adjustment for age may partially explain our lower estimate of the proportion of smoking-attributable TB disease. Moreover, Lönnroth et al. used 2008 smoking prevalence data, and the global prevalence of smoking decreased between 2008 and 2014, when our smoking prevalence estimates were made. For example, from 2008 to 2014, smoking prevalence dropped substantially in Russia (−10%, from 49% to 39%) and China (−7%, from 35% to 28%) (16). Although only an ecological-level hypothesis, it is plausible that global reductions in smoking during the past decade contributed to reduced TB incidence. Reductions in smoking prevalence in Russia and China correlated with reductions in TB incidence during the past 10 years. Annual TB incidence rates (per 100,000) decreased from 107 to 84 in Russia and from 97 to 68 in China between 2008 and 2014 (18, 19, 35). Confounding by factors specific to country-level TB dynamics and individual patient-level characteristics could not be accounted for in this ecological analysis and may account for the lack of a strong correlation between 5-year change in smoking prevalence and change in TB disease. Smoking-attributable TB mortality has been previously estimated for individual countries. For example, 25%, 32%, and 35% of TB deaths in men were attributable to smoking in South Korea, India, and Bangladesh, respectively (36–38). In a 2004 study from South Africa, investigators estimated that smoking-attributable TB mortality was 20% in both sexes (39), modestly higher than our estimated 16%, a difference likely due to higher smoking prevalence estimates used in that study. A study from China, published by Jiang et al. in 2009 (40), reported that 22.5% of TB deaths in men and 6.6% in women were attributable to smoking. Although we were unable to stratify our estimate of smoking-attributable TB deaths by sex or age, our estimate of 21.9% of TB deaths due to smoking in China was similar to the 2009 estimate among Chinese males. The biological mechanisms by which tobacco smoking increases susceptibility to pulmonary TB are likely related to alteration in cellular and humoral immune responses (41, 42) in smokers. For example, smokers have altered mucociliary clearance function (43), suppressed alveolar macrophage function (41, 44), increased iron content in the alveolar macrophages (which promotes Mycobacterium tuberculosis growth) (45, 46), and depressed phagocyte activity of monocytes (41, 47). In the context of known biologic mechanisms and numerous observational studies that have reported negative impacts of smoking on TB outcomes (48, 49), our PAP study results suggest that existing efforts in LMIC to integrate smoking cessation in patients with TB are insufficient. To date, randomized controlled trials of smoking-cessation interventions for patients with TB have not been reported, highlighting the lack of progress in evaluating and promoting tailored cessation programs for patients with TB (50). Although tobacco control policies are available worldwide, policy implementation related to TB and smoking in LMIC is inadequate (51). Of the 32 countries in our study, only 28% had evidence-based integrated tobacco guidelines, and only 25% had cessation programs within primary health care (52). Existing efforts to integrate TB and smoking control can be augmented by practical cessation programs supported by existing data and should be rigorously evaluated (53–55). First, because smoking among TB index patients increases the risk of TB infection among their contacts (56), cessation programs for patients with active TB that emphasize the harmful impact of tobacco use on household contacts may improve smoking-cessation adherence. Second, studies suggest that health-care providers who provide TB care often do not believe that smoking has an impact on TB treatment, do not perceive smoking cessation to be a part of TB care, and rarely have formal training in supporting smoking cessation efforts (57, 58). Effective coordination of tobacco cessation within TB control programs will require training for health-care workers to understand the negative impacts of smoking on TB outcomes and how to support patients in their cessation attempts. Our study had limitations. First, this study relied on data reported by WHO for estimates of TB cases and TB mortality. Although an estimated 61% of TB cases were reported to WHO in 2016, only 50% of TB cases were reported among the 32 high-burden countries (1). WHO uses reported TB cases and reported TB deaths to estimate TB incidence and TB mortality; however, the gap between reported and estimated TB cases and TB deaths is vast, especially in LMIC. For example, in 2016 there was a 4.1-million-count difference between reported TB cases (6.3 million) and estimated TB cases (10.4 million). Nonetheless, we believe our estimated TB cases and estimated TB deaths reflect the actual TB burdens due to smoking and that limitations of WHO TB reporting rates did not affect our PAP estimates. Second, TB cases and deaths due to secondhand smoke were not included in our analyses, which may underestimate our estimates of the proportion of smoking-attributable TB disease and death. Third, smoking prevalence measurement and data collection methods varied from country to country, and we did not account for the intensity or duration of smoking. Although most countries used WHO guidelines to collect smoking prevalence data, tobacco use could be underreported, especially for products other than cigarettes, commonly used in developing countries. Fourth, we assumed the relative risk estimates applied for TB disease and TB death were causal (59) and homogeneous across analyses, although the relative effect of smoking on TB disease risk and TB mortality likely varies according to sex, age, and country. Nonetheless, our sensitivity analyses accounted for various relative risk values and did not result in meaningfully different PAP estimates for either TB disease or TB mortality. Despite these limitations, we used current and reliable nationally representative data sources and sensitivity analyses, which improved the validity and generalizability of our estimates. Smoking plays a harmful role in the global TB pandemic, contributing greatly to increased risk of TB disease and TB death in high-TB-burden countries. The considerable impact of smoking on TB epidemics highlights the importance of promoting smoking cessation for people at risk of TB, especially in LMIC where the prevalence of smoking and the risk of TB are highest. Despite improvements in global tobacco control policy, most countries do not have coordinated mechanisms between TB and tobacco-control programs, and tobacco-cessation support for patients with TB is limited. Our findings suggest that increased availability and implementation of smoking-cessation interventions targeted for TB patients will reduce global TB mortality and support the goals of the End TB Strategy. Continued and expanded political commitment and strong coordination among various stakeholders, both globally and nationally, are required to effectively and aggressively enforce tobacco control and ensure that it includes policy that benefits patients with TB. ACKNOWLEDGMENTS Author affiliations: Division of Epidemiology and Biostatistics, School of Public Health, Georgia State University, Atlanta, Georgia (Genet A. Amere, Argita D. Salindri, Matthew J. Magee); Georgia State University’s Tobacco Center of Regulatory Science, School of Public Health, Georgia State University, Atlanta, Georgia (Pratibha Nayak); and Emory Global Diabetes Research Center, Hubert Department of Global Health, Rollins School of Public Health, Emory University, Atlanta, Georgia (K. M. V. Narayan). Research reported in this publication was supported by the National Institute of Allergy and Infectious Diseases of the National Institutes of Health (award R03AI133172). We thank Dr. Ruiyan Luo, Georgia State University, for her support in performing Monte Carlo simulations. We also thank Michelle Ping-Lee D’Amico for her assistance in reviewing the manuscript. Data from these analyses were presented at the 2017 Annual Meeting of the American Public Health Association, November 4–8, 2017, Atlanta, Georgia. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. Conflict of interest: none declared. Abbreviations CI confidence interval LMIC low- and middle-income countries LTBI latent tuberculosis infection PAP population attributable proportion TB tuberculosis WHO World Health Organization REFERENCES 1 World Health Organization . Global Tuberculosis Report 2017. Geneva, Switzerland: World Health Organization; 2017 . http://apps.who.int/iris/bitstream/handle/10665/259366/9789241565516-eng.pdf;jsessionid=8F31CA8593E4A4AE5180663B4797F6E8?sequence=1. 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For permissions, please e-mail: journals.permissions@oup.com. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png American Journal of Epidemiology Oxford University Press

Contribution of Smoking to Tuberculosis Incidence and Mortality in High-Tuberculosis-Burden Countries

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Abstract

Abstract Globally, 10 million incident cases of tuberculosis (TB) are reported annually, and 95% of TB cases and 80% of tobacco users reside in low- and middle-income countries. Smoking approximately doubles the risk of TB disease and TB mortality. We estimated the proportion of annual incident TB cases and TB mortality attributable to tobacco smoking in 32 high-TB-burden countries. We obtained country-specific estimates of TB incidence, TB mortality, and smoking prevalence from the World Health Organization Global TB Report (2017), tobacco surveillance reports (2015), and the Tobacco Atlas. Risk ratios for the effect of smoking on TB incidence and TB mortality were obtained from published meta-analyses. An estimated 17.6% (95% confidence interval (CI): 8.4, 21.4) of TB cases and 15.2% (95% CI: 1.8, 31.9) of TB mortality were attributable to smoking. Among high-TB-burden countries, Russia had the highest proportion of smoking-attributable TB disease (31.6%, 95% CI: 15.9, 37.6) and deaths (28.1%, 95% CI: 3.8, 51.4). Men had a greater proportion of TB cases attributable to smoking (30.3%, 95% CI: 14.7, 36.6) than did women (4.3, 95% CI: 1.7, 5.7). Our findings highlight the need for tobacco control in high-TB-burden countries to combat TB incidence and TB mortality. population attributable fraction, tobacco, tuberculosis Tuberculosis (TB) remains a leading cause of morbidity and mortality worldwide. In 2016, 10.4 million people developed active TB, and 1.3 million died from the disease, accounting for more deaths than any other infectious disease (1, 2). The vast majority of TB disease (87%) occurs in 30 high-burden countries, and 95% of TB cases and deaths occur in low- and middle-income countries (LMIC) (1, 2). The convergence of TB with noncommunicable diseases and tobacco use in LMIC threatens the End TB Strategy and Sustainable Development goals and highlights the need to modify established epidemiologic approaches to TB control (3, 4). Compared with nonsmokers, those who smoke tobacco have twice the risk of TB disease, and patients with TB who smoke have twice the risk of death during TB treatment (5–9). Currently, there are more than 1 billion tobacco users, nearly 80% of whom live in LMIC (10, 11). Separately, active TB and tobacco-related diseases constitute a substantial portion of morbidity and mortality in LMIC, where limited health resources are available to manage these costly diseases (12). However, an improved understanding of the contribution of smoking to TB disease and TB mortality is needed to better characterize the joint impact of smoking and TB on health burdens in LMIC. Although tobacco use is declining in many high-income countries, it is increasing in LMIC (13) where tobacco control policies are not well established (13–15). The extent to which changes in smoking prevalence may affect current efforts to reduce global TB incidence is largely unknown. According to previous reports, an estimated 20% of adult TB cases are attributable to smoking, compared with 16% for human immunodeficiency virus and 15% for diabetes (16, 17). However, previous studies have not estimated the proportion of country-specific TB deaths attributable to smoking in high-TB-burden countries. Furthermore, previous estimates of the proportion of TB cases attributable to smoking were not age- and sex-adjusted and did not include sensitivity analyses to assess bias from smoking-prevalence measurement error. In this study, we provide reliable estimates of the proportion of latent TB infection (LTBI) and TB disease incidence due to tobacco smoking in 32 countries with a high burden of TB. We have also estimated the proportion of TB deaths due to tobacco use. METHODS Data and study population Data from adult male and female individuals aged 15 years or older who lived in 32 high-TB-burden countries were included in the analyses. Thirty high-TB-burden countries were defined by the 2016 World Health Organization (WHO) Global TB Report as the top 20 countries with the highest absolute number of TB cases and the top 10 countries with the highest incidence rates of TB, with at least 10,000 new cases per year (1, 18). We added Uganda and Afghanistan, which were not among the 2016 WHO high-TB-burden countries but were included in 2015 (2, 19). We used 6 population-based cross-sectional data sources for our analyses (Table 1). We obtained TB case notification and TB mortality data from the 2017 WHO Global TB Report (1). Tobacco use data was acquired from the: 1) Global Adult Tobacco Survey (20), 2) WHO Global Report on Trends in Prevalence of Tobacco Smoking 2015 (21), 3) Tobacco Free Initiative country profiles (22), and 4) Tobacco Atlas (23). We obtained population size data from the US Census Bureau (24). Table 1. Epidemiologic Data Sources for Population Attributable Risk Calculations for the Contribution of Smoking to Tuberculosis Incidence and Mortality in High-Tuberculosis-Burden Countries, 2009–2016 Dataa Data Sourcesb Countries Variables Measurement Smoking prevalence Global Adult Tobacco Survey Bangladesh, Brazil, China, India, Indonesia, Nigeria, Pakistan, Philippines, Russia, Thailand, Vietnam Current tobacco smoking Self-reported WHO Global Report on Trends in Prevalence of Tobacco Smoking 2015 Cambodia, Congo, Ethiopia, Kenya, Lesotho, Liberia, Mozambique, Myanmar, Namibia, Sierra Leone, South Africa, Tanzania, Uganda, Zambia, Zimbabwe Current tobacco smoking Self-reported WHO Tobacco Free Initiative North Korea, Papua New Guinea Current tobacco smoking Self-reported Tobacco Atlas Afghanistan, Angola, CAR, DRC Daily tobacco smoking Self-reported TB incidence and TB mortality WHO 2017 TB Report N/A Population United States Census Bureau N/A Dataa Data Sourcesb Countries Variables Measurement Smoking prevalence Global Adult Tobacco Survey Bangladesh, Brazil, China, India, Indonesia, Nigeria, Pakistan, Philippines, Russia, Thailand, Vietnam Current tobacco smoking Self-reported WHO Global Report on Trends in Prevalence of Tobacco Smoking 2015 Cambodia, Congo, Ethiopia, Kenya, Lesotho, Liberia, Mozambique, Myanmar, Namibia, Sierra Leone, South Africa, Tanzania, Uganda, Zambia, Zimbabwe Current tobacco smoking Self-reported WHO Tobacco Free Initiative North Korea, Papua New Guinea Current tobacco smoking Self-reported Tobacco Atlas Afghanistan, Angola, CAR, DRC Daily tobacco smoking Self-reported TB incidence and TB mortality WHO 2017 TB Report N/A Population United States Census Bureau N/A Abbreviations: CAR, Central African Republic; DRC, Democratic Republic of Congo ; N/A, not applicable; TB, tuberculosis; WHO, World Health Organization. a We obtained TB case notification and TB mortality data from the 2017 WHO Global TB Report (1). Tobacco use data was acquired from: 1) Global Adult Tobacco Survey (20), 2) WHO Global Report on Trends in Prevalence of Tobacco Smoking 2015 (21), 3) Tobacco Free Initiative country profiles (22), and 4) the Tobacco Atlas (23). We obtained age- and sex-specific population data from the US Census Bureau (24). b Data sources were chosen in order of priority from the first row to the fourth. Table 1. Epidemiologic Data Sources for Population Attributable Risk Calculations for the Contribution of Smoking to Tuberculosis Incidence and Mortality in High-Tuberculosis-Burden Countries, 2009–2016 Dataa Data Sourcesb Countries Variables Measurement Smoking prevalence Global Adult Tobacco Survey Bangladesh, Brazil, China, India, Indonesia, Nigeria, Pakistan, Philippines, Russia, Thailand, Vietnam Current tobacco smoking Self-reported WHO Global Report on Trends in Prevalence of Tobacco Smoking 2015 Cambodia, Congo, Ethiopia, Kenya, Lesotho, Liberia, Mozambique, Myanmar, Namibia, Sierra Leone, South Africa, Tanzania, Uganda, Zambia, Zimbabwe Current tobacco smoking Self-reported WHO Tobacco Free Initiative North Korea, Papua New Guinea Current tobacco smoking Self-reported Tobacco Atlas Afghanistan, Angola, CAR, DRC Daily tobacco smoking Self-reported TB incidence and TB mortality WHO 2017 TB Report N/A Population United States Census Bureau N/A Dataa Data Sourcesb Countries Variables Measurement Smoking prevalence Global Adult Tobacco Survey Bangladesh, Brazil, China, India, Indonesia, Nigeria, Pakistan, Philippines, Russia, Thailand, Vietnam Current tobacco smoking Self-reported WHO Global Report on Trends in Prevalence of Tobacco Smoking 2015 Cambodia, Congo, Ethiopia, Kenya, Lesotho, Liberia, Mozambique, Myanmar, Namibia, Sierra Leone, South Africa, Tanzania, Uganda, Zambia, Zimbabwe Current tobacco smoking Self-reported WHO Tobacco Free Initiative North Korea, Papua New Guinea Current tobacco smoking Self-reported Tobacco Atlas Afghanistan, Angola, CAR, DRC Daily tobacco smoking Self-reported TB incidence and TB mortality WHO 2017 TB Report N/A Population United States Census Bureau N/A Abbreviations: CAR, Central African Republic; DRC, Democratic Republic of Congo ; N/A, not applicable; TB, tuberculosis; WHO, World Health Organization. a We obtained TB case notification and TB mortality data from the 2017 WHO Global TB Report (1). Tobacco use data was acquired from: 1) Global Adult Tobacco Survey (20), 2) WHO Global Report on Trends in Prevalence of Tobacco Smoking 2015 (21), 3) Tobacco Free Initiative country profiles (22), and 4) the Tobacco Atlas (23). We obtained age- and sex-specific population data from the US Census Bureau (24). b Data sources were chosen in order of priority from the first row to the fourth. The WHO Global TB Report has provided epidemiologic TB surveillance at global and country levels annually since 1997 (2). The Global Adult Tobacco Survey is a household survey, developed in 2007 by the Global Tobacco Surveillance System, which collects nationally representative tobacco-use data among persons aged 15 years or older. The Global Adult Tobacco Survey includes 25 LMIC where tobacco burdens are high (22). The WHO Global Report on Trends in Prevalence of Tobacco Smoking 2015 includes estimated age-specific current tobacco smoking prevalence based on Bayesian hierarchical meta-regression modeling and projected tobacco smoking prevalence trends in WHO regions (21). The Tobacco Free Initiative provides country-specific tobacco surveillance data (22). Tuberculosis incidence and mortality To estimate country-specific TB incidence rates, we obtained TB notification data from the 2017 WHO Global TB Report for the 32 highest TB-burden countries (1). In the absence of directly measured, country-level TB incidence rates, TB case notification rates provide proxy estimates for TB incidence that include notified and undiagnosed TB cases (19). A TB notification indicates that TB has been diagnosed in a patient and reported within the national surveillance system to WHO (25). The TB notification rate comprises the number of new and relapsed TB cases notified in a given year per 100,000 population (25). In 2017, 201 countries reported TB incidence data to WHO (1). We used TB notification rates for our estimates of TB incidence, because it includes sex- and age-specific data. In 2016, notifications of newly diagnosed TB cases represented 61% of estimated incident cases worldwide (1). To determine country-specific rates of TB mortality, we used the reported number of TB deaths where treatment outcome was indicated as TB deaths. A TB death was defined as all-cause mortality during TB treatment (19). We extracted 2015 TB mortality data from the 2017 WHO Global TB Report for all countries except for Angola, for which only 2014 data was available (1). Relative risk for TB disease and TB mortality associated with smoking We obtained relative risk estimates for the associations between smoking and LTBI, between smoking and TB incidence, and between smoking and TB mortality from studies reported by Bates et al. (6), Slama et al. (5), and Lin et al. (26), all in 2007. The relative risk of TB disease in smokers versus nonsmokers was reported to be 2.3 (95% confidence interval (CI): 2.0, 2.8) (6), 2.3 (95% CI: 1.8, 3.0) (5), and 2.0 (95% CI: 1.6, 2.6) (26). The reported relative risk for TB mortality, comparing smokers with nonsmokers, was reported as 2.1 (95% CI: 1.4, 3.4) (6), 2.2 (95% CI: 1.3, 3.7) (5), and 2.0 (95% CI: 1.1, 3.5) (26). For LTBI, we used a relative risk of 1.7 (95% CI: 1.5, 2.0) from Bates et al. (6). We used a relative risk of 2.3 (95% CI: 1.5, 2.8) for smoking-TB disease as reported in 2 systematic reviews (5, 6). For TB mortality, we used a relative risk of 2.0 (95% CI: 1.1, 3.7), comparing smokers with nonsmokers (26). Smoking prevalence Smoking prevalence data were obtained from 4 previously described sources for 32 countries (Table 1). Age- and sex-specific smoking prevalence data were extracted from the Global Adult Tobacco Survey for 11 countries (age-bands (years) reported as 15–24, 25–44, 45–64, ≥65) (22), which was our primary data source, and from the WHO Global Report on Trends in Prevalence of Tobacco Smoking 2015 for 15 countries (age-band (years) reported as 15–24, 25–39, 40–54, 55–69, and ≥70) (21). When country data were unavailable in the primary source, we used the next available data source (Table 1). For countries without age-stratified data, we used Tobacco Free Initiative country profiles and the Tobacco Atlas to estimate smoking prevalence (22, 23). The smoking prevalence data used for this study was based on the definition of current tobacco use, except for Afghanistan, Angola, and the Central African Republic. For Afghanistan, Angola, and the Central African Republic, we used daily tobacco use. Current tobacco use included daily smoking and occasional smoking of any type of smoked tobacco (27, 28). Smoked tobacco included manufactured cigarettes, bidi, hookah (water pipes), hand-rolled cigarettes, pipes of tobacco, cigars, cheroots, cigarillos, dhaba (bamboo water pipes), and any other tobacco products (27). Population data The 2016 age- and sex-specific population data for the 32 highest TB-burden countries were extracted from the US Census Bureau (24). The US Census Bureau estimates the population size of countries by collecting demographic data from censuses, surveys, vital registration, and administrative records (24). Statistical calculations We estimated the proportions of LTBI, TB disease, and TB death due to smoking using standard population attributable proportion (PAP) formulas (29). We first calculated unadjusted estimates of PAP for LTBI, TB disease incidence, and TB mortality for the 32 countries (29). PAP calculations were made using age- and sex-specific smoking prevalence data. For each PAP calculation (LTBI, active TB incidence, and TB mortality) we used estimated country-specific smoking prevalence and respective relative risks comparing smokers with nonsmokers. We used 95% confidence intervals of the relative risks from published estimates (5, 6, 26) to calculate the upper and lower PAP estimates for each country. We estimated excess numbers of active TB cases attributable to smoking for each country in each age and sex stratum by multiplying age- and sex-specific PAPs by the corresponding country-specific reported TB cases from WHO. Numbers of TB deaths attributable to smoking were estimated by multiplying the PAP for each country by the number of reported TB deaths from corresponding countries. Formulas for PAP calculations were: LatentTBInfection=Prevalenceofsmoking(RR−1)/(1+Prevalenceofsmoking(RR−1))WhereRR=RelativeriskofLTBI(1.7,95%CI:1.5,2.0) TBIncidence=Prevalenceofsmoking(RR−1)/(1+Prevalenceofsmoking(RR−1))WhereRR=RelativeriskofTBdisease(2.3,95%CI:1.5,2.8) TBMortality=Prevalenceofsmoking(RR−1)/(1+Prevalenceofsmoking(RR−1))WhereRR=RelativeriskofTBmortality(2.0,95%CI:1.1,3.7) In secondary descriptive ecological analyses, we compared the 5-year change in smoking prevalence with the 5-year change in estimated TB incidence for the 26 countries where smoking prevalence data were available in the same data sets described above (21). We plotted the country-level changes in smoking prevalence and change in TB incidence rate for 2010 and 2015 using a scatter plot. To estimate the relationship between 5-year change in TB incidence and smoking prevalence from 2010 to 2015, we calculated the Pearson correlation coefficient and P value. Sensitivity analysis We used Monte Carlo simulation to measure the amount of systematic error due to uncertainty in the smoking prevalence and relative risk estimates (30). We simulated smoking prevalence for each country using a normal distribution with mean equal to the reported point estimates for each country according to the Global Adult Tobacco Survey and the WHO Global Report on Trends in Prevalence of Tobacco Smoking 2015 and standard deviation derived from the 95% confidence intervals. We reproduced the natural logarithms of the relative risks for TB disease and TB mortality using the normal distribution with corresponding mean of the relative risk and standard deviation derived from the 95% confidence interval around the relative risk (for TB disease, relative risk = 2.3, 95% confidence interval (CI): 1.5, 2.8; for TB mortality, relative risk = 2.0, 95% CI: 1.1, 3.7). The relationships between smoking prevalence and the relative risks were assumed to be independent. The estimated PAPs for TB disease and TB mortality were based on 1,000 Monte Carlo simulations. RESULTS In 2016, an estimated 3.4 billion people over the age of 15 years lived in 32 high-TB-burden countries; in those countries, the estimated number of TB cases and TB deaths that year were 8.3 million and 1.1 million, respectively,. The crude smoking prevalence in the 32 countries was 21.5% (95% CI: 20.2, 23.0), representing 722 million smokers (Web Figure 1A and 1B, available at https://academic.oup.com/aje). Smoking prevalence was higher among men (38.8%) than among women (3.9%). In adults aged 15 years or older, LTBI attributable to smoking was 13.2% (95% CI: 8.8, 17.7). The proportion of LTBI attributable to smoking ranged from 2.8% (95% CI: 1.8, 3.9) in Nigeria to 22.2% (95% CI: 15.2, 28.9) in Russia (Web Table 1). The crude proportion of TB disease incidence attributable to tobacco smoking was 19.6% (95% CI: 8.7, 24.5), and the age-adjusted PAP was 17.6% (95% CI: 8.4, 21.4), accounting for an estimated 1.3 million excess cases each year (Table 2). The country-specific proportion of TB disease attributable to tobacco smoking ranged from 4.7% (95% CI: 1.9, 6.3) in Nigeria to 31.6% (95% CI: 15.9, 37.6) in Russia (Table 2, Web Figure 1C). Smoking-attributable TB disease was higher among men (30.3%) than among women (4.3%) (Table 3). Among men, the proportion of TB disease attributable to smoking ranged from 8.7% in Nigeria to 46.6% in Indonesia. Among women, the proportion ranged from 0.0% in North Korea to 22.0% in Russia (Table 3). Table 2. Estimated Proportion of Tuberculosis Disease Attributable to Tobacco Smoking Among Adults in 32 High-Tuberculosis-Burden Countries, 2009–2016 Country Smoking Prevalencea Crudeb Age-Adjustedc No. of Excess TB Casesd PAP, % 95% CI PAP, % 95% CI Afghanistan 13.0e 14.4 6.1, 18.5 Angola 9.2e 10.7 4.4, 13.9 Bangladesh 23.0 23.0 10.3, 28.7 18.6 9.2, 22.3 59,130 Brazil 17.2 18.3 7.9, 23.1 18.1 7.9, 22.8 14,037 Cambodia 21.2 21.6 9.6, 27.1 18.7 9.0, 22.7 8,422 CAR 8.6e 10.0 4.1, 13.0 China 28.1 26.8 12.3, 33.0 22.4 11.4, 26.6 176,649 Congo 13.9 15.3 6.5, 19.6 13.4 6.1, 16.7 3,195 DRC 6.4 7.7 3.1, 10.1 Ethiopia 4.3 5.3 2.1, 7.0 4.8 2.0, 6.3 7,932 India 14.0 15.4 6.5, 19.7 14.3 6.5, 17.8 363,861 Indonesia 34.8 31.2 14.8, 37.9 24.9 13.2, 29.1 238,368 Kenya 13.5 14.9 6.3, 19.1 13.3 6.0, 16.6 15,758 Lesotho 22.6 22.7 10.2, 28.3 18.7 9.3, 22.3 2,554 Liberia 12.1 13.6 5.7, 17.5 12.6 5.5, 15.8 1,681 Mozambique 18.9 19.7 8.6, 24.9 16.6 7.6, 20.6 24,605 Myanmar 20.0 20.6 9.1, 26.0 20.8 9.7, 25.5 35,727 Namibia 21.6 21.9 9.8, 27.4 20.3 9.3, 25.2 2,622 Nigeria 3.9 4.8 1.9, 6.4 4.7 1.9, 6.3 34,819 North Korea 20.1 20.7 9.1, 26.0 Pakistan 12.4 13.9 5.8, 17.8 12.1 5.5, 15.0 55,900 PNG 26.3 25.5 11.6, 31.5 Philippines 28.3 26.9 12.4, 33.1 24.1 11.7, 29.1 120,731 Russia 39.1 33.7 16.4, 40.6 31.6 15.9, 37.6 26,678 Sierra Leone 31.9 29.3 13.8, 35.8 26.1 12.7, 31.7 5,367 South Africa 19.4 20.1 8.84, 25.4 19.5 8.9, 24.2 72,580 Tanzania 16.3 17.5 7.5, 22.2 10.9 4.8, 13.6 17,471 Thailand 24.0 23.8 10.7, 29.6 23.9 11.5, 29.7 26,345 Uganda 10.1 11.6 4.8, 15.0 10.2 4.4, 13.0 8,078 Vietnam 23.8 23.6 10.6, 29.4 19.7 9.9, 23.5 21,678 Zambia 14.6 16.0 6.8, 20.4 14.0 6.3, 17.5 9,563 Zimbabwe 14.6 16.0 6.8, 20.4 13.9 6.4, 17.2 4,486 Weighted average 21.5 19.6 8.7, 24.5 17.6 8.4, 21.4 1,358,237 Country Smoking Prevalencea Crudeb Age-Adjustedc No. of Excess TB Casesd PAP, % 95% CI PAP, % 95% CI Afghanistan 13.0e 14.4 6.1, 18.5 Angola 9.2e 10.7 4.4, 13.9 Bangladesh 23.0 23.0 10.3, 28.7 18.6 9.2, 22.3 59,130 Brazil 17.2 18.3 7.9, 23.1 18.1 7.9, 22.8 14,037 Cambodia 21.2 21.6 9.6, 27.1 18.7 9.0, 22.7 8,422 CAR 8.6e 10.0 4.1, 13.0 China 28.1 26.8 12.3, 33.0 22.4 11.4, 26.6 176,649 Congo 13.9 15.3 6.5, 19.6 13.4 6.1, 16.7 3,195 DRC 6.4 7.7 3.1, 10.1 Ethiopia 4.3 5.3 2.1, 7.0 4.8 2.0, 6.3 7,932 India 14.0 15.4 6.5, 19.7 14.3 6.5, 17.8 363,861 Indonesia 34.8 31.2 14.8, 37.9 24.9 13.2, 29.1 238,368 Kenya 13.5 14.9 6.3, 19.1 13.3 6.0, 16.6 15,758 Lesotho 22.6 22.7 10.2, 28.3 18.7 9.3, 22.3 2,554 Liberia 12.1 13.6 5.7, 17.5 12.6 5.5, 15.8 1,681 Mozambique 18.9 19.7 8.6, 24.9 16.6 7.6, 20.6 24,605 Myanmar 20.0 20.6 9.1, 26.0 20.8 9.7, 25.5 35,727 Namibia 21.6 21.9 9.8, 27.4 20.3 9.3, 25.2 2,622 Nigeria 3.9 4.8 1.9, 6.4 4.7 1.9, 6.3 34,819 North Korea 20.1 20.7 9.1, 26.0 Pakistan 12.4 13.9 5.8, 17.8 12.1 5.5, 15.0 55,900 PNG 26.3 25.5 11.6, 31.5 Philippines 28.3 26.9 12.4, 33.1 24.1 11.7, 29.1 120,731 Russia 39.1 33.7 16.4, 40.6 31.6 15.9, 37.6 26,678 Sierra Leone 31.9 29.3 13.8, 35.8 26.1 12.7, 31.7 5,367 South Africa 19.4 20.1 8.84, 25.4 19.5 8.9, 24.2 72,580 Tanzania 16.3 17.5 7.5, 22.2 10.9 4.8, 13.6 17,471 Thailand 24.0 23.8 10.7, 29.6 23.9 11.5, 29.7 26,345 Uganda 10.1 11.6 4.8, 15.0 10.2 4.4, 13.0 8,078 Vietnam 23.8 23.6 10.6, 29.4 19.7 9.9, 23.5 21,678 Zambia 14.6 16.0 6.8, 20.4 14.0 6.3, 17.5 9,563 Zimbabwe 14.6 16.0 6.8, 20.4 13.9 6.4, 17.2 4,486 Weighted average 21.5 19.6 8.7, 24.5 17.6 8.4, 21.4 1,358,237 Abbreviations: CAR, Central African Republic; CI, confidence interval; DRC, Democratic Republic of Congo; PAP, population attributable proportion; PNG, Papua New Guinea; TB, tuberculosis. a Current tobacco smoking prevalence. b TB disease incidence based on relative risk of 2.3 (95% CI: 1.5, 2.8) (crude). c TB disease incidence based on relative risk of 2.3 2.3 (95% CI: 1.5, 2.8) (age-adjusted); blank if no age-specific data. d Excess cases based on age-adjusted PAP except for countries with no age-specific data. e Daily smoking prevalence (percentage of population). Table 2. Estimated Proportion of Tuberculosis Disease Attributable to Tobacco Smoking Among Adults in 32 High-Tuberculosis-Burden Countries, 2009–2016 Country Smoking Prevalencea Crudeb Age-Adjustedc No. of Excess TB Casesd PAP, % 95% CI PAP, % 95% CI Afghanistan 13.0e 14.4 6.1, 18.5 Angola 9.2e 10.7 4.4, 13.9 Bangladesh 23.0 23.0 10.3, 28.7 18.6 9.2, 22.3 59,130 Brazil 17.2 18.3 7.9, 23.1 18.1 7.9, 22.8 14,037 Cambodia 21.2 21.6 9.6, 27.1 18.7 9.0, 22.7 8,422 CAR 8.6e 10.0 4.1, 13.0 China 28.1 26.8 12.3, 33.0 22.4 11.4, 26.6 176,649 Congo 13.9 15.3 6.5, 19.6 13.4 6.1, 16.7 3,195 DRC 6.4 7.7 3.1, 10.1 Ethiopia 4.3 5.3 2.1, 7.0 4.8 2.0, 6.3 7,932 India 14.0 15.4 6.5, 19.7 14.3 6.5, 17.8 363,861 Indonesia 34.8 31.2 14.8, 37.9 24.9 13.2, 29.1 238,368 Kenya 13.5 14.9 6.3, 19.1 13.3 6.0, 16.6 15,758 Lesotho 22.6 22.7 10.2, 28.3 18.7 9.3, 22.3 2,554 Liberia 12.1 13.6 5.7, 17.5 12.6 5.5, 15.8 1,681 Mozambique 18.9 19.7 8.6, 24.9 16.6 7.6, 20.6 24,605 Myanmar 20.0 20.6 9.1, 26.0 20.8 9.7, 25.5 35,727 Namibia 21.6 21.9 9.8, 27.4 20.3 9.3, 25.2 2,622 Nigeria 3.9 4.8 1.9, 6.4 4.7 1.9, 6.3 34,819 North Korea 20.1 20.7 9.1, 26.0 Pakistan 12.4 13.9 5.8, 17.8 12.1 5.5, 15.0 55,900 PNG 26.3 25.5 11.6, 31.5 Philippines 28.3 26.9 12.4, 33.1 24.1 11.7, 29.1 120,731 Russia 39.1 33.7 16.4, 40.6 31.6 15.9, 37.6 26,678 Sierra Leone 31.9 29.3 13.8, 35.8 26.1 12.7, 31.7 5,367 South Africa 19.4 20.1 8.84, 25.4 19.5 8.9, 24.2 72,580 Tanzania 16.3 17.5 7.5, 22.2 10.9 4.8, 13.6 17,471 Thailand 24.0 23.8 10.7, 29.6 23.9 11.5, 29.7 26,345 Uganda 10.1 11.6 4.8, 15.0 10.2 4.4, 13.0 8,078 Vietnam 23.8 23.6 10.6, 29.4 19.7 9.9, 23.5 21,678 Zambia 14.6 16.0 6.8, 20.4 14.0 6.3, 17.5 9,563 Zimbabwe 14.6 16.0 6.8, 20.4 13.9 6.4, 17.2 4,486 Weighted average 21.5 19.6 8.7, 24.5 17.6 8.4, 21.4 1,358,237 Country Smoking Prevalencea Crudeb Age-Adjustedc No. of Excess TB Casesd PAP, % 95% CI PAP, % 95% CI Afghanistan 13.0e 14.4 6.1, 18.5 Angola 9.2e 10.7 4.4, 13.9 Bangladesh 23.0 23.0 10.3, 28.7 18.6 9.2, 22.3 59,130 Brazil 17.2 18.3 7.9, 23.1 18.1 7.9, 22.8 14,037 Cambodia 21.2 21.6 9.6, 27.1 18.7 9.0, 22.7 8,422 CAR 8.6e 10.0 4.1, 13.0 China 28.1 26.8 12.3, 33.0 22.4 11.4, 26.6 176,649 Congo 13.9 15.3 6.5, 19.6 13.4 6.1, 16.7 3,195 DRC 6.4 7.7 3.1, 10.1 Ethiopia 4.3 5.3 2.1, 7.0 4.8 2.0, 6.3 7,932 India 14.0 15.4 6.5, 19.7 14.3 6.5, 17.8 363,861 Indonesia 34.8 31.2 14.8, 37.9 24.9 13.2, 29.1 238,368 Kenya 13.5 14.9 6.3, 19.1 13.3 6.0, 16.6 15,758 Lesotho 22.6 22.7 10.2, 28.3 18.7 9.3, 22.3 2,554 Liberia 12.1 13.6 5.7, 17.5 12.6 5.5, 15.8 1,681 Mozambique 18.9 19.7 8.6, 24.9 16.6 7.6, 20.6 24,605 Myanmar 20.0 20.6 9.1, 26.0 20.8 9.7, 25.5 35,727 Namibia 21.6 21.9 9.8, 27.4 20.3 9.3, 25.2 2,622 Nigeria 3.9 4.8 1.9, 6.4 4.7 1.9, 6.3 34,819 North Korea 20.1 20.7 9.1, 26.0 Pakistan 12.4 13.9 5.8, 17.8 12.1 5.5, 15.0 55,900 PNG 26.3 25.5 11.6, 31.5 Philippines 28.3 26.9 12.4, 33.1 24.1 11.7, 29.1 120,731 Russia 39.1 33.7 16.4, 40.6 31.6 15.9, 37.6 26,678 Sierra Leone 31.9 29.3 13.8, 35.8 26.1 12.7, 31.7 5,367 South Africa 19.4 20.1 8.84, 25.4 19.5 8.9, 24.2 72,580 Tanzania 16.3 17.5 7.5, 22.2 10.9 4.8, 13.6 17,471 Thailand 24.0 23.8 10.7, 29.6 23.9 11.5, 29.7 26,345 Uganda 10.1 11.6 4.8, 15.0 10.2 4.4, 13.0 8,078 Vietnam 23.8 23.6 10.6, 29.4 19.7 9.9, 23.5 21,678 Zambia 14.6 16.0 6.8, 20.4 14.0 6.3, 17.5 9,563 Zimbabwe 14.6 16.0 6.8, 20.4 13.9 6.4, 17.2 4,486 Weighted average 21.5 19.6 8.7, 24.5 17.6 8.4, 21.4 1,358,237 Abbreviations: CAR, Central African Republic; CI, confidence interval; DRC, Democratic Republic of Congo; PAP, population attributable proportion; PNG, Papua New Guinea; TB, tuberculosis. a Current tobacco smoking prevalence. b TB disease incidence based on relative risk of 2.3 (95% CI: 1.5, 2.8) (crude). c TB disease incidence based on relative risk of 2.3 2.3 (95% CI: 1.5, 2.8) (age-adjusted); blank if no age-specific data. d Excess cases based on age-adjusted PAP except for countries with no age-specific data. e Daily smoking prevalence (percentage of population). Table 3. Estimated Number and Proportion of Tuberculosis Disease Attributable to Tobacco Smoking According to Sex Among Adults in 32 High-Tuberculosis-Burden Countries, 2009–2016 Country Men Women No. of TB Casesa PAP, % 95% CIb No. of Excess TB Casesc No. of TB Casesa PAP, % 95% CIb No. of Excess TB Casesc Afghanistan 9,004 22.9 10.3, 28.6 2,066 14,519 3.5 1.4, 4.7 510 Angola 14,001 17.8 7.7, 22.6 2,497 9,317 2.0 0.8, 2.7 190 Bangladesh 125,646 36.8 18.3, 43.9 46,179 87,336 1.9 0.7, 2.6 1,670 Brazil 50,383 21.9 9.7, 27.4 11,046 22,537 14.6 6.1, 18.6 3,280 Cambodia 15,089 34.5 16.9, 41.5 5,213 13,171 4.5 1.8, 5.9 589 CAR 5,275 17.1 7.4, 21.8 904 3,574 1.9 0.7, 2.6 68 China 535,618 40.7 20.9, 48.1 218,252 238,185 3.0 1.2, 4.0 7,207 Congo 5,294 25.5 11.6, 31.5 1,349 4,037 2.2 0.8, 2.9 87 DRC 64,101 15.6 6.6, 19.9 9,989 48,684 1.5 0.6, 2.1 748 Ethiopia 61,198 9.5 3.9, 12.4 5,830 48,956 0.6 0.2, 0.9 316 India 1,107,520 24.0 10.8, 29.8 265,875 551,470 3.6 1.4, 4.8 20,035 Indonesia 192,516 46.6 25.1, 54.0 89,621 133,490 3.4 1.3, 4.5 4,527 Kenya 44,799 24.6 11.2, 30.5 11,022 24,865 2.7 1.0, 3.5 661 Lesotho 4,194 37.5 18.8, 44.7 1,574 2,536 0.6 0.2, 0.9 16 Liberia 4,293 23.3 10.5, 29.1 1,001 2,015 3.5 1.4, 4.7 71 Mozambique 33,255 30.0 14.2, 36.6 9,983 29,301 7.3 3.0, 9.6 2,153 Myanmar 67,911 32.9 15.9, 39.8 22,376 37,977 9.6 3.9, 12.5 3,658 Namibia 4,710 30.2 14.3, 36.8 1,423 3,306 12.5 5.2, 16.1 414 Nigeria 57,163 8.7 3.5, 11.3 4,955 34,872 0.5 0.2, 0.7 180 North Korea 61,102 36.3 18.0, 43.4 22,201 35,648 0.0 0.0 0 Pakistan 160,044 22.4 10.0, 28.0 35,844 154,588 2.7 1.0, 3.5 4,108 PNG 2,247 32.7 15.7, 39.5 734 2,095 15.7 6.7, 20.6 332 Philippines 188,226 38.3 19.3, 45.5 72,044 96,016 10.5 4.3, 13.6 10,057 Russia 62,462 43.9 23.1, 51.3 27,422 26,672 22.0 9.8, 27.5 5,869 Sierra Leone 7,195 39.3 20.0, 46.6 2,831 4,477 15.8 6.7, 20.1 706 South Africa 128,842 29.4 13.8, 35.9 37,852 87,642 9.2 3.8, 12.0 8,069 Tanzania 36,162 27.3 12.6, 33.6 9,876 21,973 4.7 1.9, 6.2 1,034 Thailand 46,870 37.7 18.9, 44.9 17,682 22,324 3.3 1.3, 4.4 730 Uganda 26,573 18.6 8.1, 23.5 4,948 12,927 3.4 1.3, 4.5 438 Vietnam 76,979 38.1 19.2, 45.3 29,349 23,275 1.8 0.7, 2.4 416 Zambia 23,197 24.7 11.2, 30.6 5,724 12,960 4.9 2.0, 6.5 641 Zimbabwe 15,436 26.7 12.3, 32.9 4,119 10,349 2.5 1.0, 3.4 262 Weighted averaged 3,237,305 30.3 14.7, 36.6 981,781 1,821,094 4.3 1.7, 5.7 79,042 Country Men Women No. of TB Casesa PAP, % 95% CIb No. of Excess TB Casesc No. of TB Casesa PAP, % 95% CIb No. of Excess TB Casesc Afghanistan 9,004 22.9 10.3, 28.6 2,066 14,519 3.5 1.4, 4.7 510 Angola 14,001 17.8 7.7, 22.6 2,497 9,317 2.0 0.8, 2.7 190 Bangladesh 125,646 36.8 18.3, 43.9 46,179 87,336 1.9 0.7, 2.6 1,670 Brazil 50,383 21.9 9.7, 27.4 11,046 22,537 14.6 6.1, 18.6 3,280 Cambodia 15,089 34.5 16.9, 41.5 5,213 13,171 4.5 1.8, 5.9 589 CAR 5,275 17.1 7.4, 21.8 904 3,574 1.9 0.7, 2.6 68 China 535,618 40.7 20.9, 48.1 218,252 238,185 3.0 1.2, 4.0 7,207 Congo 5,294 25.5 11.6, 31.5 1,349 4,037 2.2 0.8, 2.9 87 DRC 64,101 15.6 6.6, 19.9 9,989 48,684 1.5 0.6, 2.1 748 Ethiopia 61,198 9.5 3.9, 12.4 5,830 48,956 0.6 0.2, 0.9 316 India 1,107,520 24.0 10.8, 29.8 265,875 551,470 3.6 1.4, 4.8 20,035 Indonesia 192,516 46.6 25.1, 54.0 89,621 133,490 3.4 1.3, 4.5 4,527 Kenya 44,799 24.6 11.2, 30.5 11,022 24,865 2.7 1.0, 3.5 661 Lesotho 4,194 37.5 18.8, 44.7 1,574 2,536 0.6 0.2, 0.9 16 Liberia 4,293 23.3 10.5, 29.1 1,001 2,015 3.5 1.4, 4.7 71 Mozambique 33,255 30.0 14.2, 36.6 9,983 29,301 7.3 3.0, 9.6 2,153 Myanmar 67,911 32.9 15.9, 39.8 22,376 37,977 9.6 3.9, 12.5 3,658 Namibia 4,710 30.2 14.3, 36.8 1,423 3,306 12.5 5.2, 16.1 414 Nigeria 57,163 8.7 3.5, 11.3 4,955 34,872 0.5 0.2, 0.7 180 North Korea 61,102 36.3 18.0, 43.4 22,201 35,648 0.0 0.0 0 Pakistan 160,044 22.4 10.0, 28.0 35,844 154,588 2.7 1.0, 3.5 4,108 PNG 2,247 32.7 15.7, 39.5 734 2,095 15.7 6.7, 20.6 332 Philippines 188,226 38.3 19.3, 45.5 72,044 96,016 10.5 4.3, 13.6 10,057 Russia 62,462 43.9 23.1, 51.3 27,422 26,672 22.0 9.8, 27.5 5,869 Sierra Leone 7,195 39.3 20.0, 46.6 2,831 4,477 15.8 6.7, 20.1 706 South Africa 128,842 29.4 13.8, 35.9 37,852 87,642 9.2 3.8, 12.0 8,069 Tanzania 36,162 27.3 12.6, 33.6 9,876 21,973 4.7 1.9, 6.2 1,034 Thailand 46,870 37.7 18.9, 44.9 17,682 22,324 3.3 1.3, 4.4 730 Uganda 26,573 18.6 8.1, 23.5 4,948 12,927 3.4 1.3, 4.5 438 Vietnam 76,979 38.1 19.2, 45.3 29,349 23,275 1.8 0.7, 2.4 416 Zambia 23,197 24.7 11.2, 30.6 5,724 12,960 4.9 2.0, 6.5 641 Zimbabwe 15,436 26.7 12.3, 32.9 4,119 10,349 2.5 1.0, 3.4 262 Weighted averaged 3,237,305 30.3 14.7, 36.6 981,781 1,821,094 4.3 1.7, 5.7 79,042 Abbreviations: CAR, Central African Republic; CI, confidence interval; DRC, Democratic Republic of Congo; PAP, population attributable proportion; PNG, Papua New Guinea; TB, tuberculosis. a Number of TB cases reported in 2016 among men and women in each country. b Confidence interval calculated based on relative risk of 2.3 (95% CI: 1.5, 2.8). c Number of excess TB cases based on reported number of TB cases. d The weighted average calculated based on the number of TB cases. Table 3. Estimated Number and Proportion of Tuberculosis Disease Attributable to Tobacco Smoking According to Sex Among Adults in 32 High-Tuberculosis-Burden Countries, 2009–2016 Country Men Women No. of TB Casesa PAP, % 95% CIb No. of Excess TB Casesc No. of TB Casesa PAP, % 95% CIb No. of Excess TB Casesc Afghanistan 9,004 22.9 10.3, 28.6 2,066 14,519 3.5 1.4, 4.7 510 Angola 14,001 17.8 7.7, 22.6 2,497 9,317 2.0 0.8, 2.7 190 Bangladesh 125,646 36.8 18.3, 43.9 46,179 87,336 1.9 0.7, 2.6 1,670 Brazil 50,383 21.9 9.7, 27.4 11,046 22,537 14.6 6.1, 18.6 3,280 Cambodia 15,089 34.5 16.9, 41.5 5,213 13,171 4.5 1.8, 5.9 589 CAR 5,275 17.1 7.4, 21.8 904 3,574 1.9 0.7, 2.6 68 China 535,618 40.7 20.9, 48.1 218,252 238,185 3.0 1.2, 4.0 7,207 Congo 5,294 25.5 11.6, 31.5 1,349 4,037 2.2 0.8, 2.9 87 DRC 64,101 15.6 6.6, 19.9 9,989 48,684 1.5 0.6, 2.1 748 Ethiopia 61,198 9.5 3.9, 12.4 5,830 48,956 0.6 0.2, 0.9 316 India 1,107,520 24.0 10.8, 29.8 265,875 551,470 3.6 1.4, 4.8 20,035 Indonesia 192,516 46.6 25.1, 54.0 89,621 133,490 3.4 1.3, 4.5 4,527 Kenya 44,799 24.6 11.2, 30.5 11,022 24,865 2.7 1.0, 3.5 661 Lesotho 4,194 37.5 18.8, 44.7 1,574 2,536 0.6 0.2, 0.9 16 Liberia 4,293 23.3 10.5, 29.1 1,001 2,015 3.5 1.4, 4.7 71 Mozambique 33,255 30.0 14.2, 36.6 9,983 29,301 7.3 3.0, 9.6 2,153 Myanmar 67,911 32.9 15.9, 39.8 22,376 37,977 9.6 3.9, 12.5 3,658 Namibia 4,710 30.2 14.3, 36.8 1,423 3,306 12.5 5.2, 16.1 414 Nigeria 57,163 8.7 3.5, 11.3 4,955 34,872 0.5 0.2, 0.7 180 North Korea 61,102 36.3 18.0, 43.4 22,201 35,648 0.0 0.0 0 Pakistan 160,044 22.4 10.0, 28.0 35,844 154,588 2.7 1.0, 3.5 4,108 PNG 2,247 32.7 15.7, 39.5 734 2,095 15.7 6.7, 20.6 332 Philippines 188,226 38.3 19.3, 45.5 72,044 96,016 10.5 4.3, 13.6 10,057 Russia 62,462 43.9 23.1, 51.3 27,422 26,672 22.0 9.8, 27.5 5,869 Sierra Leone 7,195 39.3 20.0, 46.6 2,831 4,477 15.8 6.7, 20.1 706 South Africa 128,842 29.4 13.8, 35.9 37,852 87,642 9.2 3.8, 12.0 8,069 Tanzania 36,162 27.3 12.6, 33.6 9,876 21,973 4.7 1.9, 6.2 1,034 Thailand 46,870 37.7 18.9, 44.9 17,682 22,324 3.3 1.3, 4.4 730 Uganda 26,573 18.6 8.1, 23.5 4,948 12,927 3.4 1.3, 4.5 438 Vietnam 76,979 38.1 19.2, 45.3 29,349 23,275 1.8 0.7, 2.4 416 Zambia 23,197 24.7 11.2, 30.6 5,724 12,960 4.9 2.0, 6.5 641 Zimbabwe 15,436 26.7 12.3, 32.9 4,119 10,349 2.5 1.0, 3.4 262 Weighted averaged 3,237,305 30.3 14.7, 36.6 981,781 1,821,094 4.3 1.7, 5.7 79,042 Country Men Women No. of TB Casesa PAP, % 95% CIb No. of Excess TB Casesc No. of TB Casesa PAP, % 95% CIb No. of Excess TB Casesc Afghanistan 9,004 22.9 10.3, 28.6 2,066 14,519 3.5 1.4, 4.7 510 Angola 14,001 17.8 7.7, 22.6 2,497 9,317 2.0 0.8, 2.7 190 Bangladesh 125,646 36.8 18.3, 43.9 46,179 87,336 1.9 0.7, 2.6 1,670 Brazil 50,383 21.9 9.7, 27.4 11,046 22,537 14.6 6.1, 18.6 3,280 Cambodia 15,089 34.5 16.9, 41.5 5,213 13,171 4.5 1.8, 5.9 589 CAR 5,275 17.1 7.4, 21.8 904 3,574 1.9 0.7, 2.6 68 China 535,618 40.7 20.9, 48.1 218,252 238,185 3.0 1.2, 4.0 7,207 Congo 5,294 25.5 11.6, 31.5 1,349 4,037 2.2 0.8, 2.9 87 DRC 64,101 15.6 6.6, 19.9 9,989 48,684 1.5 0.6, 2.1 748 Ethiopia 61,198 9.5 3.9, 12.4 5,830 48,956 0.6 0.2, 0.9 316 India 1,107,520 24.0 10.8, 29.8 265,875 551,470 3.6 1.4, 4.8 20,035 Indonesia 192,516 46.6 25.1, 54.0 89,621 133,490 3.4 1.3, 4.5 4,527 Kenya 44,799 24.6 11.2, 30.5 11,022 24,865 2.7 1.0, 3.5 661 Lesotho 4,194 37.5 18.8, 44.7 1,574 2,536 0.6 0.2, 0.9 16 Liberia 4,293 23.3 10.5, 29.1 1,001 2,015 3.5 1.4, 4.7 71 Mozambique 33,255 30.0 14.2, 36.6 9,983 29,301 7.3 3.0, 9.6 2,153 Myanmar 67,911 32.9 15.9, 39.8 22,376 37,977 9.6 3.9, 12.5 3,658 Namibia 4,710 30.2 14.3, 36.8 1,423 3,306 12.5 5.2, 16.1 414 Nigeria 57,163 8.7 3.5, 11.3 4,955 34,872 0.5 0.2, 0.7 180 North Korea 61,102 36.3 18.0, 43.4 22,201 35,648 0.0 0.0 0 Pakistan 160,044 22.4 10.0, 28.0 35,844 154,588 2.7 1.0, 3.5 4,108 PNG 2,247 32.7 15.7, 39.5 734 2,095 15.7 6.7, 20.6 332 Philippines 188,226 38.3 19.3, 45.5 72,044 96,016 10.5 4.3, 13.6 10,057 Russia 62,462 43.9 23.1, 51.3 27,422 26,672 22.0 9.8, 27.5 5,869 Sierra Leone 7,195 39.3 20.0, 46.6 2,831 4,477 15.8 6.7, 20.1 706 South Africa 128,842 29.4 13.8, 35.9 37,852 87,642 9.2 3.8, 12.0 8,069 Tanzania 36,162 27.3 12.6, 33.6 9,876 21,973 4.7 1.9, 6.2 1,034 Thailand 46,870 37.7 18.9, 44.9 17,682 22,324 3.3 1.3, 4.4 730 Uganda 26,573 18.6 8.1, 23.5 4,948 12,927 3.4 1.3, 4.5 438 Vietnam 76,979 38.1 19.2, 45.3 29,349 23,275 1.8 0.7, 2.4 416 Zambia 23,197 24.7 11.2, 30.6 5,724 12,960 4.9 2.0, 6.5 641 Zimbabwe 15,436 26.7 12.3, 32.9 4,119 10,349 2.5 1.0, 3.4 262 Weighted averaged 3,237,305 30.3 14.7, 36.6 981,781 1,821,094 4.3 1.7, 5.7 79,042 Abbreviations: CAR, Central African Republic; CI, confidence interval; DRC, Democratic Republic of Congo; PAP, population attributable proportion; PNG, Papua New Guinea; TB, tuberculosis. a Number of TB cases reported in 2016 among men and women in each country. b Confidence interval calculated based on relative risk of 2.3 (95% CI: 1.5, 2.8). c Number of excess TB cases based on reported number of TB cases. d The weighted average calculated based on the number of TB cases. Overall, 15.2% (95% CI: 1.8, 31.9) of TB deaths in adults aged 15 years or older were attributable to tobacco smoking. The proportion of TB deaths attributed to smoking ranged from 3.8% (95% CI: 0.4, 9.5) in Nigeria to 28.1% (95% CI: 3.8, 51.4) in Russia. Russia (28.1%), Indonesia (25.8%), and Sierra Leone (24.2%) were the top 3 countries in terms of proportion of smoking-attributable TB deaths (Table 4). Although the proportions of TB cases (14.3%, 95% CI: 6.5, 17.8) and TB deaths (12.3%, 95% CI: 1.4, 27.4) attributable to tobacco smoking in India were low (ranked 19 and 22, respectively), the absolute number of TB cases and TB deaths were highest. Table 4. Estimated Proportion and Number of TB Deaths Attributable to Tobacco Smoking Among Adults in 32 High-Tuberculosis-Burden Countries, 2009–2016 Country Crude TB Mortalitya No. of Deaths Attributable to Smokingb No. of TB Deathsc Estimated No. of TB Casesd Estimated No. of TB Deathsd PAP, % 95% CI Afghanistan 11.5 1.3, 26.0 62 542 57,000 11,000 Angola 8.4 0.9, 19.9 119 1,417 95,000 18,000 Bangladesh 18.7 2.25, 38.3 1,460 7,806 324,000 66,000 Brazil 14.7 1.7, 31.7 891 6,069 77,000 5,400 Cambodia 17.5 2.1, 36.4 83 475 47,000 3,200 CAR 7.9 0.9, 18.8 17 212 15,900 2,700 China 21.9 2.7, 43.1 1,950 8,890 795,000 50,000 Congo 12.2 1.4, 27.3 16 129 23,100 3,100 DRC 6.0 0.6, 14.7 265 4,413 223,000 53,000 Ethiopia 4.12 0.4, 10.4 153 3,712 158,000 26,000 India 12.3 1.4, 27.4 7,061 57,494 2,557,000 423,000 Indonesia 25.8 3.4, 48.4 2,042 7,908 960,000 110,000 Kenya 11.9 1.3, 26.7 552 4,639 147,000 29,000 Lesotho 18.4 2.2, 38.0 201 1,093 13,600 1,100 Liberia 10.8 1.2, 24.6 31 283 12,600 2,800 Mozambique 15.9 1.9, 33.8 538 3,384 137,000 22,000 Myanmar 16.7 2.0, 35.1 1,087 6,523 169,000 25,000 Namibia 17.8 2.1, 36.8 129 728 13,000 750 Nigeria 3.8 0.4, 9.5 188 5,016 351,000 115,000 North Korea 16.7 2.0, 35.2 469 2,802 116,000 11,000 Pakistan 11.0 1.2, 25.1 488 4,425 467,000 44,000 PNG 20.8 2.6, 41.5 28 134 31,000 3,600 Philippines 22.1 2.8, 43.3 1,470 6,665 502,000 22,000 Russia 28.1 3.8, 51.4 2,259 8,035 84,000 12,000 Sierra Leone 24.2 3.1, 46.3 52 216 19,900 3,400 South Africa 16.3 1.9, 34.4 3,111 19,148 380,000 23,000 Tanzania 14.0 1.6, 30.6 495 3,531 151,000 28,000 Thailand 19.4 2.3, 39.3 918 4,743 110,000 8,600 Uganda 9.2 1.0, 21.4 281 3,058 75,000 11,000 Vietnam 19.2 2.3, 39.1 450 2,340 111,000 13,000 Zambia 12.7 1.4, 28.3 270 2,116 54,000 4,800 Zimbabwe 12.7 1.4, 28.3 328 2,571 31,000 1,200 Weighted averagee 15.2 1.8, 31.9 27,462 180,517 8,307,100 1,152,650 Country Crude TB Mortalitya No. of Deaths Attributable to Smokingb No. of TB Deathsc Estimated No. of TB Casesd Estimated No. of TB Deathsd PAP, % 95% CI Afghanistan 11.5 1.3, 26.0 62 542 57,000 11,000 Angola 8.4 0.9, 19.9 119 1,417 95,000 18,000 Bangladesh 18.7 2.25, 38.3 1,460 7,806 324,000 66,000 Brazil 14.7 1.7, 31.7 891 6,069 77,000 5,400 Cambodia 17.5 2.1, 36.4 83 475 47,000 3,200 CAR 7.9 0.9, 18.8 17 212 15,900 2,700 China 21.9 2.7, 43.1 1,950 8,890 795,000 50,000 Congo 12.2 1.4, 27.3 16 129 23,100 3,100 DRC 6.0 0.6, 14.7 265 4,413 223,000 53,000 Ethiopia 4.12 0.4, 10.4 153 3,712 158,000 26,000 India 12.3 1.4, 27.4 7,061 57,494 2,557,000 423,000 Indonesia 25.8 3.4, 48.4 2,042 7,908 960,000 110,000 Kenya 11.9 1.3, 26.7 552 4,639 147,000 29,000 Lesotho 18.4 2.2, 38.0 201 1,093 13,600 1,100 Liberia 10.8 1.2, 24.6 31 283 12,600 2,800 Mozambique 15.9 1.9, 33.8 538 3,384 137,000 22,000 Myanmar 16.7 2.0, 35.1 1,087 6,523 169,000 25,000 Namibia 17.8 2.1, 36.8 129 728 13,000 750 Nigeria 3.8 0.4, 9.5 188 5,016 351,000 115,000 North Korea 16.7 2.0, 35.2 469 2,802 116,000 11,000 Pakistan 11.0 1.2, 25.1 488 4,425 467,000 44,000 PNG 20.8 2.6, 41.5 28 134 31,000 3,600 Philippines 22.1 2.8, 43.3 1,470 6,665 502,000 22,000 Russia 28.1 3.8, 51.4 2,259 8,035 84,000 12,000 Sierra Leone 24.2 3.1, 46.3 52 216 19,900 3,400 South Africa 16.3 1.9, 34.4 3,111 19,148 380,000 23,000 Tanzania 14.0 1.6, 30.6 495 3,531 151,000 28,000 Thailand 19.4 2.3, 39.3 918 4,743 110,000 8,600 Uganda 9.2 1.0, 21.4 281 3,058 75,000 11,000 Vietnam 19.2 2.3, 39.1 450 2,340 111,000 13,000 Zambia 12.7 1.4, 28.3 270 2,116 54,000 4,800 Zimbabwe 12.7 1.4, 28.3 328 2,571 31,000 1,200 Weighted averagee 15.2 1.8, 31.9 27,462 180,517 8,307,100 1,152,650 Abbreviations: CAR, Central African Republic; CI, confidence interval; DRC, Democratic Republic of Congo; PAP, population attributable proportion; PNG, Papua New Guinea; TB, tuberculosis. a TB death attributable to smoking calculated based on relative risk of 2.0 (95% CI: 1.1, 3.7). b Excess TB death based on reported TB deaths. c Number of reported TB deaths in 2015. d Estimated number of TB cases (2016) and deaths (2015). e The weighted average calculated based on the number of TB deaths. Table 4. Estimated Proportion and Number of TB Deaths Attributable to Tobacco Smoking Among Adults in 32 High-Tuberculosis-Burden Countries, 2009–2016 Country Crude TB Mortalitya No. of Deaths Attributable to Smokingb No. of TB Deathsc Estimated No. of TB Casesd Estimated No. of TB Deathsd PAP, % 95% CI Afghanistan 11.5 1.3, 26.0 62 542 57,000 11,000 Angola 8.4 0.9, 19.9 119 1,417 95,000 18,000 Bangladesh 18.7 2.25, 38.3 1,460 7,806 324,000 66,000 Brazil 14.7 1.7, 31.7 891 6,069 77,000 5,400 Cambodia 17.5 2.1, 36.4 83 475 47,000 3,200 CAR 7.9 0.9, 18.8 17 212 15,900 2,700 China 21.9 2.7, 43.1 1,950 8,890 795,000 50,000 Congo 12.2 1.4, 27.3 16 129 23,100 3,100 DRC 6.0 0.6, 14.7 265 4,413 223,000 53,000 Ethiopia 4.12 0.4, 10.4 153 3,712 158,000 26,000 India 12.3 1.4, 27.4 7,061 57,494 2,557,000 423,000 Indonesia 25.8 3.4, 48.4 2,042 7,908 960,000 110,000 Kenya 11.9 1.3, 26.7 552 4,639 147,000 29,000 Lesotho 18.4 2.2, 38.0 201 1,093 13,600 1,100 Liberia 10.8 1.2, 24.6 31 283 12,600 2,800 Mozambique 15.9 1.9, 33.8 538 3,384 137,000 22,000 Myanmar 16.7 2.0, 35.1 1,087 6,523 169,000 25,000 Namibia 17.8 2.1, 36.8 129 728 13,000 750 Nigeria 3.8 0.4, 9.5 188 5,016 351,000 115,000 North Korea 16.7 2.0, 35.2 469 2,802 116,000 11,000 Pakistan 11.0 1.2, 25.1 488 4,425 467,000 44,000 PNG 20.8 2.6, 41.5 28 134 31,000 3,600 Philippines 22.1 2.8, 43.3 1,470 6,665 502,000 22,000 Russia 28.1 3.8, 51.4 2,259 8,035 84,000 12,000 Sierra Leone 24.2 3.1, 46.3 52 216 19,900 3,400 South Africa 16.3 1.9, 34.4 3,111 19,148 380,000 23,000 Tanzania 14.0 1.6, 30.6 495 3,531 151,000 28,000 Thailand 19.4 2.3, 39.3 918 4,743 110,000 8,600 Uganda 9.2 1.0, 21.4 281 3,058 75,000 11,000 Vietnam 19.2 2.3, 39.1 450 2,340 111,000 13,000 Zambia 12.7 1.4, 28.3 270 2,116 54,000 4,800 Zimbabwe 12.7 1.4, 28.3 328 2,571 31,000 1,200 Weighted averagee 15.2 1.8, 31.9 27,462 180,517 8,307,100 1,152,650 Country Crude TB Mortalitya No. of Deaths Attributable to Smokingb No. of TB Deathsc Estimated No. of TB Casesd Estimated No. of TB Deathsd PAP, % 95% CI Afghanistan 11.5 1.3, 26.0 62 542 57,000 11,000 Angola 8.4 0.9, 19.9 119 1,417 95,000 18,000 Bangladesh 18.7 2.25, 38.3 1,460 7,806 324,000 66,000 Brazil 14.7 1.7, 31.7 891 6,069 77,000 5,400 Cambodia 17.5 2.1, 36.4 83 475 47,000 3,200 CAR 7.9 0.9, 18.8 17 212 15,900 2,700 China 21.9 2.7, 43.1 1,950 8,890 795,000 50,000 Congo 12.2 1.4, 27.3 16 129 23,100 3,100 DRC 6.0 0.6, 14.7 265 4,413 223,000 53,000 Ethiopia 4.12 0.4, 10.4 153 3,712 158,000 26,000 India 12.3 1.4, 27.4 7,061 57,494 2,557,000 423,000 Indonesia 25.8 3.4, 48.4 2,042 7,908 960,000 110,000 Kenya 11.9 1.3, 26.7 552 4,639 147,000 29,000 Lesotho 18.4 2.2, 38.0 201 1,093 13,600 1,100 Liberia 10.8 1.2, 24.6 31 283 12,600 2,800 Mozambique 15.9 1.9, 33.8 538 3,384 137,000 22,000 Myanmar 16.7 2.0, 35.1 1,087 6,523 169,000 25,000 Namibia 17.8 2.1, 36.8 129 728 13,000 750 Nigeria 3.8 0.4, 9.5 188 5,016 351,000 115,000 North Korea 16.7 2.0, 35.2 469 2,802 116,000 11,000 Pakistan 11.0 1.2, 25.1 488 4,425 467,000 44,000 PNG 20.8 2.6, 41.5 28 134 31,000 3,600 Philippines 22.1 2.8, 43.3 1,470 6,665 502,000 22,000 Russia 28.1 3.8, 51.4 2,259 8,035 84,000 12,000 Sierra Leone 24.2 3.1, 46.3 52 216 19,900 3,400 South Africa 16.3 1.9, 34.4 3,111 19,148 380,000 23,000 Tanzania 14.0 1.6, 30.6 495 3,531 151,000 28,000 Thailand 19.4 2.3, 39.3 918 4,743 110,000 8,600 Uganda 9.2 1.0, 21.4 281 3,058 75,000 11,000 Vietnam 19.2 2.3, 39.1 450 2,340 111,000 13,000 Zambia 12.7 1.4, 28.3 270 2,116 54,000 4,800 Zimbabwe 12.7 1.4, 28.3 328 2,571 31,000 1,200 Weighted averagee 15.2 1.8, 31.9 27,462 180,517 8,307,100 1,152,650 Abbreviations: CAR, Central African Republic; CI, confidence interval; DRC, Democratic Republic of Congo; PAP, population attributable proportion; PNG, Papua New Guinea; TB, tuberculosis. a TB death attributable to smoking calculated based on relative risk of 2.0 (95% CI: 1.1, 3.7). b Excess TB death based on reported TB deaths. c Number of reported TB deaths in 2015. d Estimated number of TB cases (2016) and deaths (2015). e The weighted average calculated based on the number of TB deaths. In Monte Carlo simulation to estimate smoking prevalence misclassification and relative risk misspecification, the proportions of TB disease and TB death attributable to smoking were 17.7% (95% CI: 9.4, 27.0) and 17.9% (95% CI: 1.5, 35.7), respectively (Table 5). Table 5. Sensitivity Analysis for Proportion of TB Disease and Deaths, Among Adults in 32 High-Tuberculosis-Burden Countries, Attributable to Tobacco Smoking Based on Monte Carlo Analysis, 2009–2016 Country Smoking Prevalence TB Disease TB Mortality Point Estimate, %a 95% CIa PAP, % 95% CI PAP, % 95% CI Afghanistanb 13.0 10.0, 15.9 11.5 5.6, 18.7 11.9 1.0, 25.9 Angolab 9.2 6.2, 12.2 8.4 3.5, 14.4 8.7 0.5, 20.4 Bangladesh 23.0 21.9, 24.2 18.6 10.0, 28.3 18.9 1.6, 37.2 Brazil 17.2 16.7, 17.7 14.7 7.7, 22.4 15.0 1.2, 30.8 Cambodia 21.2 16.2, 27.3 17.5 9.2, 27.2 17.9 1.8, 36.2 CARb 8.6 5.6, 11.5 7.9 3.5, 13.7 8.2 0.6, 19.7 China 28.1 26.7, 29.7 21.8 11.9, 32.7 21.9 2.0, 42.4 Congo 13.9 9.9, 18.3 12.1 5.5, 19.8 12.5 1.0, 27.5 DRCb 6.4 3.5, 9.3 6.1 2.4, 11.3 6.3 0.4, 15.2 Ethiopia 4.3 3.0, 5.6 4.2 1.8, 7.3 4.4 0.3, 10.5 India 14.0 13.4, 14.6 12.3 6.4, 19.4 12.7 1.0, 27.2 Indonesia 34.8 33.2, 36.4 25.7 14.2, 37.3 25.8 3.1, 48.5 Kenya 13.5 9.9, 17.3 11.9 5.8, 19.6 12.3 1.0, 26.2 Lesotho 22.6 16.6, 29.4 18.3 9.2, 28.5 18.6 1.5, 38.0 Liberia 12.1 6.5, 20.8 10.7 3.6, 20.4 11.0 0.7, 26.2 Mozambique 18.9 12.2, 27.7 15.8 7.2, 26.6 16.0 1.5, 33.5 Myanmar 20.0 16.1, 29.6 16.6 8.1, 26.7 16.9 1.6, 35.5 Namibia 21.6 15.5, 28.8 17.6 8.8, 28.6 17.9 1.4, 36.9 Nigeria 3.9 3.3, 4.5 3.8 1.8, 6.5 4.0 0.3, 9.4 North Koreab 20.1 17.2, 23.0 16.7 8.8, 26.0 17.0 1.4, 34.3 Pakistan 12.4 11.2, 13.3 11.1 5.7, 17.6 11.5 0.8, 24.4 PNGb 26.3 23.4, 29.2 20.7 11.1, 32.8 20.9 1.9, 41.4 Philippines 28.3 27.0, 29.5 21.9 11.9, 32.8 22.1 2.0, 42.3 Russia 39.1 37.8, 40.5 27.9 15.9, 40.4 27.6 2.7, 50.1 Sierra Leone 31.9 22.0, 42.3 23.9 11.9, 37.0 23.9 2.6, 47.0 South Africa 19.4 15.5, 24.1 16.2 8.2, 25.7 16.5 1.5, 34.8 Tanzania 16.3 11.7, 21.3 13.9 6.5, 22.3 14.2 1.2, 30.9 Thailand 24.0 22.8, 25.1 19.3 10.2, 29.0 19.5 1.7, 38.3 Uganda 10.1 7.3, 13.6 9.3 4.3, 15.4 9.6 0.7, 21.4 Vietnam 23.8 22.7, 24.9 19.2 10.2, 29.4 19.4 1.7, 38.4 Zambia 14.6 10.0, 19.5 12.8 6.1, 21.5 13.2 0.9, 28.5 Zimbabwe 14.6 10.8, 18.5 12.6 6.1, 20.4 13.0 0.9, 28.9 Weighted average 21.5 20.2, 23.0 17.7 9.4, 27.0 17.9 1.5, 35.7 Country Smoking Prevalence TB Disease TB Mortality Point Estimate, %a 95% CIa PAP, % 95% CI PAP, % 95% CI Afghanistanb 13.0 10.0, 15.9 11.5 5.6, 18.7 11.9 1.0, 25.9 Angolab 9.2 6.2, 12.2 8.4 3.5, 14.4 8.7 0.5, 20.4 Bangladesh 23.0 21.9, 24.2 18.6 10.0, 28.3 18.9 1.6, 37.2 Brazil 17.2 16.7, 17.7 14.7 7.7, 22.4 15.0 1.2, 30.8 Cambodia 21.2 16.2, 27.3 17.5 9.2, 27.2 17.9 1.8, 36.2 CARb 8.6 5.6, 11.5 7.9 3.5, 13.7 8.2 0.6, 19.7 China 28.1 26.7, 29.7 21.8 11.9, 32.7 21.9 2.0, 42.4 Congo 13.9 9.9, 18.3 12.1 5.5, 19.8 12.5 1.0, 27.5 DRCb 6.4 3.5, 9.3 6.1 2.4, 11.3 6.3 0.4, 15.2 Ethiopia 4.3 3.0, 5.6 4.2 1.8, 7.3 4.4 0.3, 10.5 India 14.0 13.4, 14.6 12.3 6.4, 19.4 12.7 1.0, 27.2 Indonesia 34.8 33.2, 36.4 25.7 14.2, 37.3 25.8 3.1, 48.5 Kenya 13.5 9.9, 17.3 11.9 5.8, 19.6 12.3 1.0, 26.2 Lesotho 22.6 16.6, 29.4 18.3 9.2, 28.5 18.6 1.5, 38.0 Liberia 12.1 6.5, 20.8 10.7 3.6, 20.4 11.0 0.7, 26.2 Mozambique 18.9 12.2, 27.7 15.8 7.2, 26.6 16.0 1.5, 33.5 Myanmar 20.0 16.1, 29.6 16.6 8.1, 26.7 16.9 1.6, 35.5 Namibia 21.6 15.5, 28.8 17.6 8.8, 28.6 17.9 1.4, 36.9 Nigeria 3.9 3.3, 4.5 3.8 1.8, 6.5 4.0 0.3, 9.4 North Koreab 20.1 17.2, 23.0 16.7 8.8, 26.0 17.0 1.4, 34.3 Pakistan 12.4 11.2, 13.3 11.1 5.7, 17.6 11.5 0.8, 24.4 PNGb 26.3 23.4, 29.2 20.7 11.1, 32.8 20.9 1.9, 41.4 Philippines 28.3 27.0, 29.5 21.9 11.9, 32.8 22.1 2.0, 42.3 Russia 39.1 37.8, 40.5 27.9 15.9, 40.4 27.6 2.7, 50.1 Sierra Leone 31.9 22.0, 42.3 23.9 11.9, 37.0 23.9 2.6, 47.0 South Africa 19.4 15.5, 24.1 16.2 8.2, 25.7 16.5 1.5, 34.8 Tanzania 16.3 11.7, 21.3 13.9 6.5, 22.3 14.2 1.2, 30.9 Thailand 24.0 22.8, 25.1 19.3 10.2, 29.0 19.5 1.7, 38.3 Uganda 10.1 7.3, 13.6 9.3 4.3, 15.4 9.6 0.7, 21.4 Vietnam 23.8 22.7, 24.9 19.2 10.2, 29.4 19.4 1.7, 38.4 Zambia 14.6 10.0, 19.5 12.8 6.1, 21.5 13.2 0.9, 28.5 Zimbabwe 14.6 10.8, 18.5 12.6 6.1, 20.4 13.0 0.9, 28.9 Weighted average 21.5 20.2, 23.0 17.7 9.4, 27.0 17.9 1.5, 35.7 Abbreviations: CAR, Central African Republic; CI, confidence interval; DRC, Democratic Republic of Congo; PAP, population attributable proportion; PNG, Papua New Guinea; TB, tuberculosis. a Point estimate and 95% confidence interval for smoking prevalence from World Health Organization reports (20, 21). b 95% confidence intervals were calculated based on the average standard error from the 26 countries. Table 5. Sensitivity Analysis for Proportion of TB Disease and Deaths, Among Adults in 32 High-Tuberculosis-Burden Countries, Attributable to Tobacco Smoking Based on Monte Carlo Analysis, 2009–2016 Country Smoking Prevalence TB Disease TB Mortality Point Estimate, %a 95% CIa PAP, % 95% CI PAP, % 95% CI Afghanistanb 13.0 10.0, 15.9 11.5 5.6, 18.7 11.9 1.0, 25.9 Angolab 9.2 6.2, 12.2 8.4 3.5, 14.4 8.7 0.5, 20.4 Bangladesh 23.0 21.9, 24.2 18.6 10.0, 28.3 18.9 1.6, 37.2 Brazil 17.2 16.7, 17.7 14.7 7.7, 22.4 15.0 1.2, 30.8 Cambodia 21.2 16.2, 27.3 17.5 9.2, 27.2 17.9 1.8, 36.2 CARb 8.6 5.6, 11.5 7.9 3.5, 13.7 8.2 0.6, 19.7 China 28.1 26.7, 29.7 21.8 11.9, 32.7 21.9 2.0, 42.4 Congo 13.9 9.9, 18.3 12.1 5.5, 19.8 12.5 1.0, 27.5 DRCb 6.4 3.5, 9.3 6.1 2.4, 11.3 6.3 0.4, 15.2 Ethiopia 4.3 3.0, 5.6 4.2 1.8, 7.3 4.4 0.3, 10.5 India 14.0 13.4, 14.6 12.3 6.4, 19.4 12.7 1.0, 27.2 Indonesia 34.8 33.2, 36.4 25.7 14.2, 37.3 25.8 3.1, 48.5 Kenya 13.5 9.9, 17.3 11.9 5.8, 19.6 12.3 1.0, 26.2 Lesotho 22.6 16.6, 29.4 18.3 9.2, 28.5 18.6 1.5, 38.0 Liberia 12.1 6.5, 20.8 10.7 3.6, 20.4 11.0 0.7, 26.2 Mozambique 18.9 12.2, 27.7 15.8 7.2, 26.6 16.0 1.5, 33.5 Myanmar 20.0 16.1, 29.6 16.6 8.1, 26.7 16.9 1.6, 35.5 Namibia 21.6 15.5, 28.8 17.6 8.8, 28.6 17.9 1.4, 36.9 Nigeria 3.9 3.3, 4.5 3.8 1.8, 6.5 4.0 0.3, 9.4 North Koreab 20.1 17.2, 23.0 16.7 8.8, 26.0 17.0 1.4, 34.3 Pakistan 12.4 11.2, 13.3 11.1 5.7, 17.6 11.5 0.8, 24.4 PNGb 26.3 23.4, 29.2 20.7 11.1, 32.8 20.9 1.9, 41.4 Philippines 28.3 27.0, 29.5 21.9 11.9, 32.8 22.1 2.0, 42.3 Russia 39.1 37.8, 40.5 27.9 15.9, 40.4 27.6 2.7, 50.1 Sierra Leone 31.9 22.0, 42.3 23.9 11.9, 37.0 23.9 2.6, 47.0 South Africa 19.4 15.5, 24.1 16.2 8.2, 25.7 16.5 1.5, 34.8 Tanzania 16.3 11.7, 21.3 13.9 6.5, 22.3 14.2 1.2, 30.9 Thailand 24.0 22.8, 25.1 19.3 10.2, 29.0 19.5 1.7, 38.3 Uganda 10.1 7.3, 13.6 9.3 4.3, 15.4 9.6 0.7, 21.4 Vietnam 23.8 22.7, 24.9 19.2 10.2, 29.4 19.4 1.7, 38.4 Zambia 14.6 10.0, 19.5 12.8 6.1, 21.5 13.2 0.9, 28.5 Zimbabwe 14.6 10.8, 18.5 12.6 6.1, 20.4 13.0 0.9, 28.9 Weighted average 21.5 20.2, 23.0 17.7 9.4, 27.0 17.9 1.5, 35.7 Country Smoking Prevalence TB Disease TB Mortality Point Estimate, %a 95% CIa PAP, % 95% CI PAP, % 95% CI Afghanistanb 13.0 10.0, 15.9 11.5 5.6, 18.7 11.9 1.0, 25.9 Angolab 9.2 6.2, 12.2 8.4 3.5, 14.4 8.7 0.5, 20.4 Bangladesh 23.0 21.9, 24.2 18.6 10.0, 28.3 18.9 1.6, 37.2 Brazil 17.2 16.7, 17.7 14.7 7.7, 22.4 15.0 1.2, 30.8 Cambodia 21.2 16.2, 27.3 17.5 9.2, 27.2 17.9 1.8, 36.2 CARb 8.6 5.6, 11.5 7.9 3.5, 13.7 8.2 0.6, 19.7 China 28.1 26.7, 29.7 21.8 11.9, 32.7 21.9 2.0, 42.4 Congo 13.9 9.9, 18.3 12.1 5.5, 19.8 12.5 1.0, 27.5 DRCb 6.4 3.5, 9.3 6.1 2.4, 11.3 6.3 0.4, 15.2 Ethiopia 4.3 3.0, 5.6 4.2 1.8, 7.3 4.4 0.3, 10.5 India 14.0 13.4, 14.6 12.3 6.4, 19.4 12.7 1.0, 27.2 Indonesia 34.8 33.2, 36.4 25.7 14.2, 37.3 25.8 3.1, 48.5 Kenya 13.5 9.9, 17.3 11.9 5.8, 19.6 12.3 1.0, 26.2 Lesotho 22.6 16.6, 29.4 18.3 9.2, 28.5 18.6 1.5, 38.0 Liberia 12.1 6.5, 20.8 10.7 3.6, 20.4 11.0 0.7, 26.2 Mozambique 18.9 12.2, 27.7 15.8 7.2, 26.6 16.0 1.5, 33.5 Myanmar 20.0 16.1, 29.6 16.6 8.1, 26.7 16.9 1.6, 35.5 Namibia 21.6 15.5, 28.8 17.6 8.8, 28.6 17.9 1.4, 36.9 Nigeria 3.9 3.3, 4.5 3.8 1.8, 6.5 4.0 0.3, 9.4 North Koreab 20.1 17.2, 23.0 16.7 8.8, 26.0 17.0 1.4, 34.3 Pakistan 12.4 11.2, 13.3 11.1 5.7, 17.6 11.5 0.8, 24.4 PNGb 26.3 23.4, 29.2 20.7 11.1, 32.8 20.9 1.9, 41.4 Philippines 28.3 27.0, 29.5 21.9 11.9, 32.8 22.1 2.0, 42.3 Russia 39.1 37.8, 40.5 27.9 15.9, 40.4 27.6 2.7, 50.1 Sierra Leone 31.9 22.0, 42.3 23.9 11.9, 37.0 23.9 2.6, 47.0 South Africa 19.4 15.5, 24.1 16.2 8.2, 25.7 16.5 1.5, 34.8 Tanzania 16.3 11.7, 21.3 13.9 6.5, 22.3 14.2 1.2, 30.9 Thailand 24.0 22.8, 25.1 19.3 10.2, 29.0 19.5 1.7, 38.3 Uganda 10.1 7.3, 13.6 9.3 4.3, 15.4 9.6 0.7, 21.4 Vietnam 23.8 22.7, 24.9 19.2 10.2, 29.4 19.4 1.7, 38.4 Zambia 14.6 10.0, 19.5 12.8 6.1, 21.5 13.2 0.9, 28.5 Zimbabwe 14.6 10.8, 18.5 12.6 6.1, 20.4 13.0 0.9, 28.9 Weighted average 21.5 20.2, 23.0 17.7 9.4, 27.0 17.9 1.5, 35.7 Abbreviations: CAR, Central African Republic; CI, confidence interval; DRC, Democratic Republic of Congo; PAP, population attributable proportion; PNG, Papua New Guinea; TB, tuberculosis. a Point estimate and 95% confidence interval for smoking prevalence from World Health Organization reports (20, 21). b 95% confidence intervals were calculated based on the average standard error from the 26 countries. The scatterplot examining ecological trends in country-specific smoking prevalence and PAP for TB disease incidence did not suggest a relationship between 5-year change in smoking prevalence and 5-year change in TB incidence for 26 countries (Web Figure 2). The correlation between 5-year change in smoking prevalence with change in TB incidence was r = 0.05 (P = 0.81). DISCUSSION Overall, we estimated that tobacco smoking accounted for more than 1 of every 6 cases of incident TB disease in the 32 high-TB-burden countries. Similarly, we estimated that tobacco smoking accounted for more than 1 of every 7 TB deaths in these same countries. We estimated that the proportion of TB disease attributable to smoking was more than 6 times higher in men than in women, due to high smoking prevalence among men. Our PAP calculations demonstrate an enormously negative impact of smoking on TB disease and TB death. These findings highlight an urgent need to improve existing efforts to integrate tobacco control initiatives within TB control programs and vice versa. Previous studies from individual countries have estimated the proportion of TB incidence attributable to smoking and reported findings consistent with our results. For example, 17% of TB cases in Taiwan (31) and 14% of TB cases in India (32) were attributable to smoking. Our results aligned with those from a study from Hong Kong that reported that 33% of TB cases were attributable to smoking among men and 9% to smoking among women (8). In most countries, smoking prevalence among TB patients is higher than in the general population. For example, in 2008, 43% of men with active TB disease in Ethiopia were smokers while the population prevalence estimate of smoking among Ethiopian men was 8.1% (33). In South Africa during 2011, 56% of all TB patients were current smokers, and the population smoking prevalence was 19.4% (34). Our PAP estimate was lower than that reported in a 2010 study by Lönnroth et al. (16), who estimated that 21% of incident TB was attributable to smoking among 22 high-TB-burden countries. Our study’s inclusion of 10 more countries than Lönnroth et al. and adjustment for age may partially explain our lower estimate of the proportion of smoking-attributable TB disease. Moreover, Lönnroth et al. used 2008 smoking prevalence data, and the global prevalence of smoking decreased between 2008 and 2014, when our smoking prevalence estimates were made. For example, from 2008 to 2014, smoking prevalence dropped substantially in Russia (−10%, from 49% to 39%) and China (−7%, from 35% to 28%) (16). Although only an ecological-level hypothesis, it is plausible that global reductions in smoking during the past decade contributed to reduced TB incidence. Reductions in smoking prevalence in Russia and China correlated with reductions in TB incidence during the past 10 years. Annual TB incidence rates (per 100,000) decreased from 107 to 84 in Russia and from 97 to 68 in China between 2008 and 2014 (18, 19, 35). Confounding by factors specific to country-level TB dynamics and individual patient-level characteristics could not be accounted for in this ecological analysis and may account for the lack of a strong correlation between 5-year change in smoking prevalence and change in TB disease. Smoking-attributable TB mortality has been previously estimated for individual countries. For example, 25%, 32%, and 35% of TB deaths in men were attributable to smoking in South Korea, India, and Bangladesh, respectively (36–38). In a 2004 study from South Africa, investigators estimated that smoking-attributable TB mortality was 20% in both sexes (39), modestly higher than our estimated 16%, a difference likely due to higher smoking prevalence estimates used in that study. A study from China, published by Jiang et al. in 2009 (40), reported that 22.5% of TB deaths in men and 6.6% in women were attributable to smoking. Although we were unable to stratify our estimate of smoking-attributable TB deaths by sex or age, our estimate of 21.9% of TB deaths due to smoking in China was similar to the 2009 estimate among Chinese males. The biological mechanisms by which tobacco smoking increases susceptibility to pulmonary TB are likely related to alteration in cellular and humoral immune responses (41, 42) in smokers. For example, smokers have altered mucociliary clearance function (43), suppressed alveolar macrophage function (41, 44), increased iron content in the alveolar macrophages (which promotes Mycobacterium tuberculosis growth) (45, 46), and depressed phagocyte activity of monocytes (41, 47). In the context of known biologic mechanisms and numerous observational studies that have reported negative impacts of smoking on TB outcomes (48, 49), our PAP study results suggest that existing efforts in LMIC to integrate smoking cessation in patients with TB are insufficient. To date, randomized controlled trials of smoking-cessation interventions for patients with TB have not been reported, highlighting the lack of progress in evaluating and promoting tailored cessation programs for patients with TB (50). Although tobacco control policies are available worldwide, policy implementation related to TB and smoking in LMIC is inadequate (51). Of the 32 countries in our study, only 28% had evidence-based integrated tobacco guidelines, and only 25% had cessation programs within primary health care (52). Existing efforts to integrate TB and smoking control can be augmented by practical cessation programs supported by existing data and should be rigorously evaluated (53–55). First, because smoking among TB index patients increases the risk of TB infection among their contacts (56), cessation programs for patients with active TB that emphasize the harmful impact of tobacco use on household contacts may improve smoking-cessation adherence. Second, studies suggest that health-care providers who provide TB care often do not believe that smoking has an impact on TB treatment, do not perceive smoking cessation to be a part of TB care, and rarely have formal training in supporting smoking cessation efforts (57, 58). Effective coordination of tobacco cessation within TB control programs will require training for health-care workers to understand the negative impacts of smoking on TB outcomes and how to support patients in their cessation attempts. Our study had limitations. First, this study relied on data reported by WHO for estimates of TB cases and TB mortality. Although an estimated 61% of TB cases were reported to WHO in 2016, only 50% of TB cases were reported among the 32 high-burden countries (1). WHO uses reported TB cases and reported TB deaths to estimate TB incidence and TB mortality; however, the gap between reported and estimated TB cases and TB deaths is vast, especially in LMIC. For example, in 2016 there was a 4.1-million-count difference between reported TB cases (6.3 million) and estimated TB cases (10.4 million). Nonetheless, we believe our estimated TB cases and estimated TB deaths reflect the actual TB burdens due to smoking and that limitations of WHO TB reporting rates did not affect our PAP estimates. Second, TB cases and deaths due to secondhand smoke were not included in our analyses, which may underestimate our estimates of the proportion of smoking-attributable TB disease and death. Third, smoking prevalence measurement and data collection methods varied from country to country, and we did not account for the intensity or duration of smoking. Although most countries used WHO guidelines to collect smoking prevalence data, tobacco use could be underreported, especially for products other than cigarettes, commonly used in developing countries. Fourth, we assumed the relative risk estimates applied for TB disease and TB death were causal (59) and homogeneous across analyses, although the relative effect of smoking on TB disease risk and TB mortality likely varies according to sex, age, and country. Nonetheless, our sensitivity analyses accounted for various relative risk values and did not result in meaningfully different PAP estimates for either TB disease or TB mortality. Despite these limitations, we used current and reliable nationally representative data sources and sensitivity analyses, which improved the validity and generalizability of our estimates. Smoking plays a harmful role in the global TB pandemic, contributing greatly to increased risk of TB disease and TB death in high-TB-burden countries. The considerable impact of smoking on TB epidemics highlights the importance of promoting smoking cessation for people at risk of TB, especially in LMIC where the prevalence of smoking and the risk of TB are highest. Despite improvements in global tobacco control policy, most countries do not have coordinated mechanisms between TB and tobacco-control programs, and tobacco-cessation support for patients with TB is limited. Our findings suggest that increased availability and implementation of smoking-cessation interventions targeted for TB patients will reduce global TB mortality and support the goals of the End TB Strategy. Continued and expanded political commitment and strong coordination among various stakeholders, both globally and nationally, are required to effectively and aggressively enforce tobacco control and ensure that it includes policy that benefits patients with TB. ACKNOWLEDGMENTS Author affiliations: Division of Epidemiology and Biostatistics, School of Public Health, Georgia State University, Atlanta, Georgia (Genet A. Amere, Argita D. Salindri, Matthew J. Magee); Georgia State University’s Tobacco Center of Regulatory Science, School of Public Health, Georgia State University, Atlanta, Georgia (Pratibha Nayak); and Emory Global Diabetes Research Center, Hubert Department of Global Health, Rollins School of Public Health, Emory University, Atlanta, Georgia (K. M. V. Narayan). Research reported in this publication was supported by the National Institute of Allergy and Infectious Diseases of the National Institutes of Health (award R03AI133172). 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For permissions, please e-mail: journals.permissions@oup.com. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model)

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American Journal of EpidemiologyOxford University Press

Published: Sep 1, 2018

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