Smoking-attributable mortality in Bangladesh: proportional mortality study

Bull World Health Organ 2013;91:757–764 | doi: http://dx.doi.org/10.2471/BLT.13.120196 Research 757 Smoking-attributable mortality in Bangladesh: proportional mortality study Dewan S Alam,a Prabhat Jha,b Chinthanie Ramasundarahettige,b Peter Kim Streatfield,a Louis W Niessen,a Muhammad Ashique H Chowdhury,a Ali T Siddiquee,a Shyfuddin Ahmeda & Timothy G Evansc Introduction Deaths attributable to smoking are projected to increase substantially throughout the 21st century and much of the increase will occur in low- and middle-income countries1 such as Bangladesh, whose population of 150 million makes it the seventh most populous country in the world. More than half of Bangladeshi men over the age of 25 years smoke cigarettes or bidis, small handmade cigarettes containing about one fourth the amount of tobacco found in cigarettes.2 A nation- ally representative case–control study in neighbouring India showed that in 2010 smoking caused about 20% of all deaths among males aged 30 to 69 years.3 Smoking cessation rates are relatively low in Bangladesh and India,2 but Bangladeshi men are, on average, younger than Indian men when they start smoking and they smoke more cigarettes or bidis daily than Indian men.2,4 Bidis account for most of the tobacco smoked in India, but in Bangladesh cigarettes represent about half of all the tobacco smoked. According to recent studies in high-income countries, men and women who start smoking as young adults and do not quit have a threefold risk of dying relative to those who have never smoked.5,6 Prospective studies are required to determine whether the same extreme risks hold true for Bangladesh and other low- and middle-income countries. Of the estimated 21.9 million smokers in Bangladesh, 21.2 million are males and only 0.7 million are females. Thus, only the effects of smoking among men can be reliably studied at present. The objective of this study was to assess the effects of smoking on cause-specific mortality among Bangladeshi men between the ages of 25 and 69 years. We conducted a retro- spective case–control study using data on cause of death and smoking status for all men in this age group who died in the subdistrict of Matlab in rural Bangladesh between 2003 and 2010. Although tobacco chewing is common in Bangladesh, its effects will be reported in a separate paper since chewing causes fewer diseases than smoking, most notably oral cancer.7 Methods Study design As part of the INDEPTH Network, the International Centre for Diarrhoeal Disease Research, Bangladesh (icddr,b), has main- tained a comprehensive Health and Demographic Surveillance System (HDSS) in Matlab, in the district (zilla) of Chandpur, since 1966.8,9 Matlab is a rural area (upazila) located about 55 km south-east of Dhaka, the capital city. It covers 184 km2 and has 142 villages, each with about 1500 people. The total population of Matlab is about 225 000. To track fatal events as part of the HDSS, trained field research assistants visit households where a death has occurred from 6 to 12 weeks after the death and administer a structured verbal autopsy questionnaire to any relative who lived with the deceased. The purpose is to obtain from these respondents information on the symptoms, signs and medical details surrounding the Objective To directly estimate how much smoking contributes to cause-specific mortality in Bangladesh. Methods A case–control study was conducted with surveillance data from Matlab, a rural subdistrict. Cases (n = 2213) and controls (n = 261) were men aged 25 to 69 years who had died between 2003 and 2010 from smoking-related and non-smoking-related causes, respectively. Cause-specific odds ratios (ORs) were calculated for “ever-smokers” versus “never-smokers”, with adjustment for education, tobacco chewing status and age. Smoking-attributable deaths among cases, national attributable fractions and cumulative probability of surviving from 25 to 69 years of age among ever-smokers and never-smokers were also calculated. Findings The fraction of ever-smokers was about 84% among cases and 73% among controls (OR: 1.7; 99% confidence interval, CI: 1.1–2.5). ORs were highest for cancers and lower for respiratory, vascular and other diseases. A dose–response relationship was noted between age at smoking initiation and daily number of cigarettes or bidis smoked and the risk of death. Among 25-year-old Bangladeshi men, 32% of ever-smokers will die before reaching 70 years of age, compared with 19% of never-smokers. In 2010, about 25% of all deaths observed in Bangladeshi men aged 25 to 69 years (i.e. 42 000 deaths) were attributable to smoking. Conclusion Smoking causes about 25% of all deaths in Bangladeshi men aged 25 to 69 years and an average loss of seven years of life per smoker. Without a substantial increase in smoking cessation rates, which are low among Bangladeshi men, smoking-attributable deaths in Bangladesh are likely to increase. a Centre for Control of Chronic Diseases, International Centre for Diarrhoeal Disease Research Bangladesh, 68 Shaheed Tajuddin Ahmed Sarani, Mohakhali, Dhaka 1212, Bangladesh. b Centre for Global Health Research, St Michael’s Hospital at University of Toronto, Toronto, Canada. c Human Development Network, The World Bank, Washington, United States of America. Correspondence to Dewan S Alam (e-mail: dsalam@icddrb.org). (Submitted: 26 February 2013 – Revised version received: 12 June 2013 – Accepted: 13 June 2013 – Published online: 12 July 2013 ) Bull World Health Organ 2013;91:757–764 | doi: http://dx.doi.org/10.2471/BLT.13.120196758 Research Smoking-attributable mortality in Bangladesh Dewan S Alam et al. death. Field staff are instructed not to try to arrive at a diagnosis of the cause of death. Instead, causes of death are assigned by two trained physicians at icddr,b in accordance with the Interna- tional statistical classification of diseases and related health problems, tenth revi- sion (ICD-10) and using standardized disease coding guidelines developed for other INDEPTH sites.8,10 Subjects Cases were men aged 25 to 69 years of age who had died from causes strongly associated with tobacco smoking:1,7,11 cancers of the lung, mouth and larynx (ICD-10 codes: C00–14, C32–34); can- cers of the digestive organs (C16–26, C48, D01, D12–13); all other cancers (rest of C00-D48, excluding C60–63 and C69–72); chronic lower respiratory dis- eases (J40–47); pulmonary tuberculosis (A15–19); all other respiratory diseases (rest of J00–99); stroke (I60–64); isch- aemic heart disease (I20–25); all other vascular diseases (rest of I00–99); cir- rhosis (K70–77); and other medical causes (rest of A00-R99, excluding the diseases not associated with tobacco smoking, which were the causes of death among controls). Controls were men who had died of causes not associated with tobacco, such as intestinal infec- tions (A00–09); other bacterial diseases (A30–99); viral infections (B01–77); cancers of the male genital organs (C60–63); cancers of the brain and eye (C69–72); endocrine, nutritional and metabolic diseases (E00–07, E25–35, E40–46, E50–64, E70–90); mental and behavioural disorders (F00–99); diseases of the nervous system (G00– 99), diseases of the eye and adnexa (H00–95); diseases of the appendix and hernias (K35–40); diseases of the skin (L00–99); diseases of the musculoskel- etal system (M00–99); diseases of the genitourinary system (N00–99), and injuries (T00-Y99). We excluded women from the analyses because the smoking preva- lence among Bangladeshi women is very low. According to the nationally repre- sentative Global Adult Tobacco Survey, or GATS, in 2009 smoking prevalence among living Bangladeshi women 15 years of age or older was only about 1.5%.2 It was somewhat higher, at 5.7%, among deceased women aged 20 years of age or older in our study. The field questionnaire contained questions on the smoking and alcohol consumption history of the deceased in- dividual. Smoking history included the type of tobacco smoked (e.g. cigarette or bidi tobacco [combined into a single question]; tobacco for pipe or hookah) or chewed (e.g. betel leaf with or with- out tobacco, tobacco powder, rolled tobacco); the amount smoked; the age (in years) at initiation and cessation of smoking; and the duration of tobacco smoking or chewing. The field ques- tionnaire did not separate the number of cigarettes from the number of bidis smoked, so we treated them together in the analysis. We excluded 156 men from the analysis because 34 of them drank alcohol, 11 smoked only pipe and the remainder had missing information on smoking status, education or cause of death. We compared “ever-smokers” – i.e. people who smoked at the time of the survey (“current smokers”) or who had smoked in the past (“former smok- ers”) – with “never-smokers”. This was appropriate because most former smok- ers (214/324) had smoked for more than 10 years. Moreover, excess hazard depends strongly not only on recent smoking habits but also on smoking habits in early adult life.1,7,11 Statistical methods We used proportional mortality to relate bidi or cigarette smoking to various specific and general medical causes of death.12,13 The assumption behind pro- portional mortality is that the smoking patterns among the deceased in the con- trol group are similar to those observed in the general population. However, in reality smoking prevalence was lower among the general population of men surveyed in 2009,2 than among our de- ceased controls, perhaps because smok- ing caused some excess deaths among controls. Thus, the net effect would be an underestimation of the differences be- tween ever-smokers and never-smokers. Other reporting biases should equally affect the cases and controls.12 We calculated cause-specific odds ratios (ORs) (as approximations of rela- tive risks [RRs]) for ever-smokers versus never-smokers using logistic regression, with adjustment for educational status (illiterate, below secondary school, secondary school or above), history of tobacco chewing (yes, no) and age (in continuous years). We calculated the smoking-attributable deaths among cases by multiplying the number of ever- smokers among the cases by: 1 1− RR (1) where RR represents the ratio of the odds of death in ever-smokers to the odds of death in never-smokers adjusted for age, education and chewing tobacco status. To calculate the national attributable fractions we used the following standard formula: p p ( ) ( ) RR RR − + − 1 1 1 (2) with the RRs derived from the Matlab results and smoking prevalence (p) from the GATS survey in 2009.2 About 80% of the Bangladeshi population lives in rural areas similar to Matlab, so the use of the RRs estimated in this study does not introduce a major bias in the calculation of overall national attributable fractions. In Bangladesh, national cause-of-death statistics are based on self-reporting, which can be unreliable.14 For this reason, to generate national cause-of-death estimates we applied, to the total deaths reported by the United Nations for Bangladesh, the proportions of the major causes of death found in Matlab.15 In Chandpur zilla, the rates of all-cause mortality among adult males are comparable to the rates observed in the whole of Bangladesh, but child mortality rates are lower.14 We calculated the cumulative probability of surviving from 25 until 69 years of age for ever-smokers and never-smokers, with adjustment for any differences in age, education and use of chewing to- bacco. To do so, we combined the RRs estimated from Matlab with national smoking prevalence1 and age-specific Bangladeshi death rates as reported by the United Nations,15 following methods described in previous studies.3,6 Results The Matlab HDSS recorded a total of 9708 deaths among individuals aged 20 years or older (5296 males, 4412 fe- males). Of these deaths, 2474 occurred in men aged 25 to 69 years. Table 1 presents data for the 2213 cases and 261 controls. Cases were older than controls on average, whereas both groups had similar educational levels and similar rates of use of chewing tobacco. Among Bull World Health Organ 2013;91:757–764 | doi: http://dx.doi.org/10.2471/BLT.13.120196 759 Research Smoking-attributable mortality in BangladeshDewan S Alam et al. the deceased, smoking prevalence was highest among those who had been il- literate or between the ages of 40 and 60 years when they died (data not shown). About 84% (1855/2213) of the cases were ever-smokers (Table 1), as compared with 73% (191/261 data not shown) of the controls. The OR for all causes of death, representing the odds in ever-smokers versus the odds in never-smokers, was 1.7 (99% confidence interval, CI: 1.1–2.5) after adjusting for any differences in age, education and use of chewing tobacco (Table 2). This corresponds to 31% of all 2213 deaths among the cases, equivalent to an excess of 692 deaths among smokers between the ages of 25 and 69 years in Matlab. About 94% of the men who died from cancers of the lung, oral cavity or larynx were ever-smokers (162/172); 103 men died from lung cancer and of these men, 97 were ever-smokers. The ORs were notably lower for digestive organ cancers than for other cancers. The ORs and the proportions of deaths due to smoking were highest for cancers; they were lower or similar for respiratory Table 1. Demographic characteristics of cases and controls in study on the effects of smoking on cause-specific mortality, Matlab, Bangladesh Characteristic No. (%) of casesa (n = 2 213) No. (%) of controlsa (n = 261) Age at death (years) 25–29 27 (1.2) 11 (4.2) 30–39 110 (5.0) 39 (14.9) 40–49 330 (14.9) 46 (17.6) 50–59 580 (26.2) 66 (25.3) 60–69 1166 (52.7) 99 (37.9) Education Illiterate 1082 (48.9) 134 (51.3) Below secondary 1031 (46.6) 117 (44.8) Secondary or higher 100 (4.5) 10 (3.8) Tobacco chewing Yesb 1071 (48.4) 108 (41.4) No 1142 (51.6) 153 (58.6) Smoking status Current smokerc 1557 (70.4) 165 (63.2) Former smoker 298 (13.5) 26 (10.0) Never-smoker 358 (16.2) 70 (26.8) a Cases and controls were men aged 25 to 69 years who had died between 2003 and 2010 from smoking- related and non-smoking-related causes, respectively. b Includes current and former users of chewing tobacco. c “Current smoker” applies to those who quit smoking within 5 years of their death. Current and former smokers combined represent ever-smokers. Table 2. Deaths among ever-smokers and odds of dying among ever-smokers versus never-smokers, by cause, and smoking-associated deaths among men aged 25 to 69 years, Matlab, Bangladesh, 2003–2010 Cause of death No. of deaths in 2003–2010 No. (%) of ever-smokers among the deceaseda ORb (99% CI) No. (%) of excess deaths due to smoking Cancer of lung, oral cavity or larynx 172 162 (94.2) 5.17 (2.0–13.4) 131 (76) Cancers of digestive organs 182 141 (77.5) 1.19 (0.6–2.2) 23 (12) Other cancers 75 64 (85.3) 1.85 (0.7–4.8) 29 (39) All cancersc 429 367 (85.5) 1.94 (1.1–3.3) 183 (43) Chronic lower respiratory diseases 172 146 (84.9) 1.44 (0.7–2.9) 45 (26) Pulmonary tuberculosis 78 67 (85.9) 1.82 (0.7–4.7) 30 (39) Other respiratory diseases 61 52 (85.2) 1.62 (0.6–4.7) 20 (33) All respiratory diseases 311 265 (85.2) 1.58 (0.9–2.8) 95 (30) Stroke 193 157 (81.3) 1.42 (0.8–2.6) 46 (24) Ischaemic heart disease 368 311 (84.5) 1.94 (1.1–3.3) 151 (41) Other vascular diseases 465 387 (83.2) 1.48 (0.9–2.5) 126 (27) All vascular diseases 1026 855 (83.3) 1.66 (1.1–2.6) 323 (31) Cirrhosis 121 100 (82.6) 1.67 (0.8–3.6) 0 (0) Other medical causesd 233 189 (81.1) 1.46 (0.8–2.6) 60 (26) Ill-defined medical causes 93 79 (84.9) 1.66 (0.7–3.9) 31 (34) All medical causese 2213 1855 (83.8) 1.68 (1.1–2.5) 692 (31) CI, confidence interval; OR, odds ratio. a Former and current smokers make up the category of “ever-smokers”. b ORs represent odds of death from specific cause among ever-smokers versus never-smokers, adjusted for age, education and tobacco chewing status. c Except those of the male genital organs, brain and eye. d All other medical deaths excluding cancer, respiratory, vascular and some deaths from causes not associated with tobacco considered as controls in this study. e Deaths from all causes except injury and others not associated with tobacco smoking. Note: See methods for ICD 10 codes used to define the cases. The 261 controls include all injury deaths and deaths that are not attributable to tobacco smoking (see methods for ICD-10 codes). Bull World Health Organ 2013;91:757–764 | doi: http://dx.doi.org/10.2471/BLT.13.120196760 Research Smoking-attributable mortality in Bangladesh Dewan S Alam et al. diseases, vascular diseases and other medical causes of death. In Bangladesh, men aged 25 to 69 years initiate smoking at an average age of 18.6 years (Appendix A, available at: www.cghr.org/tobacco) and nearly all smokers report having initiated smoking before the age of 25 years.2 As shown in Fig. 1, in our study, those who started smoking before this age had greater odds of dying than never- smokers (OR: 1.9) and than those who started smoking after the age of 25 years (OR: 1.4; χ2 test for trend 12.1; P < 0.0001). The mean daily number of cigarettes or bidis smoked by males who died was 11. A dose–response analysis (comparing 1757 ever-smokers with 438 never-smokers for whom informa- tion on smoking amount was avail- able) showed that those smokers who consumed from 20 to 50 (mean: 23) cigarettes or bidis per day had a much higher odds of dying (OR: 2.7) when compared with never-smokers, than those who consumed 10 to 19 cigarettes or bidis (mean: 12) daily (OR: 1.6) or than those who smoked 1 to 9 (mean: 6) cigarettes or bidis a day (OR: 1.3; χ2 test for trend 16.3; P < 0.001). Applying the Matlab relative risk to the national death totals suggests that about 42 800 Bangladeshi men aged 25 to 69 years died in 2010 from smoking-attributable diseases. This was equivalent to about 25% of the 172 200 deaths from all diseases in men in this age group in 2010 (Table 3). We did not attribute to smoking any deaths from cirrhosis, ill-defined conditions or in- jury. Of the smoking-attributable deaths, about 50% (21 700/42 800) were caused by vascular disease and about 26% by cancer (11 400). The cumulative probability of dying between the ages of 25 and 69 years was much higher for ever-smokers than for never-smokers (Fig. 2). At this death rate, 32% of 25-year-old Bangladeshi male ever-smokers would die before the age of 70 years, versus only 19% of 25-year-old never-smokers. Marked differences in the risk of death between ever-smokers and never-smokers were seen among those as young as 60 years – 14% dead by that age among smokers; only 8% dead among never-smokers. These data suggest that the average 25-year-old Bangladeshi male smoker currently loses an average of seven years of life because of smoking. Discussion Bangladeshi men between the ages of 25 and 69 years who have smoked at some Fig. 1. Odds ratios (ORs) and excess deaths due to smoking, by age of smoking initiation and daily number of cigarettes or bidis smoked by men aged 25 to 69 years, Bangladesh, 2003–2010 ORa (99%CI) No. (%) of smoking- associated excess deaths Age started smoking 25 years or later (30)b 1.4 (0.9–2.2) 219 (25) Before 25 years (21)b 1.9 (1.2–3.0) 367 (42) Quantity of cigarettes/bidis smoked per day 1 to 9 (6)c 1.3 (0.8–2.2) 121 (21) 10 to 19 (12)c 1.6 (1.0–2.5) 261 (32) 20 to 50 (23)c 2.7 (1.4–5.3) 219 (59) Not caused by smoking Excess risk from smoking 99% confidence interval 0 1 2 3 4 a ORs represent the odds of dying among ever-smokers relative to the odds among never-smokers, adjusted for age, education and tobacco chewing status. b The figure in parentheses is the median age of smoking initiation. c The figure in parentheses is the mean number of cigarettes or bidis smoked. Table 3. Estimated smoking-attributable deaths, by cause, among men aged 25 to 69 years and population-attributable fraction, Bangladesh, 2010 Cause of death No. of deaths in 2003–2010 All Bangladesh, 2010 Smoking- attributable deaths (thousands)a Total deaths (thousands)b Population-attributable fraction (%) All vascular diseases 1026 21.7 71.4 30.3 All cancersc 429 11.4 29.9 38.3 Respiratory diseases except tuberculosis 233 4.0 16.2 24.4 Other medical causesd 233 3.8 16.2 23.3 Pulmonary tuberculosis 78 1.9 5.4 35.1 Cirrhosis 121 0.0 8.4 0.0 Ill-defined cause 93 0.0 6.5 0.0 Injury/other cause not associated with tobacco 261 0.0 18.2 0.0 Total 2474 42.8 172.2 24.8 a Smoking prevalence of 66% noted in the GATS2 was used to calculate smoking attributable deaths. b Cause-specific total deaths were estimated by multiplying total deaths as reported by the United Nations by proportions of cause-specific deaths in study. c Except those of the male genital organs, brain and eye. d All other deaths from medical causes except cancer, respiratory diseases, vascular diseases and deaths not associated with tobacco smoking (considered as controls in this study). Bull World Health Organ 2013;91:757–764 | doi: http://dx.doi.org/10.2471/BLT.13.120196 761 Research Smoking-attributable mortality in BangladeshDewan S Alam et al. point have a risk of dying of a tobacco- related disease that is 70% higher than the risk among never-smokers of similar age, educational level and tobacco chew- ing status. Our cases were men who had died from diseases that have been causally associated with smoking in other studies1,3,5-7,11-12 and we observed a well-defined dose–response relationship between age at smoking initiation and the number of cigarettes or bidis smoked and the risk of dying. Admittedly, how- ever, not all smokers died of diseases associated with tobacco-attributable diseases and not all such diseases oc- curred among smokers. Thus, smoking is an important cause of most, but not all, of the excess deaths among smok- ers in Bangladesh. Cumulative survival analysis revealed that a typical Ban- gladeshi smoker currently loses about seven years of life because of smoking. This combines an average loss of zero years of life for some smokers not killed by smoking with a loss far in excess of seven years in some smokers who were killed by smoking. The ORs for ever-smokers versus never-smokers are slightly higher among Bangladeshi men than among Indian men (OR: 1.6).3 The propor- tion of all deaths in men aged 25 to 69 years that is due to smoking is also higher in Bangladesh (25%) than in India (20%). Subtle but potentially important differences in smoking patterns between the two countries might have an influence on the risk of specific diseases. Bangladeshi bidis are wrapped in cigarette paper rather than the tendu leaf commonly used to wrap Indian bidis. Cigarette smoking is much more common among Ban- gladeshi males than Indian males.2,4 In our study, lung cancer caused more than 10% of the deaths among smok- ers in Bangladesh (5300/42 800) but a much smaller proportion of the deaths among smokers in India.3 By contrast, pulmonary tuberculosis accounted for only 4% (2000) of the deaths among smokers in our study but for a much higher proportion of the deaths in Indian smokers.3 This may be because prompt short-course tuberculosis treatment is available in Matlab.16 Bangladeshi men have higher smoking cessation rates than Indian men but initiate smoking at a younger age and smoke more sticks on a given day.2,4 Smoking may well have caused some of the deaths we defined as our controls, such as deaths from diabetes. Thus, we may be underestimating the true risk of death from smoking in Bangladeshi men. Moreover, there was a higher proportion of ever-smokers among our controls (73%) than among the males of the same age in the GATS (66%).2 One of the strengths of the propor- tional mortality method is that most biases, such as recall bias, would apply to cases and controls equally.12 Indeed, we observed few differences between cases and controls in terms of education and tobacco chewing. Few Bangladeshis re- port drinking alcohol17 and we excluded any self-reported drinkers. However, the 121 deaths from cirrhosis suggest that in Bangladesh drinking is underreported for cultural reasons. The elevated risk of dying from cirrhosis observed in ever-smokers relative to never-smokers suggests that most of the heavy alcohol drinkers also smoked and vice versa. The combination of drinking and smoking should also exist among controls, many of whom died of injuries. Thus, we might be slightly underestimating the risks of smoking. However, the exclusion of men who drank alcohol does not explain the marked differences in mortality observed between ever-smokers and never-smokers. Deaths in the control group (n = 261) were fewer than ideal. Consequently, the ORs associated with specific diseases had wide CIs. However, the cause-specific ORs in our study are consistent with those seen in India3,18,19 and other Asian countries.12 Similarly, some deaths may have been assigned to the wrong cause on verbal autopsy.20,21 This would tend to raise the ratio of the risk in smokers to the risk in non-smok- ers in the case of some diseases and to lower this ratio in the case of others. The proportion of vascular deaths among all deaths in men in Matlab (about 41%) is higher than the proportion seen in crude national cause-of-death patterns in Bangladesh or the proportion seen in India in men of comparable age.3,14 Thus, we might be overestimating the absolute number of smoking-attributable deaths from vascular disease (but not the odds). Fig. 2. Cumulative probability of dying between the ages of 25 and 69 years among male ever-smokers and never-smokers in Bangladesh, at 2010 death rates Cu m ul at ive p ro ba bi lit y o f d ea th (% ) 40 30 20 10 0 6% 4% 8% 14% 19% 32% 7 years Age (years) Ever-smoker Never-smoker 30 40 50 60 70 Note: The horizontal arrow shows that the death rates experienced by never-smokers at the age of 70 years are experienced seven years earlier by ever-smokers. Thus, smokers lose seven years of life on average. This combines a loss of zero years among smokers not killed by smoking with a loss of far more than seven years among those killed by smoking. Bull World Health Organ 2013;91:757–764 | doi: http://dx.doi.org/10.2471/BLT.13.120196762 Research Smoking-attributable mortality in Bangladesh Dewan S Alam et al. However, the computed ORs and the ab- solute number of smoking-attributable deaths from any cause are affected less, if at all, by the misclassification of specific diseases. Most of the misclassification on verbal autopsy is confined to people who die in old age.20 Our study focused on men aged 25 to 69 years and fewer than 4% of the deaths among these men were assigned to ill-defined causes. Bangladesh already has about 20 million male smokers and it is likely that they will experience a loss in lifespan of more than the seven years that we estimated in this study. Bangladeshi men still smoke fewer cigarettes per day and initiate smoking at a later age than men in most high-income countries. Urban male smokers in Bangladesh consume more cigarettes than bidis and smoke more per day than rural smokers.2 Re- cent increases in income in Bangladesh have also made smoking relatively more affordable.22 For cultural reasons, few women smoke in Bangladesh, but there is no guarantee that this will hold in the future. Recent prospective studies in high-income countries have shown that male or female lifelong smokers who start smoking as young adults and do not quit have an excess risk of dying 200% as high – corresponding to an RR three times as high – as ever-smokers and live, on average, one decade less than never- smokers.5,6 Indeed, Indian men who smoke cigarettes in these large quantities already appear to be losing a decade of life.3 Of Bangladeshi men aged 45 to 64 years, only 15% are former smokers and 63% are current smokers.2 By contrast, in the United States of America, where smoking cessation has become common, former smokers are about three times more numerous than current smokers among men this same age.6 About one quarter of the deaths in Bangladeshi men between the ages of 25 and 69 years are due to smok- ing. Tobacco control in Bangladesh is still at an early stage; the Smoking and Tobacco Products Usage (Control) Act, which was passed in 2005, has been implemented only partially.22 Efforts to accelerate tobacco control in Ban- gladesh are warranted. Cigarette prices in the country are among the lowest in the world; bidis are even cheaper than cigarettes.22 Hence, the most effective way to encourage smoking cessation in Bangladesh would probably be to im- pose a substantial excise tax on tobacco products. Prominent warning labels using graphic images, bans on smok- ing in public places, strict restrictions on tobacco advertising and promotion, and expanded access to smoking ces- sation services are other interventions that can be implemented in Bangladesh to encourage men to stop smoking and deter women and youth from taking up smoking.1,23 ■ Acknowledgements This paper is dedicated to the late Sir Richard Doll (1912–2005), who would have turned 100 on 28 October 2012. The opinions expressed here are those of the authors and do not necessarily represent those of the institutions where the authors are employed. Funding: Funding for this study was pro- vided by the Fogarty International Centre of the US National Institutes of Health (grant TW007939-01), the Canadian Institute of Health Research (IEG-53506), the Bill & Melinda Gates Foundation (Grant 51447) and the Oxford Health Alliance Vision 2020 (Grant 5444447). PJ is supported by a University of To- ronto Endowed Chair. DA is supported by icddr,b. Competing interests: None declared. صخلم يبسانتلا تايفولا لدعم ةسارد :شيدلاغنب في ينخدتلا ببسب تايفولا لدعم في ببستلا في ينخدتلا ةهماسم ىدلم شرابلما ريدقتلا ضرغلا .شيدلاغنب في تايفولا ،بلاتام نم دصرت تانايب عم ةنراقم ةلاح ةسارد تيرجأ ةقيرطلا )2213 = ددعلا( تلاالحا تناكو .ةيفير ةيعرف ةقطنم يهو لىإ 25 نم مهرماعأ حواترت لاجرل )261 = ددعلا( طباوضلاو قلعتت بابسلأ 2010و 2003 يماع ينب مهفتح اوقل ًاماع 69 باسح متو .لياوتلا لىع ينخدتلاب قلعتت لا بابسأو ينخدتلاب “ينمئادلا يننخدلما” ىدل )ORs( بابسلأا ةددمح ةيحجرلأا بسن ميلعتلاب ةصاخ تلايدعت لاخدإ عم ،“ًاقلطم يننخدلما يرغ” لباقم ببسب تايفولا باسح ًاضيأ مت ماك .نسلاو غبتلا غضم ةلاحو ديعصلا لىع بابسلأ بسنت يتلا روسكلاو ،تلاالحا ينب ينخدتلا لىإ 25 نس نم ةايلحا ديق لىع ءاقبلل يمكاترلا لماتحلااو ،ينطولا .ًاقلطم يننخدلما يرغو ينمئادلا يننخدلما ينب ًاماع 69 84 لياوح ينمئادلا يننخدلما ىدل روسكلا بسن تناك جئاتنلا :1.7 :ةيحجرلأا ةبسن( طباوضلا ينب % 73و تلاالحا ينب % بسن تغلبو .)2.5 – 1.1 :ةقثلا لصاف ،ةقث لصاف % 99 سيفنتلا زاهلجاو ناطسرلا ضارملأ اتهلادعم لىعأ ةيحجرلأا ةقلاع دوجو ظحولو .اهيرغو ةيومدلا ةيعولأا ضارمأو ليفسلا يمويلا ددعلاو ينخدتلا ءدب دنع رمعلاو ةعرجلل ةباجتسلاا ينب ينبو .تولما رطخو اهنيخدت متي يتلا يديبلا رئاجس وأ رئاجسلل % 32 نأ دجن ،ًاماع 25 رمعلا نم ينغلابلا ينيشدلاغنبلا لاجرلا نم اماع 70 نس مهغولب لبق نوتومي فوس ينمئادلا يننخدلما نم ماع فيو .ًاقلطم نونخدي لا نيذلا نم % 19 ةبسنب ةنراقم ،رمعلا في اهتظحلام تتم يتلا تايفولا لك نم % 25 ةبسن تناك ،2010 ًاماع 69 لىإ 25 نم مهرماعأ حواترت نيذلا ينيشدلاغنبلا لاجرلا .ينخدتلا لىإ عجرت )ةافو ةلاح 42000 يأ( تايفولا تلااح نم % 25 لياوح في ينخدتلا ببستي جاتنتسلاا 69 لىإ 25 نم مهرماعأ حواترت نيذلا شيدلاغنب في لاجرلا في .نخدم لك ةايح نم تاونس عبس هطسوتم ام ةراسخ لىإو ،ًاماع ةضفخنلما ،ينخدتلا نع علاقلإا تلادعم في ةيربك ةدايز نودبو ببسب تايفولا دادزت نأ حجرلما نم ،شيدلاغنب في لاجرلا ينب .شيدلاغنب في ينخدتلا Bull World Health Organ 2013;91:757–764 | doi: http://dx.doi.org/10.2471/BLT.13.120196 763 Research Smoking-attributable mortality in BangladeshDewan S Alam et al. 摘要 孟加拉国归因于吸烟的死亡率：比例死亡率研究 目的 直接估算吸烟对孟加拉国死因别死亡率有多大的 贡献。 方法 使用来自农村小区 Matlab 的监测数据进行病例 对照研究。病例组 (n = 2213) 和对照组 (n = 261) 分别是 2003 年到 2010 年间因吸烟相关和非吸烟相关原因死 亡的 25 岁到 69 岁的男性。计算“曾经吸烟者”和“非 吸烟者”的死因别优势比（OR），计算中针对教育程度、 嚼烟草状态和年龄进行调整。还计算了病例中的吸烟 归因死亡、全国可归因分数以及 25 岁到 69 岁曾经吸 烟者和非吸烟者中的累计生存概率。 结果 曾经吸烟者的分数在病例组中约为 84%，在对照 组中为 73%（OR ：1.7 ；99% 置信区间，CI ：1.1–2.5）。 OR 对于癌症来说最高，对于呼吸道、血管和其他疾 病来说较低。在开始吸烟年龄以及每日吸食香烟或比 迪烟数与死亡风险之间有明显的剂量 – 反应关系。 在 25 岁孟加拉国男性中，32% 的曾经吸烟者将活不到 70 岁，非吸烟者的这个比例则是 19%。在 2010 年孟 加拉国有案可查的 25 岁到 69 岁男性的全部死亡（即 4.2 万例死亡）中，大约 25% 可归因于吸烟。 结论 在孟加拉国 25 岁到 69 岁男性的全部死亡中，吸 烟造成的死亡约占 25%，每名吸烟者平均损失七年的 寿命。如果没有戒烟率的显著提高（这个比例在孟加 拉国男性中很低），可归因于吸烟的死亡很可能还会 增加。 Résumé Mortalité attribuable au tabagisme au Bangladesh: une étude proportionnelle de la mortalité Objectif Estimer la contribution directe du tabagisme à la mortalité par cause au Bangladesh. Méthodes Une étude cas-témoins a été menée avec les données de surveillance de Matlab, un sous-district rural. Les cas (n = 2213) et les contrôles (n = 261) étaient des hommes âgés de 25 à 69 ans décédés entre 2003 et 2010 des suites ou non du tabagisme, respectivement. Les rapports des cotes (RC) par cause ont été calculés pour les « fumeurs depuis toujours » par rapport aux « non-fumeurs », avec un ajustement pour l’éducation, la consommation de tabac à mâcher et l’âge. On a également calculé les décès attribuables au tabagisme parmi les cas, les fractions attribuables à la population nationale et la probabilité de survie de 25 à 69 ans chez les fumeurs depuis toujours et chez les non-fumeurs. Résultats La fraction des fumeurs depuis toujours était d’environ 84% chez les cas et de 73% chez les contrôles (RC: 1,7; intervalle de confiance de 99%, IC: 1,1–2,5). Les rapports de cotes étaient les plus élevés pour les cancers et plus bas pour les maladies respiratoires, vasculaires et autres. Une relation dose-réponse a été notée entre l’âge de l’initiation au tabagisme et le nombre de cigarettes ou de « bidi s» fumées chaque jour et le risque de mortalité. Chez les hommes du Bangladesh de 25 ans, 32% des fumeurs depuis toujours mourront avant l’âge de 70 ans, par rapport à 19% pour les non-fumeurs. En 2010, environ 25% de tous les décès observés chez les hommes du Bangladesh âgés de 25 à 69 ans (c’est-à-dire 42 000 décès) étaient attribuables au tabagisme. Conclusion Le tabagisme est à l’origine de 25% de tous les décès chez les hommes du Bangladesh âgés de 25 à 69 ans, et d’une perte moyenne de 7 années de vie pour les fumeurs. Sans une augmentation importante des taux d’abandon du tabac, qui sont faibles chez les hommes du Bangladesh, les décès attribuables au tabagisme augmenteront probablement dans ce pays. Резюме Сопряженная с курением смертность в Бангладеш: пропорциональное исследование смертности Цель Напрямую оценить влияние курения на показатели причинно-обусловленной смертности в Бангладеш. Методы Исследование методом «случай-контроль» проводилось по данным наблюдений в аграрном подокруге Матлаб. Популяцию исследования (n = 2213) и контрольную группу (n = 261) составили мужчины в возрасте 25-69 лет, умершие в период между 2003 и 2010 годом в силу связанных и не связанных с курением причин. Были рассчитаны отношения рисков (ОР) по конкретным причинам смерти для «постоянно куривших» и «никогда не куривших» лиц, с поправками на уровень полученного образования, отношение к жеванию табака и возраст. Также были вычислены доля связанных с курением смертей среди включенных в исслеование случаев смерти, национальные коэффициенты и интегральная вероятность выживания лиц в возрасте 25-69 лет для постоянно курящего и никогда не курившего населения. Результаты Доля постоянно куривших составила 84% среди исследованных случаев и 73% в контрольной группе (ОР: 1,7; доверительный интервал (ДИ) 99%: 1,1–2,5). Наиболее высокие риски были отмечены для онкологических заболеваний, наименее высокие — для респираторных, сердечно-сосудистых и других заболеваний. Была установлена связь «доза-эффект» возраста начала курения и количества ежедневно выкуриваемых сигарет или биди с риском смерти. 32% постоянно курящих 25-летних бангладешских мужчин не доживут до 70-летнего возраста, тогда как среди некурящих эта доля составит 19%. В 2010 году около 25% всех смертей бангладешских мужчин в возрасте 25-69 лет (т. е. 42 000 смертей) были связаны с курением. Вывод Курение является причиной примерно 25% смертей у бангладешских мужчин в возрасте 25-69 лет и снижает продолжительность жизни курильщиков в среднем на семь лет. Весьма вероятно, что в отсутствие существенного увеличения темпов отказа от курения (весьма низких среди бангладешских мужчин) сопряженная с курением смертность в Бангладеш продолжит расти. Bull World Health Organ 2013;91:757–764 | doi: http://dx.doi.org/10.2471/BLT.13.120196764 Research Smoking-attributable mortality in Bangladesh Dewan S Alam et al. Resumen Mortalidad atribuible al tabaquismo en Bangladesh: estudio de mortalidad proporcional Objetivo Estimar directamente la medida en la que el tabaquismo contribuye a la mortalidad por causa específica en Bangladesh. Métodos Se realizó un estudio de casos y controles con datos de vigilancia de Matlab, un subdistrito rural. Los casos (n = 2213) y los controles (n = 261) se trataron de hombres de edades entre 25 y 69 años que habían fallecido entre 2003 y 2010 por causas relacionadas y no relacionadas con el tabaquismo, respectivamente. Las razones de posibilidades por causa específica se calcularon para los «fumadores de siempre» frente a los «nunca fumadores», ajustando la educación, el consumo de tabaco de mascar y la edad. También se calcularon las muertes atribuibles al tabaquismo entre los casos, las fracciones nacionales atribuibles y la probabilidad acumulada de sobrevivir de los 25 a los 69 años de edad entre los fumadores de siempre y los nunca fumadores. Resultados La fracción de fumadores de siempre fue de aproximadamente el 84% entre los casos y el 73% entre los controles (razón de posibilidades: 1,7; intervalo de confianza 99%: 1,1–2,5). Las razones de posibilidades fueron las mayores en casos de cánceres y menores en casos de enfermedades vasculares, respiratorias y de otros tipos. Se señaló una relación dosis-respuesta entre la edad de la iniciación en el tabaquismo y el número diario de cigarrillos o bidis fumados y el riesgo de muerte. Entre los hombres de Bangladesh de 25 años, el 32% de los fumadores de siempre fallecerán antes de alcanzar los 70 años, comparado con el 19% de los nunca fumadores. En 2010, aproximadamente el 25% de las muertes observadas en los hombres de Bangladesh de entre 25 y 69 años (42 000 muertes) fueron atribuibles al tabaquismo. Conclusión El tabaquismo causa aproximadamente el 25% de todas las muertes en los hombres de Bangladesh de entre 25 y 69 años y una pérdida media de siete años de vida en cada fumador. Sin un aumento significativo en las tasas de abandono del tabaquismo, que son bajas entre los hombres de Bangladesh, es probable que aumenten las muertes atribuibles al tabaquismo en Bangladesh. References 1. Jha P. Avoidance. Nat Rev Cancer 2009;9:655–64. doi: http://dx.doi. org/10.1038/nrc2703 PMID:19693096 2. Global Tobacco Surveillance System. Global Adult Tobacco Survey – Bangladesh report 2009. Dhaka: World Health Organization, Country office for Bangladesh; 2009. 3. Jha P, Jacob B, Gajalakshmi V, Gupta PC, Dhingra N, Kumar R et al.; RGI-CGHR Investigators. A nationally representative case-control study of smoking and death in India. N Engl J Med 2008;358:1137–47. doi: http:// dx.doi.org/10.1056/NEJMsa0707719 PMID:18272886 4. Global Tobacco Surveillance System. Global Adult Tobacco Survey – India report 2010. New Delhi, India: World Health Organization and Ministry of Health and Family Welfare; 2010. 5. Pirie K, Peto R, Reeves GK, Green J, Beral V; Million Women Study Collaborators. The 21st century hazards of smoking and benefits of stopping: a prospective study of one million women in the UK. Lancet 2013;381:133–41. doi: http://dx.doi.org/10.1016/S0140-6736(12)61720-6 PMID:23107252 6. Jha P, Ramasundarahettige C, Landsman V, Rostron B, Thun M, Anderson RN et al. 21st-century hazards of smoking and benefits of cessation in the United States. N Engl J Med 2013;368:341–50. doi: http://dx.doi.org/10.1056/ NEJMsa1211128 PMID:23343063 7. International Agency for Research on Cancer. Vol. 83. Tobacco smoke and involuntary smoking. In: IARC monographs on the evaluation of the carcinogenic risks of chemicals to humans. Lyon: IARC; 2004. 8. Centre for health and population research. Health and demographic surveillance system – Matlab, volume.36: registration of health and demographic events 2003. Dhaka: ICDDR, B; 2005. 9. Alam N, Chowdhury HR, Bhuiyan MA, Streatfield PK. Causes of death of adults and elderly and healthcare-seeking before death in rural Bangladesh. J Health Popul Nutr 2010;28:520–8. doi: http://dx.doi.org/10.3329/jhpn. v28i5.6161 PMID:20941904 10. International statistical classification of diseases and related health problems, 10th revision. Geneva: World Health Organization; 2008. 11. Peto R, Lopez AD, Boreham J, Thun M. Mortality from smoking in developed countries, 1950–2000. 2nd ed. Available from: www.ctsu.ox.ac.uk/~tobacco/ [accessed 30 June 2013]. 12. Liu BQ, Peto R, Chen ZM, Boreham J, Wu Y-P, Li J-Y et al. Emerging tobacco hazards in China: 1. Retrospective proportional mortality study of one million deaths. BMJ 1998;317:1411–22. doi: http://dx.doi.org/10.1136/ bmj.317.7170.1411 PMID:9822393 13. Zaridze D, Brennan P, Boreham J, Boroda A, Karpov R, Lazarev A et al. Alcohol and cause-specific mortality in Russia: a retrospective case-control study of 48,557 adult deaths. Lancet 2009;373:2201–14. doi: http://dx.doi. org/10.1016/S0140-6736(09)61034-5 PMID:19560602 14. Bangladesh Bureau of Statistics. Report of Sample Vital Registration System, 2010. Dhaka: Ministry of Planning, Government of the People’s Republic of Bangladesh; 2010. 15. United Nations, Department of Economic and Social Affairs, Population Division. World population prospects, the 2012 revision. New York: UN; 2012. Available from: http://esa.un.org/unpd/wpp/Excel-Data/mortality.htm [accessed 30 June 2013]. 16. Chowdhury AM, Chowdhury S, Islam MN, Islam A, Vaughan JP. Control of tuberculosis by community health workers in Bangladesh. Lancet 1997;350:169–72. doi: http://dx.doi.org/10.1016/S0140-6736(96)11311-8 PMID:9250184 17. Razzaque A, Nahar L, Abu Haider MGM, Karar ZA, Islam MS, Yunus M. Sociodemographic differentials of selected noncommunicable diseases risk factors among adults in Matlab, Bangladesh: findings from a WHO STEPS survey. Asia Pac J Public Health 2011;23:183–91. doi: http://dx.doi. org/10.1177/1010539510392743 PMID:21159696 18. Gajalakshmi V. Peto R, Kanaka S, Jha P. Smoking and mortality from tuberculosis and other diseases in India: retrospective study of 43000 adult males and 35000 controls. Lancet 2003;362:507–15. doi: http://dx.doi. org/10.1016/S0140-6736(03)14109-8 PMID:12932381 19. Gupta PC. Survey of sociodemographic characteristics of tobacco use among 99,598 individuals in Bombay, India using handheld computers. Tob Control 1996;5:114–20. doi: http://dx.doi.org/10.1136/tc.5.2.114 PMID:8910992 20. Jha P, Gajalakshmi V, Gupta PC, Kumar R, Mony P, Dhingra N et al.; RGI-CGHR Prospective Study Collaborators. Prospective study of one million deaths in India: rationale, design, and validation results. PLoS Med 2006;3:e18. doi: http://dx.doi.org/10.1371/journal.pmed.0030018 PMID:16354108 21. Dikshit R, Gupta PC, Ramasundarahettige C, Gajalakshmi V, Aleksandrowicz L, Badwe R et al.; Million Death Study Collaborators. Cancer mortality in India: a nationally representative survey. Lancet 2012;379:1807–16. doi: http://dx.doi.org/10.1016/S0140-6736(12)60358-4 PMID:22460346 22. Barkat A, Chowdhury AU, Nargis N, Rahman M, Khan MS, Kumar A et al. The economics of tobacco and tobacco taxation in Bangladesh. Paris: International Union Against Tuberculosis and Lung Disease; 2012. 23. Jha P, Chaloupka FJ. Curbing the epidemic: governments and the economics of tobacco control. Washington: The World Bank; 1999.