Cancers attributable to tobacco smoking in France in 2015

Cancers attributable to tobacco smoking in France in 2015 Abstract Background The evidence on the carcinogenicity of tobacco smoking has been well established. An assessment of the population-attributable fraction (PAF) of cancer due to smoking is needed for France, given its high smoking prevalence. Methods We extracted age- and sex-specific national estimates of population and cancer incidence for France, and incidence rates of lung cancer among never smokers and relative risk (RR) estimates of smoking for various cancers from the American Cancer Prevention Study (CPS II). For active smoking, we applied a modified indirect method to estimate the PAF for lung and other tobacco smoking-related cancer sites. Using the RR estimates for second-hand smoking, the proportion of never smokers living with an ever-smoking partner derived from survey, and marital status data, we then estimated the PAF for lung cancer attributable to domestic passive smoking. Results Overall in France in 2015, 54 142 and 12 008 cancer cases in males and females, respectively, were attributable to active smoking, accounting for 28 and 8% of all cancer cases observed among adult (30+ years) males and females. Additionally, 36 and 142 lung cancer cases, respectively among male and female never smokers, were attributable to second-hand smoke resulting from their partner’s active smoking, corresponding to 4.2 and 6.7% of lung cancer cases which occurred in never smoker males and females, respectively. Conclusions Tobacco smoking is responsible for a significant number of potentially avoidable cancer cases in France in 2015. More effective tobacco control programmes are critical to reduce this cancer burden. Introduction The evidence on the carcinogenicity of tobacco smoking has grown vastly since the reports of an association between cigarette smoking and carcinoma of the lung in 1950.1–3 The International Agency for Research on Cancer (IARC) has included cancers of the lung, larynx, oral cavity, pharynx, nasal cavity and paranasal sinuses, oesophagus, stomach, pancreas, liver, kidney, ureter, bladder, uterine cervix, colon and rectum, acute myeloid leukaemia and the mucinous tumours of the ovary in the list of cancers caused by tobacco smoking.4,5 Exposure to second-hand smoke has also been found to increase the risk of lung cancer in never smokers and has been classified as carcinogenic.4 France is one of the high-income European countries with the highest daily smoking prevalence: in 2014, 28% (32% in men and 24% in women) of the French population were daily tobacco smokers.6,7 In order to reduce the smoking prevalence in France, the public health authority has launched a national programme of tobacco control (Programme national de réduction du tabagisme), aiming to reduce the number of daily smokers by 10% in 2019.8 It is therefore of great public health interest to provide the up-to-date estimates of the proportion and number of cancers attributable to active and passive smoking. This article provides, for 2015, estimates of the number and proportion of cancer cases attributable to active smoking in France for all cancers identified by IARC to be caused by smoking. It also estimates the number and proportion of lung cancer cases among never smokers due to exposure to passive smoking in their home. Methods Estimation of population-attributable fractions Active smoking We estimated the population-attributable fractions (PAFs) and numbers of cancer cases attributable to cigarette smoking using an indirect method of Peto and Lopez (1992),9 modified by Parkin (2011) and used in similar projects for the UK and Australia.10,11 This method relies on two main assumptions for high-income populations: (i) active tobacco smoking is the most important risk factor for lung cancer; (ii) lung cancer incidence among never smokers is fairly small and roughly constant across populations of a given sex and age. The number of lung cancers due to active smoking can be calculated as the difference between the observed number of lung cancers and the expected number if the population had the incidence rate of never smokers. Data The data required for the analysis include, from the same population, the sex and age-specific incidence rates of lung cancer among never smokers and relative risks (RRs) for individual cancers in smokers in comparison to never smokers.12–14 We used the lung cancer incidence rates in never smokers reported in Parkin (2011), which are estimated from lung cancer death rates in the second Cancer Prevention Study (CPS II study) for the period 1982–02.10,13 The CPS II is an American prospective cohort study, involving roughly 1.2 million participants, over 30 years old at the baseline survey in 1982 with a 20-year follow-up.12,13 Similar to previous studies, we used for most cancer sites the RRs of death from cancer among current smokers as compared to never smokers from analyses based on the CPS II study. We chose to use the RRs of cancer death instead of incidence, because they are estimated from cohort studies with long duration of follow-up and sample-size large enough to produce accurate risk estimates even for less common cancers. However, for mucinous ovarian cancer, the RR estimate for cancer incidence from a meta-analysis by Jordan et al. (2006) was used, as no RR for mortality or incidence have been estimated for the CPS II cohort.15 And for colorectal cancer, we used the RR for cancer incidence estimated by Hannan et al. (2009) from the follow-up of the CPS II Nutrition Cohort.16 Most other RRs are derived from the CPS II study re-analysis conducted by Ezzati et al. (2005) adjusted for important covariates (including age, race, marital status, education, employment, food and alcohol consumption).14 The RRs used are listed in table 1 with their sources. Table 1 Estimated relative risks (RRs)a of dying from cancers for current smokers compared to never smokers by cancer sites Cancer site ICD10 Relative risk (95% CI) Reference Males Females Oral cavity & pharynx C01–14 10.9 5.1 US Surgeon General’s report 20043 Oesophagus C15 6.8 7.8 US Surgeon General’s report 20043 Stomach C16 2.2 (1.8–2.7) 1.5 (1.2–1.9) Ezzati et al. 200514 Colon-rectum C18–20 1.2 (1.0–1.6) 1.3 (1.0–1.7) Hannan et al. 200916 Liver C22 2.3 (1.5–3.8) 1.5 (0.8–2.7) Ezzati et al. 200514 Pancreas C25 2.2 (1.7–2.8) 2.2 (1.8–2.8) Ezzati et al. 200514 Larynx C32 14.6 13.0 US Surgeon General's report 20043 Lung C33–34 21.3 (17.7–25.6) 12.5 (10.9–14.3) Ezzati et al. 200514 Cervix C53 1.5 (0.9–2.6) Ezzati et al. 200514 Ovary (mucinous) C56.9 2.1 (1.7–2.7) Jordan et al. 200615 Kidney C64–66, C68 2.5 (1.8–3.6) 1.5 (1.0–2.1) Ezzati et al. 200514 Urinary bladder C67 3.0 (2.1–4.3) 2.4 (1.5–4.1) Ezzati et al. 200514 Acute myelogenous leukaemia C92.0 1.9 (1.3–2.9) 1.2 (0.8–1.8) Ezzati et al. 200514 Cancer site ICD10 Relative risk (95% CI) Reference Males Females Oral cavity & pharynx C01–14 10.9 5.1 US Surgeon General’s report 20043 Oesophagus C15 6.8 7.8 US Surgeon General’s report 20043 Stomach C16 2.2 (1.8–2.7) 1.5 (1.2–1.9) Ezzati et al. 200514 Colon-rectum C18–20 1.2 (1.0–1.6) 1.3 (1.0–1.7) Hannan et al. 200916 Liver C22 2.3 (1.5–3.8) 1.5 (0.8–2.7) Ezzati et al. 200514 Pancreas C25 2.2 (1.7–2.8) 2.2 (1.8–2.8) Ezzati et al. 200514 Larynx C32 14.6 13.0 US Surgeon General's report 20043 Lung C33–34 21.3 (17.7–25.6) 12.5 (10.9–14.3) Ezzati et al. 200514 Cervix C53 1.5 (0.9–2.6) Ezzati et al. 200514 Ovary (mucinous) C56.9 2.1 (1.7–2.7) Jordan et al. 200615 Kidney C64–66, C68 2.5 (1.8–3.6) 1.5 (1.0–2.1) Ezzati et al. 200514 Urinary bladder C67 3.0 (2.1–4.3) 2.4 (1.5–4.1) Ezzati et al. 200514 Acute myelogenous leukaemia C92.0 1.9 (1.3–2.9) 1.2 (0.8–1.8) Ezzati et al. 200514 a RRs used for the main analysis. Table 1 Estimated relative risks (RRs)a of dying from cancers for current smokers compared to never smokers by cancer sites Cancer site ICD10 Relative risk (95% CI) Reference Males Females Oral cavity & pharynx C01–14 10.9 5.1 US Surgeon General’s report 20043 Oesophagus C15 6.8 7.8 US Surgeon General’s report 20043 Stomach C16 2.2 (1.8–2.7) 1.5 (1.2–1.9) Ezzati et al. 200514 Colon-rectum C18–20 1.2 (1.0–1.6) 1.3 (1.0–1.7) Hannan et al. 200916 Liver C22 2.3 (1.5–3.8) 1.5 (0.8–2.7) Ezzati et al. 200514 Pancreas C25 2.2 (1.7–2.8) 2.2 (1.8–2.8) Ezzati et al. 200514 Larynx C32 14.6 13.0 US Surgeon General's report 20043 Lung C33–34 21.3 (17.7–25.6) 12.5 (10.9–14.3) Ezzati et al. 200514 Cervix C53 1.5 (0.9–2.6) Ezzati et al. 200514 Ovary (mucinous) C56.9 2.1 (1.7–2.7) Jordan et al. 200615 Kidney C64–66, C68 2.5 (1.8–3.6) 1.5 (1.0–2.1) Ezzati et al. 200514 Urinary bladder C67 3.0 (2.1–4.3) 2.4 (1.5–4.1) Ezzati et al. 200514 Acute myelogenous leukaemia C92.0 1.9 (1.3–2.9) 1.2 (0.8–1.8) Ezzati et al. 200514 Cancer site ICD10 Relative risk (95% CI) Reference Males Females Oral cavity & pharynx C01–14 10.9 5.1 US Surgeon General’s report 20043 Oesophagus C15 6.8 7.8 US Surgeon General’s report 20043 Stomach C16 2.2 (1.8–2.7) 1.5 (1.2–1.9) Ezzati et al. 200514 Colon-rectum C18–20 1.2 (1.0–1.6) 1.3 (1.0–1.7) Hannan et al. 200916 Liver C22 2.3 (1.5–3.8) 1.5 (0.8–2.7) Ezzati et al. 200514 Pancreas C25 2.2 (1.7–2.8) 2.2 (1.8–2.8) Ezzati et al. 200514 Larynx C32 14.6 13.0 US Surgeon General's report 20043 Lung C33–34 21.3 (17.7–25.6) 12.5 (10.9–14.3) Ezzati et al. 200514 Cervix C53 1.5 (0.9–2.6) Ezzati et al. 200514 Ovary (mucinous) C56.9 2.1 (1.7–2.7) Jordan et al. 200615 Kidney C64–66, C68 2.5 (1.8–3.6) 1.5 (1.0–2.1) Ezzati et al. 200514 Urinary bladder C67 3.0 (2.1–4.3) 2.4 (1.5–4.1) Ezzati et al. 200514 Acute myelogenous leukaemia C92.0 1.9 (1.3–2.9) 1.2 (0.8–1.8) Ezzati et al. 200514 a RRs used for the main analysis. The size of the French population in 2015 by sex and age group was obtained from the French National Institute for Statistics and Economic Studies datasets (INSEE).17 The number of cancer cases in France in 2015 by age, sex and site was estimated by applying the observed incidence rates for 2013 reported by the national network of cancer registries (FRANCIM) to the 2015 population.18 To estimate the number of mucinous ovarian cancers, we applied the age-specific proportions of mucinous ovarian cancers reported by the FRANCIM for 2009–13 (shown in Supplementary table S1) to the age-specific numbers of ovarian cancer cases estimated for 2015. Analysis The statistical analysis was performed in two steps. First, we calculated the expected number of lung cancer cases in France if smoking was absent for a given sex s and age a, by multiplying the sex- and age-specific lung cancer rate among never smokers ILs,a from the CPS II study by the corresponding population size Ns,a in France in 2015. The number of lung cancer cases attributable to smoking was estimated as the difference between the observed number of lung cancer cases OLs,a and the expected number in the absence of smoking in 2015. The PAF for lung cancer due to tobacco smoking is then estimated as PAFLs,a=OLs,a-ILs,aNs,aOLs,a (1) For all the other cancer sites i, we used the conventional PAF formula,19 for each sex and age category: PAFis,a=Pes,arris-11+Pes,arris-1  (2) where Pes,a  is the pseudo smoking prevalence in the population, and rris the RR for cancer site i in smokers as compared to never smokers. Pes,a was calculated as the expected proportion of tobacco smokers in the French population which explains the estimated smoking-attributable fraction of lung cancers using the RR of lung cancer rrLs  provided by the CPS II study.10 It summarizes the cumulative effect of the smoking history among former and current smokers in the population with a single indicator. Pes,a= PAFLs,a1-PAFLs,arrLs-1  (3) Having calibrated the prevalence of smoking on the risk in the CPS II population, one can use Equation (2) to estimate the corresponding PAFs. The numbers of cancer cases attributable to smoking for each site are the products of the PAFs and the total incidence for each site. Domestic passive smoking Because never smokers exposed to second-hand smoke are at increased risk of lung cancer, we estimate the PAF and the number of lung cancer cases attributable to passive smoking. Due to lack of exposure data for passive smoking in workplaces and other public areas, we restrict the analysis to domestic passive smoking. Data The RR estimates of passive smoking on lung cancer are most robust for never smokers who have lived with a partner who smokes. Because data on exposure to passive smoking at work and other public places in France are not readily available, we restrict the analysis to never smokers who were living in the same household as a smoking partner. Relative risks The RRs for lung cancer incidence in never smokers who were exposed to tobacco smoke from a smoking partner were obtained from the meta-analysis published in the IARC Monograph volume 83 (2004).4 The RRs for males and females never smokers were 1.37 (95% CI 1.02–1.82) and 1.24 (95% CI 1.14–1.34), respectively. Exposure Because there is no data available in France on the proportion of never smokers living with a smoker, it was estimated following the methods described by Parkin (2011).10 Briefly, we used the marital status data in 2005 published by INSEE and the tobacco smoking prevalence (categorized in never, former and current smoker) from a 2005 national health survey (Baromètre Santé, 2005),20 allowing a 10-year latency time for the occurrence of lung cancer. Both data are available by sex and five-year age groups in 2005. Recognizing that couples tend to be concordant for smoking status and as proposed by Wald et al. (1986)21 and used by Parkin (2011),10 we assumed that ever smokers and never smokers were three times more likely to live with a partner with the same smoking status than with one having different smoking status. We also assumed that couples were in the same five-year age-group. The estimation is detailed in Supplementary table S3. Analysis The corresponding PAFs are estimated using the conventional equation PAFs,a=PNwT(s,a)(RR(s)-1)PNwTs,aRR(s)-1+1 (4) where PNwT(s, a) denotes the proportion of never smokers who were living with partners who had ever smoked. The number of lung cancer cases is the product of the estimated PAF and the total number of lung cancer cases estimated among never smokers. The latter is obtained by multiplying the proportion of never smokers by the number of lung cancer cases not attributed to active smoking. Sensitivity analysis for active smoking We additionally performed sensitivity analysis to test different assumptions for active smoking, by applying alternative smoking prevalence and alternative RR estimates, and by including female breast cancer for which there is limited evidence of tobacco carcinogenicity. Detailed descriptions of methods and corresponding results are provided in the Supplementary methods and Supplementary tables S5 and S6. Results Active smoking Overall, 66 150 cancer cases (54 142 in men and 12 008 in women) were attributable to active smoking, accounting for 28 and 8% of all cancer cases diagnosed in 2015 among French men and women over 30 years old (table 2). Table 2 Estimated number (Tob. Attrib.) and proportion (PAF) of cancer cases attributable to active tobacco smoking by sex according to cancer site in France in 2015 Cancer site Males Females Total Lung Observed 29 097 11 353 40 450 Tob. Attrib. 25 494 7192 32 686 PAF (%) 88 63 81 Oral cavity & pharynx Observed 10 193 3060 13 253 Tob. Attrib. 8177 1281 9458 PAF (%) 80 42 71 Bladder Observed 10 307 2237 12 544 Tob. Attrib. 4046 287 4333 PAF (%) 39 13 35 Oesophagus Observed 4509 1108 5617 Tob. Attrib. 3101 497 3598 PAF (%) 69 45 64 Kidney Observed 8020 4072 12 092 Tob. Attrib. 2940 314 3254 PAF (%) 37 8 27 Larynx Observed 3025 415 3440 Tob. Attrib. 2547 281 2828 PAF (%) 84 68 82 Liver Observed 7359 1713 9072 Tob. Attrib. 2500 117 2617 PAF (%) 34 7 29 Colon & rectum Observed 21 824 17 822 39 646 Tob. Attrib. 1838 771 2608 PAF (%) 8 4 7 Pancreas Observed 5748 5554 11 302 Tob. Attrib. 1778 749 2527 PAF (%) 31 13 22 Stomach Observed 4745 2423 7168 Tob. Attrib. 1388 145 1533 PAF (%) 29 6 21 Acute myelogenous leukaemia Observed 1527 1364 2891 Tob. Attrib. 334 55 389 PAF (%) 22 4 13 Cervix Observed 2863 2863 Tob. Attrib. 265 265 PAF (%) 9 9 Mucinous ovary Observed 306 306 Tob. Attrib. 54 54 PAF (%) 18 18 Total Observed (All Sites) 190 254 155 919 346 173 Tob. Attrib. 54 142 12 008 66 150 PAF (%) 28 8 19 Cancer site Males Females Total Lung Observed 29 097 11 353 40 450 Tob. Attrib. 25 494 7192 32 686 PAF (%) 88 63 81 Oral cavity & pharynx Observed 10 193 3060 13 253 Tob. Attrib. 8177 1281 9458 PAF (%) 80 42 71 Bladder Observed 10 307 2237 12 544 Tob. Attrib. 4046 287 4333 PAF (%) 39 13 35 Oesophagus Observed 4509 1108 5617 Tob. Attrib. 3101 497 3598 PAF (%) 69 45 64 Kidney Observed 8020 4072 12 092 Tob. Attrib. 2940 314 3254 PAF (%) 37 8 27 Larynx Observed 3025 415 3440 Tob. Attrib. 2547 281 2828 PAF (%) 84 68 82 Liver Observed 7359 1713 9072 Tob. Attrib. 2500 117 2617 PAF (%) 34 7 29 Colon & rectum Observed 21 824 17 822 39 646 Tob. Attrib. 1838 771 2608 PAF (%) 8 4 7 Pancreas Observed 5748 5554 11 302 Tob. Attrib. 1778 749 2527 PAF (%) 31 13 22 Stomach Observed 4745 2423 7168 Tob. Attrib. 1388 145 1533 PAF (%) 29 6 21 Acute myelogenous leukaemia Observed 1527 1364 2891 Tob. Attrib. 334 55 389 PAF (%) 22 4 13 Cervix Observed 2863 2863 Tob. Attrib. 265 265 PAF (%) 9 9 Mucinous ovary Observed 306 306 Tob. Attrib. 54 54 PAF (%) 18 18 Total Observed (All Sites) 190 254 155 919 346 173 Tob. Attrib. 54 142 12 008 66 150 PAF (%) 28 8 19 Table 2 Estimated number (Tob. Attrib.) and proportion (PAF) of cancer cases attributable to active tobacco smoking by sex according to cancer site in France in 2015 Cancer site Males Females Total Lung Observed 29 097 11 353 40 450 Tob. Attrib. 25 494 7192 32 686 PAF (%) 88 63 81 Oral cavity & pharynx Observed 10 193 3060 13 253 Tob. Attrib. 8177 1281 9458 PAF (%) 80 42 71 Bladder Observed 10 307 2237 12 544 Tob. Attrib. 4046 287 4333 PAF (%) 39 13 35 Oesophagus Observed 4509 1108 5617 Tob. Attrib. 3101 497 3598 PAF (%) 69 45 64 Kidney Observed 8020 4072 12 092 Tob. Attrib. 2940 314 3254 PAF (%) 37 8 27 Larynx Observed 3025 415 3440 Tob. Attrib. 2547 281 2828 PAF (%) 84 68 82 Liver Observed 7359 1713 9072 Tob. Attrib. 2500 117 2617 PAF (%) 34 7 29 Colon & rectum Observed 21 824 17 822 39 646 Tob. Attrib. 1838 771 2608 PAF (%) 8 4 7 Pancreas Observed 5748 5554 11 302 Tob. Attrib. 1778 749 2527 PAF (%) 31 13 22 Stomach Observed 4745 2423 7168 Tob. Attrib. 1388 145 1533 PAF (%) 29 6 21 Acute myelogenous leukaemia Observed 1527 1364 2891 Tob. Attrib. 334 55 389 PAF (%) 22 4 13 Cervix Observed 2863 2863 Tob. Attrib. 265 265 PAF (%) 9 9 Mucinous ovary Observed 306 306 Tob. Attrib. 54 54 PAF (%) 18 18 Total Observed (All Sites) 190 254 155 919 346 173 Tob. Attrib. 54 142 12 008 66 150 PAF (%) 28 8 19 Cancer site Males Females Total Lung Observed 29 097 11 353 40 450 Tob. Attrib. 25 494 7192 32 686 PAF (%) 88 63 81 Oral cavity & pharynx Observed 10 193 3060 13 253 Tob. Attrib. 8177 1281 9458 PAF (%) 80 42 71 Bladder Observed 10 307 2237 12 544 Tob. Attrib. 4046 287 4333 PAF (%) 39 13 35 Oesophagus Observed 4509 1108 5617 Tob. Attrib. 3101 497 3598 PAF (%) 69 45 64 Kidney Observed 8020 4072 12 092 Tob. Attrib. 2940 314 3254 PAF (%) 37 8 27 Larynx Observed 3025 415 3440 Tob. Attrib. 2547 281 2828 PAF (%) 84 68 82 Liver Observed 7359 1713 9072 Tob. Attrib. 2500 117 2617 PAF (%) 34 7 29 Colon & rectum Observed 21 824 17 822 39 646 Tob. Attrib. 1838 771 2608 PAF (%) 8 4 7 Pancreas Observed 5748 5554 11 302 Tob. Attrib. 1778 749 2527 PAF (%) 31 13 22 Stomach Observed 4745 2423 7168 Tob. Attrib. 1388 145 1533 PAF (%) 29 6 21 Acute myelogenous leukaemia Observed 1527 1364 2891 Tob. Attrib. 334 55 389 PAF (%) 22 4 13 Cervix Observed 2863 2863 Tob. Attrib. 265 265 PAF (%) 9 9 Mucinous ovary Observed 306 306 Tob. Attrib. 54 54 PAF (%) 18 18 Total Observed (All Sites) 190 254 155 919 346 173 Tob. Attrib. 54 142 12 008 66 150 PAF (%) 28 8 19 In 2015, 32 686 (25 494 in men and 7192 in women) of the 40 450 lung cancer cases (29 097 in men and 11 353 in women) diagnosed in the French population aged 30 years and above were attributable to active smoking, corresponding to PAFs of 88% for men and 63% for women (table 3). Table 2 shows, in men and women respectively, the estimated numbers and proportions of cancer cases attributable to active smoking, by cancer sites. Detailed estimates by age are provided in Supplementary tables S2a and b. Besides lung, cancer sites that have the highest PAFs include larynx (84% in men and 68% in women), oral cavity and pharynx (80% in men and 42% in women) and oesophagus (69% in men and 45% in women). Cancer sites (besides lung) that account for the largest number of cases due to smoking include oral cavity and pharynx (8177 in men and 1281 in women), bladder (4046 in men and 287 in women) and oesophagus (3101 in men and 497 in women). Table 3 Estimated lung cancer cases and proportion (PAF) attributable to smoking according to sex in France in 2015 Males Females Age Population size (INSEE) Cases observed (FRANCIM) Rates in never smokers per 100 000 (CPS II) Cases in never smokers PAF (%) Cases attributable to smoking Population size (INSEE) Cases observed (FRANCIM) Rates in never smokers per 100 000 (CPS II) Cases in never smokers PAF (%) Cases attributable to smoking (1) (2) (3) (4)=(1)*(3) (5)=(6)/(2) (6)= (2)−(4) (1) (2) (3) (4)=(1)*(3) (5)=(6)/(2) (6)= (2)−(4) 30–34 1 975 801 56 1.6 32 44 24 2 039 647 51 2.5 51 0 0 35–39 1 943 589 106 2.4 47 56 59 1 972 714 100 3.2 63 37 37 40–44 2 196 838 285 3.4 75 74 210 2 214 598 248 4.3 95 62 153 45–49 2 150 383 925 4.8 103 89 822 2 196 770 576 6.2 136 76 440 50–54 2 119 033 1940 7.3 155 92 1785 2 201 318 969 8.8 194 80 775 55–59 1 985 794 3647 11.1 220 94 3427 2 111 389 1818 12.5 264 85 1554 60–64 1 898 518 4809 17.4 330 93 4479 2 063 366 1809 17.2 355 80 1454 65–69 1 715 932 5448 27 463 91 4985 1 898 126 1493 25 475 68 1018 70–74 1 099 046 4044 40.9 450 89 3594 1 279 448 1148 33.9 434 62 714 75–79 937 796 3290 61.1 573 83 2717 1 228 485 1172 46.6 572 51 600 80–84 726 400 2862 87.3 634 78 2228 1 128 190 1092 61.9 698 36 394 85+ 597 816 1685 87.3 522 69 1163 1 330 620 877 61.9 824 6 53 Total 19 346 946 29 097 – 3603 88 25 494 21 664 671 11 353 – 4161 63 7192 Males Females Age Population size (INSEE) Cases observed (FRANCIM) Rates in never smokers per 100 000 (CPS II) Cases in never smokers PAF (%) Cases attributable to smoking Population size (INSEE) Cases observed (FRANCIM) Rates in never smokers per 100 000 (CPS II) Cases in never smokers PAF (%) Cases attributable to smoking (1) (2) (3) (4)=(1)*(3) (5)=(6)/(2) (6)= (2)−(4) (1) (2) (3) (4)=(1)*(3) (5)=(6)/(2) (6)= (2)−(4) 30–34 1 975 801 56 1.6 32 44 24 2 039 647 51 2.5 51 0 0 35–39 1 943 589 106 2.4 47 56 59 1 972 714 100 3.2 63 37 37 40–44 2 196 838 285 3.4 75 74 210 2 214 598 248 4.3 95 62 153 45–49 2 150 383 925 4.8 103 89 822 2 196 770 576 6.2 136 76 440 50–54 2 119 033 1940 7.3 155 92 1785 2 201 318 969 8.8 194 80 775 55–59 1 985 794 3647 11.1 220 94 3427 2 111 389 1818 12.5 264 85 1554 60–64 1 898 518 4809 17.4 330 93 4479 2 063 366 1809 17.2 355 80 1454 65–69 1 715 932 5448 27 463 91 4985 1 898 126 1493 25 475 68 1018 70–74 1 099 046 4044 40.9 450 89 3594 1 279 448 1148 33.9 434 62 714 75–79 937 796 3290 61.1 573 83 2717 1 228 485 1172 46.6 572 51 600 80–84 726 400 2862 87.3 634 78 2228 1 128 190 1092 61.9 698 36 394 85+ 597 816 1685 87.3 522 69 1163 1 330 620 877 61.9 824 6 53 Total 19 346 946 29 097 – 3603 88 25 494 21 664 671 11 353 – 4161 63 7192 Table 3 Estimated lung cancer cases and proportion (PAF) attributable to smoking according to sex in France in 2015 Males Females Age Population size (INSEE) Cases observed (FRANCIM) Rates in never smokers per 100 000 (CPS II) Cases in never smokers PAF (%) Cases attributable to smoking Population size (INSEE) Cases observed (FRANCIM) Rates in never smokers per 100 000 (CPS II) Cases in never smokers PAF (%) Cases attributable to smoking (1) (2) (3) (4)=(1)*(3) (5)=(6)/(2) (6)= (2)−(4) (1) (2) (3) (4)=(1)*(3) (5)=(6)/(2) (6)= (2)−(4) 30–34 1 975 801 56 1.6 32 44 24 2 039 647 51 2.5 51 0 0 35–39 1 943 589 106 2.4 47 56 59 1 972 714 100 3.2 63 37 37 40–44 2 196 838 285 3.4 75 74 210 2 214 598 248 4.3 95 62 153 45–49 2 150 383 925 4.8 103 89 822 2 196 770 576 6.2 136 76 440 50–54 2 119 033 1940 7.3 155 92 1785 2 201 318 969 8.8 194 80 775 55–59 1 985 794 3647 11.1 220 94 3427 2 111 389 1818 12.5 264 85 1554 60–64 1 898 518 4809 17.4 330 93 4479 2 063 366 1809 17.2 355 80 1454 65–69 1 715 932 5448 27 463 91 4985 1 898 126 1493 25 475 68 1018 70–74 1 099 046 4044 40.9 450 89 3594 1 279 448 1148 33.9 434 62 714 75–79 937 796 3290 61.1 573 83 2717 1 228 485 1172 46.6 572 51 600 80–84 726 400 2862 87.3 634 78 2228 1 128 190 1092 61.9 698 36 394 85+ 597 816 1685 87.3 522 69 1163 1 330 620 877 61.9 824 6 53 Total 19 346 946 29 097 – 3603 88 25 494 21 664 671 11 353 – 4161 63 7192 Males Females Age Population size (INSEE) Cases observed (FRANCIM) Rates in never smokers per 100 000 (CPS II) Cases in never smokers PAF (%) Cases attributable to smoking Population size (INSEE) Cases observed (FRANCIM) Rates in never smokers per 100 000 (CPS II) Cases in never smokers PAF (%) Cases attributable to smoking (1) (2) (3) (4)=(1)*(3) (5)=(6)/(2) (6)= (2)−(4) (1) (2) (3) (4)=(1)*(3) (5)=(6)/(2) (6)= (2)−(4) 30–34 1 975 801 56 1.6 32 44 24 2 039 647 51 2.5 51 0 0 35–39 1 943 589 106 2.4 47 56 59 1 972 714 100 3.2 63 37 37 40–44 2 196 838 285 3.4 75 74 210 2 214 598 248 4.3 95 62 153 45–49 2 150 383 925 4.8 103 89 822 2 196 770 576 6.2 136 76 440 50–54 2 119 033 1940 7.3 155 92 1785 2 201 318 969 8.8 194 80 775 55–59 1 985 794 3647 11.1 220 94 3427 2 111 389 1818 12.5 264 85 1554 60–64 1 898 518 4809 17.4 330 93 4479 2 063 366 1809 17.2 355 80 1454 65–69 1 715 932 5448 27 463 91 4985 1 898 126 1493 25 475 68 1018 70–74 1 099 046 4044 40.9 450 89 3594 1 279 448 1148 33.9 434 62 714 75–79 937 796 3290 61.1 573 83 2717 1 228 485 1172 46.6 572 51 600 80–84 726 400 2862 87.3 634 78 2228 1 128 190 1092 61.9 698 36 394 85+ 597 816 1685 87.3 522 69 1163 1 330 620 877 61.9 824 6 53 Total 19 346 946 29 097 – 3603 88 25 494 21 664 671 11 353 – 4161 63 7192 Domestic passive smoking Table 4 shows, by age and sex, the proportion and number of lung cancer cases attributable to domestic passive smoking in 2015. Detailed estimates, including the estimated prevalence of never smokers living with an ever smoker in 2005 and the number of lung cancer cases among never smokers in 2015, are provided in Supplementary tables S4a and b. In sum, 36 and 142 lung cancer cases among male and female never smokers were attributable to exposure of smoking from a partner, corresponding to 4.2 and 6.7% of lung cancer occurring in male and female never smoker respectively. Table 4 Estimated number and proportion (PAF) of lung cancer cases attributable to domestic passive smoking in France in 2015 Age in 2015 (years) Males Females Never smokers in 2015 (%) Lung cancer cases not attributable to smoking Lung cancer cases among never smokers PAF of domestic passive smoking (%) Lung cancer cases attributable to domestic passive smoking Never smokers in 2015 (%) Lung cancer cases not attributable to smoking Lung cancer cases among never smokers PAF of domestic passive smoking (%) Lung cancer cases attributable to domestic passive smoking (1) (2) (3) (4) (5)=(4)/100*(3) (1) (2) (3) (4) (5)=(4)/100*(3) Source Baromètre 2014 Table 3 (3)=(1)/100*(2) Supplementary table S4a Baromètre 2014 Table 3 (3)=(1)/100*(2) Supplementary table S4b 30–34 26.0 32 8.2 0.3 0 37.8 51 19.3 0.7 0 35–39 30.1 47 14.0 2.4 0 32.6 63 20.6 3.1 1 40–44 28.4 75 21.2 5.5 1 36.6 95 34.9 5.2 2 45–49 23.7 103 24.5 7.3 2 36.3 136 49.4 6.7 3 50–54 27.0 155 41.8 7.9 3 34.9 194 67.6 7.1 5 55–59 20.4 220 45.0 7.4 3 37.1 264 97.9 8.2 8 60–64 19.7 330 65.1 6.9 5 46.2 355 164.0 8.6 14 65–69 19.4 463 89.9 4.8 4 49.0 475 232.5 9.3 22 70–74 24.5 450 110.1 4.4 5 56.3 434 244.2 8.9 22 75–79 24.5 573 140.4 3.2 4 56.3 572 322.3 8.6 28 80–84 24.5 634 155.4 3.0 5 56.3 698 393.2 6.8 27 85+ 24.5 522 127.9 2.4 3 56.3 824 463.7 2.4 11 Total – 3603 843 4.2 36 – 4161 2110 6.7 142 Age in 2015 (years) Males Females Never smokers in 2015 (%) Lung cancer cases not attributable to smoking Lung cancer cases among never smokers PAF of domestic passive smoking (%) Lung cancer cases attributable to domestic passive smoking Never smokers in 2015 (%) Lung cancer cases not attributable to smoking Lung cancer cases among never smokers PAF of domestic passive smoking (%) Lung cancer cases attributable to domestic passive smoking (1) (2) (3) (4) (5)=(4)/100*(3) (1) (2) (3) (4) (5)=(4)/100*(3) Source Baromètre 2014 Table 3 (3)=(1)/100*(2) Supplementary table S4a Baromètre 2014 Table 3 (3)=(1)/100*(2) Supplementary table S4b 30–34 26.0 32 8.2 0.3 0 37.8 51 19.3 0.7 0 35–39 30.1 47 14.0 2.4 0 32.6 63 20.6 3.1 1 40–44 28.4 75 21.2 5.5 1 36.6 95 34.9 5.2 2 45–49 23.7 103 24.5 7.3 2 36.3 136 49.4 6.7 3 50–54 27.0 155 41.8 7.9 3 34.9 194 67.6 7.1 5 55–59 20.4 220 45.0 7.4 3 37.1 264 97.9 8.2 8 60–64 19.7 330 65.1 6.9 5 46.2 355 164.0 8.6 14 65–69 19.4 463 89.9 4.8 4 49.0 475 232.5 9.3 22 70–74 24.5 450 110.1 4.4 5 56.3 434 244.2 8.9 22 75–79 24.5 573 140.4 3.2 4 56.3 572 322.3 8.6 28 80–84 24.5 634 155.4 3.0 5 56.3 698 393.2 6.8 27 85+ 24.5 522 127.9 2.4 3 56.3 824 463.7 2.4 11 Total – 3603 843 4.2 36 – 4161 2110 6.7 142 Table 4 Estimated number and proportion (PAF) of lung cancer cases attributable to domestic passive smoking in France in 2015 Age in 2015 (years) Males Females Never smokers in 2015 (%) Lung cancer cases not attributable to smoking Lung cancer cases among never smokers PAF of domestic passive smoking (%) Lung cancer cases attributable to domestic passive smoking Never smokers in 2015 (%) Lung cancer cases not attributable to smoking Lung cancer cases among never smokers PAF of domestic passive smoking (%) Lung cancer cases attributable to domestic passive smoking (1) (2) (3) (4) (5)=(4)/100*(3) (1) (2) (3) (4) (5)=(4)/100*(3) Source Baromètre 2014 Table 3 (3)=(1)/100*(2) Supplementary table S4a Baromètre 2014 Table 3 (3)=(1)/100*(2) Supplementary table S4b 30–34 26.0 32 8.2 0.3 0 37.8 51 19.3 0.7 0 35–39 30.1 47 14.0 2.4 0 32.6 63 20.6 3.1 1 40–44 28.4 75 21.2 5.5 1 36.6 95 34.9 5.2 2 45–49 23.7 103 24.5 7.3 2 36.3 136 49.4 6.7 3 50–54 27.0 155 41.8 7.9 3 34.9 194 67.6 7.1 5 55–59 20.4 220 45.0 7.4 3 37.1 264 97.9 8.2 8 60–64 19.7 330 65.1 6.9 5 46.2 355 164.0 8.6 14 65–69 19.4 463 89.9 4.8 4 49.0 475 232.5 9.3 22 70–74 24.5 450 110.1 4.4 5 56.3 434 244.2 8.9 22 75–79 24.5 573 140.4 3.2 4 56.3 572 322.3 8.6 28 80–84 24.5 634 155.4 3.0 5 56.3 698 393.2 6.8 27 85+ 24.5 522 127.9 2.4 3 56.3 824 463.7 2.4 11 Total – 3603 843 4.2 36 – 4161 2110 6.7 142 Age in 2015 (years) Males Females Never smokers in 2015 (%) Lung cancer cases not attributable to smoking Lung cancer cases among never smokers PAF of domestic passive smoking (%) Lung cancer cases attributable to domestic passive smoking Never smokers in 2015 (%) Lung cancer cases not attributable to smoking Lung cancer cases among never smokers PAF of domestic passive smoking (%) Lung cancer cases attributable to domestic passive smoking (1) (2) (3) (4) (5)=(4)/100*(3) (1) (2) (3) (4) (5)=(4)/100*(3) Source Baromètre 2014 Table 3 (3)=(1)/100*(2) Supplementary table S4a Baromètre 2014 Table 3 (3)=(1)/100*(2) Supplementary table S4b 30–34 26.0 32 8.2 0.3 0 37.8 51 19.3 0.7 0 35–39 30.1 47 14.0 2.4 0 32.6 63 20.6 3.1 1 40–44 28.4 75 21.2 5.5 1 36.6 95 34.9 5.2 2 45–49 23.7 103 24.5 7.3 2 36.3 136 49.4 6.7 3 50–54 27.0 155 41.8 7.9 3 34.9 194 67.6 7.1 5 55–59 20.4 220 45.0 7.4 3 37.1 264 97.9 8.2 8 60–64 19.7 330 65.1 6.9 5 46.2 355 164.0 8.6 14 65–69 19.4 463 89.9 4.8 4 49.0 475 232.5 9.3 22 70–74 24.5 450 110.1 4.4 5 56.3 434 244.2 8.9 22 75–79 24.5 573 140.4 3.2 4 56.3 572 322.3 8.6 28 80–84 24.5 634 155.4 3.0 5 56.3 698 393.2 6.8 27 85+ 24.5 522 127.9 2.4 3 56.3 824 463.7 2.4 11 Total – 3603 843 4.2 36 – 4161 2110 6.7 142 Discussion Overall, 66 150 (or 19%) of all new cancer cases among adults in France in 2015 can be attributable to active smoking, representing 28 and 8% of all cancer cases diagnosed in men and women over 30 years of age. Almost half of those cases (32 686) were lung cancer. Among never smokers, past exposure to domestic passive smoking caused 178 cases of lung cancer. Our results are consistent with previous studies. In 2000, 27% of the cancer cases in men and 6% in women in France were found to be attributable to active smoking22 vs. 28 and 8% in 2015 in this study. While prevalence of current smoking in men has declined progressively from about 60% in early 1970s to around 40% in 2000 and remained relatively stable thereafter, it has increased progressively in women from about 25% to over 30% during the same period.23 In 2014, the prevalence estimates in men and women were 38 and 30%, respectively.7 This overall male-downward and female-upward trends in smoking prevalence have been reflected in smoking-attributable deaths. Deaths due to smoking in French men decreased from 66 000 in 1985 to 59 000 in 2010, corresponding to PAFs of 23 and 21%, respectively. In contrast, deaths in French women increased from 4700 in 1985 to 19 000 in 2010, corresponding to PAFs of 1 and 7%.24 Consequently, smoking-related cancer burden is expected to increase among females in the foreseeable future, given the ascending trend in smoking observed in French women. Also worrisome is the high and rising prevalence of adolescent smoking, e.g. the prevalence of 16-year olds daily smokers increased from 17% in 2007–08 to 23% in 2011.23 Several limitations should be considered. First, we used the lung cancer incidence rates among never smokers in the US to estimate the PAFs for lung cancer in France, assuming the factors that cause lung cancer among never smokers and the exposure to these factors among never smokers to be identical in both populations. Second, the sensitivity analyses using RRs from CPS II and smoking prevalence in France (with different latency times) are not ideal, as it assumes that the smokers in France and in the CPS II cohort have the same past smoking history. Results from sensitivity analysis (see Supplementary material) using RRs from the European Prospective Investigation into Cancer and Nutrition (EPIC) study suggest that this may be a concern for the PAF estimates for some cancer sites (e.g. oesophagus) where the RRs from the CPS II and the EPIC study differ markedly. Third, for most cancer sites, we used the RRs of deaths instead of incidence. This is based on (i) the assumption that the death rates are the same among cancer patients whether their cancer is tobacco related or not and (ii) the clear advantage of using RR estimates from a study with large sample-size and long duration of follow-up i.e. 20 years in CPS II. As for domestic passive smoking, the RRs were derived from never smokers currently living with smokers. The corresponding PAF is therefore likely to be underestimated since the estimation fails to account for: (i) never smokers who have previously lived with a smoking partner and separated only recently; (ii) never smokers currently living with a former smoker who quit smoking only recently. To reduce this bias, following Parkin (2011), we estimated the PAF using the proportion of never smokers who were living with someone who had ever smoked in 2005. However, we may still have underestimated the true burden of passive smoking. First, the best data source we could find for marital status does not include unmarried partners living together, a common demographic status in France. Second, the current analysis does not include exposure to smoking from cohabiting members other than their partners, as such data are lacking. All these limitations are potential sources of underestimation. Additionally, the choice of 10-year latency for lung cancer in never smokers is arbitrarily based on data availability and the assumption that the prevalence of living with an ever-smoking partner has been constant over the past 2–3 decades. This could also lead to underestimations, as the level of passive exposure to indoor smoking was likely higher in the 1990s due to limited awareness of the harmful effects of passive smoking on health and tobacco control regulations in place. Finally, we were unable to assess the PAFs for exposure to passive smoking at workplaces and other public spaces due to lack of data. In conclusion, smoking was responsible for a significant share of cancer cases in France in 2015. Over the past decades, legislation has been passed to reduce tobacco consumption and exposure to second-hand tobacco smoke (e.g. loi Veil, 1976; loi Evin, 1991; décret, 2006).25 Comprehensive smoking-free policy was further strengthened in February 2007 for workplaces, shopping centres, transportation hubs, hospitals and schools.26 Subsequently, the bans were extended to hospitality places, such as bars, restaurants, hotels and casinos in January 2008.26 Despite France’s commendable initiatives to de-normalize tobacco use, including the recent adoption of plain packaging, tobacco taxation and advertizing restrictions, a sizeable proportion of the country’s population are currently tobacco smokers. France also remains one of the highest tobacco-consuming developed countries, falling behind the U.K., Canada, Australia and New Zealand which all have reduced smoking prevalence to below 20% (vs. over 30% in France).27,28 Accordingly, the present and predicted smoking pattern in France and its impact on population health should be alarming to the pro-tobacco control stakeholders. Due to the long latency time between smoking and the occurrence of cancer, and the high historical smoking prevalence in France, cancer incidence and mortality are not likely to decline in the foreseeable future, particularly for female cohorts that smoked most heavily and are still young. More tobacco control policies specifically targeting females should be devised. Given the recent rise in tobacco consumption in 2005–10 (has stabilized since) and the rising smoking prevalence among adolescents, the long-term smoking-related cancer burden may continue to increase.7,29 Hence, more in-depth research must be done to better understand the reasons for the present failures to reduce tobacco consumption despite generally strong tobacco control policies.28 Specifically, we need to investigate how increases in the retail price of tobacco products and their magnitude affect consumption, why its positive effects on consumption have often not been sustained over time in France, and whether periodic adjustment by changing the affordability will address this. As 17% of smokers in France used the less expensive roll-your-own cigarettes in 2010, monitoring the consumption and regulating the price of cheap cigarettes and other substitute products are also necessary.30 Meanwhile, reinforcement and adoption of more effective regulations on smoking are needed to achieve sustained reduction in smoking and thus lower the cancer burden in France. Supplementary data Supplementary data are available at EURPUB online. Acknowledgements The authors would like to thank Drs. D. Max Parkin, Lesley Rushton and the Steering Committee of the project entitled ‘Définition des priorités pour la prévention du cancer en France métropolitaine: la fraction de cancers attribuables aux modes de vie et aux facteurs environnementaux’. The authors would also like to thank the French Cancer Registries Network (FRANCIM) for providing cancer incidence data for France. Funding This work was funded by the French National Cancer Institute (INCa, grant nr. 2015-002). The funding source had no role in the collection, analysis or interpretation of the data or in the decision to submit the manuscript for publication. Conflicts of interest: None declared. Key points A total of 54 142 and 12 008 cancer cases, in adult (30+ years old) males and females respectively, were attributable to active smoking in France in 2015. Cancer sites that account for the largest number of cases due to smoking include lung, oral cavity and pharynx, bladder and oesophagus. A total of 36 and 142 of all lung cancer cases, among adult male and female never smokers respectively, were attributable to second-hand smoke resulting from their partner’s active smoking. Cancer incidence and mortality are not likely to decline in the foreseeable future in France, given its high historical smoking prevalence. Effective tobacco control regulations need to be adopted and strengthened to achieve sustained reduction in smoking and thus reduce the cancer burden in France. References 1 Wynder EL , Graham EA . Tobacco smoking as a possible etiologic factor in bronchiogenic carcinoma: a study of six hundred and eighty-four proved cases . JAMA 1950 ; 143 : 329 – 36 . Google Scholar CrossRef Search ADS 2 Doll R , Hill AB . Smoking and carcinoma of the lung: preliminary report . Br Med J 1950 ; 2 : 739 – 48 . Google Scholar CrossRef Search ADS PubMed 3 United States Public Health Service . Report of the Advisory Committee to the Surgeon General of the Public Health Service: Smoking and health. 1964 . 4 International Agency for Research on Cancer (IARC) . Tobacco smoke and involuntary smoking . IARC Monogr Eval Carcinog Risks Hum 2004 ; 83 : 1 – 1473 . PubMed 5 International Agency for Research on Cancer (IARC) . Personal habits and indoor combustions . IARC Monogr Eval Carcinog Risks Hum 2012 ; 100 : 1 – 538 . 6 European Commission . Attitudes of Europeans towards tobacco and electronic cigarettes . Spec Eurobarom 2015 ; 429 : 214 . 7 Guignard R , Beck F , Richard J , Lermenier A , Wilquin J-L , Nguyen-Thanh V . La consommation de tabac en France en 2014 : caractéristiques et évolutions récentes . Evolutions 2015 ; 31 : 1 – 6 . 8 Plan Cancer 2014-2019 . Objectif 10: Programme national de réduction du tabagisme 2014-2019. 2015 . 9 Peto R , Lopez AD , Boreham J , et al. Mortality from tobacco in developed countries: indirect estimation from national vital statistics . Lancet 1992 ; 339 : 1268 – 78 . Google Scholar CrossRef Search ADS PubMed 10 Parkin DM . Tobacco-attributable cancer burden in the UK in 2010 . Br J Cancer 2011 ; 105 : S6 – 13 . Google Scholar CrossRef Search ADS PubMed 11 Pandeya N , Wilson LF , Bain CJ , et al. Cancers in Australia in 2010 attributable to tobacco smoke . Aust N Z J Public Health 2015 ; 39 : 464 – 70 . Google Scholar CrossRef Search ADS PubMed 12 Garfinkel L . Cancer mortality in nonsmokers: prospective study by the American Cancer Society . 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Available at: https://www.insee.fr/. 18 Santé Pays De La Loire . Le réseau FRANCIM : Les registres des cancers en France . 2015 . 19 Levin M . The occurrence of lung cancer in man . Acta Unio Int Contra Cancrum 1953 ; 9 : 531 – 41 . Google Scholar PubMed 20 Institut national de prévention et d’éducation pour la santé . Baromètre santé 2005. 2006 . Available at: http://inpes.santepubliquefrance.fr/Barometres/BS2005/ouvrage/index.asp. 21 Wald NJ , Nanchahal K , Thompson SG , Cuckle HS . Does breathing other people’s tobacco smoke cause lung cancer? Br Med J (Clin Res Ed) 1986 ; 293 : 1217 – 22 . Google Scholar CrossRef Search ADS PubMed 22 International Agency for Research on Cancer (IARC) . IARC Working Group Reports: Attributable causes of cancer in France in the Year 2000. 2007 . 23 L’Observatoire français des drogues et des toxicomanies (OFDT). Drogues et addictions, données essentielles. 2013 . 24 Ribassin-Majed L , Hill C . Trends in tobacco-attributable mortality in France . Eur J Public Health 2015 ; 25 : 824 – 8 . Google Scholar CrossRef Search ADS PubMed 25 Santé Publique France . La législation antitabac en France. Available at: http://inpes.santepubliquefrance.fr/10000/themes/tabac/legislation.asp. 26 Fong GT , Craig LV , Guignard R , et al. Evaluation of the smoking ban in public places in France one year and five years after its implementation: findings from the ITC France survey . Bull Epidemiol Hebd (Paris) 2013 ; 20 : 217 – 23 . Google Scholar PubMed 27 Lermenier-Jeannet A . Tobacco in France: overview of 2004–2014. Tendances 2014 ; 92 : 1 – 6 . 28 McNeill A , Guignard R , Beck F , et al. Understanding increases in smoking prevalence: case study from France in comparison with England 2000-10 . Addiction 2015 ; 110 : 392 – 400 . Google Scholar CrossRef Search ADS PubMed 29 Guignard R , Beck F , Richard J , Peretti-watel P . Le tabagisme en France. Analyse de l'enquête Baromètre santé 2010. Institut national de prévention et d'éducation pour la santé (INPES) . Saint Denis 2013 ; 56 pages. 30 Currie L , Townsend J , Leon M , et al. Policy recommendations for tobacco taxation in the European Union integrated research findings from the PPACTE project. 2012 . © The Author(s) 2018. Published by Oxford University Press on behalf of the European Public Health Association. All rights reserved. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png The European Journal of Public Health Oxford University Press

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© The Author(s) 2018. Published by Oxford University Press on behalf of the European Public Health Association. All rights reserved.
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Abstract

Abstract Background The evidence on the carcinogenicity of tobacco smoking has been well established. An assessment of the population-attributable fraction (PAF) of cancer due to smoking is needed for France, given its high smoking prevalence. Methods We extracted age- and sex-specific national estimates of population and cancer incidence for France, and incidence rates of lung cancer among never smokers and relative risk (RR) estimates of smoking for various cancers from the American Cancer Prevention Study (CPS II). For active smoking, we applied a modified indirect method to estimate the PAF for lung and other tobacco smoking-related cancer sites. Using the RR estimates for second-hand smoking, the proportion of never smokers living with an ever-smoking partner derived from survey, and marital status data, we then estimated the PAF for lung cancer attributable to domestic passive smoking. Results Overall in France in 2015, 54 142 and 12 008 cancer cases in males and females, respectively, were attributable to active smoking, accounting for 28 and 8% of all cancer cases observed among adult (30+ years) males and females. Additionally, 36 and 142 lung cancer cases, respectively among male and female never smokers, were attributable to second-hand smoke resulting from their partner’s active smoking, corresponding to 4.2 and 6.7% of lung cancer cases which occurred in never smoker males and females, respectively. Conclusions Tobacco smoking is responsible for a significant number of potentially avoidable cancer cases in France in 2015. More effective tobacco control programmes are critical to reduce this cancer burden. Introduction The evidence on the carcinogenicity of tobacco smoking has grown vastly since the reports of an association between cigarette smoking and carcinoma of the lung in 1950.1–3 The International Agency for Research on Cancer (IARC) has included cancers of the lung, larynx, oral cavity, pharynx, nasal cavity and paranasal sinuses, oesophagus, stomach, pancreas, liver, kidney, ureter, bladder, uterine cervix, colon and rectum, acute myeloid leukaemia and the mucinous tumours of the ovary in the list of cancers caused by tobacco smoking.4,5 Exposure to second-hand smoke has also been found to increase the risk of lung cancer in never smokers and has been classified as carcinogenic.4 France is one of the high-income European countries with the highest daily smoking prevalence: in 2014, 28% (32% in men and 24% in women) of the French population were daily tobacco smokers.6,7 In order to reduce the smoking prevalence in France, the public health authority has launched a national programme of tobacco control (Programme national de réduction du tabagisme), aiming to reduce the number of daily smokers by 10% in 2019.8 It is therefore of great public health interest to provide the up-to-date estimates of the proportion and number of cancers attributable to active and passive smoking. This article provides, for 2015, estimates of the number and proportion of cancer cases attributable to active smoking in France for all cancers identified by IARC to be caused by smoking. It also estimates the number and proportion of lung cancer cases among never smokers due to exposure to passive smoking in their home. Methods Estimation of population-attributable fractions Active smoking We estimated the population-attributable fractions (PAFs) and numbers of cancer cases attributable to cigarette smoking using an indirect method of Peto and Lopez (1992),9 modified by Parkin (2011) and used in similar projects for the UK and Australia.10,11 This method relies on two main assumptions for high-income populations: (i) active tobacco smoking is the most important risk factor for lung cancer; (ii) lung cancer incidence among never smokers is fairly small and roughly constant across populations of a given sex and age. The number of lung cancers due to active smoking can be calculated as the difference between the observed number of lung cancers and the expected number if the population had the incidence rate of never smokers. Data The data required for the analysis include, from the same population, the sex and age-specific incidence rates of lung cancer among never smokers and relative risks (RRs) for individual cancers in smokers in comparison to never smokers.12–14 We used the lung cancer incidence rates in never smokers reported in Parkin (2011), which are estimated from lung cancer death rates in the second Cancer Prevention Study (CPS II study) for the period 1982–02.10,13 The CPS II is an American prospective cohort study, involving roughly 1.2 million participants, over 30 years old at the baseline survey in 1982 with a 20-year follow-up.12,13 Similar to previous studies, we used for most cancer sites the RRs of death from cancer among current smokers as compared to never smokers from analyses based on the CPS II study. We chose to use the RRs of cancer death instead of incidence, because they are estimated from cohort studies with long duration of follow-up and sample-size large enough to produce accurate risk estimates even for less common cancers. However, for mucinous ovarian cancer, the RR estimate for cancer incidence from a meta-analysis by Jordan et al. (2006) was used, as no RR for mortality or incidence have been estimated for the CPS II cohort.15 And for colorectal cancer, we used the RR for cancer incidence estimated by Hannan et al. (2009) from the follow-up of the CPS II Nutrition Cohort.16 Most other RRs are derived from the CPS II study re-analysis conducted by Ezzati et al. (2005) adjusted for important covariates (including age, race, marital status, education, employment, food and alcohol consumption).14 The RRs used are listed in table 1 with their sources. Table 1 Estimated relative risks (RRs)a of dying from cancers for current smokers compared to never smokers by cancer sites Cancer site ICD10 Relative risk (95% CI) Reference Males Females Oral cavity & pharynx C01–14 10.9 5.1 US Surgeon General’s report 20043 Oesophagus C15 6.8 7.8 US Surgeon General’s report 20043 Stomach C16 2.2 (1.8–2.7) 1.5 (1.2–1.9) Ezzati et al. 200514 Colon-rectum C18–20 1.2 (1.0–1.6) 1.3 (1.0–1.7) Hannan et al. 200916 Liver C22 2.3 (1.5–3.8) 1.5 (0.8–2.7) Ezzati et al. 200514 Pancreas C25 2.2 (1.7–2.8) 2.2 (1.8–2.8) Ezzati et al. 200514 Larynx C32 14.6 13.0 US Surgeon General's report 20043 Lung C33–34 21.3 (17.7–25.6) 12.5 (10.9–14.3) Ezzati et al. 200514 Cervix C53 1.5 (0.9–2.6) Ezzati et al. 200514 Ovary (mucinous) C56.9 2.1 (1.7–2.7) Jordan et al. 200615 Kidney C64–66, C68 2.5 (1.8–3.6) 1.5 (1.0–2.1) Ezzati et al. 200514 Urinary bladder C67 3.0 (2.1–4.3) 2.4 (1.5–4.1) Ezzati et al. 200514 Acute myelogenous leukaemia C92.0 1.9 (1.3–2.9) 1.2 (0.8–1.8) Ezzati et al. 200514 Cancer site ICD10 Relative risk (95% CI) Reference Males Females Oral cavity & pharynx C01–14 10.9 5.1 US Surgeon General’s report 20043 Oesophagus C15 6.8 7.8 US Surgeon General’s report 20043 Stomach C16 2.2 (1.8–2.7) 1.5 (1.2–1.9) Ezzati et al. 200514 Colon-rectum C18–20 1.2 (1.0–1.6) 1.3 (1.0–1.7) Hannan et al. 200916 Liver C22 2.3 (1.5–3.8) 1.5 (0.8–2.7) Ezzati et al. 200514 Pancreas C25 2.2 (1.7–2.8) 2.2 (1.8–2.8) Ezzati et al. 200514 Larynx C32 14.6 13.0 US Surgeon General's report 20043 Lung C33–34 21.3 (17.7–25.6) 12.5 (10.9–14.3) Ezzati et al. 200514 Cervix C53 1.5 (0.9–2.6) Ezzati et al. 200514 Ovary (mucinous) C56.9 2.1 (1.7–2.7) Jordan et al. 200615 Kidney C64–66, C68 2.5 (1.8–3.6) 1.5 (1.0–2.1) Ezzati et al. 200514 Urinary bladder C67 3.0 (2.1–4.3) 2.4 (1.5–4.1) Ezzati et al. 200514 Acute myelogenous leukaemia C92.0 1.9 (1.3–2.9) 1.2 (0.8–1.8) Ezzati et al. 200514 a RRs used for the main analysis. Table 1 Estimated relative risks (RRs)a of dying from cancers for current smokers compared to never smokers by cancer sites Cancer site ICD10 Relative risk (95% CI) Reference Males Females Oral cavity & pharynx C01–14 10.9 5.1 US Surgeon General’s report 20043 Oesophagus C15 6.8 7.8 US Surgeon General’s report 20043 Stomach C16 2.2 (1.8–2.7) 1.5 (1.2–1.9) Ezzati et al. 200514 Colon-rectum C18–20 1.2 (1.0–1.6) 1.3 (1.0–1.7) Hannan et al. 200916 Liver C22 2.3 (1.5–3.8) 1.5 (0.8–2.7) Ezzati et al. 200514 Pancreas C25 2.2 (1.7–2.8) 2.2 (1.8–2.8) Ezzati et al. 200514 Larynx C32 14.6 13.0 US Surgeon General's report 20043 Lung C33–34 21.3 (17.7–25.6) 12.5 (10.9–14.3) Ezzati et al. 200514 Cervix C53 1.5 (0.9–2.6) Ezzati et al. 200514 Ovary (mucinous) C56.9 2.1 (1.7–2.7) Jordan et al. 200615 Kidney C64–66, C68 2.5 (1.8–3.6) 1.5 (1.0–2.1) Ezzati et al. 200514 Urinary bladder C67 3.0 (2.1–4.3) 2.4 (1.5–4.1) Ezzati et al. 200514 Acute myelogenous leukaemia C92.0 1.9 (1.3–2.9) 1.2 (0.8–1.8) Ezzati et al. 200514 Cancer site ICD10 Relative risk (95% CI) Reference Males Females Oral cavity & pharynx C01–14 10.9 5.1 US Surgeon General’s report 20043 Oesophagus C15 6.8 7.8 US Surgeon General’s report 20043 Stomach C16 2.2 (1.8–2.7) 1.5 (1.2–1.9) Ezzati et al. 200514 Colon-rectum C18–20 1.2 (1.0–1.6) 1.3 (1.0–1.7) Hannan et al. 200916 Liver C22 2.3 (1.5–3.8) 1.5 (0.8–2.7) Ezzati et al. 200514 Pancreas C25 2.2 (1.7–2.8) 2.2 (1.8–2.8) Ezzati et al. 200514 Larynx C32 14.6 13.0 US Surgeon General's report 20043 Lung C33–34 21.3 (17.7–25.6) 12.5 (10.9–14.3) Ezzati et al. 200514 Cervix C53 1.5 (0.9–2.6) Ezzati et al. 200514 Ovary (mucinous) C56.9 2.1 (1.7–2.7) Jordan et al. 200615 Kidney C64–66, C68 2.5 (1.8–3.6) 1.5 (1.0–2.1) Ezzati et al. 200514 Urinary bladder C67 3.0 (2.1–4.3) 2.4 (1.5–4.1) Ezzati et al. 200514 Acute myelogenous leukaemia C92.0 1.9 (1.3–2.9) 1.2 (0.8–1.8) Ezzati et al. 200514 a RRs used for the main analysis. The size of the French population in 2015 by sex and age group was obtained from the French National Institute for Statistics and Economic Studies datasets (INSEE).17 The number of cancer cases in France in 2015 by age, sex and site was estimated by applying the observed incidence rates for 2013 reported by the national network of cancer registries (FRANCIM) to the 2015 population.18 To estimate the number of mucinous ovarian cancers, we applied the age-specific proportions of mucinous ovarian cancers reported by the FRANCIM for 2009–13 (shown in Supplementary table S1) to the age-specific numbers of ovarian cancer cases estimated for 2015. Analysis The statistical analysis was performed in two steps. First, we calculated the expected number of lung cancer cases in France if smoking was absent for a given sex s and age a, by multiplying the sex- and age-specific lung cancer rate among never smokers ILs,a from the CPS II study by the corresponding population size Ns,a in France in 2015. The number of lung cancer cases attributable to smoking was estimated as the difference between the observed number of lung cancer cases OLs,a and the expected number in the absence of smoking in 2015. The PAF for lung cancer due to tobacco smoking is then estimated as PAFLs,a=OLs,a-ILs,aNs,aOLs,a (1) For all the other cancer sites i, we used the conventional PAF formula,19 for each sex and age category: PAFis,a=Pes,arris-11+Pes,arris-1  (2) where Pes,a  is the pseudo smoking prevalence in the population, and rris the RR for cancer site i in smokers as compared to never smokers. Pes,a was calculated as the expected proportion of tobacco smokers in the French population which explains the estimated smoking-attributable fraction of lung cancers using the RR of lung cancer rrLs  provided by the CPS II study.10 It summarizes the cumulative effect of the smoking history among former and current smokers in the population with a single indicator. Pes,a= PAFLs,a1-PAFLs,arrLs-1  (3) Having calibrated the prevalence of smoking on the risk in the CPS II population, one can use Equation (2) to estimate the corresponding PAFs. The numbers of cancer cases attributable to smoking for each site are the products of the PAFs and the total incidence for each site. Domestic passive smoking Because never smokers exposed to second-hand smoke are at increased risk of lung cancer, we estimate the PAF and the number of lung cancer cases attributable to passive smoking. Due to lack of exposure data for passive smoking in workplaces and other public areas, we restrict the analysis to domestic passive smoking. Data The RR estimates of passive smoking on lung cancer are most robust for never smokers who have lived with a partner who smokes. Because data on exposure to passive smoking at work and other public places in France are not readily available, we restrict the analysis to never smokers who were living in the same household as a smoking partner. Relative risks The RRs for lung cancer incidence in never smokers who were exposed to tobacco smoke from a smoking partner were obtained from the meta-analysis published in the IARC Monograph volume 83 (2004).4 The RRs for males and females never smokers were 1.37 (95% CI 1.02–1.82) and 1.24 (95% CI 1.14–1.34), respectively. Exposure Because there is no data available in France on the proportion of never smokers living with a smoker, it was estimated following the methods described by Parkin (2011).10 Briefly, we used the marital status data in 2005 published by INSEE and the tobacco smoking prevalence (categorized in never, former and current smoker) from a 2005 national health survey (Baromètre Santé, 2005),20 allowing a 10-year latency time for the occurrence of lung cancer. Both data are available by sex and five-year age groups in 2005. Recognizing that couples tend to be concordant for smoking status and as proposed by Wald et al. (1986)21 and used by Parkin (2011),10 we assumed that ever smokers and never smokers were three times more likely to live with a partner with the same smoking status than with one having different smoking status. We also assumed that couples were in the same five-year age-group. The estimation is detailed in Supplementary table S3. Analysis The corresponding PAFs are estimated using the conventional equation PAFs,a=PNwT(s,a)(RR(s)-1)PNwTs,aRR(s)-1+1 (4) where PNwT(s, a) denotes the proportion of never smokers who were living with partners who had ever smoked. The number of lung cancer cases is the product of the estimated PAF and the total number of lung cancer cases estimated among never smokers. The latter is obtained by multiplying the proportion of never smokers by the number of lung cancer cases not attributed to active smoking. Sensitivity analysis for active smoking We additionally performed sensitivity analysis to test different assumptions for active smoking, by applying alternative smoking prevalence and alternative RR estimates, and by including female breast cancer for which there is limited evidence of tobacco carcinogenicity. Detailed descriptions of methods and corresponding results are provided in the Supplementary methods and Supplementary tables S5 and S6. Results Active smoking Overall, 66 150 cancer cases (54 142 in men and 12 008 in women) were attributable to active smoking, accounting for 28 and 8% of all cancer cases diagnosed in 2015 among French men and women over 30 years old (table 2). Table 2 Estimated number (Tob. Attrib.) and proportion (PAF) of cancer cases attributable to active tobacco smoking by sex according to cancer site in France in 2015 Cancer site Males Females Total Lung Observed 29 097 11 353 40 450 Tob. Attrib. 25 494 7192 32 686 PAF (%) 88 63 81 Oral cavity & pharynx Observed 10 193 3060 13 253 Tob. Attrib. 8177 1281 9458 PAF (%) 80 42 71 Bladder Observed 10 307 2237 12 544 Tob. Attrib. 4046 287 4333 PAF (%) 39 13 35 Oesophagus Observed 4509 1108 5617 Tob. Attrib. 3101 497 3598 PAF (%) 69 45 64 Kidney Observed 8020 4072 12 092 Tob. Attrib. 2940 314 3254 PAF (%) 37 8 27 Larynx Observed 3025 415 3440 Tob. Attrib. 2547 281 2828 PAF (%) 84 68 82 Liver Observed 7359 1713 9072 Tob. Attrib. 2500 117 2617 PAF (%) 34 7 29 Colon & rectum Observed 21 824 17 822 39 646 Tob. Attrib. 1838 771 2608 PAF (%) 8 4 7 Pancreas Observed 5748 5554 11 302 Tob. Attrib. 1778 749 2527 PAF (%) 31 13 22 Stomach Observed 4745 2423 7168 Tob. Attrib. 1388 145 1533 PAF (%) 29 6 21 Acute myelogenous leukaemia Observed 1527 1364 2891 Tob. Attrib. 334 55 389 PAF (%) 22 4 13 Cervix Observed 2863 2863 Tob. Attrib. 265 265 PAF (%) 9 9 Mucinous ovary Observed 306 306 Tob. Attrib. 54 54 PAF (%) 18 18 Total Observed (All Sites) 190 254 155 919 346 173 Tob. Attrib. 54 142 12 008 66 150 PAF (%) 28 8 19 Cancer site Males Females Total Lung Observed 29 097 11 353 40 450 Tob. Attrib. 25 494 7192 32 686 PAF (%) 88 63 81 Oral cavity & pharynx Observed 10 193 3060 13 253 Tob. Attrib. 8177 1281 9458 PAF (%) 80 42 71 Bladder Observed 10 307 2237 12 544 Tob. Attrib. 4046 287 4333 PAF (%) 39 13 35 Oesophagus Observed 4509 1108 5617 Tob. Attrib. 3101 497 3598 PAF (%) 69 45 64 Kidney Observed 8020 4072 12 092 Tob. Attrib. 2940 314 3254 PAF (%) 37 8 27 Larynx Observed 3025 415 3440 Tob. Attrib. 2547 281 2828 PAF (%) 84 68 82 Liver Observed 7359 1713 9072 Tob. Attrib. 2500 117 2617 PAF (%) 34 7 29 Colon & rectum Observed 21 824 17 822 39 646 Tob. Attrib. 1838 771 2608 PAF (%) 8 4 7 Pancreas Observed 5748 5554 11 302 Tob. Attrib. 1778 749 2527 PAF (%) 31 13 22 Stomach Observed 4745 2423 7168 Tob. Attrib. 1388 145 1533 PAF (%) 29 6 21 Acute myelogenous leukaemia Observed 1527 1364 2891 Tob. Attrib. 334 55 389 PAF (%) 22 4 13 Cervix Observed 2863 2863 Tob. Attrib. 265 265 PAF (%) 9 9 Mucinous ovary Observed 306 306 Tob. Attrib. 54 54 PAF (%) 18 18 Total Observed (All Sites) 190 254 155 919 346 173 Tob. Attrib. 54 142 12 008 66 150 PAF (%) 28 8 19 Table 2 Estimated number (Tob. Attrib.) and proportion (PAF) of cancer cases attributable to active tobacco smoking by sex according to cancer site in France in 2015 Cancer site Males Females Total Lung Observed 29 097 11 353 40 450 Tob. Attrib. 25 494 7192 32 686 PAF (%) 88 63 81 Oral cavity & pharynx Observed 10 193 3060 13 253 Tob. Attrib. 8177 1281 9458 PAF (%) 80 42 71 Bladder Observed 10 307 2237 12 544 Tob. Attrib. 4046 287 4333 PAF (%) 39 13 35 Oesophagus Observed 4509 1108 5617 Tob. Attrib. 3101 497 3598 PAF (%) 69 45 64 Kidney Observed 8020 4072 12 092 Tob. Attrib. 2940 314 3254 PAF (%) 37 8 27 Larynx Observed 3025 415 3440 Tob. Attrib. 2547 281 2828 PAF (%) 84 68 82 Liver Observed 7359 1713 9072 Tob. Attrib. 2500 117 2617 PAF (%) 34 7 29 Colon & rectum Observed 21 824 17 822 39 646 Tob. Attrib. 1838 771 2608 PAF (%) 8 4 7 Pancreas Observed 5748 5554 11 302 Tob. Attrib. 1778 749 2527 PAF (%) 31 13 22 Stomach Observed 4745 2423 7168 Tob. Attrib. 1388 145 1533 PAF (%) 29 6 21 Acute myelogenous leukaemia Observed 1527 1364 2891 Tob. Attrib. 334 55 389 PAF (%) 22 4 13 Cervix Observed 2863 2863 Tob. Attrib. 265 265 PAF (%) 9 9 Mucinous ovary Observed 306 306 Tob. Attrib. 54 54 PAF (%) 18 18 Total Observed (All Sites) 190 254 155 919 346 173 Tob. Attrib. 54 142 12 008 66 150 PAF (%) 28 8 19 Cancer site Males Females Total Lung Observed 29 097 11 353 40 450 Tob. Attrib. 25 494 7192 32 686 PAF (%) 88 63 81 Oral cavity & pharynx Observed 10 193 3060 13 253 Tob. Attrib. 8177 1281 9458 PAF (%) 80 42 71 Bladder Observed 10 307 2237 12 544 Tob. Attrib. 4046 287 4333 PAF (%) 39 13 35 Oesophagus Observed 4509 1108 5617 Tob. Attrib. 3101 497 3598 PAF (%) 69 45 64 Kidney Observed 8020 4072 12 092 Tob. Attrib. 2940 314 3254 PAF (%) 37 8 27 Larynx Observed 3025 415 3440 Tob. Attrib. 2547 281 2828 PAF (%) 84 68 82 Liver Observed 7359 1713 9072 Tob. Attrib. 2500 117 2617 PAF (%) 34 7 29 Colon & rectum Observed 21 824 17 822 39 646 Tob. Attrib. 1838 771 2608 PAF (%) 8 4 7 Pancreas Observed 5748 5554 11 302 Tob. Attrib. 1778 749 2527 PAF (%) 31 13 22 Stomach Observed 4745 2423 7168 Tob. Attrib. 1388 145 1533 PAF (%) 29 6 21 Acute myelogenous leukaemia Observed 1527 1364 2891 Tob. Attrib. 334 55 389 PAF (%) 22 4 13 Cervix Observed 2863 2863 Tob. Attrib. 265 265 PAF (%) 9 9 Mucinous ovary Observed 306 306 Tob. Attrib. 54 54 PAF (%) 18 18 Total Observed (All Sites) 190 254 155 919 346 173 Tob. Attrib. 54 142 12 008 66 150 PAF (%) 28 8 19 In 2015, 32 686 (25 494 in men and 7192 in women) of the 40 450 lung cancer cases (29 097 in men and 11 353 in women) diagnosed in the French population aged 30 years and above were attributable to active smoking, corresponding to PAFs of 88% for men and 63% for women (table 3). Table 2 shows, in men and women respectively, the estimated numbers and proportions of cancer cases attributable to active smoking, by cancer sites. Detailed estimates by age are provided in Supplementary tables S2a and b. Besides lung, cancer sites that have the highest PAFs include larynx (84% in men and 68% in women), oral cavity and pharynx (80% in men and 42% in women) and oesophagus (69% in men and 45% in women). Cancer sites (besides lung) that account for the largest number of cases due to smoking include oral cavity and pharynx (8177 in men and 1281 in women), bladder (4046 in men and 287 in women) and oesophagus (3101 in men and 497 in women). Table 3 Estimated lung cancer cases and proportion (PAF) attributable to smoking according to sex in France in 2015 Males Females Age Population size (INSEE) Cases observed (FRANCIM) Rates in never smokers per 100 000 (CPS II) Cases in never smokers PAF (%) Cases attributable to smoking Population size (INSEE) Cases observed (FRANCIM) Rates in never smokers per 100 000 (CPS II) Cases in never smokers PAF (%) Cases attributable to smoking (1) (2) (3) (4)=(1)*(3) (5)=(6)/(2) (6)= (2)−(4) (1) (2) (3) (4)=(1)*(3) (5)=(6)/(2) (6)= (2)−(4) 30–34 1 975 801 56 1.6 32 44 24 2 039 647 51 2.5 51 0 0 35–39 1 943 589 106 2.4 47 56 59 1 972 714 100 3.2 63 37 37 40–44 2 196 838 285 3.4 75 74 210 2 214 598 248 4.3 95 62 153 45–49 2 150 383 925 4.8 103 89 822 2 196 770 576 6.2 136 76 440 50–54 2 119 033 1940 7.3 155 92 1785 2 201 318 969 8.8 194 80 775 55–59 1 985 794 3647 11.1 220 94 3427 2 111 389 1818 12.5 264 85 1554 60–64 1 898 518 4809 17.4 330 93 4479 2 063 366 1809 17.2 355 80 1454 65–69 1 715 932 5448 27 463 91 4985 1 898 126 1493 25 475 68 1018 70–74 1 099 046 4044 40.9 450 89 3594 1 279 448 1148 33.9 434 62 714 75–79 937 796 3290 61.1 573 83 2717 1 228 485 1172 46.6 572 51 600 80–84 726 400 2862 87.3 634 78 2228 1 128 190 1092 61.9 698 36 394 85+ 597 816 1685 87.3 522 69 1163 1 330 620 877 61.9 824 6 53 Total 19 346 946 29 097 – 3603 88 25 494 21 664 671 11 353 – 4161 63 7192 Males Females Age Population size (INSEE) Cases observed (FRANCIM) Rates in never smokers per 100 000 (CPS II) Cases in never smokers PAF (%) Cases attributable to smoking Population size (INSEE) Cases observed (FRANCIM) Rates in never smokers per 100 000 (CPS II) Cases in never smokers PAF (%) Cases attributable to smoking (1) (2) (3) (4)=(1)*(3) (5)=(6)/(2) (6)= (2)−(4) (1) (2) (3) (4)=(1)*(3) (5)=(6)/(2) (6)= (2)−(4) 30–34 1 975 801 56 1.6 32 44 24 2 039 647 51 2.5 51 0 0 35–39 1 943 589 106 2.4 47 56 59 1 972 714 100 3.2 63 37 37 40–44 2 196 838 285 3.4 75 74 210 2 214 598 248 4.3 95 62 153 45–49 2 150 383 925 4.8 103 89 822 2 196 770 576 6.2 136 76 440 50–54 2 119 033 1940 7.3 155 92 1785 2 201 318 969 8.8 194 80 775 55–59 1 985 794 3647 11.1 220 94 3427 2 111 389 1818 12.5 264 85 1554 60–64 1 898 518 4809 17.4 330 93 4479 2 063 366 1809 17.2 355 80 1454 65–69 1 715 932 5448 27 463 91 4985 1 898 126 1493 25 475 68 1018 70–74 1 099 046 4044 40.9 450 89 3594 1 279 448 1148 33.9 434 62 714 75–79 937 796 3290 61.1 573 83 2717 1 228 485 1172 46.6 572 51 600 80–84 726 400 2862 87.3 634 78 2228 1 128 190 1092 61.9 698 36 394 85+ 597 816 1685 87.3 522 69 1163 1 330 620 877 61.9 824 6 53 Total 19 346 946 29 097 – 3603 88 25 494 21 664 671 11 353 – 4161 63 7192 Table 3 Estimated lung cancer cases and proportion (PAF) attributable to smoking according to sex in France in 2015 Males Females Age Population size (INSEE) Cases observed (FRANCIM) Rates in never smokers per 100 000 (CPS II) Cases in never smokers PAF (%) Cases attributable to smoking Population size (INSEE) Cases observed (FRANCIM) Rates in never smokers per 100 000 (CPS II) Cases in never smokers PAF (%) Cases attributable to smoking (1) (2) (3) (4)=(1)*(3) (5)=(6)/(2) (6)= (2)−(4) (1) (2) (3) (4)=(1)*(3) (5)=(6)/(2) (6)= (2)−(4) 30–34 1 975 801 56 1.6 32 44 24 2 039 647 51 2.5 51 0 0 35–39 1 943 589 106 2.4 47 56 59 1 972 714 100 3.2 63 37 37 40–44 2 196 838 285 3.4 75 74 210 2 214 598 248 4.3 95 62 153 45–49 2 150 383 925 4.8 103 89 822 2 196 770 576 6.2 136 76 440 50–54 2 119 033 1940 7.3 155 92 1785 2 201 318 969 8.8 194 80 775 55–59 1 985 794 3647 11.1 220 94 3427 2 111 389 1818 12.5 264 85 1554 60–64 1 898 518 4809 17.4 330 93 4479 2 063 366 1809 17.2 355 80 1454 65–69 1 715 932 5448 27 463 91 4985 1 898 126 1493 25 475 68 1018 70–74 1 099 046 4044 40.9 450 89 3594 1 279 448 1148 33.9 434 62 714 75–79 937 796 3290 61.1 573 83 2717 1 228 485 1172 46.6 572 51 600 80–84 726 400 2862 87.3 634 78 2228 1 128 190 1092 61.9 698 36 394 85+ 597 816 1685 87.3 522 69 1163 1 330 620 877 61.9 824 6 53 Total 19 346 946 29 097 – 3603 88 25 494 21 664 671 11 353 – 4161 63 7192 Males Females Age Population size (INSEE) Cases observed (FRANCIM) Rates in never smokers per 100 000 (CPS II) Cases in never smokers PAF (%) Cases attributable to smoking Population size (INSEE) Cases observed (FRANCIM) Rates in never smokers per 100 000 (CPS II) Cases in never smokers PAF (%) Cases attributable to smoking (1) (2) (3) (4)=(1)*(3) (5)=(6)/(2) (6)= (2)−(4) (1) (2) (3) (4)=(1)*(3) (5)=(6)/(2) (6)= (2)−(4) 30–34 1 975 801 56 1.6 32 44 24 2 039 647 51 2.5 51 0 0 35–39 1 943 589 106 2.4 47 56 59 1 972 714 100 3.2 63 37 37 40–44 2 196 838 285 3.4 75 74 210 2 214 598 248 4.3 95 62 153 45–49 2 150 383 925 4.8 103 89 822 2 196 770 576 6.2 136 76 440 50–54 2 119 033 1940 7.3 155 92 1785 2 201 318 969 8.8 194 80 775 55–59 1 985 794 3647 11.1 220 94 3427 2 111 389 1818 12.5 264 85 1554 60–64 1 898 518 4809 17.4 330 93 4479 2 063 366 1809 17.2 355 80 1454 65–69 1 715 932 5448 27 463 91 4985 1 898 126 1493 25 475 68 1018 70–74 1 099 046 4044 40.9 450 89 3594 1 279 448 1148 33.9 434 62 714 75–79 937 796 3290 61.1 573 83 2717 1 228 485 1172 46.6 572 51 600 80–84 726 400 2862 87.3 634 78 2228 1 128 190 1092 61.9 698 36 394 85+ 597 816 1685 87.3 522 69 1163 1 330 620 877 61.9 824 6 53 Total 19 346 946 29 097 – 3603 88 25 494 21 664 671 11 353 – 4161 63 7192 Domestic passive smoking Table 4 shows, by age and sex, the proportion and number of lung cancer cases attributable to domestic passive smoking in 2015. Detailed estimates, including the estimated prevalence of never smokers living with an ever smoker in 2005 and the number of lung cancer cases among never smokers in 2015, are provided in Supplementary tables S4a and b. In sum, 36 and 142 lung cancer cases among male and female never smokers were attributable to exposure of smoking from a partner, corresponding to 4.2 and 6.7% of lung cancer occurring in male and female never smoker respectively. Table 4 Estimated number and proportion (PAF) of lung cancer cases attributable to domestic passive smoking in France in 2015 Age in 2015 (years) Males Females Never smokers in 2015 (%) Lung cancer cases not attributable to smoking Lung cancer cases among never smokers PAF of domestic passive smoking (%) Lung cancer cases attributable to domestic passive smoking Never smokers in 2015 (%) Lung cancer cases not attributable to smoking Lung cancer cases among never smokers PAF of domestic passive smoking (%) Lung cancer cases attributable to domestic passive smoking (1) (2) (3) (4) (5)=(4)/100*(3) (1) (2) (3) (4) (5)=(4)/100*(3) Source Baromètre 2014 Table 3 (3)=(1)/100*(2) Supplementary table S4a Baromètre 2014 Table 3 (3)=(1)/100*(2) Supplementary table S4b 30–34 26.0 32 8.2 0.3 0 37.8 51 19.3 0.7 0 35–39 30.1 47 14.0 2.4 0 32.6 63 20.6 3.1 1 40–44 28.4 75 21.2 5.5 1 36.6 95 34.9 5.2 2 45–49 23.7 103 24.5 7.3 2 36.3 136 49.4 6.7 3 50–54 27.0 155 41.8 7.9 3 34.9 194 67.6 7.1 5 55–59 20.4 220 45.0 7.4 3 37.1 264 97.9 8.2 8 60–64 19.7 330 65.1 6.9 5 46.2 355 164.0 8.6 14 65–69 19.4 463 89.9 4.8 4 49.0 475 232.5 9.3 22 70–74 24.5 450 110.1 4.4 5 56.3 434 244.2 8.9 22 75–79 24.5 573 140.4 3.2 4 56.3 572 322.3 8.6 28 80–84 24.5 634 155.4 3.0 5 56.3 698 393.2 6.8 27 85+ 24.5 522 127.9 2.4 3 56.3 824 463.7 2.4 11 Total – 3603 843 4.2 36 – 4161 2110 6.7 142 Age in 2015 (years) Males Females Never smokers in 2015 (%) Lung cancer cases not attributable to smoking Lung cancer cases among never smokers PAF of domestic passive smoking (%) Lung cancer cases attributable to domestic passive smoking Never smokers in 2015 (%) Lung cancer cases not attributable to smoking Lung cancer cases among never smokers PAF of domestic passive smoking (%) Lung cancer cases attributable to domestic passive smoking (1) (2) (3) (4) (5)=(4)/100*(3) (1) (2) (3) (4) (5)=(4)/100*(3) Source Baromètre 2014 Table 3 (3)=(1)/100*(2) Supplementary table S4a Baromètre 2014 Table 3 (3)=(1)/100*(2) Supplementary table S4b 30–34 26.0 32 8.2 0.3 0 37.8 51 19.3 0.7 0 35–39 30.1 47 14.0 2.4 0 32.6 63 20.6 3.1 1 40–44 28.4 75 21.2 5.5 1 36.6 95 34.9 5.2 2 45–49 23.7 103 24.5 7.3 2 36.3 136 49.4 6.7 3 50–54 27.0 155 41.8 7.9 3 34.9 194 67.6 7.1 5 55–59 20.4 220 45.0 7.4 3 37.1 264 97.9 8.2 8 60–64 19.7 330 65.1 6.9 5 46.2 355 164.0 8.6 14 65–69 19.4 463 89.9 4.8 4 49.0 475 232.5 9.3 22 70–74 24.5 450 110.1 4.4 5 56.3 434 244.2 8.9 22 75–79 24.5 573 140.4 3.2 4 56.3 572 322.3 8.6 28 80–84 24.5 634 155.4 3.0 5 56.3 698 393.2 6.8 27 85+ 24.5 522 127.9 2.4 3 56.3 824 463.7 2.4 11 Total – 3603 843 4.2 36 – 4161 2110 6.7 142 Table 4 Estimated number and proportion (PAF) of lung cancer cases attributable to domestic passive smoking in France in 2015 Age in 2015 (years) Males Females Never smokers in 2015 (%) Lung cancer cases not attributable to smoking Lung cancer cases among never smokers PAF of domestic passive smoking (%) Lung cancer cases attributable to domestic passive smoking Never smokers in 2015 (%) Lung cancer cases not attributable to smoking Lung cancer cases among never smokers PAF of domestic passive smoking (%) Lung cancer cases attributable to domestic passive smoking (1) (2) (3) (4) (5)=(4)/100*(3) (1) (2) (3) (4) (5)=(4)/100*(3) Source Baromètre 2014 Table 3 (3)=(1)/100*(2) Supplementary table S4a Baromètre 2014 Table 3 (3)=(1)/100*(2) Supplementary table S4b 30–34 26.0 32 8.2 0.3 0 37.8 51 19.3 0.7 0 35–39 30.1 47 14.0 2.4 0 32.6 63 20.6 3.1 1 40–44 28.4 75 21.2 5.5 1 36.6 95 34.9 5.2 2 45–49 23.7 103 24.5 7.3 2 36.3 136 49.4 6.7 3 50–54 27.0 155 41.8 7.9 3 34.9 194 67.6 7.1 5 55–59 20.4 220 45.0 7.4 3 37.1 264 97.9 8.2 8 60–64 19.7 330 65.1 6.9 5 46.2 355 164.0 8.6 14 65–69 19.4 463 89.9 4.8 4 49.0 475 232.5 9.3 22 70–74 24.5 450 110.1 4.4 5 56.3 434 244.2 8.9 22 75–79 24.5 573 140.4 3.2 4 56.3 572 322.3 8.6 28 80–84 24.5 634 155.4 3.0 5 56.3 698 393.2 6.8 27 85+ 24.5 522 127.9 2.4 3 56.3 824 463.7 2.4 11 Total – 3603 843 4.2 36 – 4161 2110 6.7 142 Age in 2015 (years) Males Females Never smokers in 2015 (%) Lung cancer cases not attributable to smoking Lung cancer cases among never smokers PAF of domestic passive smoking (%) Lung cancer cases attributable to domestic passive smoking Never smokers in 2015 (%) Lung cancer cases not attributable to smoking Lung cancer cases among never smokers PAF of domestic passive smoking (%) Lung cancer cases attributable to domestic passive smoking (1) (2) (3) (4) (5)=(4)/100*(3) (1) (2) (3) (4) (5)=(4)/100*(3) Source Baromètre 2014 Table 3 (3)=(1)/100*(2) Supplementary table S4a Baromètre 2014 Table 3 (3)=(1)/100*(2) Supplementary table S4b 30–34 26.0 32 8.2 0.3 0 37.8 51 19.3 0.7 0 35–39 30.1 47 14.0 2.4 0 32.6 63 20.6 3.1 1 40–44 28.4 75 21.2 5.5 1 36.6 95 34.9 5.2 2 45–49 23.7 103 24.5 7.3 2 36.3 136 49.4 6.7 3 50–54 27.0 155 41.8 7.9 3 34.9 194 67.6 7.1 5 55–59 20.4 220 45.0 7.4 3 37.1 264 97.9 8.2 8 60–64 19.7 330 65.1 6.9 5 46.2 355 164.0 8.6 14 65–69 19.4 463 89.9 4.8 4 49.0 475 232.5 9.3 22 70–74 24.5 450 110.1 4.4 5 56.3 434 244.2 8.9 22 75–79 24.5 573 140.4 3.2 4 56.3 572 322.3 8.6 28 80–84 24.5 634 155.4 3.0 5 56.3 698 393.2 6.8 27 85+ 24.5 522 127.9 2.4 3 56.3 824 463.7 2.4 11 Total – 3603 843 4.2 36 – 4161 2110 6.7 142 Discussion Overall, 66 150 (or 19%) of all new cancer cases among adults in France in 2015 can be attributable to active smoking, representing 28 and 8% of all cancer cases diagnosed in men and women over 30 years of age. Almost half of those cases (32 686) were lung cancer. Among never smokers, past exposure to domestic passive smoking caused 178 cases of lung cancer. Our results are consistent with previous studies. In 2000, 27% of the cancer cases in men and 6% in women in France were found to be attributable to active smoking22 vs. 28 and 8% in 2015 in this study. While prevalence of current smoking in men has declined progressively from about 60% in early 1970s to around 40% in 2000 and remained relatively stable thereafter, it has increased progressively in women from about 25% to over 30% during the same period.23 In 2014, the prevalence estimates in men and women were 38 and 30%, respectively.7 This overall male-downward and female-upward trends in smoking prevalence have been reflected in smoking-attributable deaths. Deaths due to smoking in French men decreased from 66 000 in 1985 to 59 000 in 2010, corresponding to PAFs of 23 and 21%, respectively. In contrast, deaths in French women increased from 4700 in 1985 to 19 000 in 2010, corresponding to PAFs of 1 and 7%.24 Consequently, smoking-related cancer burden is expected to increase among females in the foreseeable future, given the ascending trend in smoking observed in French women. Also worrisome is the high and rising prevalence of adolescent smoking, e.g. the prevalence of 16-year olds daily smokers increased from 17% in 2007–08 to 23% in 2011.23 Several limitations should be considered. First, we used the lung cancer incidence rates among never smokers in the US to estimate the PAFs for lung cancer in France, assuming the factors that cause lung cancer among never smokers and the exposure to these factors among never smokers to be identical in both populations. Second, the sensitivity analyses using RRs from CPS II and smoking prevalence in France (with different latency times) are not ideal, as it assumes that the smokers in France and in the CPS II cohort have the same past smoking history. Results from sensitivity analysis (see Supplementary material) using RRs from the European Prospective Investigation into Cancer and Nutrition (EPIC) study suggest that this may be a concern for the PAF estimates for some cancer sites (e.g. oesophagus) where the RRs from the CPS II and the EPIC study differ markedly. Third, for most cancer sites, we used the RRs of deaths instead of incidence. This is based on (i) the assumption that the death rates are the same among cancer patients whether their cancer is tobacco related or not and (ii) the clear advantage of using RR estimates from a study with large sample-size and long duration of follow-up i.e. 20 years in CPS II. As for domestic passive smoking, the RRs were derived from never smokers currently living with smokers. The corresponding PAF is therefore likely to be underestimated since the estimation fails to account for: (i) never smokers who have previously lived with a smoking partner and separated only recently; (ii) never smokers currently living with a former smoker who quit smoking only recently. To reduce this bias, following Parkin (2011), we estimated the PAF using the proportion of never smokers who were living with someone who had ever smoked in 2005. However, we may still have underestimated the true burden of passive smoking. First, the best data source we could find for marital status does not include unmarried partners living together, a common demographic status in France. Second, the current analysis does not include exposure to smoking from cohabiting members other than their partners, as such data are lacking. All these limitations are potential sources of underestimation. Additionally, the choice of 10-year latency for lung cancer in never smokers is arbitrarily based on data availability and the assumption that the prevalence of living with an ever-smoking partner has been constant over the past 2–3 decades. This could also lead to underestimations, as the level of passive exposure to indoor smoking was likely higher in the 1990s due to limited awareness of the harmful effects of passive smoking on health and tobacco control regulations in place. Finally, we were unable to assess the PAFs for exposure to passive smoking at workplaces and other public spaces due to lack of data. In conclusion, smoking was responsible for a significant share of cancer cases in France in 2015. Over the past decades, legislation has been passed to reduce tobacco consumption and exposure to second-hand tobacco smoke (e.g. loi Veil, 1976; loi Evin, 1991; décret, 2006).25 Comprehensive smoking-free policy was further strengthened in February 2007 for workplaces, shopping centres, transportation hubs, hospitals and schools.26 Subsequently, the bans were extended to hospitality places, such as bars, restaurants, hotels and casinos in January 2008.26 Despite France’s commendable initiatives to de-normalize tobacco use, including the recent adoption of plain packaging, tobacco taxation and advertizing restrictions, a sizeable proportion of the country’s population are currently tobacco smokers. France also remains one of the highest tobacco-consuming developed countries, falling behind the U.K., Canada, Australia and New Zealand which all have reduced smoking prevalence to below 20% (vs. over 30% in France).27,28 Accordingly, the present and predicted smoking pattern in France and its impact on population health should be alarming to the pro-tobacco control stakeholders. Due to the long latency time between smoking and the occurrence of cancer, and the high historical smoking prevalence in France, cancer incidence and mortality are not likely to decline in the foreseeable future, particularly for female cohorts that smoked most heavily and are still young. More tobacco control policies specifically targeting females should be devised. Given the recent rise in tobacco consumption in 2005–10 (has stabilized since) and the rising smoking prevalence among adolescents, the long-term smoking-related cancer burden may continue to increase.7,29 Hence, more in-depth research must be done to better understand the reasons for the present failures to reduce tobacco consumption despite generally strong tobacco control policies.28 Specifically, we need to investigate how increases in the retail price of tobacco products and their magnitude affect consumption, why its positive effects on consumption have often not been sustained over time in France, and whether periodic adjustment by changing the affordability will address this. As 17% of smokers in France used the less expensive roll-your-own cigarettes in 2010, monitoring the consumption and regulating the price of cheap cigarettes and other substitute products are also necessary.30 Meanwhile, reinforcement and adoption of more effective regulations on smoking are needed to achieve sustained reduction in smoking and thus lower the cancer burden in France. Supplementary data Supplementary data are available at EURPUB online. Acknowledgements The authors would like to thank Drs. D. Max Parkin, Lesley Rushton and the Steering Committee of the project entitled ‘Définition des priorités pour la prévention du cancer en France métropolitaine: la fraction de cancers attribuables aux modes de vie et aux facteurs environnementaux’. The authors would also like to thank the French Cancer Registries Network (FRANCIM) for providing cancer incidence data for France. Funding This work was funded by the French National Cancer Institute (INCa, grant nr. 2015-002). The funding source had no role in the collection, analysis or interpretation of the data or in the decision to submit the manuscript for publication. Conflicts of interest: None declared. Key points A total of 54 142 and 12 008 cancer cases, in adult (30+ years old) males and females respectively, were attributable to active smoking in France in 2015. Cancer sites that account for the largest number of cases due to smoking include lung, oral cavity and pharynx, bladder and oesophagus. A total of 36 and 142 of all lung cancer cases, among adult male and female never smokers respectively, were attributable to second-hand smoke resulting from their partner’s active smoking. Cancer incidence and mortality are not likely to decline in the foreseeable future in France, given its high historical smoking prevalence. Effective tobacco control regulations need to be adopted and strengthened to achieve sustained reduction in smoking and thus reduce the cancer burden in France. 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Institut national de prévention et d'éducation pour la santé (INPES) . Saint Denis 2013 ; 56 pages. 30 Currie L , Townsend J , Leon M , et al. Policy recommendations for tobacco taxation in the European Union integrated research findings from the PPACTE project. 2012 . © The Author(s) 2018. Published by Oxford University Press on behalf of the European Public Health Association. All rights reserved. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)

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The European Journal of Public HealthOxford University Press

Published: May 7, 2018

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