Quantifying the mediating effects of smoking and occupational exposures in the relation between education and lung cancer: the ICARE study

Smoking only partly explains the higher lung cancer incidence observed among socially deprived people. Occupational exposures may account for part of these inequalities, but this issue has been little investigated. We investigated the extent to which smoking and occupational exposures to asbestos, silica and diesel motor exhaust mediated the association between education and lung cancer incidence in men. We analyzed data from a large French population-based case–control study (1976 lung cancers, 2648 controls). Detailed information on lifelong tobacco consumption and occupational exposures to various carcinogens was collected. We conducted inverse probability-weighted marginal structural models. A strong association was observed between education and lung cancer. The indirect effect through smoking varied by educational level, with the strongest indirect effect observed for those with the lowest education (OR = 1.34 (1.14–1.57)). The indirect effect through occupational exposures was substantial among men with primary (OR = 1.22 (1.15–1.30) for asbestos and silica) or vocational secondary education (OR = 1.18 (1.12–1.25)). The contribution of smoking to educational differences in lung cancer incidence ranged from 22 % (10–34) for men with primary education to 31 % (−3 to 84) for men with a high school degree. The contribution of occupational exposures to asbestos and silica ranged from 15 % (10–20) for men with a high school degree to 20 % (13–28) for men with vocational secondary education. Our results highlight the urgent need for public health policies that aim at decreasing exposure to carcinogens at work, in addition to tobacco control policies, if we want to reduce socioeconomic inequalities in the cancer field.

[1]  J. Mackenbach,et al.  Trends in smoking behaviour between 1985 and 2000 in nine European countries by education , 2005, Journal of Epidemiology and Community Health.

[2]  H. Morgenstern,et al.  Education and lung cancer among never smokers. , 2014, Epidemiology.

[3]  J. Oppert,et al.  Walking and cycling for commuting, leisure and errands: relations with individual characteristics and leisure-time physical activity in a cross-sectional survey (the ACTI-Cités project) , 2015, International Journal of Behavioral Nutrition and Physical Activity.

[4]  M. Khlat,et al.  Educational inequalities in smoking over the life cycle: an analysis by cohort and gender , 2015, International Journal of Public Health.

[5]  H. Møller,et al.  Histological subtype of lung cancer in relation to socio-economic deprivation in South East England , 2008, BMC Cancer.

[6]  O. Gaye,et al.  Risk of Lung Cancer Associated With Occupational Exposure to Mineral Wools: Updating Knowledge From a French Population-Based Case–Control Study, the ICARE Study , 2013, Journal of occupational and environmental medicine.

[7]  M. Abrahamowicz,et al.  Modelling smoking history using a comprehensive smoking index: application to lung cancer , 2006, Statistics in medicine.

[8]  Stijn Vansteelandt,et al.  Odds ratios for mediation analysis for a dichotomous outcome. , 2010, American journal of epidemiology.

[9]  Jack Siemiatycki,et al.  Socioeconomic Position and Lung Cancer Risk: How Important is the Modeling of Smoking? , 2012, Epidemiology.

[10]  C. Friedenreich,et al.  Physical activity and lung cancer risk in the European Prospective Investigation into Cancer and Nutrition Cohort , 2006, International journal of cancer.

[11]  M. Goldberg,et al.  MATGENE: A program to develop job-exposure matrices in the general population in France , 2011, Occupational and Environmental Medicine.

[12]  R. Goldbohm,et al.  Socioeconomic status and lung cancer incidence in men in The Netherlands: is there a role for occupational exposure? , 1997, Journal of epidemiology and community health.

[13]  Stijn Vansteelandt,et al.  A simple unified approach for estimating natural direct and indirect effects. , 2012, American journal of epidemiology.

[14]  D. Hafeman "Proportion explained": a causal interpretation for standard measures of indirect effect? , 2009, American journal of epidemiology.

[15]  Severine Deguen,et al.  Air quality and social deprivation in four French metropolitan areas--a localized spatio-temporal environmental inequality analysis. , 2014, Environmental research.

[16]  J. Klumbienė,et al.  Effect of nationwide tobacco control policies on smoking cessation in high and low educated groups in 18 European countries , 2008, Tobacco Control.

[17]  S. Fincham,et al.  Socioeconomic status and lung cancer risk in Canada. , 2001, International journal of epidemiology.

[18]  Francesco Forastiere,et al.  Methodological issues regarding confounding and exposure misclassification in epidemiological studies of occupational exposures. , 2007, American journal of industrial medicine.

[19]  M. Khlat,et al.  Widening inequalities in smoking initiation and cessation patterns: a cohort and gender analysis in France. , 2011, Drug and alcohol dependence.

[20]  W. Sherlaw,et al.  Examining Tobacco Control Strategies and Aims Through a Social Justice Lens: An Application of Sen's Capability Approach , 2011 .

[21]  Paolo Vineis,et al.  The role of smoking and diet in explaining educational inequalities in lung cancer incidence. , 2009, Journal of the National Cancer Institute.

[22]  D. Luce,et al.  Occupational Exposure to Diesel Motor Exhaust and Lung Cancer: A Dose-Response Relationship Hidden by Asbestos Exposure Adjustment? The ICARE Study , 2015, Journal of cancer epidemiology.

[23]  F. Berrino,et al.  The contribution of risk factors to the higher incidence of invasive and in situ breast cancers in women with higher levels of education in the European prospective investigation into cancer and nutrition. , 2011, American journal of epidemiology.

[24]  K. Leffondré,et al.  Heavy smoking and lung cancer: Are women at higher risk? Result of the ICARE study , 2014, British Journal of Cancer.

[25]  Sharon Friel,et al.  Closing the gap in a generation: health equity through action on the social determinants of health , 2008, The Lancet.

[26]  P. Peretti-Watel,et al.  Les Français et la cigarette en 2005 : un divorce pas encore consommé , 2007 .

[27]  T. VanderWeele,et al.  When is the difference method conservative for assessing mediation? , 2015, American journal of epidemiology.

[28]  R. Balicer,et al.  Reliability of self-reported smoking history and age at initial tobacco use. , 2005, Preventive medicine.

[29]  K. Overvad,et al.  Does insufficient adjustment for smoking explain the preventive effects of fruit and vegetables on lung cancer? , 2004, Lung cancer.

[30]  Alastair H. Leyland,et al.  Air Pollution, Social Deprivation, and Mortality: A Multilevel Cohort Study , 2007, Epidemiology.

[31]  G. Watt,et al.  Social class differences in lung cancer mortality: risk factor explanations using two Scottish cohort studies. , 2001, International journal of epidemiology.

[32]  L. Thygesen,et al.  Assessing natural direct and indirect effects through multiple pathways. , 2014, American journal of epidemiology.

[33]  Ellen Imbernon,et al.  Matgéné: a program to develop job-exposure matrices in the general population in France. , 2011, The Annals of occupational hygiene.

[34]  M. Petticrew,et al.  Population tobacco control interventions and their effects on social inequalities in smoking: systematic review , 2008, Tobacco Control.

[35]  B. Brunekreef,et al.  Air pollution and lung cancer incidence in 17 European cohorts: prospective analyses from the European Study of Cohorts for Air Pollution Effects (ESCAPE). , 2013, The Lancet. Oncology.

[36]  D. Luce,et al.  Investigation of occupational and environmental causes of respiratory cancers (ICARE): a multicenter, population-based case-control study in France , 2011, BMC public health.

[37]  S. Hercberg,et al.  Compliance with French nutrition and health program recommendations is strongly associated with socioeconomic characteristics in the general adult population. , 2010, Journal of the American Dietetic Association.

[38]  P. Boffetta,et al.  Occupational exposure to diesel exhausts and risk for lung cancer in a population-based case-control study in Italy. , 2006, Annals of oncology : official journal of the European Society for Medical Oncology.

[39]  F. Clavel-Chapelon,et al.  Lung cancers attributable to environmental tobacco smoke and air pollution in non-smokers in different European countries: a prospective study , 2007, Environmental health : a global access science source.

[40]  E. Riboli,et al.  Occupational exposures contribute to educational inequalities in lung cancer incidence among men: Evidence from the EPIC prospective cohort study , 2010, International journal of cancer.

[41]  J. Mackenbach,et al.  Socio-economic Differences in Risk Factors for Morbidity and Mortality in the European Community , 1997, Journal of health psychology.

[42]  K. Leffondré,et al.  Temporal patterns of occupational asbestos exposure and risk of pleural mesothelioma , 2011, European Respiratory Journal.

[43]  P. Nilsson,et al.  Socio-economic status and lung cancer risk including histologic subtyping--a longitudinal study. , 2006, Lung cancer.