Cigarette smoking and lung cancer in women: Results of the French ICARE case–control study
Introduction
In 2005, the age-standardised incidence rate of female lung cancer in France was 12.6, with a 5.1% annual increase [1]. While incidence is still higher among men, the gap has narrowed. The incidence rates for the 3 major types of female lung cancer (small cell carcinoma, squamous cell carcinoma and adenocarcinoma) have increased, with a more rapid increase in the case of adenocarcinoma, which is the predominant form in women while squamous cell carcinoma prevails in men [2].
A hundred years ago, lung cancer affected men almost exclusively and the early epidemiologic studies that allowed cigarette smoking to be established as the major cause of lung cancer only included men. Since 1980, a growing number of epidemiological surveys have pinpointed the risk of female lung cancer related to smoking [3], [4], [5], [6], [7], [8], [9], [10], [11]. However the associations between lung cancer in women and tobacco smoking vary between countries. The highest estimates come from North American studies, with relative risk close to 20, while the lowest come from Asian studies with RR approaching 2. European estimates are intermediate. Most of these variations are very likely explained by differences in prevalence of smoking but smoking habits such as use of a filter or inhalation may also vary from one country to the other. Dark tobacco is a common product in Europe and Latina America contrary to North America where blond tobacco is mainly used. Lifestyle and diet could also contribute to these differences. In France, the only study on the relationship between cigarette smoking and the risk of lung cancer among women dates back to 1987 and included 96 cases [12].
In order to explore the role of lifestyle, environmental, occupational as well as genetic susceptibility risk factors in respiratory cancers we set up in France a large population based case–control study including lung and upper aero digestive tract cancers. Based on this study, we examined the magnitude of the risk of lung cancer related to smoking among French women. More precisely we will estimate relative risks relative to intensity, total duration of smoking, pack-years, as well as to the type of tobacco smoked, the pattern of inhalation and the use of filter or non-filter cigarettes. We will also examine the decline in risk among ex smokers and the influence of age at beginning. The use of more flexible methods such as restricted cubic splines will allow us to model dose–effect relationship (intensity, total duration and time since cessation), while avoiding strong assumptions on the shape of the curves.
Section snippets
Study population
The ICARE study, conducted from 2001 to 2007, is a large multicenter population-based case–control study on respiratory cancers. The study was carried out in 10 of the 11 French départements that include a population-based general cancer registry, covering approximately 13% of the French population, i.e. 8 million people. Each registry participated over 1–5 years, during which time we included all incident lung and UADT cancers. This analysis focuses on women with lung cancer and their
Results
The main characteristics of the 648 cases and 775 controls are presented in Table 1. The cases averaged 57 years of age at interview compared to 60 years for the controls. Half the cases had adenocarninomas (53%), 17% had squamous cell carcinomas and 15% small cell carcinomas.
A detailed analysis of the tobacco habits of controls, per birth cohort, shows a regular increase in the proportion of women who smoke over time and a modification of their smoking habits. Women born in the 1960s started
Discussion
Our objective was to examine in detail the association between lung cancer and cigarette smoking in French women, using a large population based case–control study.
Our study was set up in collaboration with the French network of cancer registries (FRANCIM), allowing us to recruit lung cancer cases in almost all of the different healthcare facilities in the included départements. As the survival in lung cancer is very poor, a great effort has been done to minimize the delay between the diagnosis
Conflict of interest
None declared.
Acknowledgement
This work was supported by the Fondation de France, the French National Research Agency (ANR), the Fondation for Medical Research (FRM), The French Institute for Public Health Surveillance (Institut de veille sanitaire, InVS), The Health and Sport department (Direction Générale de la Santé et des Sports), Organization for the Research on Cancer (Association pour la Recherche sur le Cancer, ARC), Ministère du travail, de la Solidarité et de la Fonction Publique (Direction Générale du Travail),
References (40)
- et al.
Cancer incidence and mortality in France over the period 1980–2005
Rev Epidemiol Sante Publique
(2008) - et al.
Lung cancer risk among Czech women: a case–control study
Prev Med
(2002) - et al.
Lung cancer among women in France. Analysis of the 904 French women with lung cancer included in the KBP-2000-CPHG study of the French College of General Hospital-based Pneumologists (CPHG)
Lung Cancer
(2004) - et al.
Trends in incidence and prognosis of the histological subtypes of lung cancer in North America, Australia, New Zealand and Europe
Lung Cancer
(2001) - et al.
Cigarette filter and the incidence of lung adenocarcinoma among Tunisian population
Lung Cancer
(2007) - et al.
Impact of filter cigarette smoking on lung cancer histology
Prev Med
(1997) - et al.
International lung cancer trends by histologic type: male:female differences diminishing and adenocarcinoma rates rising
Int J Cancer
(2005) - et al.
Association of family history of cervical, ovarian, and uterine cancer with histological categories of lung cancer: the Iowa Women's Health Study
Cancer Epidemiol Biomarkers Prev
(1997) - et al.
Sex differences in lung-cancer risk associated with cigarette smoking
Int J Cancer
(1993) - et al.
Gender and histologic type variations in smoking-related risk of lung cancer
Epidemiology
(1992)
Are female smokers at higher risk for lung cancer than male smokers? A case–control analysis by histologic type
Am J Epidemiol
Smoking and cancer risk in Korean men and women
Cancer Causes Control
Cancer incidence in female smokers: a 26-year follow-up
Int J Cancer
Mortality in women and men in relation to smoking
Int J Epidemiol
Lung cancer and cigarette smoking in women: a multicenter case–control study in Europe
Int J Cancer
Lung cancer and women: results of a French case–control study
Br J Cancer
Modern epidemiology
Statistical methods in cancer research – the analysis of case control studies
Evolution of epidemiologic ideas: annotated readings on concepts and methods
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