IJC International Journal of Cancer

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1 IJC International Journal of Cancer Evolution of pleural cancers and malignant pleural mesothelioma incidence in France between 1980 and 2005 N. Le Stang 1,2,3, A. Belot 4,5,6,7, A. Gilg Soit Ilg 1,8, P. Rolland 1,9, P. Astoul 10, S. Bara 11, P. Brochard 12,13, A. Danzon 11, P. Delafosse 11, P. Grosclaude 11, A.-V. Guizard 11, E. Imbernon 8, B. Lapôtre-Ledoux 11, K. Ligier 11, F. Molinié 11, J.-C. Pairon 14,15,16, E.-A. Sauleau 11, B. Trétarre 11, M. Velten 11, N. Bossard 4,5,6, M. Goldberg 8, G. Launoy 2,3, F. Galateau-Sallé 1,2,3 1 Registre multicentrique à vocation nationale des mésothéliomes pleuraux (MESONAT), F-14033, France 2 ERI3 INSERM Cancers & Populations, FRANCIM, Caen, F-14033, France 3 Centre Hospitalier Universitaire, Caen, F-14033, France 4 Hospices Civils de Lyon, Service de Biostatistique, Lyon, F-69424, France 5 Université de Lyon; Université Lyon I, Villeurbanne, F-69622, France 6 CNRS, UMR 5558, Laboratoire Biostatistique Santé, Pierre-Bénite, F-69495, France 7 Institut de Veille Sanitaire, Département des Maladies Chroniques et des Traumatismes, St Maurice, F-94415, France 8 Institut de Veille Sanitaire, Département santé travail, St Maurice, F-94415, France 9 Institut de Veille Sanitaire, Département santé travail, Equipe associée en santé travail, Bordeaux, F-33000, France 10 Division d oncologie thoracique, Département des maladies pulmonaires, Faculté de médecine (Université de la Méditerranée), Assistance Publique Hôpitaux de Marseille, Hôpital Sainte-Marguerite, Marseille, F-13274, France 11 Réseau français des registres de cancer FRANCIM, Faculté de médecine, Toulouse, F-31000, France 12 EA 3672, Laboratoire Santé-Travail-Environnement, Université Bordeaux 2, Bordeaux, F-33076, France 13 Service de Médecine du Travail et de Pathologies Professionnelles, CHU de Bordeaux, Bordeaux, F-33076, France 14 INSERM, Unité 955, Créteil, F-94000, France 15 Université Paris 12, Faculté de médecine, F-94000, France 16 CHI Créteil, Service de pneumologie et pathologie professionnelle, Créteil, F-94010, France The evolution of pleural cancers and malignant pleural mesothelioma incidence in France between 1980 and 2005 was analysed using data derived from the French network of cancer registries (FRANCIM) and the French National Mesothelioma Surveillance Program (PNSM). Mesothelioma proportions in pleural cancers were calculated by diagnosis year in the period. Our results suggest that the incidences of pleural cancer and mesothelioma levelled off in French men since 2000 and continued to increase in French women. A decrease of the annual pleural cancer incidence average in men was noticed (23.4% of annual rate of change) between 2000 and The proportion of pleural cancers that were mesothelioma was unchanged between 1980 and 2003 with an average of 86%. The age standardised incidence rate of pleural mesothelioma remained relatively stable between 1998 and 2005 with a slight falling trend. For women, the age standardised incidence rate of pleural cancers and mesothelioma increased during the period Additionally, the proportion of pleural cancers that were mesothelioma increased during the same period of time. Finally, the increased trend observed in the incidence of pleural mesothelioma and cancers in women is credibly due to their under diagnosis in the period. The comparison between the French incidence and the American and British ones shows that the decreasing trend in incidence of mesothelioma and pleural cancers in French men since 2000 is potentially associated with a lower amphibole consumption and by the implementation of safety regulations at work from Key words: pleural cancers, malignant pleural mesothelioma, incidence, time trends, cancer registry, PNSM DOI: /ijc History: Received 9 Feb 2009; Accepted 23 Jun 2009; Online 30 Jun 2009 Correspondence to: N. Le Stang, Registre MESONAT, Service d Anatomie Pathologique - Niv 3, Centre Hospitalier Universitaire de Caen, Avenue de la Côte de Nacre, CAEN Cedex, France, Fax: þ , The incidence of pleural cancers, specifically malignant pleural mesothelioma in men, has shown a consistent increase in many industrialised countries for several decades. Despite marked variations from one country to another, a rise of mesothelioma incidence and mortality has been observed in European countries, including Great Britain, Denmark, Norway, Italy, and in Canada and Japan. 1 7 Incidence calculated projections suggest a peak in men around 2017 in the Netherlands, around 2014 in Australia and between 2011 and 2015 in Great Int. J. Cancer: 126, (2010) VC 2009 UICC

2 Le Stang et al. 233 Table 1. Distribution of pleural cancers diagnosed between 1980 and 2003 according to district and gender District Registration period Men (N) Men (%) Women (N) Women (%) Total (N) Calvados Doubs Hérault Isère Loire-Atlantique Manche Bas-Rhin Haut-Rhin Somme Tarn Vendée Total , ,457 Britain Nevertheless, mesothelioma incidence in men in the United States and in the population of Sweden seems to have levelled off in the 1990s In Finland, a reduction of the incidence increase was also noted in the early 1990s. 18 In France, mesothelioma incidence and mortality rates increased between 1980 and In men, the incidence rates for 100,000 person-year were 0.6 in 1980 and 1.4 in 2000 and mortality rates for 100,000 person-year were 1.0 in 1980 and 1.7 in In women, incidence rates for 100,000 person-year were 0.1 in 1980 and 0.4 in 2000 and mortality rates for 100,000 person-year were 0.4 in 1980 and 0.4 in In 1998, Gilg Soit Ilg et al. published an estimate of the future burden of mortality from mesothelioma in France. 20 An age-period-cohort model, performed according to mortality data, predicted a peak of deaths from mesothelioma in 2020 with 900 annual deaths according to the second optimistic hypothesis. Banaei et al. also predicted a continuous increase of mortality of French men with a maximum around Since these last predictions (1998 and 2000), more recent incidence data has become available in France. This study aims to assess the evolution of malignant pleural cancers and malignant mesothelioma incidence in France from population-based data available from 1980 to Material and Methods Two sets of data were used. First, the French network of cancer registries (FRANCIM) provided data from local cancer registries operating at the district level (France is subdivided into 100 départements or districts). Local data are checked and standardised before inclusion in a common database. Case information recorded in the database including cancer topography and morphology are validated using the tools provided by the International Agency for Research on Cancer. National incidence estimates are regularly provided through short predictions from age-cohort-period models. Regarding pleural cancer incidence, available data are Figure 1. French districts recording pleural cancers between 1980 and provided by 11 local registries which had at least 5 years of registration covering the districts of Calvados, Doubs, Hérault, Isère, Loire-Atlantique, Manche, Bas-Rhin, Haut-Rhin, Somme, Tarn and Vendée (Table 1; Fig. 1). The topography (C38.4) and morphology of the pleural cancers were recorded according to the International Classification of Diseases for Oncology Third Edition (ICD-O-3) since Only certified primary tumours (morphology behaviour code /3) contributed to the calculation of incidence rates. The second set of data came from the French National Mesothelioma Surveillance Program (PNSM), established in In the 1990s, a network of extremely implied pathologists, lung specialists, oncologists, thoracic surgeons and occupational practitioner, allowed the implementation of an exhaustive registration of pleural tumours, difficult to organise at the same level for peritoneal mesotheliomas. The PNSM main procedures have been described in detail elsewhere. 22 Twenty-one districts were selected for this program

3 234 Evolution of Pleural Cancers in France between 1998 and 2003 of which 11 districts were covered by the FRANCIM network (Bouches-du-Rhône, Calvados, Côte d Or, Dordogne, Doubs, Gironde, Hérault, Isère, Landes, Loire-Atlantique, Lot-et-Garonne, Manche, Orne, Pyrénées- Atlantiques, Bas-Rhin, Haut-Rhin, Somme, Tarn, Var, Seine- Saint-Denis, Val-de-Marne) (Fig. 1). Each district included in the PNSM has developed special procedures for identifying and reporting primary pleural tumours within a very short period after diagnosis. Local data are checked and standardised before inclusion in a common database. A standardised procedure of pathological and clinical confirmation of the diagnosis is applied to all reported cases. The pathological diagnosis certification is provided by the Mesopath Group (expert pathologists in the field). Three experts, blinded to asbestos exposure and medical records, classify each case certain, probable, uncertain (because of unclassifiable lesion or inadequate materials) or excluded. If these three experts disagree, the case is reviewed collectively during a consensus meeting and is classified as above according to a quorum of at least eleven experts. When the case cannot be confirmed pathologically (uncertain case or because the samples were inadequate or not available), a clinical assessment is organised, based on questions to the attending physician and the patient s CT scan and records. Finally, cases are classified as very likely mesothelioma diagnosis, improbable mesothelioma diagnosis or impossible to determine. The estimation of the evolution of national incidence rates for pleural cancers has been performed using FRANCIM data between 1980 and These estimates were calculated by applying incidence/mortality ratios observed in the area covered by the 11 contributing cancer registries to the French national mortality estimate. This ratio was used to anticipate a possible lack of representativeness of the area covered by registries to measure French cancer incidence. A detailed description of the methodology is given in Belot et al. 23 Briefly, data of incidence, mortality and population were tabulated by 1-year class for age and cohort. To obtain incidence and mortality estimates, separate age-cohort models were used with a linear by linear interaction between age and cohort, which is equivalent to an age-period-cohort model with a second-order period term p The second-order period term p 2 was introduced in the model only when it was statistically significant (likelihood ratio test, a ¼ 1%). As each of the 11 district covered different period of incidence, the covariate district was introduced as a factor in the model to avoid confounding space and time effects. Finally, combining values predicted from (i) modelling of incidence in the area covered by the registries, (ii) modelling of mortality in the area covered by the registries, and (iii) modelling of mortality in France, we obtained an estimate of the incidence rate in France (thus, the number of incident cases) for the period Note that the estimates of the incidence rates for years 2004 and 2005 were obtained using (shortterm) projections from the age-period-cohort model using incidence observed in registries between 1980 and Figure 2. Evolution of pleural cancer incidence rates by gender between 1980 and 2005 in France. Mesothelioma mortality data has been available in France only since Before 2000, data on mesothelioma was gathered together with other primary pleural cancers. Therefore, because the estimation of national incidence rates requires mortality data, the evolution of national incidence rate could only be investigated for pleural cancers and not for mesothelioma. The evolution of pleural mesothelioma between 1998 and 2005 was investigated using data collected in 21 districts involved in PNSM. Incidence rates of pleural cancers and of pleural mesothelioma were standardised by the direct method using the World population age-structure as the reference and were expressed for 100,000 person-year, from Francim data and PNSM data, respectively. Note that estimates for years 2004 and 2005 were obtained by linear projections from the age-standardised incidence using incidence observed over the period in the PNSM area. These two sets of data were interesting to study together because they differed on the one hand by their population cover, 14% of French population covered by the Francim network against 30% covered by the PNSM area, and on the other hand by their case definition. Indeed, the 21 districts of the PNSM area were chosen to be representative of France regarding the main demographic, employment and economic activity characteristics. 22 Furthermore, mesothelioma cases studied within the PNSM framework were ascertained after initial registration, by the standardised procedure of pathological and clinical confirmation of the diagnosis. Results Evolution of the national incidence rates of pleural cancers Table 1 shows the distribution of the 1,457 patients with a pleural cancer registered by the 11 FRANCIM cancer registries between 1980 and 2003 according to district and gender (79% of men and 21% of women). The gender repartition of patients with a pleural cancer is statistically the same in each district (Chi-square p ¼ 0.064). The evolution of the pleural cancer incidence estimates in men and women between 1980

4 Le Stang et al. 235 Table II. Number of cases of pleural cancers in france in the period Year Evolution rate in period (%) Gender Incidence Men Obs (N) Rate Women Obs (N) Rate Age-standardised rate world per 100,000 person-year. and 2005 in France are described in Figure 2 and the estimated number of new pleural cancer cases in 2005 in men and women are presented in Table 2. The p of the likelihood ratio test for a significant effect of the second-order period term was equal to in men, resulting in the downturn curvatures showed (Fig. 2). In women, the second-order period term was not significant (p ¼ ). In 2005, pleural cancers were estimated to be 906 new cases (of which 71% occurred in men) in France. In 1980, the number of new cases was only about 343 (Table 2). In men, the world age-standardised incidence rate was estimated to be 1.2 cases for 100,000 person-year in From these estimates, despite an overall increase of þ1.7% per year in incidence of pleural cancers over the period, the incidence of pleural cancers decreased by 3.4% per year between 2000 and 2005 (Fig. 2, Table 2). In women, the world age-standardised incidence rate was estimated to be 0.4 cases for 100,000 person-year in Time trends showed a constant increase of incidence for 100,000 person-year during all the period with an annual rate of change of 3.1% over (0.2 cases in 1980 against 0.4 in 2005). However, this incidence rise was less pronounced during the most recent period (1.8% of annual rate of change) than during the overall period (Fig. 2, Table 2). Figure 3. Age-incidence standardised incidence rate world of pleural mesothelioma for 100,000 person-year by diagnosis year on the PNSM area. Evolution of the incidence of pleural mesothelioma in PNSM districts Between 1998 and 2003, 1,286 patients have been recorded for a suspicion of pleural mesothelioma (site code C38.4) of which 1,001 were certified (78%) as pleural malignant mesothelioma (histological codes 9050/3, 9051/3, 9052/3 and 9053/3), 6 (<1%) as other pleural tumours of mesothelial origin (histological codes 9052/0 and 9054/0), and 140 were excluded (11%) (18 other pleural primary tumours, 67 secondary pleural cancers, 16 pleural reactive lesions and 39 excluded for undetermined diagnosis). One hundred thirty nine remained uncertain (11%). Figure 3 presents the evolution from 1998 to 2003 and the estimates for 2004 and 2005 of the world age-standardised incidence rates of pleural mesothelioma for 100,000 person-year in the districts covered by the PNSM. In men, the incidence remained rather stable between 1998 and 2005 with a slight falling trend. The incidence rate for 100,000 person-year in men was 1.11 in 1998 and was estimated to be 0.93 in The incidence rate for 100,000 person-year in women increased between 0.18 in 1998 and 0.29 in Proportion of mesotheliomas among pleural cancers in districts covered by a registry The pathological and clinical review procedures of the PNSM definitely exclude about 10% of the reported cases (secondary pleural cancers or pleural benign lesions). 26 As there is a large overlap in the districts covered by FRANCIM and PNSM registries, this could at least partly explain the apparent recent decrease in pleural cancer incidence. We calculated for each gender and each 6-year period the proportion of mesotheliomas among pleural cancer cases (Table 3). Of the 1,457 pleural cancers collected by FRANCIM cancer registries between 1980 and 2003, 1,226 were diagnosed for a pleural malignant mesothelioma (histological codes 9050/3, 9051/3, 9052/3 and 9053/3). In men, the proportion of mesothelioma was 86% on average and did not significantly vary during the period. In women, the proportion was 76% and

5 236 Evolution of Pleural Cancers in France Table 3. Proportion of mesothelioma in pleural cancers by gender and diagnosis year in 11 cancer registries Men Mesothelioma (N) Pleural cancers (N) M/P 1 (%) M/P 95% CI Women Mesothelioma (N) Pleural cancers (N) M/P 1 (%) M/P 95% CI Total Mesothelioma (N) Pleural cancers (N) M/P 1 (%) M/P 95% CI M/P is the proportion of mesothelioma in pleural cancers. Table 4. Asbestos consumption and population of united kingdom, united states and france between 1950 and 1995 Country United Kingdom Asbestos consumption Population Asbestos consumption 1 per million inhabitants United States Asbestos consumption Population Asbestos consumption 1 per million inhabitants France Asbestos consumption Population Asbestos consumption 1 per million inhabitants Ratio France:US:UK 1:5:2 1:2:2 1:1:1 1:1:1 1:1:1 1:1:1 1:0:0 1:0:0 1 Asbestos consumption (in thousand of tons). 2 Population in million of inhabitants. significantly increased (p < ) over the study period from 48% [95% CI: %] in the first 6-year period to 86% [95% CI: %] in the last one. Discussion Our results suggest that in French men, after a regular increase since 1980, the national incidence of pleural cancer and mesothelioma has levelled off since Short-term projections showed a decrease of the pleural cancer incidence rate ( 3.4% of annual rate of change) between 2000 and The proportion of pleural cancers that were mesothelioma was stable between 1980 and 2003 with an average of 86%. In the districts covered by the PNSM, the age-standardised incidence rate of pleural mesothelioma remained rather stable between 1998 and 2003 with a slight falling trend. For women, age-standardised incidence rates of pleural cancers and mesothelioma increased during the period , but less markedly in the recent years. The rise in the proportion of mesotheliomas paralleled the age-standardised incidence rate of pleural cancers during the same period of time, from 48% [95% CI: %] in to 86% [95% CI: %] in , a proportion identical with that in men during the latest period, suggesting that pleural mesotheliomas in women were under diagnosed before 1997 probably as the result of a secondary pleural cancer diagnosis. The decline of the pleural cancer incidence between 2000 and 2005 for men is contemporary with the PNSM implementation in 1998 and of its pathological validation procedure of the mesothelioma diagnosis which excludes about

6 Le Stang et al % of the cases regularly registered. 22 However, when restricted to the PNSM data, a levelling off trend is also apparent, suggesting that the evolution of the incidence of pleural cancers was only partially explained by a modification in registration practices within registries or by the improvement of the pathological diagnosis of mesothelioma. This does not seem to be the case for women, for which the increasing trend of incidence seems to be largely explained by under diagnosis between 1980 and The decline of pleural cancer incidence in men that we observed contrasts with the previous projections for France which predicted a peak of mesothelioma around ,21 In other countries, the evolution of mesothelioma incidence and mortality over a recent period is contrasted. In Great Britain, there was since 1968 an increasing mortality trend for both men and women, from 153 deaths in 1968 to 1848 in 2001 and an estimated peak of around annual deaths for the period, whereas a decreasing incidence trend for men was associated with a stable incidence trend for women since the early 1990s in the United States The decline and the difference between the predicted peak and the observed values in France is close to the American findings which relied on mesothelioma incidence data from the Surveillance, and End Results (SEER), a programme which had no specific pathological validation procedure for mesothelioma diagnosis. In the United States (US), a peak of approximately 2,000 cases has been estimated around the period , but the peak of mesothelioma age-adjusted incidence occurred earlier around 1990 and has started to decline since then. 13,14 The difference in trends between countries may be partly explained by differences in the type of asbestos imports. In industrialised countries, different types of asbestos have been used, mainly chrysotile and two types of amphibole, amosite and crocidolite. In occupational cohorts, the exposure specific risk of mesothelioma was in the ratio 1:100:500 for chrysotile, amosite and crocidolite, respectively The US imported mainly chrysotile and amosite, whereas the United Kingdom References (UK) imported more crocidolite asbestos. In France, the main imports were chrysotile asbestos. 30 The asbestos consumption peaked in France and in the US in the 1970s and earlier in UK, in the 1960s (Table 4). 31 The asbestos consumption per million inhabitants in these three countries presented a ratio for France, US and UK, respectively, of 1:5:2 in the 1950s, of 1:2:2 in the 1960s and of 1:1:1 between 1970 and The proportion of amphibole among asbestos imports on the period was 1:1:4 for France, US and UK, respectively. 20 Another likely explanation for the decreasing trend in men since the 2000s in France is the implementation of the first regulations regarding asbestos exposure at work in 1977 (introduction of threshold limit value in occupational settings), which would be consistent with a latency period of about 30 years between exposure to asbestos and the onset of mesothelioma, and the fact that the vast majority of mesotheliomas in men are induced by occupational exposure to asbestos. 29 The same regulations regarding asbestos exposure at work were implemented in 1972 in US and later in 1987 in UK. In summary, the increased trend in incidence of pleural mesothelioma and cancers in French women is credibly due to their under diagnosis in the period. The decreasing trend in incidence of mesothelioma and pleural cancers in French men since 2000, if confirmed in the future, is potentially associated with lower amphibole consumption and by the implementation of the first safety regulations at work from Acknowledgements The authors wish to thank Dr. Allen Gibbs for his encouragement and critical suggestions and Ms. Sophie Amossé, Ms. Anne-Marie Aude, Ms. Céline Berthaut, Ms. Hélène Berron, Ms. Gaétane Blaizot, Ms. Véronique Bouvier, Ms. Laurence Calatayud, Ms. Soizick Chamming s, Ms. Christine Cotté, Mr. Pierre Czernichow, Ms. Marie-Line de Abreu, Ms. Anne de Quillacq, Mr. Stéphane Ducamp, Ms. Cécile Dufour, Ms. Catherine Frenay, Ms. Céline Gramond, Ms. Mireille Grandadam, Ms. Valérie Queuche, Ms. Christine Madeline, Ms. Myriam Ramadour, Ms. Anne-Delphine Tagri and Ms. Blandine Wurtz for the data management and quality. 1. Bianchi C, Bianchi T. Malignant mesothelioma: global incidence and relationship with asbestos. Ind Health 2007;45: Peto J, Decarli A, La Vecchia C, Levi F, Negri E. The European mesothelioma epidemic. Br J Cancer 1999;79: MakV,DaviesE,PutchaV,Choodari- Oskooei B, Møller H. The epidemiology and treatment of mesothelioma in South East England Thorax 2008;63: Ulvestad B, Kjaerheim K, Møller B, Andersen A. Incidence trends ofmesothelioma in Norway, Int J Cancer 2003;107: Marinaccio A, Montanaro F, Mastrantonio M, Uccelli R, Altavista P, Nesti M, Seniori Costantini A, Gorini G. Predictions of mortality from pleural mesothelioma in Italy: a model based on asbestos consumption figures supports results from age-period-cohort models. Int J Cancer 2005;115: Marrett LD, Ellison LF, Dryer D. Canadian cancer statistics at a glance: mesothelioma. CMAJ 2008;178: Kanazawa N, Ioka A, Tsukuma H, Ajiki W, Oshima A. Incidence and survival of mesothelioma in Osaka, Japan. Jpn J Clin Oncol 2006;36: Segura O, Burdorf A, Looman C. Update of predictions of mortality from pleural mesothelioma in the Nederlands. Occup Environ Med 2003;60: Burdorf A, Järvholm B, Englund A. Explaining differences in incidence rates of pleural mesothelioma between Sweden and The Netherlands. Int J Cancer 2005;113: Leigh J, Davidson P, Hendrie L, Berry D. Malignant mesothelioma in Australia, Am J Ind Med 2002;41: Clements M, Berry G, Shi J, Ware S, Yates D, Johnson A. Projected mesothelioma

7 238 Evolution of Pleural Cancers in France incidence in men in New South Wales. Occup Environ Med 2007;64: Hodgson JT, McElvenny DM, Darnton AJ, Price MJ, Peto J. The expected burden of mesothelioma mortality in Great Britain from 2002 to Br J Cancer 2005;92: Weill H, Hughes J, Churg A. Changing trends in US mesothelioma incidence. Occup Environ Med 2005;62: Price B, Ware A. mesothelioma trends in United States: an update based on surveillance., and end results program. Data for 1973 through Am J Epidemiol 2004;159: Price B. Analysis of Current Trends in United States Mesothelioma Incidence. Am J Epidemiol 1997;145: Järvholm B, Englund A, Albin M. Pleural mesothelioma in Sweden: an analysis of the incidence according to the use of asbestos. Occup Environ Med 1999;56: Hemminki K, Li X. Mesothelioma incidence seems to have levelled off in Sweden. Int J Cancer 2003;103: Karjalainen A, Pukkala E, Mattson K, Tammilehto L, Vainio H. Trends in mesothelioma incidence and occupational mesotheliomas in Finland in Scand J Work Environ Health 1997;23: Remontet L, Esteve J, Bouvier AM, Grosclaude P, Launoy G, Ménégoz F, Exbrayat C, Tretare B, Carli PM, Guizard AV, Troussard X, Bercelli P, et al. Cancer incidence and mortality in France over the period Rev Epidemiol Sante Publique 2003;51: Ilg AG, Bignon J, Valleron AJ. Estimation of the past and future burden of mortality from mesothelioma in France. Occup Environ Med 1998;55: Banaei A, Auvert B, Goldberg M, Gueguen A, Luce D, Goldberg S. Future trends in mortality of French men from mesothelioma. Occup Environ Med 2000; 57: Goldberg M, Imbernon E, Rolland P, Gilg Soit Ilg A, Savès M, de Quillacq A, Frenay C, Chamming s S, Arveux P, Boutin C, Launoy G, Pairon JC, et al. The French National Mesothelioma Surveillance Program. Occup Environ Med 2006;63: Belot A, Grosclaude P, Bossard N, Jougla E, Benhamou E, Delafosse P, Guizard AV, Molinié F, Danzon A, Bara S, Bouvier AM, Trétarre B, et al. Cancer incidence and mortality in France over the period Rev Epidemiol Sante Publique 2008; 56: Clayton D, Schifflers E. Models for temporal variation in cancer rates. I: Age- Period and Age-Cohort models. Stat Med 1987;6: Clayton D, Schifflers E. Models for temporal variation in cancer rates. II. Age- Period-Cohort models. Stat Med 1987;6: Estève J, Benhamou E, Raymond L. Statistical methods in cancer research. IV. Descriptive epidemiology. Lyon: International Agency for Research on Cancer, IARC Scientific Publications Hodgson JT, Darnton A. The quantitative risks of mesothelioma and lung cancer in relation to asbestos exposure. Ann Occup Hyg 2000;44: Price B, Wilson R. Trends in mesothelioma incidence and asbestos exposure evaluation. In:Nolan RP, Langer AM, Ross M, Wicks FJ, Martin RF, eds. Health effects of chrysotile-asbestos: contribution of science to risk management decisions. Canadian Mineralogist Special Publication 5, 2001, pp McDonald JC, McDonald AD. The epidemiology of mesothelioma in historical context. Eur Respir J 1996;9: Goldberg M, Banaei A, Goldberg S, Auvert B, Luce D, Guéguen A. Past occupational exposure to asbestos among men in France. Scand J Work Environ Health 2000; 26: Virta RL. Worldwide asbestos supply and consumption trends from 1900 through 2003: U.S. Geological Survey Circular Virginia:U.S. Geological Survey, Available only online.

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