Incidence of gastrointestinal cancers in France

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1 Masson, Paris, Gastroenterol Clin Biol 2004;28: ORIGINAL ARTICLE Incidence of gastrointestinal cancers in France Anne-Marie BOUVIER (1), Laurent REMONTET (2), Eric JOUGLA (3), Guy LAUNOY (4), Pascale GROSCLAUDE (5), Antoine BUÉMI (6), Brigitte TRETARRE (7), Michel VELTEN (8), Vincent DANCOURT (9), François MENEGOZ (10), Anne-Valérie GUIZARD (11), Josette MACÉ LESEC H (12), Jung PENG (13), Paolo BERCELLI (14), Patrick ARVEUX (15), Jacques ESTÈVE (2), Jean FAIVRE (1) (1) Registre des cancers digestifs de la Côte-d Or, Équipe INSERM 0106, BP 87900, Dijon Cedex ; (2) Service de Biostatistiques, Centre Hospitalier Lyon-Sud, Pierre-Bénite, Lyon ; (3) INSERM, CépiDc ; (4) Registre des cancers digestifs du Calvados ; (5) Registre des cancers du Tarn ; (6) Registre des cancers du Haut-Rhin ; (7) Registre des cancers de l Hérault ; (8) Registre des cancers du Bas-Rhin ; (9) Registre des cancers digestifs de la Saône-et-Loire ; (10) Registre des cancers de l Isère ; (11) Registre des cancers de la Manche ; (12) Registre des cancers du Calvados ; (13) Registre des cancers de la Somme ; (14) Registre des cancers de Vendée et de Loire-Atlantique ; (15) Registre des cancers du Doubs. SUMMARY Aim Monitoring cancer incidence and time trends is essential for cancer research and health care planning. The aim of the study was to compare the incidence of gastrointestinal cancers in twelve administrative area in France to estimate the national cancer incidence during 2000 compared with the preceding 20 years. Methods Incidence data was provided by cancer registries and mortality data by the French national medical research institute (INSERM). The two data sets were modeled separately over the period using age-cohort models. The incidence/mortality ratio obtained from these models was applied to the mortality rates of an age-cohort model of the entire population. Results The estimated number of new cases of gastrointestinal cancer was 61,465 in Colorectal cancer was the leading localization with 36,257 cases. The incidence of gastrointestinal cancers was slightly higher in northern than in southern area. Incidence of esophageal cancer was three times that of liver cancer. Variations in incidence were less marked for other localizations. The incidence of gastric and esophageal cancer in the male population decreased between 1980 and 2000, on average by slightly more than 2% per year. Incidence of other cancers increased. The number of new cases of colorectal cancer increased by 50%. The rise in the incidence of liver cancer was particularly striking, with an increase from 2000 incident cases in 1980 to nearly 6000 in Conclusion For most localizations, incidence of gastrointestinal cancers displays few geographical differences in France, but there has been a striking change in incidence trends over the past 20 years. The full text of this article is available in English, free of charge, on the Web on: RÉSUMÉ Incidence des cancers digestifs en France Anne-Marie BOUVIER, Laurent REMONTET, Eric JOUGLA, Guy LAUNOY, Pascale GROSCLAUDE, Antoine BUÉMI, Brigitte TRETARRE, Michel VELTEN, Vincent DANCOURT, François MENEGOZ, Anne-Valérie GUIZARD, Josette MACÉ LESEC H, Jung PENG, Paolo BERCELLI, Patrick ARVEUX, Jacques ESTÈVE, Jean FAIVRE (Gastroenterol Clin Biol 2004;28: ) Objectif La connaissance de l incidence des cancers est essentielle à la recherche en cancérologie et à la planification en santé publique. L objectif du travail actuel était de décrire l incidence des cancers digestifs dans 12 départements, d estimer leur incidence nationale en 2000 et leur évolution au cours des 20 dernières années. Méthode Les données d incidence provenaient des registres de cancers et les données de mortalité ont été fournies par le Centre d épidémiologie sur les causes médicales de décès de l Inserm. L estimation des taux nationaux pour l année 2000 s appuie sur une modélisation distincte, avec un modèle âge-cohorte, de l incidence et de la mortalité observées au cours de la période Le rapport incidence/mortalité obtenu à partir de cette modélisation est appliqué aux taux de mortalité d un modèle âge-cohorte issu des données de l ensemble de la France. Résultats Le nombre estimé de cancers digestifs était de en Les cancers colorectaux représentaient à eux seuls cas. L incidence des cancers était un peu plus élevée au Nord qu au Sud de la Loire. Les variations d incidence se situaient dans un rapport de 1 à 3 pour le cancer de l œsophage et le cancer du foie. Elles étaient moins marquées pour les autres localisations. L incidence des cancers de l estomac et des cancers de l œsophage chez l homme a diminué entre 1980 et 2000, en moyenne d un peu plus de 2 % par an. L incidence des autres localisations est en augmentation. Le nombre de nouveaux cas de cancers du côlon a augmenté de 50 %. L augmentation d incidence du cancer du foie est très importante, le nombre de cas est passé de près de à près de Conclusion En dehors des cancers de l œsophage et du foie, les variations géographiques de l incidence des cancers digestifs en France sont peu marquées. Par contre, leur incidence s est profondément modifiée en 20 ans. Monitoring cancer incidence and time trends is essential for cancer research and health care planning. Cancer registries provide the best means of evaluating the burden of cancer on the general population. The primary Reprints : A.-M. BOUVIER, à l adresse ci-dessus. function of these registries is to collect data, and to routinely record all new cases of cancer diagnosed in a defined geographical area. Periodic analysis of cancer registry databases discloses incidence trends and provides information on changes in the characteristic features of the cancers. Comparisons can be made with similar registries in other areas. FRANCIM is the registry network in France where data collected in individual registries combined to provide an overall picture of gastrointestinal cancer 877

2 A.-M. Bouvier et al. Table I. Incidence a of gastrointestinal cancers in 12 French areas Period Incidence a des cancers digestifs selon le sexe, dans 12 départements Période Esophagus Stomach Small bowel Colon-rectum M F M F M F M F Bas-Rhin Calvados Côte-d Or Doubs Haut-Rhin Hérault Isère Loire-Atlantique Manche Saône-et-Loire Somme Tarn France a per 100,000 inhabitants standardized for the world population. nationwide. Previous analyses have provided a map of cancer incidence by geographic region as well as an estimate of national incidence for [1, 2]. This study revealed regional differences in the incidence of gastrointestinal cancers and underscored the relative predominance of colorectal cancer in all regions [3, 4]. Data collection and analysis continue. The purpose of the present work was to describe the incidence of gastrointestinal cancers in twelve administrative areas in France and to estimate national incidence for Findings were compared with the 1980 figures. Material and methods Study populations Incidence data issued from twelve administrative areas with cancer registries participating in the Francim network. These twelve aeras which cover about 15% of the surface area of France were: Bas-Rhin (1,024,000 inhabitants), Calvados (647,000 inhabitants), Côte-d Or (506,000 inhabitants), Doubs (498,000 inhabitants), Haut-Rhin (706,000 inhabitants), Hérault (895,000 inhabitants), Isère (1,091,000 inhabitants), Loire-Atlantique (1,132,000 inhabitants), Manche (481,000 inhabitants), Saône-et-Loire (544,000 inhabitants), Somme (554,000 inhabitants) and Tarn (341,000 inhabitants). The study period was for all registries (colorectal cancer alone for Loire-Atlantique, all localizations except liver for Manche). Data were collected in compliance with a standard procedure proposed by the Francim network and were transferred to the Biostatistics Unit of Lyon University Hospital for analysis. In addition to quality controls performed by each registry, data coherence was verified using a control program developed by the International Center for Cancer Research (IARCtools Version 2.0, CIRC, Lyon, France). In the event of incoherence, a second quality control was performed by the issuing registry. Data retained for this analysis were gender, age, date of diagnosis, residence at time of diagnosis, and tumor localization and morphology (ICD-O, International Classification of Disease for Oncology) [5]. Gastrointestinal cancer mortality data for , required to estimate the number of gastrointestinal cancers nationwide, were provided by the Center of epidemiology of medical causes of death (CépiDc) of the national medical research institute (INSERM). CépiDc records all deaths (cause, gender, age) occurring in France by administrative area and by calendar year. To determine the population exposed to the risk of cancer, 1982, 1990, and 1999 census data were provided by the national statistics bureau (INSEE). Population estimates were extrapolated by the Francim network for years without a census. The number of person-years for the period was the sum of the number of persons exposed to risk for each of these five years. Statistical analysis Specific rates were calculated by age group and crude rates by gender and localization. Rates were then standardized in accordance with the demographic structure of the world population to allow comparison with rates observed in other regions of the world. Cumulative incidence was determined as the sum of 1-year age group rates. The cumulative incidence, expressed per 100,000 inhabitants, provides an index of the risk of developing cancer before the age of 74. The estimated national incidences for the year 2000 were established by modelizing the observed incidences and the mortality figures. Age and cohort effects were smoothed using an age-cohort model. The incidence of gastrointestinal cancer in France was determined by applying the incidence/mortality ratio obtained from the twelve registries to age-cohort-adjusted national mortality figures. This method makes the hypothesis that the incidence/mortality relationship observed in the aeras participating in the Francim network is representative of the national situation. The present statistical analysis was performed using an improved methodology, allowing better precision than in the two previous estimates. Incidence for preceding years was re-calculated to establish methodologically comparable data. Annual variations (expressed in percentages) were calculated with an age-cohort model, presuming a linear cohort effect. Results Geographical distribution ( ) Small geographical differences in the incidence of gastrointestinal cancers as issued from the twelve cancer registries are displayed in tables I and II. For cancer of the esophagus there was a wide variation in incidence in males. Areas with high incidence (Manche, Somme, Calvados), with intermediary incidence (Bas-Rhin, Côte-d Or, Doubs, Haut-Rhin Saône-et-Loire) and with low incidence (Isère, 878

3 Incidence of gastrointestinal cancers in France Hérault and Tarn) could be distinguished. Rates varied 4-fold. Cancer of the esophagus was exceptional in women. The gender ratio varied from 4 to 19 in the different areas. The geographical distribution of gastric cancer exhibited similar patterns in men and women. Incidences were lower in southern areas (Hérault and Tarn) and higher in Manche in both sexes and in Haut-Rhin in men. The gender ratio, about 2.5, changed little from one area to another. Incidence of small bowel cancer was not different between areas and was more frequent in women in Haut-Rhin. Few geographic differences were noted for colorectal cancer. The incidence ratios, compared to standardized ratios, from regions with high to low risk was 1.6 for men and 1.5 for women. Colorectal cancer was more frequent in both sexes in Bas-Rhin and Haut-Rhin and overall was more frequent in women than men (gender ratio depending on the area). The incidence was close to the national average in the other areas. Incidence of primary liver cancer was two to three times lower in southern areas (Hérault and Tarn) than in the other areas (particularly Isère, Haut-Rhin, and Bas-Rhin). Few differences were observed for cancer of the pancreas. For males, incidence in the areas with the highest rate was less than twice that in areas with the lowest rate; the difference was greater in females (2.5-fold). The sex ratio varied from 1 to 2.4 except in Hérault where it was particularly high. No major differences between areas was observed for bile duct cancer, which was characterized by female predominance, except in Hérault and Tarn. Cancer frequency The estimated number of new cases of cancers in France in 2000 was 161,025 in men and 117,228 in women. The estimates were 36,957 in men and 25,508 in women for gastrointestinal cancer. Gastrointestinal cancer thus accounted for 22.9% and 21.8% of all cancers in the male and female populations, respectively. World standardized rates were 74.2 in men and 34.2 in women per 100,000 inhabitants. Considering the entire population, colorectal cancer was the third leading cancer after breast and prostate cancer. It was the leading gastrointestinal cancer with 36,300 cases per year, i.e. 13% of all incident cancers (table III). Looking at the ten most frequent cancers in France, gastric cancer ranked number nine with slightly more than 7000 new cases annually and primary liver cancer number ten with nearly 6000 new cases annually. In males, colorectal cancer accounted for 53% of all gastrointestinal cancers. The probability of developing colorectal cancer before the age of 74 years was 4.9% in men and 2.9% in women. Primary liver cancer was the second leading gastrointestinal cancer, representing 14% of all cancers. By order of decreasing frequency, other gastrointestinal cancers in men ranked as follows: stomach and esophagus (about 10% of gastrointestinal cancers in men), pancreas (7%), bile ducts (2%), and small bowel (1%). In females, pancreatic and gastric cancers displayed nearly equivalent proportions (about 12% of gastrointestinal cancers in women), ranking second after colorectal cancer (66%). In women, other cancers ranked as follows: biliary tract (5%), esophagus (4%), primary liver (4%), and small bowel (1%). Incidence trends Estimated new cases and sex standardized rates for 1980 and 2000 are given in table IV. There was a general decline in the incidence of gastric cancer since 1980: -2.0% per year in men and -2.5% per year in women. The same type of trend was observed for esophageal cancer in men (-2.1% per year) but for women the incidence increased (+ 2.4% per year). The rising incidence of colorectal cancer reached + 1.0% per year for men and + 0.8% per year for women. The incidence of small bowel cancer also increased over the last twenty years, especially in men where the rate doubled. The greatest increase in incidence was observed for primary liver cancer: + 4.8% per year for men and + 3.4% per year for women. The number of new cases of primary liver cancer increased from nearly 2000 in 1980 to nearly 6000 in A less spectacular increase was observed in the incidence of pancreatic cancer: + 1.3% per year in men and + 2.1% per year in women. For biliary tract cancer, annual variations were small: 0.0% for men and -0.6% for women. Tableau II. Incidence a of gastrointestinal cancers in 12 French areas Period Incidence a des cancers digestifs selon le sexe dans 12 départements Période Liver Pancreas Biliary tract M F M F M F Bas-Rhin Calvados Côte-d Or Doubs Haut-Rhin Hérault Isère Loire-Atlantique Manche Saône-et-Loire Somme Tarn France a per 100,000 inhabitants standardized for the world population. 879

4 A.-M. Bouvier et al. Table III. Gastrointestinal cancer in France: estimates for Estimation du nombre annuel de nouveaux cas et des taux d incidence des cancers digestifs en France selon le sexe en Incident cases Crude rate Standardized rate a Cumulative rate (%) b M F M F M F M F Esophagus Stomach Small bowel Colon-rectum Liver Pancreas Biliary tract a per 100,000 inhabitants standardized for the world population; b cumulative rate 0-74 years per 100 inhabitants for the cohort born in 1928; M: male, F: female. Discussion These data provide useful informations concerning recent trends in the incidence of gastrointestinal cancer in France. The present analysis follows two earlier reports which covered seven areas for the period [6] and nine areas for the period [7]. The present analysis devoted to the period included data collected in twelve administrative areas covering approximately 15% of the total surface area of France. Analyzing the geographical distribution of gastrointestinal cancers in areas covered by a cancer registry raises the problem of database comparability. One of the objectives of the cancer registry network developed in France is to promote standard rules for data collection. The lack of an established evaluation criterion for registry quality made it difficult to verify data. Data validity was therefore checked using a set of criteria: rate of histological proof, incidence-mortality ratio, proportion of subjects aged over 75. In certain countries, the proportion of cases solely established from death certificates is a criterion. This approach cannot be used in France because of the imprecision of death certificates. Qualityof-registration criteria are reported for each registry in Cancer Incidence in Five Continents [8] where only data fulfilling the quality criteria are published. Since the analysis of French registries has not revealed any significant deviation, it can be concluded that the differences observed in the present study are not related to registration procedures. The methodology used to estimate national incidence was based on the incidence/mortality ratio which has been improved since the earlier estimates. Incidence and mortality data observed in the populations covered by a registry were adjusted using an age-cohort model. The estimated incidence/mortality ratio produced by the model was applied to the mortality rates predicted by an age-cohort model resulting from mortality data for the entire French population. Alcohol and smoking have been recognized as the two main risk factors for cancer of the esophagus for many years. An estimated 80% of all cases can be attributed to alcohol- and smokingrelated risks [9]. However, inter-area differences in smoking habits and alcohol consumption are insufficient in explaining the wide differences observed. In an attempt to understand this discrepancy, a case-control study was conducted in the cities of Caen (high risk), Dijon (average risk), and Toulouse (low risk). This study revealed that the level of alcohol consumption explained at best 10% of regional differences in incidence [9]. Conversely, the habit of spiking coffee with spirits (calvados) explains 60 to 70% of the difference in incidence. Calvados is no more dangerous than any other alcohol, unless consumed hot. The study demonstrated that drinking strong spirits hot is highly dangerous. This corroborates a report on consumption of hot maté in Uruguay and Brazil [10]. It was also found that aniseed-flavored alcoholic beverages are as Table IV. Trends in national incidence of gastrointestinal cancers between 1980 and Évolution de l incidence nationale des cancers digestifs entre 1980 et Number of cases Men Women Esophagus Stomach Small bowel Colon rectum Liver Pancreas Biliary tract a : per 100,000 inhabitants standardized for the world population. 880

5 Incidence of gastrointestinal cancers in France dangerous as hot calvados, but that drinking habits, similar in all regions, cannot explain the regional variations [9]. Regional differences can also be explained, though to a lesser degree, by the protective effect of fruits and vegetables [11]. In France, incidences of cancer of the esophagus in men decreased from 4,984 in 1998 to 4,040 in 2000, while in women incidence rose from 473 to 928. A similar pattern is observed for cancers of the ear, nose and throat, which have similar causes [12]. In men, these trends are explained by decreased alcohol consumption, while alcohol consumption and smoking have increased in women. There was little difference in the incidence of gastric cancer between the areas included in this study. The lowest rates were found in the South of France. The protective effect of the Mediterranean diet rich in fruits and vegetables could explain these findings. Cancer of the stomach was the fourth ranking cancer in [6] and the ninth in Incidence has declined more than 35% in both sexes over the last 20 years. More detailed analysis shows that the pattern is not the same for all gastric cancers. Cancer of the cardia has remained stable while incidence of cancer in the distal two-thirds of the stomach is on the decline [13, 14]. The lower incidence of distal cancers can be explained both by a cohort effect related to decreased prevalence of Helicobacter pylori infection and by a period effect, which is related to widespread use of refrigeration allowing consumption of fresh fruits and vegetables throughout the year and to the decline in the consumption of salted and smoked food [15]. The causes of proximal cancers are less well known. Between 1980 and 2000, the number of new cases of colorectal cancer increased approximately 50%, with a more marked increase in men than women. Population aging explains a large part of this variation; the age-adjusted increase rate was 16%. Most reports have clearly demonstrated the effect of high-calorie diet, sedentary lifestyle, and low-vegetable diet [14]. In Japan, incidence of colorectal cancer has become as high as in western countries since the adoption of western-style diets. This indicates that changes in diet may have an effect on the risk of colorectal cancer over a 10-year period. Colorectal cancer did not display important differences between areas. The highest incidence was found in two areas in Alsace, Bas-Rhin and Haut-Rhin. In general, the incidence of gastrointestinal cancer is higher in Alsace than other regions of France. Mass screening for colorectal cancer is being implemented in twenty administrative areas including seven covered by cancer registries. The goal is to reduce colorectal cancer-related mortality, but the program can also be expected to have a long-term lowering effect on incidence. Primary liver cancer was rarer in southern areas (Hérault, Tarn) than in other areas where it was 2 to 3 times more frequent. The reason for this difference is not known. Etiological inquiries would be required to examine this point. One of the more remarkable findings of the present analysis is the very strong rise in the incidence of primary liver cancer. The increase is more marked in men. Primary liver cancer has become the second most frequent gastrointestinal cancer in the male population. By enabling diagnosis of formerly unrecognized tumors, advances in imaging techniques over the last twenty years could explain at least part of this trend. Morphological criteria used for diagnosis are also more precise, but the fact that the incidence trend is not the same in men as in women suggests that factors other than improved diagnostic procedures are involved. More than three-quarters of the patients who develop liver cancer have cirrhosis. It has been suggested that one effect of improved prognosis of cirrhosis and better management would be to allow liver cancer enough time to develop. The increased incidence of viral hepatitis (B and C)-related cirrhosis is another factor affecting the increased incidence of primary liver cancer [16]. For cancer of the small bowel and the biliary tract, the incidences observed in the areas studied were quite similar. These cancers are less frequent than digestive tract or hepatic cancers and represent 1.3 and 3.1% respectively of all gastrointestinal cancers. Their incidence is also on the rise but less so than for primary liver cancer. Here again, imaging techniques may have an effect. The causes of these cancers are poorly elucidated making it difficult to interpret the observed trends. Summarizing, with the exception of cancer of the esophagus and primary liver cancer, the geographical distribution of gastrointestinal cancers varies little in France. 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