Changing Pattern of Oesophageal Cancer Incidence in France
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1 International Journal of Epidemiology O International Epktemlotogical Association 1994 Vol. 23, No. 2 rinted In Great Britain Changing attern of Oesophageal Cancer Incidence in France G LAUNOY,* J FAIVRE," IENKOWSKI,* C MILAN," M GIGNOUX* AND D OTT1ER* Launoy G (Registre des Cancers Digestifs du Calvados, Faculte de medecine, CHU C6te de Nacre, Caen Cedex, France), Faivre J, ienkowski, Milan C, Gignoux M and ottier D. Changing pattern of oesophageal cancer incidence in France. International Journal of Epktemiology\994; 23: Background Data from several Western countries suggest a rapid increase in the incidence of adenocarcinoma of the oesophagus, as well as variations in the sex ratio and the subsite distribution of oesophageal cancer. Although France has a high incidence rate of oesophageal cancer in males, no information was available on trends in its occurrence. The purpose of this study was to report changes in the pattern of oesophageal cancer incidence in three regions of France. Methods. Data from the three population-based cancer registries of Calvados, Cote d'or and Haute-Garonne were used to study time trends of oesophageal cancer by sex, age, subsite and histological type between 1978 and Annual incidence rates have been standardized by the direct method using the world standard population. To test the trend in cancer incidence, either an exponential curve of the form y = ae was fitted to the annual incidence rates by means of a regression technique, or incidence rates were compared between two 5-year periods after age standardization by Mantel-Haenszel test. Results. The mean annual variation of oesophageal cancer in males was - 2.9% in Calvados ( < 0.05), + 0.5% in Cote d'or () and % in Haute-Garonne (< 0.05). The corresponding figures in females were + 7.9% (), % (< 0.05) and % (). The significant variations in males (decrease In Calvados and increase in Haute-Garonne) were confined to the oldest age group ( 65 years). With regard to subsite, incidence in males increased in Haute-Garonne for the upper and the middle third, while there was a significant decrease in Calvados only for the middle third. For histological type, no increase in adenocarcinoma was noticed in males while there was a slight increase in incidence in females (statistically significant in Calvados). Conclusions. In France, the incidence of oesophageal cancer has decreased in the high-risk region (Calvados) in males, while there was a slight increase in the three studied regions in females. The important rise in incidence of oesophageal adenocarcinomas observed in some Western countries has yet to be seen in France. Data from the US 1 the UK 2 and Switzerland 3 suggest a rapid increase in the incidence of adenocarcinoma of the oesophagus as well as variations in the sex ratio and the subsite distribution of oesophageal cancer. Among Western countries, France has an exceptionally high incidence rate for oesophageal cancer in males. Large variation in incidence has been reported between the North West and the South of France. 4 In spite of its importance, no information was available on changing patterns of incidence of this cancer in France. The purpose of this study was to analyse the trends of oesophageal cancer incidence rate by year of diagnosis, sex, age, subsite and histological type in different geographical areas using data from three population-based digestive cancer registries in France. Registre des Cancers Digestifs du Calvados, Faculte de mmecine, CHU C6te de Nacre, Caen Cedex, France. Digestive Cancers Registry of Cote d'or, France. t Digestive Cancers Registry of Haute-Garonne, France. OULATIO AND METHODS The study included all cases of oesophageal carcinoma (OC) registered between 1978 and 1987 in the Calvados and Cote d'or regions and between 1982 and 1987 in the Haute-Garonne region (where the cancer registry was created more recently). The three cancer registries are population-based and include inhabitants in Calvados, in Cote d'or and in Haute- Garonne (data from the 1990 census). Data have been collected from public and private pathology laboratories, university and local hospitals, the 'Anti-cancer Institute', private surgeons and gastroenterologists. A total of 1659 oesophageal cancers were recorded: 1056 in Calvados, 381 in Cote d'or and 222 in Haute-Garonne. Overall age-standardized incidence rates in males were 28.6/ in Calvados, 11.6/ in Cote d'or and 5.9/ in Haute-Garonne. Corresponding figures for females were 1.6/ , 1.0/ and 0.6/ For all cases sex, age at diagnosis, subsite, and histological type were recorded. The cancer site was coded according to the International Classification of 246
2 OESOHAGEAL CANCER IN FRANCE Calvados-p<0.05 C6ted'Or- * Hte-Garonne-p<0.05 Diseases for Oncology 5 using four categories: upper third (UT) (150.3), middle third (MT) (150.4), lower third (LT) (150.5) and unspecified (150.9). Endoscopic data, radiological data and surgical data were taken into consideration when determining the subsite. When the cancer overlapped two subsites, it was coded as the upper site. The subsite was known in 92.3% of the cases (92.8% for Calvados, 96.3% for Cote d'or and 82.8% for Haute- Garonne). Histological type was determined according to the World Health Organization classification. There was no histology in 9.5% of the cases (10.9% in Calvados, 7.6% in Cote d'or and 6.3% in Haute-Garonne). FIGURE 1 Trends of cancer of the oesophagus in three French regions in males opulation data used in calculating incidence rates were based on estimates of the population of the three regions by year, age and sex by interpolation from the census data provided by the Institut National de la Statistique et des Etudes Economiques (IEE). To facilitate comparisons, annual incidence rates have been standardized by the direct method using the world standard population. To test the trend in cancer incidence an exponential curve in the form y = ae h was fitted to the annual incidence rates by means of a regression technique. This allowed a direct interpretation of the annual average per cent change which is given together with the TABLE 1 Mean annual variation in age-standardized incidence rate for oesophageal cancer in males according to age and location Calvados Cote d'or Haute-Garonne Age group <64 > % (-2.0,+3.0) -5.0%»(-9.7,-0.2) + 2.0% (-5.4,+9,4) + 1.9% (-4.8,+ 8.5) %(-5.2,+25.1) %* (+0.4,+29.7) Location Upper third Middle third Lower third -1.0% (-5.5,+3.4) - 3.0W (- 6.0,0) + 2.3% (-4.7,+9 J) + 6.3% (-4.1,+ 16.6) + 0.5% (- 4.8,+ 5.9) -3.1% (-17.1,+ 10.8) %* (+2.2,+22.6) %'(+2.1,+22.5) % (-4.8,+44.6) All -2.9%»(-5.8,0) + 0.5%(-4.8,+5.9) %* (+ 2.2,+ 22,6)
3 248 INTERNATIONAL JOURNAL OF EIDEMIOLOGY Calvados- C6ted'Or-p<0.05 * Hte-Garonne- FIGURE 2 Trends of cancer of the oesophagus in three French regions in females 95% confidence interval (CI). When the number of patients was too small, for instance in females, incidence rates were compared between two 5-year periods: and This was done only for Calvados and Cote d'or after age standardization by Mantel- Haenszel test. RESULTS Time Trends According to Sex Time trends in age-adjusted incidence rates by sex are shown in Figures 1 and 2. In males the overall incidence of OC decreased in Calvados by an average of- 2.9% (± 2.9) per year and increased in Haute-Garonne by % (± 10.2) per year and in Cote d'or by + 0.5% (± 5.3) per year. In females, the incidence of OC increased in all three regions. The mean annual variation was 19.4% (± 16.0) in Cote d'or, 7.9% (± 10.4) in Calvados and 50.7%(± 51.9) in Haute-Garonne. Consequently, the sex ratio decreased in Calvados from 26.4 in the period to 15.6in the period (<0.05) and in Cote d'or from 16 to 11.1 ( < 0.05). In Haute- Garonne, the sex ratio was 9.8 for the period. Time Trends According to Age In males, under the age of 65, no time trend was identified in any region (Table 1), but for males aged > 65, a TABLE 2 Comparison ofoesophageal cancer mddence (and numbers) in females by age and location after age standardization between two 5-year periods Calvados Cote d'or Age group «64 > 64 Location Upper third Middle third Lower third 0.6 (8) 9.4(21) 03(4) 1-3(19) 0.3(5) 1.3(17) 12.1 (27) 0.6(9) 1.1(17) 1.0(15) (5) 5.3 (10) 0.5(6) 0.5(6) 02(2) 0.6(6) 6.6(13) 02(3) 0.5(6) 0.7(9) 0.08 * Not significant.
4 OESOHAGEAL CANCER IN FRANCE 249 TABLE 3 Comparison of oesophageal cancer incidence (and numbers) by hislological type after age standardization between mt> 5-year periods Calvados Cote d'or Main Squamous ccd carcinoma Aden oca rtinoma Others No histology Females Squamous cell carcinoma Adenocarcinoma Others No histology * Not significant 26.9 (384) 1.4(20) 2.2(31) 4.5(65) 1.4(21) 0.4(6) 27.6 (404) 1-2(18) 1.6(23) 2.6(37) 2.1 (32) 0.6(10) 0.1 (2) decrease in incidence was observed in Calvados (/" < 0.05) and an increase in Haute-Garonne (< 0.05). In females, the incidence of OC increased in both age groups in Calvados and in Cote d'or but not significantly (Table 2). Time Trends According to Subsite Mean annual variation in age-adjusted incidence rates for the three locations of OC in males are given in Table 1. Incidence of oesophageal cancer in males increased for the three studied subsites in Haute-Garonne. The mean annual increase was statistically significant for the upper third and the middle third. In Cote d'or, the incidence remained steady whatever the subsite. In Calvados, there was a significant decrease in incidence of cancers of the middle third, while the other subsites remained stable. Table 2 shows the evolution of incidence for females in Calvados and C6te d'or regions over two 5-year periods: incidence of cancers of the upper third and middle third remained steady, while incidence of cancer of the lower third increased slightly in both regions. Therefore, the proportion of lower third cancers increased considerably in both sexes: in Calvados, from 25.8% to 30.0% in males () and from 17.8% to 36.5% in females () and in Cote d'or, from 28.1 % to 31.8% in males () and from 14.2% to 50.0% in females ( < 0.05). Time Trends According to Histological Type Table 3 shows the evolution of the different histological types of OC in Calvados and Cote d'or in both sexes. In males, cancers with no histology decreased significantly in both regions. In females, the incidence of adenocarcinoma (ADC) and squamous cell cancer (SCQ increased in both regions. Only ADC in Calvados increased in a significant way. When data from the two areas were combined, the mean age of ADC was higher than that of 1 <0.02 < (136) 0.4(5) 2.1 (24) 1.0(12) 03(3) 135(158) 11(13) 0.8 (8) 1.3(16) 0.2(2) <0.02 SCC in males (66.2 versus 62.2, < 0.05). There was however no difference in females (68.3 versus 68.4, ). In males in Calvados adenocarcinomas represented 4.6% of known histological types (20/435) for the period and 4.2% (18/427) for the period. The corresponding figures in Cote d'or were 3.5% (5/141) and 7.6% (13/171). In females the corresponding figures were 4.3% (1/23) and 23.3% (10/43) in Calvados, 0% (0/12) and 11.8% (2/17) in Cote d'or. In Calvados, the sex ratio for SCC was 22.4 and 5.2 for adenocarcinoma. Unfortunately, numbers were too small to calculate similarfiguresfor Cote d'or. DISCUSSION A study such as this which aims to analyse the changing pattern of OC incidence needs accurate and complete data on distribution of cancer by subsite and histological type. In some registries adenocarcinomas of the oesophagus have been systematically coded as adenocarcinomas of the cardia. 6 ' 7 Our data come from three population-based cancer registries which collect detailed data on localization of cancer and histological type. The data are extensively cross-checked and validated. It is believed that nearly all cases of OC are registered and hence the data needed for this study are largely complete. However the subsite remained unspecified in 7.7% of the cases and there was no histological examination for 9.5%. The proportion of cases without histological proof decreased over the study period. This is presumably due to the use of endoscopy which, for instance, increased in Cote d'or from 81%in 1978 to 98% in Time trends analysis of OC incidence in France over the past 10 years has revealed varying results for males. In the lower-risk region (Haute-Garonne), the overall incidence increased for all sites in a significant way. In
5 250 INTERNATIONAL JOURNAL OF EIDEMIOLOGY the intermediate-risk region (Cote d'or), the incidence remained steady, but in the high-risk region (Calvados), there was a significant decrease in incidence mainly in relation to a decrease in the over 65 year age group and for the middle third. Recent data have shown that observed trends in OC incidence cannot be systematically related to changes in alcohol and tobacco consumption and certain dietary changes in the population, e.g increased intake of fruits and vegetables, may have overridden the effect of alcohol and tobacco. 8 aradoxical trends in cancer mortality rates in relation to smoking and drinking have been observed in Europe. 9 However, case-control studies conducted in France have shown that, in men, nearly 90% of the risk of OC can be attributed to alcohol and tobacco consumption. 8 ' 9 Thus for males, despite the lack of accurate data on trends of alcohol consumption in this region, the observed decrease in incidence in Calvados could be related to a change in alcohol consumption. The reduction of alcohol consumption in France between 1943 and 1948 due to World War II was followed by a drop in OC mortality. l0 These data suggest that any effect of a reduction in alcohol and tobacco abuse would be seen rapidly. Time trend analysis of incidence in other Western countries which share, at least partly, common aetiological factors, do not indicate considerable change in overall incidence. Incidence data from the last three volumes of Cancer Incidence in Five Continents, l3 ~ 15 which cover a 15-year period, show stability or a slight decrease in males. However, in females, there is a slight increase in incidence similar to that observed in the three studied areas in France, which could be attributed to the increased use of tobacco and alcohol by women. 16 These trends tend to reduce the epidemiological differences of OC between high-, intermediate- and low-risk areas in France and to reduce the male/female ratio which remains, however, in France, the highest in the world. Data from US population-based cancerregistriesparticipating in the SEER programme indicate that incidence rates for adenocarcinoma of the oesophagus are rapidly rising.' In Connecticut the proportion of adenocarcinoma has increased from 4% between 1955 and 1969 to 23% between 1983 and Similar trends have also been reported in the West Midlands, in the UK 2 and in the canton of Vaud, Switzerland. 3 In contrast, such significant changes were not found in France during the short period of this study. There was only a slight increase in the incidence of adenocarcinoma of the oesophagus mainly in females, which was statistically significant only in Calvados. In this region, during the same period ( ), the incidence of adenocarcinoma of the cardia remained steady in both sexes. 17 During the period, adenocarcinoma still represented only 6% of histologically verified OC in Calvados and 8% in Cote d'or. The important rise in the incidence of oesophageal adenocarcinoma observed in some Western countries, where they represent about one-third of all OC, has yet to be seen in France. Contrary to observations in other areas in the world, our data show that the male to female ratio for adenocarcinoma is lower than that for squamous cell carcinomas. In addition, the mean age at diagnosis for adenocarcinoma in males is higher than that for squamous cell carcinoma while it is similar in females. In contrast to squamous cell carcinomas, most adenocarcinomas are found in the lower third. Similar figures are also reported in other studies. 18 Other data indicate that whereas the incidence of squamous cell carcinoma is inversely related to socioeconomic status, the incidence of adenocarcinoma is directly correlated to this factor. For example, whites in the US have a higher risk of developing adenocarcinoma but a lower risk of squamous cell carcinoma in comparison to blacks. Descriptive epidemiological and case-control data suggest that the different histological types of OC exhibit at least partly different aetiologies. Alcohol and tobacco consumption seem to have less effect on the development of adenocarcinoma than on the development of squamous cell carcinoma. 20 One known predisposing condition for adenocarcinoma of the oesophagus is Barrett's oesophagus. It has been reported that about 90% of oesophageal adenocarcinomas were found to be associated with such lesions. 21 The prevalence of Barrett's oesophagus appears to be too high (376 per in an autopsy series) to justify a systematic endoscopic surveillance of all cases. Other factors which result in a high-risk of malignant change must be identified in order to propose a secondary prevention strategy. In fact, adenocarcinomas of the oesophagus seem to share common epidemiological characteristics not with squamous cell cancer of the oesophagus but rather with adenocarcinomas of the cardia suggesting a common aetiology. 22 The aetiology of adenocarcinomas of both the oesophagus and the cardia must be more accurately characterized. Although no increase in incidence of this cancer has yet been seen in France, this challenge is of importance because of its continued increase in incidence in many areas in the world. ACKNOWLEDGEMENT This work was conjointly supported by Institut National de la Sant6 et de la Recherche Medicale and Direction Generate de la Sante.
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