© The Author (2008). Published by Oxford University Press. All rights reserved
Trend in Incidence of Adenocarcinoma of the Esophagus in Japan, 1993–2001
1 Yamagata Prefectural Medical Center for Cancer and Life-style Related Disease, Yamagata
2 Cancer Information Services and Surveillance Division, Center for Cancer Control and Information Services, National Cancer Center, Tokyo, Japan
For reprints and all correspondence: Akiko Shibata, Yamagata Prefectural Medical Center for Cancer and Life-style Related Disease, 1800 Aoyagi Yamagata, 990-2292 Yamagata, Japan. E-mail: shibata_a{at}ypch.gr.jp
Received April 10, 2008; accepted June 17, 2008
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Abstract |
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Background: Several studies with population-based cancer registry data have suggested that incidence of adenocarcinoma of the esophagus has been increasing since 1970 in some European and North American countries and Australia. However, data from Asian countries with regard to the incidence of esophageal cancer by histological type based on the population-based cancer registry are lacking. The aim of this study was to describe the incidence of esophageal cancer by histological type in a Japanese population.
Methods: Cancer incidence data for 1993–2001 from 15 population-based cancer registries were collected by the Japan Cancer Surveillance Research Group in 2005. We used data from eight registries corresponding to inclusion criteria for data quality.
Results: Squamous cell carcinoma remains the predominant type in all esophageal cancers in Japan. The ratio of squamous cell carcinoma to adenocarcinoma is 26:1. For adenocarcinoma, estimated average annual percentage change was 4.7% (95% confidence interval: 0.7, 8.9) in men and 6.0% (2.4, 9.8) in women. Age-adjusted incidence rate (the world standard population) per 100 000 for 2001 was 0.3 in men and 0.05 in women. Incidence of squamous cell carcinoma was increasing slightly in men and nearly constant in women. Age-adjusted incidence rate for 2001 was 8.2 in men and 1.0 in women.
Conclusion: No dramatic increase in adenocarcinoma has occurred, and absolute incidence remains low in Japan.
Key Words: esophagus adenocarcinoma incidence
A rising trend of incidence of adenocarcinomas of the esophagus was first reported from the USA in 1991 (1). Several subsequent reports on the incidence of esophageal cancer by histological type based on population-based cancer registries have revealed dramatic increases in the incidence of adenocarcinomas of the esophagus in the USA, Canada, Australia and some European countries over the last three decades (2–7). Some studies have investigated the associations between this increasing trend and factors, such as misclassification of tumor sites (lower esophagus versus gastric cardia) or over-diagnosis resulting from increased use of upper endoscopy (8,9), and concluded that the rising trend was unlikely to be explained by such information bias.
Recent studies suggest that being a white male, high body-mass index (BMI), Barrett's esophagus, gastro-esophageal reflux disease (GERD) and absence of Helicobacter pylori (H. pylori) infection represent substantial risk factors for adenocarcinomas of the esophagus (10). In Japan, risk factors such as obesity and absence of H. pylori infection seem to be increasing (11,12), and we thus need to start monitoring trends in the incidence of adenocarcinoma of the esophagus. A previous study based on the data collected from a lot of hospitals throughout Japan has reported that no increase in the relative proportion of adenocarcinomas among all reported esophageal cancers was identified over the period 1980–94 (13). International Agency for Research on Cancer provides incidence rates of esophageal cancer by histological type from Osaka, Miyagi and Nagasaki cancer registries up to 1997, respectively (14). However, incidence rates of esophageal cancer by histological type throughout Japan have not been available.
In 2005, a research group supported by the Ministry of Health, Labor and Welfare started collecting cumulative incidence data from several population-based cancer registries in Japan that met various criteria for data quality, and included the data into a database. The purpose of this study was to describe the trends in the incidence of esophageal cancer by histological type in Japan during 1993–2001.
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MATERIALS AND METHODS |
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We used cancer incidence data for 1993–2001 from 15 population-based cancer registries collected by the Japan Cancer Surveillance Research Group in 2005. Since 1975, national estimates of cancer incidence in Japan have been provided and published by this research group (15,16).
All primary malignant neoplasms of the esophagus (International Classification of Diseases for Oncology, Third Edition: ICD-O-3) topography codes C15.0–C15.9, morphology codes 8000–9581 and behavior code 3, excluding lymphomas, were included in this study. Seven registries were excluded from the analysis because the percentage of histologically verified diagnosis (%HV) of esophageal cancers comprised <70% registered cases. Finally, this analysis was performed using the data from the following eight registries: Miyagi, Yamagata, Niigata, Fukui, Shiga, Osaka, Saga and Nagasaki. Mean proportion of death certificate only (DCO) cases was 15.6% and %HV was 79.1% in these registries between 1993 and 2001. The population covered by the eight registries totaled 19 400 747, corresponding to 15% of the total population of Japan in 1997. Mortality data were obtained from the Japanese Ministry of Health, Labor and Welfare using the National Vital Statistics.
Esophageal cancers were divided into the following histological categories: squamous cell carcinoma (ICD-O-3 codes 8050–8084), adenocarcinoma (ICD-O-3 codes 8140–8384), other specified malignant neoplasm (ICD-O-3 codes 8011–8046, 8090–8131 and 8380–9581) and neoplasm not otherwise specified (NOS) (ICD-O-3 codes 8000–8010). Esophageal cancers were also classified according to one of the following subtypes: upper third or cervical area (ICD-O-3 codes C15.0 and C15.3), middle third or thoracic (ICD-O-3 codes C15.1 and C15.4), lower third or abdominal (ICD-O-3 codes C15.2 and C15.5) and origin intermediate or NOS (ICD-O-3 codes C15.8 and C15.9). Cancer cases were classified according to age (5-year age groups up to +85 years) and sex.
Statistical Methods
Incidence and mortality rates were estimated and age-adjusted to the 1985 Japanese model population or the world model population using direct adjustment. Point estimates and 95% confidence intervals (CIs) of estimated average annual percentage change (EAPC) in incidence and mortality rates during the study period were estimated by fitting a log-linear regression model to the standardized incidence using the least squares method. The model was of the form log Y = a + bx, where Y is the estimated standardized incidence rate and x is the year of incidence. The expression 100 (10b – 1) is an estimate of the annual percentage change in this rate. All statistical analyses were performed using Intercooled Stata 8.0 for Windows software (StataCorp LP, College Station, TX, USA).
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RESULTS |
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During the period from 1993 to 2001, a total of 20 093 patients were diagnosed with esophageal cancer in the eight regional cancer registries in Japan. Proportions of esophageal cancer by histological type, sub-site, calendar year of diagnosis and sex are shown in Table 1. Squamous cell carcinoma was the predominant histological type during the study period (mean percentage: 73.3% for men; 66.0% for women). Mean percentage of adenocarcinomas was <3% and the ratio of squamous cell carcinomas to adenocarcinomas was 26:1. The distribution of cases with histology of ‘other types and unspecified' was almost constant throughout 9 years and mean percentage was 25.3%. Since sub-sites belonging to ‘origin intermediate or NOS' accounted for 60.1%, we could not perform further analysis of sub-sites.
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Age-standardized (the 1985 Japanese model population) incidence rates (ASIRs) and mortality rates (ASMRs) per 100 000 person-years of esophageal carcinoma between 1993 and 2001 are shown in Fig. 1. For men, incidence rates were slowly increasing, with an EAPC of 1.68% (95% CI: +0.73, +2.63) and a point-estimated ASIR (the world model population) for 2001 of 11.5. For women, incidence rates were nearly constant, and point-estimated ASIR (the world model population) for 2001 was 1.5. Mortality rates increased slightly for men (EAPC: 1.22; 95% CI: 0.13, 2.33) and declined gradually for women (EAPC: –1.09; 95% CI: –2.55, 0.08).
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Figure 2 shows the trends in ASIR by the histological types of esophageal cancer. Incidence rates were 7- to 8-fold higher in men than in women irrespective of histological type. Risk of squamous cell carcinoma was over 20-fold greater than that of adenocarcinoma, regardless of sex. Incidence of squamous cell carcinoma increased slightly during the period for men, but was nearly constant in women. Table 2 shows the incidence trends of esophageal cancer by histological types expressed as EAPC over the interval. For men, we observed annual increases in the incidence of all esophageal cancers and all histological subtypes. Point-estimated ASIRs (world population) in 2001 for adenocarcinoma and squamous cell carcinoma were 0.3 and 8.2, respectively. For women, annual changes were not significant in the incidence of all esophageal cancers, squamous cell carcinomas and other types and NOS carcinomas, with only adenocarcinomas showing an annual increasing trend. Point-estimated ASIRs (world population) in 2001 for adenocarcinoma and squamous cell carcinoma were 0.05 and 1.0, respectively.
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DISCUSSION |
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Our data demonstrate that no dramatic increase in adenocarcinoma of the esophagus has occurred in Japan. Although incidence rates of adenocarcinoma of the esophagus are gradually increasing in both sexes, absolute incidence rates remain much lower than those of squamous cell carcinoma and those of most Western countries (1,3–6).
Vizcaino et al. (6) described the time-trend of the incidence of both major histological types of esophageal carcinomas in selected countries worldwide. According to that description, Western countries, with some exceptions, are displaying increasing incidence rates of adenocarcinoma and relatively stable or decreasing rates of squamous cell carcinoma. In most countries in 1970s, the rates of squamous cell carcinoma among men were over one per 100 000 person-years (the world population model) and those of adenocarcinoma were below one per 100 000 person-years. However, in the USA (white), Canada, Australia, Scotland, Denmark and Iceland, the incidence rates of adenocarcinoma among men have caught up with or surpassed those of squamous cell carcinoma up to 1995 and rates of adenocarcinoma reached over one per 100 000 person-years. Reliable incidence data for esophageal cancer by histological types are limited. Fernandes et al. (7) reported that the incidence rate of squamous cell carcinoma among men had decreased to 3.9 per 100 000 person-years and those of adenocarcinoma was increasing gradually up to 0.5 per 100 000 person-years in 2002 in Singapore. For the current study in Japan, the incidence rate of squamous cell carcinoma among men was still 8.2 per 100 000 person-years (world population), whereas the rate of adenocarcinoma was 0.3 per 100 000 person-years in 2001. With regard to adenocarcinoma, the incidence trends in Japan resemble those in Singapore.
The most potent risk factors for adenocarcinomas of the esophagus appear to be obesity and the absence of H. pylori infection (10). The association between high BMI and adenocarcinoma of the esophagus has been investigated in numerous studies, and a meta-analysis eventually supported a positive association in 2006 (17). In Japan, although the proportion of overweight adults (BMI 
25) increased from 19.0 to 22.4% (x1.23) between 1980 and 1995, that percentage is still only half the level of many Western and Oceanian countries (WHO: Global Database on Body Mass Index. http://www.who.int/bmi/index.jsp). Another possible risk factor for adenocarcinoma of the esophagus is the absence of H. pylori infection. However, previous study results regarding this inverse association have been inconsistent, and many investigators have speculated that H. pylori infections causing severe pangastritis could decrease gastric acid secretion and protect against the development of GERD, Barrett's esophagus and adenocarcinoma of the esophagus (10). In Japan, more than 80% of the population born before 1950 is positive for H. pylori (12,18), and an active recommendation for eradication of H. pylori in patients with gastric ulcer was just started in 2000. The majority of individuals covered in this study were thus still likely to be H. pylori positive. The insignificant increase in the incidence of adenocarcinoma is likely to have resulted from a lower prevalence of overweight adults and higher prevalence of H. pylori positive individuals in the Japanese population compared with Western countries.
For squamous cell carcinoma of the esophagus, incidences are stable or decreasing slowly in both sexes in most countries (6). As an exception, the incidence of squamous cell carcinoma among females increased rapidly in Switzerland between 1980 and 1995. Conversely, incidence of squamous cell carcinoma decreased progressively in Singapore between 1968 and 2002 (7).
The strongest risk factors for squamous cell carcinoma of the esophagus are smoking and drinking (19). According to the Japanese National Survey, the proportion of daily smokers decreased by 12% among men and increased by 2.6% among women between 1989 and 2004, and 43% of the male population and 12% of the female population remained daily smokers as of 2004 (20). In the same way, the proportion of daily drinkers decreased by 3.1% among men and increased by 2.2% among women between 1989 and 2002, and 49% of the male population and 8.5% of the female population were still daily drinkers as of 2002. Considering the higher prevalence of these risk factors in the Japanese population, the high absolute incidence of squamous cell carcinoma is likely.
The present study displays some limitations. First, despite using combined data from multiple regional cancer registries offering better quality data, DCO was 15.6%. This is considerably inferior to the international standard level (6). However, we consider our data trustworthy enough to evaluate the trends of incidence rate for esophageal cancer by histological subtype, as 5-year relative survival rate for esophageal cancer remains poor in Japan, at 26% in 1993–96, and the trends in the incidence and mortality of all esophageal cancers have been changing in parallel during the study period (21).
Secondly, our data included 
25% of the cases with unspecified histology, 10-fold greater than the cases with adenocarcinoma. However, we consider that our data were sufficient to allow the observation of the incidence trends for esophageal cancer by major histological subtype, since the proportion of histologically unspecified carcinomas was stable throughout the study period. And these data are the only available measures to discuss incidence rate of esophageal cancer by histological type throughout Japan.
In conclusion, we identified that no dramatic increase in adenocarcinoma of the esophagus has occurred and the absolute incidence remained low in Japan. The incidence trends for esophageal cancer by histological type in Asia appear to differ from those of many Western countries. This fact could be useful in identifying risk factors for adenocarcinomas of the esophagus.
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Funding |
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This study was supported by the 3rd-term Comprehensive 10-year Strategy for Cancer Control.
Conflict of interest statement
None declared.
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Acknowledgements |
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Data used in this publication were collected by the Japan Cancer Surveillance Research Group. The contributions of the following regional cancer registries are gratefully acknowledged: Miyagi, Yamagata, Chiba, Kanagawa, Niigata, Fukui, Aichi, Shiga, Osaka, Tottori, Okayama, Saga, Nagasaki, Kumamoto and Okinawa.
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