Decreasing Trend of Esophageal Adenocarcinoma in Hong Kong

While the incidence of esophageal squamous cell carcinoma is decreasing, the incidence of esophageal adenocarcinoma is increasing in the Western Europe and United States (1-4). In Japan, there was increased incidence of both esophageal adenocarcinoma and squamous cell carcinoma (5). Decreasing Helicobacter pylori infection, rising prevalence of gastroesophageal reflux disease, and increased occurrence of Barrett's esophagus are important causes of the increasing trend of esophageal adenocarcinoma (5, 6).

However, the ratio of esophageal adenocarcinoma versus squamous cell carcinoma has not increased in last two decades in a Taiwan study (7). In Hong Kong, gastroesophageal reflux disease is getting more common with 3% to 7% of the population reporting heartburn or acid reflux equal or more than once weekly (8) and the prevalence of H. pylori has decreased from 58.4% in 1994 (9) to 50% in 1998 and 40% in 2002 (10). Hong Kong Chinese adopt a Westernized life-style. These may theoretically increase esophageal adenocarcinoma locally. However, data concerning the trend of esophageal adenocarcinoma and the ratio of adenocarcinoma versus squamous cell carcinoma in Hong Kong are not available. Therefore, a study examining the actual and relative incidence of esophageal adenocarcinoma and squamous cell carcinoma in the last two decades in Hong Kong was conducted.

Data of patients with newly diagnosed esophageal cancer during the period 1984 to 2003 were obtained from the Hong Kong Cancer Registry. The cases of esophageal cancer corresponded to the C15 code of the 10th revision of the International Classification of Diseases. The Hong Kong Cancer Registry is population-based and is a member of the International Association of Cancer Registries. It has series of comprehensive cross-checking programs to ensure the accuracy of the data. This registry has access to nearly all hospital/laboratory cancer data in both private and public sectors. Population data during the corresponding period were obtained from Hong Kong Census and Statistics Department. Midyear population data were used in the calculation of the incidence rate. Cases were grouped into four periods, namely 1984 to 1988, 1989 to 1993, 1994 to 1998, and 1999 to 2003.

Age standardized rate (WSR) for esophageal cancer was calculated based on the world standard population published in the WHO World Health Statistics Annual 1997 to 1999. Average WSR of each period was calculated by averaging the WSR of the 5 years in each period with adjustment made for cases with missing histology.

During the period 1984 to 2003, there were 10,751 new cases of esophageal neoplasm diagnosed (8,637 males and 2,114 females). As shown in Table 1, the number of esophageal squamous cell carcinoma increased from 1921, in 1984 to 1998, to 2062, in 1999 to 2003. Instead the number of esophageal adenocarcinoma declined from 224, in 1984 to 1988, to 131, in 1998 to 2003. The trends were the same in both males and females.

WSRs of esophageal adenocarcinoma and squamous cell carcinoma in males, females, and overall were plotted in Figs. 1, 2, and 3, respectively. A progressive downward trend of WSR was seen in males from 16.38 of 100,000 in 1984 to 1988 to 8.99 of 100,000 in 1998 to 2003 for esophageal squamous cell carcinoma and from 1.72 of 100,000 in 1984 to 1988 to 0.55 of 100,000 in 1998 to 2003 for esophageal adenocarcinoma. There was a similar decline of WSR in females: from 3.20 of 100,000 in 1984 to 1988 to 1.65 of 100,000 in 1998 to 2003 for esophageal squamous cell carcinoma and from 0.56 of 100,000 in 1984 to 1988 to 0.14 of 100,000 in 1998 to 2003 for esophageal adenocarcinoma. The overall WSR declined from 9.45 of 100,000 in 1984 to 1988 to 5.27 of 100,000 in 1998 to 2003 for esophageal squamous cell carcinoma and from 1.10 of 100,000 in 1984 to 1988 to 0.34 of 100,000 in 1998 to 2003 for esophageal adenocarcinoma.

The declines of WSR were higher for esophageal adenocarcinoma than esophageal squamous cell carcinoma. This was evidenced from the decreasing ratio of esophageal adenocarcinoma versus esophageal squamous cell carcinoma from 11.7% in 1984 to 1988 to 6.4% in 1998 to 2003 (Fig. 4). This ratio was decreasing among both males and females.

Our study showed that both the incidence of esophageal adenocarcinoma and ratio of esophageal adenocarcinoma versus esophageal squamous cell carcinoma decreased in the period from 1984 to 2003 among Hong Kong Chinese. This scenario was different from those observed in Western Europe, United States, and Japan, wherein the incidence of esophageal adenocarcinoma was increasing (1-4). It was also different from the scenario in Taiwan and Korea, wherein the ratio of esophageal adenocarcinoma versus squamous cell carcinoma has not increased in the last two decades (7, 11).

As shown in Table 2, the ratio of esophageal adenocarcinoma in Hong Kong was much higher than the published data in other countries in East Asia. It was unlikely to be due to incorrect coding because reliable data from the Hong Kong Cancer Registry was used, which is a member of the International Association of Cancer Registries. Data with missing histology was higher in 1980s (22.5%), but progressively improved to only 4.7% in 2000s. Moreover, missing histology would bias the data toward underestimation of adenocarcinoma. Therefore, this higher reported ratio of esophageal adenocarcinoma in Hong Kong was likely genuine. However, it was much lower than that in the United States, wherein the incidence of esophageal adenocarcinoma had surpassed esophageal squamous cell carcinoma around 1990 (1).

The local prevalence of H. pylori infection is decreasing (10), whereas the prevalence of gastroesophageal reflux disease is getting more common (8). However, Barrett's esophagus was uncommon, and 94% of reflux esophagitis were either Los Angeles grade A or grade B esophagitis (12). There is no definite answer, but this situation might change if Westernization and increasing weight continues in the Hong Kong population. It was noted that increased occurrence of Barrett's esophagus, but not just increasing prevalence of gastroesophageal reflux disease, caused the increasing trend of esophageal adenocarcinoma (5, 6). Therefore, the increased prevalence of gastroesophageal reflux disease did not lead to an increase of esophageal adenocarcinoma locally, as the case in Western countries.

Population-based case-control study confirmed the important role of a diet in the carcinogenesis of esophageal adenocarcinoma (13). However, the association between dietary intake and esophageal adenocarcinoma was nonsignificant in cohort study in Europe (14, 15). A cohort study showed that overweight and obese subjects also had increased relative risks (1.40 and 3.96, respectively) of esophageal adenocarcinoma when compared with subjects with normal weight (16). This was further supported by a metaanalysis (17). Hong Kong population adopted a Westernized life-style early in the past century with decreased intake in vegetables, tomato, fruits, fish, and poultry, but increased consumption of processed meat, fat, beer, and liquor. In a telephone study in Hong Kong, only 15% to 21% of respondents consumed fruit at least twice a day, ∼50% consumed vegetable at least twice a day, and ∼40% ate high-fat food more than once weekly (18). The local prevalence of obesity was comparable with that of the United States recently (19). The percentage of central obesity doubled in men (from 12.2% to 26.7%), but remained stable in women in the past one decade (20). This direction of life-style changes might explain the higher local rate of esophageal adenocarcinoma than other East Asian countries, but did not support the decreasing incidence of esophageal adenocarcinoma in Hong Kong.

In conclusion, the incidence of esophageal adenocarcinoma and ratio of esophageal adenocarcinoma versus esophageal squamous cell carcinoma decreased among Hong Kong Chinese in spite of a decreasing prevalence of H. pylori infection, an increasing trend of gastroesophageal reflux disease, increasing prevalence of obesity, and unsatisfactory dietary habit. There are probably other changes in Hong Kong leading to the decline in esophageal adenocarcinoma locally.