© The Authors (2008). Published by Oxford University Press. All rights reserved
Alcohol Drinking and Gastric Cancer Risk: An Evaluation Based on a Systematic Review of Epidemiologic Evidence among the Japanese Population
1 Division of Epidemiology, Department of Public Health and Forensic Medicine, Tohoku University Graduate School of Medicine, Sendai, Japan
2 Epidemiology and Prevention Division, Research Center for Cancer Prevention and Screening, National Cancer Center, Tokyo, Japan
3 Department of Preventive Medicine/Biostatistics and Medical Decision Making, Nagoya University Graduate School of Medicine, Nagoya, Japan
4 Department of Epidemiology and Preventive Medicine, Gifu University Graduate School of Medicine, Gifu, Japan
5 Department of Epidemiology and International Health, Research Institute, International Medical Center of Japan, Tokyo, Japan
6 Department of Preventive Medicine, Saga Medical School, Faculty of Medicine, Saga University, Saga, Japan
For reprints and all correspondence: Taichi Shimazu, Epidemiology and Prevention Division, Research Center for Cancer Prevention and Screening, National Cancer Center, 5-1-1 Tsukiji, Chuo-ku, Tokyo 104-0045, Japan. E-mail: tshimazu{at}gan2.res.ncc.go.jp
Received August 6, 2007; accepted October 17, 2007
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Abstract |
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Background: We reviewed epidemiologic studies on the association between alcohol drinking and gastric cancer among the Japanese population. This report is one of a series of articles by our research group, which is evaluating the existing evidence concerning the association between health-related lifestyles and cancer.
Methods: Original data were collected by searches of MEDLINE using PubMed, or searches of the Ichushi database, complemented with manual searches. Evaluation of associations was based on the strength of evidence and the magnitude of association, together with biological plausibility as evaluated previously by the International Agency for Research on Cancer.
Results: Of the 11 cohort studies evaluated, nine showed no association between alcohol drinking and gastric cancer, and one study showed a strong positive association among men. All of 11 case–control studies found no association between alcohol drinking and gastric cancer. By anatomical subsites of gastric cancer, only three studies have evaluated the association between alcohol drinking and gastric cancer, and one cohort study found a positive association for cardia and upper-third gastric cancer in men. Few studies conducted among the Japanese population have made a detailed assessment of alcohol drinking, possible important confounding factors such as smoking and diet and anatomical subsites of gastric cancer.
Conclusion: We conclude that epidemiologic evidence for an association between alcohol drinking and gastric cancer risk remains insufficient due to the methodological quality of studies that have been conducted among the Japanese population.
Key Words: systematic review • epidemiology • alcohol drinking • gastric cancer • Japanese
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The most recent evaluation from the International Agency for Research on Cancer (IARC) concluded in 2007 that alcoholic beverages are carcinogenic to humans (Group 1) and are causally related to cancers of the oral cavity, pharynx, larynx, esophagus, liver, colorectum and female breast (1,2). However, epidemiologic studies on the association between alcoholic beverages and gastric cancer have been inconsistent and the interpretation of the findings is not clear (1–3).
As the majority of these reports were based on evidence from Western populations, their applicability to the Japanese population is unknown. The Japanese commonly consume different types of beverages from Western populations and have a relatively high prevalence of the variant allele of aldehyde dehydrogenase 2 (4), which is related to a high blood concentration of acetaldehyde (5). In addition to the factors related to alcohol, the prevalence of Helicobacter pylori infection (6) and the proportion of gastric cancers occurring in the distal stomach (7) are higher among the Japanese than among Western populations. Therefore, the magnitude of association among Japanese might differ from that among other populations.
The objective of the present study was to review epidemiologic studies on the association between alcohol drinking and gastric cancer among the Japanese population. The findings were summarized and the magnitude of the effect was evaluated. This report is one of a series of articles by our research group, which is investigating the associations between lifestyle factors and major types of cancer in Japan (8–15).
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Original data for this review were collected by searches of MEDLINE using PubMed complemented by manual searches of references from relevant articles when necessary. All epidemiologic studies on the association between alcohol drinking and gastric cancer incidence or mortality among Japanese from January 1966 to May 2007, including papers in press if available, were identified using the search terms ‘alcohol’, ‘drinking’, ‘gastric cancer’, ‘stomach cancer’, ‘cohort studies’, ‘case–control studies’, ‘Japan’ and ‘Japanese’ as key words found in the abstract. A search of the Ichushi (Japana Centra Revuo Medicina) database was also done to identify studies written in Japanese from 1983 to May 2007. Papers written in English or Japanese were reviewed, and only studies on Japanese populations living in Japan were included. The individual results were summarized in the tables separately by study design as cohort or case–control studies. In the case of multiple publications of analyses of the same or overlapping datasets, only data from the largest or the most recent studies were included, and incidence was also given priority in a single publication describing both incidence and mortality.
Evaluation was made based on the strength of evidence and the magnitude of association. Relative risks (RRs) or odds ratios (ORs) in each epidemiologic study were grouped by magnitude of association, giving consideration to statistical significance (SS) or not SS (NS), as strong, <0.5 or >2.0 (SS); moderate, either (i) <0.5 or >2.0 (NS), (ii) >1.5–2 (SS) or (iii) 0.5 to <0.67 (SS); weak, either (i) >1.5–2 (NS), (ii) 0.5 to <0.67 (NS) or (iii) 0.67–1.5 (SS); or no association, 0.67–1.5 (NS). After this process, the strength of evidence was evaluated in a similar manner to that used in the WHO/FAO Expert Consultation Report (16), where evidence was classified as ‘convincing’, ‘probable’, ‘possible’ and ‘insufficient’. In brief, the following criteria were used (8): convincing: evidence based on a substantial number of epidemiologic studies showing consistent associations between exposure and disease, with little or no evidence to the contrary, with a biologically plausible association. Probable: evidence based on epidemiologic studies showing fairly consistent associations, but with perceived shortcomings in the available evidence or some evidence to the contrary that precludes a more definite judgment. Possible: evidence based mainly on findings from case–control and cross-sectional studies, requiring more studies to support the tentative associations, which should also be biologically plausible. Insufficient: evidence based on findings of a few studies that are suggestive, but insufficient to establish an association, requiring more well-designed research to support the tentative associations. We assumed that biological plausibility corresponded to the judgment of the recent evaluation from the IARC (1,2,17). The final judgment is made based on the consensus of research group members and is not necessarily objective. In addition, when there was ‘convincing’ or ‘probable’ evidence of a positive or inverse association, we conducted a meta-analysis to obtain summary estimates of the association. Details of the evaluation methods are described elsewhere (8).
Main Features and Comments
We identified 11 cohort studies (18–28) and 11 case–control studies (29–39) (Tables 1 and 2, respectively). Among the cohort studies, three presented results by gender (20,21,26), six for men only (18,19,22,23,25,27) and two for men and women combined (24,28). The respective numbers for the case–control studies were three (32,38,39), three (29,30,36) and five (31,33–35,37).
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A summary of the magnitude of association for the cohort studies and case–control studies is shown in Tables 3 and 4, respectively. Of the 11 cohort studies evaluated, most showed no association between alcohol drinking and gastric cancer. Among these studies, nine showed no association (18,20,22–28), and the other two showed a strong positive (21) and a weak positive (19) association among men, respectively. All 11 case–control studies demonstrated no association between alcohol drinking and gastric cancer (29–39).
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By anatomical subsites, few studies had evaluated the association between alcohol drinking and gastric cancer, and the association was inconsistent (25,38,39), similar to studies among other populations (3). In one cohort study (25), alcohol drinking showed a moderate positive association with cardia and upper-third gastric cancer, but not with distal gastric cancer in men. One case–control study analysed the association with cardia, middle and antrum gastric cancer separately (38). The point estimate of the OR in male drinkers tended to be highest for cardia cancer and decreased towards the distal part of the stomach compared with never drinkers, although the results were not statistically significant. Another case–control study also presented the results by subsite, and drinking dose showed a stronger association with middle gastric cancer than with other subsites in men and women (39). Three studies reported no clear difference in risk pattern according to histologic subtype (intestinal and diffuse type) (25,32,39).
There were several methodological concerns in the Japanese studies reviewed here. First, assessment of drinking status was not detailed. Few studies assessed drinking status with validated questionnaires (25,27,28) in cohort studies. Therefore, it is necessary to consider the possible misclassification of drinking dose or frequency that would attenuate the association between alcohol drinking and gastric cancer risk. Moreover, early studies reviewed here did not differentiate between never and past drinkers. It is important to evaluate the risk of gastric cancer in past drinkers, because past drinkers could include those who gave up drinking due to ill health. Some recent studies have investigated the association with gastric cancer by distinguishing between past and never drinkers (24,26–28,34,35,38). Compared with never drinkers, two studies reported an increased risk of gastric cancer in past drinkers (24,38). In addition, the types of alcoholic beverages consumed among Japanese differ from those consumed by other populations, but this was considered in only two studies (22,31).
Second, few studies reported an adjusted risk of gastric cancer by important possible confounding factors. Although H. pylori is an established risk factor for gastric cancer (40), only one case–control study reported the OR adjusted for H. pylori infection (39). If alcohol drinking is related to H. pylori infection status, it could confound the association between alcohol drinking and gastric cancer. However, a cross-sectional study among Japanese men showed that alcohol drinking was not associated with H. pylori IgG antibody seropositivity (41). Thus, H. pylori infection status may not confound the association between alcohol drinking and gastric cancer risk. In fact, one case–control study presented the association between alcohol drinking and gastric cancer after adjustment for H. pylori infection and smoking status (39), and the magnitude of the association was similar to that in studies without adjustment for H. pylori infection status. Compared with never drinkers, the OR in the highest category of drinking dose (pure alcohol intake/day multiplied by years of drinking) was 1.40 (0.85–2.31) in men and 0.75 (0.43–1.30) in women. In the evaluation from the IARC, confounding by H. pylori infection was not considered as a major concern, because an association was seen in areas where the majority of the population had been infected by H. pylori (2).
Smoking is a potential confounder. Our previous review of Japanese studies regarding smoking and gastric cancer concluded that there is convincing evidence that tobacco smoking moderately increases the risk of gastric cancer (14). Since alcohol drinking is often related to smoking, confounding by smoking could elevate the risk of alcohol drinking. Of all the 22 studies reviewed, seven cohort studies (18,19,21–23,25,27) and three case–control studies (35,36,39) reported their results after adjustment for, or stratification by, smoking status.
Dietary factors are also potential confounders to be considered. Especially, it is important to consider salt intake, and fruit and vegetable consumption, which potentially increase and decrease gastric cancer risk (3), respectively. Two cohort studies reported their results after adjustment for consumption of fruit and vegetables (25,27), and one cohort study reported its results after adjustment for consumption of salty foods (25).
Third, misclassification of cardia cancer could occur because, until recently in Japan, the upper third of the stomach was called the cardia based on the guidelines for gastric cancer classification (42). This misclassification might have attenuated any positive association between alcohol drinking and cardia cancer if there is a causal relationship between alcohol drinking and cardia cancer, as suggested by several case–control studies among Western populations (3).
In experimental animals, the IARC evaluated the carcinogenic effect of ethanol on various sites including the forestomach, and concluded that there is sufficient evidence of carcinogenicity (1,2). However, epidemiologic findings on the association between alcohol drinking and gastric cancer among the Japanese population are inconclusive due to the quality of the methodology employed. Further, well designed epidemiologic studies are needed to provide a more detailed assessment of alcohol drinking, possible important confounding factors and anatomical subsites of gastric cancer.
Evaluation of Evidence on Alcohol Drinking and Gastric Cancer Risk in Japanese
From these results, and on the basis of assumed biological plausibility, we conclude that there is insufficient evidence that alcohol drinking increases the risk of gastric cancer in the Japanese population.
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Third Term Comprehensive 10-year Strategy for Cancer Control from the Ministry of Health, Labour and Welfare, Japan.
Conflict of interest statement None declared.
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Research group members: Shoichiro Tsugane (principal investigator), Manami Inoue, Shizuka Sasazuki, Motoki Iwasaki, Tetsuya Otani (until 2006), Norie Kurahashi (since 2007), Taichi Shimazu (since 2007) (National Cancer Center, Tokyo); Ichiro Tsuji (since 2004), Yoshitaka Tsubono (in 2003) (Tohoku University, Sendai); Yoshikazu Nishino (Miyagi Cancer Research Institute, Natori, Miyagi); Kenji Wakai (Nagoya University, Nagoya); Keitaro Matsuo (since 2006) (Aichi Cancer Center, Nagoya); Chisato Nagata (Gifu University, Gifu); Tetsuya Mizoue (International Medical Center of Japan, Tokyo); Keitaro Tanaka (Saga University, Saga).
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