Dietary Patterns and Colorectal Adenomas in Japanese Men

The Self-Defense Forces Health Study

Tetsuya Mizoue1 , Taiki Yamaji1, Shinji Tabata1,2, Keizo Yamaguchi1,3, Eiichi Shimizu3, Masamichi Mineshita3, Shinsaku Ogawa2 and Suminori Kono1

1 Department of Preventive Medicine, Faculty of Medical Sciences, Kyushu University, Higashiku, Fukuoka, Japan.
2 Self-Defense Forces Fukuoka Hospital, Fukuoka, Japan.
3 Self-Defense Forces Kumamoto Hospital, Kumamoto, Japan.

Received for publication July 7, 2004; accepted for publication September 10, 2004.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The role of dietary patterns in colorectal carcinogenesis remains unclear in Asian populations. Using 1999–2002 data, the authors investigated the association between dietary patterns and colorectal adenomas in 1,341 Japanese men who underwent total colonoscopy. Information about diet was obtained using a 74-item food frequency questionnaire prior to the colonoscopy. Three dietary patterns were generated by factor analysis: 1) a high-dairy, high-fruit and -vegetable, high-starch, low-alcohol pattern; 2) an "animal food" pattern; and 3) a Japanese pattern. Logistic regression analysis was used to estimate the odds ratio of having colorectal adenomas with the adjustment for potential confounding variables including body mass index, smoking, alcohol, and leisure-time physical activities. A significant inverse association was found for the high-dairy, high-fruit and -vegetable, high-starch, low-alcohol pattern; the odds ratios for the second, third, and fourth quartiles were 0.97 (95% confidence interval: 0.70, 1.36), 0.71 (95% confidence interval: 0.50, 1.01), and 0.62 (95% confidence interval: 0.43, 0.90), respectively, compared with the lowest (ptrend = 0.003). Similar associations were observed for larger adenomas or for each subsite of the colorectum. The Japanese and "animal food" patterns were not clearly associated with colorectal adenomas. A dietary pattern including greater consumption of dairy products and fruits and vegetables with low alcohol consumption may be associated with decreased risk of colorectal adenomas.

adenoma; cross-sectional studies; diet


Abbreviations: DFSA, high-dairy, high-fruit and -vegetable, high-starch, low-alcohol (dietary pattern).


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Colorectal cancer is a major cause of cancer deaths in developed countries. Geographic and time-trend analyses, as well as migrant studies, strongly suggest that environmental factors, especially diet, play an important role in the pathogenesis of colorectal cancer (13). However, analytical epidemiologic studies have yielded conflicting findings; for example, a body of evidence suggesting a protective role of vegetables or dietary fiber (4) has been either challenged (58) or supported (9, 10) by recent large-scale studies. In Japan, colorectal cancer mortality has markedly increased over the last several decades (11) and is now among the highest levels in the world (12). Time-trend analysis has suggested that decreased consumption of dietary fibers (13) or grains (14) may account for the increase in mortality. Yet it is largely unknown which lifestyle changes associated with Westernization or modernization have contributed to the rapid increase of colorectal cancer in Japan, or whether the traditional Japanese diet protects against this type of cancer.

Analysis of dietary patterns has recently drawn a great deal of attention as a method of investigating the role of foods or nutrients in studies of chronic diseases. Approaches of this sort, dealing with a combination of several foods, can overcome problems arising from close intercorrelation and potential effect modifications among numerous foods or nutrients (15). Factor-analysis studies of Western populations have suggested that a certain dietary pattern may be predictive of colorectal cancer risk (1618). Dietary patterns generated by factor analysis, however, are sample specific and may not be applicable to populations having different dietary cultures. While having adopted a Western-style diet, many Japanese still consume large amounts of traditional foods, including rice, fish, and soybean products (19). Thus, dietary patterns among Japanese may differ considerably from those among Western populations.

The aim of the present study was therefore to investigate dietary patterns in relation to the risk of colorectal adenoma, a precursor of colorectal cancer (20, 21), using data from preretirement check-ups among male Self-Defense Forces officials in Japan.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Study setting
The data used were derived from the Self-Defense Forces Health Study, a cross-sectional survey of male Self-Defense Forces officials who participated in a preretirement health examination at two hospitals (Fukuoka and Kumamoto) in Japan. The study procedure has been described elsewhere (22, 23). In short, all officials undergo a comprehensive health examination before retirement; total colonoscopy is included as a routine procedure. Study questionnaires about health-related lifestyles were distributed prior to colonoscopy to male examinees on the first day of hospital admission for examination. Research assistants checked the questionnaire for unanswered questions and apparently inconsistent answers and, if necessary, sought clarification from the study subjects.

Results of laboratory tests and colonoscopic findings, including histologies for polyp, were extracted from clinical reports. Written informed consent was obtained from study participants. The study protocol has been approved by the ethics committee of Kyushu University.

Study subjects
The present study used data from April 1999 through March 2002. Among 2,390 male Self-Defense Forces officials who underwent the examination, 2,370 (99 percent) agreed to participate in the present study. After excluding men with histories of cancer, stroke, myocardial infarction, coronary revascularization, inflammatory bowel diseases, colorectal surgery, or diabetes mellitus, we kept 2,141 men in the analysis of dietary patterns. Of these, we excluded men who did not receive colonoscopy (n = 57), who underwent partial or unsuccessful colonoscopy (n = 177), or who had colorectal polyp removal prior to the examination (n = 148). Of the remaining 1,759 subjects who completed total colonoscopy, 764 men were identified as having colorectal polyps including hyperplastic nodules. Of these, 476 men had their polyps histologically confirmed: cancer (n = 1), carcinoid (n = 1), adenoma (n = 346), and other histologies (n = 128). Only 29 men had adenomas of 10 mm or larger, and nine had tubulovillous or villous adenomas. The data for the 346 men who had adenoma (case group) and 995 men who were free from any colorectal polyp and cancer (referent group) were analyzed to assess the association between dietary patterns and colorectal adenomas.

Dietary assessment
Information about diet was collected using a food frequency questionnaire designed to assess the average intakes of 74 food items, food groups, and food preparations over the previous year. The questionnaire was an expanded version of a 45-item food frequency questionnaire that was developed on the basis of a published questionnaire (24) and was validated against the 28-day dietary record (25). The expansion of food items was done with reference to food consumption in the National Nutrition Survey (19) and a dietary questionnaire developed elsewhere in Japan (26). Participants were asked to choose from seven response options for most dietary items, ranging from "never/less than one per month" to "two to three times per day." Different response schemes were used for green tea, coffee, and rice (five options) and for alcoholic beverages (six options). Daily consumers of green tea, coffee, or rice were asked about the number of cups or bowls consumed per day. Current drinkers, defined as those who have consumed alcoholic beverages weekly for at least 1 year in their lifetime and who were drinking at the time of the survey, were asked about the frequency of consumption and the amount of consumption per occasion of five alcoholic beverages, that is, sake (a Japanese wine), shochu (a Japanese distilled beverage), beer, whiskey, and wine. The amount of consumption per occasion was used in the estimation of total ethanol intake from these alcoholic beverages, but only the frequency of consumption for each alcoholic beverage was used in the analysis of dietary patterns.

Grouping of food factors
Before the analysis of dietary patterns, intakes of green tea, coffee, or rice were converted into units of cups or bowls per day, while those of other dietary items were quantified in terms of frequency per week. Five dietary questions that overlapped with or were duplicated by others (collective consumption of cooked vegetables, apples, mandarin oranges, other oranges, watermelons) and three questions about food spreads (butter, margarine, and jam/honey) were not used. Furthermore, some foods or food groups similar in nutritional content or culinary use were combined, leaving 39 food items for the purposes of the present study.

Statistical analysis
Dietary patterns were generated by factor analysis (principal components) using SAS PROC FACTOR statistical software (27). Factor analysis is a technique to reduce a number of variables into fewer independent factors. To make interpretation easier, a linear transformation called a "rotation" is normally performed on the initial factor solution. We used an orthogonal rotation procedure (varimax rotation), which maintains the uncorrelated nature of the factors and tries to get the original variables to load high on one of the factors and low on the rest. When factor scores are used as independent variables in a subsequent regression analysis, this procedure has the advantage over oblique rotation that the analysis is less subject to problems of collinearity. In determining the number of factors to retain, we consider eigenvalue, the scree test, and interpretability. Eleven factors satisfied the criteria for eigenvalues greater than one, and the scree plot showed small breaks in the eigenvalues after factor 5, suggesting three or four factors to retain. Postrotated factor loadings revealed that three factors well describe distinctive dietary patterns of the study population.

We thus retained the three dietary patterns and designated them as 1) a high-dairy, high-fruit and -vegetable, high-starch, low-alcohol (DFSA) pattern; 2) an "animal food" pattern; and 3) a Japanese pattern, according to the food items showing high loading (absolute value) with respect to each dietary pattern. We confirmed that these three dietary factors emerged when all 74 food items in our questionnaire were simply included in factor analysis. A factor score for each dietary pattern was calculated by weighting consumption of each food item by the corresponding factor loading and summing the resulting values. This score ranks individuals in terms of how closely they conform to the dietary pattern.

The potential confounding variables considered were hospital (Fukuoka or Kumamoto), age (treated as a continuous variable), parental history of colorectal cancer (absent or present), occupational rank (three categories), body mass index (<22, 22–23.9, 24–25.9, and ≥26 kg/m2), smoking (lifetime nonsmoker, former smoker, and current smoker using <15, 15–24, or ≥25 cigarettes/day), and leisure-time physical activity, expressed as the sum of metabolic equivalents for each activity multiplied by the corresponding hours of such activity per week (none, <20, 20–39.9, and ≥40 metabolic equivalent-hours). Quartiles of factor scores of each dietary pattern among controls were used for cutoff values. Multiple logistic regression that included terms for the above-mentioned variables was performed to estimate the odds ratio and 95 percent confidence interval of colorectal adenomas according to quartiles of scores for each dietary pattern, taking the lowest quartile group as the referent group. Analyses were repeated for adenomas of 5 mm or larger (n = 140) or according to the location of the lesion (proximal colon including the cecum, ascending colon, liver flexure, transverse colon, and splenic flexure; distal colon including the descending colon and sigmoid colon; and the rectum). Logistic regression analysis was performed using SAS PROC LOGISTIC software (27).


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Table 1 shows factor loadings, which are equivalent to simple correlations between the food items and the dietary patterns. A positive loading indicates that the food item is positively associated with the dietary pattern, and a negative loading indicates an inverse association with the dietary pattern. The DFSA dietary pattern was characterized by frequent intake of fermented dairy products, milk, confectionaries, bread, fruits, and vegetables and infrequent intake of shochu, a local alcoholic beverage in the study areas. The "animal food" dietary pattern was characterized by various kinds of animal foods, including red meat, poultry, seafood excluding fish, processed meat and fish products, and fried or broiled foods. The Japanese dietary pattern was characterized by traditional foods in Japan (soybean products, seaweed, pickles, and green tea), vegetables, and fish. The proportion of the total variance explained by the three factors was 24 percent.


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TABLE 1. Factor-loading matrix for dietary patterns, Self-Defense Forces Health Study, Japan, 1999–2002*
 
Table 2 shows the association of dietary patterns with potential confounding variables and alcohol consumption among men free from colorectal polyp or cancer (referent group). Examinees at the Kumamoto hospital had a higher score for the Japanese dietary pattern but lower scores for the DFSA and "animal food" dietary patterns than those at the Fukuoka hospital. This reflects the geographic characteristics of dietary patterns; the southern parts of Kyushu Island, including Kumamoto, are less urbanized than the northern parts, including Fukuoka. Men with a high score for the DFSA dietary pattern tended to have higher occupational positions and consumed smaller amounts of alcohol. Men with high scores for the "animal food" dietary pattern tended to consume greater amounts of alcohol. Men in the upper quartiles of the Japanese dietary pattern tended to be nonsmokers and engaged in higher levels of leisure-time physical activity, and they consumed greater amounts of alcohol.


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TABLE 2. Dietary patterns in relation to potential confounding variables and alcohol intake among referents, Self-Defense Forces Health Study, Japan, 1999–2002
 
As shown in table 3, the DFSA dietary pattern was inversely associated with the risk of colorectal adenomas, showing a 40 percent reduced odds ratio among men in the highest quartile of the dietary pattern compared with those in the lowest. This association was slightly more evident for adenomas with a diameter of 5 mm or larger. No apparent association was observed for either the "animal food" dietary pattern or the Japanese dietary pattern.


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TABLE 3. Logistic regression results for the association between dietary patterns and colorectal adenoma, Self-Defense Forces Health Study, Japan, 1999–2002
 
The DFSA dietary pattern was inversely associated with adenomas at all subsites of the colorectum (table 4). The association was slightly stronger for the proximal colon in terms of the odds ratio of 0.5 for the highest quartile of the dietary pattern score and test for the trend association (ptrend = 0.003), but the confidence intervals of odds ratios for this site overlapped substantially with those for other sites. The Japanese and "animal food" dietary patterns were not measurably associated with colon adenomas. However, a nonsignificant positive association with rectal adenomas was observed for the Japanese pattern, while a nonsignificant inverse association was found for the "animal food" pattern. The odds ratios for the upper three quartiles combined compared with the lowest were 1.64 (95 percent confidence interval: 0.83, 3.25) and 0.64 (95 percent confidence interval: 0.36, 1.13) for the Japanese pattern and "animal food" pattern, respectively.


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TABLE 4. Logistic regression results for the association between dietary patterns and colorectal adenoma according to the location of the lesion, Self-Defense Forces Health Study, Japan, 1999–2002
 

    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
We investigated the association between major dietary patterns and colorectal adenomas among middle-aged Japanese men. Of the three dietary patterns we identified, the DFSA dietary pattern showed a significant, inverse association with the risk of colorectal adenomas.

Strengths and limitations
Our study had several strengths. Selection bias in terms of study participation was unlikely because of nonselective recruitment for the preretirement health examination, which included total colonoscopy as a routine procedure, and high study participation rate. The questionnaire was distributed and collected prior to colonoscopy, and thus recall bias associated with adenoma status was also unlikely. The control series consisted of only subjects who were confirmed via total colonoscopy to be free from any colorectal polyp and cancer, leading to a more valid assessment compared with studies based on partial colonoscopy. We controlled for major known or suspected confounding factors. The uniform background of the study subjects in terms of occupation, sex, and age was also advantageous in maintaining comparability between cases and controls, although this uniformity limits the extent to which we may generalize from the present findings.

The present study also features some limitations. For one, the dietary questionnaire has not been validated. However, the former version, including questions and response options similar to those of the present questionnaire, has been validated against 7-day, year-round dietary records (25). Most nutrients and foods demonstrated fairly good correlation between the dietary record and questionnaire; relatively high correlation coefficients of 0.80, 0.77, 0.58, and 0.58 were observed for bread, fruits, dairy products, and pickled vegetables, respectively. Nondifferential misclassification in our dietary assessment could distort risk estimates toward the null. Such a bias may be minimal for the analysis of the DFSA dietary pattern, composed of food items showing good correlation between the dietary record and questionnaire, but this bias could be the reason for the lack of an apparent association with the "animal food" or Japanese dietary pattern.

Limitations of factor analysis arise from the arbitrary decisions (15) involved in selecting and grouping foods for analysis from the questionnaire, in determining the number of factors to retain, in choosing the method of rotation of the initial factors to increase the interpretability of the dietary pattern, and in labeling dietary patterns according to their factor loadings. Masaki et al. (28) identified four major dietary patterns using baseline data of a cohort of male employees in Tokyo. Similar to our study, their study identified a "Western breakfast" dietary pattern and an "animal" dietary pattern, suggesting the existence of dietary patterns common to the Japanese. Our derived dietary patterns accounted for 24 percent of the total variance, which is comparable with a figure observed in a previous study (17) but less than that reported in a Japanese study (28). Caution needs to be exercised when comparing the variance explained across studies, which is determined by various factors including the number of variables in analysis.

Interpretation of findings
A dietary pattern characterized by frequent intakes of dairy products, confectionaries, and fruits and vegetables, as well as by infrequent consumption of shochu, a local alcoholic beverage, was inversely associated with the risk of colorectal adenomas. This dietary pattern seems to consist of relatively healthy selections of foods found in Western countries and includes foods of probably low consumption in Japan. According to the food balance sheet (29), per capita supplies of dairy products in Japan and among developed countries in the year 2001 were 66 kg (181 g/day) and 197 kg (540 g/day), respectively; the corresponding values for fruits were 53 kg (145 g/day) and 83 kg (227 g/day). Although the associations between these foods and colorectal cancer have been inconsistent, the present results are in agreement with the existing body of evidence, including findings from recent studies, indicating that high consumption of dairy products or calcium (3034) and high consumption of fruits, fruit juices, or fruit fiber (10, 3538) are each associated with reduced risk of colorectal cancer or adenoma. A positive association of alcohol consumption and colorectal adenomas or cancer has been reported in many studies, including those in Japan (23, 39). In addition to independent effects, there may be complex interactions among food factors constituting the DFSA dietary pattern. For example, fruit juices may enhance calcium absorption (40), and reduced alcohol intake increases the bioavailability of folate (41). The glycemic effects of a high-starch or a high-sugar diet and their contribution to increased risk of colorectal cancer have been suspected, but epidemiologic findings are inconsistent on this point (42, 43). Our finding of an inverse association between the DFSA dietary pattern and colorectal adenomas provides the following suggestions: that a high-starch diet may inhibit, rather than promote, the formation of colorectal adenomas and that the adverse effects of a high-starch diet, if any, may not be so strong as to negate the protective effects of other foods contributing to this dietary pattern on adenoma risk. The inverse association of this dietary pattern with adenoma risk was somewhat stronger for the proximal colon than for other sites. Random error could be an explanation. Alternatively, the dietary pattern may be more closely involved in the formation of adenomas in the proximal colon.

The Japanese dietary pattern was characterized by high consumption of many plant foods, including traditional Japanese foods (soybean products, seaweed, pickles) and vegetables. A diet rich in various plant foods could potentially reduce cancer risk because of their many biologically active chemicals (44). However, the Japanese dietary pattern was not apparently associated with colonic adenomas. In studies of Western populations, inverse associations between similar dietary patterns (designated "prudent" or "healthy" patterns) and colorectal cancer have been unclear (18) or limited to subgroups (17). The lack of such an association in our study may contradict a body of evidence supporting an inverse association between vegetables and colorectal cancer (4) but agree with results of recent prospective, but not all (10, 37), studies reporting no association between vegetables or fiber and colorectal cancer or adenoma (58). As most of the adenomas in the present study were small in size and less malignant in nature, the present finding is in line with a hypothesis that vegetables are inversely associated with the progression of colorectal adenomas to cancer but not with the initial appearance of adenomas (38). We found a nonsignificant positive association between the Japanese dietary pattern and the risk of rectal adenomas. Studies in Japan (4549) have consistently shown that frequent consumption of preserved foods including pickled vegetables and dried/salted fish, typical of the Japanese diet, is associated with increased risk of colorectal cancer; of these studies, three documented a significant association specifically for the rectum (4648). These preserved foods contain N-nitroso compounds (50), which are potent carcinogens (51). Among other foods characterizing the Japanese pattern, broiled fish is a potential source of exposure to carcinogenic heterocyclic amine (52), although we are not aware of any epidemiologic findings suggesting a relation between broiled fish and colorectal cancer risk.

Meat, especially red meat, processed meat, or meat broiled at high temperature, has been associated with colorectal cancer (53, 54) or adenoma (55). A study in Japan found a significant positive association between intake of animal protein and the risk of colorectal adenoma (56). However, we find no increase in the risk of colorectal adenomas associated with the "animal food" dietary pattern. Besides possible bias due to misclassification in the dietary assessment (as discussed above), the lack of such an association for colon adenomas in our study may be attributable to the moderate consumption of meat in Japan (mean daily intake of total meat: 96 g for men aged 40–49 years (19)). In addition, poultry has contributed to the healthy or prudent dietary patterns in Western populations (1618). The diversity of animal food sources may dilute the potential carcinogenic effects of a specific animal food. Furthermore, it is possible that moderate intake of animal foods prevents carcinogenesis because these foods provide nutrients such as methionine and folate, which are beneficial in DNA synthesis and DNA methylation (57). In this context, our finding showing an increased risk of rectal adenomas associated with the lowest quartile of the "animal food" pattern may be of note and is consistent with results of certain studies relating to colorectal cancer in Japan (45, 48, 58).

In conclusion, the present results indicate that a dietary pattern characterized by frequent consumption of dairy products, confectionaries, bread, fruits, and vegetables but low intake of local alcoholic beverages is associated with a reduced risk of colorectal adenomas in Japanese men. Nonsignificant associations for rectal adenomas, based on an analysis including only 63 men with adenomas in the rectum, should set a limit to causal inference. However, since the incidence of rectal cancer in Japan has been high among industrial countries (12), the question as to whether a Japanese-style diet or a diet low in animal foods promotes carcinogenesis of the rectum warrants further investigation.


    ACKNOWLEDGMENTS
 
This work was supported by a grant-in-aid for scientific research on priority areas (12218226) from the Ministry of Education, Culture, Sports, Science, and Technology, Japan, and by a Health and Labor Sciences research grant for research on cancer prevention and health services research from the Ministry of Health, Labor, and Welfare, Japan.

The authors thank the ward nurses of Self-Defense Forces Fukuoka and Kumamoto hospitals for their assistance in conducting the study.


    NOTES
 
Reprint requests to Dr. Tetsuya Mizoue, Department of Preventive Medicine, Faculty of Medical Sciences, Kyushu University, 3-1-1, Maidashi, Higashiku, Fukuoka 812-8582, Japan (e-mail: mizoue{at}phealth.med.kyushu-u.ac.jp). Back


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 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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