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4 Department of Nutrition, Food Studies, and Public Health, New York University, New York City, NY 10012; 5 Division of Cancer Prevention and Population Sciences, National Cancer Institute, Bethesda, MD 20892; 6 Division of Public Health Sciences, Cancer Prevention Program, Fred Hutchinson Cancer Research Center and Department of Epidemiology, University of Washington, Seattle, WA 98109; 7 University of Pittsburgh Medical Center, Pittsburgh, PA 15232; 8 MD Anderson Cancer Center, Houston, TX 77030; 9 Information Management Systems, Inc., Silver Spring, MD 20904; and 10 Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD 20892
* To whom correspondence should be addressed. E-mail: beth.dixon{at}nyu.edu.
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ABSTRACT |
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 TOP ABSTRACT IntroductionMethodsResultsDiscussionLITERATURE CITED |
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5 vs. 
2 = 0.74, 95% CI = 0.64–0.85; P-trend < 0.001). Comparable results were found for men who had intakes most similar to the DASH Eating Plan or a Mediterranean dietary pattern. Women who most complied with the USDA Food Guide recommendations had an 18% reduced risk for colorectal adenoma, but subgroup analyses revealed protective associations only for current smokers (OR USDA score 5 vs. 2 = 0.52, 95% CI = 0.31–0.89; P-trend < 0.01) or normal-weight women (OR USDA score 5 vs. 2 = 0.74, 95% CI = 0.55–0.99; P-trend = 0.08). Following the current U.S. dietary recommendations or a Mediterranean dietary pattern is associated with reduced risk of colorectal adenoma, especially in men.
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Introduction |
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Although intervention studies like the Polyp Prevention Trial did not reduce recurrence of colorectal adenoma, actual adherence to the multiple dietary goals (low fat, high dietary fiber, and high fruit and vegetable intake) was limited to a small sample of subjects (12,13). Results from observational studies of dietary patterns and colorectal cancer have been more consistent, but most of these studies use data-driven methods (e.g. factor analysis and cluster analysis) that are not intended for evaluation of formal dietary guidelines (14). The creation of dietary scores is a common, intuitively simple way to assess adherence to recommended eating patterns in relation to health outcomes (15). The objective of this study was to determine whether dietary scores that assess adherence to the USDA Food Guide recommendations, the DASH Eating Plan, and a Mediterranean dietary pattern are associated with reduced risk of distal colorectal adenoma, a precursor of colorectal cancer, in a large sample of U.S. men and women.
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Methods |
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Study participants.
Successful sigmoidoscopy examinations (defined as insertion to at least 50 cm with >90% of mucosa visible or suspect lesion found) were carried out for 56,176 men and women aged 55–74 y in the screening arm of the trial. Of these participants, 51,028 (91%) completed a FFQ and other risk factor questionnaires at study entry. We excluded participants for 1 or more of the following reasons: missing data for more than 7 items on the FFQ (n = 451); extreme values for energy intake defined as lowest and highest 1% of gender-specific energy intake (n = 947); previous history of cancer, except basal-cell skin cancer (n = 2329); and self-reported history of ulcerative colitis, Crohn's disease, familial polyposis, colorectal polyps, or Gardner's syndrome (n = 4614). Adenoma was defined as advanced if the polyps were large (1 cm), had high-grade dysplasia (including cancer in situ), or had villous elements (including tubulo-villous adenomas). We also excluded participants if they had hyperplastic polyps only (n = 1501), benign lesions not further specified (n = 108), colorectal lesions (polyps or cancer) of unknown location (n = 279), polyps of uncertain histology or cancer (n = 1,513), histology data pending at the time of analysis (n = 83), or were under medical follow-up but did not have additional endoscopy after a positive screening (n = 2565).
After all exclusions, this study included 3592 cases with pathologically verified left-sided adenomatous polyps of the distal colon (descending colon, sigmoid colon, or rectum) and 33,971 controls with no suspicion of neoplasia at this site on either sigmoidoscopic screening exam (n = 32,415) or from a follow-up endoscopy after a suspect screen (n = 1556). Data for this analysis were updated through September 2002.
Creation of dietary scores. We assessed usual dietary intake over the 12 mo prior to enrollment using a 137-item FFQ that included 77 items with usual portion size, 10 questions about meat cooking practices, and 14 questions about vitamin/mineral supplement use. This FFQ was modeled after 3 well-established and validated questionnaires: the National Cancer Institute's Diet History Questionnaire (18), the Block FFQ (19), and the Willett FFQ (20). Values for daily intake of energy, nutrients (e.g. macronutrients, vitamins, minerals, and types of fatty acids), added sugars, drinks of alcohol, and servings from 27 food groups (e.g. grains, vegetables, fruits, dairy, meat and meat equivalents, and subgroups within the 5 main food groups) were determined from national dietary data and the Pyramid food group servings database from the 1994–96 Continuing Survey of Food Intakes by Individuals using the method developed by Subar et al. (21). This method disaggregates food mixtures (e.g. pizza) into their component ingredients or foods (e.g. pizza dough, tomato sauce, and cheese) before assigning items to their respective discrete food groups (e.g. grains, vegetables, and dairy).
We created an 8-point USDA score to reflect adherence to the USDA Food Guide recommendations included in the appendix of the 2005 Dietary Guidelines for Americans (7). Suggested amounts of foods for this eating pattern vary across a range of energy intakes12 (1000–3200 kcal/d) to meet the needs of different age and gender groups in the U.S. population. We used recommendations from the 2000 kcal/d eating plan for men and from the 1600 kcal/d eating plan for women that are appropriate for men and women who are 51 y and have lifestyles that include mostly light physical activity associated with typical daily life (characteristics of the PLCO study population). For their USDA scores, men and women received 1 point if the minimum recommended number of daily servings from each of the 5 main USDA food groups was met according to the sex-specific eating plans (i.e. for men at 2000 kcal/d: 6 servings13/d of grains, 3 servings/d of dairy products, 4 servings/d of fruits, 5 servings/d of vegetables, 5.5 oz14/d of meat and meat equivalents; for women at 1600 kcal/d: 5 servings/d of grains, 3 servings/d of dairy products, 3 servings/d of fruits, 4 servings/d of vegetables, 5 oz/d of meat and meat equivalents). Men and women also received 1 point if their average daily consumption of saturated fat was less than the recommended 10% of total energy intake, if their added sugar intake was 7% of total energy intake, and if their alcohol intake was 2 drinks15/d for men and 1 drink/d for women. We included these 3 components because the 2005 Dietary Guidelines for Americans state that "the discretionary calorie allowance covers all calories from added sugars, alcohol, and the additional fat found in even moderate fat choices from the milk and meat group," which is primarily saturated fat. The USDA Food Guide also includes a separate recommendation for intake of oils in grams, which are primarily polyunsaturated and MFA. We did not include this recommendation as a separate component in the USDA score because the USDA servings database used with the PLCO FFQ did not separate gram amounts from oils and gram amounts from solid fat.
We used similar methods to create a 9-point DASH score to reflect adherence to the DASH Eating Plan included in the appendix of the 2005 Dietary Guidelines for Americans (7). The DASH Eating Plan states that "whole grains are recommended for most servings to meet fiber recommendations." We considered intake of 67% of grains as whole grains as "most servings." Accordingly, men and women received 1 point if they consumed the minimum recommended number of daily servings from each of the 6 main food groups according to their sex-specific eating plan [i.e. for men at 2000 kcal/d: 4.7 (67% x 7) servings/d of whole grains, 4 servings/d of vegetables, 4 servings/d of fruits, 2 servings/d of dairy products, <6 oz/d of meat and meat equivalents, and 4 servings/d of nuts, seeds, and legumes; for women at 1600 kcal/d: 4 (67% x 6) servings/d of grains, 3 servings/d of vegetables, 4 servings/d of fruits, 2 servings/d of dairy products, <6 oz/d of meat and meat equivalents, 3 servings/d of nuts, seeds, and legumes]. Men and women also received 1 point if their average daily consumption of saturated fat was less than the recommended 5% of total energy intake, if their added sugar intake was 3% of total energy intake, and if their alcohol intake was at or below the recommended 2 drinks/d for men and 1 drink/d for women. We used a cut-point of 5% for saturated fat intake based on estimates generated from a 1-wk menu of the DASH Eating Plan provided in the 2005 Dietary Guidelines for Americans. To be consistent with the USDA score, we used the average recommended contribution of added sugars to total energy intake (i.e. 3%) for the different energy levels of DASH Eating Plans as the cut-point for both men and women.
For comparison, we created a dietary score representing a Mediterranean dietary pattern based on the methodology of Trichopoulou et al. (11). The MED score has a maximum of 9 points, counting 1 point if: daily servings of vegetables, legumes, fruits and nuts, cereals, and fish, and the ratio of grams of MFA to grams of SFA were equal to or greater than the sex-specific median intake of the study population; daily servings of meat (including red meat, poultry, organ meats, and processed meats) and dairy foods were less than the sex-specific median intake of the study population; and alcohol intake was 10–50 g/d for men and 5–25 g/d for women. In our study population, the respective cut-points for men were: 4.86 servings/d of vegetables, 0.17 servings/d of legumes, 3.15 servings/d of fruits and nuts, 6.37 servings/d of cereals, 0.51 oz/d of fish, 1.14 MFA:SFA ratio, <3.23 oz/d of meat, and <1.58 servings/d of dairy. The respective cut-points for women were: 4.39 servings/d of vegetables, 0.11 servings/d of legumes, 3.33 servings/d of fruits and nuts, 4.98 servings/d of cereals, 0.45 oz/d of fish, 1.10 MFA:SFA ratio, <2.09 oz/d of meat, and <1.42 servings/d of dairy.
Statistical analysis.
To determine prevalence OR of colorectal adenoma, we created logistic regression models with the USDA, DASH, and MED dietary scores entered as continuous or categorical variables. USDA and DASH score categories of 2, 3, 4, and 5 and MED score categories of 2, 3, 4, 5, and 6 were selected due to lower numbers of cases in the extreme categories. Outcome variables included all colorectal adenoma, colon adenoma, rectal adenoma, nonadvanced adenoma, and advanced adenoma. Because our findings differed by sex, we conducted separate models for men and for women. All models were adjusted for screening center, age at randomization into the trial, and daily energy intake. For men, all models were also adjusted for ethnic origin (American Indian/Alaskan Native, Asian, Hispanic, non-Hispanic black, non-Hispanic white, or Pacific Islander), educational attainment (<12 y of school, 12 y of school/high school equivalent, some college, college graduate, or postgraduate), BMI in kg/m2, physical activity (none, <1, 1, 2, 3, 4+ h/wk of vigorous activity), smoking (never, quit smoking 20 y ago and smoked 1 pack/d, quit smoking 20 y ago and smoked >1 pack/d, quit smoking <20 y ago and smoked 1 pack/d, quit smoking <20 y ago and smoked >1 pack/d, ever smoked cigar or pipe, currently smokes cigarettes), use of aspirin and ibuprofen separately (no regular use, <2, 2–3, 4, 8, 12–16, 30, 60 times per month), and calcium intake from dietary supplements (in milligrams per day). For women, all models were adjusted for BMI, smoking, calcium intake from dietary supplements, and use of hormone replacement therapy (never, former, or current). These covariates were selected based on the literature and because they were significant (P < 0.05) in most models for all colorectal adenoma for each sex. The test for trend was determined using the median value of each category of each score included in each model.
We conducted stratified analyses for smoking status (never, former, or current) and BMI (<25 kg/m2 for normal weight vs. 25–29.9 kg/m2 for overweight vs. 30 kg/m2 for obese), because the interaction terms with smoking status or BMI category and each dietary score in the fully adjusted models for all colorectal adenoma had P-values <0.1. We also created multivariate models to determine whether individual components of the USDA, DASH, and MED dietary scores were independently associated with the colorectal adenoma outcomes.
All analyses were conducted using SAS version 9.1 (SAS Institute). Significance was determined by a 2-sided P-value <0.05.
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Results |
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5) was greater for women, participants from ethnicities other than non-Hispanic white or black, and participants who had years of education beyond high school, exercised more frequently, never smoked, and took aspirin, ibuprofen, or a multivitamin regularly (Supplemental Table 1). Adherence to the DASH Eating Plan (DASH score 5) was difficult to achieve for all participants, whereas participant characteristics associated with adherence to a Mediterranean dietary pattern (MED score 6) were similar to the USDA Food Guide. In general, participants' age and BMI did not vary but energy intake and calcium intake from dietary supplements increased with adherence to all 3 dietary scores.
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5) had 26% reduced risk of colorectal adenoma, 23% reduced risk of colon adenoma (descending colon and sigmoid), and 40% reduced risk of rectal adenoma compared with men who least complied with the recommendations (USDA score 2). Men who most complied with the USDA Food Guide recommendations also had 29% reduced risk for nonadvanced adenoma and 22% reduced risk for advanced adenoma. Women who most complied with the USDA Food Guide recommendations had an 18% reduced risk of colorectal adenoma compared with women who least complied with the recommendations, but significance was not achieved when the outcome was either colon or rectal adenoma or if colorectal adenoma was advanced.
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5) had a 25% reduced risk of colorectal adenoma and a 33% reduced risk for advanced adenoma compared with men who least complied with the DASH Eating Plan (DASH score 2). We also observed 5% reduced risk of colorectal adenoma per unit increase in the MED score (Table 4). Men whose diets most represented a Mediterranean dietary pattern (MED score 6) had a 21% reduced risk of colorectal adenoma and 29% reduced risk for advanced adenoma compared with men whose diets were least similar to a Mediterranean dietary pattern (MED score 2). In women, following the DASH Eating Plan or a Mediterranean dietary pattern was not associated with risk of colorectal adenoma (Tables 3 and 4).
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Results from analyses of individual components of the 3 scores showed that men who met the USDA score criteria for grains, fruits, saturated fat, and alcohol intake had reduced risk of colorectal adenoma compared with men who did not meet the respective criteria (Supplemental Table 5). Meeting the DASH score criteria for fruits and alcohol intake and the MED score criteria for cereals, fruits and nuts, and meat intake were also associated with reduced risk of colorectal adenoma in men. Men who met the Mediterranean diet criterion for alcohol intake had increased risk of colorectal adenoma. In women, only meeting the USDA or MED score criterion for intake of grains or cereals was associated with reduced risk of colorectal adenoma.
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Discussion |
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Other studies have evaluated cancer risk with dietary scores that included aspects of the USDA Food Guide recommendations and reported mixed results. In general, higher variety or diversity scores have been associated with reduced risk of colorectal cancer and other cancers (22–26), although increased dietary diversity was associated with increased risk of colorectal cancer in men from western New York (27). The USDA Healthy Eating Index score was not associated with overall cancer risk in U.S. nurses or health professionals (28,29), whereas an index score that included servings from food groups, body weight, and physical activity was associated with reduced risk of colon cancer in postmenopausal women (30). Scores created to assess a Mediterranean dietary pattern have also shown reduced risk of different cancers (11,31). To date, no studies have evaluated a DASH Eating Pattern with cancer. The DASH diet was developed to reduce hypertension and risk of cardiovascular disease, although key dietary recommendations (e.g. high fruit and vegetable intake) are important for cancer prevention.
Our study has the advantage of large numbers of men and women from diverse U.S. geographic areas examined for screening purposes, largely avoiding the selection biases associated with clinical studies. It is difficult, however, to explain the risk differences observed between men and women for the 3 dietary scores. Like men, women showed reduced risk of colorectal adenoma with increasing adherence to the USDA Food Guide recommendations, but significance was achieved only in women who currently smoked or were normal weight. Among overweight and obese women, it is possible that the adiposity overwhelms the protective effect of healthful eating. It is also possible that dietary patterns high in fruits and vegetables may be more beneficial in smokers, a finding previously shown for lung cancer in male smokers compared with nonsmokers (32). Our results in women may also reflect the inability to completely adjust for other colorectal tumor risk factors or lower statistical power from smaller sample sizes across categories of dietary scores. Underreporting energy intake may be another explanation and has been shown to reduce the likelihood of meeting the criteria for certain food groups (33), which differ across the 3 eating patterns. However, we have no reason to believe that women would have underreported more so than men in our study population.
Dietary scores have general limitations, described in detail elsewhere (14), that may also contribute to our findings. Measurement error in the dietary data is especially important to mention because it may be much larger than previously appreciated (34,35), although how this error applies to dietary scores is unknown. Interpretation of adherence to dietary guidelines or what constitutes a Mediterranean dietary pattern varies among researchers, as shown by the many dietary scores that have been created and evaluated for different health outcomes in different populations (36–38). The scores in our study had similar criteria for a few components (e.g. grains, fruits, dairy), but further differentiation of certain food groups and evaluation of their respective cut-points may add insight into risk differences observed between men and women. For example, in the MED score, meat and fish are separate components with cut-points of 2–3 oz/d for meat and 
0.5 oz/d for fish. In contrast, the meat component in the USDA and DASH scores includes fish and meat equivalents (e.g. eggs and soy products) and 5–6 oz/d is recommended. Recommendations for daily alcohol intake also differ between the U.S. recommendations and a Mediterranean dietary pattern, yielding different results for that component with risk for colorectal adenoma. However, the exclusion of alcohol intake from the 3 scores and subsequent adjustment for alcohol intake as a potential confounder in the regression models did not change our findings.
In conclusion, following the recommendations of the USDA Food Guide, the DASH Eating Pattern, or a Mediterranean dietary pattern was associated with reduced risk of colorectal adenoma of the distal large bowel in men. Women who followed the USDA Food Guide recommendations also had reduced risk of colorectal adenoma, but this was true only for women who currently smoked or were normal weight. Findings from our study suggest that following current U.S. dietary recommendations or a Mediterranean dietary pattern could improve colorectal cancer prevention and control, especially in men.
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FOOTNOTES |
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2 Author disclosures: L. B. Dixon, A. F. Subar, U. Peters, J. L. Weissfeld, R. S. Bresalier, A. Risch, A. Schatzkin, and R. B. Hayes, no conflicts of interest.
3 Supplemental Tables 1–5 are available with the online posting of this paper at jn.nutrition.org.
11 Abbreviations used: DASH, Dietary Approaches to Stop Hypertension; MFA, monounsaturated fatty acid; PLCO, Prostate, Lung, Colorectal, and Ovarian.
15 1 drink = 12 oz beer, 5 oz wine, or 1.5 oz 80-proof distilled spirits.
Manuscript received 5 March 2007. Initial review completed 3 April 2007. Revision accepted 27 August 2007.
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