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American Journal of Epidemiology Advance Access originally published online on September 18, 2007
American Journal of Epidemiology 2007 166(10):1174-1185; doi:10.1093/aje/kwm194
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American Journal of Epidemiology © The Author 2007. Published by the Johns Hopkins Bloomberg School of Public Health. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org.

ORIGINAL CONTRIBUTIONS

Whole Grains and Risk of Pancreatic Cancer in a Large Population-based Case-Control Study in the San Francisco Bay Area, California

June M. Chan1,2, Furong Wang1 and Elizabeth A. Holly1,3

1 Department of Epidemiology and Biostatistics, School of Medicine, University of California, San Francisco, San Francisco, CA
2 Department of Urology, School of Medicine, University of California, San Francisco, San Francisco, CA
3 Department of Health Research and Policy, School of Medicine, Stanford University, Stanford, CA

Correspondence to Dr. Elizabeth A. Holly, Box 1228, Department of Epidemiology and Biostatistics, University of California, San Francisco, 3333 California Street, Suite 280, San Francisco, CA 94118-1944 (e-mail: elizabeth.holly{at}ucsf.edu, furong.wang{at}ucsf.edu).

Received for publication December 26, 2006. Accepted for publication May 31, 2007.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Epidemiologic data suggest that consumption of whole-grain products may be inversely associated with risk of pancreatic cancer. Grain intake was examined in a population-based case-control study of pancreatic cancer in the San Francisco Bay Area (1995–1999). A 131-item semiquantitative food frequency questionnaire was administered to 532 cases and 1,701 controls. Odds ratios and 95% confidence intervals were computed as estimates of relative risk. Persons who consumed ≥2 servings of whole grains daily had a lower risk of pancreatic cancer than persons who consumed <1 serving/day (odds ratio (OR) = 0.60, 95% confidence interval (CI): 0.31, 1.2; trend-p = 0.04). Similar results were observed for brown rice (OR = 0.72, 95% CI: 0.44, 1.2; trend-p = 0.01) and tortillas (OR = 0.56, 95% CI: 0.35, 0.89; trend-p = 0.02). Consumption of doughnuts (≥2 servings/week vs. <1 serving/month) conferred increased risk (OR = 1.8, 95% CI: 1.2, 2.7; trend-p = 0.003). Consumption of cooked breakfast cereals (≥2 servings/week vs. <1 serving/month) was positively associated with risk (for oatmeal/oat bran, OR = 1.3, 95% CI: 1.0, 1.7; for other cooked breakfast cereals, OR = 2.1, 95% CI: 1.4, 3.3). Dietary fiber was inversely associated with risk (for highest quartile vs. lowest, OR = 0.65, 95% CI: 0.47, 0.89; trend-p = 0.02). These data provide some support for the hypothesis that consuming more whole-grain or high-fiber foods may reduce the risk of pancreatic cancer. Refined grains were not associated with risk.

case-control studies; cereals; diet surveys; dietary fiber; pancreatic neoplasms

Abbreviations: CI, confidence interval; OR, odds ratio


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Identifying modifiable risk factors to prevent pancreatic cancer could have a substantial public health impact, as pancreatic cancer is the most fatal cancer in the United States (1). Several studies have suggested that diets high in fiber (2–7), low in glycemic load (8), or high in whole grains (9, 10) may confer some protection against pancreatic cancer. Several plausible biologic mechanisms have been hypothesized to underlie these associations, including the beneficial effects of fiber, whole grains, or low-glycemic-load diets on insulin resistance, triglyceride levels, and high density lipoprotein levels. Each of these may directly influence pancreatic cancer risk or interact with other factors such as diabetes to affect risk (8). To further explore these relations, we examined intake of grain and cereal within a large population-based case-control study of pancreatic cancer in the San Francisco Bay Area, California.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Study population
Details of the study design, selection of the study population, and results of studies of tumor tissue, genetic factors, and other factors have been published previously (11–23). In brief, between 1995 and 1999, men and women with incident adenocarcinoma of the exocrine pancreas were identified in six counties (Alameda, Contra Costa, Marin, San Francisco, San Mateo, and Santa Clara) of the San Francisco Bay Area, using rapid case ascertainment through the Northern California Cancer Center. These patients were designated "in-area cases." Pancreatic cancer diagnoses were confirmed by contacting the patients' physicians and using Surveillance, Epidemiology, and End Results abstracts. Eligible in-area cases were 21–85 years old, residents of one of the six Bay Area counties, alive, and able to complete an in-person interview in English. Sixty-five eligible out-of-area cases also were interviewed. They were seen at University of California, San Francisco, clinics and met the same criteria as in-area cases except that they were residents of counties adjacent to the six Bay Area counties. There was a 67 percent response rate among the 798 eligible cases, and 532 cases completed an interview for this study. Eight percent of patients refused to participate. Control participants were frequency-matched to cases by sex and age within 5-year categories and were selected from the target population using random digit dialing. Controls older than 65 years were supplemented by random selection from Health Care Financing Administration (now the Centers for Medicare and Medicaid Services) lists. A 67 percent response rate was observed among the 2,525 eligible controls, and 1,701 controls completed an interview for this study. No proxy interviews were conducted.

The study protocol was reviewed and approved by the University of California, San Francisco, Institutional Review Board, and written informed consent was obtained from all participants prior to interview.

Intake of foods and nutrients
Participants were asked to report their frequency of intake of individual food items 1 year before cancer diagnosis (for cases) or 1 year before interview (for controls) using a previously validated 131-item semiquantitative food frequency questionnaire (24–26). This food frequency questionnaire has been validated in a variety of populations, including men from the Health Professionals Follow-up Study; men and women in South Dakota and Wyoming, of whom 59 percent had a high school education or less; African-American men with prostate cancer living in Detroit, Michigan; and a nationally representative sample of 1,300 men and women from the Eating at America's Table Study (27–29). In a validation study of 127 men conducted within the Health Professionals Follow-up Study cohort, mean nutrient intakes were similar when assessed by the questionnaire and by two 1-week diet records administered 6 months apart. Coefficients for correlation between calorie-adjusted nutrient intake measured by diet records and the questionnaire were high after adjustment for week-to-week variation in diet-record intake (mean r = 0.7; range, 0.3–0.9) (25). In a validation study conducted within the Nurses' Health Study using an abbreviated version of the questionnaire, questionnaire responses were compared with diet records among 173 women. The correlation coefficients (corrected for within-person variation assessed by the diet records) for several of the grain items of interest were high: 0.71 for pie, 0.57 for cake, 0.60 for biscuits, 0.79 for cereal, 0.71 for white bread, and 0.77 for dark bread (30). This questionnaire also has been used previously in other studies to examine the relations of whole-grain intake to obesity and breast cancer risk (31, 32).

Study participants were asked to average their intake of seasonal food over the entire year. The options for frequency of food intake were: never, <1/month, 1–3/month, 1/week, 2–4/week, 5–6/week, 1/day, 2–3/day, 4–5/day, and ≥6/day. The specified portion size of each food item as provided on the questionnaire was considered one serving, and the food frequency responses were transformed into servings per day. For example, total consumption of whole-grain products was computed by combining reported servings per day of all individual whole-grain food items.

Consumption of individual grain items and overall categories of whole grains, refined grains, mixed grains, and sweetened refined grains were examined. Cereals were examined separately, because many brands/types were consumed and cereal could not be classified within whole- or refined-grain categories. Thus, cold cereal, cooked oatmeal/oat bran, and other cooked breakfast cereals were examined as individual items. Additionally, cooked oatmeal/oat bran was considered as part of whole-grain consumption. Whole grains included brown rice, tortillas, popcorn, other grains (bulgar, couscous, kasha, etc.), oat bran added to food, other bran added to food, wheat germ, and cooked oatmeal/oat bran. Refined grains included white rice, white bread, bagels/English muffins/rolls, muffins/biscuits, pizza, pasta, pancakes/waffles, and pretzels. Mixed grains included dark bread, crackers, Triscuits (Nabisco, East Hanover, New Jersey), Wheat Thins (Nabisco), cold cereal, and other cooked breakfast cereals. Sweetened refined grains included ready-made cookies, homemade cookies, ready-made sweet rolls, homemade sweet rolls, ready-made cake, homemade cake, ready-made pie, homemade pie, doughnuts, and brownies. The range of the correlation coefficients between all of the grain items was 0.00–0.28, and the mean was 0.05. The strongest correlations were observed for items such as homemade cake and homemade pie (r = 0.28) and ready-made cake and ready-made pie (r = 0.23).

This questionnaire was designed to classify people according to their daily intake of certain nutrients over the course of 1 year. Nutrients that were included in this paper were total carbohydrate, dietary fiber, and crude fiber. The questionnaires were mailed to the Department of Nutrition at the Harvard School of Public Health for determination of specific nutrient intake data. Those investigators computed nutrient intakes by assigning a daily frequency weight to the individual food intake data collected from the questionnaire. Further details on the methods used for nutrient assessment with this questionnaire can be found elsewhere (25).

Statistical methods
Odds ratios and 95 percent confidence intervals were computed using unconditional logistic regression for estimation of the relative risk (hereafter called risk) of pancreatic cancer. No substantial differences in odds ratios were observed when participants with extremely low (<500 kcal/day) or extremely high (>3,500 kcal/day) caloric intake were excluded, so these participants were retained in the final analyses. The energy-adjusted residual model was used to estimate risks of pancreatic cancer according to nutrient intake (33). The linear trend test was performed using the Wald procedure. Potentially confounding effects were investigated for energy intake (total calories), sex, body mass index, cigarette smoking, race, education, diabetes, and intake of other food groups. Total caloric intake was divided into quartiles based on consumption among controls, by sex (men: ≤1,545, 1,546–1,925, 1,926–2,364, and ≥2,365 kcal/day; women: ≤1,333, 1,334–1,695, 1,696–2,113, and ≥2,114 kcal/day). Body mass index was estimated from self-reported usual adult weight and height (weight (kg)/height (m)2) as a measure of total adiposity and was divided into three groups (<25, 25.0–29.9, ≥30 kg/m2) based on the World Health Organization criteria for obesity (34). Smokers were defined as participants who had smoked more than 100 cigarettes in their lifetime or had smoked a pipe or cigar at least once a month for 6 months or more. Participants were classified into the following groups: never smokers; former cigarette smokers who had quit smoking more than 15 years previously; former cigarette smokers who had quit smoking 1–15 years previously; current cigarette smokers or former smokers who had quit within the past year; and pipe and/or cigar smokers. Participants self-reported their race as White, Black/African American, Asian/Pacific Islander, or "other." Educational level was grouped as less than high school, high school, 1–4 years of college, and graduate school. History of diabetes was self-reported as yes or no. We also considered intake of other food groups (i.e., red meat, white meat, dairy foods, vegetables and fruits, eggs, and fish) in quartiles based on previous work in this population (12, 16).

We employed stepwise logistic regression modeling (using p = 0.05) to determine the variables that provided the best fit among the potentially confounding factors. Of these factors, energy intake modified the association between grains and pancreatic cancer. For comparability with other studies and our previous publications, we present a parsimonious model in the tables that was adjusted for the matching factors of age and sex and for total energy intake and a full multivariable model additionally adjusted for putative risk factors: race, education, smoking, history of diabetes, body mass index, other grains, and other food groups. The results for men and women were initially examined separately, but there were no appreciable differences by sex. Therefore, all results presented are for men and women combined. All statistical tests were two-sided, and p values were considered statistically significant at less than 0.05. Statistical analyses were conducted using SAS software, version 9.1 (SAS Institute, Inc., Cary, North Carolina).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Overall, cases and controls were quite similar (table 1) with regard to age, race, sex, body mass index, and history of diabetes. As expected, cases were more likely than controls to be current smokers. Controls also were slightly more educated than the cases.


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  		TABLE 1. Demographic characteristics of pancreatic cancer patients and controls in a population-based case-control study, San Francisco Bay Area, California, 1995–1999

 
There was an inverse trend for total servings of whole-grain products and pancreatic cancer risk in multivariable analyses adjusted for age, sex, total energy, body mass index, race, education, smoking, history of diabetes, and other food groups (for ≥2 servings/day vs. <1 serving/day, odds ratio (OR) = 0.60, 95 percent confidence interval (CI): 0.31, 1.2; trend-p = 0.04) (table 2). We also examined the relation between each individual whole-grain item and risk of pancreatic cancer (table 2). An inverse association was observed for brown rice and tortillas, with a suggestion of an inverse association for popcorn. The trend for "other" grains (such as bulgar, kasha, and couscous) was associated with reduced risk (trend-p = 0.03). In contrast, cooked oatmeal or oat bran was slightly positively associated with risk (trend-p = 0.02).


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  		TABLE 2. Association between consumption of whole-grain foods and risk of pancreatic cancer in a population-based case-control study, San Francisco Bay Area, California, 1995–1999

 
Total refined grains (OR = 0.80, 95 percent CI: 0.55, 1.2) and individual refined grain items were not associated with risk of pancreatic cancer (table 3). Mixed-grain products also were not associated with pancreatic cancer risk (OR = 1.0, 95 percent CI: 0.73, 1.5), with the exception of "other cooked breakfast cereal" (not including oatmeal or oat bran), which was positively associated with an approximate doubling of risk (trend-p < 0.0001). Null associations were observed for the following individual refined and mixed-grain products: white bread, white rice, bagels/English muffins/rolls, pizza, pretzels, muffins/biscuits, dark bread, crackers, and cold cereal. Pasta and pancakes/waffles were inconsistently associated with risk, with the medium consumption group having elevated risks but not the highest consumption group. There was no overall association between pancreatic cancer and total sweetened refined grains (OR = 0.74, 95 percent CI: 0.42, 1.3) (table 4). Among individual items, doughnuts (trend-p = 0.003), ready-made pie (trend-p = 0.01), and ready-made cake (trend-p = 0.04) were positively associated with pancreatic cancer risk in the full multivariable model. Ready-made or homemade cookies, sweet rolls/coffee cake/other pastry, and brownies were not associated with risk of pancreatic cancer.


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  		TABLE 3. Association between consumption of refined-grain and mixed-grain foods and risk of pancreatic cancer in a population-based case-control study, San Francisco Bay Area, California, 1995–1999

 

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  		TABLE 4. Association between consumption of sweetened refined-grain foods and risk of pancreatic cancer in a population-based case-control study, San Francisco Bay Area, California, 1995–1999

 
Lastly, fiber, but not total carbohydrates, was inversely associated with risk of pancreatic cancer (table 5). Both crude (trend-p = 0.009) and dietary (trend-p = 0.02) fiber were associated with a 30–35 percent reduction in pancreatic cancer risk when the fourth quartiles of intake were compared with the first quartiles in the full multivariable model.


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  		TABLE 5. Association between consumption of carbohydrate and fiber and risk of pancreatic cancer in a population-based case-control study, San Francisco Bay Area, California, 1995–1999

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
These data provide some support for the hypothesis that whole-grain foods and fiber may provide protection against pancreatic cancer. In contrast, intakes of total refined grains and total mixed grains were not associated with risk of pancreatic cancer. The small to moderately elevated risks observed for cooked oatmeal/oat bran and other cooked breakfast cereals, respectively, were contrary to our hypotheses, as oatmeal/oat bran is typically considered a source of whole grains. The lack of an inverse association may be partly explained by our inability to distinguish consumption of "instant" or sweetened hot cereal from consumption of less refined cereal preparations; however, this does not necessarily explain the observed elevation in risk, and further study is warranted.

These results are somewhat consistent with those of previous studies that have observed inverse associations for fiber, whole grains, and glycemic load or glycemic index, because whole-grain foods generally have a lower glycemic index. A 1998 meta-analysis of four studies that examined low versus high intake of whole grains in relation to pancreatic cancer risk reported a pooled odds ratio of 0.70 (95 percent CI: 0.54, 0.86) (9). In particular, individual grain/cereal food items that have previously been reported to be inversely associated with risk of pancreatic cancer include whole-grain or whole-wheat bread (35, 36) and high-fiber cereal products (37), although these results were not all statistically significant. Notably, in a large case-control study, Nkondjock and Ghadirian (38) reported almost a 50 percent reduction in pancreatic cancer risk (trend-p = 0.004) associated with a "fruit and vegetable dietary pattern." Individual food items comprising such a pattern included rice/pasta, whole grains, and cold breakfast cereals, whereas refined grains were part of the "Western dietary pattern" and were not associated with risk (38).

Other studies have found a lower risk of pancreatic cancer associated with higher fiber or carbohydrate intake (3–7, 39–41). In contrast to our results, a few researchers concurrently reported null (3, 5, 6, 42) or increased (4, 7, 43, 44) risks of pancreatic cancer for total carbohydrate consumption. Additionally, in a few studies, investigators reported an elevated risk for individual grain products (35, 36, 40, 45), while in others they reported null associations for grains (46, 47), fiber (37, 39), or glycemic index or load (48, 49). The majority of the other studies that evaluated fiber, whole grains, or glycemic load/index used proxy interviews, and only one was larger than the current study, with 802 cases (43). Of the three prospective studies that examined glycemic index or glycemic load (8, 48, 49), only in the Nurses' Health Study (8) did investigators report a positive association for glycemic load and risk of pancreatic cancer (relative risk = 1.5, 95 percent CI: 1.0, 2.5). This result was particularly high among women who had a high body mass index or were sedentary (relative risk = 2.7, 95 percent CI: 1.0, 7.0) (8).

Whole grains have been linked to a reduction in risk of various cancers, including colorectal, gastric, digestive tract, pancreatic, endometrial, and oral cancers (9). Currently, plausible biologic mechanisms with which to explain the inverse association between whole grains and fiber and pancreatic cancer risk are speculative, and there are limited experimental or correlative scientific data available. However, leading hypotheses involve whole grains' ability to modify insulin metabolism and their effects on cholesterol or inflammatory pathways. Whole-grain intake has been inversely related to levels of insulin, markers of glycemic control, cholesterol, homocysteine, C-peptide, and leptin, suggesting how these foods may directly or indirectly help to protect against the development of pancreatic cancer (50). Interestingly, lower dietary cholesterol intake and use of statin medications have been inversely linked to pancreatic cancer risk (12, 51, 52), while the cyclooxygenase-2 pathway has been identified as potentially important in pancreatic cancer development (53, 54). The observation of an association between whole grains and pancreatic cancer that is independent of diabetes status suggests that whole grains (or nutrients contained in whole grains) may influence pancreatic carcinogenesis through mechanisms other than insulin sensitivity. Overall, whole grains are richer than refined grains in many of the phytonutrients purported to beneficially affect the risk of pancreatic cancer, including antioxidants, fiber, and folate (55). In vitro studies also support antiproliferative effects of wheat-germ extract on MIA (melanoma inhibitory activity) pancreatic adenocarcinoma cells through a reduction in glucose uptake and decreased synthesis of nucleic acid ribose (56).

Strengths of this study included the large sample size, the population-based design, the lack of proxy interviews, the collection of detailed dietary data from a validated semiquantitative food frequency questionnaire, and the low refusal rate of 8 percent. The primary reason for lost patients was aggressive disease and the high mortality rate of pancreatic cancer. Several limitations should also be considered when interpreting the results of this study. In particular, as in all case-control investigations, there may have been recall bias due to differential reporting of past diet by cases versus controls. However, controls were more likely than cases to have changed their diets in the previous decade, and controls reported having redirected their diets towards more healthy food choices over time (16). This argues against the likelihood that the observed associations were due to recall bias among the cases. Additionally, because risk factors for pancreatic cancer are not widely known within the general population, differential recall between cases and controls is less likely to have played a substantial role. We had no data in this study on the effects of glycemic load or glycemic index. However, a dietary pattern characterized by a low glycemic load is often richer in fiber and whole grains (55, 57). Lastly, multiple comparisons were made in this study, and some results could have been due to chance. However, this study was designed to test specific hypotheses related to foods and food groups, and the outcomes of the analyses were generally consistent with our a priori hypotheses that consumption of whole grains, fiber, or grains contributing to a low-glycemic-load diet might be beneficially linked to pancreatic cancer risk (58).

In conclusion, these data provide some evidence that consuming more whole-grain products or fiber may provide protection against pancreatic cancer.


   ACKNOWLEDGMENTS
 
This study was supported by National Cancer Institute grants CA59706, CA89726, CA09889, CA108370, and CA121846 from the National Institutes of Health, the Rombauer Pancreatic Cancer Research Fund, and the David J. Hasbun Pancreatic Cancer Research Fund.

Conflict of interest: none declared.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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