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Fiber from Whole Grains, but not Refined Grains, Is Inversely Associated with All-Cause Mortality in Older Women: The Iowa Women’s Health Study David R. Jacobs, Jr, PhD, Mark A. Pereira, PhD, Katie A. Meyer, MPH, and Lawrence H. Kushi, ScD Division of Epidemiology, School of Public Health, University of Minnesota, Minneapolis, Minnesota (D.R.J., M.A.P., L.H.K.), Department of Epidemiology, School of Public Health, Harvard University, Cambridge, Massachusetts (K.A.M.) Key words: diet, epidemiology, prospective study, whole grain, fiber, mortality, Iowa Women’s Health Study Background: Inconsistencies in epidemiologic findings relating grain fiber to chronic disease may be explained by differentiating nutrient-rich fiber derived from whole grain vs. nutrient-poor fiber derived from refined grain. Objective: Given that phytochemicals are most varied and abundant in the outer layers of grains, we tested the hypothesis that whole grain fiber consumption is associated with a reduced mortality risk in comparison to a similar amount of refined grain fiber. Design: 11040 postmenopausal women enrolled in the Iowa Women’s Health Study, matched on total grain fiber intake, but differing in the proportion of fiber consumed from whole vs. refined grain, were followed from baseline in 1986 through 31 December, 1997, during which time 1341 deaths occurred in 124,823 observed woman-years. Results: After multivariate adjustment in proportional hazards regression, women who consumed on average 1.9 g refined grain fiber/2000 kcal and 4.7 g whole grain fiber/2000 kcal had a 17% lower mortality rate (RR⫽0.83, 95% CI⫽0.73– 0.94) than women who consumed predominantly refined grain fiber: 4.5 g/2000 kcal, but only 1.3 g whole grain fiber/2000 kcal. Conclusion: Inferences from studies that have reported associations between grain fiber intake and morbidity or mortality may be limited by not differentiating fiber sources. Future studies should distinguish fiber from whole vs. refined grains. Public health policy should differentiate whole grains from refined, and recommend increased consumption of the former. INTRODUCTION fiber may be consumed when a large enough quantity of refined grain is eaten. Furthermore, case-control reports of the association of grain fiber with cancer are inconsistent [5–10]. Therefore, it was hypothesized that the nutrients eaten with fiber (e.g., antioxidants and minerals) play a role in protection against chronic disease and that results of studies of grain fiber intake would depend on the mix of fiber from whole grain vs. refined grain [4,11]. Whole grain fiber is nutrient-rich [11] and confers health benefits that may result in increased longevity, while refined grain fiber is nutrient-poor [11] and offers no such protection when all other factors are held constant [2]. We studied this hypothesis, as described below, by comparing the risk of total mortality between postmenopausal women who reported eating Twenty-five years ago Burkitt and colleagues [1] hypothesized that the rare occurrence in Africa of “Western” diseases (e.g., coronary heart disease and colon cancer) was partly due to a diet characterized by high fiber, minimally processed plant foods. This hypothesis has often been used to promote the idea that high fiber diets may help to prevent chronic diseases and perhaps extend life. Findings [2,3] of reduced risk of cancer, coronary heart disease and total mortality in people who have high intake of whole grain, a high fiber food, support the Burkitt hypothesis. However, an apparently increased cancer risk associated with refined grain intake has been noted [4] in case-control studies, even though a fairly large amount of grain Mark A. Pereira, Ph.D., is now at the Harvard Medical School, Children’s Hospital, Division of Endocrinology, Boston, Massachusetts. Lawrence H. Kushi, Sc.D., is now at Teachers College, Columbia University, New York, New York. Address reprint requests to: David R. Jacobs, Jr., Ph.D., Division of Epidemiology, School of Public Health, University of Minnesota, 1300 South Second St., Suite 300, Minneapolis, MN, 55454. Journal of the American College of Nutrition, Vol. 19, No. 3, 326S–330S (2000) Published by the American College of Nutrition 326S Grain Fiber and Mortality in Women equivalent amounts of grain fiber, in one case derived primarily from refined grain foods, in the other primarily from foods made with whole grain. METHODS Subjects The Iowa Women’s Health Study is a prospective cohort study of postmenopausal women living in the state of Iowa. In January, 1986, a random sample of 99,826 women between the ages of 55 and 69 years with a valid Iowa driver’s license were mailed a 16-page questionnaire and invited to participate. The 41,836 women who returned the baseline questionnaire compose the study cohort. Responders were slightly leaner, older and more likely to live in rural, less affluent counties than were non-respondents [12]. Women were excluded from these analyses if they reported implausibly high (⬎5000 kcal) or low (⬍600 kcal) energy intake (n⫽538) or left 30 or more items blank on the food frequency questionnaire (n⫽2,782), leaving 38,740 women. Of these, 11,040 were included in the matched design, described below under Statistical Analysis. Data Collection r⫽0.24. A study of nurses using a similar questionnaire found high correlations with 28 days of food records for pertinent food items: 0.75 for cold breakfast cereals, 0.61 for white bread, and 0.66 for dark bread [17]. The exposure of interest for the current analyses was dietary fiber from foods that were primarily composed of grains. The total grain food group intake was subdivided into refined and whole grains as previously outlined [2,3]. Table 1 lists the whole and refined grain foods that were queried, with their respective assumed values for dietary fiber. Case Ascertainment Vital status of cohort members was determined through December 31, 1997, via annual linkage with the State Health Registry of Iowa, the National Death Index and follow-up questionnaires mailed in 1987, 1989, 1992 and 1997. During followup, 4761 of the women died. Of these, 983 deaths were attributed to coronary heart disease (ICD-9 codes 410 – 414 and 429.2) and 2049 to cancer(ICD-9 codes 140 –239). Table 1. Whole and Refined Grain Foodsa and their Fiber Assignments The baseline questionnaire and measurements were designed to examine factors that may be involved in chronic disease etiology, including age, body mass index (BMI), waistto-hip ratio (WHR), physical activity, and cigarette smoking. BMI was calculated as kg/m2 from self-measured weight and height. Waist to hip ratio was calculated as the average of two measurements taken by a friend or spouse of participants using a paper tape measure provided with the questionnaire [13]. Questions on the frequency of moderate and vigorous leisuretime activity [14] were combined to create a three-level physical activity score. Pack-years of smoking were calculated from information on the intensity and duration of cigarette smoking. Other participant characteristics, such as age at first live birth or prevalent hypertension, diabetes, heart disease or cancer were self-reported. Food Whole Grain Dark bread Whole grain breakfast cerealb Popcorn Cooked oatmeal Wheat germ Brown rice Bran Other grains (e.g., bulgar, kasha) Refined Grain Sweets/desserts Cookies Brownies Donuts Home baked cakes Ready make cakes Pie White bread, including pita bread Pasta English muffins, bagels, or rolls Refined grain breakfast cerealb White rice Muffins or biscuits Pancakes or waffles Pizza Dietary Assessment A 127-item food frequency questionnaire similar to that used in the 1984 Nurses’ Health Study assessed habitual dietary intake over the past year [15]. The validity of the food frequency questionnaire was evaluated in this cohort by comparing nutrient values determined from the questionnaire to values estimated from the average of five 24-hour dietary recall surveys in 44 participants [16]. The intake of crude fiber was highly reproducible, r⫽0.8 between two questionnaires administered six months apart; agreement with the average crude fiber intake reported on five 24-hour recalls administered four months before the last food frequency questionnaire was lower, JOURNAL OF THE AMERICAN COLLEGE OF NUTRITION Fiber Assignment (g/ serving) 1.1 ⱖ3.0 1.1 4.0 0.9 3.3 1.5 3.2 0.6 0.7 0.8 0.5 1.1 2.2 0.6 2.2 1.3 ⱕ2.5 1.0 2.0 2.0 5.2 a Foods are listed in order of frequency of intake in the cohort. The brand name or generic cereal specified was coded for whole grain content; breakfast cereals with a whole grain or bran content of 25% or more by weight were classified as whole grain. b 327S Grain Fiber and Mortality in Women Statistical Analysis A matched design was used to assess the hypothesis that, for constant total grain fiber intake, mortality was lower in women whose predominant grain fiber source was whole grain foods than in women whose predominant grain fiber source was refined grain foods. We compared two groups of women, matched to consume approximately 6 g/day of total grain fiber (Table 2). The high refined grain fiber group, who on average consumed 77% of their grain fiber from refined grain sources, consisted of 3559 women who reported consuming ⬍3.6 g/2000 kcal of whole grain fiber and ⱖ3.6 g/2000 kcal of refined grain fiber. The high whole grain fiber group, who consumed on average 71% of their grain fiber from whole grain sources, consisted of 7481 women who reported consuming between 3.6 and 6 g/2000 kcal of whole grain fiber and ⬍3.6 g/2000 kcal of refined grain fiber. Women consuming higher levels of whole grain fiber were excluded from this group because there were very few matching women consuming more than 6 g/2000 kcal from refined grain. The difference in death rates between the matched groups became larger, the higher the refined grain fiber cutpoint used to define the matched groups. The mortality in the high whole grain fiber group relative to the high refined grain fiber group was studied using proportional hazards regression models which also contained the independent variables age and energy intake. Because whole grain intake is strongly associated with a healthier lifestyle [2], a multivariate adjusted model added the covariates listed in the footnote to Table 4. RESULTS The women who derived 71% of their total grain fiber from whole grain were older, consumed less total fat and carbohydrate, more total dietary fiber, more fruits and vegetables, red meat, fish and seafood, and alcohol, were less likely to smoke, Table 2. Mean ⫾ Standard Deviation of Grain Fiber Intake (g/2000 kcal) in Iowa Women Aged 55 to 69 in 1986 in Two Groups Matched on Eating Approximately 6 g/2000 kcal per Day of Total Grain Fiber Intake Whole grain fiber Refined grain fiber 71% of total grain 77% of total grain fiber intake* fiber intake** Sample size Whole grain fiber intake Refined grain fiber intake Total grain fiber intake (group matching criterion) 7481 4.7 ⫾ 0.07 1.9 ⫾ 0.8 3559 1.3 ⫾ 1.0 4.5 ⫾ 0.9 6.6 ⫾ 1.0 5.8 ⫾ 1.2 * 3.6-6 g/2000 kcal of whole grain fiber and ⬍3.6 g/2000 kcal of refined grain fiber. ** ⬍3.6 g/2000 kcal of whole grain fiber and ⱖ3.6 g/2000 kcal of refined grain fiber. 328S Table 3. Baseline Means or Percentages in Iowa Women Aged 55 to 69 in 1986 in Two Groups Matched on Eating Approximately 6 g/2000 kcal per Day of Total Grain Fiber Intake Number of women Age (years) Energy (kcal/day) Total fat (% kcal) Saturated fat (% kcal) Carbohydrate (% kcal) Total dietary fiber intake (g/2000 kcal) Fruit and vegetables (servings/week) Red meat (servings/week) Fish & seafood (servings/ week) Alcohol intake (g/day) Cigarette smoking (packyears) (% ever smoked) BMI (kg/m2) Waist-hip ratio Age at first live birth (years) Physical activity (% highly active) Education (%⬎ high school) Hormone replacement therapy (% users) Vitamin supplement use (%) Currently married (%) Prevalence of self-reported disease (%) Hypertension Diabetes Heart disease Cancer Whole grain fiber 71% of total grain fiber intake* Refined grain fiber 77% of total grain fiber intake** 7481 61.8 1838 33.4 11.6 49.3 23.3 3559 61.4† 1847 34.5† 11.6 50.2† 19.2† 47 35† 5.8 1.9 5.3† 1.3† 3.4 8.1 2.3† 11.0† 31 27.0 0.834 20.7 27 37† 27.2 0.846† 20.3 18† 43 41 32† 35† 36 77 27† 74† 36 7 9 10 37 6 10 9 * 3.6-6 g/2000 kcal of whole grain fiber and ⬍3.6 g/2000 kcal of refined grain fiber. ** ⬍3.6 g/2000 kcal of whole grain fiber and ⱖ3.6 g/2000 kcal of refined grain fiber. † p ⬍ 0.001. Age is unadjusted, energy intake is age adjusted, and all other variables are age and energy intake adjusted; adjustment is by linear regression. had a smaller waist to hip ratio, were more physically active, had more education, were more likely taking hormone replacement therapy and vitamin supplements, and were more likely to be married. Most of these differences were small between the groups matched on total grain fiber intake (Table 3). There were 1341 total deaths among the 11,040 women studied (124,823 woman-years). Among these, 1240 deaths in 10,444 women had complete data for multivariate analysis. After multivariate adjustment in proportional hazards regression, the women who consumed on average 1.9 g refined grain fiber/2000 kcal and 4.7 g whole grain fiber/2000 kcal had a VOL. 19, NO. 3 Grain Fiber and Mortality in Women Table 4. Proportional Hazards Regression Analysis of Mortality in Iowa Women Matched on Total Grain Intake in 1986 and Followed from 1986 to 1997 Total mortality Coronary heart disease mortality Other cardiovascular disease mortality All cancer mortality All other mortality Hazard Rate Ratio adjusted for age and energy intake Hazard Rate Ratio multivariate adjusted* 0.75 (0.67,0.84) 0.82 (0.64,1.05) 0.83 (0.73,0.94) 0.89 (0.66,1.20) 0.72 (0.54,0.96) 0.75 (0.54,1.06) 0.83 (0.70,0.99) 0.74 (0.64,0.84) 0.92 (0.75,1.12) 0.83 (0.71,0.97) * Adjusted for age, energy intake, educational status, marital status, hypertension, diabetes, heart disease, cancer, body mass index, waist to hip ratio, age at first birth, physical activity score, ever smoker, pack years of cigarette smoking, alcohol intake, vitamin supplement use, hormone replacement therapy use, percent of energy from total fat, saturated fat, and carbohydrates, intake per 1000 kcal of fiber from nongrain sources, intake of red meat, and intake of fish and seafood. 17% lower mortality rate (RR⫽0.83, 95% CI⫽0.73– 0.94) than the women who consumed predominantly refined grain fiber: 4.5 g/2000 kcal, but only 1.3 g whole grain fiber/2000 kcal (Table 4). These findings reflected, in part, reductions among 274 coronary heart disease deaths (247 in multivariate analyses), 190 other cardiovascular deaths (180 in multivariate analyses), 566 cancer deaths (527 in multivariate analyses), and 877 other deaths (813 in multivariate analyses). Compared to the high refined grain fiber consumers after adjustment for the demographic, behavioral and physiologic characteristics, the high whole grain fiber women suffered less of each cause of death, statistically significant for non-cardiovascular, non-cancer mortality (Table 4). Women who were excluded from the matched design because they consumed more than 6 g/2000 kcal of whole grain fiber, generally accompanied by small amounts of refined grain fiber, had statistically significantly reduced total, coronary heart disease, and all cancer mortality rates, compared to women who ate little whole grain fiber (data not shown). COMMENT In these data, a similar amount of total grain fiber had dissimilar associations with total mortality, depending on whether the fiber came from foods that contained primarily whole grain or refined grain. The fiber only from whole grain was associated with reduced risk of mortality. These observations imply that consumption of the plant constituents that are botanically linked to fiber may confer important health benefits above and beyond effects of the fiber itself. Among these constituents, found abundantly in the bran and germ of whole JOURNAL OF THE AMERICAN COLLEGE OF NUTRITION grains, are minerals, vitamins, phenolic compounds and phytoestrogens [11]. Although individuals who consume large quantities of refined grain may consume relatively high amounts of grain fiber, this fiber derived from cell walls in the starchy endosperm is nutrient-poor, as it does not include the biochemicals found in the nutrient-rich bran and germ. This is not to say that dietary fiber itself is not important, for instance in modulating the glycemic index [18,19], reducing gastric transit time and lowering serum cholesterol [20 –23]. Jacobs et al. [4,24] reviewed case-control studies of cancers and intake of whole grain foods, finding generally reduced risk associated with higher whole grain intake. Follow-up analyses in the Iowa Women’s Health Study [2,3] broadened the findings of the reviews on whole grain and cancer. In the Iowa women studied here, followed for nine years, total, cancer, and CHD mortality were reduced in those who reported habitual consumption of whole grain foods. In contrast, these causes of death tended to be positively associated with refined grain intake [3]. One interpretation of the findings of these earlier studies is that whole grain protects against chronic diseases because it is a “high fiber” food. However, the findings of the current analyses imply that this may be an oversimplification, because refined grain also contains grain fiber, although in smaller concentrations than does whole grain. If enough refined grain foods are eaten, a fairly large amount of grain fiber can be consumed, albeit with several times the amount of starch in comparison to whole grain foods. Taken together, the findings of previous studies and of this matched analysis suggest that the potential health effects of grain fiber may depend on its source. The group-matched design used here did not work perfectly, in that the mean level of total grain fiber differed between the matched groups by 0.8 g/2000 kcal. Perfect matching was not possible because of the inverse correlation between whole grain fiber intake and refined grain fiber intake (r⫽⫺0.24). Findings were robust to modifications in cutpoints defining the matched groups; the estimate of mortality difference between matched groups was enhanced, but the number of subjects in the higher refined grain fiber group dropped rapidly, the higher the cutpoint chosen for higher vs. lower refined grain fiber (data not shown). We also considered a proportional hazards regression strategy in the whole cohort, with the two fiber terms included as continuous variables. However, we determined that the full cohort analysis strategy was more effective for whole grain fiber than for refined grain fiber. The whole grain fiber proportional hazards regression coefficient was inverse in all analyses, but the refined grain fiber regression coefficient varied greatly and had a large standard error. The limited range of intake of refined grain fiber intake led to a substantially less reliable estimation of the association of mortality with refined grain fiber than with whole grain fiber. This problem of limited range of refined grain fiber intake was circumvented in the matched design. The problem of limited range of intake may 329S Grain Fiber and Mortality in Women have contributed to inconsistent findings concerning total grain fiber in populations that consume little whole grain [5–10,25]. Future studies should attempt to separate grain fiber-containing foods into those that are nutrient-rich (whole grains) and those that are nutrient-poor (refined grains). Although further basic research, including feeding studies in animals and humans, on the effects of nutrients and constituents associated with fiber is needed, as recently suggested by Jacobs et al., [2,3] and Willett [26], public health recommendations should more clearly differentiate between carbohydrates that are nutrient-rich (e.g., at least part whole grain breads and breakfast cereals) and those that nutrient-poor, due to refining or other processing. REFERENCES 1. 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