Journal of the American College of Nutrition, Vol. 18, No. 6, 591-597 (1999)
Published by the American College of Nutrition
The Effect of Particle Size of Whole-Grain Flour on Plasma Glucose, Insulin, Glucagon and Thyroid-Stimulating Hormone in Humans
Kay M. Behall, PhD,
Daniel J. Scholfield, BS and
Judith Hallfrisch, PhD
The Diet and Human Performance Laboratory, Beltsville Human Nutrition Research Center, Agricultural Research Service, US Department of Agriculture, Beltsville, Maryland
Address reprint requests to: Kay M. Behall, Ph.D., Building 308, BARC-East, Diet and Human Performance Laboratory, Beltsville Human Nutrition Research Center, ARS, USDA, Beltsville, MD 20705-2350
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ABSTRACT
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Objective: Although it is well known that consumption of whole-grain foods with higher fiber content results in beneficial health effects, most Americans usually prefer bread made with white flour. Changes in bread texture and undesirable intestinal responses have been reported as reasons for avoiding consumption of whole-grain foods or high-fiber menus. The purpose of this study was to determine whether consumption of bread made with ultra-fine-ground whole-grain wheat flour retained beneficial effects while reducing undesirable effects.
Methods: Twenty-six men and women, 31 to 55 years of age, consumed glucose solutions or bread made with traditional white, conventional whole-grain wheat (WWF), or ultra-fine whole-grain wheat (UFWF) flour (1 g carbohydrate/kg body weight) in a Latin square design after two days of controlled diet. The effect on glycemic response was determined by comparing blood variables, after a tolerance test with white bread, WWF bread, and UFWF bread, with those after a glucose tolerance test.
Results: Men and women had similar responses to all tolerances except postprandial TSH. Glucose and insulin levels one half hour after the glucose load were significantly higher than after any of the bread tolerances. Glucose, but not insulin, areas under the curve were significantly higher after the glucose load than areas after the three breads. Consumption of UFWF resulted in glucose and insulin responses, as well as areas under the curve, similar to those after consumption of conventional whole-wheat bread.
Conclusion: The particle size of whole grain wheat flour did not substantially affect glycemic responses.
Key words: wheat particle size, glucose, insulin, glucagon, thyroid hormones
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INTRODUCTION
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Most health organizations and government agencies involved in the health of the nation recommend an increase in consumption of dietary fiber [1,2]. Diets high in dietary fiber have been reported to result in a number of beneficial health effects, including reduced heart disease [3], hypertension [4], colon cancer [5], diabetes [6] and obesity [7]. However, the median dietary fiber intakes reported between 1988 and 1991 for men and women in the United States were 17.0 and 13.8 g/d, respectively [8]. Less than one-third of the U.S. population over 20 years of age met the target of five or more servings of fruits and vegetables per day recommended in the Healthy People 2000 objectives, and more than half of adults consumed less than one serving of fruit daily. The intake of total carbohydrate in the United States in between 1988 and 1991 was approximately 50% of total energy intake, with approximately half of this consumed from complex carbohydrate sources (39.5% from grain products, 8.3% from vegetables, and 1.8% from nuts and legumes) [8].
Replacing white bread with whole-grain breads is usually mentioned as one way to accomplish an increase in dietary fiber because grain products constitute the largest source of complex carbohydrate. Consumption of carbohydrate from white bread is five times that of whole grain wheat, rye, and other dark breads [9]. Adding the intake of complex carbohydrate from other sources, such as doughnuts, cookies and cakes, increases the ratio of white flour to whole-grain flour to seven. Although there has been some recent increase in the consumption of whole-grain flours and as people get older they consume more whole-grain foods [10], Americans seem to prefer white flour. Many factors influence the food choices people make [11]. One deterrent to whole-grain consumption is the perception that diets high in dietary fiber cause undesirable gastrointestinal side effects, such as irritation of the lining of the small intestine, diarrhea and flatulence [11].
The source, amount and form of the carbohydrate consumed were reported to make a difference in the observed glucose response to the food [12–14], and the particle size of food was shown to be inversely related to glucose and insulin responses in some foods [15,16]. The purpose of this study was to compare the effects of traditional white bread with those of whole-grain breads made with conventional whole-wheat flour and with fine-ground whole-wheat flour to determine whether particle size of the wheat fiber affects glycemic response.
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MATERIALS AND METHODS
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Subjects
Twenty-six free living volunteers were selected for and completed the dietary study after clinical analysis of fasting blood and urine samples and a medical evaluation (Table 1). Subjects were excluded if they had abnormal fasting glucose, evidence of an infection, were hypertensive or were taking prescription drugs. Subjects were ask to discontinue any vitamin or mineral supplements for the duration of the study. The study was approved by the Institutional Review Board of The Johns Hopkins School of Public Health and the U.S. Department of Agriculture Human Studies Committee. Medical supervision was provided by Dr. Benjamin Caballero, Division of Human Nutrition, The Johns Hopkins University School of Public Health.
Study Design
Subjects consumed a controlled standardized menu containing 30% fat, 55% carbohydrate and 15% protein for two days before and the day of each carbohydrate tolerance test. The standard diet was designed to contain a moderately high percentage of carbohydrate without foods known to lead to colonic gas production. The menu was identical during each of the four periods (Table 2). Based on body weight, subjects were placed on one of seven energy levels and consumed that same amount of energy during all four periods. Nutrient content of the menu was similar to dietary recommendations [17].
Subjects came to the Beltsville Human Nutrition Research Center’s Human Diet Facility each day before breakfast to be weighed, eat breakfast and pick up lunch and dinner. They were required to consume all foods and beverages given and nothing else unless approved by the principal investigator. Intake of all additional items such as water, noncaloric beverages, salt and pepper was recorded daily. On Friday evenings subjects were required to consume all food by eight p.m. On the following morning, subjects arrived at the center between six and eight a.m. Fasting blood and breath samples were collected. Subjects then consumed either a glucose solution or a test bread containing an equal amount of carbohydrate (1 g carbohydrate/kg body weight based on the mean of Thursday and Friday weights). Test breads were provided by Glen Weaver at Con Agra Grain Processing Company, Omaha, Nebraska. All breads were made with hard white winter wheat (Platte variety). The particle size of the white bread flour was all less than 150 µm. The conventional whole grain wheat flour particle size ranged from 850 µm to <150 µm; the distribution was 100% <850 µm, 95% <425 µm, 90% <250 µm, 80% <180 µm, and 50% <150 µm. The fine ground whole grain wheat flour particle size ranged from 150 µm to <37 µm; the distribution was 100% <150 µm, 90% <73 µm, 53% <42 µm, and 45% <37 µm. Nutrient content of the breads is listed in Table 3. Blood samples were collected at 0.5, 1, 2 and 3 hours after consumption of the test food. Blood samples were drawn by a certified phlebotomist. These blood samples were collected so that blood glucose and glucoregulatory hormone responses could be measured. Breath samples were also collected before and after the tolerances. These results have been previously reported [18]. The test carbohydrates were given in a Latin square design.
Sample Collection and Analyses
Blood was centrifuged and plasma was separated and stored at -80°C until analyzed on site. Plasma was analyzed for glucose, insulin, glucagon and thyroid-stimulating hormone (TSH). Glucose was determined on an automated spectrophotometric system (Baker Instruments Corp, Allentown, PA). Insulin (ICN Biomedicals, Inc., Costa Mesa, CA), glucagon and TSH (Diagnostics Products Corporation, Los Angeles, CA) were determined by radioimmunoassay. Because fasting levels and curve shape were different, response areas were calculated by using the method of Wolever and Jenkins [19], which uses differences above fasting levels for glucose and insulin.
Statistical Analyses
Sample size calculations prior to the study by power analysis determined that a 10% difference in parameters could be detected with a sample size of eight if each gender had to be analyzed separately. Data were statistically analyzed by using a linear models procedure for repeated-measures analysis of variance (PCSAS, version 6.11, SAS Institute, Cary, NC). Data were evaluated for the main effects of carbohydrate type (glucose or breads), gender and interactions between gender and carbohydrate type. Data reported are least-squares means and standard errors of the means (SEMs) and differences between groups were determined by least significant differences using the critical level of significance of p<0.05.
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RESULTS
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Plasma glucose response did not significantly differ (p < 0.16) for the men and women after the four tolerance tests; therefore, combined values are shown (Fig. 1). Significant differences were observed in plasma glucose after the three breads were consumed (treatment, p<0.02; treatment by time, p<0.0001). Plasma glucose concentration was significantly higher at 0.5 hours and lower at three hours after the glucose than after any bread. After the glucose and the white bread tolerance tests, plasma glucose at one hour was higher than levels observed after the tolerance tests for either whole-grain bread. No other interactions were observed. The glucose area under the curve above fasting was, to two hours, significantly (p<0.0001) higher after the glucose tolerance test than after all bread tolerance tests (Table 4). The areas under the curve after the bread tolerance tests were not significantly different. Areas under the curve did not differ between the sexes (p<0.50) and no treatment-by-gender interaction was observed (p<0.81).
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Fig. 1. Glucose response of 26 subjects to tolerance tests for glucose or three breads. Least-square means±SEM. Within a collection time, glucose values with different superscripts were significantly different. Glucose was significantly affected by treatment (p<0.02), time (p<0.0001) and treatment-by-time interaction (p<0.0001).
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Plasma insulin response of the men and women after the tolerance tests was not significantly different (p<0.98). Significant differences were observed in plasma insulin between the glucose tolerance test and three bread tolerance tests (treatment by time, p<0.001) (Fig. 2). Plasma insulin concentration was higher at 0.5 hours and lower at three hours after the glucose tolerance test than after any bread tolerance test. Plasma insulin responses after the whole-grain breads were not significantly different. The insulin areas under the curve were not significantly different between the glucose and the bread tolerance tests (treatment, p<0.4) or between the genders (p<0.65), and no interaction was observed (p<0.77) (Table 4).
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Fig. 2. Insulin response of 26 subjects to tolerance tests for glucose or three breads. Least-square means±SEM. Within a collection time, insulin values with different superscripts were significantly different. Insulin was significantly affected by time (p<0.0001) and by treatment-by-time interaction (p<0.001).
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Plasma glucagon response did not significantly differ (p<0.09) between the men and women after the four tolerance tests. Significant differences were observed in plasma glucagon between the glucose tolerance test and three bread tolerance tests (treatment, p<0.005; treatment by time, p<0.0001) (Fig. 3). Plasma glucagon was significantly lower at 0.5 and one hour after the glucose tolerance test than after any bread tolerance test and significantly lower at two hours than after the glucose tolerance test or after either the WWF or the UFWF bread tolerance test. Glucagon levels after the white bread tolerance test were not significantly different from those after the WWF bread, but were significantly lower than those after the UFWF bread tolerance test at 1, 2 and 3 hours. The glucagon responses of the two whole-wheat breads were not statistically different.
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Fig. 3. Glucagon response of 26 subjects to tolerance tests for glucose or three breads. Least-square means±SEM. Within a collection time, glucagon values with different superscripts were significantly different. Glucagon was significantly affected by treatment (p<0.005), time (p<0.0001) treatment-by-time interaction (p<0.0001).
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TSH tolerance response did not differ by gender (p<0.61) or by treatment (p<0.27). A significant gender-by-time interaction (p<0.0002) was observed. Since no treatment effect was observed, TSH responses after all treatments were combined by gender (Fig. 4). Men and women had similar postprandial decreases in TSH from fasting to one hour; levels in men at two and three hours returned toward fasting levels, whereas those of the women continued to decrease. Mean TSH levels of the men at three hours after all of the tolerance tests were significantly higher than those of the women.
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Fig. 4. Thyroid stimulating hormone (TSH) response of 26 subjects to tolerance tests for glucose or three breads. Least-square means±SEM. Within a collection time, TSH values with different superscripts were significantly different. TSH was significantly affected by time (p<0.0001) and by gender-by-time interaction (p<0.0002).
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DISCUSSION
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Gender differences were not observed between the different treatments for glucose or glucoregulatory hormone responses reported here. No gender difference in insulin response after a tolerance test has been reported, although glucose uptake per unit mass by muscle was reported to be greater in women than men [20,21]. Among African-Americans tested by Falkner et al. [22], women had higher insulin/glucose ratios and insulin sums after a glucose tolerance test and lower insulin-stimulated glucose utilization than did men. No gender difference in glucagon response observed during insulin clamp studies [23,24] has been reported. Unlike with insulin and glucagon, a gender difference in TSH response regardless of treatment was observed in the study reported here: the responses of men returned to fasting levels sooner than those of women. Kamat et al. [25] reported meal composition (standard or low energy/high fiber) at lunch or dinner had a significant influence on the postprandial levels of serum TSH. Serum TSH decreased twice as much following the standard lunch or dinner than following the low energy meals. A significant meal by time by gender interaction (p<0.04) was reported although not described in detail. A significant meal by gender interaction (p<0.002) was also reported for resin uptake of triiodothyronine. Men had higher response after the standard meals than after the low energy meals, whereas the opposite response was observed in the women.
Several previous studies have shown that size of food particle has a significant effect on insulin and/or glucose responses [15,26]. Read et al. [15] examined the effect on glycemic response of thorough mastication versus no chewing for pieces of corn, rice, apple and potato. Foods consumed in large pieces or without chewing resulted in lower postprandial glucose levels than observed after the same food had been thoroughly chewed. Collier and O’Dea [26] reported lower glucose and insulin response after 75 g carbohydrate from whole brown rice than after ground brown rice in diabetic and normal subjects. Within each group of subjects, glucose and insulin responses were similar after consumption of the ground brown rice and after the glucose tolerance test. The authors concluded the observed differences were due to the physical form of the complex carbohydrate rather than the metabolic differences between the subject groups.
Although swallowing whole grains or large pieces of food can decrease the glycemic response, this procedure is not generally practiced nor could it be recommended. Consumption of the same food, differing in fiber content or in coarseness of the flour or grain particles, more commonly occurs. Neither particle size of the whole-wheat flour nor the fiber content of the bread significantly affected the insulin, glucose or TSH area under the curve. Peak insulin response was delayed from 0.5 to one hour after all breads compared with the glucose tolerance test. Postprandial plasma glucose was lower at one hour after both whole-wheat bread tolerance tests than after the white bread tolerance test, but the difference was not significant.
As opposed to our observations, Heaton et al. [27] observed higher plasma insulin response (peak response and area under the curve) after isocaloric wheat-based meals containing fine flour than after those containing coarse flour, cracked grains or whole grains. When cornmeal was fed, plasma insulin showed a similar increased response to decreased particle size. Similar to our results, plasma glucose after the fine-flour meal was not different from that observed after coarse flour [27]. Holt and Miller [28] also fed test meals containing four different grades of wheat. Plasma glucose and insulin responses (area under the curve) were highest after the fine-flour meal, followed by the coarse flour and cracked grain, with the lowest area under the curve observed after the whole-grain meal. Postprandial satiety was reported to be inversely related to the insulin response. O’Donnell et al. [29] fed obese subjects with ileostomies coarse and fine whole-meal flours in a test meal pattern similar to that of Heaton et al. [27]. The obese subjects had higher glucose and insulin response areas under the curve after the fine-ground than after the coarse whole-meal flour. Unabsorbed starch in the ileostomy effluent was significantly higher after the meal containing the coarse whole meal, indicating slower and less complete starch digestion in the meal containing the coarse particle flour.
Jenkins et al. [16] reported a significant decrease in glycemic index (white bread baseline) when their barley bread contained 50% (glycemic index of 62) and their bulgur bread contained 75% (glycemic index of 69) or more of the available carbohydrate from barley kernels or cracked wheat kernels, respectively. Liljeberg et al. [30] observed significantly lower glycemic and insulin indexes after coarse bread products containing kernels from wheat, rye or barley, but not after oats, than they did after white bread. In the study reported here, when white bread is used as the baseline tolerance test, glycemic index values for WWF bread (85.2) and UFWF bread (79.3) are similar to those observed by Liljeberg et al. [30] after the coarse wheat bread (73.8), but our decreases were not statistically significant. We also did not see a corresponding decrease in insulin response.
No change in postprandial glycemic or insulin response was observed between two different particle sizes when meals were fed with either wheat fiber or beet pulp [31]. D’Emden et al. [32] observed no difference in glycemic response (area under the curve) between white and semolina bread or between white and wholemeal spaghetti. The breads had higher glycemic and insulin responses than did either spaghetti. Insulin response was similar between the two breads, but insulin response after whole-meal spaghetti was greater than that after white-flour spaghetti, a finding which they attributed to the protein content of the whole-meal spaghetti. The authors concluded that the physical form of the food rather than the fiber content and particle size was the major factor influencing glycemic response.
It appears that, although it was not significant, the increased fiber content of our whole grain wheat and ultra-fine-ground whole wheat decreased the glycemic index. The area under the curve for the glucagon response significantly increased as the glucose response decreased, even though insulin response did not change.
Particle size appears to exert the greatest affect on glycemic and insulin response when large food or grain particles are present. Studies using regular white and whole-wheat flours did not report significant differences observed in plasma glucose or insulin concentrations when whole grains or coarse whole meals were used. The form of the food consumed must also be considered. Use of the ultra-fine whole wheat in a pasta product might result in substantially lower glucose and insulin responses. Results indicate that consumption of ultra-fine whole-grain bread containing more total fiber than white bread, while maintaining a texture similar to that of white bread, can result in a moderately lower glucose response than does consumption of white bread. Health benefits have been associated with consumption of whole grain foods. However, traditional white bread is still the primary bread consumed by the American population. Ultra-fine whole wheat flour may be more acceptable to the typical American than conventional whole-wheat bread while providing the beneficial effects of reduced glycemic response and increased intake of total dietary fiber.
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ACKNOWLEDGMENTS
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We thank Evelyn Lashley, Chief Dietitian of the Human Study Facility, for her conscientious supervision; research cooks Linda Lynch and Sue Burns for excellent food preparation and cheerful interaction with subjects; Daniel J. Scholfield for study coordination; Willa Mae Clark and Anna van der Sluijs for analysis of the breath samples; Elisa Armero for painless phlebotomy; and all subjects who participated in the study.
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FOOTNOTES
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An abstract including information in this manuscript was presented at the Federation of American Societies for Experimental Biology, New Orleans, LA, April 9, 1997.
Received February 1, 1999.
Accepted August 1, 1999.
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TOP
ABSTRACT
INTRODUCTION
