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Journal of the American College of Nutrition, Vol. 18, No. 2, 159-165 (1999)
Published by the American College of Nutrition

Effect of Wheat Bran on Serum Lipids: Influence of Particle Size and Wheat Protein

David JA Jenkins, MD, FACN,,, Cyril WC Kendall, PhD,,, Vladimir Vuksan, PhD,,, Livia SA Augustin, MSc,,, Christine Mehling, RD,,, Tina Parker, RD, Edward Vidgen, BSc,,, Brenda Lee, MSc,,, Dorothea Faulkner, RD, Hilda Seyler, MSc, Robert Josse, MD, Lawrence A Leiter, MD,, Philip W Connelly, PhD, and Victor Fulgoni, III, PhD

Department of Nutritional Sciences (D.J.A.J., C.W.C.K., V.V., L.S.A.A., C.M., E.V., B.L., L.A.L.), Faculty of Medicine, University of Toronto, Toronto, Ontario, CANADA
Department of Biochemistry (P.W.C.), Faculty of Medicine, University of Toronto, Toronto, Ontario, CANADA
Department of Laboratory Medicine and Pathobiology (P.W.C.), Faculty of Medicine, University of Toronto, Toronto, Ontario, CANADA
Clinical Nutrition and Risk Factor Modification Center (D.J.A.J., C.W.C.K., V.V., L.S.A.A., C.M., T.P., E.V., B.L., D.F., H.S.), St. Michael’s Hospital, Toronto, Ontario, CANADA
Department of Medicine, Division of Endocrinology and Metabolism (R.J., L.A.L., P.W.C.), St. Michael’s Hospital, Toronto, Ontario, CANADA
The Kellogg Company (V.F.), Battle Creek, Michigan

Address reprint requests to: David JA Jenkins, MD, FACN, Clinical Nutrition and Risk Factor Modification Center, St Michael’s Hospital, 61 Queen St. East, Toronto, Ontario, CANADA M5C 272


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Objective: Wheat fiber appears to protect from cardiovascular disease despite its lack of consistent effect on serum lipids. We therefore wished to determine whether reported inconsistencies in the effect of wheat bran resulted from differences in particle size or its high gluten content.

Methods: Two studies were conducted. In one-month metabolic diets, 24 hyperlipidemic subjects consumed breads providing an additional 19 g/d dietary fiber as medium or ultra-fine wheat bran and extra protein (10% of energy as wheat gluten). In two-week ad libitum diets, 24 predominantly normolipidemic subjects consumed breakfast cereals providing an additional 19 g/d of dietary fiber as coarse or a mixture of ultra-fine and coarse wheat bran with no change in gluten intake. Both studies followed a randomized crossover design with control periods when subjects ate low-fiber breads and cereals respectively with no added gluten. Fasting blood lipids were measured on day zero and at the end of each phase.

Results: Wheat bran had no effect on total, LDL or HDL cholesterol irrespective of particle size or level of gluten in the diet. However, consumption of increased gluten in the metabolic study was associated with a 13±4% reduction in serum triglycerides (p=0.005) which was not seen in the normal-gluten ad libitum study.

Conclusions: The protective effect of wheat fiber in cardiovascular disease cannot be explained by an effect of wheat bran in reducing serum cholesterol although in hyperlipidemic subjects displacement of carbohydrate by gluten on the high-fiber phases was associated with lower serum triglycerides.

Key words: wheat bran, dietary fiber, wheat gluten, vegetable protein, triglycerides, cardiovascular disease


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
SUBJECTS AND METHODS
 RESULTS
 CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Insoluble cereal fiber intake in the context of a Western diet reflects wheat-fiber consumption and has consistently been associated with a reduced risk of cardiovascular disease in epidemiological studies [1,2]. In general, the effect of wheat bran on blood lipids has not provided a reason for the reduced cardiovascular risk [3–7] since the majority of studies have found no lipid reduction. Nevertheless, there remain a significant number of studies where diets containing wheat bran have been associated with lower serum cholesterol or lipoprotein concentrations [8–19]. In view of the epidemiological evidence, these studies require explanation.

In this context two of the unanswered questions were whether the effect of wheat-bran particle size or wheat-bran protein content contributed to the lipid lowering in those studies where a reduction in serum cholesterol was observed. Theoretically, finer particle-size wheat bran may reduce serum cholesterol by increasing the surface area for bile-acid binding [20] or altering the amount or proportion of the short-chain fatty acids produced [21]. Alternatively, the vegetable protein associated with wheat bran may influence serum lipids [22]. Since there is no clear evidence that wheat bran influences cardiovascular risk by reduction in blood pressure [23–28], we considered that the effect of wheat bran on blood lipids continued to warrant further investigation.

To this end, we have assessed the effect of ultra-fine, medium and coarse wheat brans on serum lipids and whether the effect was modified by higher wheat protein (gluten) intake.


   SUBJECTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
RESULTS
 CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 
A total of 48 healthy men and women took part in two studies. The metabolic study involved 16 men and eight women with a mean (±SD) age of 57±10 years (range 35 to 72 years) and body mass index (BMI) 25.3±3.0 kg/m2 (range 18.9 to 31.5 kg/m2). In the ad libitum study, there were twelve men and twelve women with a mean age of 36±12 y (range 17 to 57 y) and BMI of 24.5±2.7 kg/m2 (range 18.4 to 29.0 kg/m2). No subject had clinical or biochemical evidence of hepatic or renal disease. None were taking cholesterol-lowering medications, ß-blocking agents or L-thyroxine. One woman was on hormone replacement therapy. In the ad libitum study, one subject was taking an oral hypoglycemic agent for the control of type 2 diabetes. Dosage levels of all medications were maintained constant over study periods. Subjects for the metabolic study were recruited from among patients attending the hospital clinical nutrition center and by newspaper advertisement, on the basis of a history of elevated serum cholesterol [29] and in whom serum low-density lipoprotein (LDL) cholesterol was demonstrated to be raised (>4.1 mmol/L) on at least one occasion prior to starting the metabolic study (mean serum LDL cholesterol 4.55±0.79 mmol/L prior to the metabolic phases). Subjects in the ad libitum group were recruited by advertisement from among university and hospital staff and students (mean serum LDL cholesterol 3.07±0.86 mmol/L prior to the ad libitum phases).

Both studies consisted of three phases, with wheat fiber provided at two levels of particle size and a low-wheat fiber control. Each study followed a randomized crossover design with all subjects participating in all three phases in the study. In the metabolic study, subjects were provided with three one-month metabolic diets that were identical, apart from the bread, which was the vehicle for wheat bran. Dietary periods were separated by minimum two-week washout periods during which subjects returned to their habitual diets. In the ad libitum study, subjects followed their habitual diets throughout. High-wheat fiber and low-wheat fiber breakfast cereals were provided for two-week periods separated by two-week unsupplemented washout periods. In both studies, fasting body weight was assessed at weekly intervals and fasting blood was obtained immediately prior to the start and at the end of each phase, with additional samples taken at week two in the metabolic study.

The studies were approved by the Ethics Review Committee of the University of Toronto.

Diets
The macronutrient profiles of the three dietary phases of the two studies as consumed are given in Table 1. In the metabolic study, the foods eaten in all three phases were identical apart from the bread. Complete diets were packed at a central location and delivered weekly by courier to the subjects’ homes at a time convenient to them. The metabolic diets followed a seven-day rotating menu plan. All food eaten was weighed and checked on each subject’s menu plan. If additional items were consumed, these were weighed and recorded on the menu plan. These menu plans were returned to the dietitian at weekly intervals to assess compliance, calculate dietary intake and make adjustments based on body weight measurements. In the ad libitum study, the basic diet was the subject’s self-selected diet that, during the treatment phase, also included the breakfast cereal provided. Breakfast cereals were weighed in daily portions and provided to subjects at weekly intervals during the treatment phases. Seven-day diet histories were obtained during the last week of each phase.


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  		Table 1. Calculated Dietary Intakes (Mean±SEM) for Treatment Periods of the Metabolic and Ad Libitum Studies

 
For the metabolic diet, energy intake was assessed for weight maintenance using standard tables [30], with adjustment for the subjects physical activity and pre-study seven-day diet history [31]. Diets were devised and dietary intakes calculated using a database in which the majority of foods had been analyzed in the laboratory by Association of Official Analytical Chemists methods for fat, protein [32] and fiber [33] with available carbohydrate by difference. The fatty acid composition was determined by gas chromatography [34]. The food composition tables of the US Department of Agriculture [35] and food labels were used for foods that had not been analyzed directly. This approach was also used for calculating the nutrient intakes in the ad libitum study.

High Fiber Breads and Breakfast Cereals
In the metabolic study, the bread contributed approximately 18% of the total energy intake for each subject. The macronutrient composition of the low-wheat fiber bread as a percent of energy was 1.4% protein, 4.2% fat, 94.3% available carbohydrate and provided 0.57 g fiber per MJ of diet (2.4 g/1000 kcals) or approximately 6 g fiber/d. The respective figures for the high-wheat fiber breads were 53.1% protein, 10.5% fat, 36.4% available carbohydrate with 2.37 g fiber per MJ of diet (9.9 g/1000 kcals) or approximately 25 g fiber/d. The increase in fiber in the high-wheat fiber breads was the result of addition of medium and ultra-fine particle size wheat brans (Parrheim Foods, Saskatoon, SK) with mean particle sizes of 758 µm and 50 µm, respectively, assessed by the rho-tap method [36]. The high level of added gluten in the high-wheat fiber breads raised the protein content and facilitated the creation of palatable breads. In the ad libitum study, the three breakfast cereals each provided 0.116 MJ (485 kcal/d), 16 g protein, 6 g fat and 93 g available carbohydrate on a daily basis. The low-wheat fiber breakfast cereal was a mixture of two flake cereals (Cornflakes, 60 g, and Special K, 58 g; The Kellogg Co, Battle Creek, MI) and contributed 2.4 g fiber daily. The coarse particle size wheat bran breakfast cereal was a high-wheat fiber flake (branflakes, 145 g/d) containing a mixture of coarse brans with a mean particle size of 1185 µm. The medium particle size wheat bran breakfast cereal was a mixture of Cornflakes (47 g/d) and wheat bran flakes (100 g/d) which contained a combination of ultra-fine and coarse particle size wheat bran in the ratio of 3:2 on the basis of grams of cereal fiber and had a mean particle size of 692 µm. Both high-wheat fiber breakfast cereals contributed 21.5 g fiber daily (i.e., 19.1 g/day more than the low-wheat fiber breakfast cereal). Corn oil (5 g/d) was also provided in separate containers with the low-wheat fiber breakfast cereal to match fat intake in the high-wheat-fiber breakfast cereals. Consumption of breakfast cereals was recorded on the diet record and oil containers and any uneaten breakfast cereals were returned at the end of the study to be weighed.

Lipid Analyses
Serum stored at -70°C was analysed according to the Lipid Research Clinics protocol [37] for total cholesterol, triglycerides and high-density lipoprotein (HDL) cholesterol, after dextran sulfate-magnesium chloride precipitation [38], in a single batch. Low-density lipoprotein cholesterol was calculated [39] on all but two subjects in the metabolic study who had a serum triglyceride concentration above 4.0 mmol/L on one or more occasions. Serum apolipoprotein A-I and B were measured by end-point nephelometry (Behring Diagnostics) [40].

Statistical Analysis
The results are expressed as mean±SEM. Treatment differences were assessed using the General Linear Model procedure (PROC GLM/SAS) with end-of-treatment value as the response variable and the following main effects: diet, gender, treatment order (sequence), diet-by-sequence, gender-by-sequence, a random term due to subject nested within gender-by-sequence interaction and baseline as the covariate [41]. In the case of simultaneous comparison of three means, the Student-Newman-Keuls (SNK) multiple range test option in PROC GLM/SAS [41] was applied to the data after establishment of a significant F-value by ANOVA. Where one treatment was compared with the other two, the CONTRAST statement in PROC GLM/SAS was used [41]. Paired two-tailed Student’s t-test was employed to confirm a lack of difference between two treatments.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 
In both studies, compliance was satisfactory and similar for the three treatments. On the metabolic study, subjects consumed (mean±SD) 94.7±8.4% of the dietary energy provided on the low-wheat-fiber diet. The respective figures for the coarse and the fine wheat-fiber diets were 93.2±10.9% and 90.4±9.7% respectively. There were no significant differences in weight change between treatments. At the end of the metabolic study, (mean±SEM) body weights were 71.6±2.3 kg, low-wheat-fiber diet, 71.7±2.4 kg, medium-wheat-fiber diet and 71.9±2.3 kg, ultra-fine wheat fiber diet. In the ad libitum study, all the breakfast cereals were reported as consumed. No differences in weight change or final body weight were seen between treatments in the ad libitum study (69.9±2.5 kg, low-wheat-fiber diet, 70.0±2.4 kg, coarse-wheat-fiber diet and 69.9±2.4 kg, medium-wheat-fiber diet).

No significant differences were seen in serum lipids or lipoproteins in either study related to wheat bran, independent of wheat bran particle size or level of gluten intake (Tables 2 and 3). The exception was a lower triglyceride level (13±4%, p=0.005, CONTRAST statement in PROC GLM/SAS [41]) on the metabolic study associated with the higher gluten intake on both fine- and coarse-wheat-fiber diets by comparison with the low-gluten low-wheat-fiber diet (Table 2, Figure 1). No difference was seen in triglyceride levels on the ad libitum study where gluten levels were similar across low-wheat-fiber and high-wheat-fiber phases (Table 3, Figure 1). The triglyceride reduction therefore appears to relate to the increased gluten levels, but not to the wheat fiber.


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  		Table 2. Metabolic Study: Body Weight, Blood Lipid and Blood Pressure Data (Mean+SEM) at the End of the Treatment Periods (n=24)

 

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  		Table 3. Ad Libitum Study: Body Weight, Blood Lipid and Blood Pressure Data (Mean+SEM) at the End of the Treatment Periods (n=24)

 


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  		Fig. 1. Difference from control in serum triglyceride concentration on the two wheat bran treatments, high-gluten (metabolic, n=24) and normal-gluten (ad libitum, n=24). In the metabolic study, the high-gluten high-wheat fiber treatments were associated with a mean (±SEM) reduction of 13±4% (p=0.005) in serum triglycerides which was not seen with the normal-gluten high-wheat fiber treatments in the ad libitum study (CONTRAST statement in PROC GLM/SAS [41]).

 

   DISCUSSION
 
Wheat bran had no effect on serum cholesterol despite differences in particle size and increased levels of wheat gluten. It is therefore unlikely that the protective effect of insoluble cereal fiber in cardiovascular disease [1,2] relates to lower serum cholesterol.

While it has been accepted that wheat bran has no effect on serum lipids [42], at least twelve studies over the last three decades have suggested that wheat fiber may lower total and LDL cholesterol [9–14], very-low-density lipoprotein (VLDL) cholesterol [8], raise HDL cholesterol [15,16] or lower serum triglycerides [11,12,17–19]. The question therefore arose as to whether these results related to differences in particle size of the wheat bran or the associated wheat gluten and whether these factors may also have been important in the context of the reduced cardiovascular-disease risk associated with wheat fiber [1,2]. Furthermore, it is possible that the lipid changes were related to other differences in the diets not associated with wheat bran.

Almost no studies on wheat bran that have assessed the effect on serum lipids have reported the particle size of the wheat bran used. Nevertheless, dietary fibers have been shown to bind bile acids in vitro [20], including lignin [43], which constitutes 3% of the weight of wheat bran [36,44]. Lignin administration has been shown to lower serum cholesterol [45], and it is possible that the more finely ground wheat bran with a greater surface area would have bound more bile acids and so reduced serum cholesterol. However, in the present study, use of a very wide range of wheat-bran particle sizes, from ultra fine to coarse, had no effect on serum cholesterol, suggesting that particle size is therefore unlikely to provide an explanation for the differences in blood lipid responses to wheat bran reported in the literature [8–19].

Fourteen percent of the weight of wheat bran or 27% of its energy content is protein [46]. Studies which increase wheat bran intake may therefore increase protein intake as wheat protein. As a result, increased intake of cereal fiber in wheat bran products is also likely to increase wheat-protein intake. Whole meal bread has 17.1% of energy as protein versus 14.3% for white bread [46]. Vegetable (soy) protein has been shown to reduce atherosclerosis in rabbits [47], and high-protein, high-fiber intakes increase bile-acid losses in humans [48]. We therefore wondered whether the interaction of fiber with higher vegetable-protein (wheat gluten) intake might have been responsible for the lipid-lowering effect of wheat bran in studies where this was reported. However, even in the presence of high-gluten intake, there was no evidence to suggest an effect from wheat bran in lowering serum cholesterol.

Nevertheless, serum triglycerides were reduced in both high-wheat-fiber phases of the metabolic study. No such effect was seen during the high-wheat-fiber phases of the ad libitum study, and for this reason it is likely that the triglyceride reduction was related to substitution of wheat gluten for carbohydrate in the high-wheat-fiber phases of the metabolic study. The divergent effects on serum triglyceride seen in the metabolic and the ad libitum studies could be due to a difference in subjects as well as diets. For instance, wheat fiber may have an effect in an insulin-resistant population, but not in an insulin-sensitive group. In support of this, cereal fiber has been shown to be protective against the development of type 2 diabetes [49,50]. In an attempt to resolve this issue we determined the association of the treatment effect with the subject’s mean baseline triglyceride, BMI and age. The treatment effect was defined as the difference in serum triglyceride between the control and the mean of fine and coarse final triglyceride values. The hyperlipidemic and normolipidemic subject groups were assessed separately. We have also repeated this analysis on the treatment differences expressed as a percentage of the four-week control value. A significant association was seen between age in the hypertriglyceridemic group (older subjects) and percentage-treatment difference in serum triglyceride (r=0.41, P=0.046). To resolve the issue, studies are required of insulin-resistant subjects comparing high-cereal-fiber diets with and without increased gluten intakes and studies of low-fiber diets, also with and without gluten.

In type 2 diabetes, an exchange of 15% of total energy as carbohydrate for olive oil resulted in a 24% reduction in serum triglycerides [51]. In our metabolic study, an exchange of approximately 10% of daily energy from carbohydrate to wheat gluten resulted in a 13% mean reduction in serum triglycerides (Figure 1), an effect similar to that of olive oil. It is possible that the reduction in triglyceride was the result of the lower level of carbohydrate in the diet and that substituting other caloric sources for carbohydrate would result in a similar effect. For example, such an effect may be seen with substitution of saturated fat for carbohydrate, but in this instance LDL cholesterol concentrations will also be increased. Nevertheless, while a number of studies have demonstrated that an increased proportion of fat, especially monounsaturated fat reduces serum triglyceride levels [51–54], no studies have assessed the effect of wheat gluten.

The protective effect of wheat bran in terms of cardiovascular disease is difficult to ascribe to reductions in serum lipids or blood pressure, nor have antioxidant properties been ascribed to wheat bran. A possible effect, however, may be that of wheat bran on clotting factors. Earlier studies have been divided respecting this action of dietary fiber [26,27,55]; however, a recent report from the National Heart Lung and Blood Institute Family Heart Study documents an inverse association between dietary fiber and PAI-1; this finding may provide a link between cardiovascular risk reduction and increased fiber consumption [56].


   CONCLUSION
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 CONCLUSION
ACKNOWLEDGMENTS
 REFERENCES
 
We conclude that neither reduced particle size nor additional gluten resulted in a cholesterol-lowering effect with respect to wheat bran. The protective role of wheat fiber in cardiovascular disease must be mediated by some mechanism other than serum-cholesterol reduction. It is possible that higher wheat-fiber diets may also be associated with increased cereal protein and that this may result in lower serum triglycerides. However, a reduction in cardiovascular-disease risk associated with lower triglycerides, as opposed to changes in the lipoproteins, apolipoproteins or their ratios, although of much current interest, is less clear.


   ACKNOWLEDGMENTS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 CONCLUSION
 ACKNOWLEDGMENTS
REFERENCES
 
The study was funded by The University-Industry Research Partnership Program of the Natural Sciences and Engineering Research Council of Canada and The Kellogg Company, Toronto, Ontario, Canada.

The authors wish to thank Kellogg Canada Inc, Etobicoke, ON, Parrheim Foods Ltd, Saskatoon, SK, Loblaw Brands Ltd, Toronto, ON, Western Creamery Inc, Downsview, ON, Bestfoods Canada Inc, Etobicoke, ON, and Kraft Canada Inc, Don Mills, ON, for their generous donations of foods used in this study. The authors would also like to extend sincere thanks to Ken Fulcher of Parrheim Foods Ltd, Kathy Galbraith of Natural Temptations Bakery, Burlington, ON, Beth Olson of The Kellogg Company, Battle Creek, MI, Robert Chenaux and Larry Griffin of Loblaw Brands Ltd, Jim Smith of Western Creamery Inc, Jeanne D’Arc Charron of Bestfoods Canada Inc, Dayle Sunohara of Kraft Canada Inc, and Cheri Graves of Cedar Lake-MGM Foods, Cedar Lake, MI, for their assistance on this project. Thanks are also extended to Yu-Min Li, Renato Novokmet and George Koumbridis who provided excellent technical assistance.

Received August 1, 1998. Accepted October 1, 1998.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 

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