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The Effect of Wheat Bran Particle Size on Laxation and Colonic Fermentation

Clinical Nutrition and Risk Factor Modification Center (D.J.A.J., C.W.C.K., L.S.A.A., V.V., B.L., C.C.M., T.P., D.F., H.S., E.V.) St. Michael’s Hospital
Department of Nutritional Sciences (D.J.A.J., C.W.C.K., L.S.A.A., V.V., Y.-M.L., E.V.) University of Toronto, Toronto, Ontario
The Kellogg Company, Battle Creek, Michigan (V.F.)

Address reprint requests to: David JA Jenkins, Clinical Nutrition and Risk Factor Modification Center, St. Michael’s Hospital, 61 Queen St. East, Toronto, Ontario, CANADA, M5C 2T2.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
Objective: Due to perceived inferior fecal bulking ability, finely ground wheat bran is not recommended for treatment of colonic disorders, despite possible short chain fatty acid generation with potential benefits for colonic mucosal health. We therefore tested the effects of very fine particle size wheat bran on colonic function.

Methods: Two studies, each with three phases, were undertaken in healthy subjects in a randomized crossover design. In one study (metabolic, n=23) subjects took three diets containing either an additional 19 g/d dietary fiber with mean particle size (MPS) 50µm or 758µm in bread or a control low fiber bread. In the other study where the supplement was provided as a breakfast cereal (ad libitum, n=24) the respective wheat bran MPS were 692µm and 1158µm and the control was low fiber. Fecal collections were obtained during the last week of each diet. In the metabolic study, fecal short chain fatty acids were measured and 12-hour breath gas collections obtained.

Results: In both studies, wheat bran supplements significantly increased fecal bulk compared to the control (p<0.004), with no significant differences between brans of different particle size and no differences in fecal water content. However, higher fecal butyrate concentrations (p<0.007), butyrate output and breath CH₄ levels (p=0.025) were seen on the low MPS wheat bran compared to the other two treatments, suggesting increased bacterial fermentation.

Conclusions: Fine MPS wheat bran is an effective fecal bulking agent and may have added advantages if increased butyrate concentrations promote colonic mucosal integrity.

Key words: wheat bran, dietary fiber, short chain fatty acids, butyrate, methane, functional foods

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
Despite the broad range of potential health implications attributed to wheat bran, the ideal particle size in which it should be fed is still not clearly defined. Wheat fiber in bread and breakfast cereals is one of the major fiber sources in the Western diet [1]. Medium to coarse ground wheat brans have been the food industry standard since the early 1900’s. Consumption of wheat bran, a largely insoluble fiber source, and other insoluble cereal fibers has been advocated for the treatment of colonic disorders [2–4] and has been associated with reduced risk for major chronic diseases including heart disease [5,6], diabetes [7,8] and colon cancer [9,10]. Wheat bran has been shown to be one of the most effective fiber laxatives on a per gram basis [11] with a linear dose response [12]. However, there is a scientific belief [13–16], reflected in official guidelines [17,18], that only coarse or medium particle size wheat brans, as opposed to fine wheat bran, should be used for laxative purposes, despite the potential superior palatability of finely ground wheat bran [16]. Furthermore, compared to coarse wheat bran, finely ground wheat bran may be more readily fermented [19]. It may therefore provide additional benefits in terms of colonic mucosal health through increased short chain fatty acid synthesis [20–24] and bile acid binding[25,26]. In view of the importance of wheat bran as a fiber source in the human diet, we felt that the ideal form in which this cereal fiber is fed warranted further assessment.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
A total of 47 healthy men and women took part in two studies. The metabolic study involved 15 men and eight women with a mean±SD age of 58±9 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). The ad libitum study included 12 men and 12 women with a mean age of 36±12 years (range 17 to 57 years) and BMI of 24.5±2.7 kg/m² (range 18.4 to 29.0 kg/m²). No subject had a history of gastrointestinal disease, and none was taking laxatives. None had clinical or biochemical evidence of liver disease, diabetes or thyroid dysfunction. Subjects for the metabolic study were recruited with raised LDL-cholesterol levels (>4.1 mmol/L) [27] as part of our assessment of wheat bran on blood lipids to be reported elsewhere (mean LDL-cholesterol concentration 4.55 mmol/L). Both studies consisted of three phases, wheat fiber given at two levels of mean particle size and a control phase. Each study followed a randomized crossover design with all subjects participating in all three phases of 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. Complete diets designed for weight maintenance [28] were prepackaged and delivered to subjects’ homes by courier at weekly intervals. Dietary treatments were separated by a minimum two-week washout period where subjects returned to their habitual diets. In the ad libitum study, subjects followed their habitual diets throughout the three two-week treatment periods during which they were provided with high and low-fiber breakfast cereals. Again, treatment periods were separated by two-week washout periods. In both studies, fasting body weight was assessed at weekly intervals, and three-day fecal collections in the metabolic study and four-day fecal collections in the ad libitum study were obtained during the last week of each phase [28]. Subjects were provided by courier to their homes with fecal collection kits consisting of under-seat lavatory frames, plastic bags and a supply of frozen CO₂ in an approximately two cubic foot capacity polystyrene storage container. Prior to defecation plastic bags were suspended from the under-seat frames. After defecation the plastic bag was removed, sealed with an elastic band, and an adhesive label with the subject’s name, date and time was placed on the bag. The bag was then stored immediately on frozen CO₂ in the polystyrene container prior to shipment to the laboratory by courier. Separate 5–10 g fecal samples were also obtained in the metabolic study by 21 subjects for short chain fatty acid (SCFA) measurement after suction biopsy of the freshly passed feces during the three day fecal collection using a modified plastic syringe. These samples (n=21 subjects) were placed in 25 mL plastic screw cap containers prior to analysis. During the fecal collection period subjects kept a diary of times of defecation, and this was checked against the collections delivered. In addition, in the metabolic study subjects obtained end expiratory breath samples collected in plastic syringes with two-way taps using a modified Haldane-Priestly tube (n=21 subjects), where possible on the last day of the fecal collection [29]. The baseline sample was obtained immediately before breakfast, and further samples were obtained at hourly intervals for 12 hours with lunch and dinner taken at approximately the fifth and eleventh hour respectively. The foods eaten were part of the subject’s regular metabolic diet for that phase with one third of the test bread eaten at each meal. The aim of the breath gas collection was to obtain a mean breath H₂ and CH₄ value representing one day for each phase. Accordingly subjects had been instructed on how to collect their own end expiratory samples. All subjects were provided with self-tarring electronic scales. Throughout the metabolic study subjects were asked to check all food items eaten against the day’s menu provided, noting the weights of any items not consumed, and to return these forms to the dietitian for discussion at the end of each week. In the ad libitum study, subjects were instructed how to complete a weighed seven-day food record, to commence recording during the last week of each phase on the forms provided and to return these forms to the dietitian on completion for discussion and coding. During the week of the fecal collection period, subjects filled out a daily symptom diary, noting the times of all feces passed together with any abdominal discomfort or flatulence using a seven-point semantic scale [30]. The studies were approved by the Ethics Review Committee of the University of Toronto.

Diets and High Fiber Foods
The calculated macronutrient profiles [28] of the three dietary phases of the two studies as consumed are presented in Table 1. On the metabolic study, the foods eaten in all three phases were identical apart from the bread, which contributed approximately 18% of the subjects’ energy intake. The background diets were low-saturated fat, lacto-vegetarian diets. In the ad libitum study, the basic diet was the subject’s self-selected diet, which was supplemented with the test breakfast cereals. In the one-month metabolic diets, subjects took on average an additional 19 to 20 g/d dietary fiber in breads as very fine (mean particle size [MPS] 50 µm) or medium (MPS 758 µm) wheat bran, or a low-fiber control bread. In the two-week ad libitum diets, subjects took an additional 19 g/d dietary fiber in breakfast cereals containing either a mixture of very fine and coarse wheat bran, giving a medium mean particle size wheat bran (MPS 692 µm), or coarse wheat bran alone (MPS 1185 µm), or a low-fiber control cereal. The bran breads contained a high level of gluten (23.9% of baked weight) to facilitate creation of a palatable high wheat fiber bread.

Statistical Analysis
The results are expressed as mean±SE. 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 and a random term due to subject nested within the gender-by-sequence interaction [38]. In the case of simultaneous comparison of three means, the Student Newman Keuls (SNK) multiple range test option in PROC GLM/SAS [38] 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 [38]. This approach was used for the indices of fermentation, SCFA and breath gases, where fine wheat bran was predicted to enhance colonic fermentation by comparison with the other two phases. Paired two-tailed Student’s t test was employed to confirm a lack of difference between two treatments. The strength of linear associations between various factors was assessed using Pearson product-moment correlation (PROC CORR/SAS) [38]. Based on previous studies we determined that 24 subjects were required to detect a significant 24 g/d difference in fecal output (assuming an effect SD of 40 g/d, =0.8, ß=0.05). Due to possibly greater variability in dietary intake we used four-day fecal collections on the ad libitum study as opposed to three-day collections on the metabolic study. Nevertheless, the ad libitum study fecal data had a smaller SD of effect than the metabolic data, although in both cases the subject numbers were greater than those required to detect a significant treatment effect (n=16 and n=22, respectively) [38].

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
In the metabolic study, compliance was similar for the three supplements. On the low-fiber control phase of the metabolic study, subjects consumed (mean±SD) 94.7±8.4% of the dietary calories provided. The figures for the medium particle size and fine wheat bran diets were 93.2±10.9% and 90.4±9.7%, respectively. There were no significant differences in body weight change between treatments. At the end of the metabolic study, body weights were (mean±SE) 71.4±2.4 kg, low-fiber control; 71.4±2.5 kg, medium particle size wheat bran; and 71.7±2.4 kg, fine wheat bran. In the ad libitum study, all supplements were reported as consumed. Again, no differences in weight change or final body weight were seen between phases (69.9±2.5 kg, low-fiber control; 70.0±2.4 kg, coarse wheat bran; 69.9±2.4 kg medium particle size wheat bran).

In both studies the fecal output on the wheat bran treatments were significantly different from their respective controls (p<0.05) with no significant difference between the brans regardless of particle size (Fig. 1). The mean fecal weights in the metabolic study were 211±23 g/d low-fiber control; 279±23 g/d medium particle size wheat bran; and 268±23 g/d fine wheat bran. Similarly, in the ad libitum study the mean fecal weights were 141±12 g/d, low-fiber control; 182±11 g/d, coarse wheat bran; and 187±14 g/d, medium particle size wheat bran. The increase from control in fecal output on the larger mean particle size wheat bran related significantly to the increase on the finer mean particle size wheat bran (metabolic study, r=0.68, p<0.001; ad libitum study, r=0.68, p<0.001). Furthermore, there was no difference in fecal water concentration in either the metabolic study (78±1%, low-fiber control; medium particle size, 79±1%; fine, 78±1%) or the ad libitum study (76±1%, low-fiber control; coarse, 77±1%; medium particle size, 77±1%).

View larger version (21K): [in this window] [in a new window]   Fig. 1. Individual and mean (±SE) differences in fecal bulk from the low-fiber control for the coarse and fine wheat brans on both the metabolic (n=23) and ad libitum (n=24) studies. Compared with the low-fiber control, the fine and medium particle size wheat brans increased mean daily fecal output in the metabolic study (58±21 g/d, p=0.012 and 68±25 g/d, p=0.011, respectively), and a similar increase was seen with the medium and coarse wheat brans in the ad libitum study (45±14 g/d, p=0.003 and 41±12 g/d p=0.002, respectively).

View larger version (17K): [in this window] [in a new window]   Fig. 2. Individual and mean (±SE) percentage differences in fecal butyrate concentrations for fine versus medium particle size and fine versus low-fiber control treatments on the metabolic study (n=21). Fine wheat bran increased mean fecal butyrate concentrations by 34±13% (p=0.013) compared with the low-fiber control and 33±13% (p=0.023) compared with medium particle size wheat bran.

View larger version (16K): [in this window] [in a new window]   Fig. 3. Breath methane profile (12 hour) on the metabolic studies (n=21). Fine wheat bran increased mean daily methane concentration when the data from the medium particle size wheat bran and low-fiber control were combined (p=0.025 CONTRAST statement PROC GLM/SAS) [38].

	DISCUSSION

 
Wheat bran is one of the most effective dietary fiber fecal bulking agents [11]. Despite a very substantial reduction in mean particle size, fine wheat bran remained an effective laxative. Furthermore, fine wheat bran increased fecal butyrate concentrations and raised breath CH₄ levels indicating in-creased colonic bacterial fermentation. In view of the lack of significant difference in fecal bulking and the possible advantage of increased fecal butyrate concentrations for mucosal health [39], current advice against using fine wheat bran in favor of coarse as a public health measure and in the treatment of colonic disorders may warrant reassessment [11,13–15,17,18].

Over the last 60 years, most [13–16] but not all [40] studies have indicated reduced fecal bulking when wheat bran particle size was reduced. Studies analyzing similar particle sizes to those used in our metabolic study demonstrated that, relative to control, fine wheat bran had 76% of the fecal bulking effect compared to coarse particle size wheat bran [16]. This figure was similar to the 84% observed in our study. Nevertheless, as with our studies, the fine wheat bran in all reports still resulted in a significant increase in fecal bulk [13–16,40,41]. It is possible that the higher protein intakes on the wheat fiber phases of the metabolic study may have altered the results. However in a previous study a similar increase in protein intake had no effect on fecal bulk or the laxative effect of wheat fiber [42].

Increased water holding capacity of coarse wheat bran has been proposed as an explanation for its greater fecal bulking action [13,15]. However, in common with a number of other studies, we failed to find a significant difference in the water content of feces after wheat bran consumption, regardless of particle size [40,43].

This is the first study we are aware of to assess the effect of particle size on fecal SCFA concentrations or breath gases as indicators of colonic fermentation. Dietary fibers are fermented in the colon to short chain fatty acids. Wheat fiber is one of the less well fermented fiber sources [44]. It is nevertheless recognized to be a substrate for colonic microflora [45]. A report on the direct measurement of dietary fiber in the feces indicated that only 6% of the cellulosic fraction was fermented in the colon after feeding coarse wheat bran as opposed to 23% after fine wheat bran [13]. Slow colonic fermentation, such as is associated with bacterial breakdown of resistant starch, may be accompanied by increased butyrate synthesis [46,47]. The slow fermentation of fine wheat bran along the length of the colon may also be the explanation for the higher butyrate concentration and daily fecal output seen in our study. Butyrate is a preferred substrate for colonic mucosal cells, and, as a component of SCFA enema, it has been used to treat diversion colitis [20]. Trials have also been undertaken of butyrate use in ulcerative colitis with some studies showing promise [21] and others not [22]. It is possible that a sustained slow release of butyrate may be of greater benefit than intermittent rectal administration [21], in which case the sustained intra-luminal fermentation of fine wheat bran may provide a useful source of butyrate in ulcerative colitis.

Butyrate is also considered to have anti-neoplastic properties, possibly through maintaining acetylation of DNA on the nuclear histone [23]. A reduced proportion of fecal butyrate has been associated with an increased likelihood of a diagnosis of colon cancer in subjects investigated for colonic disease [24].

	CONCLUSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
We conclude that fine wheat bran, despite being somewhat less effective than larger particle size wheat bran, is still a very effective fecal bulking agent and likely to be of similar use in the treatment of constipation and related disorders. In addition to the potential increased bulk with dilution of bile acids and other potential carcinogens, the ability of fine wheat bran to increase butyrate levels might also contribute to colonic mucosal health. Finally, its increased fermentability will liberate minerals from the bran for colonic absorption in the presence of increased short chain fatty acid synthesis [48], possibly enhancing the effectiveness of fine wheat bran in reducing risk factors for the development of a number of chronic diseases. However, speculations on these possible benefits of fine wheat bran remain to be tested in relevant long-term trials, for example, those involving individuals who are at increased risk for colonic disease. Nevertheless, these data support the use of fine wheat bran to create palatable high fiber foods in which the form of the wheat bran may confer additional health advantages.

	ACKNOWLEDGMENTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
Funded by the University-Industry Research Partnership Program of the Natural Sciences and Engineering Research Council of Canada and The Kellogg Company, Toronto, Canada.

The authors wish to thank Kellogg Canada Inc, Etobicoke, ON; Parrheim Foods Ltd, Saskatoon, SK; Loblaw Brands Ltd, Toronto, ON; Westhill Dairy Inc, Downsview, ON; Bestfoods Canada Inc, Etobicoke, ON; and Kraft Canada Inc, Don Mills, ON, for the generous donation 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 Westhill Dairy Inc, Jeanne D’Arc Charron of Bestfoods Canada Inc, and Dayle Sunohara of Kraft Canada Inc, for their assistance on this project. Thanks are also extended to Renato Novokmet, George Koumbridis and Nalini Irani who provided excellent technical assistance.

Received October 1, 1998. Accepted December 1, 1998.

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TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 

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