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Journal of the American College of Nutrition, Vol. 17, No. 6, 609-616 (1998)
Published by the American College of Nutrition

Physiological Effects of Resistant Starches on Fecal Bulk, Short Chain Fatty Acids, Blood Lipids and Glycemic Index

David J.A. Jenkins, MD, FACN, Vladimir Vuksan, PhD, Cyril W.C. Kendall, PhD, Pierre Würsch, PhD, Roger Jeffcoat, PhD, Susan Waring, BSc, Christine C. Mehling, RD, Edward Vidgen, BSc, Livia S.A. Augustin, MSc and Evelyn Wong, MSc

Department of Nutritional Sciences (D.J.A.J., V.V., C.W.C.K., C.C.M., E.V., L.S.A.A., E.W.), Faculty of Medicine, University of Toronto and the Clinical Nutrition and Risk Factor Modification Center, St Michael’s Hospital, Toronto, Ontario
Nestle Research Center (P.W.), Lausanne, Switzerland
National Starch and Chemical Company (R.J., S.W.), Bridgewater, New Jersey

Address reprint requests to: David JA Jenkins, MD, PhD, FACN, St. Michael’s Hospital, 61 Queen Street East, 6th Floor, Toronto, Ontario, CANADA M5C 2T2


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Objective: To assess the effects on fecal bulking, fecal short chain fatty acid (SCFA) production, blood lipids and glycemic indices of two different forms of resistant starch (RS2 and RS3) from a high-amylose cornstarch.

Methods: Twenty-four healthy subjects (12 men; 12 women) consumed four supplements taken for 2 weeks in random order separated by 2-week washout periods. The supplements were a low-fiber (control) and supplements providing an additional 30 g dietary fiber as wheat bran (high-fiber control) or the equivalent amount of resistant starch analyzed gravimetrically as dietary fiber from RS2 or RS3. Four-day fecal collections and 12-hour breath gas collections were obtained at the end of each period. Fasting blood was taken at the beginning and end of each period. Glycemic indices of supplements were also assessed.

Results: The wheat bran supplement increased fecal bulk 96±14 g/day compared with the low-fiber control (p<0.001) with the mean for both resistant starches also being greater (22±8 g/day) than the low-fiber control (p=0.013). On the resistant starch phases, the mean fecal butyrate:SCFA ratio, which has been suggested to have positive implications for colonic health, was significantly above the low-fiber control by 31±14% (p=0.035). Resistant starches did not alter serum lipids, urea or breath H2 or CH4. No significant differences in glycemic index were seen between the RS and control supplements.

Conclusion: The potential physiological benefits of the resistant starches studied appear to relate to colonic health in terms of effects on fecal bulk and SCFA metabolism.

Key words: resistant starch, fecal bulk, blood lipids, glycemic index, colon, short chain fatty acids


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
SUBJECTS AND METHODS
 RESULTS
 CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Health benefits have been ascribed to starches and starchy foods that are either relatively or absolutely resistant to digestion in the small intestine [1–5]. A wide range of factors determine the rate of digestion of starch in foods, including the structure of the starch itself, the physical characteristics of the food and the presence of other nutrient and antinutrient components [6–8]. The rate of small intestinal digestion of the starch determines the glycemic index of the food. Slowly digested or low glycemic index foods have been associated with improved diabetes control [2,9–11], reductions in blood lipids [12–14] and, in the longer term, may even decrease risk for the development of diabetes [3,4]. Starches which escape small intestinal absorption may contribute to fecal bulk [15,16], alter the colonic microflora, increase fecal nitrogen losses and short chain fatty acid synthesis, especially butyrate [17], and possibly reduce the risk of colon cancer [18]. Starches, which are resistant to amylolytic digestion, contribute to the dietary fiber figure in the AOAC gravimetric determination of dietary fiber [19]. These starches include granular starches which have been termed RS2, as well as crystalline retrograded starches which have been termed RS3 [20].

We have selected two sources of resistant cornstarch to compare with the effect of wheat bran fed in feeding studies where supplements were fed on the basis of ‘dietary fiber’ equivalency. One starch was a high amylose granular resistant cornstarch, RS2; and the other was a high amylose non-granular, dispersed and retrograded resistant cornstarch, RS3 [20]. Our aim was to compare the effects of these two resistant starches with the effect of wheat bran in areas related to colonic function, glycemic control and serum lipid metabolism.


   SUBJECTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
RESULTS
 CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Subjects
Twenty-four healthy subjects (12 men, 12 pre-menopausal women) were recruited from university and hospital staff and students. Their mean (±SE) age was 33±2 years (range 22 to 53 years) and body mass index 23.7±0.6 kg/m2 (range 19.4 to 34.2 kg/m2). Subjects were normolipidemic and none had a history of diabetes, renal or hepatic disease or were taking medications. The majority of subjects had participated in at least one previous study using the same protocol and were familiar with the requirements of the study including fecal, urine and expired breath gas collections. A further group of 14 subjects (seven men and seven women) age 33±3 years, body mass index 22.7±0.7 kg/m2 took part in the glycemic index testing of the supplements (cereals, n=10; muffins, n=11).

The study was approved by the Ethics Committees of the University of Toronto and St. Michael’s Hospital. Informed consent was obtained from all participants.

Protocol
The study followed a crossover design where subjects received four treatments in random order. Treatment periods were 2 weeks in duration separated by 2-week washout periods. During treatment periods, subjects received supplements of breakfast cereals and muffins, contributing on average approximately 30% of the mean recorded energy intake for the group (Tables 1 and 2). The supplements all had the same macronutrient profile and were the vehicles for providing the test components for the four treatments: low-fiber control, wheat bran (high-fiber control), granular high-amylose starch (RS2) and a retrograded non-granular high-amylose starch (RS3). This RS3 was produced by digesting the {alpha}1–6 branch points (the amylopectin component of the starch) after cooking the starch to destroy the starch granules by dispersing the starch polymers. The linear {alpha}1–4 linked starch chains are then allowed to retrograde by forming close bundles of hydrogen bonded starch chains which are highly resistant to digestion. Subjects recorded their level of satiety on day 10 of each treatment phase using a 7-point bipolar scale (-3 extremely hungry, 0 neutral, +3 fully satiated) [21–23].


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  		Table 1. Calculated Daily Dietary Intakes* (Mean±SE) for Week 2 of Treatment Periods (n=24)

 

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  		Table 2. Composition and Daily Contribution of Supplements as Analyzed

 
Subjects were weighed and 12-hour fasting blood samples obtained in the morning prior to commencing each phase and at the end of week 2. Seven-day diet histories were obtained prior to the start of the study and for the last week of each phase. In addition, at the end of each phase, 12-hour expired air and 4-day fecal collections were obtained. End expiratory air was sampled hourly over 12 hours using Haldane-Priestly tubes [24]. Breath samples were aspirated into 10 mL plastic syringes attached to three-way taps. Samples were analyzed within 24 hours or stored additionally at -20°C for a maximum of 2 days prior to analysis. Subjects were provided with underseat lavatory frames and plastic bags for fecal collections. All samples passed were recorded and the date and time written on adhesive labels and placed on the plastic bags which were stored on frozen CO2 in polystyrene containers. Immediately on passing feces, 5 mL core biopsies were obtained by subjects for short chain fatty acid analysis and placed on frozen CO2 in plain plastic tubes. All samples were delivered to the laboratory on completion of collections. Serum and fecal samples for SCFA analysis were stored at -70°C prior to analysis.

In addition, 50 g available carbohydrate portions of the cereal and muffin supplements were fed individually after overnight fasts to a separate group of subjects to establish their glycemic indices. Care was taken to ensure that 50 g available carbohydrate portions were used for glycemic index testing for each supplement despite the fact that small differences existed between supplements in the total available carbohydrate fed on a daily basis in the two-week studies (Table 2). Supplements were taken by subjects in random order on separate days. Fifty g available carbohydrate portions of white bread were used as the standard and fed on at least three occasions during the glycemic index testing. Supplements were eaten over a 10-minute period together with water, black tea or coffee [25]. The beverage type and amount were selected by the subject and were maintained throughout the glycemic index testing. Finger prick blood samples were obtained with Autolet lancets (Owen Munford, Oxford) fasting and 15, 30, 45, 60, 90 and 120 minutes after starting to eat. Capillary blood, approximately 100 µL, was collected into fluoro-oxalate tubes, placed on ice and later stored at -20°C prior to analysis within 3 days [25].

Dietary Supplements
The cereals were provided in 59 to 83 g portions, depending on the supplement, to be consumed daily together with four muffins having total mean weight of 204 to 264 g (Table 2). The aim was to provide 30 g of total dietary fiber (TDF) daily as wheat bran to compare with 30 g resistant starch analyzed gravimetrically as dietary fiber from RS2 (44.6 g of resistant starch analyzed as dietary fiber per 100 g of total starch) and RS3 (32.8 g TDF equivalency per 100 g of total starch) analyzed by the gravimeter AOAC method [19]. In other respects, the supplements had a similar macronutrient profile and were designed to deliver a similar daily energy intake (Table 2). The cereals were manufactured in one batch, while the muffins were baked in two batches, prior to the start and approximately half way through the study. Muffins were stored at -20°C prior to use. Supplements were analyzed on repeated occasions during the course of each phase. Muffins for resistant starch analysis were freeze-dried using liquid nitrogen both after being freshly baked and after freezing and thawing to simulate the manner in which they would have been stored by subjects prior to consumption. The method of storage did not alter the results. Daily resistant starch intakes provided by the supplements are given in Table 2.

Analyses
Frozen serum stored at -70°C was analyzed at the end of the study so that all samples from a given individual were analyzed in the same batch. Serum was analyzed for total cholesterol, triacylglycerol and high-density lipoprotein (HDL) cholesterol after dextran sulphate and magnesium chloride precipitation, by techniques of the Lipid Research Clinics [26]. Low-density lipoprotein (LDL) cholesterol was calculated [27]. Serum apolipoprotein A1 and B were measured by an ELISA technique [28]. Frozen serum was also analyzed for creatinine and urea in the routine clinical chemistry laboratory using standard methods for Kodak Ektachem analyzers (Eastman Kodak, Rochester, NY).

Breath H2 and CH4 were analyzed using a Quintron gas chomatogram (Quintron Microanalyzer Model DP, Quintron Company, Milwaukee, WI).

Four-day fecal samples, stored at -20°C, were weighed to the nearest g. Fecal short chain fatty acids (SCFA) were measured on separate frozen 5 g aliquots of whole feces obtained at the time of the 4-day collection and stored at -70°C. Short chain fatty acids were determined by high-pressure liquid chromatography (HPLC) [29] after vacuum distillation [30].

Capillary blood samples from glycemic index testing were analyzed using a YSI glucose analyzer (YSI 2300, Yellow Spring Instruments, Yellow Springs, OH).

Supplements were analyzed for macronutrients and dietary fiber by AOAC methods [19,31]. Samples were analyzed for resistant starch by the method of Goni et al [32]. Diet records were assessed using a database derived from USDA data [33].

Statistical Analysis
The results are expressed as mean±SE. Glycemic index was calculated as the blood glucose area above baseline for the food expressed as a percentage of the corresponding mean blood glucose area for the three white bread tests taken by that subject [25].

The differences between the treatment means, whether changes or 2-week values, unless stated otherwise, were assessed by Student-Newman-Keuls multiple range test in SAS [34]. Where baseline levels were measured (e.g., serum lipids), they were included in the model as a covariate. In the case of paired data for two treatments, student’s t-test (two-tailed) was also used to test the difference. The strength of linear associations between various factors was assessed using Pearson product-moment correlations.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 
The macronutrient profiles of diets during all four treatments, expressed as a percentage of energy intakes, were similar (Table 1). No significant differences were seen in body weight changes between treatments. Compliance was good as 98.7±0.5% of cereal supplements and 96.0±1.2% of muffin supplements were recorded as consumed with no significant differences between treatments. Complete satiety scores for the four treatments were recorded by 18 subjects. Both the RS2 and RS3 supplements produced significantly greater satiety scores (1.4±0.2 and 1.2±0.3, respectively, p<0.05) than the low-fiber control (0.6±0.2). The high-fiber control (1.1±0.2) had an intermediate value for satiety which was not statistically significantly different from the other supplements.

Fecal Bulk
The fecal output on the wheat bran supplement (258±22 g/day) was significantly greater than the other three (RS2, 187±24 g/day; RS3, 182±23 g/day; low-fiber control, 163±23 g/day; p<0.010) (Table 3). Nevertheless, by comparison with the low-fiber control increases in fecal outputs were seen on both RS2 and RS3 supplements of 24±9% (p=0.017) and 29±14% (p=0.046), respectively (Fig. 1). Assessed by student’s t-test for paired data (two-tailed), the mean increase in fecal output when data on both resistant starches for a given subject were combined was 22±8 g/day greater than the low-fiber control (p=0.013).


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  		Table 3. Fecal Weight and Short Chain Fatty Acids on the Low-fiber Control, Wheat Bran and Resistant Starch (Mean of Two) Treatments (n=24)

 


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  		Fig. 1. Percentage differences in fecal bulk from the low-fiber control for the wheat bran, RS2 and RS3 supplements in 24 subjects.

 
Fecal Short Chain Fatty Acids (SCFA)
Only the wheat bran supplement resulted in significantly greater fecal output of total and individual SCFAs. The increase in SCFA output resulted from the greater total fecal output since wheat bran did not increase the concentration or the molar ratios of any of the SCFAs compared to the other three treatments. However, direct paired t-test comparison of the mean of the two resistant starch treatments with the low-fiber control demonstrated an increase in both butyrate concentration by 56±18% (p=0.006) and in the butyrate:total SCFA ratio by 31±14% (p=0.035) (Table 3). This increase in butyrate concentration was seen when the RS2 and RS3 starches were compared individually with the low-fiber control (45±17%, p=0.015 and 66±26%, p=0.020, respectively) (Fig. 2). Similarly, direct comparison of the butyrate concentration on wheat bran with the low-fiber control indicated a 48±21% increase (p=0.030) (Table 3). No significant difference was seen in the butyrate:total SCFA ratio.



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  		Fig. 2. Percentage differences in fecal butyrate concentrations from the low-fiber control for the wheat bran, RS2 and RS3 supplements in 24 subjects.

 
Breath H2 and CH4
No materially significant differences were seen between treatments in the mean concentrations of breath H2 (low fiber control, 9±1 ppm; wheat bran, 11±2 ppm; RS2 10±1 ppm; RS3 9±2 ppm) and CH4 (low fiber control, 8±2 ppm; wheat bran, 6±3 ppm; RS2 13±4 ppm; RS3 8±3 ppm).

Serum Urea and Creatinine
No statistically significant differences between treatments were seen in baseline values, the change from baseline or week 2 values for serum urea or creatinine.

Serum Lipids
Baseline values were similar for all treatments as were the changes from zero time and the 2-week values for lipids and lipoproteins (data not shown). There were no significant associations between blood lipids and with fecal SCFA or breath gas measurements.

Glycemic Index
No differences were seen in the glycemic responses expressed as glycemic index for any of the supplements provided either as breakfast cereals or muffins (Fig. 3). The one exception was the wheat bran flake breakfast cereal which had a glycemic index significantly below the negative control cereal (88±15 vs. 126±18, p=0.030) assessed by students t-test.



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  		Fig. 3. Glycemic indices (mean±SE of cereal supplements (upper panel) and muffin supplements (lower panel) tested in 10 and 11 subjects, respectively. The glycemic index of the wheat bran cereal is significantly lower than that of the low-fiber control cereal (p=0.030).

 

   DISCUSSION
 
The present study in which two resistant starches were incorporated into foods confirms the small increase in fecal bulk seen in other studies [15,16,35] and indicates an increase in fecal butyrate as recorded for some, but not all, resistant starches [17]. No effects were seen on serum lipids, breath hydrogen and methane or serum urea, which might have related to increased colonic fermentation or other actions of dietary fiber. No significant differences were observed between the two resistant starches.

The increase in fecal output was modest as has been reported for other sources of resistant starch by other investigators [15,35–37]. Such studies have demonstrated increases in fecal output ranging from 1.6 to 2.7 g per g of resistant starch in the diet for potato, banana, wheat and maize. These values represented only 32% to 55% the fecal bulk observed with wheat bran fiber (4.9 g per g fiber) [35]. In the present study by comparison with the negative control, the two resistant starches produced approximately 23% of the increase in fecal output per g of ‘resistant’ starch as was seen with wheat fiber from the wheat bran supplement when both were measured as dietary fiber by the gravimetric method [19].

One of the interests in resistant starch has been its ability to provide a substrate for the colonic microflora and so promote the synthesis of short chain fatty acids, especially butyrate. It has been proposed that colonic diseases including ulcerative colitis are energy deficiency disorders [38] where butyrate is acknowledged as an important energy source for the colonocyte [39]. Although increased colonic butyrate levels do not appear necessary for the protective action of wheat bran in chemically induced colon cancer [40], patients with colon cancer have been shown to have reduced fecal butyrate:SCFA ratios at the time of initial investigation [41]. Our data confirmed a higher mean fecal butyrate:SCFA ratio when the resistant starch supplements were consumed and an increased butyrate concentration by comparison with the low fiber control. Increased fecal butyrate outputs have been demonstrated using both whole food and commercial sources of resistant starch in some studies [15,42,43] but not in others [36,37]. An increase in the molar proportion of butyrate has also been observed when the ileostomy effluent of subjects who were fed a high resistant starch diet was fermented in vitro [17].

No significant difference was seen in mean breath H2 or CH4 over the day between the resistant starch treatments and the low-fiber control or wheat bran supplemented diets, all of which produced moderate concentrations of H2 and CH4. White bread, in significant amounts, is well known to produce appreciable elevations of breath H2 [44,45] possibly related to a starch-protein interaction. The lack of effect with resistant starch may be related to its slower rate of fermentation [46]. In view of the fact that only modest, inconsistent or non-significant elevations of breath H2 have been reported in previous studies of resistant starch [36,37,47] the results seen here are not unexpected, despite positive results in acute studies where resistant starch from mixed food sources was fed [48].

No direct effect of resistant starch was seen on serum lipids in agreement with recent studies using RS2 and RS3 as the sources, but where the starch was fed in an uncooked product [49] as opposed to a cooked product used here. The previous observation of a lipid lowering effect of resistant starch in rats may not therefore be applicable to man [50] and the effects are more similar to those of insoluble dietary fiber than to the cholesterol lowering action of soluble fibers [51–53].

No effect of resistant starch was seen on glycemic index. This point is important since it highlights the difference between "slow release" or "lente" carbohydrates and truly "resistant" starches. Slow release or lente carbohydrate foods, some of which would be classified as RS1 resistant starches, are slowly digested in the small intestine, as opposed to rapidly available glucose (RAG) [54], and result in reduced postprandial glycemic and insulinemic profiles [55]. These low glycemic index foods are the result of many factors including food form [56–58] and the nature of the starch [14,59–60]. On the other hand, the available starch portion of the RS2 and RS3 starches used here appear to be readily digested.

Unexpectedly, a significantly lower glycemic index was seen with the wheat bran flake cereal compared to the control. This effect was not seen with the muffin supplements. Furthermore, in previous studies no differences have been reported between high and low wheat fiber baked goods such as breads [59]. We therefore have no explanation for the wheat bran cereal effect which may relate to the nature of cereal processing.


   CONCLUSION
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 CONCLUSION
ACKNOWLEDGMENTS
 REFERENCES
 
The major physiological effect of resistant starches therefore appears to be as substrate for colonic fermentation with a modest fecal bulking activity. The increased butyrate generation may have implications for the luminal health of the enterocyte. Studies in healthy humans and subjects with chronic disease (ulcerative colitis, recurrent colonic polyps) are, however, required to assess longer term effects of feeding significant amounts of dietary resistant starch.


   ACKNOWLEDGMENTS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 CONCLUSION
 ACKNOWLEDGMENTS
REFERENCES
 
We thank Yumin Li, Renato Novokmet, George Koumbridis and Nalini Irani for their excellent technical assistance.

Funded by the University-Industry Partnership Programme of NSERC Canada, and Nacan Products Ltd., Canada.

Received February 1, 1998. Accepted May 1, 1998.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 

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