The Influence of Dietary Fiber Source on Human Intestinal Transit and Stool Output1

K. L. WRICK,2 J. B. ROBERTSON, P. J. VAN SOEST, B. A. LEWIS, J. M. RIVERS, D. A. ROE AND L. R. HACKLER3 Department of Animal Science, Division of Nutritional Sciences, Cornell University, Ithaca, NY 14853 ABSTRACT Wheat bran ground to a coarse and fine particle size, purified cellulose and ethanol-extracted cabbage fiber, fed to 24 adult males during an 80-day metabolic trial, were examined for effects on intestinal transit time, taxation and stool composition. Brilliant blue, plastic pellets, polyethylene glycol (PEG)-4000 and Cr(III) mordanted onto isolated bran fiber were simultaneously administered for transit measurements. Intersubject variability in response to fiber source was highly significant for all transit and stool measurements. Only coarse bran or cellulose addition increased transit speed (decreased transit time) over basal rates. Grinding of bran significantly reduced fecal output because of reduced fecal water. Only subjects consuming cellulose or fine bran reported difficult or uncomfortable defecations. Though cabbage produced the smallest fecal output, stools had a high moisture content comparable to those obtained from coarse bran, which suggests a large microbial output in response to a fermentable sub strate. Significant negative correlations were produced when changes in dry matter or cell wall intakes were regressed with Cr (III) transit. These findings suggest that the level of either food or fiber in the diet are variables that influence intestinal transit time and should be controlled in studies measuring it. Increases in fiber intake linearly in creased fecal output of water and dry matter. Regression slopes were characteristic of each fiber source. J. Nutr. 113: 1464-1479, 1983. INDEXING KEY WORDS fiber transit time stool output human

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Investigations assessing the effects of dietary fiber on mouth-to-anus transit time in humans have often yielded conflicting and, hence, inconclusive results. Only a few of the investigations reported successfully measured digesta passage for those on controlled diets (1-3). Wheat bran has been the main fiber source tested, though oat flakes (4), bagasse (5), purified cellulose (6), guar gum (1), pectin (3, 7) and fruits and/or vegetables (14, 8, 9) were tested in some studies. Bagasse was effective in reducing transit time, whereas the effect of orange fiber was only slight (4), and added cellulose or pectin had no effect,
which SUggestS that different fiber SOUrCeS

normal controls. Types of disorders have varied within experiments and have included spastic colon, proctitis (10), constipation (8, 10, 11), diverticular disease (10, 12), diarrhea and irritable bowel syndrome (11). The differential passage of chromic oxide and polyethylene glycol (PEG) demonstrated in subjects with diverticular disease and cholerrhoeic enteropathy (13) suggests that a certain disease state can affect marker passage more profoundly than any dietary variable. Nearly all studies that allowed self-selected diets did not mention a control for total level _
19SS American Institute of Nutrition. Received (or publication 29

exert different effects on intestinal function. _. . n | . j , Occasionally, marker transit data trom sub*^

March 1983 ' Supported in part by Department of National cancer institute Grant NO Hnou, urbana, ILeisoi

Health. Education and Welfare,

jects with gastrointestinal disturbances were i r i i i

compared to those obtained from healthy,
1464

Present address: TWoodhiiiBoad, Andov" MA018l?I . Present address: Department of Foods and Nutrition. University of II-

FIBER SOURCE, TRANSIT TIME AND STOOL OUTPUT

1465

of food intake, which has consistently been a variable affecting rate of digesta passage in animals (14-18). Experiments in humans generally have not been designed to assess the extent that intersubject variability, dis ease condition and the amount or composi tion of diet are factors affecting digesta pas sage rates in addition to the presence of bran or other fiber source. Studies of dietary fibers and their effects on bowel function have indicated various changes in stool output and composition, not all of which are solely attributable to waterbinding properties measurable in vitro (19). Research reports examining the effects of added dietary fibers on stool bulk and com position have been reviewed (20), and it is generally agreed that fiber addition to an otherwise low fiber diet increases stool vol ume and improves taxation. This latter term is somewhat ill defined but usually refers to the frequency and/or ease of defecation. Dietary fiber is not a uniform material and varies widely in chemical composition and physical properties with taxonomic class. Large differences between intact vegetable and cereal fibers and isolated cellulose prep arations have been reported for measure ments of hydration capacity (21, 22), bulk volume (22, 23) and fermentive capacity (24, 25). Variability in physicochemical proper ties permits speculation that the source, level of intake and the bulk density (particle size) of dietary fiber consumed would alter the rate of digesta passage, the total fecal output of water and dry matter (DM), the frequency of defecation and the moisture content of the stool. These hypotheses were tested in a hu man metabolic trial by using healthy subjects with no history of gastrointestinal disease. An analysis of present methods for mouth-toanus transit time measurement and compartmental turnover kinetics is presented elsewhere (26, 26a). MATERIALSAND METHODS Subjects, diets and experimental plan

tion of diets (26-28). The highlights of the conduct of the study are presented here. Fiber sources used were white wheat bran ground to a coarse or fine particle size (R073691 American Association of Cereal Chem ists, St. Paul, MM) purified wood cellulose (SW-40 food grade Solka Floe, Brown Co., Berlin, NH) and ethanol-extracted cabbage fiber (28). Particle size distributions and other compositional data are presented in table 1. All fiber sources were baked into breads, which actually provided from 13-18 g of cell wall (CW) daily [neutral detergent residue (NDR) or NDR plus pectin in the case of cabbage fiber]. Breads with added fiber were substituted for white bread in the basal diet, which contained approximately 1% NDR by analysis. During the 80-day metabolic trial, the 12 subjects in group 1 changed fiber source with each 2-week experimental pe riod, and the basal diet was given only during period 5, the last period, extended to 3 weeks to account for delays in transit time. Since every subject was fed each fiber source, the experimental design was balanced across diets to eliminate the effect of preceding treatment. The 12 subjects of group 2 re mained on the same fiber source for the du ration of the study beginning with period 2. The 2400-kcal diet proved insufficient to maintain body weight in many subjects. Cal culated energy requirements based on indi vidual weight loss data indicated a need to increase caloric consumption by 0, 21, 42 or 63% in selected subjects. These changes in total dietary intake did not influence the chemical composition of the diet, and were instituted at period 4. During period 5, group 2 doubled their fiber intake. Though these dietary changes were unanticipated at the outset, they ultimately provided a means to examine the effects of increasing DM and CW intake on transit and stool output mea surements during periods 3-5. DM and CW consumption were calculated for all subjects from diet homogenates collected and ana lyzed weekly.

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Other reports have presented the details of subject selection criteria, selection, prep aration and analysis of fiber sources, basal diet composition and the statistical distribu

Stool collections
All feces were collected in a device similar to that described by Hinton et al. (29). On their receipt at the metabolic unit, appro-

1466

WRICK

ET AL. 1

TABLE

Analysis of dietary fibers

Coarse bran Particle size, (% distribution > 2380 Mm 2380 > 1190 Mm 1190>590Mm 590 > 297 Mm 297 > 149 Mm 149 > 74 Mm < 74 Mm Geometric Geometric mean diameter, so, nm pm by weight) 0.18 16.22 52.48 28.92 1.90 0.19 0.12 744.4 1.671 O 0.02 0.06 23.04 49.01 12.30 15.58 172.9 2.173 2.95 1.35 0.60 7.63 46.63 13.56 27.27 142.9 2.805 0.16 O 40.92 44.70 10.49 2.05 1.68 484.4 1.838 Fine bran Cellulose Cabbage

Chemical composition of fibers

Dry matter, % Cell wall, % NDR Hemicellulose, % Cellulose, % Lignin, % NDR content breads,2 % 91.1 44.0 30.9 9.3 3.3 13.6 90.8

39.3
27.2

8.9
2.8 12.8

93.8 100.0 2.6 96.5 0.1 17.8

86.7 44.3' 7.3 31.1 1.0 9.9'

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Physical properties of fibers

Bulk volume:

as fed, ml/g per unit NDR, ml/g

Hydration capacity, ml/g NDR

3.3 8.2
3.5

2.1 5.2 2.7

13.0 13.9
1.4

4.7 12.3 20.7 powder was

1 NDR value (neutral detergent residue) excludes 29% pectin. Total dietary fiber content of cabbage 73% and of cabbage bread 16.3%. 2 Basal diet white bread contained 1% dietary fiber.

priate data were recorded and samples were weighed, frozen and subsequently lyophilized. Dried samples were seived through a 2.36-mm screen to remove particulate mark ers. All 1650 samples were assayed individ ually for markers, none were pooled. The record of wet and dry stool weights permitted calculation for each subject of weekly outputs of total feces (TF), DM, total fecal water (TFW), the percent water con tent of stools and laxation rate, defined here as the number of stools passed per week. Marker selection, administration and analysis All markers were given at breakfast on days 1 and 7 of each period for all subjects. During period 5, markers were given on days 1, 7 and 17. Brilliant blue. Subjects swallowed 100 mg of brilliant blue (F. D. & C. Blue No. 1, Allied

Chemical, Morristown, NJ), a food coloring preparation typical of dye markers used in human balance trials (30), in a gelatin capsule without added carboxymethylcellulose. The time of first fecal appearance was the only datum recorded, since the dye could not be quantitated in lyophilized stools. PEG. PEG (Union Carbide Chemicals, New York, NY) with an approximate molec ular weight of 4000 was diluted in water such that subjects ingested 1.0 g of marker for each dose. Lyophilized stools were analyzed in duplicate by using the method of Malawar and Powell (31), by using a 2 mg:l gum arabic solution and a Bausch and Lomb 20 spectrophotometer (Rochester, NY) with a red filter. A wavelength of 685 nm was used since the blue dye marker contributed absorbance at 650 nm when present in fecal filtrates. A separate test indicated minimal interference of the dye marker at this wave length (27).

FIBER SOURCE, TRANSIT TIME AND STOOL OUTPUT

1467

Radiopaque plastic pellets. Plastic pellets (Portex, Ltd., Hythe, Kent, England, CT 216JL) such as those described by Hinton et al. (29) were ingested in a dose of 25 each, packed in a gelatin capsule. Lyophilized stools were hand screened for pellet retrieval. Chromium-mordanted bran CW. This marker, successfully applied to ruminant digesta passage trials, has not been previously used in human intestinal transit experiments. It was prepared by mordanting Cr (III) onto wheat bran CWs (32, 33). Briefly, starch-free coarse or fine bran CW preparations were thoroughly washed with water, dried at 65, soaked in a 10% (wt/vol) sodium dichromate solution and kept at 100for 24 hours. Fibers were washed and suspended in water acidi fied to pH 3.3 with ascorbic acid. The re sulting greenish fibers were washed, dried, and weighed into gelatin capsules such that each dose provided 35-45 mg Cr. Chromium (III) has an affinity for free hydroxyl groups present in CW cellulose or hemicellulose, forming either strong ligands or other cross-links with them, such that they are impervious to digestive or microbial en zymes. Chromium (III) mordant prepara tions used in ruminant digestibility studies were 100% recoverable on the fiber after 72 hours of incubation with rumen mi crobes (32). Coarse bran mordants were given to sub jects on coarse bran diets, fine bran mordants were given to all other diets because attempts to attach Cr III onto cabbage fiber or purified cellulose were unsuccessful. The amount of bran fiber contributed by the markers was less than 0.5 g each dose and was not ex pected to influence passage for those fed the nonbran diets. Fecal Cr recovery was assessed by atomic absorption spectrophotometry (Perkin-Elmer Model 305, Perkin-Elmer, Norwalk, CT, 357.9 nm wavelength, 0.017 slit width, hol low cathode lamp and an air-acetylene flame). Fecal sample preparation required that chromic oxide be solubilized, and involved ashing the dried sample, fusing the ash with potassium nitrate crystals over a direct flame, and dissolving fused samples in known quan tities of distilled water (33). Samples were appropriately diluted so that any Cr present was within the linear range of the standard curve (0-5 /ig/ml).

Calculation of transit time indices

Complete passage of all markers did not occur for several days following their inges tion permitting analysis of excretion curves for the pellet, PEG, and Cr markers. A num ber of transit indices historically used in hu man and animal passage studies that were calculated for the 730 administered markers are discussed separately (26) and include the time to marker first appearance (30), the time to 80% recovery (29), mean transit time and compartment turnover as estimated from kinetic analysis of excretion curves (36). This report is limited to the mean transit time (MTT) for marker passage. The estimate of MTT represents the in tegrated average of a marker excretion curve. It has been used in ruminant passage studies (33, 34), in small intestine transit studies in humans that used multiple indicator dilution techniques (35) and several dietary fiber studies in humans (1, 3, 9, 27, 37). The equa tion is:

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where t, is the time between marker admin istration and the ith defecation, and M, is the amount of marker in the fth defecation. Statistical analysis

The SAS General Linear Models procedure (38), a form of multiple linear regression on 0,1 variables (39) was used to analyze the marker passage data collected on group 1 subjects. Traditional analysis of variance pro cedures would not lend themselves to an un balanced data matrix, i.e., one which had occasional missing values. A linear model approach fits the experimental observations to a regression equation, which in turn can be used to estimate or predict a result when the effects of one or more factors are re moved. This statistical approach was more rigorous in that known sources of experi mental variability, such as the effects from subject, experimental period, or carryover effect from the previous diet, were statisti cally quantified and removed from the ef fects of fiber source, the dietary variable of special interest. An R2 value calculated along with typical analysis of variance statistics served as a cor-

1468

WRICK ET AL.

relation coefficient between the estimates predicted by the equation and the actual ob servations used to derive it. The Rz can be viewed as an estimator of how well the data fit a linear model and is reported in all of the analysis results. Analysis of variance was performed on data from group 1 subjects only. The order of presentation of diets to group 2 did not permit a statistical analysis by this means.

pieces for pellet retrieval. Pellet recovery was significantly lower in stools from cellulose diets (P = 0.02) compared to recovery when the basal diet was fed. Recoveries were sig nificantly influenced by subject effects (P = 0.02). Mean fecal Cr recovery from 244 doses of Cr-mordanted bran was 84.0 16.9%. Re covery of potassium dichromate standards averaged 93.2%, with a coefficient of varia tion of 6%. Incomplete conversion to chromicoxide and occasional marker overlap between RESULTS periods are explanations for results other Marker recovery. Mean recovery for 242 than 100%. doses of l g PEG was 85.3 12.6%. The Cr recoveries from group 1 subjects were procedure used was designed for analysis of not influenced by intersubject variability. intestinal perfusates and may not be ade However, analysis of Cr recoveries during periods 1-4 revealed a significant carryover quate for rehydrated fecal material. Recov ery of a known amount of PEG added to effect from a previous diet of cellulose (P = 0.03), which significantly depressed Cr re fecal material prior to lyophilizing ranged from 68-72%. Other investigators have re covery during the following experimental ported difficulties in recovering PEG from period, regardless of what new fiber source dried feces, noting that it can associate with was fed. The reason behind this observation particulate matter if samples are frozen (36). is not clear. A possible explanation might be Recovery from cow feces has ranged from that cellulose sufficiently altered the colonie 40-60% (40) and in vitro tests (41) have re microflora such that there was a microbial ported adsorption of PEG onto vegetable fi interaction with the mordant, which some bers even after centrifuging at 14,000 X g how influenced recovery of the metal. There were no significant effects of subject, for 1 hour. A significantly low recovery of PEG was period, previous diet or fiber source on the found for group 1 subjects consuming cab time for first appearance in feces of brilliant bage (P = 0.05) compared to the recovery blue. The failure of dye markers to be quan of the marker when the basal diet was fed. tifiable in feces precludes their usefulness in This suggests that the fiber composition of transit studies. the diet may influence the recovery of a wa Experimental variables influencing marker ter-soluble marker. The microbial population transit and stool output. The levels of sig induced by cabbage fiber consumption might nificance of subject, period, previous diet and produce bacterial cell walls of a different fiber source effects on transit and stool output nature capable of binding the marker in ly- are listed in table 2. Intersubject differences ophilized stools. If so, PEG binding by stool were highly significant as was variation due components could interfere with solubiliza- to fiber source. Analysis of stool output data from periods 1-3 are shown because a sep tion and filtration of the marker during anal arate analysis indicated a strong period effect ysis, causing low recoveries. Mean recovery of 244 administrations of (P < 0.0004) from the increase in intake im radiopaque plastic pellets was 98.2 3.5%. posed at period 4. Previous diet effects were Recoveries other than 100% could be attrib significant only for the water content of the stool. R2 values range from 0.57 to 0.88, as uted to either miscounting during marker preparation or recovery, or fracture during might be expected for biological data, and handling of some very hard, compact stool suggest these data fit a linear equation rea samples. Stools from subjects consuming cel sonably well. lulose lacked the friable characteristics of The addition of different fiber sources to those consuming bran, and had to be ham a low fiber, basal diet (table 3). A comparison mered in order to break them into smaller of transit time and stool output data from

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FIBER SOURCE, TRANSIT TIME AND STOOL OUTPUT TABLE 2

Significance of experimental variables influencing marker transit and stool output in group 1 subjects time (MTT)

1469

dietProbability0.070.060.002'0.740.390.800.620.25of Previous source0.0020.010.0020.00010.00010.00020.020.0

1-4)PelletsPEGCr-mordantStool MTT (periods

a F0.760.990.700.970.550.920.660.05Fiber greater

1-3)2TF.gDM, output per week (periods gTFW, gLaxation defecationsStool rate, water content, %R20.720.570.790.710.670.730.750.88Subject0.00010.00010.00010.00010.00040.00010.00010.0001Period
1The significant period effect was shown in a separate analysis to be from the increase in dietary intake imposed at period 4. 2 Analysis excludes period 4 data because of the significant (P < 0.0004) intake effects present for all output measurements except taxation rate.

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diets containing fiber and the low fiber basal diet was made on group 1 data, periods 1-5. Because the basal diet was fed exclusively during period 5, data were corrected for ef fects of subject and diet only and were tested against the basal diet for significance. Coarse bran and cellulose provided the fastest transit, regardless of marker type. The MTT values obtained from fine bran and cabbage diets were not significantly different from those obtained on the basal diet. A sep arate analysis of data from periods 1 to 4 corrected transit observations for previous

diet and experimental period effects. Re gardless of marker type, only coarse bran and cellulose provided significantly faster transit times than cabbage (0.0005 < P <s0.05), whereas fine bran did not. Addition of coarse bran, fine bran or cel lulose provided outputs of TF, DM and TFW significantly greater than those obtained on the basal diet. Addition of any of the four fiber sources significantly increased the laxation rate by 1-2 stools per week, though this change was probably not noticeable to the subjects. Consumption of coarse bran or cab-

TABLE 3 Influence of five experimental diets on marker transit, stool output and taxation rate in group 1 subjects1
Stool output and taxation transitFiber Mean

sourceCoarse

feces matter(DM)g251'227'235"172'b173b11.20.46Total fecal rate37.7'7.T6.9P6.0a5.2b0.380.66Stool water (TFW)g846'666'723"b600b545b38.10.66Laxation water%77.3'73.6ab74.3ab76.3*74.7b0.650.73 mordanthr40.9-57.4h47.9'64.4'b62.4b5.10.66Total (TF)g1096"893'957'771.b718b48.20.53Dry

branFine branCelluloseCabbageBasalSEMR1Pelletsht35.8'51.5'b47.0-b58.5<b56.5b5.30.63PEG2hr38.9"50.1'b46.7"60.6"1161. lb6.70.59timeCr-

' Means not sharing a common superscript < 0.05). Intersubject variability was significant ylene glycol. ' Measured as defecations.

letter in the same column are significantly different (0.0005 < P (P < 0.0001) as were effects of fiber source (P < 0.02). 2 Polyeth

1470

WRICK ET AL

bage fibers provided stools of higher moisture content than did the basal diet alone. Com plaints of difficulty in passage of hard stools were confined to the subjects consuming cel lulose and fine bran. To compare the effects of different fiber sources without the influence of increased dietary intake, data from periods 1-3, for group 1 subjects were separately analyzed, and fiber sources were tested against cabbage for significance. Only subject and diet effects were significant, carryover effects from the previous diet were not. Relative to cabbage fiber, coarse bran and cellulose fibers pro vided significantly greater taxation rates and outputs of TF, DM and TFW. Fine bran provided a significantly larger output of TF and DM but stools of a significantly lower moisture content than the cabbage fiber. Particle size effects. Transit and stool out put data from the two bran diets were ex amined in a separate linear model and anal ysis for group 1 subjects. As shown in table 4, coarse bran provided significantly faster marker passage than finely ground bran re gardless of marker type, confirming the data of Kirwan et al. (42) and Heller et al. (27). These authors found significant particle size effects on intestinal transit time using a less rigorous statistical analysis. Fine-grinding caused a reduced bulking effect because a smaller volume of the colon was occupied.

Fermentation data revealed no effect of grinding on fermenlability in vitro (43). Coarse bran produced significantly greater stool outputs of higher moisture content. Comparison of bran and cellulose fibers. (table 5) Subjects fed coarse bran produced stools of significantly greater water content, and outputs of TF and TFW were also higher than stools from subjects fed cellulose. The taxation rate and DM outputs were not sig nificantly different. A comparison of data from subjects consuming fine bran and cel lulose was made because of the particle size difference present between coarse bran and cellulose fibers. No significant differences were found for any of the stool measure ments. Marker comparison. A separate analysis of MTT values from all 3 markers from group 1 subjects, periods 1-4, revealed no signifi cant differences in transit time estimates be tween marker types. Data were corrected for effects of subject, period, previous diet and fiber source. Changes in total food (DM) and fiber (CW) intake levels. Calculations of weekly intakes of DM and CW permitted exami nation of the effects of increasing fiber intake on transit time and fecal output by linear regression analysis. Appropriate regression statistics derived from relating either DM intake to Cr-MTT, or CW intake to Cr-MTT,

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TABLE 4 Bran particle size effects on marker transit and stool output for group 1 subjects'-2 Coarse bran Mean timePellets, transit hrPEG, hrCr-mordant, hrStool Fine bran

outputTotal gDry fces (TF), gTotal matter (DM), gLaxation fecal water (TFW), defecationsStool rate, water content, %18.1'47.7'26.7"953"219733"6.678.5'34.056.442.58312096225.674.94.78.45.046.89.638.50.70.90.840.490.820.820.690.840 ' Transit data from periods 1-4 were analyzed, whereas stool output data from periods 1-3 were analyzed because of the significant intake effect (P = 0.0001) on all measurements when period 4 was included. 2 Intersubject variability was significant for all measurements (P < 0.005) except stool dry matter content. Means are signif icantly different (P < 0.03) from fine bran.

FIBER SOURCE, TRANSIT TIME AND STOOL OUTPUT TABLE 5

Comparison of coarse bran and cellulose effects on stool composition for group subjects, periods l-3l Weekly outputs Total feces (TF) Dry matter (DM) Total fecal water (TFW) Laxation rate3 and taxation rate

1471

Stool water content

branCelluloseSEMfi2958'80849.80.8322021011.90.69737"59839.40.866.26.20.560.8977.8"73.90.710.86 Coarse

1 Analysis excludes data from period 4 when increases in dietary intake were imposed. 2 Intersubject variability was significant (P < 0.05). 3 Measured as defecations. ' Means are significantly different from cellulose (0.001 < P < 0.01).

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outputs of TF, TFW, DM, water content and taxation rate are shown in tables 6 and 7, respectively. Data for periods 3-5 were used from all 24 subjects. These periods were se lected because they represented the broadest spectrum of fiber intakes, i.e., the total diet increases of 0, 21, 42 or 63% beginning at period 4, the basal level of intake for group 1 during period 5, and the approximate dou bling of fiber intake level for group 2 during period 5. Of the seven sets of regressions per formed, those providing significant regres sion equations are plotted in figures 1-6. All are discussed in greater detail below. DM intake and Cr-MTT. The dashed regression line in figure 1 shows a sig

nificant decrease in Cr-MTT as DM in take increases, regardless of diet type. These data predict a 7- to 8-hour de crease in MTT with each 100-g increase in total DM intake. When transit data from individual diets were examined, only fine bran showed a significantly negative regression slope, though coarse bran, cabbage and the low fiber basal diets showed negative trends in the data. The negative trend on the low fiber basal diet is of interest because CW intakes were maintained between 3.5 and 5.0 g per day, despite an increase in DM intake of over 30% in some subjects. The exception to these trends was the cel lulose diet, which showed a distinct

TABLE 6 Regression analysis of dry matter (DM) intake on Cr-MTT in Cr-MTT for 24 subjects, periods 3-5'

Change

with increasing

DM intake

Correlation forAll dietsCoarse branFine branCelluloseCabbage

coeff. (r)-0.32-0.24-0.62+0.36-0.35

slope (b)-0.08-0.12t

0)-2.78

P(b *

0.02-2.90 0.05Intercept105.6128.4
S 9Correlation -0.17P0.01NS0.01NSN NSRegression

Basaldf7113141413 ' Abbreviations

as follows: df, degrees

of freedom;

r, correlation

coefficient;

P, level of significance

of r; t, t

statistic; P(b & 0), level of significance

of t for regression slope unequal

to zero; NS, not significant.

1472 7Regression 'Correlation

WRICK AL.TABLE ET

analysis of cell wall (CW) intake levels on taxation rate and stool composition for 24 subjects, periods 3-5

0)0.010.020.020.010.010.010.010.010.010.010.010.02 * (b)-1.50-2.63-5.7140.7451.0054.2639.109.611.616.911.45.431.138.842.327.70.130.2 vs:1. of CW intake

Cr-MTTAll dietsCoarse branFine branCelluloseCabbage2.

Total outputAll fecal dietsCoarse bran2Fine bran2CelluloseCabbage3.

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Dry outputAll matter dietsCoarse bran3Fine bran3Cellulose3Cabbage4.

Total waterAll fecal dietsCoarse bran2Fine branCelluloseCabbage5.

rateAll Laxation dietsCoarse branFine branCelluloseCabbage6.

Percent water contentAll dietsCoarse branFine branCelluloseCabbagedf711314141387171618198717161719861616171682171616158617161718r-0.20-0.48-0.58+0.02-0.610.770.780.800.610.410

1Abbreviations as follows: df, degrees of freedom; r, correlation coefficient; P, level of significance of r; t, t statistic; P(b & 0) level of significance of /, for regression slope unequal to zero; NS, not significant. 2 Regression slope significantly greater than cellulose (P < 0.01). 3 Regression slope significantly greater than cabbage (P < 0.01).

though not significant tendency for an increase in Cr-MTT with an increase in DM intake. CW intake and Cr-MTT. The regres sion plots relating CW intake to CrMTT showed similar results to those of

DM intake (fig. 2). An increase in CW intake from all sources showed a signif icant decrease in Cr-MTT. These data predict a 7- to 8-hour decrease in MTT with each 5-g increase in CW intake. Regression of Cr-MTT on CW intake from individual diets resulted in signif-

FIBER SOURCE, TRANSIT TIME AND STOOL OUTPUT 140

1473

120

100

-z
c.

80

LFB 60
all data

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40

CB

20

400

5)0

600 Dry Matter Intake, g/wk

700

800

Fig. l Change in Cr transit time with increasing dry matter intakes. , CB (coarse bran); O, FB (fine bran); A, Ca (cabbage); V, Ce (cellulose); D, LFB (basal diet). Regression slopes for all data and FB were significantly greater than zero (P s 0.05). Dotted lines indicate trends (not significant) for respective diets.

icant negative slopes for fine bran and cabbage. The steep negative slope ob tained for cabbage fiber implies that vegetable matter is the most effective fiber source in reducing transit time with only slight increases in CW intake. However, the 10-12 g of cabbage fiber consumed in this study, equivalent to 2.2 kg of fresh cabbage daily, provided MTT values of approximately 100 hours, ranking it as the fiber source least ef fective in reducing transit. These data predict that a steady consumption of about 200 g of fresh cabbage daily (about 2.5 g of dietary fiber) for 10 to 14 days would have provided an MTT of about 144 hours or 6 days. Clearly, vegetable fibers at levels commonly con sumed contribute little to speed of digesta passage.

CW intake and TF output (fig. 3). An increase in CW intake from all fiber sources correlated with an increased TF output. Significant positive correlations and regression slopes were obtained for diets containing coarse bran, fine bran and cellulose but not for the cabbage diet, though a trend for increased output was present in these data. Regression slopes in table 1 predict the expected increase in output of feces per gram of CW consumed. CW intake and DM output (fig. 4). Sig nificant positive correlation coefficients and regression slopes were obtained when DM outputs from all experimental diets were regressed collectively or in dividually against CW intake level. Pre dicted increases in DM output with each

1474
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WRICK ET AL

120

100

80

to
Ce
40

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andata

20

CB

10

15

20

25

30

35

40

45

Cell Wall Intake, g/wk

Fig. 2 Change in Cr transit with increasing fiber intake. , CB (coarse bran); O, FB (fine bran); A, Ca (cabbage); V, Ce (cellulose); D, basal diet. Regression slopes are significantly greater than zero (P <, 0.02) for all data, FB and Ca (solid lines). Dotted lines indicate trends for CB and Ce, which were not significant.

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CB (coarse bran); O, FB (fine bran); A, Ca Fig. 3 Change in fecal output with increasing cell wall intakes. , (cabbage) V, Ce (cellulose); D, basal diet. All regression slopes are significantly greater than zero, (P = 0.01) except for cabbagi ;e (dotted line).

FIBER SOURCE, TRANSIT TIME AND STOOL OUTPUT

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Fig. 4 Change in dry matter output with increasing cell wall intake. , CB (coarse bran); O, FB (fine bran); A, Ca (cabbage); V, Ce (cellulose); D, basal diet. All regression slopes are significantly greater than zero (P <, 0.02).

additional gram of CW intake were about 11-12 g for bran and cellulose diets but only about 5 g for the cabbage diet. An increase in CW intake equiv alent of 2 kg of fresh cabbage daily in
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creased DM output by about half the amount obtained for the other fiber sources fed at comparable levels of CW. CW intake and TFW output (fig. 5). Regression analysis of TFW output data

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Fig. 5 Change in total fecal water output with increasing cell wall intake. , CB (coarse bran); O, FB (fine bran); A, Ca (cabbage); V, Ce (cellulose); D, basal diet. All regression slopes are significantly greater than zero (P A 0.05) except for cabbage.

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WRICK ET AL.

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Fig. 6 Change in laxation rate with increasing cell wall intakes. CB (coarse bran); O, FB (fine bran); A, Ca (cabbage); V, Ce (cellulose); D, basal diet. Regression slopes are significantly greater than zero (P 0.02) for Ce, Ca, and all data.

from all experimental diets against CW intake level produced a significant pos itive correlation and regression slope, which predicted an increase of 31 g of water output with each additional gram of CW intake. Significant positive cor relations and regression slopes were also obtained for all fiber sources except cab bage, in spite of the high moisture con tent present in the stools produced from that diet. CW intake and laxation rate (fig. 6). An increase in CW intake correlated sig nificantly with an increase in laxation rate when data from all experimental diets were collectively analyzed (regres sion slope b = 0.13). Regression analysis of laxation rates from individual fiber sources revealed that increased intakes of either coarse or fine bran did not sig nificantly increase the number of stools per week. A positive correlation was ob tained between an increase in either cel lulose or cabbage fiber intake and lax ation rate; however, the rate of increase per gram of fiber consumed was less than one stool per week.
CW intake and percent water content of stools. A change of fiber intake did

not correlate with any change in the percent water composition of feces for any fiber source except fine bran, which produced a positive regression slope.
DISCUSSION

The effects of fiber source on mean transit time reported here clearly support the hy pothesis that dietary fiber will provide faster passage of digesta residues than a diet free of or extremely low in fiber, but this conclu sion cannot be extended to all fiber sources. The finding that coarse bran behaves so differently from vegetable fiber supports the conclusions of Cummings et al. (1), who re ported different responses in colonie function when bran, apple, carrot, cabbage and guar gum were fed under controlled conditions. Our findings are in concert with the expec tation that noncrystalline cellulose and pec tin, predominant in cabbage fiber, are readily fermented in the colon, causing considerable loss of bulk. Fiber digestibilities calculated for these subjects averaged 75% for cabbage CW, 52% for cabbage hemicellulose and 82% for cabbage cellulose (43). These CW and cellulose digestibility coefficients were the highest of all fiber sources fed, despite the high level consumed (equivalent of 2 kg fresh cabbage daily).

FIBER SOURCE, TRANSIT TIME AND STOOL OUTPUT

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Solka Floe behaved similarly to coarse bran. Purified cellulose has no CW structure, but its high bulk volume despite small par ticle size was responsible for its effect on tran sit. Its relative nonfermentability was con firmed by the consistently negative trends in digestibility coefficients in group 2 subjects who consumed cellulose as the sole fiber source for 66 days (43). Addition of dietary fibers to a low fiber diet increased fecal outputs of water and DM to variable extents depending on the fiber source. A fiber source of a sufficiently large particle size to insure an intact CW structure and sufficient lignification to resist extensive fermentation of CW constituents is the most effective in promoting bulkier stools of high moisture content. Coarse bran met these re quirements in this investigation and insured more frequent defecations. Fine grinding diminished all these characteristics as might be predicted by the reduced bulk volume and hydration capacity observed in vitro. This finding confirms earlier reports regarding particle size effects on stool weight (27, 42, 44). Also of interest was the observation that cellulose and fine bran influenced stool out put similarly, probably because of their com parable particle size. The remarkable excep tion was the difference in stool water content. Relative to the other fibers tested, fine bran produced stools of the lowest moisture con tent, a surprising result in light of a water holding capacity greater than that for cel lulose in vitro. The significant increase in stool water content with coarse bran reported here refutes several earlier observations (4446), perhaps because the large intersubject variability inherent to human studies masked fiber particle size effects on stool water com position in these reports. The finding that larger, bulkier, moister stools were produced with the coarse bran in this study has ther apeutic implications for constipated patients. Cabbage fiber was fermented so extensively (28) that its influence on fecal output was considerably less than that of coarse bran, and compared closely with the basal diet. Fiber source effects on stool composition and laxation rates are of interest because they do not parallel the effects of transit time. Coarse bran provided the fastest transit in this study, followed by cellulose and fine bran. Transit times on the cabbage diet were

not significantly different from those on the basal diet. In spite of low fecal outputs and slow transit, cabbage fiber matched coarse bran in stool water content. These observations suggest several points: 1. Stool water content is a function of fiber source, not transit time, and is generally un influenced by fiber level. 2. Delayed transit times do not assure the passage of hard dry stools. Though colonie rsorptionmechanisms theoretically have more time to dehydrate colon contents, veg etable fibers induce a sufficiently large microbial mass that is itself high in water un available for absorption. 3. Different fiber sources serve as stool softeners by different means. Vegetable fiber induces the formation of microbial cells high in moisture content by virtue of its extensive fermentation. Coarse bran also induces the formation of a microbial mass by fermen tation, but to a lesser extent and maintains a sufficient CW structure, because of the lignin present, to entrap water. 4. Comfortable laxation is a function of stool water content and/or fiber particle size rather than fecal bulk. Coarse bran provided the greatest fecal output and cabbage the lowest, but neither were reported to cause the hard, dry, difficult-to-pass stools asso ciated with constipation. Such laxation dif ficulties were confined to the cellulose and fine bran fibers. Apparently ease of defeca tion is not a function of transit time. Stool moisture variations alone are not suf ficient evidence that fiber induces microbial growth in response to a fermentable sub strate. Increased cabbage fiber consumption in group 2 subjects, equivalent to over 4 kg of fresh cabbage daily did not significantly increase fecal mass (figure 3), but was found to dramatically increase fecal nitrogen con tent (43). Fecal nitrogen was least influenced by cellulose, the least fermentable fiber (28). Only traces of dietary nitrogen are expected to escape upper tract absorption, and mi crobes are capable of incorporating nonprotein nitrogen into their own cell mass. These findings support the assumption that differ ent fiber sources influence stool composition as regards moisture and microbial cells. The data in figures 1 and 2 suggest that the total food and/or fiber intake levels are

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1478

WRICK ET AL. (1978) Colonie response to dietary fibre from carrot, cabbage, apple, bran, and guar gum. Lancet 1, 58. 2. Kelsay, J. L., Behall, K. M. & Prather, E. S. (1978) Effect of fiber from fruits and vegetables on meta bolic responses of human subjects. I. Bowel transit times, number of defecations, fecal weight, urinary excretions of energy and nitrogen, and apparent digestibilities of energy, nitrogen and fat. Am. J. Clin. Nutr. 31, 1149-1153. 3. Stasse-Woltheus, M., Albers, H. F. F., Van Jeveren, J. G. C., dejong, J. W., Hautvast, J. G. A., Hermus, R. J. J., Katan, M. B., Brydon, W. G. & Eastwood, M. A. (1980) Influence of dietary fiber from veg etables and fruits, bran or citrus pectin on serum lipids, fecal lipids, and colonie function. Am. J. Clin. Nutr. 33, 1745-1756. 4. Walker, A. R. P. (1975) Effect of high crude fiber intake on transit time and the absorption of nutrients in South African Negro children. Am. J. Clin. Nutr. 28, 1161-1169. 5. Walters, R. L., Baird, I. M., Davies, P. S., Hill, M. J., Drasar, B. S., Southgate, D. A. T., Green, J. & Morgan, B. (1975) Effects of two types of di etary fibre on fecal steroid and lipid excretion. Brit. Med. J. 2, 536-538. 6. Eastwood, M. A., Kirkpatrick, J. P., Mitchell, W. D., Bone, A. & Hamilton, T. (1973) Effects of dietary supplements of wheat bran and cellulose on feces and bowel function. Brit. Med. J. 4, 392-394. 7. Durrington, P. N., Manning, A. P., Botn,H. C. & Hartog, M. (1976) Effect of pectin on serum lipids and lipoproteins, whole-gut transit time, and stool weight. Lancet 2, 394. 8. Cowgill, G. R. & Sullivan, A. J. (1933) Further studies on the use of wheat bran as a laxative. J. Am. Med. Assoc. 100, 795-802. 9. Parks, T. G. (1973) The effects of low and high residue diets on the rate of transit and composition of the faeces. Proceedings Fourth International Sym posium on Gastro-Intestinal Motility, pp. 369-380, Mitchell Press, Vancouver, B. C. 10. Paylor, D. K., Pomare, E. W., Heaton, K. W. & Harvey, R. F. (1975) The effect of wheat bran on intestinal transit time. Gut 16, 209. 11. Harvey, R. F., Pomare, E. W., & Heaton, K. W. (1973) Effects of increased dietary fibre on bowel transit. Lancet 1, 1278-1280. 12. Findlay, J. M., Smith, A. N., Mitchell, W. D., An derson, A. J. B. & Eastwood, M. A. (1974) Effects of unprocessed bran on colon function in normal subjects and in diverticular disease. Lancet I, 146149. 13. Findlay, J. M., Mitchell, W. D., Eastwood, M. A., Anderson, A. J. B*& Smith, A. N. (1974) Intestinal streaming patterns in cholerrhoeic enteropathy and diverticular disease. Gut 15, 207-212. 14. Castle, E. J. (1956) The rate of passage of food stuffs through the alimentary tract of goats. I. Studies on adult animals fed hay and concentrates. Brit. J. Nutr. 10, 15-23. 15. Coombe, J. B. & Kay, R. N. B. (1965) Passage of digesta through the intestines of sheep. Retention times in the small and large intestine. Brit. J. Nutr. 19, 325-338.

variables that can significantly influence digesta passage and that should be controlled in prudently designed studies that measure human intestinal transit or involve the use of indigestible markers. Negative relation ships between digesta passage rates and food intake levels have been reported in experi mental animals (14-18). The data for puri fied cellulose suggest anomalous behavior rel ative to other fiber sources with intact CW structures. This observation warrants further study, especially if purified cellulose prepa rations are to be considered as a means of "fortifying" foods commercially. The similar behavior of the pellets, PEG and Cr markers suggests that solid and liquid phases of digesta pass through the human digestive tract in comparable fashion. Findlay et al. (13) also found nearly identical pas sage rates for Cr2Os and PEG in one human subject free of intestinal disease. Together these results suggest that, provided dietary intake is controlled, any one of the three markers studied can be used to measure hu man intestinal MTT, which can be consid ered an indicator of total tract passage time. Discussions regarding the preference for any one marker for use in gastrointestinal kinetic studies that estimate digesta retention times in individual digestive compartments are presented elsewhere (26, 26a).
ACKNOWLEDGMENTS

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The authors wish to thank Dr. Stephen N. Heller, General Mills, Inc., Minneapolis, MN and Dr. Peter Uden, the Agricultural College of Sweden, Upsala, Sweden for their assis tance in marker analysis. We appreciate the help of Dr. Lucille Stiles, Research Dietitian, and Dr. Walter Federer, Department of Biometry and Plant Breeding, Cornell Uni versity for statistical consultation. Ms. Mau reen Taupley provided untiring assistance in processing biological samples. The computer facilities and programming assistance of Dr. James G. Oakes, the Raytheon Corporation, Northboro, MA, is gratefully acknowledged.
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16. Grovum, W. L. & Williams, V. J. (1973) Rate of passage of digesta in sheep. 3. Differential rates of passage of water and dry matter from the reticulorumen, abomasum and caecum, and proximal colon. Brit. J. Nutr. 30, 231-240. 17. Grovum, W. L. & Hecker, J. F. (1973) Rate of passage in sheep. 2. The effect of food intake on digesta retention times and on water and electrolyte absorption in the large intestine. Brit. J. Nutr. 30, 221-230. 18. Grovum, W. L. & Williams, V. J. (1977) Rate of passage of digesta in sheep. 6. The effect of level of food intake on mathematical predictions of the ki netics of digestion in the reticulo-rumen and intes tines. Brit. J. Nutr. 38, 425-436. 19. Stephen, A. M. & Cummings, J. H. (1979) Waterholding by dietary fibre in vitro and its relationship to faecal output in man. Gut 20, 722-729. 20. Kelsay, J. L. (1978) A review of research on effects of fiber intake in man. Am. J. Clin. Nutr. 31, S142S159. 21. Eastwood, M. A. & Mitchell, W. D. (1976) The physiological properties of dietary fiber: a biological evaluation. In: Fiber in Human Nutrition (Spiller, G. A. & Amen, R. J., eds.), pp. 109-130, Plenum Press, New York. 22. Van Soest, P. J. & Robertson,]. B. (1976) Chemical and physical properties of dietary fiber. In: Dietary Fibre (Hawkins, W. W., ed.), Proc. Miles Sympo sium, pp. 13-25, Nutrition Society of Canada, Dalhousie University, Halifax, N.S. 23. Van Soest, P. J. (1975) Physico-chemical aspects of fibre digestion. In: Proceedings of the Fourth In ternational Symposium on Ruminant Physiology (McDonald, I. W. & Warner, A. C. I., eds.), pp. 351365, University of New England Publishing Unit, Armidale, N.S.W., Australia. 24. Van Soest, P. J. & McQueen, R. W. (1973) The chemistry and estimation of fibre. Proc. Nutr. Soc. 32, 123-129. 25. Goering, H. K., & Van Soest, P. J. (1970) Forage fiber analyses (apparatus, reagents, procedures and some applications). Agrie. Handb. No. 379, pp. 1215, ARS, USDA, Washington, DC. 26. Wrick, K. L. F. (1979) The influence of dietary fibers on intestinal passage, taxation and stool char acteristics in humans. Ph.D. thesis, Cornell Univer sity, Ithaca, NY. 26a.Van Soest, P. J., Uden, P. & Wrick, K. L. (1983) Critique and evaluation of markers for use in hu mans and farm and laboratory animals. Nutr. Rep. Int. 27, 17-28. 27. Heller, S. N., Hackler, L. R., Rivers, J. M., Van Soest, P. J., Roe, D. A., Lewis, B. A. & Robertson, J. B. (1980) Dietary fiber: the effect of particle size of wheat bran on colonie function in young adult men. Am. J. Clin. Nutr. 33, 1734-1744. 28. Ehle, F. R., Robertson, J. B. & Van Soest, P. J. (1982) Influence of dietary fibers on fermentation in the human large intestine. J. Nutr. 112, 158-166. 29. Hinton, J. M., Lennard-Jones, J. E. & Young, A. C. (1969) A new method for studying gut transit time using radiopaque markers. Gut 10, 842-847. 30. Lutwak, L. & Burton, B. T. (1964) Fecal dye

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tistical Analysis System) Institute, Inc., Raleigh, NC. 39. Searle, S. R. (1971) Linear Models, pp. 135-163, John Wiley and Sons, Inc., New York. 40. Corbe, J. L., Greenhalgh, J. F. D. & Florence, E. (1959) Distribution of chromium sesquioxide and polyethyleneglycol in the reticulo-rumen of cattle. Brit. J. Nutr. J3, 337-345. 41. McConnell, A. A., Eastwood, M. A. & Mitchell, W. D. (1974) Physical characteristics of vegetable foodstuffs that could influence bowel function. J. Sci. Food Agrie. 25, 1457-1464. 42. Kirwan, W. O., Smith, A. N., McConnell, A. A., Mitchell, W. D. & Eastwood, M. A. (1974) Action of different bran preparations on colonie function. Brit. Med. J. 4, 187-189. 43. Van Soest, P. J. (1978) Nutritional value of dietary fibers for humans. GREG Project No. 1-RO 1-CA21016-01. Final Report. Department of Health, Ed ucation and Welfare, National Cancer Institute, Washington, DC. 44. Brodribb, A. J. M. & Groves, C. (1978) Effect of bran particle size on stool weight. Gut 19, 60-63. 45. Cowgill, J. R. & Anderson, W. E. (1932) Laxative effects of wheat bran and "washed bran" in healthy man. J. Am. Med. Assoc. 98, 1866-1875. 46. Wyman, J. B., Heaton, K. W., Manning, A. P. & Wicks, A. C. B. (1976) The effect on intestinal transit and the feces of raw and cooked bran in dif ferent doses. Am. J. Clin. Nutr. 29, 1474-1479.