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Effect of dietary fiber on gastrointestinal motility and jejunal transit time in dogs
GASTROENTEROLOGY
1981;80:701-7
Effect of Dietary Fiber on Gastrointestinal Motility and Jejunal Transit Time in Dogs L. BUENO, F. PRADDAUDE, Y. RUCKEBUSCH Department
of Physiology,
Veterinary
J. FIORAMONTI, School,
Strain gauge recordings of the motility of the antrum, duodenum, and jejunum were made in 10 dogs receiving a daily meal of canned food. Addition of 30 g of either wheat bran, cellulose, or guar gum increased the duration of the postprandial pattern of motility by 41-54s in the duodenum. Only cellulose and gum caused increases in the duration of the postprandial pattern of motility in the jejunum. The normal postprandial pattern of duodenojejunal contractions consisted of bursts of 4-10 rhythmic contractions. When bran or cellulose were added, the bursts were prolonged (12-15contractions per burst) with 4-15 min intervals between bursts. In contrast, when gum was added, contractions occurred continuously at a rate of 7-8/min, but their amplitude was one-half that seen with the other fibers. The increased number of low amplitude contractions when gum was added caused the postprandial motility index to double. There was no change in the motility index when cellulose was added. Guar gum also increased the frequency of antral contractions by 129%, while bran and cellulose had no effect. Jejunal transit time and flow of digesta were measured in four dogs 2 h after the meal. Addition of bran or gum increased the transit time by 28% and 51%, respectively, but cellulose caused a 900% increase in transit time associated with a 50% reduction in the flow of digesta. Addition of different fibers causes different alterations in postprandial motility. Jejunal transit of digesta appears unrelated to the pattern of contractions. Received February 3, 1980. Accepted October 24, 1980. Address requests for reprints to: Dr. L. Bueno, Ecole Nationale Vktkinaire, Departement de Physiologie, 23 Chemin des Capelles, 31076 Toulouse Cedex, France. This study was supported by INRA (Animal Pathology Dept.). The authors are grateful to V. Rayner for helpful discussion and criticism. The authors are also grateful to Mme M. J. Fargeas and Mr. J. P. Serthelon for their technical assistance. 0 1981 by the American Gastroenterological Association OOlS-5085/81/040701-07$02.50
Toulouse.
and
France
Dietary fiber has been defined as that part of plant material which is resistant to digestion by the secretions of the gastrointestinal tract. It comprises a heterogeneous group of carbohydrate compounds including cellulose and the hemicelluloses and a noncarbohydrate substance lignin. A class of soluble substances including pectins and gums may not be true fibers but are considered part of the dietary fiber complex, because of the similar effects they can elicit in the diet (1,Z). It has long been known that adding fiber-containing foods to the diet increases fecal bulk with a significant increase in the wet weight of stool (3,4). The time taken for food residues to pass through the gut is shortened by addition of bran to a low-residue diet in both humans (5) and pigs (6). This effect is probably related to the large bowel since McCance et al. by means of radiography found an increase of the small intestinal transit time (7). In dogs, the regular cyclic contractile activity of the small intestine is disrupted by feeding. This effect has been attributed to pancreatic or gastrointestinal hormones released by nutrients (8,9) and/or to the amount of food eaten (10,ll). However, the duration of the postprandial disruption of this cyclic pattern has not yet been investigated in relation to dietary fiber intake, particularly for substances differing in their hydration capacity (12). These experiments were performed in the dog by addition of three bulking agents (wheat bran, cellulose, or guar gum) to the meal to evaluate the patterns of postprandial activity elicited in the stomach and small intestine and to compare their effects on the postprandial jejunal transit time and flow rate of digesta.
Materials and Methods Ten
anesthetized
adult mongrel dogs weighing 15-18 kg were with halothane (fluothane nd). Strain gauge
702
GASTROENTEROLOGYVol.80,No.4
BUENOETAL.
transducers were sewn on the antrum, duodenum, and jejunum at 5, 20,and 120 cm from the pylorus, respectively. The transducers were constructed according to the method described by Pascaud et al. (13), and their axes were oriented transversely in order to record the circular muscle contraction. The free ends of the strain gauge wires were brought subcutaneously to the back of the neck, and the animals were allowed to recover for 15 days after surgery before beginning the experiments. Four of these dogs were fitted with a silicone catheter inserted into the duodenum 50 cm beyond the pylorus and with a Tshaped cannula inserted into the jejunum 206 cm distal to the catheter. Each day the dogs received a standard meal of 500 g of canned food (Fido), containing 21.7% of dry matter, 7.7%of protein, 4.5% of fat, 6.9% of carbohydrates, 2.6% of minerals, and 0.5% of fiber. Once every 3 days, 30 g of purified cellulose (Solka Floe), wheat bran, or guar gum (Normacol) was either added to the daily meal or replaced the daily meal diluted in 206 ml of tap water. Two times a week in the four dogs fitted with an intestinal cannula, flow of digesta and transit time of contents were determined concomitantly 2 h after feeding according to a method previously described (14). From 0 to 4 h after the meal, an isotonic solution containing 10 g/L (C,) of polyethylene glycol (PEG) 4000 was infused through the catheter at a constant rate (f) of 1.5 ml/min. Samples of digesta were taken from the cannula at 2-min intervals, 2-2.5 h after feeding. The flow of digesta (total flow-PEG infusion) was determined from the concentration (C,) of PEG found in the samples using the following equation: F = f (C, - C&/C,. To measure the transit time, a phenol red bolus (1 ml containing 20 mg phenolsulfonphthalein) was rapidly injected through the catheter 2 h after the meal. Phenolsulfonphthalein (PSP) concentration was determined from the same samples taken for PEG determination. The mean transit time was determined from the dye-dilution curves constructed from the measured concentration of PSP in samples taken from the cannula at 2-min intervals according to Barreiro et al. (15). The water-holding ability of cellulose, bran, and guar gum was measured in vitro by the centrifugation method (16). Mechanical activity was recorded continuously by connecting the gauges to a a-channel Wheatstone bridge amplifier (Vishay, France) connected to a potentiometric recorder. Amplitude calibration of each strain gauge was performed before implantation; the transducer was clamped firmly in a horizontal position at the level of the gauge. Weights (l-5 g) were hung 1 mm from the other soldering point, and the amplitude of the response (mV) was noted, and average calibration curves were obtained. Before the first recording session, corresponding DC voltages were injected to calibrate the potentiometric recorder. An hourly motility index was obtained by summation of the area registered over the baseline and expressed in g-minutes/hour using a planimeter (Bender and Hobein, Germany). The duration of the postprandial pattern of activity corresponded to the interval between feeding and the occurrence of a phase of regular contractions on the duodenojejunum lasting 3-4 min. This phase corresponds to
the phase III of the migrating myoelectric complex (MMC) and is followed by a period of quiescence. Additional information on the flow of digesta was obtained in one dog by radiologic examination using bariumsulfate contrast medium (micropaque) injected as a bolus through the jejunal catheter 2 h after feeding each of the diets.
Results Duration
of the Postprandial
Activity
In all dogs, feeding canned food alone disrupted the cyclic activity of the antrum and duodenojejunum, causing it to be replaced by a pattern of irregular contractile waves of variable amplitude. This “postprandial” pattern lasted 10.1 f 0.9 h (mean + SD for four individual values in 10 dogs; n = 40) for the duodenum and 7.4 & 1.2 h for the jejunum (Table 1). The duration of postprandial activity was significantly (p < 0.05) shorter for the jejunum than the duodenum (Table 1). When 30 g of bran was added to the meal, the duration of the postprandial pattern of activity was significantly increased for the duodenum (54%) but not for the jejunum. By contrast, addition of 30 g of cellulose to the meal increased significantly (p < 0.01) the duration of the postprandial pattern for both the duodenum (42%) and the jejunum (74%). Compared to bran, the duration of the postprandial pattern is more constant as indicated by a lower coefficient of variation (Table 1). The presence of gum (30 g) in the meal was also accompanied by longer duodenal (41%) and jejunal (63%) postprandial patterns of activity; regular contractions corresponding to the phase III of MMC appeared on the duodenum 14.3 & 2.1 h after feeding (Table 1).
Patterns
of Postprandial
Activity
Normal postprandial activity was characterized by irregular contractile waves on both antrum and small intestine; they occurred 100 min after the meal at a mean frequency of 1.7 -t 0.7/min (n = 40) for the antrum, 3.7 + O.G/min for the duodenum, and 4.9 & O.El/min for the jejunum (Table 2). Qualitatively, the postprandial mechanical activity consisted of contractions appearing singly (isolated) or rhythmically in series of 4-10 contractile waves representing, respectively, 40% and 60% of the total number of contractions. The mean motility index (gminutes/hour) for the 6 h after feeding was similar for the duodenum and jejunum on the control diet (Figure 1). In general, adding the bulky fiber increased the frequency of contractions in the 2 h after feeding.
April
1981
Table
1.
SMALL
BOWEL
MOTILITY
AND DIETARY
FIBER
703
Duration (Hours) of the Postprandial Pattern of the Small Intestine in 10 Dogs (Mean + SD for Four Meals) Receiving 500 g of Canned Food Alone (Control) or Mixed with 30 g of Bran, Cellulose, or Gum. Percent Change in Duration Relative to Control is indicated in Parentheses. Distance from pylorus (cm)
Control
20
10.1 + 0.9
Duodenum Jejunum
r’Significantly
With cellulose
With gum --
120
different
With bran 15.3 f 3.2O (53.1%) 6.8 + 1.8* (8.1%)
7.4 + 1.2b
(p 5 0.05) from
control
values.
b Significantly
There were, however, important differences in the effects of the different fibers (Table 2). Only guar gum significantly increased the frequency of antral contraction (by 129%). Both guar gum and cellulose increased the frequency of contraction in the duodenum (by 102% and 45%, respectively). In the jejunum all three fibers increased the contraction frequency (bran 36%, cellulose 31%, and guar gum 59%) in the 2 h after feeding (Table 2). Each of the three fibers added to the diet changed the pattern of contraction although guar gum had different effects from bran and cellulose. Bran and cellulose decreased the number of isolated contractions but increased the number of contractions occurring rhythmically in series from 4-lO/min on the control diet to lo-15/min (Figure 2). Eight to 10 such series now were seen each hour occurring at very variable intervals of 4-15 min (Figure 2). These changes lasted 5 h after the addition of cellulose but were limited to 3 h when bran was added. In contrast to these results for bran and cellulose, guar gum enhanced the occurrence of isolated contractions giving a pattern of uniform contractions at a higher frequency as already described. The amplitude of the contractions varied when the different fibers were added. With guar gum the contraction amplitude did not exceed 8 g-less than the 14-16 g maximum amplitude in the jejunum on the control diet. Both bran and cellulose enhanced the amplitude of the contractions in the jejunum in the first 2 h after feeding to 20 g. Thus, when gum was added, the contractions were only 40% of the maximum amplitude when bran or cellulose was added. Although bran and cellulose increased both the frequency and amplitude of contraction in the first 2-3 h after feeding, the hourly motility index (g-minutes/hour calculated over a 6-h period after feeding) was not increased and, in fact, was significantly decreased in the jejunum on the bran diet. But for gum, despite the lower amplitude of contractions, the duodenal and jejunal hourly motility indices (n = 40) were nearly double those of the control diet because
different
14.2 f 1.9” (42.3%) 12.9 + 1.5” (74.3%) (p s 0.05) from
values
14.3 f 2.1” (43.2%) 11.0 i 1.8” (48.6%) observed
of the increase in the frequency Table 1 and Figure 1).
on the duodenum.
of contractions
(see
Effect of Bran, Cellulose, and Gum in Fasted Animals water
Figure
Ingestion of 30 g of bran diluted in 200 ml of delayed the occurrence of a new phase of
1. Postprandial motor profile of the proximal intestine and dietary fiber in dogs (n = 10). Duration of irregular contractile waves and motility index of the contractile activity (with SD) are represented for the duodenum and jejunum at 20 and 120 cm from the pylorus, respectively. The duration of the postprandial motility was increased after addition of 30 g of bran or cellulose to the standard diet, but the motility index was not. Both duration and motility index were increased after addition of gum.
GASTROENTEROLOGY
BUENO ET AL.
704
Table 2.
Frequency per Minute of Antroduodenojejunal Contractions Recorded 100 to 140 min After a Meal, in 10 Dogs (Mean k SD, for Four Meals), Receiving Canned Food Alone (Control) or Mixed with 30 g of Bran, Cellulose, or Gum Duodenum
Antrum
Jejunum
Control Bran Cellulose
1.7 * 0.7 1.9 + 0.5 1.8 f 0.5
3.7 k 0.6 4.4 f 1.3 5.4 + 0.9”
4.9 f 0.8 6.7 k 1.1” 6.4 It 1.2”
Gum
3.9 f 0.40
7.5 + 1.2”
7.0 f 0.7O
a Significantly
different
(cm)
Dc.tonce f ram
control
values.
regular
contractions (phase III of MMC) by 40-60 min on both the duodenum and the jejunum. Contractions occurred in series of 7-12 contractions sep-
arated by quiescent periods from 30 s to 4 min long. These were similar in pattern and duration to those observed when bran was added to a meal (Figure 3). The first normal MMC started on the jejunum 2.5 +0.5 h after bran feeding. The next MMC started on the duodenum 2.5 h later. A similar pattern of contractions was observed after the ingestion of cellulose. The delay before the appearance of the first
BRAN
pybxus
\
II.
(P 5 0.05) from
Vol. 80, No. 4
I
n
JJ
. I1
+20
.
.I20 t Feedlng
Figure
I
lzn
GUM
Feedlng
I hour
#l I min
at two different speeds 2. Recordings of the contractile activity of the antrum, duodenum, and jejunum after a fasted dog was given a meal containing 30 g of either bran (upper panel) or gum (lower panel), mixed with 200 ml water. The postprandial pattern of activity consisted of series of contractions for bran and omnipresent contractions of small amplitude for gum on both antrum and small intestine.
April
1981
SMALL
Antrum
( -5 cm
Duodenum(
J...
from
pylorus
from
BRAN
FIBER
705
pylorus
)
&JkUJ,.__
__I
I
(309)
hour
)l
MMC in the jejunum was less (35-45 min), and the MMC reappeared on the duodenum sooner than when bran was ingested. Guar gum ingested alone induced a pattern of uniform contractions similar to that observed when it was added to a meal. There was a 3.5-4-h disruption of MMC on the duodenum. Postprandial Rate
AND DIETARY
)
mm
t
3. Effects of ingestion of 30 g of bran, gum, or cellulose mixed with 200 ml water on the activity of the antrum, duodenum, and jejunum of a fasted dog. Total disruption of the MMC pattern occurred with gum and is associated with omnipresent contractions of small amplitude.
MOTILITY
- 20 cm from pylorus)
120 cm
Figure
BOWEL
Transit Time and Digesta-Flow
The jejunal mean transit time calculated from the dye-dilution curve of a PSP bolus injected 2 h after a standard meal was 9.5 f 1.7 min (mean f SD, n = 24) and was increased by 28 and 51%, respectively, when bran or gum was added. In the case of cellulose, a ninefold increase in the transit time was recorded (Figure 4). The flow rate of digesta measured from 2 to 4 h after a meal varied from 115 ml/ h to 310 ml/h (Table 3). This flow rate was slightly reduced with bran and was more than halved with cellulose. In the case of gum, the flow rate increased considerably (66%) so that the mean volume of contents in the intestinal segment, calculated as flow X transit time was twice that obtained for the standard meal with or without bran. Radiology Radiologic examination of one dog showed that, with the control and bran-added diets, digesta
u
GUM
(3Og)
I hour A__J
was mixed and moved onwards by slow peristalsis. With the cellulose-added diet, mixing movements with little onward propulsion of digesta occurred. With the guar gum-added diet, the jejunum was distended, and motility consisted of mixing movements with occasional onward propulsion of digesta. After an incubation of 12 h at 37.5X measurement of water-holding by the centrifugation method indicated that 1 g of gum was able to retain 23 g of water (Table 3) which was three and four times more than cellulose (7 g) and bran (5 g), respectively. Discussion Although there have been many studies on the effects of dietary fiber on colonic transit times and on the composition and amount of feces (l), no experiments have been reported on changes in small bowel motility after the addition of fiber. The addition of fiber may have profound effects on the responses of the stomach and small intestine to food; the increase in bulk of digesta may slow gastric emptying, such as has been demonstrated for guar gum in humans (17), and alter the rate of small intestinal flow, the rate of absorption, and the neuroendocrine responses to this food. In this paper we present data showing that the addition of three different dietary fibers increases the duration of the postprandial disruption of the MMC pattern of motility, suggesting that the bulking activ-
706
BUENO ET AL.
GASTROENTEROLOGY
J
06,
CELLULOSE
GUM 40
20
0
0
CONTROL 0
Figure
4.
20
BRAN
I 122 t
2 7 ml”
I
:3cim,n)
4 3 m,n
)
( 9 5
*
40mln
Phenolsulfonphthalein (PSP) concentration curves and mean transit time measured over 2 m of jejunum by injection of a PSP bolus, 2 h after feeding in dogs fed with 566 g of a standard meal, given alone or mixed with 30 g of bran, gum, or cellulose.
ing cellulose or bran had similar effects on duodenojejunal motility; yet cellulose decreased flow and prolonged the transit time, while bran had little effect on either of these parameters. In order to check that these unexpected results were not merely an artifact of the protocol used, one dog was subjected to radiology 2 h after meals of each of the four diets. With the control and the bran-added diets, contractions caused both to and fro, mixing and onward propulsion of digesta. In the diet containing the Solka floe cellulose, the contractions caused little onward movement of digesta. We suggest that this refined cellulose adheres to the intestinal wall and prevents onward propulsion. The addition of guar gum to the diet caused a pattern of continuous low-amplitude contractions with an increase in the motility index. The marker data indicated that jejunal flow was increased yet the transit time was prolonged suggesting that the intestine was distended. This may be caused by the large amounts of water absorbed by guar gum. The radiologic examination did show a distended intestine. Although at times the contractions appeared to mix but not to propel digesta onwards in a manner similar to that in the cellulose-containing meal,
Transit Time and Flow Rate of Digesta Through a ZOO-cm JejunaJ Segment from 2 to 4 h After Feeding 500 g of a Standard Diet Alone (Control) or Mixed with 30 g of Bran, Cellulose, or Gum (Values are Mean f SD for Four Meals on Each Regimen for Six Dogs)
Transit time” (mm) Flow rate of digesta (ml/h) Retention volume” (ml) Water holding (g per g of DM) a Retention
(I43
ml”
40 rnjn
ity of these fibers prolongs the period of rapid gastric emptying and small intestinal flow. The disruption was longest on the diet containing the fiber with the highest bulking activity, namely guar gum. No conclusion about the rate of gastric emptying can be made-only that the period of rapid emptying must have been prolonged. Disruption of the MMC for shorter periods was also produced by feeding each fiber alone. These results confirm once more the importance of digesta bulk apart from any hormonal or humoral effects in inducing the postprandial pattern of motility (10,ll). The three different fibers all altered the pattern and frequency of the contractions from that of the control diet. However, guar gum gave a different pattern of contraction from Solka floe cellulose and bran. The latter two fibers are both cellulose plus some hemicellulose, although they are rather different in their physical structure and particle size. Guar gum is a galactomannose polymer and has by far the greatest capacity to retain water. It is not surprising that it should induce a different motility pattern from the other fibers. More unexpected were the results of jejunal flow rate and transit time measurements. Meals containTable 3.
Vol. 88, No. 4
Control
Bran
9.5 f 2.7 172 f 41 27.2 -
12.2 * 4.3 16lf34
32.7 5.5f 1.5
Cellulose
Gum
82.3 f 10.3b
14.3 f 3.6b
55 flBb
285f 54b
75.4 7.1f 0.7
67.9 22.6f 1.2
volume calculated from the flow rate (ml/min) of digesta and the mean transit time (min). b Significantly different (p < 0.05) from control values.
SMALL BOWEL MOTILITY AND DIETARY FIBER
April 1981
occasionally a single contraction would move digesta onward a considerable distance. These findings thus confirm the flow and transit time data, although the low amplitude of contractions remains difficult to explain. Responses of flexible strain gauges in vivo are somewhat complex and their responses to active contraction of the intestinal wall, when under this passive stretch, may be less than expected from their calibration in vitro. These results then indicate that fibers alter small intestinal transit, digesta flow, and motility. The effects seem to differ for different fibers. The physical form of the fiber seems to be of particular importance as bran and Solka floe cellulose are similar in their chemical composition, yet have very different effects on digesta flow.
6. Fioramonti
7.
8.
9. 10.
11.
12.
13.
References 1. Cummings
JH. Dietary fibre. Gut 1973;14:69-81. 2. Van Soest PJ. Dietary fibers: their definition and nutritional properties. Am J Clin Nutr 1978;31:21-30. 3. Williams RD, Olmsted WH. The effect of cellulose, hemicellulose, and lignin on the weight of the stool. A contribution to the study of laxation in man. J Nutr 1936;11:433-49. 4. Eastwood MA, Hamilton T, Kirkpatrick JR, et al. The effects of dietary supplements of wheat bran and cellulose on faeces. Proc Nutr Sot 1973;32:22A. 5. Hinton JM, Lennard-Jones JG, Young AC. A new method for studying gut transit 1969;10:842-7.
times using radioopaque
markers.
Gut
14.
15.
16.
17.
707
J, Bueno L. Motor activity in the large intestine of the pig related to dietary fibres and retention time. Br J Nutr 1986;45:155-62. McCance RA, Prior KM, Widdowson EM. A radiological study of the rate of passage of brown and white bread through the digestive tract of man. Br J Nutr 1953;7:98-104. Weisbrodt NW, Copeland EM, Kearley RW, et al. Effects of pentagastrin on electrical activity of small intestine of the dog. Am J Physiol 1974;227:425-9. Bueno L, Ruckebusch M. Insulin and jejunal electrical activity in dogs and sheep. Am J Physiol 1976;230:1538-44. De Wever I, Eeckhout C, Vantrappen G, et al. Disruption effect of test meals on interdigestive motor complex in dogs. Am J Physiol 1978;4:E661-665. Eeckhout C, De Wever 1, Peeters T, et al. Role of gastrin and insulin in post-prandial disruption of migrating complex in dogs. Am J Physiol 1978;4:E666-9. Stephen AM, Cummings JH. Water holding by dietary fibre in vitro and its relationship to faecal output in man. Gut 1979;20:772-9. Pascaud XB, Genton HJH, Bass P. A miniature transducer for recording intestinal motility in unrestrained chronic rats. Am J Physiol 1978;235:E532-8. Bueno L, Fioramonti J, Ruckebusch Y. Rate of flow of digesta and electrical activity of the small intestine in dogs and sheep. J Physiol 1975;249:69-85. Barreiro MA, McKenna RD, Beck Il. Determination of transit time in the human jejunum in the simple injection indicatordilution technique. Am J Dig Dis 1968;13:222-32. McConnell AA, Eastwood MA, Mitchell WD. Physical characteristics of vegetable foodstuffs that could influence bowel function. J Sci Food Agric 1974;25:1457-1564. Holt S, Heading RC, Carter DC, Prescott LF, Tothill P. Effect of gel fibre on gastric emptying and absorption of glucose and paracetamol. Lancet 1979:24:636-g.
1981;80:701-7
Effect of Dietary Fiber on Gastrointestinal Motility and Jejunal Transit Time in Dogs L. BUENO, F. PRADDAUDE, Y. RUCKEBUSCH Department
of Physiology,
Veterinary
J. FIORAMONTI, School,
Strain gauge recordings of the motility of the antrum, duodenum, and jejunum were made in 10 dogs receiving a daily meal of canned food. Addition of 30 g of either wheat bran, cellulose, or guar gum increased the duration of the postprandial pattern of motility by 41-54s in the duodenum. Only cellulose and gum caused increases in the duration of the postprandial pattern of motility in the jejunum. The normal postprandial pattern of duodenojejunal contractions consisted of bursts of 4-10 rhythmic contractions. When bran or cellulose were added, the bursts were prolonged (12-15contractions per burst) with 4-15 min intervals between bursts. In contrast, when gum was added, contractions occurred continuously at a rate of 7-8/min, but their amplitude was one-half that seen with the other fibers. The increased number of low amplitude contractions when gum was added caused the postprandial motility index to double. There was no change in the motility index when cellulose was added. Guar gum also increased the frequency of antral contractions by 129%, while bran and cellulose had no effect. Jejunal transit time and flow of digesta were measured in four dogs 2 h after the meal. Addition of bran or gum increased the transit time by 28% and 51%, respectively, but cellulose caused a 900% increase in transit time associated with a 50% reduction in the flow of digesta. Addition of different fibers causes different alterations in postprandial motility. Jejunal transit of digesta appears unrelated to the pattern of contractions. Received February 3, 1980. Accepted October 24, 1980. Address requests for reprints to: Dr. L. Bueno, Ecole Nationale Vktkinaire, Departement de Physiologie, 23 Chemin des Capelles, 31076 Toulouse Cedex, France. This study was supported by INRA (Animal Pathology Dept.). The authors are grateful to V. Rayner for helpful discussion and criticism. The authors are also grateful to Mme M. J. Fargeas and Mr. J. P. Serthelon for their technical assistance. 0 1981 by the American Gastroenterological Association OOlS-5085/81/040701-07$02.50
Toulouse.
and
France
Dietary fiber has been defined as that part of plant material which is resistant to digestion by the secretions of the gastrointestinal tract. It comprises a heterogeneous group of carbohydrate compounds including cellulose and the hemicelluloses and a noncarbohydrate substance lignin. A class of soluble substances including pectins and gums may not be true fibers but are considered part of the dietary fiber complex, because of the similar effects they can elicit in the diet (1,Z). It has long been known that adding fiber-containing foods to the diet increases fecal bulk with a significant increase in the wet weight of stool (3,4). The time taken for food residues to pass through the gut is shortened by addition of bran to a low-residue diet in both humans (5) and pigs (6). This effect is probably related to the large bowel since McCance et al. by means of radiography found an increase of the small intestinal transit time (7). In dogs, the regular cyclic contractile activity of the small intestine is disrupted by feeding. This effect has been attributed to pancreatic or gastrointestinal hormones released by nutrients (8,9) and/or to the amount of food eaten (10,ll). However, the duration of the postprandial disruption of this cyclic pattern has not yet been investigated in relation to dietary fiber intake, particularly for substances differing in their hydration capacity (12). These experiments were performed in the dog by addition of three bulking agents (wheat bran, cellulose, or guar gum) to the meal to evaluate the patterns of postprandial activity elicited in the stomach and small intestine and to compare their effects on the postprandial jejunal transit time and flow rate of digesta.
Materials and Methods Ten
anesthetized
adult mongrel dogs weighing 15-18 kg were with halothane (fluothane nd). Strain gauge
702
GASTROENTEROLOGYVol.80,No.4
BUENOETAL.
transducers were sewn on the antrum, duodenum, and jejunum at 5, 20,and 120 cm from the pylorus, respectively. The transducers were constructed according to the method described by Pascaud et al. (13), and their axes were oriented transversely in order to record the circular muscle contraction. The free ends of the strain gauge wires were brought subcutaneously to the back of the neck, and the animals were allowed to recover for 15 days after surgery before beginning the experiments. Four of these dogs were fitted with a silicone catheter inserted into the duodenum 50 cm beyond the pylorus and with a Tshaped cannula inserted into the jejunum 206 cm distal to the catheter. Each day the dogs received a standard meal of 500 g of canned food (Fido), containing 21.7% of dry matter, 7.7%of protein, 4.5% of fat, 6.9% of carbohydrates, 2.6% of minerals, and 0.5% of fiber. Once every 3 days, 30 g of purified cellulose (Solka Floe), wheat bran, or guar gum (Normacol) was either added to the daily meal or replaced the daily meal diluted in 206 ml of tap water. Two times a week in the four dogs fitted with an intestinal cannula, flow of digesta and transit time of contents were determined concomitantly 2 h after feeding according to a method previously described (14). From 0 to 4 h after the meal, an isotonic solution containing 10 g/L (C,) of polyethylene glycol (PEG) 4000 was infused through the catheter at a constant rate (f) of 1.5 ml/min. Samples of digesta were taken from the cannula at 2-min intervals, 2-2.5 h after feeding. The flow of digesta (total flow-PEG infusion) was determined from the concentration (C,) of PEG found in the samples using the following equation: F = f (C, - C&/C,. To measure the transit time, a phenol red bolus (1 ml containing 20 mg phenolsulfonphthalein) was rapidly injected through the catheter 2 h after the meal. Phenolsulfonphthalein (PSP) concentration was determined from the same samples taken for PEG determination. The mean transit time was determined from the dye-dilution curves constructed from the measured concentration of PSP in samples taken from the cannula at 2-min intervals according to Barreiro et al. (15). The water-holding ability of cellulose, bran, and guar gum was measured in vitro by the centrifugation method (16). Mechanical activity was recorded continuously by connecting the gauges to a a-channel Wheatstone bridge amplifier (Vishay, France) connected to a potentiometric recorder. Amplitude calibration of each strain gauge was performed before implantation; the transducer was clamped firmly in a horizontal position at the level of the gauge. Weights (l-5 g) were hung 1 mm from the other soldering point, and the amplitude of the response (mV) was noted, and average calibration curves were obtained. Before the first recording session, corresponding DC voltages were injected to calibrate the potentiometric recorder. An hourly motility index was obtained by summation of the area registered over the baseline and expressed in g-minutes/hour using a planimeter (Bender and Hobein, Germany). The duration of the postprandial pattern of activity corresponded to the interval between feeding and the occurrence of a phase of regular contractions on the duodenojejunum lasting 3-4 min. This phase corresponds to
the phase III of the migrating myoelectric complex (MMC) and is followed by a period of quiescence. Additional information on the flow of digesta was obtained in one dog by radiologic examination using bariumsulfate contrast medium (micropaque) injected as a bolus through the jejunal catheter 2 h after feeding each of the diets.
Results Duration
of the Postprandial
Activity
In all dogs, feeding canned food alone disrupted the cyclic activity of the antrum and duodenojejunum, causing it to be replaced by a pattern of irregular contractile waves of variable amplitude. This “postprandial” pattern lasted 10.1 f 0.9 h (mean + SD for four individual values in 10 dogs; n = 40) for the duodenum and 7.4 & 1.2 h for the jejunum (Table 1). The duration of postprandial activity was significantly (p < 0.05) shorter for the jejunum than the duodenum (Table 1). When 30 g of bran was added to the meal, the duration of the postprandial pattern of activity was significantly increased for the duodenum (54%) but not for the jejunum. By contrast, addition of 30 g of cellulose to the meal increased significantly (p < 0.01) the duration of the postprandial pattern for both the duodenum (42%) and the jejunum (74%). Compared to bran, the duration of the postprandial pattern is more constant as indicated by a lower coefficient of variation (Table 1). The presence of gum (30 g) in the meal was also accompanied by longer duodenal (41%) and jejunal (63%) postprandial patterns of activity; regular contractions corresponding to the phase III of MMC appeared on the duodenum 14.3 & 2.1 h after feeding (Table 1).
Patterns
of Postprandial
Activity
Normal postprandial activity was characterized by irregular contractile waves on both antrum and small intestine; they occurred 100 min after the meal at a mean frequency of 1.7 -t 0.7/min (n = 40) for the antrum, 3.7 + O.G/min for the duodenum, and 4.9 & O.El/min for the jejunum (Table 2). Qualitatively, the postprandial mechanical activity consisted of contractions appearing singly (isolated) or rhythmically in series of 4-10 contractile waves representing, respectively, 40% and 60% of the total number of contractions. The mean motility index (gminutes/hour) for the 6 h after feeding was similar for the duodenum and jejunum on the control diet (Figure 1). In general, adding the bulky fiber increased the frequency of contractions in the 2 h after feeding.
April
1981
Table
1.
SMALL
BOWEL
MOTILITY
AND DIETARY
FIBER
703
Duration (Hours) of the Postprandial Pattern of the Small Intestine in 10 Dogs (Mean + SD for Four Meals) Receiving 500 g of Canned Food Alone (Control) or Mixed with 30 g of Bran, Cellulose, or Gum. Percent Change in Duration Relative to Control is indicated in Parentheses. Distance from pylorus (cm)
Control
20
10.1 + 0.9
Duodenum Jejunum
r’Significantly
With cellulose
With gum --
120
different
With bran 15.3 f 3.2O (53.1%) 6.8 + 1.8* (8.1%)
7.4 + 1.2b
(p 5 0.05) from
control
values.
b Significantly
There were, however, important differences in the effects of the different fibers (Table 2). Only guar gum significantly increased the frequency of antral contraction (by 129%). Both guar gum and cellulose increased the frequency of contraction in the duodenum (by 102% and 45%, respectively). In the jejunum all three fibers increased the contraction frequency (bran 36%, cellulose 31%, and guar gum 59%) in the 2 h after feeding (Table 2). Each of the three fibers added to the diet changed the pattern of contraction although guar gum had different effects from bran and cellulose. Bran and cellulose decreased the number of isolated contractions but increased the number of contractions occurring rhythmically in series from 4-lO/min on the control diet to lo-15/min (Figure 2). Eight to 10 such series now were seen each hour occurring at very variable intervals of 4-15 min (Figure 2). These changes lasted 5 h after the addition of cellulose but were limited to 3 h when bran was added. In contrast to these results for bran and cellulose, guar gum enhanced the occurrence of isolated contractions giving a pattern of uniform contractions at a higher frequency as already described. The amplitude of the contractions varied when the different fibers were added. With guar gum the contraction amplitude did not exceed 8 g-less than the 14-16 g maximum amplitude in the jejunum on the control diet. Both bran and cellulose enhanced the amplitude of the contractions in the jejunum in the first 2 h after feeding to 20 g. Thus, when gum was added, the contractions were only 40% of the maximum amplitude when bran or cellulose was added. Although bran and cellulose increased both the frequency and amplitude of contraction in the first 2-3 h after feeding, the hourly motility index (g-minutes/hour calculated over a 6-h period after feeding) was not increased and, in fact, was significantly decreased in the jejunum on the bran diet. But for gum, despite the lower amplitude of contractions, the duodenal and jejunal hourly motility indices (n = 40) were nearly double those of the control diet because
different
14.2 f 1.9” (42.3%) 12.9 + 1.5” (74.3%) (p s 0.05) from
values
14.3 f 2.1” (43.2%) 11.0 i 1.8” (48.6%) observed
of the increase in the frequency Table 1 and Figure 1).
on the duodenum.
of contractions
(see
Effect of Bran, Cellulose, and Gum in Fasted Animals water
Figure
Ingestion of 30 g of bran diluted in 200 ml of delayed the occurrence of a new phase of
1. Postprandial motor profile of the proximal intestine and dietary fiber in dogs (n = 10). Duration of irregular contractile waves and motility index of the contractile activity (with SD) are represented for the duodenum and jejunum at 20 and 120 cm from the pylorus, respectively. The duration of the postprandial motility was increased after addition of 30 g of bran or cellulose to the standard diet, but the motility index was not. Both duration and motility index were increased after addition of gum.
GASTROENTEROLOGY
BUENO ET AL.
704
Table 2.
Frequency per Minute of Antroduodenojejunal Contractions Recorded 100 to 140 min After a Meal, in 10 Dogs (Mean k SD, for Four Meals), Receiving Canned Food Alone (Control) or Mixed with 30 g of Bran, Cellulose, or Gum Duodenum
Antrum
Jejunum
Control Bran Cellulose
1.7 * 0.7 1.9 + 0.5 1.8 f 0.5
3.7 k 0.6 4.4 f 1.3 5.4 + 0.9”
4.9 f 0.8 6.7 k 1.1” 6.4 It 1.2”
Gum
3.9 f 0.40
7.5 + 1.2”
7.0 f 0.7O
a Significantly
different
(cm)
Dc.tonce f ram
control
values.
regular
contractions (phase III of MMC) by 40-60 min on both the duodenum and the jejunum. Contractions occurred in series of 7-12 contractions sep-
arated by quiescent periods from 30 s to 4 min long. These were similar in pattern and duration to those observed when bran was added to a meal (Figure 3). The first normal MMC started on the jejunum 2.5 +0.5 h after bran feeding. The next MMC started on the duodenum 2.5 h later. A similar pattern of contractions was observed after the ingestion of cellulose. The delay before the appearance of the first
BRAN
pybxus
\
II.
(P 5 0.05) from
Vol. 80, No. 4
I
n
JJ
. I1
+20
.
.I20 t Feedlng
Figure
I
lzn
GUM
Feedlng
I hour
#l I min
at two different speeds 2. Recordings of the contractile activity of the antrum, duodenum, and jejunum after a fasted dog was given a meal containing 30 g of either bran (upper panel) or gum (lower panel), mixed with 200 ml water. The postprandial pattern of activity consisted of series of contractions for bran and omnipresent contractions of small amplitude for gum on both antrum and small intestine.
April
1981
SMALL
Antrum
( -5 cm
Duodenum(
J...
from
pylorus
from
BRAN
FIBER
705
pylorus
)
&JkUJ,.__
__I
I
(309)
hour
)l
MMC in the jejunum was less (35-45 min), and the MMC reappeared on the duodenum sooner than when bran was ingested. Guar gum ingested alone induced a pattern of uniform contractions similar to that observed when it was added to a meal. There was a 3.5-4-h disruption of MMC on the duodenum. Postprandial Rate
AND DIETARY
)
mm
t
3. Effects of ingestion of 30 g of bran, gum, or cellulose mixed with 200 ml water on the activity of the antrum, duodenum, and jejunum of a fasted dog. Total disruption of the MMC pattern occurred with gum and is associated with omnipresent contractions of small amplitude.
MOTILITY
- 20 cm from pylorus)
120 cm
Figure
BOWEL
Transit Time and Digesta-Flow
The jejunal mean transit time calculated from the dye-dilution curve of a PSP bolus injected 2 h after a standard meal was 9.5 f 1.7 min (mean f SD, n = 24) and was increased by 28 and 51%, respectively, when bran or gum was added. In the case of cellulose, a ninefold increase in the transit time was recorded (Figure 4). The flow rate of digesta measured from 2 to 4 h after a meal varied from 115 ml/ h to 310 ml/h (Table 3). This flow rate was slightly reduced with bran and was more than halved with cellulose. In the case of gum, the flow rate increased considerably (66%) so that the mean volume of contents in the intestinal segment, calculated as flow X transit time was twice that obtained for the standard meal with or without bran. Radiology Radiologic examination of one dog showed that, with the control and bran-added diets, digesta
u
GUM
(3Og)
I hour A__J
was mixed and moved onwards by slow peristalsis. With the cellulose-added diet, mixing movements with little onward propulsion of digesta occurred. With the guar gum-added diet, the jejunum was distended, and motility consisted of mixing movements with occasional onward propulsion of digesta. After an incubation of 12 h at 37.5X measurement of water-holding by the centrifugation method indicated that 1 g of gum was able to retain 23 g of water (Table 3) which was three and four times more than cellulose (7 g) and bran (5 g), respectively. Discussion Although there have been many studies on the effects of dietary fiber on colonic transit times and on the composition and amount of feces (l), no experiments have been reported on changes in small bowel motility after the addition of fiber. The addition of fiber may have profound effects on the responses of the stomach and small intestine to food; the increase in bulk of digesta may slow gastric emptying, such as has been demonstrated for guar gum in humans (17), and alter the rate of small intestinal flow, the rate of absorption, and the neuroendocrine responses to this food. In this paper we present data showing that the addition of three different dietary fibers increases the duration of the postprandial disruption of the MMC pattern of motility, suggesting that the bulking activ-
706
BUENO ET AL.
GASTROENTEROLOGY
J
06,
CELLULOSE
GUM 40
20
0
0
CONTROL 0
Figure
4.
20
BRAN
I 122 t
2 7 ml”
I
:3cim,n)
4 3 m,n
)
( 9 5
*
40mln
Phenolsulfonphthalein (PSP) concentration curves and mean transit time measured over 2 m of jejunum by injection of a PSP bolus, 2 h after feeding in dogs fed with 566 g of a standard meal, given alone or mixed with 30 g of bran, gum, or cellulose.
ing cellulose or bran had similar effects on duodenojejunal motility; yet cellulose decreased flow and prolonged the transit time, while bran had little effect on either of these parameters. In order to check that these unexpected results were not merely an artifact of the protocol used, one dog was subjected to radiology 2 h after meals of each of the four diets. With the control and the bran-added diets, contractions caused both to and fro, mixing and onward propulsion of digesta. In the diet containing the Solka floe cellulose, the contractions caused little onward movement of digesta. We suggest that this refined cellulose adheres to the intestinal wall and prevents onward propulsion. The addition of guar gum to the diet caused a pattern of continuous low-amplitude contractions with an increase in the motility index. The marker data indicated that jejunal flow was increased yet the transit time was prolonged suggesting that the intestine was distended. This may be caused by the large amounts of water absorbed by guar gum. The radiologic examination did show a distended intestine. Although at times the contractions appeared to mix but not to propel digesta onwards in a manner similar to that in the cellulose-containing meal,
Transit Time and Flow Rate of Digesta Through a ZOO-cm JejunaJ Segment from 2 to 4 h After Feeding 500 g of a Standard Diet Alone (Control) or Mixed with 30 g of Bran, Cellulose, or Gum (Values are Mean f SD for Four Meals on Each Regimen for Six Dogs)
Transit time” (mm) Flow rate of digesta (ml/h) Retention volume” (ml) Water holding (g per g of DM) a Retention
(I43
ml”
40 rnjn
ity of these fibers prolongs the period of rapid gastric emptying and small intestinal flow. The disruption was longest on the diet containing the fiber with the highest bulking activity, namely guar gum. No conclusion about the rate of gastric emptying can be made-only that the period of rapid emptying must have been prolonged. Disruption of the MMC for shorter periods was also produced by feeding each fiber alone. These results confirm once more the importance of digesta bulk apart from any hormonal or humoral effects in inducing the postprandial pattern of motility (10,ll). The three different fibers all altered the pattern and frequency of the contractions from that of the control diet. However, guar gum gave a different pattern of contraction from Solka floe cellulose and bran. The latter two fibers are both cellulose plus some hemicellulose, although they are rather different in their physical structure and particle size. Guar gum is a galactomannose polymer and has by far the greatest capacity to retain water. It is not surprising that it should induce a different motility pattern from the other fibers. More unexpected were the results of jejunal flow rate and transit time measurements. Meals containTable 3.
Vol. 88, No. 4
Control
Bran
9.5 f 2.7 172 f 41 27.2 -
12.2 * 4.3 16lf34
32.7 5.5f 1.5
Cellulose
Gum
82.3 f 10.3b
14.3 f 3.6b
55 flBb
285f 54b
75.4 7.1f 0.7
67.9 22.6f 1.2
volume calculated from the flow rate (ml/min) of digesta and the mean transit time (min). b Significantly different (p < 0.05) from control values.
SMALL BOWEL MOTILITY AND DIETARY FIBER
April 1981
occasionally a single contraction would move digesta onward a considerable distance. These findings thus confirm the flow and transit time data, although the low amplitude of contractions remains difficult to explain. Responses of flexible strain gauges in vivo are somewhat complex and their responses to active contraction of the intestinal wall, when under this passive stretch, may be less than expected from their calibration in vitro. These results then indicate that fibers alter small intestinal transit, digesta flow, and motility. The effects seem to differ for different fibers. The physical form of the fiber seems to be of particular importance as bran and Solka floe cellulose are similar in their chemical composition, yet have very different effects on digesta flow.
6. Fioramonti
7.
8.
9. 10.
11.
12.
13.
References 1. Cummings
JH. Dietary fibre. Gut 1973;14:69-81. 2. Van Soest PJ. Dietary fibers: their definition and nutritional properties. Am J Clin Nutr 1978;31:21-30. 3. Williams RD, Olmsted WH. The effect of cellulose, hemicellulose, and lignin on the weight of the stool. A contribution to the study of laxation in man. J Nutr 1936;11:433-49. 4. Eastwood MA, Hamilton T, Kirkpatrick JR, et al. The effects of dietary supplements of wheat bran and cellulose on faeces. Proc Nutr Sot 1973;32:22A. 5. Hinton JM, Lennard-Jones JG, Young AC. A new method for studying gut transit 1969;10:842-7.
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markers.
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707
J, Bueno L. Motor activity in the large intestine of the pig related to dietary fibres and retention time. Br J Nutr 1986;45:155-62. McCance RA, Prior KM, Widdowson EM. A radiological study of the rate of passage of brown and white bread through the digestive tract of man. Br J Nutr 1953;7:98-104. Weisbrodt NW, Copeland EM, Kearley RW, et al. Effects of pentagastrin on electrical activity of small intestine of the dog. Am J Physiol 1974;227:425-9. Bueno L, Ruckebusch M. Insulin and jejunal electrical activity in dogs and sheep. Am J Physiol 1976;230:1538-44. De Wever I, Eeckhout C, Vantrappen G, et al. Disruption effect of test meals on interdigestive motor complex in dogs. Am J Physiol 1978;4:E661-665. Eeckhout C, De Wever 1, Peeters T, et al. Role of gastrin and insulin in post-prandial disruption of migrating complex in dogs. Am J Physiol 1978;4:E666-9. Stephen AM, Cummings JH. Water holding by dietary fibre in vitro and its relationship to faecal output in man. Gut 1979;20:772-9. Pascaud XB, Genton HJH, Bass P. A miniature transducer for recording intestinal motility in unrestrained chronic rats. Am J Physiol 1978;235:E532-8. Bueno L, Fioramonti J, Ruckebusch Y. Rate of flow of digesta and electrical activity of the small intestine in dogs and sheep. J Physiol 1975;249:69-85. Barreiro MA, McKenna RD, Beck Il. Determination of transit time in the human jejunum in the simple injection indicatordilution technique. Am J Dig Dis 1968;13:222-32. McConnell AA, Eastwood MA, Mitchell WD. Physical characteristics of vegetable foodstuffs that could influence bowel function. J Sci Food Agric 1974;25:1457-1564. Holt S, Heading RC, Carter DC, Prescott LF, Tothill P. Effect of gel fibre on gastric emptying and absorption of glucose and paracetamol. Lancet 1979:24:636-g.