Comparative effect of water-soluble and -insoluble dietary fiber on bowel function in rats fed a liquid elemental diet

NutritionResearch,W. 18,No. 5. pp. 883491.1998 Copyright0 1998Elsevia ScienceInc. printedin theUSA. All ri&ts resaved 0271~5317/98 $19.00+ .OO ELSEVIER

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COMPARATIVE EFFECT OF WATER-SOLUBLE AND -INSOLUBLE DIETARY ON BOWEL FUNCTION IN RATS FED A LIQUID ELEMENTAL DIET

FIBER

Kiyoshi Ebihara, PhD and Yoshihisa Nakamoto, BS Department of Biological Resources, Faculty of Agriculture, Ehime University, Matsuyama 790-0905, Japan

The effect of dietary fibers on the digestive tract mass, diamine oxidase (DAO) activities in the small intestine and plasma and pool of ammonia and organic acids such as acetic, propionic, butyric, lactic and succinic acid in the cecum in rats fed a liquid formula diet was compared. Rats were fed an elemental liquid diet (ED) or ED containing 3g/lOO ml of dietary fiber either a mixture of crystal cellulose and carboxymethyl cellulose sodium salt (CC), sugar-beet pectin (BP) or hydrolyzed xyloglucan (HXG) for 14 days. The mass of colon plus rectum was higher in rats fed CC, but not in rats fed BP and HXG than in rats fed ED. Cecal tissue mass was higher in rats fed BP and HXG, but not in rats fed CC, than in rats fed ED. Cecal contents and cecal pH were higher and lower in rats fed CC, BP and HXG than in rats fed ED. DA0 activities in the small intestine and plasma were higher in CC than in rats fed ED. Cecal ammonia were lower in rats fed CC, BP and HXG than in rats fed ED. Production of organic acids was similar between rats fed ED and CC except for acetic acid that was much lower in also improved in rats fed CC. combination of water -soluble and diet would have more beneficial soluble dietary fiber alone. 0 1998 Ehwier Science Inc.

rats fed CC. Diarrhea and loose feces were The results suggest that the addition of a -insoluble dietary fiber to a liquid formula effects on the bowel function than water-

KEY WORDS: Liquid diet, Dietary fiber, Rats

Bowel function,

Cecal organic

acids,

Liquid formula diets are used in pre- and post-operative bowel preparations to provide complete nutrition orally and in treatment of some diseases such as inflammatory bowel disease and irritable bowel syndrome. Constipation and Correspondence: Kiyoshi Ebihara, Department of Biological Resources, Faculty of Agriculture, Ehime University, Matsuyama 790-0905

883

884

K. EBIHARA and Y. NAKAMOTO

diarrhea are potentially serious problems experienced in chronic care patients who are fed exclusively on liquid formula diets. Several studies have showed that addition of dietary fiber (DF) to liquid formula diets alleviates constipation ( 1) and diarrhea (2,3). As a consequence of this perceived beneficial effect, a number of DF enriched liquid enteral diets have been introduced which have found widespread clinical usage. DF-enriched liquid formula diets are marketed in Japan, in the United States and in Europe. In order to facilitate the administration of diets through fine bore nasogastric feeding tubes, DF had to be fine and soluble in The addition of DF to liquid formula diets increases viscosity, which in turn, water. make it harder to administer the diets through fine bore nasogastric feeding tubes. Therefore, hydrolyzed

water- soluble DF with low viscosity such as polydextrose and partially However, physiological guar gum were used as DF source in Japan.

effects of DF are affected by their physical nature such as whether they are coarse Short-chain fatty or fine, soluble in water or not and more fermentable or less. acids (SCFA), which are a major product of DF fermentation, are the predominant anions in the colonic lumen and are thought to have a major impact on luminal and mucosal metabolism. The fermentation of cellulose is less extensive than that of noncellulolytic polysaccharides such as hemicellulose, pectin and guar gum. The purpose of this study was to compare the effect of water-soluble and -insoluble DF added to a liquid elemental diet on the functional changes in the small intestine and colon and on cecal organic acids.

Animals and diets. Male Wistar rats (Japan SLC, Hamamatsu, Japan) with an initial weight of approximately 80 g were used in the experiment. They were housed in individual cages with screen bottoms of stainless steel in a room maintained at 23 + 1°C with a 12-h 1ight:dark (light, 0700-1900h). Rats were acclimated by feeding a commercial solid diet (MF@; Oriental Yeast Co., Osaka, Japan) for 7 days. After acclimation, rats were divided into 4 groups of 6 rats approximately equal body weight (147 +4 g). Rats were fed an elemental liquid diet (ED) or ED containing 3g/lOO ml of dietary fiber either a mixture of crystal cellulose and carbowmethyl cellulose sodium salt (CC), sugar-beet pectin (BP) or hydrolyzed ED(Elental@, Roussel Morishita Co. Ltd., Osaka) xyloglucan (HXG) for 14 days. consisted of 4.7 g amino acids, 0.16 g lipid (soy bean oil), 2 1.2 g carbohydrate (dextrin), vitamins and minerals in 100 ml. Rats drank experimental liquid diets from calibrated feeding bottles with fitted sippers. CC is a commercial preparation named “Avicel RC-591” (Asahi Chemical Industry Co., Ltd., Tokyo, Japan), which is a mixture of crystal cellulose (average particle diameter=10 cc) and carboxymethyl cellulose sodium salt in the ratio of 89: 11 (weight). BP (Classic RU30 1, Herbstreith & Fox KG, Neuenbiirg, Germany) was gifted from Dainippon Pharmaceutical Co. Ltd. HXG is a commercial preparation named “Glyroid” (Dainippon (Osaka, Japan). Pharmaceutical Co., Ltd., Osaka, Japan), which is prepared from tamarind seed polysaccharide and consists of xyloglucan hepatosaccharide, octasaccharide and nonasaccharide. Body weight and food intake were recorded daily in the morning, and then the condition of feces of each rat was observed.

885

DIETARY FIBER AND LIQUID DIET

Sampling

and

were sacrificed

analytical

under

sodium

procedures. pentobarbital

At the end of experiment, all rats (50 mg/kg body mass, Nembutal, Abbot

Blood was collected from the Laboratories, North Chicago, Ill) anesthesia. abdominal aorta in a blood collection tube (Vacutainefl, Becton Dickinson, Franklin Plasma was separated by centrifugation at 1400 x g for 15 min at 4°C Lakes, NJ). The ileo-cecal and ceco-colonic junctions were and stored at -50°C until analyzed. ligated and the digestive tract was removed. The small intestine (the ligament of Treitz to the ileo-cecal junction) and was flushed with ice-cold saline (9 g/L NaCl), blotted on filter paper and length and weight were measured. The colon plus rectum was opened longitudinally, rinsed with ice-cold saline and length and weight were measured. Mucosal scraping of proximal ileum (7-17 cm from ileo-cecal junction) was homogenized in 10 ml of phosphate buffer (0.1 M, pH7.2) followed by centrifuging at 10,000 x g for 20 min. enzyme and protein assay.

An aliquot

of the supernatant

was used for

Activities of intestinal and plasma diamine oxidase (DAO) were assayed according to Hosoda et al. (4) using cadaverine (Wako Pure Chemical Industries, Ltd., Osaka, Japan) as substrate, One unit of DA0 activity is defined as the amount of enzyme that Alkaline phosphatase (ALP) was measured will produce 1 pmol Hz02 per min. according to Kind and King method (5) using disodium phenyl phosphate as substrate. One unit of ALP activity is defined as the amount of enzyme that will produce 1 pmol pnitrophenol per min. Maltase activity was assayed by the method of Takahashi et al. (6) and protein was measured by the method of Lowry et al. (7). The ileo-cecal and ceco-colonic junctions were ligated and the cecum was removed. The cecum was first weighed with contents (total cecal weight). The contents were drained from the ceco-colonic junction into a 50-mL vial, mixed well The cecal wall was flushed clean with ice-cold saline, blotted on and used analyses. Cecal pH was measured with a compact filter paper and weighed (cecal wall weight). pH meter using a sampling sheet (Model C-l, Horiba, Tokyo, Japan; calibrated at Cecal ammonia was determined spectrophotometrically in deproteinized (4 20°C). mL of 0.25 mol/L sulfuric acid and 50 g/L sodium tungstate dihydrate, 50 mg contents) supernatant (1500 x g, 10 min) of cecal contents (8). Cecal organic acids (acetic, propionic, n-butyric, measured by HPLC (LC-1OA; Shimadzu, Kyoto, Japan)

succinic (9).

1:l (v/v), for -

and L-lactic

acids)

were

Statistical analysis. Values are given as the means&EM and, where appropriate, significance of the difference between mean values was determined by Values of P analysis of variance coupled with Duncan’s multiple range test (10). ~0.05 were considered significant.

Rats quantity.

Rats fed ED had loose feces in lower fed BP had severe diarrhea. Rats fed HXG had loose feces in higher quantity. In rats fed CC, diarrhea

886

K. EBIHARA and Y. NAKAMOTO

and loose feces were completely

improved.

Body mass gain, food intake and intestinal weight and length of rats at sacrifice expressed per 100 g body mass are shown in Table 1. Body mass gain of rats fed BP was significantly lower than those of rats fed CC and HXG. Food intake of rats fed BP was significantly lower than those of rats fed W, CC and HXG. The weight of small intestine of rats fed CC and HXG were slightly higher than that of rats fed W. The weight of cecal wall of rats fed BP and HXG were significantly higher than that of rats fed W. The weight of colon plus rectum of rats fed CC was significantly higher than that of rats fed ED. No differences were observed for the lengths of small intestine and colon plus rectum. As shown in Table 2, the activity of DA0 in the lower ileum was significantly higher in rats fed CC, but not in rats fed BP and HXG, than in rats fed W. The activity of ALP in the lower ileum was significantly higher in rats fed CC and HXG,but not in rats fed BP, than in rats fed W. No differences were observed for maltase activity in the lower ileum and plasma ALP activity. Plasma DA0 activity was significantly higher in rats fed CC and HXG, but not in rats fed BP, than in rats fed W.

The wet weight and pH value of cecal contents and total organic acids in cecal Cecal contents were 2, 3.6 and 4.6 times greater contents were shown in Table 3. in rats fed CC, BP and HXGthan in rats fed W, respectively. Those of rats fed BPand

TABLEI Body Weight Gain, Food Intake, Intestinal Length and Organ Weight of Rats fed a Liquid Elemental Diets with or without Dietary Fiber Diets ED Body mass gain (g/2 weeks) Food intake (ml/2 weeks) Feed efficiency Organ weight (g/100 g b.w.) Small intestine Cecal wall Colon + rectum Organ length (cm/100 g b.w.) Small intestine Colon + rectum

57 * 2* 922 * 21a

cc 65 * 6b 875 * 23ab

BP 50 * 2= 741 * 1%

2.10 * 0.02ab 0.26 * 0.02a 0.33 * 0.02a

2.27 * 0.06b 2.00 * 0.07a 0.36 * O.OSab 0.42 * 0.02b 0.33 * 0.02a 0.48 f: 0.03b

38.8 * 1.2 6.3 * 0.5

39.1 * 1.7 7.6 * 0.6

43.9 * 2.3= 6.6 * 0.3a

HXG 63 * St’ 835 t32b

2.23+ 0.08b 0.78 t 0.06~ 0.39 ??0.02a 41.0 * 1.6 7.5 * 0.4

Means * SEM (n=6) not sharing a common superscript letter within the same row were significantly different at p-&OS. 1 Rats received a liquid elemental diet (ED) or ED containing 3g/lOO ml of dietary fiber either a mixture of crystal cellulose and carboxymethyl cellulose sodium salt (CC), sugar-beet pectin (BP) or hydrolyzed xyloglucan (HXG) for 14 days.

887

DIETARY FIBER AND LIQUID DIET TABLE 2 Diamine Oxidase (DAO), Alkaline Phosphatase (ALP) and Maltase Activities of Rats fed a Liquid Elemental Diets with or without Dietary Fiber1 Diets

Ileum mucosa (Wmg protein) DA0 ALP Maltase Plasma (U/ml)

DA0 ALP Means* SEM (n=6) not sharing significantly different at p
were

greater

than

significantly

ED

cc

BP

HXG

0.15 * 0.01a 0.38 * 0.02a 0.66 t 0.06

0.28 * 0.03” 0.93 * 0.16b 0.80 t 0.05

0.18 + 0.02a 0.43 * 0.04 0.72 * 0.06

0.20 * 0.04 0.73 * 0.08b 0.78 t 0.06

0.41*O.O+ 4.81zt0.04

0.98* 0.09b 4.96* 0.07

0.50zt0.06= 0.72zt0.06~ 4.8‘8 * 0.06 4.93* 0.07

a common superscript letter within the same row were 1 Rats received a liquid elemental diet (ED) or ED containing a mixture of crystal cellulose and carboxymethyl cellulose (BP) or hydrolyzed xyloglucan (HXG) for 14 days. that lower

of rats fed CC. than

that

Cecal pH values

of rats

fed ED.

of rats fed BP

However, that

of

rats fed CC was higher than that of rats fed ED. Total and concentration of ammonia in cecal contents of rats fed CC, BP and I-KG were significantly lower than those of rats fed ED. Total organic acids in cecal contents was significantly larger in rats fed HXG than in rats fed ED, CC and BP. L-lactic acid, propionic acid and n-butyric acid in the cecum were larger in rats fed HXG than in rats fed ED, CC and BP. Acetic acid was significantly smaller in rats fed CC than in rats fed ED, BP and HXG.

Constipation,

diarrhea,

atrophy

in

the ileum

and

location are potentially serious problems experienced are fed exclusively on liquid formula diets. Under dietary fiber have been found to improve constipation addition of DF in a liquid formula diet is proposed to the maintenance of small intestinal and large intestinal

colon

and

bacterial

trans-

in chronic care patients who experimental conditions, some (1) or diarrhea (2,3). The have many benefits, including function ( 11,12).

Diarrhea is one of the most common complications in patients who receive a liquid formula diet. It has been documented that diarrhea induced by consumption of a liquid formula diet was associated with the reduction in absorptive capacity and absorptive area because of the loss of brush border enzymes and mucosal cells (4,13). In rats fed CC, diarrhea and loose feces were completely improved. The weight of small intestine was slightly lower in rats fed ED than in rats fed CC. The a40 activities in intestinal mucosa and plasma hhavebeen determined as a marker for rat intestinal mucosal maturity and integrity (14). The DA0 activities in intestinal

888

K. EBIHARA and Y. NAKAMOTO TABLE 3 Cecai Contents, Cecal pH, Cecal Pool of Ammonia and Organic Acids of Rats fed a Liquid Elemental Diet with or without Dietary Fiber-1

Diets

Cecal contents

Cecaf pH

Cecal ammonia

ED

1.88 zt 0.28a

7.48 * 0.13=

tunol/cecum 20.1 * 2.4=

CC BP HXG

3.40 * 0.14b 6.70 * 0.23~ 8.46 * 0.69d

7.84 * 0.08b 6.14 zt0.06~ 5.18 * 0.07d

8.8 * 0.4b 10.6 * l.lbc 10.9 * l.lC

g

Diets

Succinic acid

ED cc BP HXG

26+6 12 * 7 ll*l 28 * 7

L-lactic acid 14+ 5a 29*14a 15* 4a 266 t 36b

Acetic acid

Propionic acid

umoVcecum 130 zt 18a 53 f lla 40 t 7b 20 2 7a 161+ 8a 49t 6a 136 2 48a 175 * 21b

pmol/g contents 10.8 * 0.6a 2.6 * 0.2b 1.6 * 0.2~ 1.3 * O.lC n-butyric acid

23 59 30 155

* * * *

10a 17a 3a lob

Total

245 160 265 764

* 39 t 2@ * 13a + 8Ob

Means * SEM (n=6) not sharing a common superscript letter within the same row were significantly different at p-&.05. 1 Rats received a liquid elemental diet (ED) or ED containing 3g/lOO ml of dietary fiber either a mixture of crystal cellulose and carboxymethyl cellulose sodium salt (CC), sugar-beet pectin (BP) or hydrolyzed xyloglucan (HXG) for 14 days. and plasma were significantly higher in rats fed CC than in rats fed ED. The activity of ALP was also higher in rats fed CC than in rats fed ED. These suggest that the addition of CC to ED significantly higher in rats fed CC than in rats fed ED. The activity of ALP was also higher in rats fed CC than in rats fed ED. These suggest that the addition of CC to ED helps to maintain an intestinal function. On the other hand, it has been shown that short-chain fatty acids (SCFA) stimulate sodium and water absorptions in the colon and should thus have an antidiarrheal effect (15). Total organic acids in cecal contents was significantly higher in rats fed HXG than in rats fed ED.

However, the addition

HXG to ED could not improve

loose feces.

Feeding with a DF-free liquid formula diet has been associated with colonic mucosal atrophy (16,17). The weight of colon plus rectum was significantly heavier in rats fed CC than in rats fed ED. The DA0 activities in intestinal mucosa and plasma were also significantly higher in rats fed CC than in rats fed ED. Therefore, it would appear that the addition of CC to ED have a good effect in terms of control of less atrophy of the colon. Total organic acids in cecal contents was significantly higher in rats fed HXG than in rats fed ED. SCFA stimulate colonic epithelial proliferation and prevent mucosal atrophy associated with a DF-free liquid enteral diet feeding (15). However, there was no significant difference between rats fed ED and rats fed HXG on the weight of the colon plus rectum. The pH values in cecal contents and cecal pool of organic acids were significantly lower and higher in rats fed HXG than in rats fed ED and CC. Lactate is absorbed

DIETARY FIBER AND LIQUID DIET

889

from the colon more slowly (18). Judging from higher lactic acid amounts in cecal contents, the higher amounts of cecal lactic acid in rats fed HXG predominantly Compared with rats fed ED, the pH contributed to the lower pH in cecal contents. Though there is no values in cecal contents of rats fed CC was significantly higher. significant difference, cecal pool of organic acids was slightly higher in rats fed ED than in rats fed CC. Laxative properties of CC may diminish the overall bacterial activity in the large bowel by decreasing the time available for fermentation in the Both BP and HXG are water-soluble DF, but the pH values and SCFA in large bowel. cecal contents were significantly lower and higher in rats fed HXG than in rats fed HXG is the mixture of xyloglucan hepatosaccharide, octasaccharide and BP. nonasaccharide. Xyloglucan has the same skeleton, g1,4 glucan, as cellulose, with a 1,6-a-D-xylose side chain. However, cellulose was fermented less readily than HXG. Both cecal pool and concentration of ammonia were significantly lower in rats fed BP, HXG and CC than in rats fed ED. Gut bacteria increase the requirement for ammonia-N during the growth phase, because ammonia an important source of Thus, it is likely that BP and HXG nitrogen for microbial protein synthesis (19). reached the cecum where these DF were used as energy sources for gut bacteria, resulting in higher ammonia-N assimilation and thus reduced ammonia levels in the Demigne and Remesy (20) have reported that fermentable DF lowered cecum. On the other hand, cellulose is poorly ammonia concentrations in the cecum. However, cellulose is an excellent bulking agent (2 1) and accelerates fermented. the transit in the large bowel, which should result in a reduction of cecal ammonia. The addition of CC to ED had more beneficial effects in terms of control of diarrhea and less atrophy of the large bowel as documanted by DA0 activities than the addition of BP and HXG to ED. CC is a mixture of water-insoluble DF (crystal cellulose) and water-soluble DF (carboxymethyl cellulose sodium salt). These show that a combination of water soluble and insoluble DF to a liquid formula diet would have more beneficial effects on the bowel function than water-soluble DF alone.

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