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The Journal of Nutrition Vol. 128 No. 10 October 1998,
pp. 1731-1736
Division of Toxic Metals, Korea Food and Drug Administration, 5 Nokbun-dong Seoul, 122-704, Korea and * Department of Food Science and Nutrition, Hallym University, Chunchon, 200-702, Korea
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ABSTRACT |
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Abstract
Introduction
Methods
Results & Discussion
References
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Sprague-Dawley rats (n = 32) were fed diets without fiber (control) or containing 1 or 5% chicory extract or 5% inulin for 4 wk; 0.2% cholesterol was added to all diets. Rats fed chicory extract and inulin diets had significantly higher serum high density lipoprotein (HDL) cholesterol and generally lower low density lipoprotein (LDL) cholesterol concentrations, thus significantly greater ratios of HDL/LDL cholesterol compared with the controls (P < 0.05). The serum apolipoprotein B/apolipoprotein A-1 ratio was significantly lower in rats fed diets containing chicory extract or inulin than that in rats fed fiber-free diets, due to significant reductions in apolipoprotein B concentration (P < 0.05). Greater liver lipid and triglyceride concentrations were observed in rats fed chicory extract or inulin diets compared with the controls (P < 0.05). However, liver phospholipid and cholesterol concentrations were not significantly different among groups (P > 0.05). Addition of 5% inulin to the diet resulted in greater cecal weight, whereas both 5% chicory extract and 5% inulin resulted in greater cecal propionic acid concentration compared with the controls (P < 0.05). Rats fed chicory extract and inulin had significantly greater fecal lipid, cholesterol and bile acid excretions than those fed fiber-free diets (P < 0.05). The results of this study suggest that the improved lipid metabolism observed in rats fed chicory extract (mainly inulin component) may be caused by an alteration in the absorption and/or synthesis of cholesterol, which might result from the changes in cecal fermentation, and by an increase in the fecal excretion of lipid, cholesterol and bile acid.
KEY WORDS: lipid metabolism · dietary fibers · chicory · inulin · rats
The hypolipidemic effects of soluble fibers have received considerable attention. The mechanisms by which soluble fibers elicit their hypocholesterolemic effects are still not clear, although many hypotheses have been proposed (Anderson and Chen 1979 Chicory (Chicorium intybus) is one of the earliest known and most widely used raw materials for the manufacture of coffee substitutes (Pazola 1987 However, no previous studies of chicory root (mainly inulin) on lipid metabolism have been reported. This study was designed to examine the effect of chicory extract or inulin on serum and liver lipids, cecal short-chain fatty acid concentrations and fecal lipid excretions.
Chicory extract and inulin.
Chicory water-soluble extract (chicory extract) was prepared as follows: dried slices of chicory root were used as the starting material and ground into powder using a micromill (Bel-Art Products, Pequannock, NJ). Distilled water (chicory root powder/distilled water 1:5 wt/v) was added and mixed for 50 min at 70°C with continuous stirring. The solubles, which are prepared by filtering the slurried mixture through a cotton cloth, were ready to be added to the experimental diets. The inulin (from chicory root) was also purchased from Sigma Chemical, St. Louis, MO.
Animals and diets.
All procedures for handling the rats were approved by the Institutional Animal Care and Use Committee of the Hallym University. Male Sprague-Dawley rats (Experimental Animal Breeding Laboratory, Seoul National University, Seoul, Korea) weighing 152 ± 5 g were fed a nonpurified diet (Rodent Laboratory Chow, Ralston Purina, St. Louis, MO) for 5 d, then the experimental diets (Table 1). The rats were maintained at 22 ± 2°C and 60 ± 5% relative humidity in a room with a 12-h light:dark cycle and given free access to food and water at all times. Rats were divided randomly into four groups of eight rats each. They were fed diets without fiber or containing 1 or 5% chicory extract or 5% inulin for 4 wk. All of the treatments including the control diet contained 0.2% cholesterol. During the last 5 d of the experimental period, fecal samples were collected for each rat and pooled, then stored at
Analyses.
The concentrations of total cholesterol (kit #276-64909; Wako Chemicals, Osaka, Japan), high-density lipoprotein (HDL) cholesterol (kit #278-67409; Wako Chemicals) and triglyceride (kit #274-69807; Wako Chemicals) in the serum were determined without extraction by enzymatic colorimetric methods. Liver cholesterol and triglyceride and fecal cholesterol concentrations were determined using the same kits as in the serum after liver and fecal samples were extracted with solvents (Folch et al. 1957 Concentration of chicory extract.
A hand refractometer (Atago, Tokyo, Japan) was used to measure the concentration of water-soluble chicory extract solution by determining the refractive index of the solution. Determining the concentration of chicory extract was necessary to calculate the amount of chicory extract for an addition to the diet.
Statistical analyses.
Data for the control, 1 or 5% chicory extract or inulin groups were analyzed by one-way ANOVA; P Food intake and growth.
Random assignment of rats to the four experimental groups resulted in initial body weights that were not different. Addition of chicory extract or inulin did not affect weight gain (Table 2). Rats fed 5% chicory extract had significantly greater food intake than those fed the control diet. However, food efficiency was not significantly different among groups. Levrat et al. (1991)
Relative organ weights.
Relative weights of small intestine and large intestine were not significantly different among groups. However, cecum weight was significantly greater in rats fed inulin than those in rats fed chicory or fiber-free diets (P < 0.05) (Table 3). The enlargement of the cecum in rats fed the inulin diet (Table 3) was in agreement with the results of Levrat et al. (1991)
Serum lipids and apolipoprotein.
Serum HDL cholesterol concentration was significantly higher in rats fed chicory extract and inulin, and LDL cholesterol concentration was lower in rats fed inulin than in controls. Therefore, the ratio of HDL/LDL cholesterol was significantly higher in rats fed chicory and inulin than in controls (P < 0.05) (Table 4). Vanhoof and De Schrijver (1995)
Liver lipids.
Liver lipid and triglyceride concentrations were significantly lower in rats fed chicory extract or inulin compared with the controls (P < 0.05); those fed 5% chicory extract or 5% inulin had significantly lower concentrations than those fed 1% chicory extract (Table 6). However, liver cholesterol concentrations were not significantly different among groups; this is in agreement with results of Vanhoof and De Schrijver (1995)
Cecal short-chain fatty acids.
Rats fed diets containing 5% chicory extract or 5% inulin had significantly greater propionic acid concentration in the cecum compared with those fed the fiber-free diet (Table 7). Concentrations of acetic acid and butyric acid were not significantly different among groups. Levrat et al. (1991)
Fecal lipids.
Addition of chicory or inulin to diets caused significantly greater fecal lipid, cholesterol and bile acid excretion in rats compared with the controls (P < 0.05) (Table 8). Rats fed 1% chicory extract also had significantly greater fecal lipid excretion than those fed 5% inulin. Fecal cholesterol and bile acid excretions were the greatest in rats fed 5% inulin, followed by those fed 5% chicory extract, 1% chicory extract and finally, controls. Greater fecal lipid, cholesterol and bile acid excretions observed in rats fed chicory extract or inulin (Table 8) were in agreement with results of other investigators (Vanhoof and De Schrijver 1995
INTRODUCTION
Abstract
Introduction
Methods
Results & Discussion
References
, Arjmandi et al. 1992, Fernandez et al. 1997, Roberfroid 1993). Elevated plasma cholesterol, especially the low density lipoprotein (LDL)4 fraction, is regarded as a primary risk factor in coronary heart disease (Anderson et al. 1990). Pectins have been shown to lower plasma cholesterol in animal and human studies (Judd and Truswell 1982 and 1985). Similar effects were observed with guar gum (Simons et al. 1982) and oat bran (Kirby et al. 1981).
). The major component of chicory root is inulin, which is a polymer of fructose with 
-(2-1) glycosidic linkages. Inulin belongs to the fructan family; naturally occurring fructans are important storage carbohydrates, widely found in various flowering plants. Fructans are present in noticeable amounts in chicory, Jerusalem artichokes (up to 20%), salsify, asparagus and onions (Nilsson et al. 1988, Rumessen et al. 1990). Because inulin is soluble in water and not hydrolyzed by human digestive enzymes, it is expected to behave like a soluble fiber and to have a hypolipidemic effect. Both the fermentability and the bifidogenic effect of chicory fructooligosaccharides have been confirmed in in vivo human studies that were performed by feeding human volunteers a standard diet containing chicory fructooligosaccharides (15 g/d for 15 d). A significant increase in the bifidobacteria population and a profound modification of the composition of the fecal flora were observed (Gibson et al. 1995). In human nutrition, inulin could constitute a promising source of soluble fiber either when present naturally in the food or when added to the diet (Roberfroid 1996). Inulin is easily extracted from plants such as chicory or Jerusalem artichokes.
MATERIALS AND METHODS
Abstract
Introduction
Methods
Results & Discussion
References
20°C. At the end of experiment, rats were deprived of food for 16 h and then anesthetized with an intraperitoneal injection of sodium pentobarbital (Entobar; Han Lim Pharm, Seoul, Korea) at 50 mg/kg body weight. A central longitudinal incision was made into the abdominal wall, and blood samples were collected into tubes by cardiac puncture. Blood samples were centrifuged at 4°C for 20 min at 1480 × g, and the serum was separated and stored at 20°C until analyzed. The liver, small intestine and large intestine were excised, weighed after intestinal contents were washed out with ice-cold 0.15 mol/L NaCl; liver was stored at 20°C until analyzed. The cecum was also excised, cut open and its contents were collected; the cecum and its contents were weighed separately. The cecal contents were homogenized and centrifuged at 4°C for 20 min at 9000 × g; the supernatants were used for the determinations of acetate, propionate and butyrate contents.
View this table:
Table 1.
Composition of experimental diets
). Serum LDL cholesterol was calculated by the method of Friedewald et al. (1972). Contents of apolipoprotein (apo) A-I (kit #356; Sigma Chemical), and apolipoprotein B (kit #357; Sigma Chemical) in the serum were measured by the immunoturbidimetric method (Rifai and King 1986). Total fat content in livers and feces was analyzed by the method of Folch et al. (1957). The concentration of liver phospholipid (kit #996-54001; Wako Chemicals) was determined by enzymatic colorimetric methods after solvent extraction (Folch et al. 1957). Feces were extracted by the method of Tokunaga et al. (1986), and the extracted solutions were used to determine bile acid concentration (kit #450; Sigma Chemical) enzymatically by the method of Mashige et al. (1981).
). Optimum operating conditions were as follows: oven temperature program; initial temperature of 40°C for 3 min, increase from 40 to 100°C at a rate of 5°C/min, hold at 100°C; injector temperature, 130°C, detector temperature, 150°C, nitrogen carrier gas flow rate, 25 mL/min, injection volume, 1 µL.
0.05 was taken as indicating no significant differences. Where ANOVA showed significant effects, differences among groups were evaluated for significance by Duncan's multiple range test (Steel and Torrie 1980).
RESULTS AND DISCUSSION
Abstract
Introduction
Methods
Results & Discussion
References
reported that moderate levels of inulin (5-10%) did not significantly affect food intake or body weight gain.
View this table:
Table 2.
Food intake and growth in rats fed fiber-free, chicory extract or inulin diets1,2
who found greater cecum weight gains in rats fed 5, 10 or 20% inulin diets. Tokunaga et al. (1986) also observed that the net weights of cecum and colon were greatly increased by Neosugar (fructooligosaccharide) feeding. Other investigators also reported that greater cecal weights were observed in rats fed 10% -cyclodextrin (Levrat et al. 1994) and 6% fructooligosaccharide diets (Campbell et al. 1997).
View this table:
Table 3.
Relative organ weights in rats fed fiber-free,
chicory extract or inulin diets1,2
found that the serum HDL/LDL cholesterol ratio was increased in normocholesterolemic rats, but not in hypercholesterolemic rats when 6% inulin was added to a diet containing 1% cholesterol and 0.1% cholic acid. In our study, serum total cholesterol concentrations were not significantly affected by chicory or inulin feeding. Our results were in agreement with those of Tokunaga et al. (1986) who found no significant difference in serum cholesterol levels between rats fed 10% fructooligosaccharide (Neosugar) and controls. However, other investigators reported a significant reduction in serum cholesterol concentration in rats fed inulin (Levrat et al. 1991) or soluble fibers (Anderson et al. 1994). Levrat et al. (1991) found that dietary inulin reduced plasma cholesterol concentration in rats in a dose-related manner in a 3-wk feeding study.
View this table:
Table 4.
Lipoprotein cholesterol and triglyceride concentrations in serum of rats fed fiber-free, chicory extract or inulin diets1,2
, Matheson et al. 1995). A diet containing 0.12% cholesterol was found to induce a moderate hypercholesterolemia such that plasma cholesterol concentrations approximated those of moderately hypercholesterolemic humans (Gallaher et al. 1993). Jennings et al. (1988) observed that 1% cholesterol feeding increased total liver lipids almost threefold and liver cholesterol concentration almost 10-fold. We also added 1 or 5% chicory extract to diets. Many investigators have generally chosen 5-10% of dietary fibers for various nutritional studies (Campbell et al. 1997, Levrat et al. 1991). The amounts of chicory extract used in this study are quite reasonable; 1 and 5% chicory extract would be equivalent to daily consumption of about 5 and 25 g dietary fiber in humans, respectively. Dietary recommendation for nonstarch polysaccharides has been 16-24 g/d (WHO 1990) and 18 g/d (UK, range = 12-24 g/d) (Cummings and Englyst 1995). These values are similar to the estimate of 10 g/1000 kcal of dietary fiber recommended by the Life Sciences Research Office Expert Panel, which also used stool weight as a physiological predictor of adequacy of fiber intake (Gallaher and Schneeman 1996). Many investigators have used rats extensively as an experimental model for various studies. However, the rat may not be an ideal model for studying lipid metabolism because it has no gall bladder and lacks plasma lipid transfer protein (Williams 1976). It is possible that interrelationships between HDL and LDL cholesterol obtained in rats do not apply in humans.
View this table:
Table 5.
Apolipoprotein (apo) concentrations in serum of rats fed
fiber-free, chicory extract or inulin diets1,2
who found no difference in liver cholesterol concentrations of hypercholesterolemic rats fed an inulin diet. Anderson et al. (1994) reported that rats fed soluble fibers such as guar gum and pectin had significantly lower liver cholesterol concentrations.
View this table:
Table 6.
Total lipid, phospholipid, cholesterol and triglyceride concentrations of liver in rats fed fiber-free, chicory extract or inulin diets1,2
observed a significant increase in cecal concentrations of acetate, propionate and butyrate in rats fed 5, 10 and 20% inulin diets. However, Campbell et al. (1997) reported that there was no significant difference in fecal short-chain fatty acid concentrations in rats fed 6% fructooligosaccharide compared with rats fed fiber-free diets. Several studies have reported that propionate may alter the cholesterol pools or hepatic cholesterolgenesis (Wright et al. 1990, Yamashita et al. 1984).
View this table:
Table 7.
Concentrations of volatile fatty acids in the cecum of rats fed fiber-free, chicory extract or inulin diets1,2
) who found greater fecal cholesterol and bile acid excretions in rats fed 6% raw or 6% baked inulin excretions than in controls. Arjmandi et al. (1992) reported that 7.5% soluble fibers such as pectin, psyllium and oat bran might exert their hypocholesterolemic effect by increasing excretion of fecal neutral sterols.
View this table:
Table 8.
Fecal lipid, cholesterol and bile acid excretions in rats fed fiber-free, chicory extract or inulin diets1,2
). Relative viscosities of chicory extract and inulin were previously determined in vitro at 37°C using a Cannon-Fenske viscometer; the values were 90, 92 and 10 mPa·s in chicory extract, inulin and control containing no non-starch polysaccharide, respectively. Other investigators also reported that nondigestible oligomers of fructose and other saccharides found in many plant foods such as chicory and artichokes showed gelling and thickening properties (Dysseler and Hoffem 1995). For comparison, we also determined the relative viscosity of pectin, which has cholesterol-lowering effects in animals and humans (Judd and Truswell 1982 and 1985); the value was 141 mPa·s.
reported that inulin did not affect plasma lipids in healthy normolipidemic women who had diets containing 14 g inulin for 4 wk. Many investigators observed that resistant starches were effective in lowering plasma cholesterol in rats (de Deckere et al. 1993; Levrat et al. 1996). However, Noakes et al. (1996) did not find a cholesterol-lowering effect of resistant starch in humans who had daily intake of 17-25 g for 4 wk. Therefore, further studies of chicory extract are required to determine whether our observations apply in humans.
reported that oat bran intake increased fecal bile acid excretion, which probably contributes to its cholesterol-lowering effect. Story (1985) also observed that most soluble fibers increased fecal excretion of bile acids and altered the percentages of various primary and secondary bile acids excreted by the liver. These changes could result in a shift of systemic cholesterol into bile synthesis and thus reduce the total body cholesterol pool.
0.97, P < 0.05) and triglyceride (r = 0.98, P < 0.05), cecal propionic acid (r = 0.99, P < 0.01), and fecal cholesterol concentrations (r = 0.98, P < 0.01) and chicory intake. However, we did not find any significant dose-dependent relationship between other variables (i.e., fecal lipid and bile acid, serum cholesterol) and chicory intake. Also, there were no significant correlations between serum lipids and fecal lipids but significant correlations between liver lipid (r = 0.98, P < 0.05), liver triglyceride (r = 0.99, P < 0.05), and cecal propionic acid (r = 0.99, P < 0.01) and fecal cholesterol. In addition, cecal propionate concentration was significantly correlated with serum cholesterol (r = 0.72, P < 0.05) and serum LDL cholesterol (r = 0.98, P < 0.05). Illman et al. (1993) observed that there was a significant negative correlation between cecal propionate and plasma cholesterol concentrations. They also found an inverse relationship between cecal propionate and butyrate, suggesting that bacterial short-chain fatty acid production had changed in response to altered steroid excretion rather than a direct effect of short-chain fatty acid or steroid excretion. However, we could not find any significant correlation between cecal propionate and butyrate.
). Bosello et al. (1984) observed that most soluble fibers decreased the absorption of lipids in the proximal intestine and increased their absorption in the midintestine, which might alter the size and composition of lipoproteins secreted by the intestine. Second, having passed through the small intestine, soluble fiber is an excellent substrate for fermentation by the micro-organisms in the large bowel. The volatile fatty acids produced by fermentation enter the blood stream and appear to suppress hepatic cholesterol synthesis (Chen and Anderson 1984). Other investigators also suggested that increased production of short-chain fatty acids might contribute to the cholesterol-lowering effect of oat gum or oat bran (Bridges et al. 1992, Wright et al. 1990). Third, the hypocholesterolemic effect of soluble fibers may also be due to alterations in hormone secretions (Kay 1982). Certain dietary fibers affect pancreatic and gastrointestinal hormones (Bhathena et al. 1974). In addition, modifications of bile acid and lipoprotein metabolism could account for the hypocholesterolemic effect (Anderson et al. 1990, Lairon 1996, Matheson et al. 1995).
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FOOTNOTES |
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Manuscript received 19 December 1997. Initial reviews completed 22 January 1998. Revision accepted 5 June 1998.
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LITERATURE CITED |
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Abstract
Introduction
Methods
Results & Discussion
References
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-hydroxylase activity is increased by dietary modification with psyllium hydrocolloid, pectin, cholesterol and cholestyramine in rats.
J. Nutr.
1995;
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