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Articles

Whole Wheat and Triticale Flours with Differing Viscosities Stimulate Cecal Fermentations and Lower Plasma and Hepatic Lipids in Rats¹

Institut Technique des Céréales et des Fourrages (ITCF), Laboratoire Qualité des Céréales, 75013 Paris, France and ^* Laboratoire Maladies Métaboliques et Micronutriments, Centre de Recherches en Nutrition Humaine Auvergne, I.N.R.A. Clermond-FD/Theix, F-63 122 St-Genès-Champanelle, France

²To whom correspondence should be addressed. E-mail: aadam{at}clermont.inra.fr.

	ABSTRACT

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Whole flours from oat, rye or barley effectively modify digestive fermentation and lipid metabolism, whereas the effectiveness of whole wheat flour has not been established. To address this question, cecal digestion, short-chain fatty acid (SCFA) metabolism and cholesterol metabolism were investigated in four groups of rats fed the following semipurified diets differing in their carbohydrate source: a control diet (purified wheat starch) and three whole cereal flour diets [Valoris wheat (Wv), Soissons wheat (Ws), or Carnac triticale (Tc)]. Wv is particularly viscous and rich in arabinoxylans, and Tc is richer in hemicellulose than wheat. Compared with controls, rats fed the whole-flour diets had enlarged ceca and a moderate acidification of the bulk pH (6.4). In these rats, the cecal SCFA pool size was enhanced (P < 0.05), and the SCFA molar ratio reflected propionic/butyric acid–rich fermentations, especially in those fed Tc. The portal SCFA concentrations reflected the rise of the acetic and propionic acid pools in the cecum, whereas portal butyric acid remained relatively low, probably reflecting extensive metabolism by the cecal wall. The fecal excretion of total steroids (bile acids + sterols) was markedly enhanced by all of the whole-flour diets, with Wv (+78%) > Tc (+64%) > Ws (+47%). In parallel, there was a significant plasma cholesterol–lowering effect for rats fed Wv (-27%) and Tc (-32%) and a plasma triglyceride–lowering effect (approximately -40%) in all rats fed whole-flour diets (P < 0.05). This effect was observed mainly for triglyceride-rich lipoprotein-cholesterol, whereas HDL cholesterol was unaffected. These results indicate that whole wheat flours can strikingly affect cecal SCFA, especially butyrate, and are effective plasma cholesterol–lowering agents.

KEY WORDS: • rats • dietary fiber • wheat flour • cholesterol • butyric acid

	INTRODUCTION

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In most Western countries, cereals (e.g., wheat, oat or rye) represent a major source of dietary fiber because they contain 9–13% total fiber, but the soluble fiber percentage varies from 20% for wheat to 50% for oats. Cereal and grain consumption, however, has decreased dramatically over the last century (1) . In addition, cereals are consumed as more refined products than in the past, which lowers the daily fiber intake. In parallel, cardiovascular diseases, diabetes, obesity, hypertension and cancers have emerged as major health problems. It has been suggested that the decrease in fiber intake contributes to the development of these problems (2 3 4 5) ; thus, diet modifications involving a substantial increase in fiber intake have been recommended. Cereal fibers are chiefly insoluble, which explains why they may help prevent constipation and diverticular disease (6 ,7) . Nevertheless, they have also been considered to be lipid-lowering agents although this effect is generally ascribed to soluble fibers (8 ,9) .

Oat, rye and barley products have generally been found to be effective cholesterol-lowering agents (10 11 12 13 14 15) , whereas the effectiveness of wheat products remains unresolved (16 ,17) . In fact, in the 1970–1980s, a series of investigations, later compiled into a review (18) , did not provide clear conclusions about the effects of wheat fiber, although there were some works showing a significant effect of these products on lipids (19 20 21) . Thereafter, studies on wheat fiber have not been frequent; rather, they have focused on purified fractions such as bran or germ (22 23 24 25 26) . Thus, little is known about the effectiveness of whole wheat flour on digestive fermentations and lipid metabolism. However, this point is nutritionally relevant because whole cereal flour represents a good way in which to improve the daily supply of fiber, minerals and other micronutrients. Whole flour is relatively rich in fiber (13%) but it contains other constituents also liable to affect lipid metabolism, i.e., specific proteins such as gluten (27) or phytosterols (28) .

To examine the effects of whole wheat flour on digestive fermentation and lipid metabolism, we compared in rats the effects of two varieties of wheat (Soissons, Ws and Valoris, Wv)³ having different fiber levels with one variety of triticale (Carnac, Tc), which is naturally more rich in hemicellulose than wheat. The two varieties of wheat that were chosen have very different viscosities.

	MATERIALS AND METHODS

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Animals and diets.

Male Wistar rats (IFFA-CREDO, l’Arbresle, France) weighing 140 g were fed semipurified diets distributed as moistened powder for 21 d. The control diet is described in Table 1 . The two varieties of wheat (Ws and Wv) and the variety of triticale (Tc) were provided by ITCF (Institut Technique des Céréales et des Fourrages, Paris, France). The flours were obtained by grinding with a 2-mm grating. Specific viscosity was measured by the Biochemistry Laboratory of ITCF (Boigneville, France) according to Saulnier et al. (29). Values were 1.44, 5.15 and 8.07 mL/g, for Ws, Wv and Tc, respectively. Rats were housed two per cage and maintained in temperature-controlled rooms (22°C), with the dark period from 2000 to 0800 h. They were maintained and handled according to the recommendations of the Institutional Ethics Committee (Clermond-Ferrand University). The body weight of rats was recorded twice per week during the experimental period. During the last 7 d of the experimental period, rats were transferred to metabolic cages and food intake and fecal excretion were recorded over the last 4 d of the experiment.

Rats were killed at the end of the dark period, when cecal fermentations are still very active (30) . They were first anesthetized with sodium pentobarbital (40 mg/kg) and maintained at 37°C. An abdominal incision was made and blood was withdrawn from the portal vein (2 mL) and the abdominal aorta (5 mL) into heparinized tubes. After centrifugation at 10,000 x g for 5 min, the plasma was collected and stored at 4°C for lipid and lipoprotein analysis. After blood sampling, the cecum with its contents was removed and weighed, and two samples of cecal contents were transferred to microfuge tubes and immediately frozen at -20°C. A portion of liver was freeze-clamped and stored at -80°C for the measurement of liver lipids.

Analytical procedure.

Short-chain-fatty acid (SCFA) concentrations were measured by gas-liquid chromatography after ethanolic extraction of plasma samples as described by Rémésy and Demigné (31) and on supernatants (8000 x g, 5 min at 4°C), after acidification by 0.2 vol H₃PO₄ 10%. Bile acids and sterols were extracted from cecal contents and feces by 40 volumes ethanolic KOH (4mol/L) and quantified using the reaction catalyzed by 3 -hydroxysteroid dehydrogenase (EC 1.1.1.50; Sigma, L’Isle D’abeau Chesnes, France) (32) . Neutral steroids were extracted three times with 1 mL hexane from a 100-µL aliquot of the alkaline ethanolic extract, after addition of 5 -cholestane as an internal standard. The solvent was evaporated under N₂ and the residue dissolved in hexane. Extract (200 µL) was injected into the gas chromatograph (Danieducational, Paris, France) fitted with a 12 m x 0.25 mm (i.d.) fused silica capillary column (BP10; SGE, Villeneuve-St-Georges, France) and a flame-ionization detector. Helium was used as the carrier gas, and the sterols were isothermally separated at 260°C. Sterol concentrations were calculated from the peak areas relative to the area of the internal standard. Triglycerides and total cholesterol were determined in plasma by enzymatic procedures using commercial kits (Biotrol, Paris, France and BioMerieux, Charbonnières-les-bains, France, respectively). Liver triglyceride and cholesterol were extracted and analyzed as described by Mazur et al. (33), and a control serum (Biotrol-33 Plus, Biotrol, Paris, France) was treated in parallel to check the accuracy of the analyses.

Plasma lipoproteins were separated on a density gradient by preparative ultracentrifugation as described (34) in a TST 41.14 swinging-bucket rotor (Kontron, Zürich, Switzerland) at 100,000 x g for 24 h (15°C). The gradient was then fractionated into 500-µL fractions, and the cholesterol and triglyceride contents of each fraction were determined by the method described for plasma samples. Because of the low level of plasma LDL and the partial overlapping of the HDL1 and HDL2 fractions in rats, only two fractions were considered, i.e., the fraction with d < 1.040 kg/L (chiefly triglyceride-rich lipoprotein, TGRLP, together with some LDL) and the fraction with d > 1.040 kg/L (HDL).

The total dietary fiber of each variety of cereal (Ws, Wv, Tc) was analyzed by the method approved by the AOAC (35) .

Calculation and data analysis.

The cecal pool was calculated as cecal concentration (µmol/L) x cecal contents volume (L). Values are given as the means ± SEM and, where appropriate, significance of differences (P < 0.05) between mean values was determined by ANOVA coupled with the Student-Newman-Keuls test.

	RESULTS

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Effects of dietary fibers on food intake and weight gain and digestive fermentations.

The total fiber contents were 12.0, 15.2 and 15.4 g/100 g whole flour for Ws, Wv and Tc, respectively, leading to fiber percentages between 8.4 and 10.8% (Table 1) .

The presence of 70% whole flour in the diet did not affect daily food intake or weight gain (Table 2). Rats fed cereal diets had significantly greater fecal excretions than controls (P < 0.001) and enlarged ceca (+58, +68 and + 61% in rats fed the Ws, Wv and Tc diets, respectively, P < 0.01), which was due principally to an increase in the weight of the cecal contents. The cecal wall was significantly heavier (P < 0.001) in rats fed cereal diets than in controls. The cecal enlargement was accompanied by a significant acidification (P < 0.001) of the cecal contents.

Only acetic acid was present in measurable amounts in arterial blood. Propionic and butyric acids are quantitatively taken up by the liver and are almost undetectable in systemic blood, but there was significantly more acetic acid in the aorta of rats fed the whole-flour diets than in controls, which reflected the development of cecal fermentations (Table 4) . Portal vein concentrations (reflecting digestive absorption) were greater than artery concentrations in all of the groups and they were generally proportional to the cecal pools of acetic and propionic acids. In contrast, the quantities of butyric acid appearing in the portal vein were relatively low and not proportional to the cecal pools, suggesting extensive metabolism by the cecal wall. The molar ratio of acetic/propionic/butyric for the SCFA in the cecum (51:28:21) and the portal vein (72:19:9) of control rats illustrates this discrepancy.

Effects of cereals on fecal steroids.

Daily cholesterol intake was not significantly different among the groups (Table 5 ). Rats fed the Wv and Tc diets had significantly greater fecal excretions of bile acids than controls (+100 and +70%, respectively), whereas coprostanol excretion was significantly enhanced in all of the cereal-fed groups to the same extent (105%). Cholesterol excretion did not differ among groups. Total steroid excretion was significantly higher than controls in rats fed the cereal diets but it did not differ among the three cereal-fed groups. Estimated cholesterol absorption was 67 µmol/d in controls and it was significantly depressed in the Wv and Tc diet groups (-42 and -37%, respectively). In rats fed the Ws diet, total steroid excretion was significantly different from controls, but due to the slight, nonsignificant difference in cholesterol intake, no significant difference was found for cholesterol absorption. However, the percentage of cholesterol absorbed relative to that consumed was lower in the cereal groups than in controls (P < 0.05).

Plasma cholesterol was lower than controls in rats fed Wv and Tc diets (-27 and -32%, respectively), and triglycerides were lower in rats fed cereal diets (from -36 to -43%) (Table 6 ). Hepatic cholesterol was significantly lower in rats fed cereal diets compared with the control group, whereas hepatic triglycerides were not affected by the diets.

View larger version (24K): [in this window] [in a new window]   Figure 1. Differences in the repartition of cholesterol (panel A) and triglycerides (panel B) in plasma lipoprotein fractions of rats fed the control, Ws (wheat Soissons), Wv (wheat Valoris) or Tc (triticale Carnac) diet. Each value is a mean of a triplicate analysis of a pool of eight plasma samples. The fractions with d < 1.040 kg/L corresponded chiefly to triglyceride-rich lipoproteins (TGRLP) with a lower contribution of LDL. The fractions with d > 1.040 kg/L corresponded essentially to HDL.

	DISCUSSION

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High propionic acid fermentations in the cecum have generally been reported with diets containing soluble substrates (guar gum, resistant starch, ß-cyclodextrin) (38 39 40 41) and for luminal pH close to 6.0. In contrast, butyric acid–rich fermentations have been observed either with cellulose-rich diets or with some types of starch that escape digestion in the small intestine (42) . Under the present conditions, fermentation of relatively limited quantities of soluble fibers in the presence of an excess of insoluble fibers seems favorable to the simultaneous production of large quantities of propionic and butyric acids. It was shown recently that an arabinoxylan-rich fiber extract from wheat flour was readily fermented at acidic pH, with high acetic acid fermentations, in contrast to the corresponding wheat bran, which yielded high propionic/butyric acid fermentations (43) . Butyrate may play an important role in vivo in the physiology of the colon and inhibit the growth of neoplastic colonic cells (44 ,45) .

Most of the insoluble moiety of the fiber fraction is composed of cellulose, considered in rats to be an inert diluent of the diet, especially crystalline cellulose. However, it is conceivable that when cellulose fibers are dispersed into the complex matrix of the flour, they are more exposed to microbial degradation. Dry matter fecal excretion (1.75 g/d) was in the same range as total fiber intake (2 g/d), even though bacteria represent a substantial percentage of fecal dry matter (up to 40–50 g/100g). Measurement of the portal SCFA concentrations showed that the portal vein-artery difference was 0.5 mmol/L in rats fed the whole-flour diets. This supply consists mainly in acetic acid and to a lesser extent in propionic acid. From available data (46) , we infer that the hepatic uptake of acetic and propionic acids was probably of similar magnitude. It is noteworthy that butyric acid appeared in very small concentration in the portal vein, even in rats fed the cereal diets and exhibiting high butyric acid fermentations. This suggests that most of the butyric acid transferred across the cecal wall was metabolized in situ even when butyric acid is 40 mmol/L in the cecum.

Inclusion of highly viscous whole flours in the diet (Wv and Tc) induced a reduction in both hepatic and plasma cholesterol levels, compared with the control group fed a fiber-free diet. Ws, which is the less viscous whole flour, was the least effective in modifying cholesterol metabolism because it did not significantly lower plasma cholesterol although it did significantly reduce liver cholesterol. Plasma triglyceride levels were markedly lowered in rats fed the whole-flour diets. Only TGRLP fraction was affected by the whole-flour diets, which is consistent with previous experiments on cholesterol-fed rats fed a fiber diet (47) . Several mechanisms that might explain the hypocholesterolemic effect of dietary fiber, whether working alone or in combination, have been proposed (48) , i.e., slowing down the rate of gastric emptying, modification of bile acid absorption and metabolism, interference with lipid absorption and metabolism, production of SCFA from fermentation of fiber in the colon, up-regulation of the hepatic LDL receptor (49) and alterations in the plasma concentration or tissue sensitivity to insulin or other hormones.

Chronic consumption of wheat bran has been shown to increase the total lipase activity present in the small intestine of rats (50) and in humans receiving 20 g/d of a corn-wheat-pectin mixture (51) . Some binding or entrapment of pancreatic lipase may occur in the presence of fibers, as shown in in vitro conditions mimicking the physiologic conditions (52) with wheat bran and to a lesser extent with pectin. Vahouny (53) also demonstrated that cellulose reduces lymphatic appearance of intestinally infused fatty acid and cholesterol. A shift of the site of intestinal lipid absorption toward a more distal part of the intestine could contribute to this effect (54) .

Neutral sterol output was increased, and notably that of coprostanol. In the feces, the ratio of coprostanol to cholesterol increased from 1:1 in controls to 1:2 in cereal-fed groups. This likely reflects a more active metabolism of sterols by the microflora in moderately acidic pH conditions. The present results indicate that the percentage of cholesterol absorption was also markedly altered by the various whole flours, from 54% (controls) to 28% in rats fed Wv wheat flour. The mechanisms of inhibition of cholesterol absorption, in which viscosity is an important contributor, have been well documented; they include disturbance of micelle formation, slowing of cholesterol transfer to the brush border across the unstirred layer and inhibition of ileal bile acid reabsorption (55 56 57) . In rats fed diets containing fiber, the intestinal bile acid pool is increased (47 ,58) . This could reflect an entrapment of bile acids within the viscous medium (59) , as well as an accelerated biliary influx. It is noteworthy that in the present experiment, whole flours generally induced a greater elimination of bile acids. It has been shown with another viscous fiber (guar gum) that the bile acid pools in the small intestine and in the cecum may be enlarged, and there may be a more effective reabsorption in the portal vein (60) . Nevertheless, this reabsorption seems insufficient to prevent the rise in fecal excretion of the bile acids. This contrasts with previous results in which wheat bran did not alter the bile acid enterohepatic cycle or the bile acid pool size (61 ,62) .

Wheat germ accounts for 2–3 g/100 g of the kernel weight and it contains 8–12 g/100 g total dietary fiber. The present diet contained 2% wheat germ, and it is conceivable that this fraction played a significant role in the hypocholesterolemic and hypotriglyceridemic effects. In previous short-term studies in rats and humans, the ingestion of raw wheat germ lowered plasma triglycerides and cholesterol (63) . Studies in hypercholesterolemic and hypertriglyceridemic humans have shown that wheat germ intake decreases VLDL cholesterol and triglycerides dramatically (64) . The mechanism at work may be an inhibition of pancreatic lipase by wheat germ proteins, which could interact with the emulsified substrate and hinder the adsorption of the enzyme on the interface (24) . The wheat germ also provides phytosterols (0.05% in the diet vs. 0.25% cholesterol), tocopherols (10 mg/kg diet) and tocotrienols (19 mg/kg diet), which may lower cholesterol (65 ,66) , but it remains to be established whether they play an important role in the cholesterol-lowering effect of the whole flours.

Another mechanism described in the literature is the potential effect of SCFA, notably propionate, on cholesterol metabolism. From early studies of isolated hepatocytes, it was postulated that propionate has an inhibitory effect on cholesterol synthesis (67 68 69) . This hypothesis received some support from observations that propionate (at concentrations <1 mmol/L) can significantly inhibit cholesterol biosynthesis from acetate in hepatocytes (70 ,71) . Nevertheless, cholesterol synthesis has repeatedly been shown to increase and not to decrease in experimental animals fed fermentable soluble fiber or propionate (72 ,73) . Moreover, by-passing the small intestine by administering pectin or propionate into ceca of pigs (74) or perfusing propionate in the colon in humans (75) did not lower serum cholesterol. This does not mean that SCFA reaching the liver do not have any capacity to modulate lipid and carbohydrate synthesis (76) . In the present study, an increase in propionate absorption was consistently found when rats were fed cereal diets (0.20 mmol/L propionate in the portal vein of rats fed Wv and Tc). However, the question of an effect of propionate on the ß-hydroxyl-ß-methyl glutarate-CoA reductase remains open.

To differing degrees, the cereal flours studied in this work were as effective as lipid-lowering agents. A substantial cholesterol-lowering effect was obtained with a limited supply of soluble fiber, and it would be interesting to examine whether the arabinoxylan fraction is specifically responsible for these effects or whether the association between soluble and insoluble fibers is more important. The present results indicate that the replacement of refined flour by whole flour in various starchy foods could be an effective means to protect against the cardiovascular risks through the hypocholesterolemic effects of fibers and also through the improved daily supply of minerals and micronutrients.

	ACKNOWLEDGMENTS

 
We wish to thank Pierre Lamby for his technical assistance. We thank Jennifer Donovan for her careful reading of the manuscript. We thank also Danièle Orlando from the ITCF laboratory for her collaboration.

	FOOTNOTES

 
¹ Supported by A.N.R.T. (Association Nationale pour la Recherche et Technique), I.N.R.A. (Institut National de la Recherche Agronomique) and I.T.C.F. (Institut Technique des Céréales et des Fourrages).

³ Abbreviations used: SCFA, short-chain fatty acids; TGRLP, triglyceride-rich lipoprotein; Tc, Carnac triticale; Ws, Soissons wheat; Wv, Valoris wheat.

Manuscript received October 16, 2000. Initial review completed December 8, 2000. Revision accepted March 19, 2001.

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