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Unité des Maladies Métaboliques et Micronutriments or
* Unité de Microbiogie, INRA de Clermont-Ferrand/Theix, 63122 St-Genes-Champanelle, France and
Station de Recherches Cidricoles, INRA de Rennes, 35650 Le Rheu, France
3To whom correspondence should be addressed. E-mail: demigne{at}clermont.inra.fr.
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ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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40 mmol/L) were found in the cecum of rats fed the PEC diet and, to a lesser extent, the PEC + PL diet. The PEC + PL diet significantly lowered plasma cholesterol, whereas both the PL and PEC + PL diets lowered plasma triglycerides. Liver cholesterol and triglyceride concentrations were lower in rats fed the PEC and PEC + PL diets. Fecal bile acid excretion was markedly reduced, whereas sterol excretion was significantly increased by dietary PEC. Rats fed the PEC and PEC + PL diets also had lower apparent cholesterol absorption than controls (30 compared with 43%). In conclusion, apple pectin and the polyphenol-rich fraction were more effective when fed combined together than when fed separately on large intestine fermentations and lipid metabolism, suggesting interactions between fibers and polyphenols of apple.
KEY WORDS: • apple • cecal fermentations • cholesterol • pectin • polyphenols
The health benefits of fruits and legumes are now widely recognized but, because their daily intake is generally inadequate, incitative campaigns (5 or 10 per day) have been launched in America and in Europe. The range of protective effects ascribed to plant foods is particularly large, especially against consequences of the plurimetabolic syndrome (cardiovascular diseases, diabetes, obesity, renal failure) as well as against some cancers and long-term disabling conditions such as osteoporosis.
Apples represent a major proportion of the fruit supply throughout the year in most Western countries because of various factors: availability in the market, diversity of cultivars and variety of conditionings (fresh fruit, juice, cider, mashed apples). It has been estimated that apples could provide 20–25% of the per capita consumption of fruit polyphenols in the United States (1) as well as 10–30% of the daily intake of fiber and potassium, depending on individual eating habits. Most of the investigations on the health effects of apples have focused on their lipid-lowering effects (2–4) or connected metabolic disturbances (5) and more recently, on their anti-oxidative properties (6–8).
The fiber in apples, which is thought to play a major role in its lipid-lowering capacities, is not found in especially high concentration (2–3 g/100 g), and soluble fibers such as pectin represent <50% of the fiber in apples. Nevertheless, it has been reported that this fraction probably contributes to the effects of apples on lipid metabolism (9). In fact, apples also contain a variety of secondary plant metabolites such as polyphenols, to which have been ascribed a multiplicity of metabolic effects, including anti-oxidative properties but also, in some cases, more direct effects on lipid metabolism (10). However, the effects of polyphenols on lipids have been investigated essentially with isoflavones (chiefly from legumes such as soybeans) or citrus flavonoids, which are not representative of apple polyphenols. These compounds are more complex and essentially represented by procyaninidins (epicatechin polymers), together with quercetin or phloretin derivatives, which are apple specific (1).
To further establish the roles of apple constituents in lowering lipids, a study was carried out in mildly hypercholesterolemic rats fed diets enriched in different apple fractions: apple pectin (PEC), a high polyphenol (PL) cider apple extract or both fractions (PEC + PL). Because most of the effects of these fractions are likely to occur in the digestive tract, the effects of the apple fractions on intestinal bile acids, large intestine fermentations and plasma and tissue lipids were also studied.
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MATERIALS AND METHODS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The pectin used was a highly methylated (70–75%) apple pectin (P8471; Sigma, St. Louis, MO). Jeanne Renard apples, a cider variety particularly rich in polyphenols at 
7 g/kg fresh weight (11), were obtained from the Cider Research Laboratory (INRA Rennes, France). Before freeze-drying, the apple cores were removed and the rest of the fruit (skin + pulp) was cut into 10-g pieces that were frozen at -80°C in aluminum-rectified trays. After 24 h deep-freezing, the samples were transferred into the freeze-dryer and dehydrated for 72 h. The freeze-dried apple pieces were then rapidly powdered in a grinder, and the resulting powder was stored desiccated at 4°C in sealed plastic bags. The semipurified diets were prepared as described in Table 1: a fiber-free (control) diet, a 5 g/100 g PEC diet, a 10 g/100 g PL diet and a mixed diet (PEC + PL) containing both 5 g/100 g pectin and 10 g/100 g freeze-dried apple. All diets had a moderate concentration of cholesterol (0.25 g/100 g) and were balanced in mono- and disaccharides (fructose, glucose and sucrose), given that these compounds represent the major part of apple dry matter. Pectin, freeze-dried apple or the mono- and disaccharides were substituted for wheat starch in the experimental diets.
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Male Wistar rats (IFFA/CREDO, L’Arbresle, France) weighing 150 g were randomly allocated to four groups of 10 rats and fed for 21 d one of the four semipurified diets distributed as a moistened powder. The rats were housed one per cage (wire bottomed, to limit coprophagy), maintained in temperature-controlled rooms (22°C), with a dark period from 2000 to 0800 h, and had access to food during the dark period. Body weight was recorded on d 0, 7, 14 and 21 of the experiment. Food intake determination and collection of feces were performed on 4 consecutive days at the end of the experiment. Rats were maintained and handled according to the recommendations of the INRA Ethics Committee, in accordance with decree no. 87-848.
At the time of sampling (0900 h), rats were killed by sodium pentobarbital (40 mg/kg) injection and maintained on a plate at 37°C. Blood was drawn from the abdominal aorta and portal vein into an heparinized syringe and plasma was obtained after centrifugation at 10,000 x g for 2 min. Aliquots of plasma were stored at 4°C for lipid determination. Liver and heart were excised and 3 g of liver and the entire heart were immediately freeze-clamped and stored at -80°C. The cecum with contents was removed and weighed. For each rat cecal contents were transferred into two microfuge tubes; one was immediately frozen at -20°C and the pH of the cecal contents was measured in the other. The cecal wall was flushed clean, blotted and weighed (cecal wall weight).
Reagents.
All reagents were analytical-reagent grade. Nitrogen and helium used during chromatographic analyses were high purity grade. The triglyceride PAP and cholesterol RTU assay kits were obtained from BioMérieux (Charbonnière-les-Bains, France). Enzymes, coenzymes and anion standards were purchased from Sigma.
Biochemical measurements.
Plasma bile acids were quantified using the reaction catalyzed by 3
-hydroxysteroid dehydrogenase (EC 1.1.1.50) in 96-well microplates (30 µL plasma + 90 µL buffer), using no-enzyme blanks for each sample. Cholesterol and triglyceride concentrations were assayed in plasma using commercial kits (see above). Liver and heart samples were homogenized and lipids were extracted with chloroform/methanol (2:1, v/v). Triglycerides in the lipid residues were saponified using 0.5 mol/L KOH-ethanol at 70°C for 30 min, after which 0.15 mol/L MgSO4 was added to neutralize the mixture. After centrifugation (2000 x g, 5 min) the supernatant was assayed for glycerol as it was for plasma. Cholesterol in the lipid residue was measured with an enzymatic procedure as described above. A polyvalent control serum (Biotrol-33-plus) was treated in parallel with samples to assess the accuracy of the results in plasma and tissue lipid analysis.
Freeze-dried small intestine or feces were powdered and aliquots extracted with 2 x 10 volumes of 0.5 mol/L KOH-ethanol at 60°C, and bile acids were then quantified using the reaction catalyzed by 3-hydroxysteroid dehydrogenase (EC 1.1.1.50). Neutral sterols in feces were extracted three times with 1 mL of 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 an N2 stream and the residue dissolved in hexane. Portions (1 µL) of this extract were injected into a gas chromatograph (Daniducational, Monza, Italy) fitted with a 12 m x 0.25 mm (I.D.) fused silica BP10 capillary column (SGE, Villeneuve-St-Georges, France) with flame-ionization detection. Helium was used as a carrier gas, and the sterols were separated using a temperature gradient from 240 to 270°C (4°C/min).
Short-chain fatty acids (SCFA) were measured by gas-liquid chromatography in supernatants of cecal contents (40,000 x g, 15 min), as described by Rémésy and Demigné (12). For analysis of non-SCFA anions, cecal supernatants were diluted 200-fold with milli-Q water (Millipore, Bedford, MA) and analyzed using a DX320 Dionex chromatograph (Sunnyvale, CA). The anions were separated on a 4 x 250 mm AS 11 column/AG 11 precolumn (flow rate, 1 mL/min). An EG40 eluent generator controlled elution by a OH- gradient (0.5 to 35 mmol/L in 20 min) and the conductimetry detector was preceded by an ASRS self-regenerating suppressor. Peaks were identified and quantified by comparison with pure anion standards.
Statistical analysis.
Values are given as the means ± SEM and, where appropriate, data were tested by two-way ANOVA using the general linear models procedure of the SuperANOVA package (Abacus, Berkley, CA). Individual comparisons were made by least-squares means. Differences of P < 0.05 were considered significant.
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RESULTS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Food intakes did not differ among the groups but the body weight gain and food conversion efficiency (FCE) were slightly reduced in rats fed diets containing pectin (Table 2). The liver weight was 4.8 g/100 g body except in rats fed the PEC + PL diet (4.2 g/100 g body). The PEC and PL diets significantly enlarged the cecum (+62 and +29%, respectively), with the maximal hypertrophy of the cecum in rats fed the PEC + PL diet (+112%). The cecal wall weight was relatively proportional to the cecal weight (25%) except in the PEC + PL–fed group (19%). The cecal pH was near neutrality in rats fed the control, PEC or PL diets, and an appreciable acidification of the cecal pH (6.5) occurred only in rats fed the PEC + PL diet. The dry matter excretion in feces was 33% greater than in controls in rats fed the PEC diet and 100% greater in rats fed the PL or PEC + PL diets.
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The total SCFA concentration in the cecum of control rats was 84 mmol/L, and in the range of 111–124 mmol/L in rats fed the other diets (Table 3). The cecal SCFA pool was larger in rats fed the PEC than in those fed the PL diet and was the highest in rats fed the PEC + PL diet. The acetate molar ratio was particularly high in rats fed diets containing PEC, and all the apple-containing diets depressed the propionate molar ratio. The butyrate concentration in the cecum of control rats was low (6.0 mmol/L) and it was significantly enhanced (P < 0.001) in rats fed the PL diet (+202%) or the PEC + PL diet (+166%). The cecal butyrate pool was significantly enlarged in all diet groups containing apple products. The maximal value, 63 µmol (+350% of controls), occurred in rats fed the PEC + PL diet (data not shown).
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20 mmol/L (chiefly chloride) in control rats and in those fed the PL diet, but it reached 70 mmol/L in rats fed the PEC diet. It was only 38 mmol/L in those fed the PEC + PL diet. The PEC diet increased the concentration of phosphate 10-fold relative to controls and this occurred, but to a lesser extent, in rats fed the PEC + PL diet. In rats fed the PEC diet, there was an accumulation of galacturonate and succinate in the cecum (20 mmol/L each), whereas these anions were essentially undetectable in control rats. Rats fed the PEC + PL diet also had detectable concentrations of succinate and galacturonate (6–9 mmol/L) and small quantities of galacturonate were also detected in rats fed the PL diet. Rats fed diets containing PL had lower concentrations of sulfate than controls (P = 0.001). Intestinal and fecal steroids.
Daily cholesterol intake was in the range of 137–147 µmol/d (Table 4). The PEC, PL and especially the PEC + PL diets decreased the bile acid concentration in feces. Bile acid excretion was unaffected in rats fed the PL diet, but was significantly reduced in rats fed the PEC and PEC + PL diets. Similar to bile acids, fecal sterol excretion was not altered in rats fed the PL diet, but the PEC and PEC + PL diets significantly increased total sterol excretion (+43 and +30%, respectively). Estimation of total steroid excretion confirmed that the PL diet did not affect this variable. Because of the opposite responses of bile acid and neutral sterol excretions in rats fed the pectin-containing diets, the increase in total steroid excretion was limited in rats fed the PEC diet (+21%) and the PEC + PL diet (+14%). There was however, a reduction in the apparent percentage of cholesterol absorption: 30% in rats fed the PEC or PEC + PL diets and 43% in controls or PL-fed rats.
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10 µmol/L, near the limit of detection (data not shown). Much greater concentrations were detected in the portal vein (60–100 µmol/L) and rats fed the PEC or PEC + PL diets had higher concentrations than control rats (P < 0.05). Plasma and organ lipids.
Control rats fed 0.25 g/100 g cholesterol were mildly hypercholesterolemic (2.5 mmol/L). Cholesterolemia in rats did not differ between rats fed the PEC or PL diet but the PEC + PL diet significantly decreased plasma cholesterol (-24% relative to controls) (Fig. 1). There was a concomitant reduction in plasma triglycerides in rats fed the PEC + PL diet (-35%, P < 0.01). Plasma triglycerides were less than in controls in rats fed the PL diet also (-29%, P = 0.03). The lipid concentrations of the liver were also responsive to the diets but not in the same way as plasma. Liver cholesterol and triglycerides were significantly lower in rats fed the PEC-containing diets but not in those fed the PL diet. Heart lipid concentrations did not differ among the groups (data not shown).
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DISCUSSION |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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300 g fresh apple) or, alternatively, 1 kg/d when expressed per BW0.75, which although definitely a high value, is not completely unrealistic if the totality of fruit and vegetable intake is taken into account. The polyphenol content of the Jeanne Renard apple is high (5- to 10-fold greater than in dessert apples) but the overall polyphenol concentration of the PL diets was 0.7 g/kg, which is not unrealistic for human diets (14). The presence of freeze-dried apple in the diet substantially enlarged the cecum and changed SCFA production, although the present apple diet contained only 1.6% fiber, a very low level for a rat experimental diet. Only 40% of the apple fiber fraction, essentially pectin (15), is soluble and the insoluble moiety is composed chiefly of glucans (nonlignified cellulose), which are relatively well fermented by the microflora. Henningsson et al. (16) reported that apple pectin is highly degradable in the rat hindgut (assessed by a low recovery of uronic acids in feces), whereas apple fiber is less effectively digested. Butyric acid–rich fermentations that occur with apples do not seem to be directly connected with the presence of pectin, given that pectin consistently promotes high acetic acid fermentation (17). Pectin fermentation in the cecum also led to a substantial accumulation of galacturonate (20 mmol/L). The physiological consequences of galacturonate accumulation are still poorly understood but uronic acids and acetate have been reported to stimulate colonic mucin secretion (18). Galacturonate is also a calcium sequestrant, which could account for the dramatic increase of soluble phosphate, being proportional to galacturonate concentration in the apple pectin groups. Succinate, which accumulates concomitantly with galacturonate, is a normal product of large bowel fermentation and is an intermediate in the synthesis of propionate (19). However, in the present experiment, the changes in the succinate concentration in rats fed the pectin diets were not accompanied by any change in the concentration of propionate, in keeping with the observations of Morita et al. (20). Galacturonate and succinate concentrations in the cecum of rats fed the PEC + PL diet were markedly lower than in those fed the PEC diet. The fact that acidic pH conditions occurred with the PEC + PL diet suggests that fermentations were probably initiated and, conceivably, substrate conditions in the cecum of rats fed the PEC + PL diet might have favored a more extensive degradation of pectin and limited galacturonate and succinate accumulation. Polyphenols are also possible modulators of digestive fermentations because they were present in high concentration in the apple freeze-dried extract and a substantial part, especially procyanidins, escapes absorption in the small intestine, reaching the large intestine where they accumulate (21). The actual effect of polyphenols (or their metabolites) on cecal bacteria is not fully understood; there is evidence of a bacteriostatic effect of tannins (21), although the effects of apple polyphenols could be less potent and merely influence the activity of the cecal microflora through, for example, changes in nitrogen stores in the large intestine (22).
It has been previously reported (2,23) that adding apple pectin to the diet of cholesterol-fed hamsters significantly reduces plasma and liver cholesterol, whereas Trautwein et al. (24) did not observe pectin effects in cholesterol-fed hamsters. It has been recently proposed that polygalacturonic acid in the pectin molecule is responsible for the cholesterol-lowering properties of pectin, and that viscosity could be an important factor in determining the lipid-lowering potency of pectin (25). The PEC diets were actually more viscous than the other diets, and this could account for the reduction of the apparent cholesterol absorption observed in rats fed these diets. In guinea pigs greater numbers of hepatic apoB/E receptors and a 100% faster LDL fractional catabolic rate, compared to controls, have been observed with the addition of pectin, although these effects are more potent with addition of psyllium (26). In the present investigation, the 5 g/100 g apple pectin diet had no effect on plasma lipids, but effectively lowered liver cholesterol and triglycerides, which could be attributed to the fact that it markedly enhanced neutral sterol excretion. Paradoxically, it has been reported that pectin could induce HMG-CoA reductase and decrease mitochondrial fatty acid oxidation and phosphatidate phosphohydrolase (27) and enhance liver cholesterogenesis (28) and lipogenesis (29). These equivocal effects on lipid metabolism enzymes, together with a propensity to generate large quantities of acetate (16), which is an effective precursor of lipid synthesis (30), could explain why pectin alone is not a consistently lipid-lowering fiber.
The association of pectin with the polyphenol-rich apple extract effectively lowered circulating cholesterol and triglyceride concentrations, in much the same way as previous experiments using whole fruit extract (4,23,31,32). It is noteworthy that the effects of the PEC + PL diet on steroid excretion and cholesterol absorption were not greater than those attributed to PEC alone. Various investigations support the view that some polyphenols (or polyphenol-rich fractions), such as citrus flavonoids (33), soy bean isoflavones (34) or grape extracts (35) may lower lipid concentrations. However, data on the flavonoids present in apples essentially focuses on quercetin (36) and seldom on other constituents such as phloretin derivatives. Another interesting feature is that PEC stimulated steroid excretion through a greater elimination of cholesterol and coprostanol, concomitantly with a reduced excretion of bile acid in feces. This feature is rather unusual because the cholesterol-lowering effects of fibers are frequently considered to indicate the accelerated oxidation of cholesterol, through induction of liver cholesterol 7-hydroxylase (CYP7a) in response to interactions of bile acids with dietary constituents (37) and depressed reabsorption from the intestine (38,39). This classical scheme implies that portal vein bile acids would be systematically depressed by the fiber diets, which contradicts the increase of portal concentrations in rats fed the PEC and PEC + PL diets. In fact, this response is consistent with previous reports of cholesterol-lowering effects and CYP7a induction, in parallel with a high rate of bile acid reabsorption in portal or ileal mesenteric veins, or from the large intestine (40–42). Furthermore, it must be noted that the effectiveness of fiber on plasma cholesterol is generally concomitant with an enlargement of the intestinal bile acid pool (which appeared only with the PEC + PL diet) (31,42), although the mechanisms are still poorly understood. Cholesterol and bile acid biosynthesis in the liver are the targets of coordinated and sophisticated processes of molecular control (43). In addition, the possibilities of molecular control have been identified in the intestine for absorption of bile acids [especially through ileal bile acid transporter (iBAT) (44)] and more recently, of cholesterol itself, through reverse transport on ABC units, which are members of a large family of ATP-binding cassette transporters involved in the energy-dependent transport of a variety of substrates (45). In this investigative area, the possible effects of fiber and/or micronutriments such as polyphenols are practically ignored, although they certainly merit further specific investigations.
In conclusion, this work illustrates the effectiveness of combining apple components PEC and PL to account for the biological effects of the whole fruit, which are less effective when used separately. This concept of interaction between nutrients, illustrated by a recent work showing that procyanidins inhibit enzymatic degradation of cell walls in apples (46), could certainly be expanded by taking into account nutrients such as vitamins or minerals, especially with respect to anti-oxidative protection (1,4,8,31).
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FOOTNOTES |
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2 O.A. was funded by a Ph.D. scholarship from the scientific committee of the Agency for Promotion of Fresh Fruits and Vegetables (APRIFEL, Paris, France).
4 Abbreviations used: ABC, ATP-binding cassette; FCE, food conversion efficiency; FFA, free fatty acids; HMGCoA, hydroxymethylglutaryl coenzyme A; iBAT, ileal bile acid transporter; PEC, apple pectin; PL, high polyphenol freeze-dried apple.
Manuscript received 1 October 2002. Initial review completed 2 November 2002. Revision accepted 20 February 2003.
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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