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Nutrient Metabolism

Rye Bread Enhances the Production and Plasma Concentration of Butyrate but Not the Plasma Concentrations of Glucose and Insulin in Pigs¹

Department of Animal Health, Welfare and Nutrition, Danish Institute of Agricultural Sciences, Research Centre Foulum, DK-8830 Tjele, Denmark

²To whom correspondence should be addressed. E-mail: knuderik.bachknudsen{at}agrsci.dk.

	ABSTRACT

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
The present investigation was undertaken to study the gastrointestinal and physiologic properties of diets based on soft and crisp wheat and rye breads similar in dietary fiber (DF; 230–235 g/kg dry matter) but with different proportions of the main DF polymers: in wheat, cellulose, and in rye, arabinoxylans (AX). The 2 diets provided all macronutrients; consequently, they had lower fat and sugar contents and a higher DF content than human mixed diets. The nutritional properties were studied in experiments in which pigs with cannulated ilea and catheterized portal veins and mesenteric arteries served as models for humans. The characteristics studied were degradation of nutrients, flow at the ileum, fecal output, absorption of nutrients deriving from the assimilation of cereal carbohydrates, and the insulin response. Apparent viscosity at the terminal small intestine, the ileal flow of water, flow and digestibility of noncarbohydrate constituents, but not of carbohydrates at the terminal ileum or the plasma concentrations of glucose and insulin, were higher when pigs consumed the rye compared with the wheat diet. The 2 diets provided approximately equal amounts of carbohydrates available for fermentation in the large intestine but because AX from the rye diet was more degradable than cellulose from the wheat diet, the quantitative degradation in the large intestine was more than twice as high when pigs consumed the former compared with the latter diet. The consequences included moister feces and significantly enhanced gut production and plasma concentrations of butyrate when pigs consumed the rye diet compared with the wheat diet.

KEY WORDS: • carbohydrates • catheterized pigs • glucose • short-chain fatty acids • butyrate

Recent epidemiologic studies showed that whole-grain cereal products possess health-promoting effects including protection against cardiovascular diseases, some forms of cancer, and type 2-diabetes (1,2). Among the cereals, rye has long been part of an ordinary diet in Scandinavia and other Northern European countries, where it is consumed as whole-grain dark soft breads and crisp breads. In countries like Denmark and Finland, dietary fiber (DF)³ from rye accounts for 30% of the intake of total DF (3,4), which makes rye the foremost important DF food items in these countries. The carbohydrate composition of rye is in many aspects similar to wheat, but rye has a higher content of fructans, arabinoxylans (AX), and mixed linked ß(1–3;1–4)-D-glucans (ß-glucans) than whole-grain wheat (5). AX represents a heterogenic group of polysaccharides of DF and is present along with cellulose and ß-glucan at various proportions in the endosperm, aleurone, and pericarp/testa tissues of the grain (6). The higher level of soluble AX in rye than wheat is due to a higher concentration of these polymers in the endosperm.

The DF composition influences the digestion and absorption processes along the gastrointestinal tract (7). In the small intestine, soluble DF raises the luminal viscosity (8) and increases the water binding capacity (WBC) of digesta (9), thereby slowing the rate of digesta movement and the rate at which glucose is delivered to the enterocytes (8). In the large intestine, the nondigested residue, which, to a large extent, consists of nondigestible carbohydrates (7,10), will stimulate bacterial fermentation and SCFA generation, and dilute the colonic content of potentially carcinogenic compounds e.g., secondary bile acids (11). The SCFAs produced (e.g., acetate, propionate, butyrate) act as acidifiers with consequences for the luminal pH and provide nutrients for the epithelial cells lining the large intestine. Butyrate, in particular, is an important metabolite because it is the principal oxidative fuel for the colonocytes, where it is metabolized by ß-oxidation (12). Butyrate was also shown to have several cellular effects i.e., influence on cell maturation, cell differentiation, and apoptosis, presumably mediated through the effect butyrate may have on gene and protein expressions (13,14).

The present investigation was undertaken to study the gastrointestinal and physiologic properties of wheat- and rye-based diets similar in DF, but with different proportions of the main DF polymers. These differences can be expected to influence the physicochemical properties of digesta materials and the digestibility in different ways, and thereby the absorption and plasma concentrations of glucose, lactic acid (LA), and SCFAs. To investigate that hypothesis, we performed studies with surgically modified pigs used as models for humans, on the luminal environment and the absorption profile of nutrients derived from the breakdown of cereal polysaccharides. We consider pigs with cannulated ilea and catheterized portal veins and mesenteric arteries to be good models for humans (8,15,16) when studying the quantitative absorption of nutrients because the cannulation of the gastrointestinal tract and catheterization of the bloodstreams enable sampling of digesta and blood in close proximity to the digestive processes and before extraction of metabolites in the liver.

	MATERIALS AND METHODS

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Breads and diets

The diets were made of wheat soft and crisp bread or rye soft and crisp bread. Wheat and rye soft breads were produced at Nordmills (Nordmills, Cerealia AB) and wheat and rye crisp bread were produced at Wasa Bread (Wasa Bread AB). The rye crisp bread contained whole-kernel rye flour, rye bran (Wasa T2), fat, and salt as the main ingredients, and the corresponding wheat crisp bread contained white wheat flour, purified wheat fiber essential as cellulose (Vitacel WF 600, Rettenmair and Söhne), sugar (sucrose), salt, and dry malt. The soft rye bread contained white wheat flour, rye bran (B3-fin, Nordmills, Cerealia AB), baker’s yeast, fat, salt, and sugar, and the corresponding soft wheat bread contained white wheat flour, vitacel, baker’s yeast, fat, salt, and sugar. Immediately after production, the soft bread was frozen at –20°C until consumption, whereas the crisp bread was stored dry. The diets prepared from soft and crisp bread were fortified with vitamins and minerals and provided 19, 15, and 66% of energy from fat, protein, and carbohydrates, respectively (Table 1). Compared with diets for optimal growth of pigs at the present physiologic state, the diets provided 45% of the recommended concentration of lysine (first limited amino acid) but 260% of the concentration of lysine for maintenance. A semisynthetic diet (SSD) was composed from wheat starch (709.8 g/kg), cellulose (80.0 g/kg), casein (182.2 g/kg), and vitamins and minerals (28 g/kg).

The pigs used in all 4 studies were from the Danish Institute of Agricultural Sciences Swine herd, Foulum, Denmark.

    Study 1. The main purpose of study 1 was to determine the physicochemical properties of ileal digesta and estimate the digestibility of carbohydrates and other macronutrients up to the end of the small intestine. The study was carried out with 8 male castrated pigs (54.5 ± 4.3 kg) selected pairwise from 4 litters. Each pig was fitted with a T-cannula in the ileum 15 cm anterior to the ileocecal junction and given antibiotic (Streptocillin) for 3 d postsurgery. After a 10-d recovery period from the surgery, the 2 groups of pigs were gradually introduced to the wheat or rye diets for 4 d and housed individually in 4-m² smooth-walled pens with a concrete floor. For the measurements of the physiochemical properties of ileal digesta and ileal digestibility, the pigs were moved to individual metabolic cages. The rye group consumed 1586 g dry matter (DM)/d [2.6% DM of body weight (BW)] and the wheat group 1591 g DM/d (2.8% DM of BW) for 1 wk. The bread was cut into pieces, mixed with chromic oxide (2 g/kg DM), and fed in equal amounts 3 times/d (0700, 1500, and 2200 h). Ileal digesta were collected hourly from 0700 to 1500 h for 3 d and frozen. On d 2, a subsample was collected from 0900 to 1000 h in the morning and 1300 to 1400 h in the afternoon and used to measure viscosity and WBC. The ileal digesta collected were pooled and frozen at –20°C.

    Study 2. The purpose of study 2 was to determine the total tract digestibility of macronutrients and the fecal bulking properties. Female pigs (n = 6) with an initial BW of 38.7 ± 2.7 kg were used for the study. The study was designed as a crossover experiment with washout periods before, between, and after the dietary interventions. The pigs were fed SSD for 1 wk in periods 1, 3 and 5, and the wheat (1862 ± 70 g DM/d; 2.8% DM of BW) and rye diets (1894 ± 72 g DM/d; 2.8% DM of BW) were fed for 2 wk in periods 2 and 4. The breads were treated as in study 1 and fed in equal amounts twice daily (0930 and 2130 h) together with a fixed amount of water (1:2.5). The stool samples were collected in plastic bags for 3 d. Stool samples were also taken from the rectum in periods 1, 3 and 5. The stool samples collected were kept frozen at –20°C.

    Study 3. The purpose of this study was to quantify the uptake and plasma concentrations of metabolites derived from the assimilation of carbohydrates, glucose, LA, and SCFAs. The study was a crossover design with 4 male castrated pigs (BW of 44.6 ± 2.4 kg) fed the 2 diets for 1 wk. Each pig was surgically fitted with 2 catheters, one in the portal vein (1.2 mm, i.d.; Buch & Holm) and the second in the mesenteric artery (1.00 mm, i.d.; Buch & Holm), and with an ultrasonic blood flow probe (14 mm, Transonic System) around the portal vein. A flowmeter (Transonic® T201D flowmeter with P-option, Transonic System) was used for measuring the flow rate. The pigs were given Streptocillin for up to 4 d after surgery. After 10 d of postsurgery recovery, the pigs were gradually introduced to the 2 experimental diets and fed 1250 ± 15 g DM/d (2.4% DM of BW) of the wheat diet or 1250 ± 24 g DM/d (2.5% DM of BW) of the rye diet. The bread was cut into pieces, mixed 1:2.5 (wt:wt) with water and fed in equal amounts 3 times/d, at 0700, 1500, and 2200 h. The portal and arterial blood samples were collected 2 times/wk on d 5 and 7 at –30, 0, 30, and 60 min, then at 60-min intervals up to 480 min after the morning feeding and then again at 540 min. The blood was collected in 2 heparinized plastic tubes (9 and 4 mL) and 1 EDTA heparinized plastic tube (2 mL) and centrifuged (3000 x g for 10 min at 8°C) to separate RBC from plasma. The plasma was kept frozen at –20°C until analysis. The blood flow (L/min) was measured at the same times as the blood samples were taken. On the days of blood sampling, any food remains were collected and a rectal sample was taken at 1200 h and frozen at –20°C.

    Study 4. The purpose of this study was to measure the absorption kinetics of glucose, LA, and SCFAs after ingestion of a single dose of the rye diet. Except for 1 pig, the group was the same as that used in study 3; the missing pig was replaced by one of similar weight (BW 48.2 ± 6.3 kg). The pigs were fed SSD 3 times/d for 4 d and the morning feeding on d 5. The pigs were then deprived of food for 24 h; on d 6, they were fed 1 dose (492 g DM; 1% DM of BW) of the rye diet, after which blood samples were taken at –30, 0, 30, and 60 min, and then at 60-min intervals to 960 min after the morning feeding; the pigs were then fed the rye diet. The whole procedure was repeated the following week. All animal experiments complied with the guidelines of the Danish Ministry of Justice with respect to animal experimentation and care of animals under study.

Analytical methods

All chemical analyses were performed in duplicate and physicochemical analyses in triplicate. Chromic oxide, LA, SCFAs, viscosity, and WBC determinations were performed on wet materials; other analyses were performed on freeze-dried materials. The DM contents of feed, digesta, and feces were determined by drying to constant weight at 103°C (practically 20 h); protein was determined by the Kjeldahl method (Reference No. 978.02) (17) using a Kjeltec 1035 autoanalyser (Foss Tecator AB). Ash was analyzed by an AOAC method (17), fat (hydrochloric acid-fat) was extracted with diethyl ether after acid-hydrolysis (18), and chromic oxide was determined using the method of Schürch et al. (19). Feces and ileum samples were analyzed for SCFAs and LA by GC as described in detail by Jensen et al. (20).

Sugars (glucose, fructose, and sucrose) and fructans in feed, ileal digesta, and fecal samples were analyzed by the enzymatic-colorimetric method of Larsson and Bengtsson (21) and the sucrose present as part of fructans corrected as described by Bach Knudsen and Hessov (22). Total starch was analyzed by the enzymatic-colorimetric method of Bach Knudsen (5), nutritional classification of the starch by the method of Englyst et al. (23), and total and insoluble ß-glucan determined by the enzymatic-colorimetric method of McCleary and Glennie-Holmes (24). Soluble ß-glucan was determined as the difference between total ß-glucan and insoluble ß-glucan after extraction of the soluble ß-glucan with water. Total nonstarch polysaccharides (NSP) and their constituent sugars were determined as alditol acetates by GLC for neutral sugars and by a colorimetric method for uronic acids using a modification of the Uppsala procedure (25) and the procedure of Englyst et al. (26) as described by Bach Knudsen (5). Content of cellulose was calculated as:

Arabinoxylans (AX) were calculated as:

and soluble NSP as:

Klason lignin in the diets was measured gravimetrically as the residue resistant to 2 mol/L H₂SO₄.

Viscosity was measured in extracts of diets and digesta following the procedure of Johansen et al. (27). Centrifugation of diet extracts and digesta samples removes materials that contribute to the rheological behavior of digesta; thus the values can be considered to be only indicative. Values of apparent viscosity at shear rate 30 s^–1 are reported. The procedure for WBC in diet and digesta followed essentially that of Canibe and Bach Knudsen (28).

Plasma concentrations of SCFAs (acetate, propionate, butyrate, and isobutyrate) were analyzed using the method of Brighenti (29); plasma concentrations of LA were analyzed by means of specific enzymes (30,31), glucose by a glucose-oxidase kit (32), and immunoreactive insulin according to Tindal et al. (33).

Calculations and statistical analysis

The content of polysaccharide residues was calculated as anhydrosugars, and all apparent digestibilities, recoveries, and net disappearance measurements in studies 1 and 2 were calculated relative to the Cr₂O₃ concentration as described by Bach Knudsen et al. (34). Because the feeding level varied throughout the experiment, the quantitative data in studies 1 and 2 were calculated at an intake level of 1250 g DM/d, similar to the intake level in study 3.

The quantitative absorption of glucose, LA, and SCFAs and apparent insulin production were calculated from the porto-arterial differences and the portal flow measurement as described by Rérat et al. (35). Insulin can be described only as apparent due to the pulsatile secretion, the hepatic and kidney extraction effects, and variable half-life values (8). The 24-h net absorption or apparent production was calculated as 3 times the measured 8-h values.

The results from study 1 were analyzed by a 1-way ANOVA model and the results from study 2 as a randomized block experiment (36). Significant differences between treatment means were identified by Student-Newman-Keul with a level of significance of P < 0.05. The daily absorption of glucose, LA, and SCFAs was analyzed as a crossover design, and the blood-flow rate, portal and arterial glucose, LA, SCFAs, and insulin were analyzed as repeated measurements (36). All statistical analyses were done using SuperAnova (Abacus Concepts).

	RESULTS

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
    Diets. The wheat and rye diets were formulated to be nearly similar in macronutrient content (Table 1). The content of total DF was 230–235 g/kg DM in both diets, but the proportion of DF polymers (AX, cellulose, and Klason lignin) varied between the 2 diets. The wheat diet had a high total content and proportion of cellulose, whereas the rye diet had a high content and proportions of AX and Klason lignin. The content of soluble NSP, predominantly as AX, was 140% higher and extract viscosity 250% higher in the rye diet compared with the wheat diet, whereas the WBC in the diets did not differ. The concentration of starch was 529 and 455 g/kg DM in the wheat and rye diets of which 64–69% was rapidly digested and 33–36% slowly digested; no starch was characterized as resistant (data not shown).

    Studies 1 and 2. The 2 diet groups did not differ in the apparent ileal digestibility of any of the carbohydrate fractions except soluble NSP (Table 2). The apparent digestibility of ash, organic matter, protein, and fat, however, was significantly lower after consumption of the rye diet compared with the wheat diet. These differences translated into a significantly higher ileal flow of digesta when pigs consumed the rye diet (200 g/h) compared with the wheat diet (116 g/h). The higher flow of ileal digesta was caused by a higher flow of water, dry solids, noncarbohydrate constituents, and organic acids, whereas the ileal flow of carbohydrates did not differ when pigs consumed the 2 diets. When the pigs consumed the rye diet, AX represented 56% of total carbohydrates, whereas cellulose accounted for 55% of the carbohydrates when the wheat diet was consumed.

View larger version (15K): [in this window] [in a new window]   FIGURE 1 Apparent viscosity (A) and WBC (B) of ileal digesta collected during morning and afternoon from pigs fed wheat- and rye-based diets (Study 1). Values are means ± SEM, n = 4.

Taken as a whole, the amount of organic residues disappearing in the large intestine was 174 g/d with carbohydrates accounting for 130 g/d when the pigs consumed the rye diet but only 72 g/d with 61 g/d carbohydrates when the pigs consumed the wheat diet.

    Study 3. The blood flow rate in the portal vein was not influenced by the diet, but varied in relation to the time after feeding. The mean flow was 30.3 mL/(kg BW · min) and the variation from 1.4 L/min at feeding increasing by 21% to 1.7 L/min 1 h after feeding, after which it decreased to 1.4 L/min before the next feeding (data not shown).

The concentrations of glucose in either the portal vein or the mesenteric artery did not differ in pigs fed the 2 diets (Fig. 2A, B and Table 3). The concentration of glucose in the portal vein and mesenteric artery was 5 mmol/L at feeding; it increased by 3 mmol/L 0.5–2 h after feeding, after which it gradually decreased to the prefeeding level before the next feeding. The concentration of glucose in the artery was less variable throughout the feeding cycle. The total amount of glucose absorbed corresponded to 98% of ingested starch and sugars after pigs consumed the rye diet and 66% of ingested starch and sugars after pigs consumed the wheat diet. The absorption rate varied from 188 to 226 mmol/h for wheat consumption and 222–300 mmol/h for rye consumption during the first 3 h after feeding, after which there was a steady decline to 18–78 mmol/h during the last 2 h before the next feeding (data not shown).

View larger version (20K): [in this window] [in a new window]   FIGURE 2 Portal and arterial blood concentrations of glucose (A) and insulin (B) after intake of the wheat- and rye-based diets (Study 3). Values are means ± SEM, n = 4. P.V., portal vein; M.A., mesenteric artery.

The average portal concentration of LA when pigs consumed the wheat diet was 1.09 mmol/L (range 0.9–1.5 mmol/L) and 1.32 mmol/L (range 0.9–2.0 mmol/L) when they consumed the rye diet (Table 3). The concentration in the mesenteric artery was closely associated with that of the portal vein at all sampling points at a level that was 0.1–0.15 mmol/L lower. At both sampling sites, the concentration of LA peaked 1 h after feeding and the total absorption of LA did not differ between the 2 diets.

Diet did not affect the concentration of total SCFAs in the portal vein for the first 4 h after feeding (Fig. 3A, B and Table 3); 5 h after feeding, however, the concentration of SCFAs in the portal vein increased when the pigs consumed the rye diet, whereas the concentration was stable in pigs consuming the wheat diet. Of the individual acids, primarily the concentration of butyrate was influenced by the dietary composition. There was also a significant difference in the concentration of butyrate in the mesentery artery. The absorption of total SCFAs was not affected, but the absorption of butyrate was significantly higher when pigs consumed the rye (13.1% of total SCFAs) compared with the wheat diet (5.7% of total SCFAs) (Table 3).

View larger version (22K): [in this window] [in a new window]   FIGURE 3 Portal and arterial blood concentrations of total SCFA (A) and butyrate (B) after intake of the wheat- and rye-based diets (Study 3). Values are means ± SEM, n = 4. P.V., portal vein; M.A., mesenteric artery.

View larger version (15K): [in this window] [in a new window]   FIGURE 4 Portal and arterial blood concentrations of glucose (A) and insulin (B) following the intake of one dose of the rye-based diet (Study 4). Values are means ± SEM, n = 4. P.V., portal vein; M.A., mesenteric artery.

The concentration of total SCFs and butyrate was constant 0–4 h after feeding but increased during the next 4 h to reach a plateau level of 800 and 55 µmol/L, respectively (Fig. 5A, B). For the entire absorption period, SCFAs and butyrate were 799 and 44 mmol, respectively (data not shown). The ingestion of the rye diet had a significant influence on the molar proportions of SCFAs in the portal vein; during the first 4 h after feeding, the proportions of acetate:propionate:butyrate:isobutyrate were 74:21:3:2 compared with 62:30:7:1 when the absorption reached the plateau level.

View larger version (18K): [in this window] [in a new window]   FIGURE 5 Portal and arterial blood concentrations of total SCFA (A) and butyrate (B) following the intake of one dose of the rye-based diet (Study 4). Values are means ± SEM, n = 4. P.V., portal vein; M.A., mesenteric artery.

	DISCUSSION

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

The quantitative glucose absorption during the first 3 h after feeding was remarkably similar to what was found in other studies (8,43,44). This is in support of the view that the rate-limiting step in starch assimilation is either the hydrolysis rate of oligosaccharides in the duodenum (35) or the final glucose transport into the depth of the enterocytes (45). When discussing the data on cereals, it should also be kept in mind that cereal starches have an open structure that enables easy access for the salivary and pancreatic -amylases, and partly gelatinized cereal starches are usually rapidly and well digested in the small intestine of humans and monogastric animals (15,23,46).

Although there was a substantial difference in the physicochemical properties of digesta materials after the pigs consumed the wheat- and rye-based diets, it did not affect either the hydrolysis of starch and sugars in the small intestine or the postprandial glucose and insulin response. The glucose level in the portal vein, however, was slightly lower than that seen in other studies with catheterized pigs fed wheat or oat breads with low or medium concentrations of DF (43) or a purified diet (8) with low concentrations of DF. The likely cause for that could be the general effect of DF on the luminal environment, which could facilitate a longer gastric retention time and a bulkier luminal environment; this would reduce the rate of hydrolysis and slow the movement of the hydrolysis products in the small intestine. Although the viscosity was higher after pigs were fed the rye diet compared with the wheat diet, it was not as efficient as seen in a study with guar gum in which Ellis et al. (8) found that the portal and arterial glucose concentrations could be reduced and peak glucose delayed when the purified diet was supplemented with either 20 or 40 g/kg of highly viscous guar gum. In a study with healthy humans, it was also found that there was no effect of the type of bread and concentration of DF on the glucose response, whereas there was a strong effect on the insulin response (47–49). The lack of effect on the glucose response in the human study, however, could be due to the measurements in the peripheral blood, which in well-regulated humans would be kept constant by graded concentrations of insulin.

Although the 2 diets did not influence either glucose or insulin concentrations in veins and arteries, the way food is consumed had a strong influence on these variables. The food fed to the pigs in study 3 was divided into 3 equal meals during the day, and there was only a minimal rise in glucose concentration in the mesenteric artery after feeding. In contrast, in study 4, the pigs had been food deprived for 24 h before feeding, which translated into a substantial rise in postprandial glucose concentration in the mesentery artery. The likely cause for that is low extraction of glucose in the liver to normalize the lower prefeeding glucose concentrations obtained after long-time food deprivation and a more pronounced stimulation of the insulin secretion. The apparent insulin production was 0.1 µmol/g starch and sugars consumed when the daily load was provided in 3 equal meals compared with 0.4 µmol/g starch and sugars when provided in 1 meal after 24 h of food deprivation.

The stomach and the small intestine (50) are the main sites of LA production; this was clearly pointed out by the better synchronization of the postprandial rise in LA concentrations in the portal vein and mesenteric artery to the uptake of glucose from the small intestine rather than the uptake of SCFAs from the large intestine. The tendencies for a higher LA concentration in the portal vein and mesenteric artery after the pigs were fed rye compared with wheat is most likely due to the higher dietary concentrations of sugars, fructans, and soluble NSP in the rye diet.

The most noticeable difference in the fermentation pattern in the large intestine is the much higher degradation of carbohydrates when the pigs consumed rye (130 g/d) compared with wheat (61 g/d) diet. It is also clear from the study that the difference is caused by the type rather than the amount of carbohydrate entering the large intestine. In pigs that consumed the wheat diet, cellulose was the main carbohydrate polymer entering the large intestine, whereas with rye consumption, it was AX; this has 2 consequences. First, AX in the rye diet is more degradable than the cellulose in the wheat diet, which stimulates bacterial fermentation, resulting in less carbohydrate residues, more protein and fat in the fecal mass, and moister feces after pigs consumed the former compared with the latter diet. Second, although high loads of cellulose typically result in stimulation of cellulytic bacteria and acetate formation (50), fermentation of AX stimulated formation of butyrate (51). Evidence for this is the significant change in molar proportion and total production after a single load of the rye diet in study 4 and the significantly higher proportion of butyrate in the portal vein and mesenteric artery after consumption of rye compared with wheat. The stimulation of butyrate production by AX-containing cereal products is in line with earlier findings demonstrating that oat AX rather than ß-glucan stimulated the formation of butyrate in the gut of pigs (51). It was also shown that wheat aleurone flour, rich in AX, increases butyrate concentration in the large intestine and reduces the colon adenoma burden in azoxymethane-treated rats (52). A recent study with healthy humans fed wheat pentosan (AX) or inulin-enriched bread (53) also showed enhanced butyrate production due to AX fermentation. Thus, there seems to be convincing evidence from this and other studies that cereal AX from rye, oats, and wheat can be used to enhance the gut production of butyrate, which may have favorable effects on colonic health (14,52). Because the effect of butyrate on gene and protein expression is not confined solely to colonocytes (13), it is of obvious interest that the enhanced gut production of butyrate raises not only the portal level of butyrate but also the arterial level, suggesting that butyrate potentially may have effects on cells not in direct proximity to the gut. This idea was further accentuated by recent findings showing that butyrate regulates the expression of insulin-like growth factor-binding protein in human mammary and prostate cells (54,55), which, to have any biological relevance, requires a raised level of butyrate in the bloodstream some distance from the gut.

In conclusion, the rye-based diets introduced a significantly higher luminal viscosity in the small intestine than did the wheat diets, resulting in a lower apparent digestibility of protein and fat but without any influence on the digestibility of starch or the plasma concentrations of glucose and insulin. The higher carbohydrate fermentation particularly as AX in the large intestine with the rye diet caused moister feces and enhanced gut production and plasma concentrations of butyrate.

	ACKNOWLEDGMENTS

 
We thank Winnie Østergaard Thomsen and Lene T. Madsen for excellent technical assistance and Lotte Tind Pedersen for checking of grammar and spelling.

	FOOTNOTES

 
¹ Supported by the Nordic Industrial Fund; the Danish Agricultural and Veterinary Research Council; Cerealia, Sweden; Wasabröd, Sweden; Vaasan & Vaasan, Finland; and Fazer Oululainen, Finland.

³ Abbreviations used: AX, arabinoxylans; BW, body weight; DF, dietary fiber; DM, dry matter; LA, lactic acid; NSP, nonstarch polysaccharides; SSD, semisynthetic diet; WBC, water binding capacity.

Manuscript received 26 January 2005. Initial review completed 15 February 2005. Revision accepted 28 March 2005.

	LITERATURE CITED

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 

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