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Effects of meal frequency and high-fibre rye-bread diet on glucose and lipid metabolism and ileal excretion of energy and sterols in ileostomy subjects

Abstract

Objective: To investigate the effect of a rye, high-fibre diet (HFD) vs a wheat, low-fibre diet (LFD), meal frequency, nibbling (Nib, seven times a day) or ordinary (Ord, three times a day), and their combined effects on blood glucose, insulin, lipids, urinary C-peptide and ileal excretion of energy, cholesterol and bile acids in humans.

Design: LFD period with Nib or Ord meal frequency followed by an HFD diet with Nib or Ord meal frequency in randomized, crossover design.

Setting: Outpatients of ileostomy volunteers were called for an investigation in research word.

Subjects: A total of 10 subjects (two female subjects, age 34 and 51 y; eight males, mean age 54.4 y, range 43–65 y) participated in the experiment. All subjects were proctocolectomized for ulcerative colitis (mean 16.0 y, range 8–29 y before the study).

Intervention: In total, 10 ileostomy subjects started with LFD for 2 weeks, the first week on either Nib (five subjects) or Ord (five subjects) and the second week on the other meal frequencies, in a crossover design, followed by a wash-out week, and continued with HFD period for 2 weeks in the same meal frequency manner. All foods consumed in both Nib or Ord regimens were identical and a high-fibre rye bread was used in the HFD period and a low-fibre wheat bread in the LFD period.

Main outcome measures: Day-profiles of blood glucose, insulin and lipids, blood lipids before and after dietary intervention, and excretion of steroids in the effluents and C-peptide in the urine.

Results: During the Nib regimen, plasma glucose and insulin peaks were lower at the end of the day with HFD compared with LFD. Urinary C-peptide excretion was significantly higher in the day-time on LFD compared with HFD (LFD-Ord vs HFD-Ord, P<0.01; LFD-Nib vs HFD-Nib, P<0.01). Plasma free-cholesterol, total cholesterol, triglycerides and phospholipids were significantly higher (P<0.05) after LFD than after HFD with the Nib regimen. A higher excretion of energy (P<0.05) and chenodeoxycholic acid (P<0.05) were observed with HFD compared with LFD regardless of meal frequency. A higher daily excretion of cholic acid, total bile acids, cholesterol, net cholesterol and net sterols (P<0.05) was observed on HFD compared with LFD with the Nib regimen.

Conclusions: An HFD decreased insulin secretion measured as a decreased excretion of C-peptide in urine and as decreased plasma insulin peaks at the end of the day during a Nib regimen. The smoother glycaemic responses at the end of the day during a Nib regimen may be a consequence of a second meal phenomenon, possibly related to the nature of dietary fibre complex.

Sponsorship: This study was supported by grants from the Swedish Council of Forestry and Agricultural Research (SJFR).

Introduction

There is a general international consensus concerning the principles of the dietary public guidelines to promote health. One core recommendation in US as well as in Europe is to build a healthy food base for healthy eating and to promote a daily, high intake of a variety of whole grain products, fruits and vegetables (United States Department of Agriculture and United States Department of Health and Human Service, 2000). A major feature that appears to determine the metabolic effect of grain products and starchy foods is the rate at which these starchy foods are digested (Jenkins et al, 1980b). Carbohydrate food, which is more slowly digested, results in reduced glucose and insulin responses (O'Dea et al, 1981; Jenkins et al, 1982). Slowly digested starchy foods appear to be either lipid neutral or to reduce concentrations of triglycerides and low-density lipoprotein (LDL) cholesterol without significant reductions or even increased concentration of high-density lipoprotein (HDL) cholesterol (Jenkins et al, 1987b, 1987c, 1988; Fontvieille et al, 1988, 1992; Wolever et al, 1992a, 1992b; Miller, 1994). Dietary fibre can also alter postprandial lipid and cholesterol responses (Cara et al, 1992; Anderson et al, 1995; Dubois et al, 1995).

Nutritional factors that may slow the absorption of starch, in particular, include dietary fibre (soluble vs insoluble), nature of starch (eg amylose vs amylopectin and degree of gelatinization), enzyme inhibitors and antinutrients, food form (determined by method of cooking, degree of hydration, or particle size), and altered food frequency (eg nibbling vs ordinary). In medium- to long-term studies (from 2 to 12 weeks), reviewed by Miller (1994) and a study by Fontvieille et al (1992), low glycemic-index diets appear to reduce urinary C-peptide excretion in diabetic subjects and normal volunteers and lower concentrations of fructosamine and/or glycosylated haemoglobin (HbA1C). A corresponding beneficial effect of high-fibre diets (HFDs) has been observed for prevention of diabetes or in non-insulin dependent diabetes mellitus patients (Rivellese et al, 1980; Simpson et al, 1981; Anderson et al, 1987; Salmeron et al, 1997) and animals (Berglund et al, 1982). In fact, until today, an HFD has been associated with a decreased risk of diabetes in seven prospective studies (Liu, 2003).

Studies by Ellis in 1934 (Ellis, 1934) suggested that insulin requirements in diabetes could be reduced considerably by increasing meal frequency. Studies 30 y later showed that normal and diabetic volunteers when shifting an ordinary (Ord) regimen of three meals to a daily isocaloric nibbling (Nib) diet of 10 meals, improved their glucose tolerance (Gwinup et al, 1963).

The earliest studies on effects of food frequency on lipid metabolism, performed on hyperlipidaemic and normal volunteers, indicated that increased meal frequency reduced total cholesterol (Cohn, 1964; Jagannathan et al, 1964; Fabry & Tepperman, 1970). A detailed 2-week study showed that if a person nibbles food 17 times a day compared with Ord the same amount of diet compiled into three meals, there was a reduction of total cholesterol, LDL cholesterol and apoprotein B (Jenkins et al, 1989). Another study using liquid-formula diets indicated that decreases in integrated insulin area, serum free fatty acids and serum cholesterol can be seen during the course of a single day with increased food frequency (continuous feeding compared with three equal meals, Wolever, 1990). The literature thus indicates that there are some similarities in the improved carbohydrate and lipid metabolisms associated with either increased food frequency, low glycemic-index diets or high dietary fibre intake. Whether the improved metabolic responses share the same mechanism(s) is not fully understood.

The aim of this study was to investigate the effect of a rye bran bread-based high-fibre diet, variation in meal frequency (Nib or Ord) and their combined effects on the responses of blood glucose, insulin and lipids, urinary C-peptide and ileal excretion of energy, cholesterol and bile acids in ileostomy subjects.

Subjects and methods

Subjects

A total of 10 subjects (two female subjects, aged 34 and 51 y; eight males, mean age 54.4 y, range 43–65 y) volunteered to participate in the experiment. All subjects were proctocolectomized for ulcerative colitis (mean 16.0 y, range 8–29 y before the study). The subjects were living in a general normal life based on physical examination and blood tests before the experiment. Their body weight at the beginning of the study ranged from 64 to 113 (mean 82.2) kg. During the study, the mean body weight varied between 82.0 and 82.3 kg. No differences in weight were seen between the periods. The body mass index (BMI) ranged between 20.7 and 35.6 (mean 28.4) kg/m2, fasting blood insulin 3.0–22.0 (mean 10.8 mU/l) and fasting blood glucose 4.8–8.6 (mean 5.6 mmol/l) at the entrée of the experiment. The study was approved by the Ethical Committee of the Umeå University Hospital.

Study design and diets

The subjects were studied for a total of five consecutive weeks on an outpatient basis. They were randomly assigned into two experimental groups, five subjects in each group. Both of the experimental groups began with a low-fibre diet (LFD) for 2 weeks in which one experimental group started with Nib (seven times a day) regimen for the first week and continued with an Ord (three times a day) regimen for the second week. The other experimental group started with Ord and continued with Nib regimen for a week in a crossover manner. After 1 week of ‘wash-out’ period and eating their own ordinary diet, both experimental groups followed an HFD for 2 weeks in which the experimental groups started and continued with the dietary regimen in the same way as in the LFD period.

The same menu, except for the bread, was used for all the dietary periods (Table 1). When on the LFD, they were given wheat-flour soft bread plus wheat crisp-bread. When on the HFD, the subjects were given experimental rye-bran soft bread combined with a whole-grain rye crisp-bread. Wheat and rye crisp-breads and rye bran were kindly provided by Wasabröd AB (Filipstad, Sweden).

Table 1 Menu of the wheat-flour, bread-based, LFD and the rye-bran, bread-based, HFD

When on both HFD and LFD with Nib regimen, the subjects ate seven identical meals per day (one seventh of the daily diet per meal). During the Ord regimen, the subjects ate three meals a day (one-seventh of the daily diet for breakfast, two-sevenths for lunch and four-sevenths for dinner). The Ord regimen corresponded to a meal pattern that can be seen rather commonly in the population. The daily dietary intake of energy and nutrients during Nib and Ord regime in the same dietary period was the same.

To keep the body weight constant three levels of daily energy intake (8500, 10 600 and 12 700 kJ for both LFD and HFD) were arranged for the subjects according to the recommendations of FAO/WHO/UNU (1985), and a ‘3-day’ dietary record was done prior to the experiment. These energy levels corresponded to 1.0, 1.25 or 1.5 portions of the daily diet. The nutrients, fibre and energy content of the diets, were calculated according to the Swedish Food Tables (Swedish National Food Administration, 1986) with a professional calculating program ‘MATs den flexible 3.0’ (1993), except for the contents of protein, fat and dietary fibre in rye bran and wheat flour where the analysed values were used. The nutrients, fibre and energy content of the diets are listed in Table 2. The energy content (excluding dietary fibre) was the same in all diets on a given energy level.

Table 2 Energy and nutritional content in the wheat-flour, bread-based, LFD and the rye-bran, bread-based, HFD

On day 1 and 2 of each experimental dietary period, the subjects were instructed by a dietitian to eat the pre-delivered experimental diet and to follow a defined dietary regimen at home. Days 3–5 in each experimental dietary period were chosen as the ‘sampling days’. On those days, the subjects were admitted to the research ward and stayed in a nearby hotel overnight. Identical diet ingestion and meal frequency was followed each day in each 5-day experimental dietary period. On days 6 and 7 the subjects were at home with free food intake.

Collection of ileostomy effluents and food samples

Ileostomy effluents were collected on the sampling days in each experimental dietary period. The ileostomy bags were changed every 2 h from 0700 to 2100 hours during each sampling day and at 0700 hours on the next day. The bags were immediately frozen on dry ice and then stored at −30°C. The ileostomy effluents from each 24-h period were then freeze-dried to constant weight, mixed, homogenized and stored at −70°C until analysis. Duplicate food samples from the sampling days in each dietary period were mixed, freeze-dried and processed in the same way as the ileostomy effluents.

Collection of blood and urine samples

Venous blood samples were taken using venous retention needles on the first sampling day in each experimental dietary period from 0800 to 2200 (totally 15 times) hourly during the sampling days under Nib regimen and 1000–1200, 1400–1600, 1800–2000 and 2200 hours (totally 10 times) during the sampling days with Ord regime. Over-night fast venous blood samples were collected in the morning 1 or 2 days before the experiment, on the sixth day of each experimental dietary period and at the end of the ‘wash-out’ week. Daytime (0700–2200) and night-time (2200–0700 next morning) urine was collected and weighed. Urine samples of day- and night-time were stored at −30°C until analysis.

Laboratory assays

Nitrogen was analysed with a modified micro-Kjeldahl technique after pre-digestion with sulphuric acid in a Tecator system with spectrophotometric determination as described by Tetlow and Wilson (1964). Fat was determined according to van de Kamer et al (1949). Dietary fibre content in rye bran, wheat and rye crisp bread was analysed by the method described by Asp et al (1983).

Serum cholesterol, free cholesterol, triglycerides and phospholipids were measured with the methods described by Mekki et al (1997). Plasma glucose concentrations were measured with an automatic analyser (Hitachi 911, 717, Japan) using an enzymatic method (GLUCO-quantRGlukos, kit nr 1447521, Boehringer Mannheim, Mannheim, Germany). Plasma insulin concentrations were analysed with a commercially available double-antibody radioimmunoassay (RIA) kit (Phadeseph Insulin RIA; Kabi Pharmacia Diagnostics AB, Uppsala, Sweden). Urinary C-peptide concentrations were analysed by RIA as well, with a commercial kit (C-peptide 125I RIA Kit, INCSTAR Corporation, Stillwater, MN, USA). Cholesterol in diet and cholesterol and bile acids in ileostomy effluents were analysed by a gas–liquid chromatography (GLC) method described by Bosaeus et al (1986). The energy content in ileostomy effluents was determined by Bomb calorimetry (Gallenkap Autobomb, Loughborough, Leicestershire, England) as described earlier (Woolf et al, 1983; Andersson et al, 1984).

Calculations and statistics

Data are presented as mean ± s.e.m. unless otherwise specified. Data from different experimental dietary periods (free cholesterol, cholesterol, triglycerides, C-peptide, insulin and glucose) were subject to Wilcoxon matched-pairs ranks test. The effects of dietary treatment on repeated concentrations of blood lipids, glucose and insulin (Nib or Ord) were also assessed by one-factor ANOVA adjusted with a Bonferroni test for multiple comparisons. A trend analysis was performed by using linear regression on peak concentrations of insulin and glucose. Statistics were performed with the SPSS program for Windows (release 9.0.1 SPSS Inc., 1999) and the SAS system for Windows (release 8.02 TS level 02M0, SAS Institute Inc., 2001).

Results

Day-profile of plasma insulin and glucose, and the daily excretion of urinary C-peptide

The day-profiles of plasma insulin are shown in Figures 1 and 2. A combined effect of diet and time was observed with decreasing peak insulin concentrations during the day on the HFD-Nib regime (R2=0.61; β=−1.6; P<0.05). The plasma insulin peaks were significantly lower at the end of the day of the HFD-Nib period compared with the LFD-Nib period only when the nonparametric test was used (Figure 1, P<0.05). During the corresponding LFD-Nib regimen, no significant linear trend was observed (β=0.45). No difference in mean insulin level was observed when the HFD (HFD-Nib, 45.2±5.5 mU/l; HFD-Ord, 67.3±9.5) was compared with the LFD with the same regimen (LFD-Nib, 49.2±7.4; LFD-Ord, 70.9±11.4) respectively. During the Ord regimen, no significant trends were observed and no differences were seen between the groups.

Figure 1
figure1

Daily profile of plasma insulin during the wheat-bread-based LFD and the rye-bread-based HFD with the Nib regimen in subjects with ileostomies: n=10 (*P<0.05 compared with corresponding time during the day based on the Wilcoxon matched-pairs rank test).

Figure 2
figure2

Daily profile of plasma insulin during the wheat-bread-based LFD and the rye-bread-based HFD with the Ord regimen in subjects with ileostomies: n=10. There were no significant differences between diets.

The day-profiles of plasma glucose are shown in Figure 3 and 4. The mean blood glucose concentration was lower on the HFD, both with Nib (5.7±0.4 mmol/l) and Ord (5.9±0.7) regime compared with the corresponding LFD, Nib (6.1±0.4, P<0.01) and Ord (6.5±0.7, P<0.05). During the Nib regimen, the plasma glucose peaks were like the insulin peaks lower at the end of the day of the HFD period compared with the LFD period (Figure 3, P<0.05) but no significant trends were observed in the peak concentrations.

Figure 3
figure3

Daily profile of plasma glucose during the wheat-bread-based LFD and the rye-bread-based HFD with the Nib regimen in subjects with ileostomies: n=10. (*P<0.05 compared with corresponding time during the day based on the Wilcoxon matched-pairs rank test).

Figure 4
figure4

Daily profile of plasma glucose during the wheat-bread-based LFD and the rye-bread-based HFD with the Ord regimen in subjects with ileostomies: n=10. There were no significant differences between diets.

The daily excretion of C-peptide (Figure 5) was significantly higher when the subjects were on the LFD than on the HFD both with the Ord (25.3±4.0 vs 13.7±3.2 nmol/day, P<0.01) and the Nib (28.6±3.8 vs 13.4±3.2, P<0.01) regimens. The excretion of C-peptide was significantly higher only in the day-time, LFD-Ord vs HFD-Ord (17.1±3.0 vs 7.3±2.3, P<0.01), LFD-Nib vs HFD-Nib (23.7±3.6 vs 9.7±2.5, P<0.01). The urinary daytime C-peptide excretion was higher with the Nib regimen compared with the Ord regime during both LFD and HFD periods, LFD-Nib vs LFD-Ord (23.7±3.6 vs 17.1±3.0, P<0.01), HFD-Nib vs HFD-Ord (9.7±2.5 vs 7.3±2.3, P<0.05). When the night-time urinary C-peptide excretion was included no significant differences were observed.

Figure 5
figure5

Daily excretion of urinary C-peptide during the wheat-bread-based LFD and the rye-bread-based HFD with the Nib or the Ord regimen in subjects with ileostomies (n=10). The downward lines in the bars are standard errors of mean at the daytime and the upward lines on the bars are standard errors of mean at the night-time. The daily excretion, the LFD-Ord vs HFD-Ord (P<0.01) and the LFD-Nib vs HFD-Nib (P<0.01). In the daytime, the LFD-Ord vs HFD-Ord, P<0.01; LFD-Nib vs HFD-Nib, P<0.01 and the LFD-Nib vs LFD-Ord, P<0.01; HFD-Nib vs HFD-Ord, P<0.05), based on the Wilcoxon matched-pairs rank test.

Day-profile of blood lipids

During the Nib regimen, the triglycerides reached a peak concentration after 5–7 h (Figure 6), while during the Ord regimen, the peak concentration was higher and it was reached in the evening (Figure 7).

Figure 6
figure6

Daily profile of plasma triglycerides during the wheat-bread-based LFD and the rye-bread-based HFD with the Nib regimen in subjects with ileostomies: n=10. There were no significant differences between diets.

Figure 7
figure7

Daily profile of plasma triglycerides during the wheat-bread-based LFD and the rye-bread-based HFD with the Ord regimen in subjects with ileostomies: n=10. There were no significant differences between diets.

No significant differences in the average total cholesterol, free cholesterol, triglycerides and phospholipids were observed between the LFD and HFD periods with the Ord or Nib regimen. During the Ord regimen (HFD and LFD), the concentration of free cholesterol and phospholipids increased during the day reaching a peak concentration in the evening, while a comparatively stable concentration was observed during the day after both Nib regimens (data not shown).

Fasting blood lipids and excretion of energy and sterols

The fasting plasma free-cholesterol, total cholesterol, triglycerides and phospholipids were significantly higher when the subjects were on the LFD than on the HFD with the Nib regimen (Table 3).

Table 3 Fasting blood lipids during the wheat-bread-based LFD and the rye-bread-based HFD with the Nib or the Ord regimen in 10 subjects with ileostomies

We observed that the fasting blood triglycerides in four out of 10 ileostomy subjects were above normal value (according to the European Atherosclerosis Society, <2.3 mmol/l, regardless of age and sex). Between the subjects with high and normal blood triglycerides, fasting blood total cholesterol, free cholesterol and phospholipids tended (not significant) to be higher in subjects with high blood triglycerides.

A higher excretion of energy was observed with the HFD compared with the LFD regardless of food intake frequency. No significant difference was observed between the Nib and Ord regimens (Table 4) with LFD or HFD.

Table 4 Energy and sterol excretion in ileostomy effluents during the wheat-bread-based LFD and the rye-bread-based HFD with the Nib or the Ord regimen in 10 subjects with ileostomies

A higher daily excretion of chenodeoxycholic acid in the ileostomy effluents was observed in the HFD as compared with the LFD with both the Nib and Ord regimens. A higher daily excretion of cholic acid, total bile acids, cholesterol, net cholesterol and net sterol in the ileostomy effluents were observed in the HFD as compared with the LFD with the Nib regimen.

Discussion

The ileostomy model has been used for many years to study the absorption of nutrients, (Sandberg et al, 1981; Langkilde et al, 1990; Schweizer et al, 1990), digestibility of the food stuffs (Englyst & Cummings, 1985; Jenkins et al, 1987a; Aman et al, 1995), and colonic fermentation (McBurney et al, 1988; Cummings & Englyst, 1991). The model was also used to study short-term dietary effects on sterol excretion, blood lipids (Tornqvist et al, 1986; Bosaeus & Andersson, 1987; Andersson, 1992; Zhang et al, 1992, 1994). It was reported that the ileostomists had a significantly higher postprandial plasma insulin concentration indicating that colectomy may affect the enteroinsular axis, leading to hyperinsulinaemia and an impaired glucose tolerance (Palnaes-Hansen et al, 1997), and that loss of the colon may be associated with several characteristics of the insulin resistance syndrome (Robertson et al, 2000). We found that five in 10 ileostomists in this experiment had high fasting and postprandial plasma insulin concentration.

We planned this study with a food intake frequency of seven times daily. According to previous studies, this frequency may be too low to detect changes in blood cholesterol concentration. However, we wanted to test a frequency that is realistic for the daily living of humans and to see if the excretion of bile acids and cholesterol was affected by the differences in food frequency. This was the major reason for using ileostomists. Two diets were used with respect to the content of the dietary fibre complex (with and without rye bran) since various fibre sources also are known to have different metabolic effects (Rivellese et al, 1980; Simpson et al, 1981; Berglund et al, 1982; Anderson et al, 1987; Salmeron et al, 1997).

For ethical reasons, only 10 times of blood sampling were collected for the day-profile of plasma insulin (and also glucose) in Ord regimen and 15 times in Nib region, causing some difficulties to compare the areas beneath the curves between Ord and Nib in the same type of diet. Plasma insulin was presented in concentration and urinary C-peptide was presented in the amount of daily excretion, representing the daily amount of insulin secretion. Although we could not see the difference in mean insulin levels between the LFD and HFD in the same dietary frequency regimens (HFD-Nib 45.2±5.4 mU/l vs LFDNib 49.2±7.4; HFD-Ord 67.3±9.5 vs LFD-Ord 70.9±11.4) the day-profile curve of insulin concentration in the HFD was gradually lower and the differences became significant compared to the LFD at the end of the day. This observation may explain why the daytime excretion of C-peptide was lower when the subjects were on the HFD than on the LFD.

The closeness of one meal to the next determines the glycemic response to the second meal: the closer the meals are, the smoother the glycaemic responses (the Staub effect, Gwinup et al, 1963). The second-meal phenomenon has also been observed with viscous fibre. Guar in one meal improved carbohydrate tolerance and reduced the insulin response to the second meal, presumably by spreading the nutrient load from the first meal (Jenkins et al, 1980a). We did not analyse the glycaemic index of our diets since that would have expanded the study too much. However, the glycaemic index (Jenkins et al, 1981) can be estimated by the peaks of glucose response. No differences were found between the two diets during the first part of the day, but a difference was found in the end of the day during the Nib regimen. The lower glucose and insulin peaks observed at the end of the day of the HFD compared to the LFD of the nibbling period may be a consequence of a second-meal phenomenon, possibly related to the nature of dietary fibre complex (Jenkins et al, 1981).

Although there continues to be uncertainty about the mechanisms, a population study from 1992 has demonstrated lower serum cholesterol and LDL-cholesterol concentrations in individuals who consume more-frequent meals (≥4 meals vs 1–2 meals per day, Edelstein et al, 1992). The slightly decreased concentration of blood cholesterol during the Nib HFD compared to the LFD may be related to the reduction in insulin secretion and postprandial nutrients after nibbling. 3-Hydroxy-beta-methylglutaryl coenzyme A (HMGCoA) reductase, a rate-limiting enzyme in cholesterol synthesis, is stimulated in amount and activity by circulating insulin (Lakshmanan et al, 1973). Reduction in insulin concentrations at the end of the day as seen in the present study during the Nib HFD compared to the LFD regimen, may result in a reduction of HMGCoA reductase activity and a decrease in the rate of hepatic cholesterol synthesis over the day (Lakshmanan et al, 1973). It has also been reported that Nib may reduce total cholesterol in blood by a decreased hepatic cholesterol synthesis (Jones et al, 1993). Dietary-fibre-rich sources such as oat bran may significantly increase faecal bile salts and cholesterol and lower blood cholesterol in ileostomists (Zhang et al, 1992). In a previous experiment in ileostomists using a rye bran-supplemented diet, no significant effect was observed on plasma total cholesterol even during a 3-week period (Zhang et al, 1994), although the excretion of conjugated bile acids was increased. In the present experiment, the combined effect of an increased faecal excretion of bile acids and cholesterol and the decreased plasma insulin and C-peptide excretion observed during the dietary HFD- Nib pattern, had together a sufficient impact to lower total plasma cholesterol concentration slightly but significantly. This marginal effect on plasma cholesterol is seen after less than 1 week of dietary intervention, which in principle corresponds to what has been previously observed during a 1-week Nib period (Jenkins et al, 1989). During the Ord period, the effects of the HFD was less pronounced, and consequently no effect was observed on the plasma cholesterol concentration.

The overall lower daily insulin concentrations, C-peptide excretion and fasting blood lipids seen during the HFDs (specially Nib regimens) compared with the LFD are all mechanisms that may be associated with the low incidence of myocardial infarction (MI) associated with an increased fibre intake (particularly cereal fibre) seen in a number of prospective, epidemiological studies (Kromhout et al, 1982; Kushi et al, 1985; Khaw & Barrett-Connor, 1987; Pietinen et al, 1996; Rimm et al, 1996; Jacobs et al, 1998; Liu et al, 1999; Wolk et al, 1999). The effect on blood lipids is modest and may be not the important factor related to a decreased risk of MI (Pietinen et al, 1996; Brown et al, 1999). The effect on glucose and insulin metabolism of whole-grain–HFDs as seen in the present and other experimental studies in humans and in animals (Berglund et al, 1982) may be a more important factor and more likely to have an impact on the risk of MI as well as diabetes.

A clear association between a high intake of cereal grain and a reduced risk of diabetes has indeed been observed in seven prospective studies (Liu, 2003). Furthermore, it has since long been known that a high intake of wheat bran (Brodribb & Humphreys, 1976; Beck & Villaume, 1987) or a mixture of wheat bran and rye bran (Sandman et al, 1983) is associated with an improved glucose tolerance in humans without diabetes. In two recent reports Juntunen et al (2002) has studied the impact of rye bran on insulin metabolism. In the first report, a lower insulinaemic response was observed after consumption of whole-grain rye bread compared with endosperm wheat bread in healthy subjects. In the second report using the frequently sampled intravenous glucose tolerance design, high-fibre rye bran bread did not alter insulin sensitivity, but it appeared to enhance insulin secretion in postmenopausal, hypercholesterolaemic women (Juntunen et al, 2003). However, in a third experimental study using the insulin clamp technique, an increased intake of whole grain caused an increased insulin sensitivity (Pereira et al, 2002). Thus, epidemiological as well as experimental evidence suggest that increased intake of fibre rich food is related to improved insulin metabolism and a decreased risk of diabetes (Liu, 2003), MI (Kromhout et al, 1982; Kushi et al, 1985; Khaw & Barrett-Connor, 1987; Pietinen et al, 1996; Rimm et al, 1996; Jacobs et al, 1998; Liu et al, 1999; Wolk et al, 1999) and stroke (Liu et al, 2000; Mozaffarian et al, 2003).

We suggest that a high intake of an HFD also influences insulin metabolism in a completely different manner. Within the whole-grain fibre complex, there are enzyme inhibitors that might inhibit the uptake of nutrients from the gut and in such a way influence insulin metabolism. In fact, we have already observed an increased excretion of energy from fat and protein (nitrogen) in ileostomy effluents when consuming HFDs containing brewer spent grain, rye bran and oat bran (Zhang et al, 1991, 1992, 1994). This hypothesis will be addressed in a follow-up experiment using the Ord and Nib diets where results will be given on the excretion of nutrients from the ileostomy effluent. In this paper also, the impact of fibre fermentation will be evaluated and discussed. Obviously, the impact of colonic fibre fermentation cannot be evaluated in a study using the ileostomy model.

In conclusion, the main finding of this study is that an HFD decreased insulin secretion measured as a decreased excretion of C-peptide in urine and as decreased plasma insulin peaks at the end of the day during a Nib regimen. The smoother glycaemic responses at the end of the day during a Nib regimen may be a consequence of a second-meal phenomenon, possibly related to the nature of dietary fibre complex.

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Acknowledgements

We are grateful for valuable advice and assistance with Bomb calorimetry measurements by Henrik Andersson, for the dietary assistance of Jeanette Molin, for the technical assistance of Sandra Dore, Margaretha Holmgren, Nadia Mekki, Inger Sjöström, Rolf Sjöström, Margaretha Tagewall, Åsa Ågren, Ann-Marie Åhrén and for advice on statistics by Roger Andersson and Mats Nilsson. This study was supported by grants from the Swedish Council of Forestry and Agricultural Research (SJFR).

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Guarantor: Jie-Xian Zhang.

Contributors: EAL and JXZ were responsible for the study design, conducting the dietary intervention, completing the statistical analysis and writing the paper. PT was responsible for the study design and conducting the dietary intervention of the study. DL was involved in the advisory of writing the paper and the analysis of the blood lipids. PÅ was involved in the concept and planning, and the analysis of the nutrients in the diets. HA was involved in the planning and the analysis of steroids in the ileostomy effluents. GH was involved in obtaining funding, the concept and planning, designing and the overall supervision of the study.

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Correspondence to J X Zhang.

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Lundin, E., Zhang, J., Lairon, D. et al. Effects of meal frequency and high-fibre rye-bread diet on glucose and lipid metabolism and ileal excretion of energy and sterols in ileostomy subjects. Eur J Clin Nutr 58, 1410–1419 (2004). https://doi.org/10.1038/sj.ejcn.1601985

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Keywords

  • meal frequency
  • high-fibre rye-bread
  • diet
  • lipids
  • glucose
  • insulin
  • human ileostomists

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