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Department of Clinical Nutrition, University of Kuopio, FIN-70211 Kuopio, Finland and * VTT Biotechnology and Food Research, FIN-02044 VTT, Finland
3To whom correspondence should be addressed.
 |
ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: • rye bread • wheat bread • cholesterol • plasma glucose • insulin • humans
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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, Knekt et al. 1994
, Morris et al. 1977
, Pietinen et al. 1996
, Rimm et al. 1996
). Of the different
sources of fiber (vegetable, fruit, cereal), cereal fiber has been
shown to have the strongest association with a reduced risk of CHD
(Morris et al. 1977
, Pietinen et al. 1996
, Rimm et al. 1996
); of the different types
of fiber, soluble fiber has been shown to be more beneficial in this
respect than insoluble fiber (Pietinen et al. 1996
). The
protective, cholesterol-lowering effect of fiber is thought to be
mediated through the ability of water-soluble, viscose fiber to
bind bile acids in the small intestine, and the bile acids are then
excreted in the feces (Gallaher and Hassel 1995
,
Kay and Truswell 1977
, Vahouny et al. 1980
). This enhances synthesis of bile acids from cholesterol
in the liver. On the other hand, short-chain fatty acids produced
in the fermentation of fiber in the large bowel may reduce serum
cholesterol through the inhibition of cholesterol synthesis in the
liver (Berggren et al. 1996
, Hara et al. 1999
, Lin et al. 1995
). However, these
last-mentioned studies were conducted in vitro or in animals, and
their results are controversial.
Solutions of viscose fiber may also retard absorption of nutrients
(Jenkins et al. 1978
, Leeds et al. 1975
);
as a result of the reduced rate of carbohydrate absorption, the insulin
response may be diminished. Because insulin has been shown to stimulate
cholesterol synthesis, lowered insulin secretion may affect plasma
cholesterol concentrations (Judd and Truswell 1985
).
Reduced concentration of plasma insulin offers further protection
against CHD (Despres et al. 1996
).
With respect to hypocholesterolemic effects, the most studied cereal is
probably oats (Glore et al. 1994
, Kahlon and Chow 1997
, Kritchevsky 1997
, Ripsin et al. 1992
). There is a consensus that the ß-glucans of oats
produce a modest reduction in blood cholesterol concentration in
normocholesterolemic and a greater reduction in hypercholesterolemic
subjects (Ripsin et al. 1992
). Barley, with its soluble
ß-glucans, and rice, with its unsaponifiable matter and oil, have
also been shown to have lipid-lowering properties (Kahlon and Chow 1997
). Because wheat fiber does not affect blood
cholesterol (Kritchevsky 1997
), it is often used as a
control in experimental studies (Glore et al. 1994
).
Rye is a commonly used cereal in northern and eastern Europe. The
dietary fiber content of rye is 16.1 g/100 g; the major fiber
components are arabinoxylan (60%), cellulose (15%) and ß-glucan
(9%) (Nilsson et al. 1997
). Rye is consumed mainly as
whole meal bread with a dietary fiber content of ~10% (Rastas et al. 1993
). To date, the effects of rye on blood lipids have
been studied only in experimental animals (Lund et al. 1993
, Zhang et al. 1992
and 1994b
) and in
ileostomy patients (Zhang et al. 1994a
). In animal
studies, rye bran has either decreased (Zhang et al. 1994b
) or has shown no effect on serum cholesterol
(Zhang et al. 1992
); rye bread has decreased plasma
cholesterol only in rats fed a high cholesterol diet (Lund et al. 1993
). In ileostomy patients, rye bran did not affect
total, HDL or LDL cholesterol concentrations (Zhang et al. 1994a
), indicating that large bowel events may influence serum
lipid concentrations. This study was conducted to investigate whether
rye bread as part of the usual diet can reduce serum lipids, and
whether it modifies glucose and insulin metabolism in healthy
free-living men and women with slightly elevated serum cholesterol.
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SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The subjects were 43 healthy adults (19 men and 24 women) recruited
from the population of healthy adults in the Helsinki area, southern
Finland (11 men and 13 women), and the Kuopio area, eastern Finland (8
men and 11 women). One man in Helsinki and one woman in Kuopio
discontinued the study due to poor compliance during the baseline
period and one woman in Kuopio due to hospitalization at the beginning
of the study. The final number of subjects was 40 (18 men and 22
women). The inclusion criteria for the study were a serum total
cholesterol concentration of 5.5–7.5 mmol/L, serum total
triacylglycerol concentration <2.5 mmol/L and body mass index within
the range 20–32 kg/m2. Subjects consuming
lipid-lowering medication were excluded. Basic characteristics of
the subjects are shown in Table 1
.
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The study was a crossover trial. The first bread period was preceded by a 2-wk baseline period. At the beginning of the baseline period, the subjects were advised to maintain their body weight and lifestyle habits (exercise, alcohol consumption, smoking) unchanged throughout the study. They also received instructions not to use cholesterol-lowering foodstuffs (e.g., Benecol®, plant stanol ester margarine, Raisio Group, Raisio, Finland) or foodstuffs that affect bowel function (plums and plum juice, dried fruit, brans and muesli, various seeds and licorice). During the baseline period, every subject kept a 4-d food record to determine individual energy intake.
After the baseline period, the subjects were randomly assigned to begin either a 4-wk rye bread or a 4-wk wheat bread period. Between the bread periods, there was a 4-wk washout period during which the subjects ate their usual diet. Serum total cholesterol, HDL cholesterol, LDL cholesterol and total triacylglycerol concentrations were measured on two consecutive days at the beginning and end of both bread periods. The aim of the duplicate measurements was to reduce individual variation in serum lipid concentrations. Single blood samples for plasma glucose and insulin analyses were collected at the same time points as the lipid collections. Subjects were weighed every 2 wk, and exercise was recorded daily during the bread periods.
Because menstruation may cause changes in plasma lipoproteins
(Cullinane et al. 1995
, Lyons Wall et al. 1994
), the duration of menstrual cycle was checked among the
premenopausal women at the beginning of the baseline period, and
adjustments were made to begin the first bread period between d 5 and
10 after the beginning of menstrual flow. To be able to finish the
study before Christmas, one premenopausal woman started the study
without the baseline period. This had no influence on the results
because there were no study treatments or measurements during the
baseline period. The lengths of the test bread periods and the washout
period between the bread periods in premenopausal women were adjusted
to the cycle length, and all blood samples were collected at the same
phase of the menstrual cycle. Because of the changes in the length of
the cycle, the rye bread period lasted only 3 wk for one woman; another
woman had a 5-wk rye bread period and a 6-wk wheat bread period.
The study was approved by the Ethics Committee of Kuopio University Hospital and each subject gave written consent for the study.
Diet.
The aim of the diet was that the test breads comprise a minimum of 20% of the daily energy intake; the goal for the difference in the intake of fiber from the test breads between the rye and wheat bread periods was 15 g/d. The only change in the diet was to replace the customarily used breads and baked products with rye breads during the rye bread period and with wheat breads during the wheat bread period. In addition to the test breads, the subjects could eat a piece of sweet pastry or a portion of porridge once a day, but this was not obligatory. These products were recommended to be rye-based products during the rye bread period and wheat-based products during the wheat bread period. Pasta and rice could be eaten as part of warm dishes in the amounts usually eaten by the subject. Otherwise, the diet was to be unchanged. The subjects were especially advised not to change the amount and type of fat and cold cuts eaten with the breads or their consumption of fiber-containing foods such as vegetables, fruit and berries.
The rye and wheat breads were obtained from two bakeries (Fazer Bakeries Ltd., Lahti, Finland and Vaasan & Vaasan Ltd., Helsinki, Finland); freshly baked, commercially used breads were available once a week from the study center. To increase variability in bread consumption, the subjects were offered four different rye breads during the rye bread period and six different white wheat breads during the wheat bread period. One of the rye breads was a dried product, i.e., crispbread; the other three breads were fresh products. The main ingredient in all rye breads was finely milled whole meal rye flour; in addition, the fresh breads contained small amounts of wheat flour to improve the structure of the bread with gluten. One fresh rye bread also contained rye grains, groats and extract of rye malt; another rye bread contained rye groats and rye malt as well as some potato flakes. The third fresh rye bread was baked longer and at a lower temperature than the other rye breads. All six wheat breads were produced from refined wheat flour.
To guarantee that the subjects ate the correct amount of test breads, they were given detailed instructions how to slice loaves (in the case of unsliced breads) and how to combine the daily portions of different products. It was easier for the subjects to estimate amount of test breads to be consumed as slices than as grams because this did not require the use of kitchen scales in estimating the amount of bread to be consumed. The test bread portions for rye breads were 27.5–40.5 g and for wheat breads, 22.5–25.0 g. One portion of rye bread contained, on average, 348 kJ energy (range 268–407 kJ) and 3.5 g fiber (range 2.4–4.2 g); the respective values for the portion of wheat bread were 278 kJ (range 258–294 kJ) and 0.6 g (range 0.5–0.6 g). Because the energy content of the bread portions varied, especially in rye breads, the subjects were advised to eat each product daily. A minimum of 4–5 portions of the test breads had to be eaten each day, and the number of portions to be eaten varied according to the daily energy intake of the individual. There was no maximum for the amount of bread to be consumed, but the subjects were advised to eat the bread in amounts that matched their normal cereal intake.
Compliance with the diet was checked by daily records and by 4-d food records. In daily records, the subjects recorded the number of portions of each rye or wheat bread consumed as well as possible consumption of other cereals, e.g., slices or pieces of pastry, or servings of porridge. In addition, bowel function and possible side effects were recorded daily. Four-day food records including one weekend day were kept by the subjects during the last 2 wk of both bread periods.
The clinical nutritionist (in Kuopio) or nurses guided by the clinical
nutritionist (in Helsinki) advised subjects on the practical management
of the diet. All 4-d food records were analyzed by the clinical
nutritionist using the Micro-Nutrica® calculation
program for nutrients (Version 2.0, Finnish Social Insurance Institute,
Turku, Finland), which included the database of Finnish foods
(Rastas et al. 1993
). The nutrient composition of the
rye and wheat breads used in the study was analyzed at VTT
Biotechnology and Food Research (Espoo, Finland) and added to the
database.
Laboratory measurements.
All samples of venous blood were collected in the morning after the subjects had fasted overnight (12 h). After the blood collection, serum samples were clotted for 30 min at room temperature and the serum was separated by centrifugation for 15 min at 2100 x g at room temperature. The plasma samples were collected in prechilled EDTA tubes and centrifugated within 30 min from the blood collection in the same manner as the serum samples; plasma was then separated. All samples were stored at -20°C until analyzed. Subjects were also weighed in the morning (light clothing, no shoes) on a digital scale.
All blood samples were analyzed at the Clinical Research Unit of the
University of Kuopio. Total cholesterol and triacylglycerols were
analyzed from the whole serum. HDL cholesterol was separated from LDL
and VLDL cholesterol by precipitation of LDL and VLDL with dextran
sulfate and magnesium chloride (Penttilä et al. 1981
). Determination of total cholesterol, triacylglycerols and
HDL cholesterol was made by enzymatic colorimetric methods with
commercial kits (Monotest Cholesterol and Peridochrom Triglyceride
GPO-PAP, Boehringer Mannheim GmbH Diagnostica, Mannheim, Germany)
using the Kone Specific Clinical Analyser (Kone, Espoo, Finland). LDL
cholesterol was calculated using the Friedewald equation modified for
molar concentrations: LDL cholesterol = total cholesterol - HDL cholesterol - 0.45 x total triacylglycerols
(Friedewald et al. 1972
).
Plasma glucose was analyzed by the enzymatic photometric method (Granutest 100, Merck, Damstadt, Germany) using Kone Specific Clinical Analyser (Kone) and plasma insulin by the RIA method (Phadaseph Insulin RIA 100, Pharmacia Diagnostica, Uppsala, Sweden).
Statistical analysis.
Normal distribution, homogeneity of variance and freedom from carryover
effect were tested before further analyses. Nonnormal variations were
log transformed (total and HDL cholesterol, total triacylglycerols,
glucose and insulin). Changes in serum lipids, plasma glucose and
insulin, and body weight during the study were tested by MANOVA,
followed by the two-tailed t test for paired data. To
control the overall 
-level, Bonferroni adjustment was used.
Differences in the absolute and proportional changes in serum lipid
concentrations among the tertiles of rye bread consumption during the
rye bread period were analyzed by the nonparametric Kruskal-Wallis
test. The comparisons in nutrient intakes between rye and wheat bread
periods were made by the Wilcoxon rank-sum test for dependent data.
Differences in the intake of fiber and fiber-containing foodstuffs
between men and women during the rye bread period were tested by the
Mann-Whitney U-test. In all analyses, P-values <0.05
were considered to be significant. The results are expressed as means
± SEM. Data were analyzed with SPSS for Windows 6.0.1
statistics program (SPSS, Chicago, IL) (Norusis 1993
).
To estimate the perceivable differences in the variables studied,
post-hoc power was calculated with the present number of subjects,
on the basis of the assumption that the power of the study is 0.80, and
using probability for type I error = 0.05. These assumptions
and the expected difference of 0.4–0.5 mmol/L in serum total
cholesterol concentration were used to estimate the sample size in the
design phase of the study.
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RESULTS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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) and the reported frequency of exercise did not differ significantly
between the bread periods either in men or in women. Bowel function and
other related variables during the rye and wheat bread periods will be
reported elsewhere.
|
Compliance with the diet was good. The subjects ate more than the
minimum recommended number of bread portions during both the rye and
wheat bread periods (Table 3). All four different rye breads offered were eaten daily during the rye
bread period, and six different wheat breads were consumed daily or
almost daily during the wheat bread period. Intake of other cereals was
less than one portion per day (Table 3)
.
|
. In
addition, the alcohol intake in women was significantly lower during
the rye bread than during the wheat bread period (Table 2)
. The intakes
of PUFA and alcohol in women were added as covariates in the MANOVA
analysis, but they did not affect the results.
The intakes of total, soluble and insoluble fiber from total diet
(Table 2)
and from the test breads (Table 4) by both men and women were significantly greater during the rye bread
period than the wheat bread period. The goal for the difference in the
daily intake of fiber from the test breads (15 g/d) between the rye and
wheat bread periods was achieved by men but not by women (Table 4)
.
However, the intakes of total and soluble fiber from rye bread
expressed per unit of energy during the rye bread period did not differ
significantly between men and women, and there was no difference in the
absolute intake of soluble fiber from the diet during the rye bread
period (Table 2)
between the men and the women. Men received more
soluble fiber from rye bread (60 vs. 50% of the total soluble fiber,
P = 0.013); however, among other sources of soluble
fiber, the women tended to eat more fruits than men (P
= 0.065, Fig. 1
).
|
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Concentrations of serum lipids during the study are presented
separately for men and women (Table 5) because the intakes of test breads were greater in men than in women;
consequently, the effects of treatment on serum lipids might have been
different in men and women. Except for the concentration of serum total
triacylglycerol in women, the serum total, HDL and LDL cholesterol and
serum total triacylglycerol concentrations did not differ significantly
at the beginning of the bread periods. MANOVA analysis revealed
significant changes during the study in concentrations of serum total
and HDL cholesterol in men (P = 0.018 and P
= 0.006, respectively; Table 5
), but not in women. However, when
the changes in serum total and HDL cholesterol concentrations in men
during the rye and wheat bread periods were analyzed, only the
reduction in the total cholesterol concentration during the rye bread
period remained significant (P = 0.002, paired
t test; Table 5
). Because there were significantly different
concentrations of serum total triacylglycerols at the beginning of the
bread periods in women, the proportional changes in serum
triacylglycerols during the rye and wheat bread periods were tested
using serum triacylglycerol concentrations at the beginning of the
bread periods as covariates, but this analysis did not reveal any
differences.
|
). The proportional reductions in serum total and LDL cholesterol
concentrations were significantly different among tertiles
(P = 0.048 and P = 0.032, respectively,
Kruskal-Wallis) and dependent on the amount of rye bread consumed by
men but not by women.
|
No significant changes were found in the fasting plasma glucose and insulin concentrations during the study.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Possible confounding effects were taken into consideration in the study design because the subjects served as their own controls and were asked to maintain their body weight (±1 kg) and lifestyle habits unchanged during the study. In addition, for premenopausal women, the phase of the menstrual cycle was taken into account. Moreover, the intakes of PUFA and alcohol and the concentrations of serum total triacylglycerol at the beginning of the bread periods, which differed significantly between the bread periods in women, were used as covariates in the analysis of the data. In men, intakes of fat, cholesterol and alcohol did not differ significantly between the bread periods, indicating that diet exerted a similar effect on serum lipids during both bread periods in men.
The probable explanation for the reduction in total and LDL cholesterol
concentration in men is the increased intake of fiber from bread during
the rye bread period. In this respect our findings are in agreement
with those of Khaw and Barrett-Connor (1987)
, who
noted that absolute intake of fiber (g/d) is more strongly and
inversely related to ischemic heart disease than is the relative fiber
intake (as a proportion of energy intake). Although the intake of fiber
from rye bread per unit energy intake was similar in men and in women,
the absolute intake of fiber by women may not have been sufficient to
reduce serum lipid concentrations. The hypocholesterolemic property of
fiber has also been found to be associated with water-soluble
fractions of fiber, but various water-soluble fibers may differ in
their ability to reduce cholesterol (Bell et al. 1990
,
Jenkins et al. 1975
, Jensen et al. 1993
).
Previous meta-analysis, which involved 20 trials, showed that daily
intake of 3 g ß-glucan from oats causes a clinical reduction,
0.13–0.16 mmol/L, in serum cholesterol (Ripsin et al. 1992
). In this study, the men received, on average, 2.0 and
women 1.5 g/d ß-glucan from rye bread during the rye bread period.
In rye, the soluble fraction of fiber is mainly viscous arabinoxylan
(Nilsson et al. 1997
). In this study, the absolute
intake of soluble fiber from the diet by men was not significantly
different from that by women during the rye bread period. However, the
proportion of soluble fiber obtained from rye bread was greater in men
than in women, indicating that women received proportionately more
soluble fiber from vegetables, fruit and berries than did men. This
finding suggests that soluble fiber from cereals decreases serum
cholesterol more effectively than fiber from vegetables and fruit. This
is in accordance with the previous findings of the inverse relationship
between the intake of total cereal fiber and risk of CHD (Morris et al. 1977
, Pietinen et al. 1996
, Rimm et al. 1996
).
The change in concentration of serum HDL cholesterol during the study
was significant for men, but the reduction during the rye bread period
(-0.09 mmol/L) was not significant and was physiologically
unimportant. In addition, the clinical unimportance of the HDL
cholesterol reduction during the rye bread period can also be seen in
the ratio of the total and HDL cholesterol concentrations, which did
not change significantly during the rye bread period. Concentration of
serum HDL cholesterol is affected by alcohol intake and body mass index
(Bolton-Smith et al. 1991
), but in this study, these
factors did not differ significantly between the bread periods for men.
We found no changes in fasting plasma glucose and insulin concentrations in this study. Post-hoc power calculations showed that any clinically important change in plasma glucose concentration should have been noted, but because of the large variation in plasma insulin concentration, the sample size in this study was too small to detect any clinically important change in plasma insulin concentration. However, due to the almost identical values at various measurements, it is likely that there were no changes in plasma glucose and insulin concentrations during the bread periods.
To our knowledge, this is the first intervention trial concerning the
effects of rye bread on serum lipid concentrations in healthy adults.
The reduction of serum total cholesterol by 8% in men in this study is
comparable with earlier studies concerning the effects of dietary
changes on blood total cholesterol (Clarke et al. 1997
).
Unfortunately, this study does not explain the mechanism behind the
cholesterol-lowering by rye bread. Some previous studies in animals
have shown that rye could affect blood lipids by increasing the hepatic
hydroxymethylglutarate (HMG)-CoA reductase activity, which regulates
cholesterol synthesis in the liver (Lund et al. 1993
),
or by increasing the total concentration of bile acids in the bile
(Zhang et al. 1994b
).
Our results indicate that men would benefit from including ~200 g rye
bread or more in their daily diet and that the cholesterol-lowering
effects can be achieved without other changes in the usual diet. About
8 slices (200 g) of rye bread per day is only 2–3 slices more than the
amount currently consumed by Finnish men (140 g/d) (The 1997
Dietary Survey of Finnish Adults 1998
) and is a realistic
amount to consume in a normal diet. Our results also show that rye
bread can easily be adopted into the daily diet in relatively large
amounts. Other high fiber products are reported to cause poor
compliance when ingested in amounts that influence serum lipids
(Hunninghake et al. 1994
, Uusitupa et al. 1992
). On the other hand, it is difficult for women to consume
the amount of rye bread that would influence serum lipids without
marked changes in the composition of their whole diet. The present
finding that rye bread, at a daily intake of 
200 g reduces serum
cholesterol, requires further confirmation; if proven, it presents a
challenge to the food industry to develop new ways in which rye fiber
can be introduced into the diet.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 Supported by the Fazer Bakeries Ltd., Vaasan & Vaasan Ltd. and the Technology Development Centre of Finland. Bakeries supplied the test breads used in the study.
4 Abbreviations used: CHD, coronary heart disease; PUFA, polyunsaturated fatty acids.
Manuscript received May 26, 1999. Initial review completed July 19, 1999. Revision accepted October 7, 1999.
|
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