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Laboratory of Nutrition Chemistry, Division of Bioresource and Bioenvironmental Sciences, Graduate School, Kyushu University, Fukuoka 812-8581, Japan and * Research Institute of Angiocardiology and Cardiovascular Clinic, Kyushu University School of Medicine, Fukuoka 812-8582, Japan
1To whom correspondence should be addressed.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: • blood pressure • Japanese diet • cholesterol • walnuts • humans
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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, Hu et al. 1998
, Prineas et al. 1993
). The favorable fatty acid composition of nuts, that is, a
relatively high percentage of polyunsaturated and monounsaturated fatty
acids, may explain their protective effect (Dreher et al. 1996
). This is further supported by the finding that both
polyunsaturated fatty acid (PUFA)-rich walnuts (Sabaté et al. 1993
) and monounsaturated fatty acid-rich almonds
(Abbey et al. 1994
) improve the coronary heart disease
risk profile by lowering LDL cholesterol.
There are no studies to date on the effects of nut consumption on the
risk of ischemic heart disease or cardiovascular risk factors in people
consuming a Japanese diet. We were thus prompted to investigate the
effects of consuming a specific type of nut in a carefully controlled
experimental situation. We report here the results of a controlled
trial of Japanese diets that compared the effects on serum lipids,
apolipoproteins (apo) and blood pressure of a diet rich in walnuts with
those of a diet that is consumed by the average Japanese person
(National Nutrition Survey of Japan 1997
, Recommended Dietary Allowance for the Japanese 1995
) but did not include nuts.
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SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Men and women who responded to campus and community advertisements were
screened by three investigators. They were excluded from the trial if
they ate nuts frequently, had known food allergies, smoked cigarettes,
had a history of hypertension or atherosclerotic or metabolic disease,
were taking any medication on a regular basis or were considered unable
to comply with the study protocol. Twenty Japanese men and 20 women
entered and completed the experiment. The first week after recruitment
was used to record the daily habitual diet of the participants. Their
nutrient intakes were calculated from a computer database of foods
based on the composition of Japanese foods (NTU system; version 6,
Human Science Laboratories, Shiga, Japan) (Table 1
). Subject characteristics are given in Table 2
.
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A controlled, single-blind, crossover design was used. All subjects consumed the average Japanese diet (reference diet) during a 5-d run-in period; this phase was followed by an 8-wk experimental period in which they followed each of two consecutive diets for 4 wk. One group consumed the walnut diet during the first period and reference diet during the second period; the other group followed the diets in reverse order. The subjects were assigned to a particular dietary sequence, with stratification on the basis of age, baseline serum cholesterol concentration and body mass index. Ten men and women consumed the walnut diet first, and the other 20 subjects, the reference diet.
The study protocol was approved by the University Hospital, Faculty of Medicine, Kyushu University, in accordance with the Helsinki Declaration of 1975 as revised in 1983, and all subjects gave informed consent. They were offered an honorarium for their participation.
Diets.
During the 61 d of the study, the subjects received all of their
meals at the nutrition-research kitchen of the university.
Breakfast and dinner were eaten on the premises, under the supervision
of one of the researchers. Lunches were packed and distributed from
1100 to 1500 h. All foods were weighed and apportioned for each
subject. The diets consumed during the study consisted of natural and
common food items and were prepared and cooked in customary ways
according to a 10-d menu cycle. Daily menus were formulated so that
there were two levels of energy intake, ranging from 10.0 to 11.1 MJ
per day for men, and from 8.37 to 9.20 MJ per day for women. The
percentage of energy from protein, carbohydrates, total fat and dietary
fiber (Table 3
) did not change during the dietary periods. The two experimental diets
were identical except that the walnut diet substituted two servings of
walnuts per day (25 or 27 g per serving, or 52 g of walnuts
per 10.0 MJ) for portions of some foods in the reference diet. The
walnuts were provided by the California Walnut Commission (Sacramento,
CA).
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and the nutrient intake for
20- to 39-y olds based on the National Nutritional Surveillance in
Japan held in 1996 (National Nutrition Survey of Japan 1997
). Total fat content accounted for ~25% of energy, with
a ratio of saturated/monounsaturated/polyunsaturated fat of 1:1.5:1.
The reference diet included foods from all major food groups but did
not contain nuts, nut butters or nut oils of any kind. The foods in the
walnut diet were identical to those in the reference diet; however, the
sizes of the portions of fatty foods such as meat were reduced, and the
amount of visible fat (oils, margarine and butter) was decreased to
accommodate the percentage of energy derived from walnuts (12.5%).
Walnuts were served in several ways, e.g., mixed in salads or cooked in
dinner entrees. Walnuts contributed 50, 8.5 and 12.6% of the total
fat, protein and fiber, respectively, of the walnut diet.
Complete duplicate samples of the two study diets were collected on 15
randomly selected days during the study period. Mixed samples were
analyzed for levels of macronutrients and fatty acids (AOAC
1987
) (Food Chemistry Center, Fukuoka, Japan). The composition
of each diet as determined by chemical analysis conformed closely to
the composition planned by computer with the NUT system (Version 6,
Human Science Laboratories). In addition, the chemical determination of
fatty acid content revealed the expected distribution for each diet
(Table 4
).
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Body weight, measured without shoes or heavy clothing, was recorded at the end of the run-in period and twice a week thereafter. Average body weight decreased by 1.3 kg for men and 0.1 kg for women over the 54-d study period, but this decrease was not related to a specific diet. The mean difference in weight lost between the dietary treatments was 0.350 kg (P = 0.797) for men and 1.18 kg (P = 0.102) for women.
Measurements.
Blood was drawn from each subject after an overnight fast at the end of
the run-in period and at the end of each dietary period (d 6, 33
and 61). Serum was obtained by centrifugation at 4°C (800 x g, 15 min). Serum and lipoprotein subfractions were
analyzed to determine concentrations of cholesterol (Allain et al. 1974
) and triacylglycerols (Spayd and Bruschi 1974
) with the use of enzyme reagent kits (Cholesterol
C-test and Triglyceride G-test, respectively; Wako Pure
Chemicals, Tokyo, Japan). HDL cholesterol (Warnick et al. 1982
) was measured by the commercially available kit (HDL-C
test, Wako Pure Chemicals). LDL cholesterol was calculated by
subtraction with the Friedewald algorithm (Friedewald et al. 1972
). For each subject, the fatty acid composition of serum
cholesterol esters, phospholipids and triacylglycerols was determined
in serum samples obtained at the end of each diet period and analyzed
according to methods previously described (Ikeda et al. 1998
). Concentrations of serum apo A-I and B (Ikeda et al. 1991
) were determined with a modified commercially
available turbidimetric assay (Apo A-I Auto·N and Apo B Auto·N;
Daiichi Pure Chemicals, Tokyo, Japan).
Blood pressure was measured with a random-zero sphygmomanometer at the end of the run-in period (d 6) and twice during each experimental diet period (d 19, 33, 47 and 61). At each session, blood pressure was measured by physicians. Measurements were obtained during fasting after a 5-min rest in a sitting position.
Statistical analysis.
Descriptive values are expressed as means ± SEM.
Statistical analysis included two-tailed t test for
the comparison of changes in outcome variables in response to dietary
treatment and diet period for the two-period crossover design, with
methods described by Fleiss (1986)
. We first tested for
possible interaction between the dietary treatment and diet period
(carry-over effect), also using a two-tailed t test
(Fleiss 1986
).
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RESULTS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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. The composition of the reference diet
was based on that of the fifth edition of the Dietary Allowance for
Japanese. The fatty acid composition of the walnut diet was closer to
that of walnut fat, with a larger proportion of PUFA, especially
-linolenic acid (Table 4)
. The significant differences in the fatty
acid composition of the serum cholesterol esters and phospholipids of
the subjects during the two dietary periods confirmed that they had
adhered closely to the diets (Tables 5
and
6). Serum triacylglycerol fatty acid composition was significantly
different (P < 0.01) in the proportions of linoleic
acid (23.9 ± 0.7 and 31.3 ± 1.4% for reference and walnut
diet, respectively, in women; 22.5 ± 0.9 and 30.7 ± 0.8%
for reference and walnut diet, respectively, in men) and -linolenic
acid (1.7 ± 0.2 and 3.9 ± 0.4% for reference and walnut
diet, respectively, for women; 1.6 ± 0.1 and 3.8 ± 0.4%
for reference and walnut diet, respectively, for men), with
significantly lower proportions of oleic and palmitic acids during the
walnut diet period (P < 0.01).
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), presumably reflecting the difference in dietary fat content in the
habitual diet and the test diet (Tables 1
and 3)
. There were no
significant differences in the total, LDL and HDL cholesterol
concentrations between the reference and walnut diet groups at the end
of the first or second period, although women who consumed the walnut
diet during the second period tended to have a lower level of total
cholesterol (P = 0.10) and LDL cholesterol
(P = 0.08) than those consuming the reference diet
during the same period. A crossover pattern from the first period to
the second period was observed in the values for total and LDL
cholesterol in men and women. Because there was no evidence of a
carry-over effect between the periods, the values for serum lipids
and lipoproteins are presented in Table 7
for all study subjects during each diet period, irrespective of the
order of diet consumption. In men, the mean serum total cholesterol
concentration during the walnut diet was 0.16 mmol/L lower than the
concentration during the reference diet period (P = 0.05), representing a reduction of 3.8%. In women, the concentration
during the walnut diet period was 0.21 mmol/L (4.9%, P
< 0.01) lower than that during consumption of the reference diet.
The serum total cholesterol concentration in men decreased in 15 of 20
subjects during the walnut diet period in comparison with the reference
diet period; similarly, 15 of 20 women had decreased cholesterol
concentration during the walnut diet period. The LDL cholesterol
concentration during the walnut diet period in women was 0.22 mmol/L
lower than the concentration during the reference diet period
(P < 0.01), representing a reduction of 11%; however,
LDL cholesterol reduction was not significant in men (P
= 0.13). There were no significant differences in serum HDL
cholesterol or triacylglycerol in men or women due to diet. The ratios
of LDL to HDL cholesterol in men and women were significantly lower
during the walnut diet period than during the reference diet period
(P < 0.05). The serum apo B concentration in men and
women was lower during consumption of the walnut diet than of the
reference diet (P < 0.05). The concentration of the
serum apo A-I was not influenced by diet.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Our results are essentially consistent, although of lesser magnitude,
with those reported by Sabaté et al. (1993)
, who
detected 12.4 and 16.3% reduction of total and LDL cholesterol,
respectively, in American men when 84 g/d walnuts replaced 20% of the
energy from fat for 4 wk in a National Cholesterol Education Program
Step 1 diet. Unlike our study, they found a significant reduction of
HDL cholesterol (4.9%) after supplementation with walnuts. However,
they reported that the ratio of LDL cholesterol to HDL cholesterol was
significantly lower after consumption of the walnut-supplemented
diet compared with the reference diet. It is therefore noteworthy that
walnut-containing diets exert beneficial effects on lipoprotein
risk profiles despite differences in race and gender.
Given the known effects of dietary fats, the composition of the fatty
acids found in the walnut diet should lower serum cholesterol
(Keys et al. 1965
), as described by Sabaté et al. (1993)
. The ratio of polyunsaturated to saturated fat
was 3.0 in the walnut diet and 1.0 in the reference diet. The walnut
diet contained relatively large amounts (~10% total fat) of the
(n-3) fatty acid, -linolenic acid (Dreher et al. 1996
), whereas it comprised ~3.8% of the reference diet.
However, recent studies have not demonstrated that -linolenic acid
has any greater cholesterol-lowering effect than linoleic acid
(Chan et al. 1991
, Kestin et al. 1990
).
Although walnuts and other foods with similar fat composition may lower
the serum cholesterol concentration through the actions of their fatty
acids, the type of dietary fiber and the very low ratio of lysine to
arginine that are characteristics of walnuts may also have some effect
in this regard (Dreher et al. 1996
, Kritchevsky et al. 1982
).
Several cross-sectional studies suggested that low fat diets or the
consumption of unsaturated fat decreases blood pressure (Salonen et al. 1988
). However, consistent with the results of
Sabaté et al. (1993)
, controlled dietary trials
have not provided clear support for this hypothesis (Sacks 1989
). Our study also does not indicate that dietary fat has a
role in the control of blood pressure because the blood pressure of our
normotensive subjects did not differ during the two study diet periods.
Recent epidemiologic studies suggest that frequent nut consumption may
be protective against coronary heart disease because of beneficial
effects on blood lipids. The protective effects of nuts appears to be
independent of other risk factors, including a number of other foods,
and was consistent across several population subgroups (Fraser et al. 1992
, Hu et al. 1998
, Prineas et al. 1993
). There are many nutritional similarities among types
of nuts (Dreher et al. 1996
). The total fat content is
high but consists largely of monounsaturated and polyunsaturated fat,
with small amounts of saturated fat (Dreher et al. 1996
). The fiber content is high, ranging from 5.2 to 14.3
g/100 g edible nut (Dreher et al. 1996
). In clinical
studies, diets supplemented with walnuts or almonds decreased serum
concentrations of LDL and total cholesterol (Abbey et al. 1994
, Spiller et al. 1998
). Thus, nuts other
than walnuts may also have cholesterol-lowering properties. This
study suggests that the apparent protective effect of nut consumption
against cardiovascular disease that was found in the study of
California Adventists (Fraser et al. 1992
), the Iowa
Womens’ Health Study (Prineas et al. 1993
) and Nurses’
Health Study (Hu et al. 1998
) may be mediated at least
in part through blood lipids.
The cardioprotective effects of -linolenic acid have been reported
in a cohort follow-up study in the United States (Ascherio et al. 1996
) and in a secondary prevention trial in Italy (de Lorgeril et al. 1994
). More recently, de Lorgeril and associates
(1999)
reported their more extended observations with the mean
follow-up time of 46 mo per patient, indicating that the initial
remarkably beneficial effects of the experimental dietary program
persisted compared with the control group consuming the prudent
Western-type diet. In that study, they confirmed that only
-linolenic acid in plasma was significantly associated with an
improved prognosis for cardiac death and nonfatal myocardial
infarction. Epidemiologic studies have consistently shown a positive
correlation between plasma cholesterol levels and the incidence of or
mortality from coronary heart diseases in various populations
(Stamler et al. 1986
, Verschuren et al. 1995
). Therefore, a walnut-containing diet may reduce
recurrence after a first myocardial infarction by reducing plasma
cholesterol level and increasing plasma -linolenic acid.
Abbey et al. (1994)
pointed out that although almonds
and walnuts were both effective in lowering plasma cholesterol, almonds
may be more beneficial than walnuts because they are rich in
monounsaturated fatty acids. It has been shown that LDL from subjects
consuming diets rich in polyunsaturated fatty acids are more prone to
oxidation in vitro than are LDL from subjects consuming monounsaturated
fatty acid–rich diets (Reaven et al. 1991
). A role for
oxidized LDL in the atherogenic process is suggested by various
experiments (Parthasarathy et al. 1987
). It is therefore
likely that LDL derived from subjects consuming a walnut diet are more
prone to in vitro oxidation than are LDL from subjects consuming the
reference diet. However, Rudel et al. (1998)
recently
demonstrated that an oleic acid– or saturated fatty acid–rich diet
resulted in more severe atherosclerotic lesion development than did a
PUFA-rich diet in LDL-receptor knockout and apo B overexpressed
mice, which carry more LDL than do wild-type mice. Therefore, it
remains to be determined what role a walnut-containing diet may
play in atherosclerosis development or prevention in experimental
animals.
In conclusion, the results of this study indicate that a diet that includes moderate quantities of walnuts without an overall increase in total dietary fat and energy decreases serum cholesterol concentration and favorably modifies the lipoprotein profile in normal Japanese men and women, an effect beyond that of the Japanese diet currently recommended for lowering cholesterol.
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ACKNOWLEDGMENTS |
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Manuscript received July 7, 1999. Initial review completed August 17, 1999. Revision accepted October 15, 1999.
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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, 
)
and female (•, 
) subjects consumed each diet, but half of the men
and women consumed the walnut diet first (open symbol); the other half
followed the reference diet first (closed symbol). Values are means
± SEM, n = 10. Asterisks indicate
*P = 0.10 and **P = 0.08 for
the corresponding female group during the second period.