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*
Department of Biochemistry, College of Medicine, National Taiwan University, Taipei;
Department of Home Economics, National Taiwan Normal University, Taipei; and
**
Department of Biochemistry, Tzu-Chi College of Medicine and Humanities, Hualien;
Cathay General Hospital, Taipei, Taiwan
3To whom correspondence should be addressed. Department of Biochemistry, College of Medicine, National Taiwan University, No. 1, Sec. 1, Jen-Ai Road, Taipei, 100 Taiwan. Telephone: 011-886-2-23921751; Fax: 011-886-2-23922538.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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-tocopherol
concentrations between vegetarians and omnivores. Our results suggest
that vegetarian diets decrease the susceptibility of LDL to oxidation
despite their higher dietary P/S ratio.
KEY WORDS: • vegetarian diet • LDL oxidation • polyunsaturated fatty acids • arachidonic acid • humans
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). Connell (1988)
recommended a sample vegetarian menu to typical
lacto-ovo-vegetarians which supplied 24.7 energy percentage (en%)4
from
fat, with 6.5 en% from saturated fatty acids (SFA), 13.6 en% from
monounsaturated fatty acids (MUFA), 4.6 en% from polyunsaturated fatty
acids (PUFA), and a polyunsaturated/saturated fatty acids (P/S) ratio
of 0.71. Practically, lacto-ovo-vegetarian diets contain about 37 en%
from fat with a P/S ratio of about 0.7 in Dutch and British
(Brants et al. 1990
, Draper et al. 1993
)
and 29 en% from fat with P/S ratio of 1 in American lactovegetarian
diet (Sacks et al. 1985
). Vegan diet studied in London
(Draper et al. 1993
) or "living food" vegan diet
studied in Finland (Agren et al. 1995
) contained 34–37
en% from fat with a P/S ratio of about 1.7. Their dietary protein was
derived mostly from cereals, and dietary fat from seeds, nuts and
avocado; therefore, MUFA constituted about half of fatty acids in the
diet (Agren et al. 1995
, Connell 1988
).
As far as we know, few of the vegetarians studied except those in Asia
consumed soybean products as major substitutes for all animal products.
A local study (Pan et al. 1993
) of young male Taiwanese
lactovegetarians (age, 18–23 y) revealed that their diets contained
27.5 en% from fat, consisting of 4.8 en% from SFA, 6.3 en% from MUFA
and 15.5 en% from PUFA. Thus the resulting P/S ratio of 3.3 is much
higher than those in the Western countries.
A prominent feature of atherosclerotic lesions is the
cholesterol-loaded macrophage foam cells (Gown et al. 1986
). Oxidative modification of LDL rather than native LDL is
believed to be the source of cholesterol (C) in foam cells
(Fogelman et al. 1980
). Oxidized LDL does occur in vivo
(Palinski et al. 1989
, Ylå-Herruala et al. 1989
), and the inhibition of such oxidation slows the progress
of atherosclerotic lesion in experimental animal models (Carew et al. 1987
, Sparrow et al. 1992
). High dietary
PUFA lowers both LDL- and HDL-C and renders LDL more susceptible to
oxidation because PUFA incorporated into LDL presents more double bonds
accessible to oxidative attack (Abbey et al. 1993
,
Berry et al. 1991
, Reaven et al. 1993
).
Low LDL-C is considered to be beneficial; however, low HDL-C
and PUFA-rich LDL are both considered to be atherogenic. Thus the
effects of long-term high PUFA diets on atherosclerotic risks are
controversial and require further investigation. As mentioned above,
Taiwanese vegetarians consume diets rich in PUFA; therefore, they are
good candidates for the investigation of the long-term effect of
high PUFA diets on plasma HDL-C concentration and susceptibility of
LDL to oxidation as reported in this study which was conducted from
August 1995 through June 1997.
|
METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Volunteer vegetarians (ages, 31–45 y) and age- and sex-matched omnivores were recruited from two different areas of Taiwan. One is a metropolitan area of 3 million population (Taipei); the other is a small city on the east coast which has a population of 100,000 (Hualien). Most of the Taipei vegetarians were recruited through Nontzan Temple and societies of vegetarians, and the counterpart omnivores were recruited from a group of apparently healthy public-service personnel who volunteered and subjected themselves to a long-term epidemiological study of cancer. In Hualien, most of the vegetarians were recruited from Tzu-Chi Buddhist community and the counterpart omnivores from personnel of Hualien hospitals. The physical activities, foods and level of economy of Taipei and Hualien subjects are very different; therefore, the data obtained from these two cities were analyzed separately. The vegetarians recruited included vegans and the lactovegetarians who ingested less than a glass (240 mL) of low-fat or skim milk per day and followed the vegetarian diet at least for 2 y. Each of the volunteers received a standardized personal interview based on a structured questionnaire concerning sociodemographic characteristics, current status of cigarette smoking, alcohol drinking, exercise, cooking oil used at home, personal and family history of major diseases and medical treatments. Anthropometric measurements were conducted. Fasting blood (20 mL) was withdrawn for routine biochemical screening of metabolic disorders and also for lipid analyses. Subjects with liver disease, diabetes, hypertension or who smoked or drank alcohol more than 10 g/d were excluded from this study. By above criteria, 26–30 apparently healthy persons participated in each group of Taipei, and 53–54 persons per group in Hualien. The lack of males in Hualien was due to few men adhering to the vegetarian diet. Among the vegetarians, about one-half were nuns and monks. About one-third of the vegetarians were vegan and about two-thirds were lacto-vegetarian. The mean (±SD) period of consuming the vegetarian diet was 7.7 ± 4.8, 8.5 ± 8.1 and 7.9 ± 4.9 y for women and men in Taipei and women in Hualien, respectively. The protocol and purpose of the study were explained to the subjects, and all the subjects gave their informed consent to the study protocol which was approved by the National Health Research Institute, Taiwan.
Dietary assessment.
The 24-h recall method was used for assessing dietary intake by three
well-trained interviewers. Household measures were used to estimate
portion sizes of food, and a database for Taiwan food composition
(Department of Health 1998
) was used to calculate the
energy and nutrient intakes.
Blood lipid and lipoprotein analysis.
Blood samples were collected from fasting subjects in EDTA (2.8 g/L)-containing tubes. Plasma HDL-C was determined after precipitation of apolipoprotein B-containing lipoproteins by phosphotungstic acid (14210 Precipitation reagent; E. Merk, Darmstadt, Germany). LDL were precipitated by heparin at their isoelectric point (pH 5.12) (14992 Precipitation reagent; E. Merk). After centrifugation at 5000 x g for 20 min, the HDL and VLDL remained in the supernatant. LDL-C was determined by subtracting C in the supernatant from total C. C and triglyceride of plasma and lipoproteins were measured by using enzymatic kits (14366 and 14354 Merckotest, E. Merk). Within-assay and between-assay coefficients of variation for cholesterol and triglycerides were within 3%.
Measurement of the in vitro oxidation of LDL.
LDL were isolated from randomly selected 10 (Taipei) or 32 (Hualien)
plasma samples of each group by sequential ultracentrifugation
(Havel et al. 1955
) at densities of 1.019–1.063 kg/L.
The isolated LDL were dialyzed extensively against 2,000 volumes of PBS
overnight and diluted with PBS to 200 mg/L of protein immediately
before LDL oxidation analysis. The LDL oxidation was initiated by the
addition of CuSO4 to a final concentration of 10 µmol/L.
For measuring thiobarbituric acid-reactive substances (TBARS)
formation, the mixture was incubated at 37°C in a shaking
water-bath, and aliquots were removed at the end of 2, 3, and
4 h. TBARS were measured according to the method of Beuge and Aust (1978)
. Formation of conjugated dienes was monitored
continuously at room temperature by measuring the absorbance at 234 nm
during the copper-catalyzed oxidation of LDL using a Hitachi U-2000
spectrophotometer (Hitachi, Tokyo, Japan) (Esterbauer et al. 1989
).
Other laboratory measurements.
LDL -tocopherol was determined by HPLC according to the method
described by Kaplan et al. (1987)
. Fatty acid
composition of LDL was determined according to the method of
Lepage and Roy (1986)
. LDL protein was determined by a
modified Lowry method (Markwell et al. 1978
).
Statistical analysis.
All values are expressed as mean ± SD. To compare the group means between vegetarians and omnivores, Student’s t test was used. Correlations between the LDL oxidation variables and LDL fatty acid composition or LDL-C were analyzed by linear regression. Statistical significance of difference was set at P < 0.05.
|
RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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. Stature did not differ between the vegetarians and omnivores. However,
body weight and body mass index (BMI) were significantly lower
(P < 0.05) in the vegetarians than in the omnivore
counterparts. Blood pressure was lower in all vegetarian groups than in
their matched omnivore groups (Table 1)
. Female vegetarians consumed
less energy. Protein, fat and cholesterol intakes were significantly
less and P/S and M/S ratios of the dietary lipids were significantly
higher in vegetarian groups, except M/S in Taipei female, than in the
matched omnivore groups. Combining all data, the P/M/S ratio of
vegetarian diets was 2.40 ± 0.99: 1.25 ± 0.70: 1 (means
± SD, n = 100) and of omnivorous
diets was 1.32 ± 0.44: 1.07 ± 0.36: 1 (means ± SD, n = 99). Intakes of vitamins C and E
did not differ between the vegetarians and the omnivores (Table 2
).
|
|
).
|
). The TBARS, measured as lipid peroxide products formed at 2, 3 and
4 h of Cu2+-induced LDL oxidation, were significantly
lower in the vegetarian groups (P < 0.005), except the
women of Taipei, than in the corresponding omnivore groups. However,
there was a clear trend (P = 0.2) of lower LDL-TBARS in
Taipei female vegetarians than in the matched omnivores. When the
LDL-TBARS data from Taipei and Hualien women were pooled,
vegetarians and omnivores differed (P < 0.001).
|
-tocopherol concentration relative to mg LDL protein or mg
LDL-C (data not shown) did not differ between vegetarian and
omnivorous groups (Table 4)
. LDL of vegetarians in Taipei (both sexes
combined) contained 4 mol/100 mol more linoleic acid and 1.7 and 0.7
mol/100 mol less arachidonic and eicosapentaenoic acids, respectively,
than those of the omnivores (Table 5
). When the data from vegetarians and omnivores of Taipei were pooled, lag
time of LDL oxidation was negatively correlated with LDL arachidonic
and eicosapentaenoic acids (r = -0.55, P
= 0.0003; r = -0.47, P = 0.003,
respectively) but not with linoleic acid (r = 0.26,
P = 0.12). LDL TBARS production in LDL oxidized for
3 h was positively correlated with these two fatty acids
(r = 0.56, P = 0.0002; r
= 0.45, P = 0.004; respectively) but negatively
correlated with LDL linoleic acid (r = -0.36,
P = 0.023). Similar correlations were found when LDL
were oxidized for 2 or 4 h.
|
|
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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1, P/M 0.5) (Agren et al. 1995
, Connell 1988
, Melby et al. 1994
, Tesar et al. 1992
). The P/S ratio of 2.4
of the vegetarian diet reported in this study was lower than that of
the other local study of Pan et al. (1993)
of young
Buddhist vegetarian diet which was of 3.3. The decreased P/S ratio
probably resulted from the increased use of cooking oils enriched with
MUFA such as high-oleic sunflower oil rather than soybean oil in
recent years. In agreement with other studies (Chen 1965
, Ko 1983
, Melby et al. 1994
,
Sacks et al. 1985
), the vegetarians had lower blood
pressure, plasma C and LDL-C than the omnivores. The HDL-C/LDL-C
ratio was higher in all vegetarian groups due to the significantly
lower LDL-C.
The most important finding in this study is that plasma LDL of
Taiwanese vegetarians was less oxidizable in vitro in spite of the
higher P/S ratio of their dietary fat. The validity of this result is
supported by the reproducible findings obtained from Taipei and
Hualien. The unexpectedly shorter lag time in women from Hualien than
that from Taipei could be due to the fact that the Taipei study was
done in winter and Hualien study was done in summer, and the sample
collected in Hualien required one more day to return to the Taipei
laboratory. Regional and seasonal differences of available foods and
activities might result in the difference of lag time in Taipei and
Hualien. Recent study in Slovakia (Nagyová et al. 1998
) has shown that TBARS in native and oxidized LDL were
significantly lower in Slovakian vegetarians. The P/S ratio of their
vegetarian diet was not indicated, but another Slovakian study
(Krajcovicová-Kudlácková et al. 1997
)
reported that vegetarian children frequently consumed oils with
high-oleate content that seemed to be different from ours.
Several dietary factors might contribute to the higher resistance of
LDL to oxidation in vegetarians. One factor is antioxidants from
vegetables and fruits: Unlike Finnish vegans (Rauma et al. 1995
) who consume strict, uncooked vegan diets and Slovakian
lacto- and lacto-ovo-vegetarians who have significantly higher intakes
and blood levels of antioxidants
(Krajcovicová-Kudlácková et al. 1995a
,
Krajcovicová-Kudlácková et al. 1995b
), the vegetarians we studied did not consume more
fruits and vegetables than the matched omnivorous controls. Neither
dietary vitamins C and E on per capita per day basis nor LDL
-tocopherol concentration differed between the vegetarians and the
omnivores although there was a trend for a higher intake of vitamin C
on a per MJ basis in vegetarians (P = 0.03, 0.09, 0.16;
for Taipei female, male and Hualien female, respectively). Therefore,
the dietary intakes of vitamins C and E could not fully explain the
significantly higher resistance of the LDL of vegetarians to in vitro
oxidation. A second factor is amount of dietary fat: The daily dietary
fat intake was low in this study (about 24 en% in the vegetarians and
28 en% in the omnivores). Schwab et al. (1998)
demonstrated that reduced-fat diets (30 en%) enriched in PUFA or
SFA oil resulted in similar susceptibility of LDL to oxidation in each
diet. Sarkkinen et al. (1993)
even demonstrated that a
low-fat diet with high polyunsaturated fat (32 en%, P/S = 0.8) decreased plasma TBARS as compared to a low-fat diet with low
polyunsaturated fat (30 en%, P/S = 0.25), and the difference in
TBARS production was not due to the serum vitamin E concentration. It
seemed that when dietary PUFA was not in excess, other dietary factors
might contribute to the susceptibility of LDL to oxidation more
dramatically than the P/S ratio. A third factor is LDL-C: increased C
intake and plasma LDL-C level have been shown to be associated with
the increased LDL oxidizability in normal subjects (Levy et al. 1996
). However, in this study, no significant correlation
between LDL-C and LDL oxidizability was found (r = -0.24, P = 0.14; r = 0.3, P
= 0.08; for lag time of LDL oxidation and LDL TBARS production,
respectively). A fourth factor is LDL-fatty acid: Contrary to
Louheratan et al.’s study (Louheratan et al. 1996) in which dietary linoleic acid intake was positively
correlated with LDL oxidizability, this study showed a negative
correlation between LDL-linoleic acid content and LDL
oxidizability. Some factors coexisted with dietary linoleic acid that
might decrease LDL oxidizability. The contents of LDL arachidonic and
eicosapentaenoic acids, which might be particularly susceptible to
oxidation, were higher in omnivores, and positively correlated with LDL
oxidizability, especially regarding arachidonic acid. The potential
deterious effect of a high concentration of blood arachidonic acid on
coronary heart disease has been suggested (Peterson et al. 1994
) but not been supported by others (Griffin et al. 1997
). Animal foods but not vegetable foods contain arachidonic
and eicosapentaenoic acids. Although they can be synthesized from
linoleic and -linolenic acids in humans, the transformation
efficiency might not be high and the resulting lower levels of
arachidonic and eicosapentaenoic acids in vegetarian LDL may have
contributed to the resistance of LDL to oxidation. The fifth factor is
dietary isoflavones: Excluding meat and fish from diet, the main source
of dietary protein in Taiwanese vegetarians is soybean products which
contain significant amount of isoflavones. Isoflavones have been shown
to exert appreciable antioxidant activity (Kurzer and Xu 1997
) and to protect LDL from oxidation (Tikkanen et al. 1998
). In our recent study (Tsai and Huang 1999
), LDL isolated from hamsters fed isoflavone-containing
soy protein were more resistant to copper-induced oxidation than
those from hamsters fed low-isoflavone soy protein or fish protein
as measured by lag time of conjugated diene formation and TBARS
production. However, intake of isoflavones was not assessed in this
study due to no database on the isoflavone content of foods available
in Taiwan. We speculate that the decreased LDL oxidizability in
vegetarians, in spite of the high PUFA intake, might be due to the
low-fat, low-arachidonic and eicosapetaenoic acids, high vitamin C
and high soybean products. Differences in lifestyle between the
vegetarians and omnivores also might have some effect.
Our data suggest that in addition to the decreased blood pressure, plasma total and LDL-C and higher HDL-C/LDL-C ratio the decreased LDL oxidizability is another beneficial effect on cardiovascular system in vegetarians in spite of the higher P/S ratio in vegetarian diet.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 Funded by the National Health Research Institute, Taiwan (DOH 85,86-HR-527).
4 Abbreviations used: BMI, body mass index; C, cholesterol; en%, energy percentage; MUFA, or M, monounsaturated fatty acids; PUFA, or P, polyunsaturated fatty acids; SFA, or S, saturated fatty acids; P/S, the ratio of P to S; TBARS, thiobarbituric acid reactive substances.
Manuscript received October 14, 1999. Initial review completed December 7, 1999. Revision accepted March 2, 2000.
|
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 C.-J. Hung, P.-C. Huang, S.-C. Lu, Y.-H. Li, H.-B. Huang, B.-F. Lin, S.-J. Chang, and H.-F. Chou Plasma Homocysteine Levels in Taiwanese Vegetarians Are Higher than Those of Omnivores J. Nutr., February 1, 2002; 132(2): 152 - 158. [Abstract] [Full Text] [PDF]
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