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Original Research Communications |
-linolenic acid on thrombotic risk factors in vegetarian men1,2,3
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Objective: We investigated whether male vegetarians (n = 17) who consumed an increased amount of dietary 
-linolenic acid (ALA) showed any changes in their tissue profile of PUFAs, plasma thromboxane concentrations, platelet aggregability, or hemostatic factors.
Design: During the study, all subjects maintained their habitual vegetarian diets except that a proportion of dietary fat was replaced with vegetable oils and margarines that were provided. Initially, all subjects consumed a low-ALA diet (containing safflower oil and safflower oil–based margarine) for 14 d; they then consumed either a moderate-ALA diet (containing canola oil and canola oil–based margarine) or a high-ALA diet (containing linseed oil and linseed oil–based margarine) for 28 d. Blood samples were collected at day 0 (baseline), day 14, and day 42.
Results: Eicosapentaenoic acid, docosapentaenoic acid, total n-3 PUFAs, and the ratio of n-3 to n-6 PUFAs were significantly increased (P < 0.05), whereas the ratio of arachidonic acid to eicosapentaenoic acid was decreased (P < 0.05), in platelet phospholipids, plasma phospholipids, and triacylglycerols after either the moderate-ALA or high-ALA diet compared with the low-ALA diet. No significant differences were observed in thrombotic risk factors.
Conclusion: ALA from vegetable oils (canola and linseed) has a beneficial effect on n-3 PUFA concentrations of platelet phospholipids and plasma lipids in vegetarian males.
Key Words: Vegetarian diet • -linolenic acid • linoleic acid • platelet fatty acid • plasma fatty acid • polyunsaturated fatty acids • hemostatic factors • thrombosis • lipoprotein lipids • men
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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-Linolenic acid (ALA; 18:3n-3) is less abundant than LA; however, it is also present in vegetable oils and is the precursor of 20- and 22-carbon n-3 long-chain PUFAs. Omnivores can obtain their 20- and 22-carbon n-3 long-chain PUFAs either from dietary ALA or directly by consumption of fish, eggs, or animal products (1). Lactoovovegetarians can gain a limited amount of 20- and 22-carbon n-3 long-chain PUFAs from milk, dairy products, and eggs. Because animals can convert ALA to 20- and 22-carbon n-3 long-chain PUFAs and plants cannot, there are no 20- or 22-carbon n-3 long-chain PUFAs in plant-based vegan diets. Thus, vegans must rely totally on endogenous synthesis from ALA by desaturation and elongation. A diet with a low ratio of n-3 to n-6 PUFAs (n-3:n-6) can cause a reduced tissue n-3:n-6 [ie, increased ratio of arachidonic acid (AA; 20:4n-6) to eicosapentaenoic acid (EPA; 20:5n-3)], which may promote production of thromboxane A2 (a potent platelet aggregating agent), leading to increased thrombosis tendency (2). Results of a recent observation study showed that the n-3:n-6 in plasma and platelet phospholipids was significantly lower in both lactoovovegetarian and vegan groups than in meat-eaters in the study population (3). Platelet aggregation stimulated by collagen and ADP in whole blood showed a significant opposite trend to the n-3:n-6 in both plasma and platelet phospholipids. Plasma 11-dehydro-thromboxane B2 (11-dehydro-TXB2), a stable metabolite of thromboxane A2, was found to be higher in lactoovovegetarian and vegan groups than in those who ate meat. That is, these data suggested that the vegetarians had a potentially greater thrombotic risk than the omnivores.
The aim of the present study was to examine the effect of dietary ALA on atherosclerotic and thrombotic risk factors. The following question was asked: Do male vegetarians who daily consume an increased dietary ALA intake compared with their habitual diet exhibit a decreased ratio of AA to EPA in tissue, decreased plasma 11-dehydro-TXB2 concentrations, and reduced in vitro platelet aggregation?
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SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Diet and study design
This was a parallel intervention study that investigated the effect of dietary ALA on atherosclerotic and thrombotic risk factors in healthy male vegetarians. To answer the question posed, the study was designed so that 2 equal groups of subjects consumed diets with either a moderately increased ALA content (moderate-ALA diet; n-3:n-6 of 
1:3) or a substantially increased ALA content (high-ALA diet; n-3:n-6 of 1:1). The 2 experimental diets were chosen based on calculations with equations developed by Lands et al (4); the ratios of 1:3 and 1:1 were predicted to give plasma phospholipid AA and long-chain n-3 PUFA contents of 67% and 15% and of 55% and 30% of total PUFAs, respectively. Because the dietary n-3:n-6 of the subjects' habitual diets was not likely to be the same, both groups were first placed on the same diet with a low n-3:n-6 (low-ALA diet; n-3:n-6 of 1:20) for 14 d and then were randomly assigned to the moderate- or high-ALA diet for the next 28 d.
During the 3 dietary periods, the subjects were not required to alter their total fat intake, but were expected to substitute 75% of their normal dietary fat with oils and margarines that were provided: safflower oil and safflower oil–based margarine during the low-ALA diet, canola oil and canola oil–based margarine during the moderate-ALA diet, and linseed oil and linseed oil–based margarine during the high-ALA diet. Subjects were also requested to refrain from consuming fish during the 42 d of the intervention. The fatty acid composition of all oils and margarines used was analyzed by a method reported previously (5) (Table 1
). The safflower oil margarine was manufactured by Nuttelex Food Products Pty Ltd (Melbourne) and was purchased from a local supermarket. The canola oil margarine was manufactured by Meadow Lea Foods Ltd (Sydney, Australia) and was purchased from a local supermarket. The linseed oil was provided by Melrose Laboratories (Box Hill, Australia) and the linseed oil margarine was provided by Meadow Lea Foods Ltd.
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Blood specimen collections
At the second (day 0), third (day 14), and fourth (day 42) appointments, subjects came to the RMIT Medical Centre in the morning after an overnight fast. After subjects sat relaxed for 10 min, venous blood was taken in 1 EDTA-treated, 2 citrate-treated, and 2 CTAD (citrate, theophylline, adenosine, and dipyridamole)-treated vacuum tubes with 21-gauge needles. Immediately after blood was collected, each subject's weight, height, waist-to-hip ratio, and blood pressure were measured. Whole-blood platelet aggregation testing, a full blood examination, and platelet isolation were performed during the 3 h after blood sampling. Plasma samples were prepared during the 2 h after blood was drawn, portioned into tubes, and stored at –20°C until analyzed.
Full blood examination
A 0.5-mL blood sample was examined by using an automated hematologic blood counting system (Coulter Counter STKR; Coulter Electronics Inc, Hialeah, FL).
Plasma lipid and lipoprotein lipids
Triacylglycerol and total cholesterol concentrations were measured in EDTA-treated plasma collected from fasting subjects by using an enzymatic colorimetric test with a centrifugal autoanalyzer (Autoanalyser System 705; Hitachi, Tokyo) and commercially available enzymatic colorimetric kits (Boehringer Mannheim, Sydney, Australia) as described previously (7). HDL cholesterol was measured after precipitating all plasma lipoproteins except HDL with polyethylene glycol 6000. LDL cholesterol was calculated from the values obtained for total cholesterol, HDL cholesterol, and triacylglycerol for each subject by using the Friedewald formula as developed by DeLong et al (8).
Platelet and plasma fatty acids
Two CTAD-treated tubes of whole blood were centrifuged at 150 x g for 10 min at room temperature, platelet-rich plasma was removed, and platelets were isolated from platelet-rich plasma by using the method published by Castaldi and Smith (9). Remaining platelet-poor blood was further centrifuged at 2000 x g for 15 min at room temperature and platelet-poor plasma was removed and stored at -20°C until analyzed for 11-dehydro-TXB2. Total lipids of platelets and EDTA-treated plasma were extracted with chloroform:methanol (1:1, by vol) containing 10 mg butylated hydroxytoluene/L (Labco, Melbourne) and 10 mg 17:0 phospholipid (diheptadecanoyl) and 17:0 triacylglycerol (triheptadecanoin)/L (Nu-Chek-Prep Inc, Elysian, MN) as internal standards as reported previously (5). The total platelet phospholipid, plasma phospholipid, and triacylglycerol fractions were separated by thin-layer chromatography. The methyl esters of the fatty acids of the platelet and plasma phospholipid and plasma triacylglycerol fractions were prepared by saponification with potassium hydroxide (0.68 mol/L in methanol) followed by transesterification with boron trifluoride in methanol (5). The fatty acid compositions of platelet and plasma phospholipids and plasma triacylglycerol were determined by gas-liquid chromatography as described previously (5).
Plasma 11-dehydro-TXB2concentration
The concentration of 11-dehydro-TXB2 in platelet-poor plasma was measured by using an enzyme immunoassay method with commercially available kits (Cayman Chemical Company, Ann Arbor, MI) as described elsewhere (10).
Plasma hemostatic factors
The following coagulation and fibrinolysis indexes were determined by using the ACL 200 system with commercially available kits (Coulter/IL Ltd, Milan, Italy) as described by Messmore (11): prothrombin time, fibrinogen, activated partial thromboplastin time, factor VII activity, plasminogen, and antithrombin III in citrated plasma
Agonist-induced in vitro whole-blood platelet aggregation
In vitro citrated whole-blood platelet aggregation stimulated by collagen (2 mg/L), arachidonic acid (1 mmol/L), and ADP (8 and 17 µmol/L) was measured as maximal aggregation (
at 5 min) and rate of aggregation (slope, /min) by using a 2-channel automatic whole-blood aggregometer (model 540VS; Chrono-log Corporation, Havertown, PA) as reported by Ingerman-Wojenski and Silver (12).
Plasma -tocopherol concentrations
EDTA-treated plasma (300 µL) was deproteinized with 300 µL ethanol containing 0.2 g all-rac--tocopheryl acetate/L as the internal standard. After extraction with 300 µL petroleum ether and evaporation of the solvent, the residue was reconstituted in 60 µL acetonitrile:dichloromethane:methanol (7:2:1). The concentration of -tocopherol was resolved by reversed-phase HPLC (model LC-10 AD; Shimadzu, Kyoto, Japan) and quantified by spectrofluorometric detection as published by Catignani and Bieri (13).
Statistical analyses
Statistical analyses were performed with the STATVIEW software program (Abacus Concepts Inc, Berkeley, CA). Descriptive statistics were initially performed. Analysis of variance (ANOVA) was used to establish whether differences existed within dietary groups. If a significant difference was found, a multiple-comparison test was performed with Bonferroni and Dunn post hoc tests to analyze differences between day 0 and day 14, day 0 and day 42, and day 14 and day 42. Comparison between the 2 dietary groups on day 42 was done by two-factor ANOVA using Bonferroni and Dunn post hoc tests. Values are reported as means ± SDs in all tables and as means ± SEMs in all figures unless specified otherwise. P values were two-tailed and a value <0.05 was considered significant.
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RESULTS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Dietary intake
There were no significant differences in mean daily intake of total energy; intake of protein, carbohydrate, and fat as a percentage of total energy; and intakes of cholesterol, fiber, vitamins, minerals, and trace elements between diet periods in either the moderate-ALA or high-ALA diet group (Table 2). Dietary fatty acid intakes are shown in Table 3. LA and ALA intakes during the moderate-ALA diet were 13.1 and 3.7 g/d, respectively, and during the high-ALA diet were 17.4 and 15.4 g/d, respectively.
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-tocopherol between diet periods in either the moderate-ALA or high-ALA diet group (Table 4). There were also no significant differences in indexes examined in full blood, hemostatic factors, or in vitro agonist-induced whole-blood platelet aggregation between diet periods in either group (Table 5 and Table 6).
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, the proportions of EPA and total n-3 PUFAs and the n-3:n-6 in platelet phospholipids were significantly higher on day 42 than on day 0 or day 14 in the high-ALA diet group (P < 0.01) and significantly higher on day 42 than on day 14 in the moderate-ALA diet group (P < 0.05). There was a 2.5-fold increase in EPA with the high-ALA diet compared with a 0.5-fold increase with the moderate-ALA diet. The ratio of AA to EPA was significantly lower on day 42 than on day 0 or day 14 in the high-ALA diet group (P < 0.01) and significantly lower on day 42 than on day 14 in the moderate-ALA diet group (P < 0.05). In the high-ALA diet group, the proportion of 22:5n-3 was significantly higher on day 42 than on day 0 or day 14 (P < 0.001). Compared with day 42 in the moderate-ALA diet group, ALA and EPA were significantly higher and the ratio of AA to EPA was significantly lower on day 42 in the high-ALA diet group. The total PUFA proportion was significantly lower on day 42 than on day 14 in the moderate-ALA diet group. The proportion of LA was significantly higher on day 14 than on day 0 or day 42 in the moderate-ALA diet group. The proportions of 22:4n-6 and 22:5n-6 were significantly lower on day 42 than on day 14 or day 0 in the high-ALA diet group. Additionally, compared with day 42 in the moderate-ALA diet group, proportions of 22:4n-6 and 22:5n-6 were significantly lower on day 42 in the high-ALA diet group. There were no significant differences between diet periods in the proportion of 22:6n-3.
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). The differences in fatty acid composition between the different ALA-based diets were similar to the changes seen in the platelet phospholipids. However, ALA was significantly higher on day 42 than on day 0 or day 14 in the high-ALA diet group (P < 0.05) and significantly higher on day 42 than on day 14 in the moderate-ALA diet group (P < 0.05). Additionally, proportions of ALA on day 42 in the high-ALA diet group were significantly higher than on day 42 in the moderate-ALA diet group (P < 0.05). There was a more than 4-fold increase in EPA with the high-ALA diet compared with a 1.8-fold increase with the moderate-ALA diet.
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). The changes in PUFAs were similar to the changes described above for plasma phospholipids. In both the high- and moderate-ALA diet groups, ALA was significantly higher on day 42 than on day 0 or day 14 (P < 0.05), with a larger increase in the high-ALA diet group (from 1% to 7% of total fatty acids). This increase was accompanied by a decrease in LA. The proportion of EPA was significantly higher on day 42 than on day 0 or day 14 in the high-ALA diet group, but there was no significant difference in the moderate-ALA diet group. The proportion of cis 18:1n-9 and total monounsaturated fatty acids was significantly higher and that of total PUFAs was significantly lower on day 42 than on day 14 in the moderate-ALA diet group because canola oil contains a high proportion of monounsaturated fatty acids and a low proportion of PUFAs.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The results showed that increased dietary ALA from either canola or linseed oil led to a significant increase in the proportion of EPA, total n-3 fatty acids, and the n-3:n-6 and to a decrease in the ratio of AA to EPA in platelet and plasma phospholipids and plasma triacylglycerols. The proportion of 22:5n-3 in platelet phospholipids and plasma lipids was significantly higher and proportions of 22:4n-6 and 22:5n-6 in platelet phospholipids were significantly lower after the high-ALA diet than at baseline. Proportions of LA and ALA in platelet and plasma phospholipids and plasma triacylglycerols after consumption of the experimental diets reflected the differences in the amounts of these fatty acid in the diets. However, these alterations did not cause any significant changes in atherosclerotic or thrombotic risk factors. This might have been due to the relatively short duration (4 wk) of the study and the formation of too little EPA.
Similar effects of ALA from canola or linseed oil on the amount of EPA in platelet phospholipids and plasma lipids were reported previously by others (14–17). Chan et al (14) and Allman et al (18) found that amounts of 22:5n-3 in platelets were significantly increased after 18 d of a linseed oil–based diet. No consistent results have been reported previously by other investigators on the effect of dietary ALA on the n-6 PUFA profile of platelet phospholipids and plasma lipids. Decreased AA concentrations in platelet phospholipids were observed by Kwon et al (19) and Mutanen et al (17) after 8 and 4 wk of canola oil–based diets, respectively. On the other hand, Mantzioris et al (15) reported no differences in AA concentrations in platelet phospholipids and plasma lipids after a 4-wk linseed oil–based diet. Allman et al (18) found that 22:4n-6 concentrations in platelet phospholipids were significantly decreased after 23 d of a linseed oil–based diet. A summary of these studies is shown in Table 10.
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6 desaturase (21). However, the in vivo conversion of dietary ALA to EPA is not as effective in raising 20- and 22-carbon n-3 long-chain PUFAs in platelet and plasma lipids as is direct consumption of EPA from fish or supplementation with fish oil (22). Mann et al (23) reported that the EPA content of platelet phospholipids increased (from 0.4% to 1.9% of total fatty acids) after 2 wk of an Atlantic salmon diet (mean EPA intake: 847 mg/d) in 29 healthy adults (15 women, 14 men; mean age: 34.8 y). In the present study, the high-ALA diet, which contained 15.4 g ALA/d, increased the EPA content of platelet phospholipids only from 0.2% to 0.5%. The effect of plant oil–based diets in the present study and red meat (lean beef and lamb) and fish diets in the study by Mann et al (23) on platelet phospholipid EPA and docosapentaenoic acid contents are shown in Figure 1 and Figure 2. The increase in platelet phospholipid EPA content was highest with fish consumption or fish oil supplementation, moderate with linseed oil or lean red meat, and lowest with canola oil.
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6 desaturation. This is effectively shown by data from studies in which 18:4n-3, which is the product of the 6 desaturation of ALA, is fed. In one such study, the EPA content of red blood cell membrane phospholipids was significantly increased from 0.8% to 1.1% when 32 stroke patients consumed a diet supplemented with blackcurrant seed oil, which is rich in 18:4n-3 and 
-linolenic acid (the diet contained 7.5% blackcurrant seed oil, 50% soybean oil, and 42.5% medium-chain triacylglycerols), for 3 wk compared with a 100%–soybean oil diet and a 50%–soybean oil + 50%–medium-chain triacylglycerol diet (24). In another study, the EPA contents of triacylglycerol, cholesteryl ester, and phospholipids of guinea pig liver were significantly higher after guinea pigs were fed a diet containing 10% blackcurrant seed oil for 40 d compared with 10% walnut oil (which contains ALA) (25). A similar result was also found in rats (26). The main dietary source of 18:4n-3 (blackcurrant seed oil) may also be a viable source of n-3 PUFAs, particularly for vegetarian groups; however, neither this PUFA nor ALA led to significant increases in 22:6n-3 in plasma and platelet lipids in short-term studies. Because the formation of 22:6n-3 from 22:5n-3 also requires a 6 desaturase, it is likely that none of the intermediate n-3 PUFAs (18:3 to 22:5) will be effective tissue sources of 22:6n-3 compared with dietary 22:6n-3. In a previous study of vegetarian males (3), 22:6n-3 was found in both platelet and plasma phospholipid fractions (0.9% and 2% of total fatty acids, respectively) of vegans despite the lack of 22:6n-3 in their diet; a similar result was found by Phinney et al (27). These results suggest that 22:6n-3 can be endogenously synthesized from the parent fatty acid ALA in humans, although this appears to be a slow process. Alternatively, it is possible that some rare vegetables or plants contain long-chain n-3 PUFAs (28). It may be useful to conduct a longer-term study with diets high in ALA to determine after what period of time plasma or platelet contents of 22:6n-3 increase; alternatively, it may be necessary for vegans and lactoovovegetarians to consume other sources of 22:6n-3 (algae-derived) to improve their 22:6n-3 contents.
No significant difference in plasma TXB2 produced by collagen stimulation of platelet-rich plasma between a canola oil–based diet and a safflower- or sunflower oil–based diet was observed at 8 wk by Kwon et al (19) or at 4 wk by Mutanen et al (17). Kwon et al (19) reported that collagen-induced in vitro whole-blood platelet aggregation was significantly reduced after 3 wk of a canola oil–based diet compared with a safflower oil–based diet. Mutanen et al (17) found that ADP- and collagen-stimulated in vitro platelet aggregation in platelet-rich plasma were not significantly different after 24 d of a canola oil–based diet compared with a sunflower oil–based diet. In 2 other studies, collagen-induced in vitro platelet aggregation in platelet rich-plasma was significantly decreased as the ratio of ALA to LA increased (18, 20). A larger trial population and a longer time period may be needed to detect effects of ALA-enriched diets from plant sources on in vitro agonist-induced platelet aggregation (in whole blood or platelet-rich plasma) and plasma TXB2 concentrations.
Freese and Mutanen (29) also found no significant differences in plasma fibrinogen concentrations and antithrombin III and factor VII activities between different ALA-based diets. In the present study, there were no significant differences in prothrombin time, activated partial thromboplastin time, or plasminogen activities with the different ALA diets. Moreover, Freese et al (20) also found that the dietary ratio of ALA to LA had no effect on antithrombin III activity. In contrast, dietary supplementation with fish oil has been reported to lower plasma fibrinogen concentrations (30, 31).
Cunnane et al (16) reported that plasma total and LDL-cholesterol concentrations were significantly lower in 10 healthy young adults (aged 25 ± 3 y) after 4 wk of ALA supplementation (linseed oil–based muffin; 9.0 g ALA/d) than after a low-ALA control diet (canola oil–based muffin; 1.4 g ALA/d). Watkins et al (TR Watkins, AC Tomeo, ML Struck, L Palumbo, ML Bierenbaum, unpublished observations, 1994) reported a similar result when 13 hyperlipemic subjects (mean age: 56 y) ate 6 slices of linseed oil–based bread daily (containing 4 g ALA/d) for 3 months: serum total and LDL-cholesterol concentrations were significantly lower than at baseline. In another study, plasma total and LDL-cholesterol concentrations were significantly reduced after 18 d of either a canola oil–based [9.5 g ALA/d; ratio of saturated to monounsaturated to polyunsaturated fatty acids (S:M:P) = 5:20:10] or a sunflower oil–based (1 g ALA/d; S:M:P = 7:7:22) diet than after a mixed-fat diet (1.4 g ALA/d; S:M:P = 14:15:7) (32). In the present study, no significant differences between the different ALA diets were observed with respect to plasma total cholesterol, triacylglycerol, LDL-cholesterol, or HDL-cholesterol concentrations. This may have been due to the habitually low saturated fatty acid and high PUFA content of the diets of the vegetarian population in the present study; during the study period the ratio of PUFAs to saturated fatty acids was essentially maintained despite the significantly different ratio of ALA to LA. In the other studies reported above, the subjects were omnivores and their plasma total and LDL-cholesterol concentrations may have decreased as a result of increases in the dietary ratio of PUFAs to saturated fatty acids. These results indicate that ALA and LA have a parallel effect on blood lipid and lipoprotein lipid concentrations. Supplementation with n-3 PUFAs from marine sources consistently results in decreases in plasma triacylglycerol concentrations (29, 33), whereas this was not true with ALA in the present study, probably because the amount of EPA produced from ALA was too low.
The results of this study indicate that canola and linseed oils have a similar effect on the fatty acid profile of platelet phospholipids and plasma lipids. The use of ALA from vegetable oils (canola and linseed) as a dietary fat for daily food preparation may have a beneficial effect on increasing the n-3 PUFA content of platelet phospholipids and plasma lipids in vegetarian populations. Because such small amounts of EPA and other long-chain n-3 PUFAs are produced after ALA-rich diets, it is clear that the 2 main sources of n-3 PUFAs (plants and fish) do not have equivalent biological effects in humans.
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FOOTNOTES |
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2 Supported by Meat Research Cooperation, Meadow Lea Foods Ltd, and Melrose Laboratories Pty Ltd, Australia.
3 Address reprint requests to A Sinclair, Department of Food Science, RMIT University, GPO Box 2476V, Melbourne, Victoria 3001, Australia. E-mail: sinclair{at}rmit.edu.au.
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F. Thies, G. Nebe-von-Caron, J. R Powell, P. Yaqoob, E. A Newsholme, and P. C Calder Dietary supplementation with eicosapentaenoic acid, but not with other long-chain n-3 or n-6 polyunsaturated fatty acids, decreases natural killer cell activity in healthy subjects aged >55 y Am. J. Clinical Nutrition, March 1, 2001; 73(3): 539 - 548. [Abstract] [Full Text] [PDF]
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