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Articles

Corn and Sesame Oils Increase Serum -Tocopherol Concentrations in Healthy Swedish Women¹

Marie Lemcke-Norojärvi^*2, Afaf Kamal-Eldin, Lars-Åke Appelqvist, Lena H Dimberg, Margareta Öhrvall^* and Bengt Vessby^*

^* Clinical Nutrition Research, Department of Public Health and Caring Science/Geriatrics, Uppsala University, Uppsala, Sweden and Department of Food Science, Swedish University of Agricultural Sciences, Uppsala, Sweden

²To whom correspondence should be addressed at Uppsala University, Department of Public Health and Caring Science/Geriatrics, Clinical Nutrition Research Unit, P.O. Box 609, SE-751 25 Uppsala, Sweden. E-mail: marie.norojarvi{at}geriatrik.uu.se

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
We studied the effects of dietary intervention with three vegetable oils (Linola, corn or sesame oil, all good sources of -tocopherol) on absolute and relative concentrations of - and -tocopherol in human serum. The oils contained only small amounts of linolenic acid but varying amounts of oleic and linoleic acids, and they had different concentrations of -tocopherol. Forty healthy female students (mean age 26 y) were randomly assigned to one of three groups and consumed a diet that contained one of the three oils for 4 wk. Refined oils were distributed as ingredients in specially prepared buns, in margarine or as dressing. Serum tocopherols, serum lipoproteins and plasma malondialdehyde concentrations were measured. The -tocopherol concentrations normalized to serum lipids increased significantly in the corn and sesame oil groups (P < 0.01), and the -/-tocopherol ratios decreased significantly from baseline concentrations in all groups (P < 0.05). The -tocopherol concentrations did not change during the diet period in any of the three groups. Serum cholesterol, serum apolipoprotein B and plasma malondialdehyde concentrations decreased significantly only in the Linola oil group (P < 0.05). These data show that a moderately modified natural diet that contains both - and -tocopherol increases the serum -tocopherol concentration in healthy women without affecting the serum -tocopherol concentration.

KEY WORDS: • vegetable oils • serum lipids • -tocopherol • -tocopherol • humans

	INTRODUCTION

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Coronary heart disease (CHD)³ is the major cause of complications and death in the Western world. Increased plasma concentrations of total and LDL cholesterol concentrations and an increased LDL/HDL ratio in plasma are among the important risk factors for development of CHD (Assman 1993 , Martin et al. 1986 ). Oxidation of LDL is considered to play an important role in the initiation of atherosclerosis (Steinberg et al. 1989 ), and circulating vitamin E may protect LDL against oxidative modification (Esterbauer et al. 1992 ). The main forms of vitamin E in the diet are the - and - tocopherols, and vegetable oils are among the richest sources of these vitamins (Eitenmiller 1997 , Parker et al. 1989 ). In a previous study, CHD patients were found to have identical serum -tocopherol concentrations but significantly lower serum -tocopherol concentrations than healthy control subjects (Öhrvall et al. 1996 ). Similar findings were reported by other authors, suggesting a possible role of low concentrations of -tocopherol as a marker of atherosclerosis (Kontush et al. 1999 , Kristenson et al. 1997 , Messner et al. 1997 ).

Studies have shown that -tocopherol contributes as much as or more than -tocopherol to the total dietary vitamin E intake (Heinonen and Piironen 1991 , Lehmann et al. 1986 , Wyatt et al. 1998 ). Although the two tocopherols are equally absorbed from the small intestine (Traber and Kayden 1989 ), the body concentrations and bioactivity of -tocopherol are only 10–20% of those of -tocopherol, which has the highest vitamin E activity in the human body (Behrens et al. 1986 , Bieri et al. 1974 ). This difference in bioavailability (and bioactivity) was related to biodiscrimination in the liver through the involvement of an -tocopherol–binding protein that preferentially binds -tocopherol (Traber et al. 1989 and 1992 ). -Tocopherol is metabolized and excreted through the bile and urine (Kayden et al. 1993 , Swanson et al. 1999 ). Several studies have shown that - and -tocopherols may influence the postabsorption transport and metabolism of the other (Clement et al. 1997 , Farwer et al. 1994 , Handelman et al. 1994 , Melchert and Pabel 1998 ). In certain doses, supplementation with -tocopherol seems to significantly decrease the -tocopherol concentrations in human serum and adipose tissue, and this effect has been found to disappear gradually after cessation of supplementation (Farwer et al. 1994 , Handelman et al. 1994 ). For example, a health survey of 18,000 Germans showed that the -tocopherol concentrations were significantly reduced in persons taking supplements containing >50 mg -tocopherol/d (Melchert and Pabel 1998 ). On the other hand, -tocopherol supplements markedly increased both the - and -tocopherol concentrations in the serum and tissues of vitamin E–deficient rats (Clement and Bourre 1997 ). It is not known, however, how dietary - and -tocopherols affect the bioavailability of the other in humans when consumed through food.

The aim of the present study was to determine whether absolute and relative concentrations of - and -tocopherols in human serum are affected by enrichment of the diet with three different oils. Linola, corn and sesame oils were chosen because they are good sources of -tocopherol. The oils contained only small amounts of linolenic acid but varying amounts of oleic and linoleic acids and had different concentrations of -tocopherol, a competitor of -tocopherol retention. In addition to serum - and -tocopherol concentrations, measurements were made of serum lipoproteins and fatty acid composition, plasma malondialdehyde and the antioxidative capacity in plasma.

	MATERIALS AND METHODS

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Subjects.

After an oral invitation, 46 female veterinary students at the Swedish University of Agricultural Sciences, Uppsala, volunteered to participate in this single-blind parallel study. After randomization but before the start of the diet period, four students declined to participate and one student was excluded due to diabetes mellitus. During the study, one subject decided to drop out before the end of the diet period. Thus, 40 subjects, with a mean age of 26 y, completed the study: 16 in the Linola, 13 in the corn and 11 in the sesame oil groups. There were no significant differences among the groups in clinical characteristics of the participants at baseline (Table 1 ). Two subjects were smokers. Six persons who reported that they normally supplemented their diet with multivitamin preparations containing -tocopherol were asked to abstain from this practice 1 wk before and throughout the study period. The study was approved by the Ethical Committee of the Medical Faculty of Uppsala University.

Fully refined Linola oil (a low linolenic genotype of linseed, developed through classic plant breeding) was produced by United Grain Growers (Winnipeg, Manitoba, Canada) in a pilot plant (Rotterdamsche Margarine Industry Romi B.V., Vlaardingen, the Netherlands). Fully refined corn oil of commercial quality was obtained from Karlshamns AB (Karlshamn, Sweden), and fully refined sesame oil was obtained from Henry Lamotte GmbH (Bremen, Germany). Margarine (80% fat) was prepared by Van den Bergh Foods (Helsingborg, Sweden) from an oil phase composed of 60% of each of the oils with 40% of a solid fat consisting of interesterified palm and coconut oils. The fatty acid composition and the - and -tocopherol concentrations in the oils and margarines used are presented in Table 2 . Buns were made from the following ingredients (g/100 g): water (271), yeast (39), oil (139), salt (2), syrup (15), crushed wheat grains (70) and wheat flour (464). Each bun weighed 54 g, contained 7.5 g oil and had the following composition: 51 g protein, 147 g fat, 396 g carbohydrate and 23 g fiber per kg (13.04 MJ/kg).

View this table: [in this window] [in a new window]   Table 2. Proportions of fatty acids and concentrations of - and -tocopherol in the Linola, corn and sesame oils and margarines123

After randomization into three groups, the participants were asked to eat three buns every day for 4 wk, which was equivalent to 22.5 g oil/d. They were also provided weekly with margarine from the oil allocated, as well as with pure oil to use freely for spread, dressing and cooking. The participants were asked not to make any changes in their lifestyle and to keep a 3-d food record during the diet period, with the assistance of a meal model, Matmallen (Håglin et al. 1995 ), a means of estimating amounts of food consumed. Two persons did not complete their 3-d food record: one from the Linola group and one from the sesame oil group. The 3-d food records were coded and converted into energy and nutrients with a computerized version of MATs 4.0 (Rudans Lättdata, Västerås, Sweden), using the database PC-Kost from the Swedish National Food Administration, first version (1996). All participants also completed a questionnaire about their medical background and dietary and smoking habits.

Analytical methods.

Blood samples were taken from an antecubital vein after an overnight fast, at baseline and after the 4-wk diet period. The - and -tocopherol concentrations were assayed by HPLC with a fluorescence detector as previously described (Öhrvall et al. 1993 ). The tocopherol concentrations are reported as the concentration divided by the concentration of cholesterol and triglycerides in serum, as suggested by Thurnham et al. (1986 ).

VLDL, LDL and HDL were isolated from serum through a combination of preparative ultracentrifugation (Havel et al. 1955 ) and precipitation with a sodium phosphotungstate and magnesium chloride solution (Seigler et al. 1981 ). Serum triglyceride and cholesterol concentrations were measured in serum and in the isolated lipoprotein fractions by enzymatic methods with an Instrumentation Laboratories (Lexington, MA) Test Cholesterol Trinder model 181618-80 and an Instrumentation Laboratories Test Triglyceride model 181610-60 in a Monarch apparatus. The concentrations of apolipoprotein (apo)B and apoA-I in serum were determined through immunoturbidimetry in a Monarch apparatus with the use of monospecific polyclonal antibodies against apoB and apoA-I, respectively (Orion Diagnostica, Espoo, Finland). The fatty acid composition in serum was determined with gas-liquid chromatography of the fatty acid methyl esters after separation of the phospholipids and cholesterol esters by thin layer chromatography, as described previously (Boberg et al. 1985 ).

Plasma concentrations of malondialdehyde (MDA) were measured with the HPLC system described by Öhrvall et al. (1994 ). The antioxidative capacity was measured with an enhanced chemiluminescent antioxidant assay essentially according to Whitehead et al. (1992 ). This technique is based on a measurement of light emission when a chemiluminescent substrate such as luminol is oxidized in a reaction catalyzed by horseradish peroxidase. The light emission is sensitive to interference by radical scavenging antioxidants, and the time period of light suppression will be related to the amount of antioxidant present. Light emissions from the chemiluminescent reaction were measured with a luminometer (1251 Luminometer; BioOrbit, Turku, Finland).

Statistics.

All variables analyzed were continuous on an interval scale and are shown as means with standard deviations. When a skewed distribution was observed, a logarithmic transformation was made. Comparisons were made within and between groups. The significance of changes over time within groups was established by Student’s paired t test. To determine the significance of differences between groups, a Student’s unpaired t test was used. The data were analyzed with use of the SAS program (SAS Institute, Cary, NC), and P-values < 0.05 were regarded as significant.

	RESULTS

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The mean daily energy and the mean protein, total fat and carbohydrate intakes were similar for all groups (Table 3 ). However, the sesame oil group had a significantly lower intake of polyunsaturated fatty acids than the Linola oil group (Table 3) , as a result of the difference in fatty acid composition between the two oils (Table 2) . The mean intakes of - and -tocopherol from buns, oils and margarines, calculated from the 3-d food record, are presented in Table 4 . These results show that the corn oil group had the highest intake of both - and -tocopherols (Table 2) . The additional intakes of - and -tocopherols from other food sources were assumed to be similar in all groups. The mean body weight remained unchanged during the study period in all three groups.

View this table: [in this window] [in a new window]   Table 4. Estimated daily intakes of - and -tocopherols from the buns, oils and margarines in Linola, corn and sesame groups calculated from the 3-d food records12

View larger version (17K): [in this window] [in a new window]   Figure 1. Serum concentrations of -tocopherol (A) -tocopherol (B) and the -/-tocopherol ratio (C) at baseline and after 4 wk of dietary intervention. Values are means ± SD; Linola oil group, n = 16; corn oil group, n = 13; and sesame oil group, n = 11. Serum tocopherols, normalized to serum lipids equal serum tocopherol (µmol/L)/[serum (cholesterol + triglycerides) (mmol/L)]. *Different from baseline, P < 0.05, **P < 0.01, ***P < 0.001.

View larger version (22K): [in this window] [in a new window]   Figure 2. Plasma concentrations of malondialdehyde (MDA) at baseline and after 4 wk of dietary intervention. Values are means ± SD; Linola oil group, n = 16; corn oil group, n = 13; and sesame oil group, n = 11. *Different from baseline, P < 0.05.

	DISCUSSION

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To the best of our knowledge, this is the first study on the effects of vegetable oil intervention on - and -tocopherol concentrations in humans. There were no significant differences in the -tocopherol concentrations after the study period in any of the groups (Fig. 1A ), which conforms with a previous finding in rats that an increased intake of -tocopherol did not decrease the serum -tocopherol concentration (Kamal-Eldin et al. 1995 ). In the Linola oil group, the serum -tocopherol concentration did not increase significantly, a finding compatible with the relatively low intake concentration (Table 4) . The habitual diet for the Swedish population is currently based on rapeseed oil and margarines (Sanders 2000 ), and the concentrations of tocopherols in one sample of refined rapeseed oil were 25.2 and 36.1 mg/100 g for - and -tocopherols, respectively (Kamal-Eldin et al. 2000 ), which means that Linola oil contains less tocopherols than rapeseed oil (Table 2) . The postdiet concentrations of -tocopherol increased (P = NS) in the Linola group and significantly in the corn and sesame oil groups (Fig. 1B ), causing a significant decrease in the -/-tocopherol ratio in all groups (Fig. 1C ). The fact that Linola oil, despite its lower concentrations of tocopherols (Table 2) , increased the -tocopherol concentration compared with the baseline "rapeseed oil" (Fig. 1B ) suggests that the amount of oils given in this study (as oils, margarines and buns) may be higher than the average amounts in the participants’ usual diet. Although the contents of -tocopherol differed substantially between the corn oil and the sesame oil (corn oil contains three times as much -tocopherol as the sesame oil; Table 2 ), both oils increased serum -tocopherol to the same concentration (Fig. 1B ). This finding may be explained by the results of Kamal-Eldin et al. (1995 and 2000 ), who showed that via an unknown mechanism, certain lignans in sesame oil increase serum -tocopherol concentrations in rats. Two major lignans were present in the sesame oil used in this study: sesamin (155 mg/100 g oil) and episesamin (169 mg/100 g oil). The concentrations of these lignans in the sesame oil margarine were 126 and 137 mg/100 g, respectively. The average daily intake of these lignans from the oil and margarine was 100 mg. No phenolic compounds were detected in the Linola or corn oil or corresponding margarines.

In view of the fact that -tocopherol competes with -tocopherol in binding to the tocopherol-binding protein, so that -tocopherol is eliminated through the bile and urine (Kayden et al. 1993 , Swanson et al. 1999 , Wechter et al. 1996 ), it was notable that the -tocopherol concentration increased significantly in the corn oil group, although the corn oil contained substantial amounts of -tocopherol (Table 2) and lacked lignans. This might indicate that - and -tocopherols did not compete significantly in this case (Table 4) . This result might be of relevance to protection against CHD, because some observational studies have indicated that low plasma concentrations of -tocopherol are associated with an increased prevalence of CHD (Gey et al. 1991 ), whereas other studies have shown that -tocopherol concentration is significantly lower in CHD patients than in control subjects (Kontush et al. 1999 , Kristenson et al. 1997 , Öhrvall et al. 1996 , Messner et al. 1996) and suggest that low concentrations of -tocopherol might be a more sensitive risk index for atherosclerosis than low concentrations of -tocopherol. Kushi et al. (1996 ) found that in postmenopausal women, the intake of vitamin E from food (with a high proportion of -tocopherol) was inversely associated with a risk of death from CHD, whereas this association was not seen for the intake of supplemental vitamin E (-tocopherol).

Because the study subjects were young women with normal concentrations of blood lipids, significant lipid-lowering effects by intervention oils were not expected and were not observed with the sesame and corn oils; thus the Linola oil caused a significant decrease in the serum cholesterol and apoB concentrations (Table 5) . Compared with the corn and sesame oils, the Linola oil contained a higher proportion of linoleic acid 18:2(n-6), namely 70% (Table 2) , which might explain the reduction in the serum cholesterol and apoB concentrations (Howard et al. 1995 ). Prior studies in rats have shown that sesame lignans (episesamin and/or sesamin) lower serum and liver cholesterol concentrations by inhibiting absorption and synthesis of cholesterol (Hirose et al. 1991 ). We did not find a cholesterol-lowering effect in the present study of healthy women with a daily intake of 100 mg episesamin and sesamin, possibly due to the young age of the participants or to the fact that larger amounts of these compounds are required to attain similar results in humans (Hirata et al. 1996 ). Furthermore, the fatty acid composition of serum lipids after the dietary intervention was found to reflect the fatty acid composition in the oils used (Table 6) . The decrease in oleic acid and (n-3) fatty acids reflects the change from rapeseed oil, which is usually used in margarines and oil in Sweden (Sanders 2000 ), to the three test oils used in this study (Table 2) .

One way of estimating the oxidative status of plasma lipids is to determine the concentration of MDA. Paradoxically, plasma MDA was significantly lowered by the Linola oil, which contained the highest proportion of unsaturated fatty acids (Table 2) . This result is in contradiction with results from in vitro studies, in which a higher degree of oxidation was found for polyunsaturated fatty acids than for monounsaturated fatty acids (Esterbauer et al. 1991 ). Our results are, however, in agreement with the previous findings that MDA was inversely correlated to the content of linoleic acid in the serum lipoprotein lipids in a healthy reference population (Öhrvall et al. 1994 ). However, MDA is only one product of the peroxidation process (Halliwell et al. 1993 ) and should preferably be combined with other specific products, such as F₂-isoprostanes, to obtain a clearer pattern of the lipid peroxidation (Basu 1998 ).

In conclusion, we have found that moderate modification of a natural diet through intervention with vegetable oils that contain both - and -tocopherol increased the serum -tocopherol concentration without affecting the serum -tocopherol concentration in healthy women. Whether the serum -tocopherol concentrations in CHD patients can be modified with the diet and whether such an effect would help to prevent the development of atherosclerosis remain to be investigated.

	ACKNOWLEDGMENTS

 
We are grateful to United Grain Growers (Winnipeg, Manitoba, Canada), Karlshamn AB (Karlshamn, Sweden) and Henry Lamotte (GmbH, Bremen, Germany) for gifts of Linola® corn and sesame oils and to Van den Bergh Foods (Helsingborg, Sweden) for preparing the margarines and for analyzing the fatty acids in the oils and margarines. Special thanks are due to Lars Berglund and Rawya Mohsen (Department of Public Health and Caring Science/Geriatrics) for performing the statistical analyses.

	FOOTNOTES

 
¹ Supported by the Swedish Council for Forestry and Agricultural Research ([SJFR] grant 50.0496/98) and Kalsec Inc. (Kalamazoo, MI).

³ Abbreviations used: BMI, body mass index; CHD, coronary heart disease; MDA, malondialdehyde.

Manuscript received June 1, 2000. Initial review completed July 31, 2000. Revision accepted December 11, 2000.

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