Background The role of dietary antioxidant vitamins in preventingcoronary heart disease has aroused considerable interest becauseof the knowledge that oxidative modification of low-densitylipoprotein may promote atherosclerosis.
Methods We studied 34,486 postmenopausal women with no cardiovasculardisease who in early 1986 completed a questionnaire that assessed,among other factors, their intake of vitamins A, E, and C fromfood sources and supplements. During approximately seven yearsof follow-up (ending December 31, 1992), 242 of the women diedof coronary heart disease.
Results In analyses adjusted for age and dietary energy intake,vitamin E consumption appeared to be inversely associated withthe risk of death from coronary heart disease. This associationwas particularly striking in the subgroup of 21,809 women whodid not consume vitamin supplements (relative risks from lowestto highest quintile of vitamin E intake, 1.0, 0.68, 0.71, 0.42,and 0.42; P for trend = 0.008). After adjustment for possibleconfounding variables, this inverse association remained (relativerisks from lowest to highest quintile, 1.0, 0.70, 0.76, 0.32,and 0.38; P for trend = 0.004). There was little evidence thatthe intake of vitamin E from supplements was associated witha decreased risk of death from coronary heart disease, but theeffects of high-dose supplementation and the duration of supplementuse could not be definitively addressed. Intake of vitaminsA and C did not appear to be associated with the risk of deathfrom coronary heart disease.
Conclusions These results suggest that in postmenopausal womenthe intake of vitamin E from food is inversely associated withthe risk of death from coronary heart disease and that suchwomen can lower their risk without using vitamin supplements.By contrast, the intake of vitamins A and C was not associatedwith lower risks of dying from coronary disease.
There is growing evidence that the oxidative modification oflow-density lipoprotein (LDL) may be critical to the developmentof atherosclerosis.1,2,3 Oxidized LDL is present in atheroscleroticplaques4; the oxidation of LDL appears to enhance the uptakeof LDL by macrophages, thereby encouraging the formation offoam cells and the development of fatty streaks1; and increasedsusceptibility to such oxidation is associated with greaterseverity of carotid atherosclerosis.5 The inhibition of atherosclerosisin laboratory animals by antioxidants such as probucol,6 butylatedhydroxytoluene,7and vitamin E8 provides further evidence ofa role for oxidative processes in the development of atherosclerosis.
Epidemiologic studies also indicate that antioxidants may havea role in preventing the development of coronary heart disease.Some studies indicate an inverse association between the intakeof vitamin E and coronary heart disease,9,10 whereas otherssuggest that vitamin C11 or provitamin A carotenoids12 may beprotective. The Iowa Women's Health Study, a prospective cohortstudy of postmenopausal women, provided an opportunity to examinewhether the dietary intake of antioxidants is related to mortalityfrom coronary heart disease.
Methods
The study participants were recruited from a random sample of99,826 women 55 to 69 years of age who had valid Iowa driver'slicenses in 1985. These women were sent a 16-page questionnairein January 1986; 41,836 women returned it, and they form thecohort under study. The mortality rates of the cohort membersand those who did not respond to the mailing were similar, exceptthat smoking-related causes of death were more common amongthe women who did not respond.13
Dietary Assessment
The base-line questionnaire included questions concerning factorspertinent to the risk of coronary heart disease. A 127-itemfood-frequency questionnaire similar to that used in the 1984survey of the Nurses' Health Study14 was also included. Thelist of foods was augmented by questions asking the respondentto specify the type of fat used, the brand of cooking oil, thenames of other regularly consumed foods, and the brand namesof multivitamin preparations and breakfast cereals, all of whichwere potential sources of vitamins. There were also questionsabout the current use and dosage of supplements of specificvitamins (such as vitamins A and E).
To evaluate the reliability of the questionnaire, we comparedthe vitamin intake in a subgroup of 44 women with their meanintake estimated from five 24-hour dietary-recall interviews.15With regard to the total intake of vitamins A, E, and C, thecorrelation coefficients for the two instruments were 0.56,0.55, and 0.76, respectively. With regard to vitamin intakeexcluding that from supplements, the corresponding coefficientswere 0.14, 0.79, and 0.53. The validity of estimates of vitaminintake from food-frequency questionnaires has been examinedin comparison with plasma levels of beta carotene (r = 0.30)and alpha-tocopherol (r = 0.41) in the Nurses' Health Study.16
Study Design
Women were excluded from the study if they had not reached menopause(569 women); if the food-frequency questionnaire had 30 or moreitems left blank (2751 women); or if their reported energy intakewas implausibly high or low (<600 or >5000 kcal per day)(317 women). Women were also excluded if they reported at baseline that a physician had told them they had angina or heartdisease or had had a heart attack (3713 women). This left 34,486women who were eligible for follow-up.
We followed the women annually by consulting the State HealthRegistry of Iowa, which collects information on deaths in Iowa.Deaths were also reported in response to follow-up questionnairesmailed in 1988, 1990, and 1992, and were identified by linkingwomen who did not respond with the National Death Index. Womenwere considered to have died of coronary heart disease if thecause of death was assigned to codes 410 through 414 or 429.2of the International Classification of Diseases, 9th Revision.Although we did not validate this coding, other studies havefound that the validity of death certificates listing coronaryheart disease as the cause of death is relatively high.17,18Many known risk factors for coronary heart disease were alsoevident in this cohort.19
The study design was approved by the Committee on the Use ofHuman Subjects in Research of the University of Minnesota.
Statistical Analysis
The length of follow-up for each woman was calculated as thenumber of days from the completion of the base-line questionnaireto the date of death or December 31, 1992, whichever came first.Among the women eligible for follow-up, 242 died of coronaryheart disease.
We studied the association of vitamin intake with mortalityfrom coronary heart disease. Dietary intake of vitamin A asretinol or provitamin A carotenoids was also assessed, becausecarotenoids have antioxidant properties but retinol does not.Because vitamins can be ingested from both foods and supplements,exposure to each vitamin was studied in three ways. First, thetotal intake of the vitamin from both food and supplements wasdetermined. Second, intake of the vitamin from food alone wasdetermined; this analysis was limited to women who had no supplementalintake of that vitamin. Finally, analyses of supplemental intakewere conducted. Because in early 1986 supplemental vitamin Awas derived almost exclusively from retinol, the analyses ofsupplemental vitamin A intake were not partitioned accordingto whether the vitamin was derived from retinol or carotene.
The association of vitamins A, E, and C with death from coronaryheart disease was examined primarily by proportional-hazardsregression analysis. Values for vitamin intake were categorizedin quintiles or other categories as appropriate, and the mortalityrate from coronary heart disease in each category was comparedwith that in the lowest intake category. The initial analysesexamined associations adjusted for age. The analyses were alsoadjusted for other factors that were significant predictorsof death from coronary heart disease or that substantially alteredthe risk estimates associated with vitamin intake. These includedtotal energy intake, history of hypertension, history of diabetesmellitus, body-mass index (calculated as the weight in kilogramsdivided by the square of the height in meters), waist-to-hipratio, history of cigarette smoking, level of physical activity,estrogen-replacement therapy, and alcohol intake.
The relative risk associated with a given category of vitaminintake was estimated by calculating the exponent of the proportional-hazardsregression coefficient for that level of intake. P values fortrend were determined, with each level of exposure weightedaccording to its median value.
Results
As reported previously,19 recognized risk factors for coronaryheart disease were evident in this cohort. Women who reportedthe following risk factors on the base-line questionnaire hadhigher age-adjusted risks of death from coronary heart diseasethan women without the risk factors: hypertension (relativerisk, 2.21; 95 percent confidence interval, 1.70 to 2.86), diabetesmellitus (relative risk, 4.72; 95 percent confidence interval,3.47 to 6.42), and current smoking (relative risk, 3.16; 95percent confidence interval, 2.37 to 4.21). Women were at decreasedrisk if they reported a high degree of physical activity (relativerisk as compared with women with a low degree of physical activity,0.49; 95 percent confidence interval, 0.35 to 0.71) or the useof estrogen-replacement therapy (relative risk as compared withnonusers, 0.72; 95 percent confidence interval, 0.55 to 0.95).Higher body-mass indexes and higher waist-to-hip ratios werealso associated with higher age-adjusted risks of death fromcoronary heart disease (P<0.001 for both).
Table 1 shows the distribution of these risk factors accordingto the intake of vitamins E and C, both overall and from foodonly; the patterns observed for vitamin A were similar to thosefor vitamin E and are not shown. The quintiles with greateroverall intake of vitamins were associated with lower mean waist-to-hipratios, smaller proportions of current smokers, and larger proportionsof women who were physically active or used estrogen-replacementtherapy. Similar patterns were seen with regard to the intakeof vitamins E and A from food sources alone. With regard tovitamin C derived from food, higher intake was associated withsmaller proportions of current smokers and greater physicalactivity but also with larger proportions of women with hypertensionand diabetes mellitus.
Table 1. Association of Various Base-Line Factors with the Risk of Coronary Heart Disease in Postmenopausal Women, According to Intake of Vitamins E and C.
Table 2 shows age- and energy-adjusted relative risks of deathfrom coronary heart disease according to overall vitamin intake.With regard to the intake of vitamin A, retinol, and carotenoids,there were suggestions of inverse associations. In the caseof vitamin A, the association showed an inconsistent dose response,with an elevated risk in the second quintile of intake (relativerisk as compared with the lowest quintile, 1.46) and a decreasedrisk in the fourth quintile (relative risk, 0.68). Overall vitaminE intake also appeared to be inversely associated with the riskof death from coronary heart disease; there were significantlydecreased risks in the third (relative risk, 0.53) and fourth(relative risk, 0.61) quintiles of intake, but the overall trendwas not statistically significant. Overall intake of vitaminC was not associated with the risk of death from coronary heartdisease.
Table 2. Relative Risks and 95 Percent Confidence Intervals (CI) of Death from Coronary Heart Disease (CHD), According to Quintile of Antioxidant Intake from Food and Supplements, among 34,486 Postmenopausal Women, 1986–1992.
Associations of overall vitamin intake with the risk of deathfrom coronary heart disease after adjustment for potential confoundersare also shown in Table 2. The suggested inverse associationswith the intake of vitamins A and E, retinol, and carotenoidwere weakened after multivariate adjustment. There was a suggestionof a positive association between overall vitamin C intake andthe risk of death from coronary heart disease (relative riskin highest vs. lowest quintile, 1.49; 95 percent confidenceinterval, 0.96 to 2.30).
Vitamin E intake was inversely associated with the risk of deathfrom coronary heart disease among women who did not take vitaminE supplements (relative risks from lowest to highest quintileof intake, 1.0, 0.68, 0.71, 0.42, and 0.42; P for trend = 0.008)(Table 3). In contrast, no association was observed for vitaminA, retinol, carotenoids, or vitamin C derived from food. Afteradjustment for potential confounders, the inverse associationwith vitamin E derived from food remained (relative risks fromlowest to highest quintile of intake, 1.0, 0.70, 0.76, 0.32,and 0.38; P for trend = 0.004).
Table 3. Relative Risks and 95 Percent Confidence Intervals (CI) of Death from Coronary Heart Disease (CHD), According to Quintile of Antioxidant Intake from Food among Postmenopausal Women Who Did Not Take Supplemental Vitamins, 1986–1992.
Table 4 shows the association of supplemental vitamin intakewith the risk of death from coronary heart disease. A relativelylow intake (1 to 5000 IU per day) of supplemental vitamin Awas associated with a decreased risk of death from coronaryheart disease (age-adjusted relative risk, 0.67; 95 percentconfidence interval, 0.47 to 0.95), but higher intake was not.Nor were the data on vitamin E and C supplements consistentwith an inverse association. Multivariate analyses also suggestedno association of supplemental vitamin intake with the riskof death from coronary heart disease.
Table 4. Relative Risks and 95 Percent Confidence Intervals (CI) of Death from Coronary Heart Disease (CHD), According to Category of Antioxidant Intake from Supplements, among 34,486 Postmenopausal Women, 1986–1992.
That the intake of vitamin E derived from food, but not fromsupplements, was inversely associated with mortality from coronaryheart disease suggested that vitamin E consumed in food maybe a marker for other dietary factors associated with the riskof coronary heart disease. We conducted further analyses withadjustment for various factors, including the intake of carotenoids,folic acid, dietary fiber, linoleic acid, linolenic acid, totalpolyunsaturated fatty acids, meat, and other foods and foodgroups. Adjusting for these factors did not substantially alterthe inverse association observed with vitamin E. For example,after adjustment for linoleic acid intake, the relative risksof death from coronary heart disease associated with levelsof vitamin E derived from food, from the lowest to the highestquintile of intake, were 1.0, 0.71, 0.79, 0.35, and 0.44 (Pfor trend = 0.019). This was the largest attenuation of theassociation observed after adjustment for any of the factorsexamined.
Table 5 shows a multivariate analysis of the association ofthe risk of death from coronary heart disease with the intakeof specific foods that are dietary sources of vitamin E. Intakeof the following was inversely associated with the risk of deathfrom coronary heart disease: margarine (P for trend = 0.048),nuts and seeds (P for trend = 0.016), and mayonnaise or creamysalad dressings (P for trend = 0.069). Additional adjustmentfor vitamin E weakened the associations, suggesting that theycould be attributed in part to the intake of vitamin E.
Table 5. Multivariate Adjusted Relative Risks and 95 Percent Confidence Intervals (CI) of Death from Coronary Heart Disease (CHD), According to Quartile of Intake of Certain Foods Containing Vitamin E, among 19,411 Postmenopausal Women Who Did Not Take Vitamin Supplements, 1986–1992.
We investigated the weak positive association of vitamin C withcoronary heart disease further by excluding deaths during thefirst two years of follow-up, since women who were ill earlyin the study may have taken vitamin C. However, this exclusiondid not substantially alter the association (multivariate adjustedrelative risks from lowest to highest quintile of intake, 1.0,1.20, 0.95, 1.09, and 1.69; P for trend = 0.017). The findingsfor vitamins A and E were also unaffected by the exclusion ofearly deaths.
Discussion
This prospective study of postmenopausal women provides evidenceof an inverse association of coronary heart disease with theintake of vitamin E from food. Women in the highest quintileof vitamin E intake had less than half the risk of death fromcoronary heart disease of women in the lowest quintile. Thisinverse association was not seen for the intake of vitamin Efrom supplements. There was also a suggestion of an inverseassociation between mortality from coronary heart disease andoverall vitamin A intake, but this association was no longerapparent after adjustment for other risk factors. Vitamin Cappeared, if anything, to be positively associated with therisk of death from coronary heart disease.
The inverse association of vitamin E intake with the risk ofdeath from coronary heart disease is generally consistent withthe findings of a growing number of epidemiologic studies. Prospectivestudies of 39,910 male health professionals9 and 87,245 femalenurses10 demonstrated that the risk of incident coronary diseasewas approximately 40 percent lower in those who consumed vitaminE supplements than in those who did not. In the study of malehealth professionals, no association was observed between vitaminE derived from food and coronary heart disease.9 A nonsignificantinverse association with vitamin E from food sources was suggestedin the study of nurses.10 In a cohort of 2226 middle-aged men,Meyer et al.20 also reported a substantially reduced risk ofdeath from coronary disease among users of vitamin E supplements.
In support of an inverse association of vitamin E intake fromfood with mortality from coronary heart disease, we have previouslyreported21 that nut consumption is inversely associated withcoronary mortality in this cohort, a finding confirmed by theseupdated analyses; nuts are among the more concentrated foodsources of vitamin E. An inverse association of nut consumptionwith mortality from coronary heart disease was also reportedin a prospective study of Seventh-Day Adventists.22 The intakeof other foods that provide vitamin E, including margarine andmayonnaise, also appeared to be inversely associated with coronarymortality in the present study. Although these foods are sourcesof vitamin E (and fat) in the diet, they are distinct in otherrespects. For example, nuts and seeds also contain protein andcarbohydrates, whereas margarine does not, and mayonnaise andcreamy salad dressings may contain cholesterol. Adjustment forvitamin E intake weakened these associations, suggesting theywere due in part to the vitamin E content of the foods. Theinverse association seen in the case of margarine contrastswith observations in the Nurses' Health Study,23 which attributeda positive association with coronary disease to the intake oftrans fatty acids.
In a prospective study in Finland, Knekt et al.24 also reporteda substantial inverse association (relative risk in highestvs. lowest third of intake, 0.35) between vitamin E derivedfrom food and coronary mortality among 2385 women; a similarinverse association was reported among the 2748 men in theircohort. They also reported a nonsignificant inverse associationbetween margarine intake and coronary mortality among men, butnot among women. As in our study, this association was diminishedafter adjustment for the intake of antioxidant vitamins.
Although we cannot eliminate the possibility that vitamin Ederived from food is a marker for other dietary factors relatedto the risk of coronary heart disease, we could not identifyany such factor. It is clear from the analyses presented here,for example, that provitamin carotenoids and vitamin C are notassociated with a decreased risk. The intake of folate, anothervitamin concentrated in vegetables that may decrease the riskof atherosclerosis,25,26,27 was also not inversely associatedwith mortality from coronary heart disease in this cohort (datanot shown). Other dietary factors that are associated with vitaminE include linoleic acid, linolenic acid, total polyunsaturatedfatty acids, and dietary fiber. However, the inverse associationbetween the risk of death from coronary heart disease and theintake of vitamin E derived from food remained after we adjustedthe analysis for these and other dietary factors.
Vitamin E intake is also associated with a more healthful cardiovascularrisk profile (Table 1). Although the inverse association remainedafter adjustment for several risk factors, the levels of riskfactors were reported by the patients, and there may be someresidual confounding. We also could not take into account potentialconfounders such as blood lipid levels or the use of nonsteroidalantiinflammatory medications. However, vitamin E intake is unlikelyto be associated with blood lipid levels.9
As for our failure to observe an inverse association betweensupplemental intake of vitamin E and coronary mortality, wehad no information on the duration of supplement intake. Inother studies,9,10 an inverse association was found among personswho had been taking supplemental vitamin E for at least twoyears. Including recent, short-term users among long-term userswould weaken the overall effect of supplemental vitamin E intakeif such an effect were limited to long-term users. In addition,relatively few women in our cohort consumed high doses of supplementalvitamin E. This would compromise the ability of our study todetect associations with mortality from coronary heart diseaseif such an effect is most apparent at high doses. Although theresults of a Finnish trial of supplementation with beta carotene(20 mg per day) and alpha-tocopherol (50 mg per day) among smokersalso do not support an effect of these supplements on the riskof death from coronary heart disease,28 the dosages may havebeen too low to affect mortality.
As with many epidemiologic studies of diet, inaccuracies ofmeasurement are a limitation. The random misclassification ofdietary habits generally decreases the ability to detect associationsbetween diet and disease.29 Thus, the observed inverse associationsof coronary mortality with vitamin E derived from food are allthe more striking. The effect of changes in diet during follow-upalso creates difficulties in interpreting these findings definitively.In the case of carotenoids, there has been increased awarenessof the potential of beta carotene to prevent cancer and thegreater availability of supplements containing beta carotene.
Given these caveats, the findings presented here do not constitutedefinitive evidence of an inverse association between vitaminE intake and mortality from coronary heart disease. Clarificationof the effects of supplemental vitamin E in an older populationappears warranted, given our findings and those of the Finnishtrial.28 More definitive evidence of an effect of supplementalvitamin E must await the results of clinical trials such asthe Women's Health Study,30 which is testing this associationin younger women. However, that study was not designed to testthe association of either vitamin E intake from food or dietarychanges with the risk of coronary heart disease. Our findingssuggest that modifying dietary habits to increase vitamin Eintake may also be worthwhile in preventing coronary heart disease.This study of older women provides information that is importantin planning intervention trials in the elderly. The observationswith regard to vitamins A and C are similarly not definitive,but they suggest that increased intake of these vitamins isnot likely to lower the risk of death from coronary heart disease.
Supported by a research grant (CA-39742) from the National Institutesof Health.
Source Information
From the Division of Epidemiology, University of Minnesota School of Public Health, Minneapolis (L.H.K., A.R.F., P.J.M.); the Department of Epidemiology and Public Health, University of Miami, Miami (R.J.P.); the Department of Epidemiology, University of Pittsburgh, Pittsburgh (Y.W.); and the Bowman Gray School of Medicine, Wake Forest University, Winston-Salem, N.C. (R.M.B.).
Address reprint requests to Dr. Kushi at the Division of Epidemiology, University of Minnesota School of Public Health, 1300 S. Second St., Suite 300, Minneapolis, MN 55454-1015.
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