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Departments of
* Nutrition and
Epidemiology, Harvard School of Public Health, Boston MA 02115 and
** Centro Centroamericano de Población, Universidad de Costa Rica, San Pedro de Montes de Oca, Costa Rica
3To whom correspondence should be addressed. E-mail: hcampos{at}hsph.harvard.edu.
| ABSTRACT |
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KEY WORDS: fatty acids palm oil soybean oil myocardial infarction cardiovascular disease
Palm oil and soybean oil are the 2 most used cooking oils worldwide (1). Palm oil is less expensive than soybean oil and has more diverse uses in nonfood industries. The palm oil industry is a major source of income for many people in the rural areas of many developing countries (2). Most of the production (84%) occurs in South East Asia (1), and most of the palm oil (8490%) is used in food preparation. Palm oil is consumed mainly in developing countries (1) that are undergoing an adverse nutritional transition and in which morbidity and mortality due to cardiovascular disease (CVD)4 are increasing (35). Soybean oil, produced mainly in the United States, Brazil, and Argentina as a secondary product of the soybean protein meal industry, is rich in cis-PUFAs. Because soybean oil is usually partially hydrogenated, it has a high content of trans-PUFAs. The atherogenic potential of palm oil was proposed because it is low in polyunsaturated and high in saturated fat (3650%), predominantly palmitic acid (68). High palm oil and coconut oil intakes were proposed as potential explanations for the high cardiovascular disease rates in Singapore compared with Hong Kong (5). Studies in humans and animals showed that palm oil per se compared with safflower oil or sunflower oil increased plasma total and LDL cholesterol (913), and compared with safflower oil, palm oil caused atherosclerosis in monkeys (14). Other studies showed no or the opposite effect (15). In contrast, soybean oil and other oils rich in PUFAs are considered beneficial for cardiovascular health (16,17). Nevertheless, a large proportion of soybean oil is partially hydrogenated, a procedure that generates trans fatty acids, which are associated with increased risk of coronary heart disease (18,19). Despite the worldwide economic and health importance of palm oil and soybean oil, there are no epidemiologic studies assessing the association between these oils and cardiovascular endpoints. We conducted a large population-based incident case-control study to determine whether the use of palm oil compared with other cooking oils was associated with the risk of nonfatal acute myocardial infarction (MI). Unlike soybean oil, which is mostly imported, palm oil is produced and used widely for cooking in Costa Rica (7,20).
| SUBJECTS AND METHODS |
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75 y old on the day of their first MI, and 3) were physically or mentally unable to answer the questionnaire. Enrollment took place while cases were in the hospitals step-down-unit. Cases were matched by age (±5 y), sex, and area of residence to population controls who were randomly identified with the aid of data from the National Census and Statistics Bureau of Costa Rica. Because of the comprehensive social services provided in Costa Rica, all persons living in the catchment area had access to medical care without regard to income. Therefore, control subjects came from the source population that gave rise to the cases and were not likely to have been having undiagnosed cardiovascular disease because of poor access to medical care. Control subjects were ineligible if they had ever had an MI or if they were physically or mentally unable to answer the questionnaires. Participation was 98% for cases and 88% for controls. All subjects gave informed consent on documents approved by the Human Subjects Committee of the Harvard School of Public Health and the University of Costa Rica. Data collection. Trained personnel visited all cases and controls at their homes for the collection of dietary and health information, anthropometric measurements, and biological specimens. Sociodemographic characteristics, smoking, socioeconomic status, physical activity, and medical history data were collected during an interview using a questionnaire with close-ended questions. Self-reported diabetes and hypertension were validated using the recommended definitions by the Expert Committee on the Diagnosis and Classification of Diabetes Mellitus (25), and the Third Joint National Committee on Detection, Evaluation, and Treatment of High Blood Pressure (26). We computed sensitivities, specificities, and positive and negative predictive values from the questionnaire data and measurements of blood pressure and blood sugar. These variables showed that self-reported assessments of diabetes and hypertension were reliable in this population (21).
Dietary assessment. We collected dietary data using a FFQ that was developed and validated specifically to assess nutrient intake among the Costa Rican population (22,27). The FFQ asked subjects to specify the principal type of oil used for cooking and frying at home and the duration of use. The type of oil was confirmed by visual inspection of the oil containers at the time of the home visit. The cooking oils were coded and periodic assessments of the fatty acid compositions of samples from the market in Costa Rica were performed at Harvard School of Public Health using a GLC procedure described elsewhere (27).
The fatty acid composition of the most widely used oils and margarines in Costa Rica were incorporated into the food composition database. The proportions of saturated, monounsaturated, polyunsaturated, and trans fatty acids in palm oil (mostly consumed in solid form) were 49.7, 39.0, 9.6, and 1.7%, respectively. Partially hydrogenated soybean oil brands used in Costa Rica between 1994 and 1998 were high in trans fatty acids (22 ± 4%) and low in
-linolenic acid (1.8 ± 0.3%). After changes in the edible oil industry in Costa Rica, the trans fatty acid content of soybean oil was reduced to 5 ± 3%, and the
-linolenic acid content increased to 5.1 ± 0.7%. The trans fatty acid content of palm oil did not change over the years, and was 1.5 ± 0.3% in our recent analyses. The trans fatty acid contents of other cooking oils analyzed were relatively low; they were 0.17 ± 0.34% for sunflower oil, 0.11 ± 0.35% for corn oil, 0.06 ± 0.13% for canola oil, and 0.02 ± 0.04% for olive oil. The fatty acid compositions of the palm and soybean oils consumed by the Costa Rican population are comparable to those of the palm and soybean oils consumed by other populations (7,28).
Adipose tissue fatty acids.
A subcutaneous adipose tissue biopsy was collected from the upper buttock, stored in a cooler with ice packs at 4°C, transported to the fieldwork station within 4 h, and stored at 80°C until analysis. Fatty acids from adipose tissue were quantified by GLC as described previously (27). Fatty acids in subcutaneous adipose tissue reflect long-term intake (29,30) and are preferred in case-control studies over other biomarkers of fatty acid intake (31). In the Costa Rican population, adipose tissue linoleic acid,
-linolenic acid, and trans fatty acids were found to be excellent biomarkers of intake (22,27). We used cis- and trans-PUFAs in adipose tissue to identify and confirm the presence of fatty acids that are likely to be responsible for the observed results.
To avoid the potential for recall bias among cases, data were collected as close to the diagnosis of MI as possible. For instance, data collection was completed within 2 wk of discharge from the hospital for 73% of the cases. A matched population control was recruited within 10 ± 11 d of the recruitment of a case. The mean (SD) interval between completion of data collection for a case and completion of data collection for a matched control was 12 (16) d.
Statistical analysis.
SAS Software version 8.00 (SAS Institute) was used for all statistical analyses. Subjects who were missing values (n = 326) for major confounders were excluded, leaving 2111 cases and 2111 matched population controls for the final analysis. If a case or control was missing data on key variables, the whole pair was deleted. If among deleted controls there was one that had complete data and matched a deleted case by age, sex, and area of residence, the 2 were rematched and added to the data set to avoid power loss. Thus, 32 cases and 32 rematched controls with complete data were included in the final data set for a total of 2111 case-control pairs. Because individual nutrients were correlated with total energy intake, each was adjusted for energy intake using regression methods (22,32). We also estimated the amount of energy consumed as fat and expressed it as a percentage of daily total energy intake. Because of the matched design, the significance of differences in the distributions of categorical variables by case-control status was tested using McNemars test; continuous variables were tested by the paired t test, if normally distributed, or by the Wilcoxon signed rank test, if not normally distributed. Differences were considered significant at P
0.05.
Because the content of trans fatty acids in soybean oil brands used before 1998 was >16%, and <10% for those used after 1998, we grouped together all brands before 1998 (mean trans content 22%) and those after 1998 (mean trans content 5%). We then divided soybean oil users into 2 groups, namely, users of soybean oil with high trans content (22%) and users of soybean oil with less trans fat (5%). This is because our earlier analyses (18) showed that a high intake of trans fat, which in this population comes mainly from partial hydrogenation of soybean oil, is associated with increased risk of MI. If not adjusted for, high trans fat intake in the reference group could confound any association between palm oil and MI. There were fewer users of oils other than palm oil or soybean oil (n = 977); therefore, they were grouped together in a category called other oils, which included consumers of sunflower oil (53%), corn oil (27%), olive oil (10%), canola oil (3%), and a few less common oils (7%). We thus modeled a 4-level categorical variable (palm oil, soybean oil with 22% trans fat, soybean oil with 5% trans fat, and other oils) as the main predictor of MI. In the analyses, palm oil was compared with soybean oil with 22% trans fat, soybean oil with 5% trans fat, or other oils as reference categories.
We assessed variables for confounding first by determining their univariate associations with MI and the type of oil used for cooking; second, we investigated the change in odds ratios (OR) when a given variable was entered into the conditional logistic regression model. In these analyses, continuous variables were analyzed as quintiles of nondietary or energy-adjusted dietary variables. We assessed the possibility of an association between palm oil consumption and MI, first univariately, then with established CVD risk factors only, and finally with dietary confounders assessed with an FFQ. Multivariate OR and 95% CI were obtained for palm oil using 22% trans-soybean oil, 5% trans-soybean oil, or other oils as the referent group. All 3 analyses used a fixed sample size of 2111 case-control pairs and the same set of covariates.
To determine whether there was a dose-response relation between the use of palm oil and MI, we reanalyzed the data using the estimated daily amount of palm oil (expressed as a percentage of total energy intake) consumed at home. This analysis was made for 926 subjects who provided their food preparation recipes for use in estimating the intake of palm oil. We used the median to divide palm oil users into 2 equal groups (low and high palm oil users) and then compared them to subjects who did not use palm oil (0% of energy from palm oil). Thus we had a 3-level categorical variable in which those below and above the median of palm oil intake were compared with non-palm oil users. Because mixing of cooking oils is not common in Costa Rica and the variable for intake of soybean oil was negatively correlated with that of palm oil, we only used the palm oil variable in the multivariate dose-response analyses. Multivariate unconditional OR and 95% CI were estimated for the low and high palm oil users relative to non-palm oil users. These unconditional logistic analyses controlled for age (quintiles), sex, area of residence, smoking (never, past, <20 cigarettes/d, and
20 cigarettes/d), history of diabetes, history of hypertension, abdominal obesity (quintiles), physical activity (quintiles), income (quintiles), intake of alcohol (never, past, and tertiles of current drinkers), total energy (quintiles), fiber (quintiles), dairy, and meat products (continuous), and trans fat in adipose tissue (quintiles).
We performed additional analyses to further explore the effects of potential confounders such as smoking, area of residence,
-linolenic acid in adipose tissue, intake of folate, alcohol, and vitamin B-6 by stratifying the analyses by these variables. In these analyses, we used unconditional logistic regression with matching variables in the model and the other variables modeled as continuous covariates. We computed the Hosmer-Lemeshow statistic to test for goodness of fit.
| RESULTS |
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-tocopherol,
-tocopherol, and adipose tissue concentrations of most carotenoids were significantly lower in cases than in controls (data not shown). The distribution of potential confounders was examined by the type of oil used for cooking (Table 2). Use of palm oil was associated with the area of residence in both cases and controls. Most palm oil users were of low socioeconomic status as shown by their income and level of education, were physically more active, and were more likely to be current smokers than users of other cooking oils. Palm oil was used more frequently (P < 0.01) for cooking by cases (30%) than by controls (23%). Compared with soybean oil and other oil users, palm oil consumers had higher intakes of saturated fat and lower intakes of total polyunsaturated fat and
-linolenic acid. The difference in intake of saturated fat was due mainly to palmitic acid.
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Compared with other types of cooking oils that are very low in trans fatty acids, palm oil was significantly associated with increased risk for MI (OR = 1.53; 95% CI: 1.271.84). Adjustment for dietary and nondietary confounders as in the preceding models attenuated the association appreciably (OR = 1.23; 95% CI: 0.991.52), mainly because of the high proportion of smokers among palm oil users (29%) compared with users of other cooking oils (14%).
In a multivariate dose-response analysis, we found that relative to non-palm oil users (0% energy from palm oil), the risk of MI among low (median intake = 3.5% of energy) and high (median intake = 7.4% energy) palm oil users was 1.27 (95% CI: 0.841.94) and 1.48 (95% CI: 0.952.33), respectively (data not shown).
We also determined whether total fat or saturated fat intake was associated with the risk of MI. As in our previous study (23), the total amount of fat consumed was not associated with MI (OR for the 5th vs. 1st quintile = 1.02; 95% CI: 0.801.30) but saturated fat was significantly associated with the risk of MI (OR for the 5th vs. 1st quintile = 1.36; 95% CI: 1.051.75) (data not shown).
We determined the percentage of difference in PUFA in adipose tissue between palm oil consumers and users of other cooking oils (Fig. 1). Compared with palm oil users, linoleic acid,
-linolenic acid, and trans fat were higher among users of soybean oil and other oils. Adipose tissue linoleic acid and
-linolenic acid were highest in users of soybean oil containing 5% trans fatty acids. In contrast, trans fat was highest among users of soybean oil with 22% trans fat. Although linoleic acid in adipose tissue of consumers of other oils was comparable to that of users of soybean oil with 5% trans fat, users of other oils were lower in
-linolenic acid. These adipose tissue fatty acid profiles are consistent with the self-reported major oils used for cooking and indicate long-term intake. Most cooking oil users reported consuming oils for a relatively long period of time e.g., 17 ± 8 y for palm oil, 12 ± 8 y for soybean oil with high trans fat, 8 ± 8 y for soybean oil with less trans fat, and 5 ± 6 y for users of other oils.
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| DISCUSSION |
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Our data support concerns about the potential for atherogenesis with the use of palm oil. Although our population study did not address the mechanism by which palm oil may increase the risk of MI, we speculate that it does so in part by leading to an increased intake of saturated fat (
3% of energy/d), an established CVD risk factor (17,23). In our previous analyses, we showed that in Costa Rica, a high intake of saturated fat was associated with an increased risk of MI (23). We further showed that palmitic acid was less potent than other saturated fatty acids but because it was consumed in large quantities, it was likely to have a large population attributable risk (23). It is noteworthy that adjustments for other food sources of saturated fat had little effect on this association, whereas adjustment for total saturated fat intake attenuated the association between palm oil and soybean oil. In addition, consumption of dairy and meat products is relatively lower in Costa Rica than in Westernized countries; thus, the bulk of saturated fat would be from vegetable oils.
The low content of linoleic and
-linolenic acids in palm oil could have contributed to the observed positive association between palm oil and MI. Linoleic acid and
-linolenic acid, as well as other (n-3) and (n-6) fatty acids, protect against coronary heart disease (16,17,33). Linoleic acid lowers total and LDL cholesterol and may improve insulin sensitivity (17,33).
-Linolenic acid may protect against MI by inhibiting platelet aggregation and thrombosis, reducing blood pressure, and preventing cardiac arrhythmias. These effects can be achieved directly by
-linolenic acid or through its conversion to long-chain (n-3) fatty acids, including eicosapentaenoic acid and docosahexaenoic acid (16,17,33). If trans fatty acids were eliminated from soybean oil, as is the current trend in Costa Rica, the amount of available
-linolenic acid in soybean oil would be higher and the beneficial effects of this oil compared with palm oil might also be greater.
The other oils, mainly sunflower oil, also were protective compared with palm oil. Although the trans fatty acid content of adipose tissue of users of other oils was comparable to that of users of soybean oil with less trans fatty acids, their
-linolenic acid content was lower. It is possible that this lower
-linolenic acid accounts in part for the difference in OR when palm oil is compared with soybean oil (OR = 1.33; 95% CI: 1.081.63) or other oils (OR = 1.23; 95% CI: 0.991.52).
There were no significant differences (OR = 1.14; 95% CI: 0.841.56) between palm oil and soybean oil with high trans fatty acids content. This is likely to be due to the increase in risk of MI in the reference group that is attributable to the high trans fatty acids and low
-linolenic acid in the soybean oil. Partial hydrogenation of soybean oil destroys
-linolenic acid, increases the trans fatty acid content of soybean oil, and may therefore raise the risk of MI among consumers of partially hydrogenated soybean oil. Our previous studies showed that trans fatty acids increase risk (18), whereas (n-3) fatty acids such as
-linolenic acid (16) protect against the risk of MI in this population. These data also suggest that the potentially positive characteristics of palm oil such as its high oleic acid content (39%) are not sufficient to compensate for the deleterious effects of its attendant high saturated fat and low concentrations of linoleic acid and
-linolenic acid.
Because part of the reason for increased risk of MI among palm oil users may be attributed to low intake of polyunsaturated fat, and because palm oil is the cheapest oil available to most people in developing countries, replacing palm oil with unsaturated cooking oils may not be a practical solution in the short term. This is because the palm oil industry is a major source of employment and income for many people who might not be able to afford other oils. Despite these social concerns, which could be addressed in the long term by redirecting palm oil to other nonhuman food uses, it is important to attend to the health concerns of palm oil consumers. The increase in the risk of MI associated with palm oil use that was demonstrated in this study is important to public health. Production and consumption of palm oil are widespread and on the increase (1,34), especially in those developing countries in which diseases of affluence are also increasing (3,3537). In Costa Rica, for instance, CVD is a leading cause of death, with ischemic heart disease accounting for 47.2% of CVD deaths (38).
In the dose-response analysis, we noted that the difference in risk of MI between low (3.5% energy) and high (7.4% energy) palm oil users was not substantial, suggesting that the type of oil used for cooking and frying is more important than the amount of oil used. It is therefore possible that recommending a decrease in intake of palm oil may not have a significant effect on public health unless it is replaced with polyunsaturated oils. It would be valuable to establish per capita consumption levels in countries that produce or import large amounts of edible palm oil. It would also be of value to determine the levels of saturation and concentration of antioxidants in the most common brands of palm oil used for cooking in other developing countries. In our study, palm oil users had significantly lower amounts of antioxidants and
-linolenic acid compared with soybean oil users (39).
These data show that compared with soybean oil users, the risk of nonfatal acute MI in palm oil users is high (863%). Because palm oil is used widely, especially in developing countries in which the cardiovascular disease burden is on the increase, projected increases in palm oil consumption could greatly affect public health. Programs that lead to the reduction in consumption of palm oil and partially hydrogenated soybean oil or to the availability of inexpensive palm oil with improved fatty acid composition, or the substitution of palm oil with unsaturated cooking oils are warranted. One potential short-term intervention is to replace saturated fat with cis-polyunsaturated (n-3) and (n-6) fatty acids in palm oil by mixing it with other unsaturated oils.
| ACKNOWLEDGMENTS |
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| FOOTNOTES |
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2 Supported by grants HL49086 and HL60692 from the National Institutes of Health. ![]()
4 Abbreviations used: CVD, cardiovascular disease; FA, fatty acid; MI, myocardial infarction; OR, odds ratio. ![]()
Manuscript received 2 June 2005. Initial review completed 28 June 2005. Revision accepted 2 August 2005.
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