Journal of the American College of Nutrition, Vol. 24, No. 4, 286-293 (2005)
Published by the American College of Nutrition
Saturated and Cis- and Trans-Unsaturated Fatty Acids Intake in Rural and Urban Costa Rican Adolescents
Rafael Monge-Rojas, MS,
Hannia Campos, PhD and
Xinia Fernández Rojas, PhD
Costa Rican Institute for Research and Education on Nutrition and Health (INCIENSA), Ministry of Health, Tres Ríos (R.M.-R.)
Department of Nutrition, Harvard School of Public Health, Boston, Massachusetts, Centro Centroamericano de Población (H.C.)
School of Human Nutrition (X.F.R.), Universidad de Costa Rica, San Pedro de Montes de Oca, Costa Rica
Address reprint requests to: Rafael Monge-Rojas, INCIENSA, Apartado 4-2250, Tres Ríos, Costa Rica. E-mail:rmonge{at}inciensa.sa.cr
 |
ABSTRACT
|
|---|
Objective: The purpose of this study is to determine whether intake of saturated fatty acids and cis- and trans-unsaturated fatty acids is associated with an urban compared to a rural lifestyle, and whether these associations are responsible for differences in plasma lipid concentrations.
Methods: Two hundred seventy-five adolescents, aged 12 to 19 years, living in rural and urban areas of San José, Costa Rica, were included in the study. All participants completed three-day food records, provided a fasting blood sample, and carried out a modified Harvard Step Test.
Results: Compared to rural, urban adolescents reported higher intakes of energy-adjusted individual and total saturated fatty acids, total n-3, total n-6 (p < 0.05). Compared to rural, urban adolescents had higher intake of 18:1 (3.65 vs. 3.25, p = 0.0001) and 18:2 (0.62 vs. 0.80, p = 0.001) trans fatty acids, as well as lower intake of carbohydrate (p < 0.05). Palm shortening was the main source of saturated fat (32%), and partially hydrogenated soybean oil used for cooking was the main source of n-3 fatty acids (33%), n-6 fatty acids (33%) and trans fatty acids (34%). Compared to rural, urban adolescents had lower systolic and diastolic blood pressure and higher plasma HDL cholesterol concentration (44 vs. 40 mg/dL, p < 0.0001), but were more likely to be sedentary (68% vs. 57%, p < 0.0001). Among environmental factors, higher carbohydrate intake was a significant determinant of a lower HDL cholesterol (ß coeff = 1.45, p = 0.04), while lauric and myristic fatty acids correlated with increased LDL cholesterol (ß coeff = 3.6, 1.7, p < 0.05).
Conclusions:A diet containing less carbohydrate and less saturated fatty acids contributes to a more beneficial lipid profile in Costa Rican adolescents, but a trend towards high trans fatty acids intake, particularly in the urban area is worrisome given the well-known adverse effects of trans fatty acids.
Key words: adolescents, trans fatty acids, saturated fatty acids, rural vs. urban, dietary intake
 |
INTRODUCTION
|
|---|
Coronary heart disease (CHD) is the main cause of death in most Latin American countries, including Costa Rica [1]. Adolescents make up a significant proportionon average 21%of the general population in these countries. Also, the extent of atherosclerotic change in early years is correlated with the presence of CHD factors in adults [2,3]. Eating habits associated with CHD risk are acquired early in life and may accelerate the development of this pathology [2,3]. Therefore, developing a healthy diet in adolescents may contribute to reducing the risk of CHD in adulthood [4].
The fatty acid composition of the diet is associated with CHD risk. Some prospective cohort studies [5,6], but not all [7,8] have found a significant positive association between saturated fat intake and risk of CHD. In the Nurses Health Study [9], replacing five percent of energy from saturated fat with cis-unsaturated fats was associated with a 42 percent reduction in CHD. Similarly, trans fatty acid intake is associated with increased risk of CHD, and replacing two percent of the energy from trans fatty acids with non-hydrogenated unsaturated fats reduced the risk of CHD by 53 percent [9]. As expected, no association between trans fatty acid intake and CHD has been found in European countries were intake of trans fatty acids is low [10,11]. Using adipose biomarkers of intake, 18:2 trans fatty acids showed the highest association with CHD in population based case-control study in Costa Rica [12,13]. In contrast, both cis n-6 fatty acids (primarily linoleic acid, 18:2n-6) and cis n-3 fatty acids reduce the risk of CHD [14]. A synergistic relation between linoleic acid and alpha-linolenic acid intake has been suggested by Djoussé et al. [15], showing that the combined intake of these fatty acids may be associated with a greater reduction in the prevalence of CHD.
In an attempt to reduce the saturated content of the diet in Costa Rica, soybean oil has been replacing palm oil the last decade [16]. In 2001, the national average intake of soybean oil was four times higher than that reported in 1991 (21.1 g/d and 5.0 g/d, respectively), while palm oil intake decreased 65 percent in relation to 1991 (10.8 g/d and 31.5 g/d, respectively) [17]. Although this was expected to have a positive effect because of increased n-3 and n-6 fatty acids, recent studies show that soybean oil used for cooking in Costa Rica is partially hydrogenated [13], resulting in a lower proportion of alpha-linolenic acid and a higher proportion of trans fatty acids, than soybean oil that is not partially hydrogenated.
For the past 20 years, mortality rates for cardiovascular disease and myocardial infarction in Costa Rica have been higher in urban than in rural areas [18]. This epidemiological profile could be explainedat least in partby establishing if the determination of CHD risk factors between both areas differs from an early age. We hypothesize that adolescents living in the urban area will have a more adverse fatty acid intake (high saturated and trans fatty acids, and low polyunsaturated fatty acids) and plasma lipid profile, than those living in the rural area. We will also examine whether dietary fatty acids explain the plasma lipid rural-urban differences.
 |
MATERIALS AND METHODS
|
|---|
Study Population
Adolescents aged 12 to 19 years from San José, Costa Rica, were included in the study, as previously described [19]. Adolescents were recruited from five urban and five rural public high schools. The schools were chosen from a list of all the public high schools in San José using a proportional-size probability formula. Both parents and students gave their written consent to participate in the study according to the rules provided by the Bioethics Committee of the Costa Rican Institute for Research and Education on Nutrition and Health (INCIENSA).
Dietary Assessment
Dietary intake was determined using three-day food records [20]. The three days included one weekend day and the next or previous two weekdays (Sunday, Monday and Tuesday or Thursday, Friday and Saturday). The adolescents used a series of photographs of foods usually consumed in Costa Rica to estimate portion size while keeping the food record [21]. Food models and fresh foods were used to verify serving size.
In order to determine the contribution of the different foods to the total selected fatty acids intake, each food was classified into one of 23 possible food groups. These include: meat, fish, pork, chicken, organ meat, eggs, cold cuts, breads, breakfast cereals, margarines, palm oil shortening, butter, partially hydrogenated soybean oil, other oils (canola oil, sunflower oil, corn oil, and olive oil), rice, legumes, milk (1% and 2% fat), cheese, other dairy products (including cream cheese, sour cream, whipping cream, ice cream, butter, and lactocrema, a mixture of butter and margarine), fruits, vegetables, chocolates and candies, and other foods (including soups, pastas, sauces, condiments, nuts, and coconut).
Energy intake and total fat were calculated using the Food Processor® for Windows version 6.0 (Esha Research, Salem, Oregon), which was modified to include the nutritional value of 60 food preparations commonly consumed in Costa Rica. Fatty acid intake was estimated using a fatty acid content database (thirty-nine cis fatty acids and ten trans fatty acids isomers) for Costa Rican foods provided by Campos, H. (unpublished data, Campos Laboratory, 2002). For this study, 33 foodsmostly those sold at the schools cafeteriaswere analyzed for fatty acid content and incorporated into our database. In the database, the fatty acid content was expressed in grams per 100 grams of total fat. The cis-trans isomer content of foods was estimated using gas chromatography, as previously described by Baylin et al. [22]. To calculate fatty acid intake of each adolescent, the following formula was used: (grams of total fat in the amount of food consumed x grams of fatty acids per 100 grams of total fat)/100. The total fat content of each food was obtained with Food Processor® for Windows version 6.0 (Esha Research, Salem, Oregon). Table 1 shows the trans fatty acid content of the foods that contributed over 80 percent of total trans fatty acids to the Costa Rican adolescents diet.
Anthropometric Measurements, Blood Pressure and Physical Activity
Weight, height, blood pressure, and fitness scores were determined using the previously described methodology [23]. Fitness score was determined using the Harvard Step Test modified by Bush et al. [24]. Each adolescent stepped up and down on a platform 33 cm high, at a rate of 30 steps per minute for 4 minutes. Upon completion of the test, the heart rate was counted for a 30-second period, starting exactly 1, 2 and 3 minutes after completion. These results were then added up and classified in scoresaccording to what Bush et al. propose [24]to determine the cardiovascular fitness score of each adolescent. Scores ranged from 1 to 5. Adolescents who scored above 3 were considered sedentary.
Biochemical Analyses
Serum triacylglycerol, cholesterol, and HDL cholesterol concentrations were measured using enzymatic reagents (Randox, England) and an automatic analyzer ASCA (LSI Instruments). LDL cholesterol was calculated with the Friedwalds et al. equation [25]. Intra-assay and inter-assay coefficients of variation for total serum cholesterol were, respectively, 2.5 and 2.9 percent, and 6 and 7 percent, respectively, for HDL cholesterol. The coefficient of variation for triglycerides was less than 4 percent for these analyses.
Statistical Data
Statistical analysis was performed using the Statistical Package for Social Sciences (SPSS Inc., version 10.0 for Windows, Chicago, Illinois). Variables were checked for outliers and normality, and where necessary, transformed using the natural logarithm. Fatty acid intakes were adjusted for total energy intake by regressing the transformed variable on total energy intake as described by Willett [26]. An analysis of variance was performed using GLM procedure in SPSS to determine whether dietary intakes vary across by gender and concentrations of urbanization. The significance of the differences between male and female means and urban and rural means was assessed using the Tukey multiple comparison test. The Stepwise multiple regression procedure was used to identify those variables associated with LDL cholesterol, HDL cholesterol and triglyceride concentrations at p < 0.05. Three multivariate models were examined; in each one, we included area, gender, age, cardiovascular fitness score, and energy intake to control for the effects of these variables.
 |
RESULTS
|
|---|
Of the 300 selected adolescents, those whose parents did not provide written consent to participate in the study and those with missing serum samples were excluded (n = 25). The final sample of 275 adolescents consisted of 131 boys and 144 girls.
The general characteristics of the studied population are shown in Table 2. When compared to rural, urban adolescents had a more beneficial profile for some risk factors, but not all. For example, urban adolescents had lower systolic and diastolic blood pressure and higher HDL cholesterol concentrations yet, they were more sedentary. Urban adolescents consumed less dietary fiber, folate, and carbohydrate, but more total energy, total fat, protein and cholesterol. Likewise, urban adolescents consumed more total saturated fatty acids, trans fatty acids, n-3 and n-6 fatty acids (Table 3).
View this table:
[in this window]
[in a new window]
|
Table 2. General Characteristics and Dietary Intake in Rural and Urban Costa Rican Adolescents Aged 1218 Years1,2
|
|
View this table:
[in this window]
[in a new window]
|
Table 3. Intake of Individual Polyunsaturated Fatty Acids in Rural and Urban Costa Rican Adolescents Aged 1218 Years12
|
|
The main trans fatty acids consumed were 18:1 and 18:2, representing 77.1% and 19.3% of the total trans fatty acids consumed, respectively. Of these trans fatty acids, the most frequently consumed isomers were 18:1n-7t and 18:2tc (data not shown).
Consumption of milk, dairy products, fast foods, vegetables, breads, bakery foods, meats, sausages, eggs, fish, and partially hydrogenated soy oil was significantly higher (p = 0.000) in urban adolescents than among their rural counterparts (data not shown). The reverse was true for fruits, roots and tubers, rice, legumes, bananas, plantains and palm shortening. There were no differences in food intake by gender.
The food sources of saturated and unsaturated fatty acids in the adolescents diet are shown in Tables 4 and 5. Palm shortening, margarine, dairy and bakery products were the major sources of saturated fat in the adolescents diet. Dairy was the major contributor of lauric (65%), myristic (67%) and stearic fatty acids (24%), while palm shortening was the main contributor of palmitic acid (33%). Partially hydrogenated soybean oil was the main contributor of n-3 fatty acids (33%), n-6 fatty acids (33%) and trans fatty acids (34%). About 35% of the total trans fatty acids consumed came from naturally occurring sources (meats, 14%; milk, 9%; other dairy products, 7%, and cheese, 5%).
In the multivariate model using LDL cholesterol concentrations as a dependent variable and adjusting for area, gender, age, cardiovascular fitness score and energy intake, the increase of LDL cholesterol concentrations was associated to an increased intake of both lauric and palmitic acid, but the effect of lauric acid on LDL cholesterol concentrations was higher than that of palmitic acid (Table 6). For each one gram increase in lauric acid intake, LDL cholesterol concentrations increased 3.6 mg/dL; while, for each one gram increase in palmitic acid intake, LDL cholesterol concentrations increased 1.7 mg/dL. Overall, higher HDL cholesterol concentrations were associated to a decrease in both the cardiovascular fitness score and the carbohydrate intake.
View this table:
[in this window]
[in a new window]
|
Table 6. Regression Models with HDL Cholesterol, LDL Cholesterol and Triglyceride as Response Variables and Nutrient Intake as Explanatory Variables
|
|
 |
DISCUSSION
|
|---|
The results of this study demonstrate that urban dwellers are exposed since adolescence to sedentary lifestyles and higher intakes of saturated fat, cholesterol and trans fatty acids, in contrast to their rural counterparts. This could explain, at least in part, the larger prevalence of CHD in Costa Rican urban areas [18]. However, urban adolescent also consumed less carbohydrate, less folate, less fiber, and more polyunsaturated fat and this study cannot distinguish which of these factors or factors will be the most relevant for CHD. It is surprising that despite a general more adverse lifestyle pattern in the urban area, urban adolescents had lower diastolic and systolic blood pressure and higher HDL cholesterol, both important risk factors for CHD. Area of residence did not have an effect on total cholesterol and LDL cholesterol concentrations probably because in addition to increased saturated fatty acids, trans fatty acids and cholesterol intake in urban adolescents they also had increased intake of polyunsaturated fat which has opposite effects.
This study showed that the effect of lauric acid on LDL cholesterol concentrations in adolescents is stronger than the effect of palmitic acid, the most abundant fatty acids in the adolescents diet. Because lauric acid intake is very low compared to palmitic acid intake (2% and 67% of the total saturated fat intake, respectively), it is possible that the attributable risk associated to lauric acid intake is low. Nonetheless, Kabagambe et al. [12] have suggested that a small increase in lauric acid intake could result in a significant increase in CHD risk for Costa Rican adults, presumably because saturated fatty acids have a stronger effect on populations with lower saturated fat intakes compared to those with high intakes [12]. For example, a 1% energy increase in lauric acid is associated with a 1.9-fold increase in the risk of non-fatal acute myocardial infarction [12].
Higher HDL cholesterol concentrations are positively associated with physical activity and inversely associated with carbohydrate intake [26]. Our data show that rural adolescents (typically more active, but with lower fat and higher carbohydrate intakes) had the lowest HDL cholesterol concentrations, a pattern that resembles that of Costa Rican rural adults [27]. HDL cholesterol decreases when dietary fat is decreased [28], because high-carbohydrate intake increases endogenous triglyceride synthesis and very low-density lipoprotein secretion [29]. Our results show that for each percentage point of increase in carbohydrate intake, serum HDL cholesterol concentrations decreased by 1.5 mg/dL.
Unsaturated fats, e.g. long-chain n-3 fatty acids, have been shown to lower the risk of CHD [26], so a low intake of n-3 fatty acids, particularly in the rural area that consumes 12 g of fish per day, is worrisome. Baylin et al. [30] have reported that alpha-linolenic acid is associated with a large and significant reduction in the risk of non-fatal acute myocardial infarction in Costa Rica, suggesting that increase consumption of vegetable oils would be beneficial. Partially hydrogenated soybean oil was the primary contributor of alpha-linolenic acid in the adolescents diet; however, it is not wise to promote its consumption yet since it was also the primary source of trans fatty acids. Partially hydrogenated soybean oil intake is greater in urban areas than in rural areas, explaining the greater consumption of trans fatty acids in urban adolescents as opposed to rural adolescents, who primarily consume palm oil shortening. This suggests that the food industrys support is necessary to modify the manufacturing processes of soy oil in order to reduce its trans fatty acid content.
The intake of total trans fatty acids by urban and rural Costa Rican adolescents is very similar to that reported for adolescents in the U.S. (2.8% of total energy) and much greater than the recommended maximum intake (1% of total energy) [3133]. In the diets of both groups of adolescents, the most frequently consumed isomer was 18:1, however the percentage of total trans fatty acids from meat and dairy products was higher in Costa Rica (36%) than in the U.S. (2025%) [34].
It is well established that trans fatty acids increase the risk of MI [35]. Clinical studies show that 18:1 trans fatty acids (77% of adolescents trans fatty acids intake) adversely affect the lipoprotein profile [36]. Specifically, 18:1 trans in subcutaneous fat are higher in patients with CHD than controls [37]. Some epidemiological studies [11,38,39] have found no association between 18:1 trans fatty acids in adipose tissue and the risk of myocardial infarction, but it has been proposed that the low-adipose tissue level of these fatty acids can explain the absence of association [13]. A study by Baylin et al. [13] show that 18:2 trans fatty acids isomers had the strongest association with CHD in Costa Rica, and the relative abundance of this isomer in adipose tissue is higher in Costa Rica than in other countries [13]. Similar results have been obtained when comparing red cell membrane fatty acids in patients with primary cardiac arrest and controls [40].
Trans fatty acids derived from meat and dairy products may also be associated with CHD [41,42]. A positive association between adipose tissue trans fatty acids found exclusively in animal products (16:1n-7trans) and non-fatal acute myocardial infarction was observed in Costa Rican adults [13]. Our data show that Costa Rican adolescents consume a considerable proportion of trans fatty acids from meat and dairy products which are also major sources of saturated fat. Therefore, strategies directed at reducing consumption of meat and high-fat dairy products will be beneficial for the reduction of total trans fatty acids as well.
 |
CONCLUSIONS
|
|---|
A higher intake of saturated and trans fatty acids was associated with an urban compared to a rural lifestyle. Urban adolescents also had a higher intake of cis-n-3 and n-6 fatty acids because partially hydrogenated soybean oil was the main source of these fatty acids. Dairy and meat products were major contributors to both saturated fat and trans fatty acids. Because there was no consistent adverse pattern in urban adolescents, this study could not identify a clear rural-urban discriminating profile. However, this study provides novel information on cis and trans fatty acids in adolescents which show trends that are worrisome given the high overall content of trans fatty acids and low n-6 and n-3 fatty acids in specific areas of Costa Rica.
 |
ACKNOWLEDGMENTS
|
|---|
The authors wish to thank Xinia Siles for her help and support, and all the adolescents who participated in the study. This work was performed in partial fulfillment of the doctoral degree of Rafael Monge-Rojas at the University of Costa Rica.
Received May 19, 2004.
Accepted June 4, 2005.
 |
REFERENCES
|
|---|
- Pan American Health Organization: "Health Statistics from the Americas." Washington, DC: PAHO,2003
.
- Williams C, Hayman L, Daniels S, Robinson T, Steinberger J, Paridon S, Bazzarre T: Cardiovascular health in childhood. Circulation106
:143
160,2002
.[Free Full Text]
- Berenson G, Srinivasan S, Nicklas T: Atherosclerosis: a nutritional disease of childhood. Am J Cardiol82
:22T
29T,1998
.[Medline]
- Lytle L: Nutritional issues for adolescents. J Am Diet Assoc102
: S8
S11,2001
.
- McGee DL, Reed DM, Yano K, Kagan A, Tillotson, J: Ten-year incidence of coronary heart disease in the Honolulu Heart Program: relationship to nutrient intake. Am J Epidemiol119
:667
676,1984
.[Abstract/Free Full Text]
- Kushi LH, Lew RA, Stare FJ, Ellison CR, el Lozy M, Bourke G, Daly L, Graham I, Hickey N, Mulcaky R: Diet and 20-year mortality from coronary heart disease: The Ireland-Boston Diet Heart Study. N Engl J Med312
:811
818,1985
.[Abstract]
- Ascherio A, Rimm EB, Giovannucci EL, Spiegelman D, Stampher MJ, Willet WC: Dietary fat and risk of coronary heart disease in men: cohort follows up study in the United States. BMJ313
:84
90,1996
.[Abstract/Free Full Text]
- Pietnen P, Ascherio A, Korhonen P, Hortman AM, Willet WC, Albanes D, Virtamo J: Intake of fatty acids and risk of coronary heart disease in a cohort of Finnish men: The Alpha-Tocopherol, Beta-Carotene Cancer Prevention Study. Am J Epidemiol145
:876
887,1997
.[Abstract/Free Full Text]
- Hu FB, Willet WC: Diet and coronary heart disease: Findings from the Nurses Health Study and Health Professionals Follow-up Study. J Nutr Health Aging5
:132
138,2001
.[Medline]
- van de Vijver LP, Kardinaal AF, Couet C, Aro A, Kafator A, Steingrimsdottir L, Amorin-Cruz JA, Moreiras O, Becker W, van Amelsvoort JM, Vidal-Jessel S, Salminen I, Moschandreas J, Sigfusson N, Martins I, Carbajal A, Ytterfors A, Poppel G: Association between trans-fatty acid intake and cardiovascular risk factors. In Europe: The TRANS-FAIR Study. Eur J Clin Nutr54
:126
135,2000
.
- Aro A, Kardinal AF, Salminen I, Kark JD, Riemersma RA, Delgado-Rodriguez M, Gomez-Aracena J, Hutturnen JK, Koklmeir L, Martin BC, Martin-Moreno JH, Mazaev VP, Ringstad J, Thamm M, vant Veer P, Kok FJ: Adipose tissue isomeric trans-fatty acids and risk or myocardial infarction in nine countries. The EUREMIC Study. Lancet345
:273
278,1995
.
- Kabagambe EK, Baylin A, Siles X, Campos H: Individual saturated fatty acids and nonfatal acute myocardial infarction in Costa Rica. Eur J Clin Nutr57
:1447
1457,2003
.[Medline]
- Baylin A, Kabagambe E, Ascherio A, Spiegelman D, Campos H: High 18:2 trans-fatty acids in adipose tissue are associated with increased risk of nonfatal acute myocardial infarction in Costa Rican adults. J Nutr133
:1186
1191,2003
.[Abstract/Free Full Text]
- Ascherio A: Epidemiologic studies on dietary fats and coronary heart disease. Am J Med113
:9S
12S,2002
.
- Djoussé L, Pankow J, Eckfeldt J, Folsom A, Hopkins P, Province M, Hong Y, Ellison RC: Relation between dietary linolenic acid and coronary artery disease in the National Heart, Lung, and Blood Institute Family Heart Study. Am J Clin Nutr74
:612
619,2001
.[Abstract/Free Full Text]
- Ministerio de Salud: Encuesta Nacional de Nutrición: Fascículo Consumo Aparente. San José, Costa Rica,1996
.
- Ministerio de Salud: Encuesta Nacional de Nutrición. San José, Costa Rica,2003
.
- Roselló M, Guzmán S: Evolución de la mortalidad por enfermedad isquémica del corazón e infarto agudo de miocardio en Costa Rica, 19702001. Rev Panam Salud Pública16
:295
301,2004
.[Medline]
- Monge-Rojas R: Dietary intake as a cardiovascular risk factor in Costa Rican adolescents. J Adolesc Health28
:328
337,2001
.[Medline]
- Arauz AG: Método de registro de alimentos de tres días. In Madrigal H, Martínez H (eds): "Manual de Encuestas de Dieta." México City: Instituto Nacional de Salud Pública, pp83
98,1996
.
- Chinnock A, Sedó-Masís P: Porciones de alimentos y preparaciones comunes en Costa Rica y equivalencias del sistema de listas de intercambio. Escuela de Nutrición Humana, Universidad de Costa Rica. San José, Costa Rica,2000
.
- Baylin A, Campos H: Arachidonic acid in adipose tissue is associated with nonfatal acute myocardial infarction in the central valley of Costa Rica. J Nutr134
:3065
3099,2004
.
- Monge-Rojas R, Beita O: Prevalence of coronary heart disease risk factors in Costa Rican adolescents. J Adolesc Health27
:210
217,2000
.[Medline]
- Bush PJ, Zucherman AE, Theiss PK, Taggart VS, Horowitz C, Sheridam MJ, Walter HJ: Cardiovascular risk factor prevention in black school children: Two year results of the "Know Your Body" program. Am J Epidemiol29
:466
492,1989
.
- Friedwald WT, Levez RI, Fredrickson DS: Estimation of the concentration of low-density lipoprotein cholesterol in plasma without use of the preparative ultracentrifuge. Clin Chem18
:499
502,1972
.[Abstract]
- Willet WC: "Nutritional Epidemiology," 2nd ed. New York: Oxford University Press,1998
.
- Kabagambe E, Baylin A, Siles X, Campos H: Comparison of dietary intakes of micro and macronutrients in rural, suburban and urban populations in Costa Rica. Public Health Nutr5
:835
842,2002
.[Medline]
- Sacks F, Katan M: Randomized clinical trials on the effects of dietary fat and carbohydrate on plasma lipoprotein and cardiovascular disease. Am J Med113
:13S
24S,2002
.
- Grundy S, Abate N, Chandalia M: Diet composition and the metabolic syndrome: What is the optimal fat intake? Am J Med113
:25S
29S,2002
.
- Baylin A, Kabagambe E, Ascherio A, Spiegelman D, Campos H: Adipose tissue, alpha-linolenic acid and non-fatal acute myocardial infarction in Costa Rica. Circulation107
:1586
1591,2003
.[Abstract/Free Full Text]
- Renaud S, Lanzmann-Petithory D: Coronary heart disease: dietary links and pathogenesis. Public Health Nutr4
:459
474,2001
.[Medline]
- Simopoulos A: N-3 fatty acid and human health: defining strategies for public police. Lipids36
: S83
S89,2001
.[Medline]
- Trumbo P, Schlicker S, Yates AA, Poos M, Nutrition Board of the Institute of Medicine, The National Academies: Dietary references intakes for energy, carbohydrate, fiber, fat, fatty acids, cholesterol, protein and amino acids. J Am Diet Assoc102
:1621
1630,2002
.[Medline]
- Allison D, Egan K, Barray L, Caughman C, Infante M, Heimbach J: Estimated intakes of trans-fatty acids and other fatty acids in the US population. J Am Diet Assoc99
:166
174,1999
.[Medline]
- Ascherio A, Katan M, Zock P, Stampfer M, Willet WC: Trans-fatty acids and coronary heart disease. N Engl J Med340
:1994
1998,1999
.[Free Full Text]
- Hu FB, Manson J, Willet WC: Types of dietary fat and risk of coronary heart disease: a critical review. J Am Coll Nutr20
:5
19,2001
.[Abstract/Free Full Text]
- Dlouhy P, Tvrzicka E, Stankova B, Vecka M, Zak A, Straka Z, Fanta J, Pachl J, Kubisova D, Rambouskova J, Bilkova D, Andel M: Higher concentration of 18:1trans-fatty acids in subcutaneous fat of persons with coronarographically documented atherosclerosis of the coronary arteries. Ann Nutr Metab47
:302
305,2003
.[Medline]
- van de Vijver L, van Poppel G, van Houwelingen A, Kruyssen DF, Homstra G: Trans-unsaturated fatty acids in plasma phospholipids and coronary heart disease: a case-control study. Atherosclerosis126
:155
116,1996
.[Medline]
- Roberts T, Wood D, Riemersma R, Gallagher P, Lampe L: Trans-isomers of oleic and linoleic acids in adipose tissue and sudden cardiac death. Lancet345
:278
282,1995
.[Medline]
- Lemaitre R, King I, Raghunathan T, Pearce R, Weinmann S, Knopp R, Copass M, Cobb L, Siscovick D: Cell membrane trans-fatty acids and the risk of primary cardiac arrest. Circulation105
:697
701,2002
.[Abstract/Free Full Text]
- Kris-Etherton PM, Emken EA, Allison DB, Dietschy JM, Nicolosi RJ, Denke MA: Trans-fatty acids and coronary heart disease risk. Am J Clin Nutr62
:655S
707S,1995
.[Abstract/Free Full Text]
- Watts GF, Jackson P, Burke V, Lewis B: Dietary fatty acids and progression of coronary artery disease in men. Am J Clin Nutr64
:202
209,1996
.[Abstract/Free Full Text]