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Combined effects of saturated fat and cholesterol intakes on serum lipids: Tehran Lipid and Glucose Study
Nutrition 25 (2009) 526 –531 www.nutritionjrnl.com
Applied nutritional investigation
Combined effects of saturated fat and cholesterol intakes on serum lipids: Tehran Lipid and Glucose Study Parvin Mirmiran, Ph.D.*, Azra Ramezankhani, M.S., and Fereidoun Azizi, M.D. Obesity Research Center, Research Institute of Endocrine Sciences, Shaheed Beheshti University of Medical Sciences, Tehran, Islamic Republic of Iran Manuscript received August 4, 2008; accepted November 8, 2008.
Abstract
Objective: This study investigated the combined effect of saturated fat and cholesterol intake on serum lipids among Tehranian adults. Methods: In 443 subjects ⱖ18 y, dietary intake was assessed. Height and weight were measured and body mass index was calculated. Serum cholesterol, triacylglycerol, high-density lipoprotein cholesterol (HDL-C), and low-density lipoprotein cholesterol levels were calculated. Cholesterol intakes ⱖ300 mg/d and saturated fat intakes ⱖ7% of total energy were defined as high intakes. Individuals were categorized into four groups based on cholesterol and saturated fat intakes. Results: Subjects’ mean age was 40.1 ⫾ 14.6 y; those in whom cholesterol and saturated fat intake was normal had significantly less energy and fat intake than those with high cholesterol and saturated fat intakes (P ⬍ 0.01). Saturated fat intake had a significant effect on serum total and HDL-C levels. Subjects with a normal saturated fat intake had significantly less serum total and HDL-C than those who had high saturated fat intake (P ⬍ 0.01 and P ⬍ 0.05, respectively). Adjusting for age, sex, and body mass index, the main effect of cholesterol intake on HDL-C was significant (P ⫽ 0.05). Mean serum HDL-C was lower in subjects who had normal cholesterol intake than in those with high cholesterol intake. Conclusion: These results show that cholesterol and saturated fat intakes have no combined effect on serum low-density lipoprotein cholesterol level, whereas cholesterol intake per se affects serum HDL-C level. © 2009 Published by Elsevier Inc.
Keywords:
Saturated fat; Cholesterol; Combined effect; Serum lipids; Tehran
Introduction Although significant reductions have occurred in the incidence of cardiovascular disease since the mid 1970s, it remains the primary cause of morbidity and mortality in many countries [1]. Risk factors of cardiovascular disease include smoking, hypercholesterolemia, hypertension, diabetes mellitus, physical inactivity, decreased high-density lipoprotein (HDL), abdominal obesity, high triacylglycerols, excessive alcohol consumption, aging, and dietary patterns [2– 4]. As early as at the beginning of the previous century, animal studies pointed to a causal role of dietary
This study was funded by the Research Institute of Endocrine Sciences, Shaheed Beheshti University of Medical Sciences, Tehran, Iran. * Corresponding author. Tel.: ⫹98-21-240-2463; fax: ⫹98-21-2402463. E-mail address: [email protected] (P. Mirmiran). 0899-9007/09/$ – see front matter © 2009 Published by Elsevier Inc. doi:10.1016/j.nut.2008.11.018
cholesterol in atherogenesis. In humans, however, most observational studies have not provided convincing evidence for an impact of cholesterol intake on coronary heart disease (CHD) [5]. The eating pattern associated with CHD is characterized by a high intake of total fat, saturated fatty acids (SFAs), and cholesterol and a low intake of fiber and polyunsaturated fatty acids. In typical Western diets, the amounts of total fat, SFA, and cholesterol are strongly correlated with each other, whereas they have negative associations with the intake of fiber and polyunsaturated fatty acids. Thus, it has not been possible to determine whether the association between the above-mentioned eating pattern and CHD is due to the high consumption of SFAs and/or cholesterol or an insufficient supply of at least one protective factor such as fiber or polyunsaturated fatty acids [5]. Some experimental and pathologic studies have shown a strong association between hypercholesterolemia and the likelihood of developing atherosclerotic CHD. The
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effects of diet on serum low-density lipoprotein cholesterol (LDL-C) have consistently been documented and high intakes of SFAs, trans-unsaturated fatty acids, cholesterol, and excess calorie intake are known to lead to obesity [6 – 8]. Some studies have shown that dietary cholesterol has a lesser regulatory effect on plasma cholesterol compared with SFAs; based on these studies, diets low in cholesterol and high in saturated fat increase LDL-C, whereas consumption of egg yolk and oyster, which have a very high cholesterol content without excess saturated fats, results in only a minimal increase in LDL-C [5–10]. Some experimental studies have shown that there are synergistic interactions of SFA and cholesterol in the regulation of serum cholesterol level [9]. In addition, differences in genetic constitution (apolipoprotein [apo] E and apoA-IV) may affect cholesterol metabolism and responses to diet [9]. Despite numerous studies done about the effect of SFA and cholesterol intake on serum lipids, there are limited data available on plasma lipid responses to the combined effect of dietary fat and cholesterol. This study was therefore conducted to investigate the combined effect of saturated fat and cholesterol intake on serum lipids among Tehranian adults.
Materials and methods This population-based cross-sectional study was a part of a dietary intake assessment that was conducted within the framework of the Tehran Lipid and Glucose Study (TLGS), a prospective study of a representative sample of residents of District 13 of Tehran, that aimed at ascertaining the prevalence of non-communicable disease risk factors and developing a healthy lifestyle to curtail these risk factors [11,12]. Subjects In the TLGS, 15 005 persons ⱖ3 y of age were selected by a multistage cluster, random sampling method. A representative sample of 1474 persons was randomly selected for dietary assessment; of these, 443 (171 men and 272 women) ⱖ18 y of age who had all the relevant data and had not used any hypoglycemic agents and lipid-lowering and antihypertensive prescription medications participated in this study. Written informed consent was obtained from each subject and the protocol of this study was approved by the research council of the Research Institute of Endocrine Sciences of Shaheed Beheshti University of Medical Sciences.
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sumption Survey Project, which has been reported in Persian [13]. Dietary intake assessment was undertaken with 2-d 24-h recalls by expert interviewers. These 2 d were selected randomly from the weekdays. Because the weekend diet does not reflect the usual diet, we did not select the weekend. The first recall was performed at the subject’s home and the second at a clinic visit in the diet unit of TLGS. These 2 d were among usual days for subjects. Standard reference tables were used to convert household portions to grams for computerization [14]. After coding of diaries, the dietary recall form was linked to a nutrient database (Nutritionist III designed for Iranian foods) and daily energy and nutrient intakes (carbohydrates, proteins, and fats) for each individual were determined from the means of the two 24-h dietary recalls. Assessment of other variables All information regarding age, sex, education, marital status, and job was obtained using validated questionnaires. Weight was measured while the subjects were minimally clothed without shoes using digital scales and recorded to the nearest 100 g. Height was measured in a standing position, without shoes, using a tape meter, while the shoulders were in a normal position [15]. Body mass index (BMI) was calculated as weight in kilograms divided by height in meters squared. A blood sample was drawn from all subjects between 07:00 and 09:00 h into Vacutainer tubes after 12- to 14-h overnight fasting [16]; the samples were centrifuged within 30 – 45 min of collection. All blood lipid analyses were done at the TLGS research laboratory on the day of blood collection. The analysis of samples was performed using a Selectra 2 autoanalyzer (Vital Scientific, Spankeren, The Netherlands). Serum total cholesterol and triacylglycerol concentrations were measured by commercially available enzymatic reagents (Pars Azmoon, Tehran, Iran), adapted to the Selectra autoanalyzer. HDL cholesterol (HDL-C) was measured after precipitation of the apoBcontaining lipoproteins with phosphotungstic acid. LDL-C was calculated according to the method of Friedewald et al. [17]; it was not calculated when the serum concentration of triacylglycerol was ⬎400 mg/dL. All samples were analyzed when the internal quality control met the acceptable criteria. Inter- and intra-assay coefficients of variation were 2% and 0.5% for total cholesterol and 1.6% and 0.6% for triacylglycerol, respectively.
Assessment of dietary intake
Definition of terms
Subjects were interviewed privately, face to face; trained interviewers using pretested questionnaires conducted the interviews. All questionnaires used in the study were validated previously in the Nationwide Household Food Con-
Intakes of cholesterol ⱖ300 mg/d were defined as high and those ⬍300 mg/d as normal. For SFA an intake ⱖ7% of total daily energy intake was defined as high and an intake ⬍7% as normal [18].
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Statistical methods All data were analyzed using SPSS 9.05 (SPSS Inc., Chicago IL, USA). The participants were classified into four groups according to SFA and cholesterol intakes as the two main factors, each having two levels (2 ⫻ 2 factorial design). Pearson’s correlation coefficient was used to determine confounding factors, using risk factors as the dependent variables and age, sex, BMI, and each of the macronutrients as the independent variables. Age, sex, and BMI had a significant correlation with serum lipids. Differences among the four dietary groups were analyzed using two-way analysis of variance with SFA and cholesterol intakes as the main factors; after this, using age, sex, and BMI as the covariates, we repeated the analysis in a separate model.
no interaction between these two factors. The main effect of SFA and cholesterol intakes on fat intake was significant (P ⬍ 0.01), although subjects whose SFA and cholesterol intakes were normal took less total fat (P ⬍ 0.01); however, there was no interaction between these two factors. Subjects whose cholesterol intake was normal had decreased fiber intake compared with subjects with high cholesterol intake (P ⬍ 0.01). There was significant interaction between SFA and cholesterol intakes on fiber intake (P ⬍ 0.01). Means of BMI and dietary intake after adjusting for age and sex are listed in Table 2. As presented in Table 2, there was no significant interaction between SFA and cholesterol intakes on BMI and dietary intake; moreover, the BMI of subjects with a high cholesterol intake was significantly greater than the BMI of those with a normal cholesterol intake (P ⬍ 0.01). Effects of SFA and cholesterol intakes on lipid profiles
Results Of the 443 participants, 171 (38.6%) were men and 272 (61.4%) were women; the mean age of the subjects was 40.1 ⫾ 14.6 y. Effects of SFA and cholesterol intakes on diet Anthropometric measurements and macronutrient intakes according to SFA and cholesterol intakes are listed in Table 1. The subjects whose SFA and cholesterol intakes were normal had decreased energy intakes compared with subjects who had high SFA and cholesterol intakes. Thus the main effect of SFA and cholesterol intakes on energy intake was significant (P ⬍ 0.01), although there was no interaction between these two factors. The main effect of SFA and cholesterol intakes on carbohydrate intake was significant (P ⬍ 0.01). Compared with subjects who had a high SFA intake, carbohydrate intake was significantly increased in subjects whose SFA was normal. Carbohydrate intake was observed to b significantly decreased in subjects whose cholesterol intake was normal (P ⬍ 0.01). There was
The means for serum lipids according to SFA and cholesterol intakes are listed in Table 3. Means of serum total cholesterol and HDL-C were decreased in subjects whose SFA intake was normal compared with subjects with a high intake of SFA. Mean serum lipids according to SFA and cholesterol intakes after adjusting for age, sex, and BMI as the covariates are listed in Table 4. The main effect of cholesterol intake on HDL-C was significant (P ⬍ 0.05), and subjects whose cholesterol intake was normal had decreased serum HDL-C compared with subjects with a high cholesterol intake.
Discussion This study shows that serum total cholesterol is decreased in subjects with normal SFA intake compared with those with a high SFA intake and this difference is independent of cholesterol intake. After adjusting for age, sex, and BMI as confounding factors, the main effect of SFA and cholesterol intakes on LDL and total cholesterol concentra-
Table 1 BMI and dietary intake in subjects with normal and high SFA and cholesterol intakes* Variable
BMI (kg/m2) Energy intake (kcal/d) Carbohydrate (g/d) Fat (g/d) Fiber (g/d)
Normal SFA intake
High SFA intake
Normal cholesterol intake (n ⫽ 77)
High cholesterol intake (n ⫽ 136)
Normal cholesterol intake (n ⫽ 110)
High cholesterol intake (n ⫽ 120)
26.8 ⫾ 4.9 1622 ⫾ 361 252 ⫾ 39 46 ⫾ 20 5.5 ⫾ 1.9
27.6 ⫾ 5.1 2550 ⫾ 485 409 ⫾ 80 70 ⫾ 25 9.2 ⫾ 5.4
26.8 ⫾ 4.8 1720 ⫾ 374 234 ⫾ 42 64 ⫾ 25 5.6 ⫾ 2.5
26.2 ⫾ 4.1 2715 ⫾ 538 387 ⫾ 73 97 ⫾ 40 7.7 ⫾ 2.6
P1
P2
P3
0.15 0.003 0.002 0.001 0.07
0.88 0.001 0.001 0.001 0.001
0.14 0.44 0.78 0.11 0.02
BMI, body mass index; P1, for main effect of SFA intake; P2, for main effect of cholesterol intake; P3, for combined effect of SFA and cholesterol intakes; SFA, saturated fatty acid * Values are means ⫾ SDs. SFA intakes ⱖ7% of total daily energy intake were defined as high and those ⬍7% as normal. Cholesterol intakes ⱖ300 mg/d were defined as high and those ⬍300 mg/d as normal.
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Table 2 BMI and dietary intake in subjects with normal and high SFA and cholesterol intakes* Variable
BMI (kg/m2) Energy intake (kcal/d) Carbohydrate (g/d) Fat (g/d) Fiber (g/d)
Normal SFA intake
High SFA intake
Normal cholesterol intake (n ⫽ 77)
High cholesterol intake (n ⫽ 136)
Normal cholesterol intake (n ⫽ 110)
High cholesterol intake (n ⫽ 120)
25.9 ⫾ 0.6 1678 ⫾ 63 260 ⫾ 9 48 ⫾ 3.7 5.5 ⫾ 0.5
27.6 ⫾ 0.4 2541 ⫾ 38 406 ⫾ 5 70 ⫾ 2 9.1 ⫾ 0.3
24.9 ⫾ 0.7 1777 ⫾ 70 244 ⫾ 10 67 ⫾ 4 5.5 ⫾ 0.5
26.6 ⫾ 0.4 2680 ⫾ 40 383 ⫾ 6 95 ⫾ 2 7.7 ⫾ 0.3
P1
P2
P3
0.09 0.03 0.01 0.001 0.12
0.003 0.001 0.001 0.001 0.001
0.999 0.71 0.66 0.35 0.135
BMI, body mass index; P1, for main effect of SFA intake after adjusting for age and sex; P2, for significant main effect of cholesterol intake after adjusting for age and sex; P3, for significant combined effect of SFA and cholesterol intake after adjusting for age and sex; SFA, saturated fatty acid * Values are means ⫾ SEs adjusted for age and sex. SFA intakes ⱖ7% of total daily energy intake were defined as high and those ⬍7% as normal. Cholesterol intakes ⱖ300 mg/d were defined as high and those ⬍300 mg/d as normal.
tions was not significant. However, it has been reported that dietary cholesterol can increase LDL-C levels, although to a lesser extent than saturated fat [9,10]. Some studies have shown that there are synergistic effects between dietary cholesterol and saturated fat on the cholesterol level of plasma [9]. Kris-Etherton [19] indicated that SFAs could cause an increase in plasma total cholesterol concentrations. Differences in the results of other studies in this field compared with ours may be due to the consumption of different classes of SFA. Metabolic studies have found that different classes of SFA have different effects on plasma lipid and lipoprotein levels; specifically, SFAs with 12–16 carbon atoms tend to increase plasma total and LDL-C levels, whereas stearic acid does not have a cholesterol-raising effect [7]. Hence, assessment of these factors in future studies is recommended. Moreover, genetic studies have suggested a relation among apoE, apoA-IV, and serum LDL-C response to dietary fatty acid and cholesterol intakes in adults [9]. Despite the complicated association between dietary cholesterol and serum cholesterol, it has been recognized that the cholesterol content of the diet must be lower, especially in a subgroup of individuals who are highly responsive to changes in cholesterol intake [5,9]. Our study also showed the main effect of cholesterol intake on serum HDL concentrations was significant; subjects with a normal cholesterol intake had decreased HDL-C compared
with subjects with a high cholesterol intake. In other studies, decreased cholesterol intake was associated with a lower apoA-I lipoprotein and therefore decreased HDL-C [9,20]. Based on reports of different studies, HDL-C level affected by sex, age, BMI, physical activity, smoking, some hormones, disease and alcohol consumption, and nutritional factors had less of an effect on HDL-C [2,4,21]. Further research assessing these factors will provide stronger evidence of this relation. The present study showed no main effect of SFA and cholesterol intakes on triacylglycerols with and without adjustment of confounding factors. Dietary intake of subjects showed that total energy and fat intakes were lower in subjects whose cholesterol and SFA intakes were normal compared with subjects with high cholesterol and SFA intakes, whereas serum triacylglycerol concentration was higher in the former group compared with the latter group. Some experimental studies have shown no relation between plasma triacylglycerols and dietary fat intake [22]. The recommendations for energy and SFA intakes in therapeutic diets are different, although no positive or negative relations between percentage of fat intake and serum lipid have been observed [22–24]. Different factors that increase serum triacylglycerol levels include diet (high fat and refined carbohydrate), estrogens, alcohol, obesity, untreated diabetes, un-
Table 3 Comparison of lipid profiles in participants with normal and high SFA and cholesterol intakes* Serum concentration
Triacylglycerol (mg/dL) Total cholesterol (mg/dL) LDL-C (mg/dL) HDL-C (mg/dL)
Normal SFA intake
High SFA intake
Normal cholesterol intake (n ⫽ 77)
High cholesterol intake (n ⫽ 136)
Normal cholesterol intake (n ⫽ 110)
High cholesterol intake (n ⫽ 120)
147 ⫾ 81 187 ⫾ 37 118 ⫾ 29 10 ⫾ 39
114 ⫾ 168 44 ⫾ 186 39 ⫾ 118 10 ⫾ 37
72 ⫾ 126 42 ⫾ 190 36 ⫾ 124 11 ⫾ 41
75⫾ 133 39 ⫾ 186 33 ⫾ 120 10 ⫾ 40
P1
P2
P3
0.73 0.001 0.27 0.03
0.58 0.1 0.53 0.15
0.66 0.44 0.64 0.67
HDL-C, high-density lipoprotein cholesterol; LDL-C, low-density lipoprotein cholesterol; P1, for main effect of SFA intake; P2, for main effect of cholesterol intake; P3, for combined effect of SFA and cholesterol intake; SFA, saturated fatty acid * Values are means ⫾ SDs. SFA intakes ⱖ7% of total daily energy intake were defined as high and those ⬍7% as normal. Cholesterol intakes ⱖ300 mg/d were defined as high and those ⬍300 mg/d as normal.
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Table 4 Comparison of lipid profiles in participants with normal and high SFA and cholesterol intakes* Variable
Triacylglycerol (mg/dL) Total cholesterol (mg/dL) LDL-C (mg/dL) HDL-C (mg/dL)
Normal SFA intake
High SFA intake
Normal cholesterol intake (n ⫽ 77)
High cholesterol intake (n ⫽ 136)
Normal cholesterol intake (n ⫽ 110)
High cholesterol intake (n ⫽ 120)
11 ⫾ 146 5 ⫾ 180 4 ⫾ 114 1.4 ⫾ 36.7
7 ⫾ 160 3 ⫾ 183 2 ⫾ 115 0.8 ⫾ 37.9
13 ⫾ 147 5 ⫾ 183 5 ⫾ 117 1.5 ⫾ 36.1
7 ⫾ 138 3 ⫾ 189 3 ⫾ 122 0.9 ⫾ 39.7
P1
P2
P3
0.31 0.26 0.18 0.64
0.82 0.34 0.47 0.05
0.27 0.70 0.66 0.31
HDL-C, high-density lipoprotein cholesterol; LDL-C, low-density lipoprotein cholesterol; P1, for main effect of SFA intake after adjusting for age, sex, and body mass index; P2, for significant main effect of cholesterol intake after adjusting for age, sex, and body mass index; P3, for significant combined effect of SFA and cholesterol intake after adjusting for age, sex, and body mass index; SFA, saturated fatty acid * Values are means ⫾ SEs adjusted for age, sex, and body mass index. SFA intakes ⱖ7% of total daily energy intake were defined as high and those ⬍7% as normal. Cholesterol intakes ⱖ300 mg/d were defined as high and those ⬍300 mg/d as normal.
treated hypothyroidism, chronic renal disease, and hepatic disease [25]. This study showed that mean carbohydrate was higher in subjects who consumed normal saturated fat compared with subjects with a high saturated fat intake; thus, increased serum triacylglycerols in the former group may be due to the high consumption of carbohydrate; this has been shown in some studies, where increased dietary carbohydrate led to increased plasma triacylglycerol levels [26,27]. In contrast, increased levels of triacylglycerols in that group may be due in part to differences in physical activity. We did not use physical activity data because the reliability and validity of the Lipid Research Clinic questionnaire, which was used in the TLGS, had not been evaluated in our country. Lack of data on the physical activity of the subjects is a limitation of the present study. The mean of fiber intake was higher in subjects with high cholesterol intakes compared with subjects with normal cholesterol intakes, whereas there was no difference in LDL-C and total cholesterol between the two groups. Recent research has confirmed the cholesterol-lowering benefits of fiber and supported new recommendations for intake amounts to lower serum cholesterol [28]. In the present study subjects with high and normal cholesterol intakes consumed 3.2 g of fiber per 1000 cal, which is only 23% of the Institute of Medicine’s recommendation of 14 g of fiber per 1000 cal [29]. Therefore, the amount of fiber intake in all groups was less than the recommended dietary intake for its beneficial effect in lowering LDL-C. After adjusting for age and sex, the mean BMI of subjects with a high cholesterol intake was significantly greater than the BMI of those with a normal cholesterol intake (P ⬍ 0.01). As presented in Table 2, total caloric consumption and carbohydrate and fat intakes in the former group were higher compared with those in the latter group (P ⬍ 0.01). The results of this study indicate that cholesterol and saturated fat intakes have no combined effect on serum triacylglycerols, total cholesterol, and LDL-C, whereas cholesterol intake has a significant effect on serum HDL-C concentration.
Acknowledgments The authors express appreciation to the participants of the Tehran Lipid and Glucose Study and acknowledge the assistance given by Ms. N. Shiva in the language editing of the manuscript.
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Applied nutritional investigation
Combined effects of saturated fat and cholesterol intakes on serum lipids: Tehran Lipid and Glucose Study Parvin Mirmiran, Ph.D.*, Azra Ramezankhani, M.S., and Fereidoun Azizi, M.D. Obesity Research Center, Research Institute of Endocrine Sciences, Shaheed Beheshti University of Medical Sciences, Tehran, Islamic Republic of Iran Manuscript received August 4, 2008; accepted November 8, 2008.
Abstract
Objective: This study investigated the combined effect of saturated fat and cholesterol intake on serum lipids among Tehranian adults. Methods: In 443 subjects ⱖ18 y, dietary intake was assessed. Height and weight were measured and body mass index was calculated. Serum cholesterol, triacylglycerol, high-density lipoprotein cholesterol (HDL-C), and low-density lipoprotein cholesterol levels were calculated. Cholesterol intakes ⱖ300 mg/d and saturated fat intakes ⱖ7% of total energy were defined as high intakes. Individuals were categorized into four groups based on cholesterol and saturated fat intakes. Results: Subjects’ mean age was 40.1 ⫾ 14.6 y; those in whom cholesterol and saturated fat intake was normal had significantly less energy and fat intake than those with high cholesterol and saturated fat intakes (P ⬍ 0.01). Saturated fat intake had a significant effect on serum total and HDL-C levels. Subjects with a normal saturated fat intake had significantly less serum total and HDL-C than those who had high saturated fat intake (P ⬍ 0.01 and P ⬍ 0.05, respectively). Adjusting for age, sex, and body mass index, the main effect of cholesterol intake on HDL-C was significant (P ⫽ 0.05). Mean serum HDL-C was lower in subjects who had normal cholesterol intake than in those with high cholesterol intake. Conclusion: These results show that cholesterol and saturated fat intakes have no combined effect on serum low-density lipoprotein cholesterol level, whereas cholesterol intake per se affects serum HDL-C level. © 2009 Published by Elsevier Inc.
Keywords:
Saturated fat; Cholesterol; Combined effect; Serum lipids; Tehran
Introduction Although significant reductions have occurred in the incidence of cardiovascular disease since the mid 1970s, it remains the primary cause of morbidity and mortality in many countries [1]. Risk factors of cardiovascular disease include smoking, hypercholesterolemia, hypertension, diabetes mellitus, physical inactivity, decreased high-density lipoprotein (HDL), abdominal obesity, high triacylglycerols, excessive alcohol consumption, aging, and dietary patterns [2– 4]. As early as at the beginning of the previous century, animal studies pointed to a causal role of dietary
This study was funded by the Research Institute of Endocrine Sciences, Shaheed Beheshti University of Medical Sciences, Tehran, Iran. * Corresponding author. Tel.: ⫹98-21-240-2463; fax: ⫹98-21-2402463. E-mail address: [email protected] (P. Mirmiran). 0899-9007/09/$ – see front matter © 2009 Published by Elsevier Inc. doi:10.1016/j.nut.2008.11.018
cholesterol in atherogenesis. In humans, however, most observational studies have not provided convincing evidence for an impact of cholesterol intake on coronary heart disease (CHD) [5]. The eating pattern associated with CHD is characterized by a high intake of total fat, saturated fatty acids (SFAs), and cholesterol and a low intake of fiber and polyunsaturated fatty acids. In typical Western diets, the amounts of total fat, SFA, and cholesterol are strongly correlated with each other, whereas they have negative associations with the intake of fiber and polyunsaturated fatty acids. Thus, it has not been possible to determine whether the association between the above-mentioned eating pattern and CHD is due to the high consumption of SFAs and/or cholesterol or an insufficient supply of at least one protective factor such as fiber or polyunsaturated fatty acids [5]. Some experimental and pathologic studies have shown a strong association between hypercholesterolemia and the likelihood of developing atherosclerotic CHD. The
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effects of diet on serum low-density lipoprotein cholesterol (LDL-C) have consistently been documented and high intakes of SFAs, trans-unsaturated fatty acids, cholesterol, and excess calorie intake are known to lead to obesity [6 – 8]. Some studies have shown that dietary cholesterol has a lesser regulatory effect on plasma cholesterol compared with SFAs; based on these studies, diets low in cholesterol and high in saturated fat increase LDL-C, whereas consumption of egg yolk and oyster, which have a very high cholesterol content without excess saturated fats, results in only a minimal increase in LDL-C [5–10]. Some experimental studies have shown that there are synergistic interactions of SFA and cholesterol in the regulation of serum cholesterol level [9]. In addition, differences in genetic constitution (apolipoprotein [apo] E and apoA-IV) may affect cholesterol metabolism and responses to diet [9]. Despite numerous studies done about the effect of SFA and cholesterol intake on serum lipids, there are limited data available on plasma lipid responses to the combined effect of dietary fat and cholesterol. This study was therefore conducted to investigate the combined effect of saturated fat and cholesterol intake on serum lipids among Tehranian adults.
Materials and methods This population-based cross-sectional study was a part of a dietary intake assessment that was conducted within the framework of the Tehran Lipid and Glucose Study (TLGS), a prospective study of a representative sample of residents of District 13 of Tehran, that aimed at ascertaining the prevalence of non-communicable disease risk factors and developing a healthy lifestyle to curtail these risk factors [11,12]. Subjects In the TLGS, 15 005 persons ⱖ3 y of age were selected by a multistage cluster, random sampling method. A representative sample of 1474 persons was randomly selected for dietary assessment; of these, 443 (171 men and 272 women) ⱖ18 y of age who had all the relevant data and had not used any hypoglycemic agents and lipid-lowering and antihypertensive prescription medications participated in this study. Written informed consent was obtained from each subject and the protocol of this study was approved by the research council of the Research Institute of Endocrine Sciences of Shaheed Beheshti University of Medical Sciences.
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sumption Survey Project, which has been reported in Persian [13]. Dietary intake assessment was undertaken with 2-d 24-h recalls by expert interviewers. These 2 d were selected randomly from the weekdays. Because the weekend diet does not reflect the usual diet, we did not select the weekend. The first recall was performed at the subject’s home and the second at a clinic visit in the diet unit of TLGS. These 2 d were among usual days for subjects. Standard reference tables were used to convert household portions to grams for computerization [14]. After coding of diaries, the dietary recall form was linked to a nutrient database (Nutritionist III designed for Iranian foods) and daily energy and nutrient intakes (carbohydrates, proteins, and fats) for each individual were determined from the means of the two 24-h dietary recalls. Assessment of other variables All information regarding age, sex, education, marital status, and job was obtained using validated questionnaires. Weight was measured while the subjects were minimally clothed without shoes using digital scales and recorded to the nearest 100 g. Height was measured in a standing position, without shoes, using a tape meter, while the shoulders were in a normal position [15]. Body mass index (BMI) was calculated as weight in kilograms divided by height in meters squared. A blood sample was drawn from all subjects between 07:00 and 09:00 h into Vacutainer tubes after 12- to 14-h overnight fasting [16]; the samples were centrifuged within 30 – 45 min of collection. All blood lipid analyses were done at the TLGS research laboratory on the day of blood collection. The analysis of samples was performed using a Selectra 2 autoanalyzer (Vital Scientific, Spankeren, The Netherlands). Serum total cholesterol and triacylglycerol concentrations were measured by commercially available enzymatic reagents (Pars Azmoon, Tehran, Iran), adapted to the Selectra autoanalyzer. HDL cholesterol (HDL-C) was measured after precipitation of the apoBcontaining lipoproteins with phosphotungstic acid. LDL-C was calculated according to the method of Friedewald et al. [17]; it was not calculated when the serum concentration of triacylglycerol was ⬎400 mg/dL. All samples were analyzed when the internal quality control met the acceptable criteria. Inter- and intra-assay coefficients of variation were 2% and 0.5% for total cholesterol and 1.6% and 0.6% for triacylglycerol, respectively.
Assessment of dietary intake
Definition of terms
Subjects were interviewed privately, face to face; trained interviewers using pretested questionnaires conducted the interviews. All questionnaires used in the study were validated previously in the Nationwide Household Food Con-
Intakes of cholesterol ⱖ300 mg/d were defined as high and those ⬍300 mg/d as normal. For SFA an intake ⱖ7% of total daily energy intake was defined as high and an intake ⬍7% as normal [18].
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Statistical methods All data were analyzed using SPSS 9.05 (SPSS Inc., Chicago IL, USA). The participants were classified into four groups according to SFA and cholesterol intakes as the two main factors, each having two levels (2 ⫻ 2 factorial design). Pearson’s correlation coefficient was used to determine confounding factors, using risk factors as the dependent variables and age, sex, BMI, and each of the macronutrients as the independent variables. Age, sex, and BMI had a significant correlation with serum lipids. Differences among the four dietary groups were analyzed using two-way analysis of variance with SFA and cholesterol intakes as the main factors; after this, using age, sex, and BMI as the covariates, we repeated the analysis in a separate model.
no interaction between these two factors. The main effect of SFA and cholesterol intakes on fat intake was significant (P ⬍ 0.01), although subjects whose SFA and cholesterol intakes were normal took less total fat (P ⬍ 0.01); however, there was no interaction between these two factors. Subjects whose cholesterol intake was normal had decreased fiber intake compared with subjects with high cholesterol intake (P ⬍ 0.01). There was significant interaction between SFA and cholesterol intakes on fiber intake (P ⬍ 0.01). Means of BMI and dietary intake after adjusting for age and sex are listed in Table 2. As presented in Table 2, there was no significant interaction between SFA and cholesterol intakes on BMI and dietary intake; moreover, the BMI of subjects with a high cholesterol intake was significantly greater than the BMI of those with a normal cholesterol intake (P ⬍ 0.01). Effects of SFA and cholesterol intakes on lipid profiles
Results Of the 443 participants, 171 (38.6%) were men and 272 (61.4%) were women; the mean age of the subjects was 40.1 ⫾ 14.6 y. Effects of SFA and cholesterol intakes on diet Anthropometric measurements and macronutrient intakes according to SFA and cholesterol intakes are listed in Table 1. The subjects whose SFA and cholesterol intakes were normal had decreased energy intakes compared with subjects who had high SFA and cholesterol intakes. Thus the main effect of SFA and cholesterol intakes on energy intake was significant (P ⬍ 0.01), although there was no interaction between these two factors. The main effect of SFA and cholesterol intakes on carbohydrate intake was significant (P ⬍ 0.01). Compared with subjects who had a high SFA intake, carbohydrate intake was significantly increased in subjects whose SFA was normal. Carbohydrate intake was observed to b significantly decreased in subjects whose cholesterol intake was normal (P ⬍ 0.01). There was
The means for serum lipids according to SFA and cholesterol intakes are listed in Table 3. Means of serum total cholesterol and HDL-C were decreased in subjects whose SFA intake was normal compared with subjects with a high intake of SFA. Mean serum lipids according to SFA and cholesterol intakes after adjusting for age, sex, and BMI as the covariates are listed in Table 4. The main effect of cholesterol intake on HDL-C was significant (P ⬍ 0.05), and subjects whose cholesterol intake was normal had decreased serum HDL-C compared with subjects with a high cholesterol intake.
Discussion This study shows that serum total cholesterol is decreased in subjects with normal SFA intake compared with those with a high SFA intake and this difference is independent of cholesterol intake. After adjusting for age, sex, and BMI as confounding factors, the main effect of SFA and cholesterol intakes on LDL and total cholesterol concentra-
Table 1 BMI and dietary intake in subjects with normal and high SFA and cholesterol intakes* Variable
BMI (kg/m2) Energy intake (kcal/d) Carbohydrate (g/d) Fat (g/d) Fiber (g/d)
Normal SFA intake
High SFA intake
Normal cholesterol intake (n ⫽ 77)
High cholesterol intake (n ⫽ 136)
Normal cholesterol intake (n ⫽ 110)
High cholesterol intake (n ⫽ 120)
26.8 ⫾ 4.9 1622 ⫾ 361 252 ⫾ 39 46 ⫾ 20 5.5 ⫾ 1.9
27.6 ⫾ 5.1 2550 ⫾ 485 409 ⫾ 80 70 ⫾ 25 9.2 ⫾ 5.4
26.8 ⫾ 4.8 1720 ⫾ 374 234 ⫾ 42 64 ⫾ 25 5.6 ⫾ 2.5
26.2 ⫾ 4.1 2715 ⫾ 538 387 ⫾ 73 97 ⫾ 40 7.7 ⫾ 2.6
P1
P2
P3
0.15 0.003 0.002 0.001 0.07
0.88 0.001 0.001 0.001 0.001
0.14 0.44 0.78 0.11 0.02
BMI, body mass index; P1, for main effect of SFA intake; P2, for main effect of cholesterol intake; P3, for combined effect of SFA and cholesterol intakes; SFA, saturated fatty acid * Values are means ⫾ SDs. SFA intakes ⱖ7% of total daily energy intake were defined as high and those ⬍7% as normal. Cholesterol intakes ⱖ300 mg/d were defined as high and those ⬍300 mg/d as normal.
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Table 2 BMI and dietary intake in subjects with normal and high SFA and cholesterol intakes* Variable
BMI (kg/m2) Energy intake (kcal/d) Carbohydrate (g/d) Fat (g/d) Fiber (g/d)
Normal SFA intake
High SFA intake
Normal cholesterol intake (n ⫽ 77)
High cholesterol intake (n ⫽ 136)
Normal cholesterol intake (n ⫽ 110)
High cholesterol intake (n ⫽ 120)
25.9 ⫾ 0.6 1678 ⫾ 63 260 ⫾ 9 48 ⫾ 3.7 5.5 ⫾ 0.5
27.6 ⫾ 0.4 2541 ⫾ 38 406 ⫾ 5 70 ⫾ 2 9.1 ⫾ 0.3
24.9 ⫾ 0.7 1777 ⫾ 70 244 ⫾ 10 67 ⫾ 4 5.5 ⫾ 0.5
26.6 ⫾ 0.4 2680 ⫾ 40 383 ⫾ 6 95 ⫾ 2 7.7 ⫾ 0.3
P1
P2
P3
0.09 0.03 0.01 0.001 0.12
0.003 0.001 0.001 0.001 0.001
0.999 0.71 0.66 0.35 0.135
BMI, body mass index; P1, for main effect of SFA intake after adjusting for age and sex; P2, for significant main effect of cholesterol intake after adjusting for age and sex; P3, for significant combined effect of SFA and cholesterol intake after adjusting for age and sex; SFA, saturated fatty acid * Values are means ⫾ SEs adjusted for age and sex. SFA intakes ⱖ7% of total daily energy intake were defined as high and those ⬍7% as normal. Cholesterol intakes ⱖ300 mg/d were defined as high and those ⬍300 mg/d as normal.
tions was not significant. However, it has been reported that dietary cholesterol can increase LDL-C levels, although to a lesser extent than saturated fat [9,10]. Some studies have shown that there are synergistic effects between dietary cholesterol and saturated fat on the cholesterol level of plasma [9]. Kris-Etherton [19] indicated that SFAs could cause an increase in plasma total cholesterol concentrations. Differences in the results of other studies in this field compared with ours may be due to the consumption of different classes of SFA. Metabolic studies have found that different classes of SFA have different effects on plasma lipid and lipoprotein levels; specifically, SFAs with 12–16 carbon atoms tend to increase plasma total and LDL-C levels, whereas stearic acid does not have a cholesterol-raising effect [7]. Hence, assessment of these factors in future studies is recommended. Moreover, genetic studies have suggested a relation among apoE, apoA-IV, and serum LDL-C response to dietary fatty acid and cholesterol intakes in adults [9]. Despite the complicated association between dietary cholesterol and serum cholesterol, it has been recognized that the cholesterol content of the diet must be lower, especially in a subgroup of individuals who are highly responsive to changes in cholesterol intake [5,9]. Our study also showed the main effect of cholesterol intake on serum HDL concentrations was significant; subjects with a normal cholesterol intake had decreased HDL-C compared
with subjects with a high cholesterol intake. In other studies, decreased cholesterol intake was associated with a lower apoA-I lipoprotein and therefore decreased HDL-C [9,20]. Based on reports of different studies, HDL-C level affected by sex, age, BMI, physical activity, smoking, some hormones, disease and alcohol consumption, and nutritional factors had less of an effect on HDL-C [2,4,21]. Further research assessing these factors will provide stronger evidence of this relation. The present study showed no main effect of SFA and cholesterol intakes on triacylglycerols with and without adjustment of confounding factors. Dietary intake of subjects showed that total energy and fat intakes were lower in subjects whose cholesterol and SFA intakes were normal compared with subjects with high cholesterol and SFA intakes, whereas serum triacylglycerol concentration was higher in the former group compared with the latter group. Some experimental studies have shown no relation between plasma triacylglycerols and dietary fat intake [22]. The recommendations for energy and SFA intakes in therapeutic diets are different, although no positive or negative relations between percentage of fat intake and serum lipid have been observed [22–24]. Different factors that increase serum triacylglycerol levels include diet (high fat and refined carbohydrate), estrogens, alcohol, obesity, untreated diabetes, un-
Table 3 Comparison of lipid profiles in participants with normal and high SFA and cholesterol intakes* Serum concentration
Triacylglycerol (mg/dL) Total cholesterol (mg/dL) LDL-C (mg/dL) HDL-C (mg/dL)
Normal SFA intake
High SFA intake
Normal cholesterol intake (n ⫽ 77)
High cholesterol intake (n ⫽ 136)
Normal cholesterol intake (n ⫽ 110)
High cholesterol intake (n ⫽ 120)
147 ⫾ 81 187 ⫾ 37 118 ⫾ 29 10 ⫾ 39
114 ⫾ 168 44 ⫾ 186 39 ⫾ 118 10 ⫾ 37
72 ⫾ 126 42 ⫾ 190 36 ⫾ 124 11 ⫾ 41
75⫾ 133 39 ⫾ 186 33 ⫾ 120 10 ⫾ 40
P1
P2
P3
0.73 0.001 0.27 0.03
0.58 0.1 0.53 0.15
0.66 0.44 0.64 0.67
HDL-C, high-density lipoprotein cholesterol; LDL-C, low-density lipoprotein cholesterol; P1, for main effect of SFA intake; P2, for main effect of cholesterol intake; P3, for combined effect of SFA and cholesterol intake; SFA, saturated fatty acid * Values are means ⫾ SDs. SFA intakes ⱖ7% of total daily energy intake were defined as high and those ⬍7% as normal. Cholesterol intakes ⱖ300 mg/d were defined as high and those ⬍300 mg/d as normal.
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Table 4 Comparison of lipid profiles in participants with normal and high SFA and cholesterol intakes* Variable
Triacylglycerol (mg/dL) Total cholesterol (mg/dL) LDL-C (mg/dL) HDL-C (mg/dL)
Normal SFA intake
High SFA intake
Normal cholesterol intake (n ⫽ 77)
High cholesterol intake (n ⫽ 136)
Normal cholesterol intake (n ⫽ 110)
High cholesterol intake (n ⫽ 120)
11 ⫾ 146 5 ⫾ 180 4 ⫾ 114 1.4 ⫾ 36.7
7 ⫾ 160 3 ⫾ 183 2 ⫾ 115 0.8 ⫾ 37.9
13 ⫾ 147 5 ⫾ 183 5 ⫾ 117 1.5 ⫾ 36.1
7 ⫾ 138 3 ⫾ 189 3 ⫾ 122 0.9 ⫾ 39.7
P1
P2
P3
0.31 0.26 0.18 0.64
0.82 0.34 0.47 0.05
0.27 0.70 0.66 0.31
HDL-C, high-density lipoprotein cholesterol; LDL-C, low-density lipoprotein cholesterol; P1, for main effect of SFA intake after adjusting for age, sex, and body mass index; P2, for significant main effect of cholesterol intake after adjusting for age, sex, and body mass index; P3, for significant combined effect of SFA and cholesterol intake after adjusting for age, sex, and body mass index; SFA, saturated fatty acid * Values are means ⫾ SEs adjusted for age, sex, and body mass index. SFA intakes ⱖ7% of total daily energy intake were defined as high and those ⬍7% as normal. Cholesterol intakes ⱖ300 mg/d were defined as high and those ⬍300 mg/d as normal.
treated hypothyroidism, chronic renal disease, and hepatic disease [25]. This study showed that mean carbohydrate was higher in subjects who consumed normal saturated fat compared with subjects with a high saturated fat intake; thus, increased serum triacylglycerols in the former group may be due to the high consumption of carbohydrate; this has been shown in some studies, where increased dietary carbohydrate led to increased plasma triacylglycerol levels [26,27]. In contrast, increased levels of triacylglycerols in that group may be due in part to differences in physical activity. We did not use physical activity data because the reliability and validity of the Lipid Research Clinic questionnaire, which was used in the TLGS, had not been evaluated in our country. Lack of data on the physical activity of the subjects is a limitation of the present study. The mean of fiber intake was higher in subjects with high cholesterol intakes compared with subjects with normal cholesterol intakes, whereas there was no difference in LDL-C and total cholesterol between the two groups. Recent research has confirmed the cholesterol-lowering benefits of fiber and supported new recommendations for intake amounts to lower serum cholesterol [28]. In the present study subjects with high and normal cholesterol intakes consumed 3.2 g of fiber per 1000 cal, which is only 23% of the Institute of Medicine’s recommendation of 14 g of fiber per 1000 cal [29]. Therefore, the amount of fiber intake in all groups was less than the recommended dietary intake for its beneficial effect in lowering LDL-C. After adjusting for age and sex, the mean BMI of subjects with a high cholesterol intake was significantly greater than the BMI of those with a normal cholesterol intake (P ⬍ 0.01). As presented in Table 2, total caloric consumption and carbohydrate and fat intakes in the former group were higher compared with those in the latter group (P ⬍ 0.01). The results of this study indicate that cholesterol and saturated fat intakes have no combined effect on serum triacylglycerols, total cholesterol, and LDL-C, whereas cholesterol intake has a significant effect on serum HDL-C concentration.
Acknowledgments The authors express appreciation to the participants of the Tehran Lipid and Glucose Study and acknowledge the assistance given by Ms. N. Shiva in the language editing of the manuscript.
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