- Email: [email protected]
Very-low-fat diets may be associated with increased risk of metabolic syndrome in the adult population
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54
YCLNU2651_proof ■ 16 October 2015 ■ 1/9
Clinical Nutrition xxx (2015) 1e9
Contents lists available at ScienceDirect
Clinical Nutrition journal homepage: http://www.elsevier.com/locate/clnu
Original article
Q5
Very-low-fat diets may be associated with increased risk of metabolic syndrome in the adult population
Q4
Sunmin Park a, 1, Jaeouk Ahn b, 1, Byung-Kook Lee c, d, * a
Department of Food and Nutrition, Institute of Basic Sciences, Hoseo University, Asan, South Korea Department of Medical IT Engineering, Soonchunhyang University, Asan, South Korea c Department of Preventive Medicine, Soonchunhyang University, Asan, South Korea d Chungju Medical Center, Chungju, Chungbuk, South Korea b
a r t i c l e i n f o
s u m m a r y
Article history: Received 12 June 2015 Accepted 30 September 2015
Background & aims: Although fat intake has often been targeted to decrease the prevalence of metabolic syndrome; however decreasing dietary fat intake has not had this result. We studied the association between fat intake and the prevalence of metabolic syndrome in adults using KNHANES 2007e2013 data, a representative sample of the non-institutionalized civilian population. Methods: This cross-sectional study included 34,003 Korean adults aged 19 years. Adjusted odds ratios (OR) for the components of metabolic syndrome were measured according to fat intake (15, 15e25, 25% of daily energy intake) while controlling for covariates that affect metabolic syndrome using linear and logistic regression analysis while incorporating the sample weights for the complex sample design of the survey. Results: Surprisingly, the prevalence of metabolic syndrome was significantly higher in the 15% fat intake group (OR ¼ 1.277), accompanied by lower daily energy intake compared to the reference group (25% fat intake). Higher daily fat intake was associated with significantly lower ORs for four components of metabolic syndrome, except diabetes mellitus, using continuous variable analysis, whereas only three serum components (serum HDL, serum triglyceride, and blood pressure) exhibited significantly higher ORs in the lowest tertile of dietary fat intake (15%) compared with the reference group (25% fat-intake tertile). Subjects in a low-fat intake group had about 5.4 g polyunsaturated fatty acid/day that did not meet the recommended intake. Consumption of grain groups was a significant predictor of low fat intake, whereas milk food groups were significant predictors of not having low fat intake. Subjects in the low-fat group (15%) had much lower daily energy intake, by 500 kcal, compared with subjects who consumed high-fat diets (25%). All nutrients except carbohydrates had significantly lower mean values in the low-fat-intake group as compared to the high-fat-intake group. Conclusions: Low fat intake, <15%, was associated with a higher incidence of metabolic syndrome in the adult population, despite the daily energy intakes being lower by 500 kcal; this may be related to lower intake of various nutrients other than carbohydrates. © 2015 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved.
Keywords: Metabolic syndrome Fat intake Carbohydrate intake Energy intake HDL
1. Introduction Metabolic syndrome is defined by the presence of related cardiovascular disease risk factors including: insulin resistance,
* Corresponding author. Department of Preventive Medicine, Soonchunhyang University, 22 Soonchunhyang-Ro Shinchang-Myun, Asan 336-745, South Korea. Tel.: þ82 10 5437 0531. E-mail address: [email protected] (B.-K. Lee). 1 Sunmin Park and Jaeouk Ahn are equally contributed to this work.
abdominal obesity, dyslipidemia, hypertension, and a proinflammatory state [1]. Metabolic syndrome has been linked to the development of type 2 diabetes mellitus, atherosclerosis, some cancers, and a profoundly increased risk of morbidity and mortality [2]. Lifestyle interventions remain the primary mode of therapy for metabolic syndrome. Some risk factors, including high-fat diet, inactivity and estrogen deficiency, are well characterized [3]. Dietary patterns are important modifiable factors that may be useful for preventing the development of metabolic syndrome. However, the relationship between the metabolic syndrome and dietary patterns has not been fully elucidated, although a high-fat diet,
http://dx.doi.org/10.1016/j.clnu.2015.09.010 0261-5614/© 2015 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved.
Please cite this article in press as: Park S, et al., Very-low-fat diets may be associated with increased risk of metabolic syndrome in the adult population, Clinical Nutrition (2015), http://dx.doi.org/10.1016/j.clnu.2015.09.010
55 56 57 58 59 60 61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65
YCLNU2651_proof ■ 16 October 2015 ■ 2/9
2
S. Park et al. / Clinical Nutrition xxx (2015) 1e9
which leads to obesity and dyslipidemia, is a widely accepted risk factor for metabolic syndrome [4,5]. The traditional Asian diet is characterized as high in carbohydrates, with an abundance of vegetables, and has been considered beneficial for preventing metabolic syndrome in the Asian population [5,6]. However, the Westernization of lifestyle and dietary patterns may result in increased prevalence of metabolic syndrome in Asian countries. Fat consumption rose remarkably, from 7.2% to 19.0% of total energy consumption, between 1969 and 1998 in Korea [7,8]. Although during that time period the prevalence of metabolic syndrome had not been measured in the population, this increase is believed have contributed to the incidence of metabolic syndrome components. Fat intake has not markedly increased in KNHANES data since 1998, remaining at about 17e19% of total energy intake, although some parts of population have markedly increased their fat intake [7,8]. Interestingly, the incidence of metabolic syndrome increased markedly in Korea, by 6.5%, between 1998 and 2007, whereas from 2008 to 2012 it increased slowly, by 1.1% [7e9]. These results have suggested that an increase in fat intake to an average of ~20% may not promote metabolic syndrome. Previous studies have demonstrated that high carbohydrate intake (>60% of energy) increases the risk of metabolic syndrome in middle-aged Korean type 2 diabetic women [3], and high-carbohydrate diets (>57.4% of energy in men and >59.1% of energy in women) are associated with a low serum HDLecholesterol concentration in US men and high serum triglyceride in US women [10]. However, pregnant Korean women have higher fat intake (about 28% of energy intake) during pregnancy, and women with higher fat intake are more likely to develop gestational diabetes [11,12]. Thus, the role of dietary fat consumption in the development of metabolic syndrome in Koreans is not clear. Furthermore, US NHANES data indicate that the prevalence of metabolic syndrome components including obesity, high blood pressure, dyslipidemia, and diabetes increased from 1982 to 2006 in adults [13,14]. However, the intake of energy, saturated fat, polyunsaturated fat, and cholesterol did not change markedly between 1988 and 2008 in US adults aged 20e74 years; indeed, it was higher during 1971e1980 than during 1988e2008 [15]. On the other hand, the prevalences of obesity and insulin resistance increased substantially over 17 years in association with increases in the percent of total fat and protein in the diets of adults aged 25 years in the Framingham Heart Study Offspring Cohort (1991e2008) [16]. Furthermore, there are ethnic differences in macronutrient intake, and these may exert different influences on the development in metabolic syndrome [17]. Thus, the amount of fat and carbohydrate intake that is beneficial for reducing metabolic syndrome remains unclear. However, in nutritional education, high fat intake is considered the major cause of metabolic diseases because it is associated with a higher incidence of metabolic syndrome in Western countries [18]. Some people in Korea try to consume food that is lower in fat, but they may not have consumed as much fat as they need. The Korean dietary reference intake (KDRI) recommends fat consumption of around 25% of energy intake [19]. Some people consume too little fat, far below the KDRI recommendation, which results in diets high in carbohydrates and low in proteins [7,8]. Asians, including Koreans, have historically consumed highcarbohydrate, low-fat diets. Researchers have considered that this dietary pattern may not be beneficial in reducing the risk of metabolic syndrome. Therefore, we hypothesized that different fat intakes modified the components of metabolic syndrome in Korean adults. We studied the association between fat intake and the prevalence of metabolic syndrome in adults 19 years of age using the KNHANES 2007e2013 data, a representative sample of the noninstitutionalized civilian population.
2. Methods 2.1. Design and data collection This study utilized data obtained from the Korea National Health and Nutrition Examination Survey (KNHANES) 2007e2013, which includes KNHANES IV (2007e2009), KNHANES V (2010e2012) and KNHANES VI (2013) surveys. KNHANES surveys are conducted annually using a rolling sampling design that involves a complex, stratified, multistage probability-cluster survey of a representative sample of the non-institutionalized civilian population in South Korea. The KNHANES is a large representative population study with rigorous quality controls. The survey is performed by the Korean Centers for Disease Control and Prevention and the Korean Ministry of Health and Welfare. It has three components: a health interview, a health examination, and a nutrition survey. The survey was approved by the Institutional Review Board of the Korean Centers for Disease Control and Prevention (approval nos. 200804EXP-01-C, 2009-01CON-03-2C, 2010-02CON-21-C and 201307CON-03-4C). The present cross-sectional analysis was restricted to adults 19 years of age who completed the health examination survey and the nutrition survey (n ¼ 34,003). Detailed descriptions of the design of the survey have been reported previously [20]. Briefly, the participants ages, education, smoking histories and alcohol intakes were obtained during the health interview. Height and weight measurements were performed, with the participants wearing light clothing and no shoes. Body mass index (BMI) was calculated as weight in kilograms divided by the square of the height in meters (kg/m2). Obesity was categorized into three groups according to the Asian obesity definition by recommended by International Obesity Task Force and the World Health Organization (WHO) Regional Office for the Western Pacific Region [21,22]: lean (BMI < 18.5), normal (18.5 BMI < 25), and obese (BMI 25). Age reported at the time of the health interview was categorized into five groups. Area of residence was categorized into urban (administrative divisions of a city) and rural areas (not classified as administrative divisions of a city). Income level was categorized into four quartile groups (1st Qe4th Q). Education level was categorized into three groups: below high school, high school, and college or higher. Occupation was categorized into four groups: clerical, manual, technical, and unemployed. Smoking status was divided into three categories: current smoker, past smoker and never-smoker. Smoking status was defined based on self-reported cigarette use: never-smokers had smoked less than 100 cigarettes in their lifetime; participants who had smoked 100 or more cigarettes were considered past or current smokers, based on current tobacco use. Alcohol consumption was assessed by asking the participants about their drinking behavior during the month prior to the interview, including their average frequency (days per month) of alcoholic beverage consumption and amount (in mL) of alcoholic beverages ingested on a single occasion. The responses were converted into the amount of pure alcohol (in grams) consumed per day. Alcohol consumption status was categorized into four groups according to average daily alcohol consumption: nondrinkers, and light (1e15 g), moderate (16e30 g), and heavy (>30 g) drinkers. Regular exercise was defined as regular exercising 30 min at a time at least five times per week, as moderate exercise activities (swimming slowly, playing doubles tennis or volleyball, and participating in occupational or recreational activities while carrying light objects), or for 20 min at a time at least three times per week in vigorous exercise activities (running, climbing, cycling fast, swimming fast, playing football, basketball, squash or
Please cite this article in press as: Park S, et al., Very-low-fat diets may be associated with increased risk of metabolic syndrome in the adult population, Clinical Nutrition (2015), http://dx.doi.org/10.1016/j.clnu.2015.09.010
66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65
YCLNU2651_proof ■ 16 October 2015 ■ 3/9
S. Park et al. / Clinical Nutrition xxx (2015) 1e9
3
singles tennis, jumping rope and participating in occupational or recreational activities while carrying heavy objects).
food frequency questionnaire (FFQ) in 2012, only 5 years' data (2007e2011) were used for dietary assessment and food grouping.
2.2. Definition of metabolic syndrome
2.6. Statistical analysis
Based on the 2005 revised National Cholesterol Education Program-Adult Treatment Panel III criteria and the Korean Society for the Study of Obesity criteria for waist circumference, metabolic syndrome was defined as the presence of three or more of the following: 1) elevated blood pressure (average systolic blood pressure 130 mmHg or diastolic blood pressure 85 mmHg) or current blood pressure medication use; 2) low HDL-cholesterol level (<40 mg/dl); 3) elevated serum TG level (150 mg/dl) or current anti-dyslipidemic medication use; 4) elevated fasting blood glucose level (100 mg/dl) or current anti-diabetic medication use; and 5) abdominal obesity (waist circumference 90 cm) [12,16,17].
Statistical analyses were performed using SAS software (version 9.4; SAS Institute, Cary, NC, USA) and SUDAAN (Release 11.0; Research Triangle Institute, Research Triangle Park, NC, USA), a software package that incorporates sample weights and adjusts analyses for the complex sample design of the survey. Survey sample weights were used in all analyses to produce estimates that were representative of the non-institutionalized civilian Korean population. Descriptive statistics of participants according to daily fat intake (%) were obtained by determining frequency distributions of categorical demographic variables; lifestyle factors and the presence of metabolic syndrome components, and statistical significances were determined using chi-squared tests. Adjusted odds ratios (ORs) and 95% confidence intervals (CI) for metabolic syndrome and its components according to daily fat intake (15.0, 15.0e25.0, <25.0%) were calculated using logistic regression analysis after covariate adjustment. Covariates were sex, age, residence area, occupation, income, education level, drinking status, obesity, and physical activity. Next, to evaluate the associations of selected study variables and 11 food intake groups obtained from the food frequency questionnaire with daily fat intake status, adjusted ORs for low fat intake (15.0%) were calculated using ordinal logistic regression analysis after covariate adjustment. Finally, adjusted means and 95% CIs of daily nutrient intakes according to daily fat intake (%) were calculated using analysis of covariance (ANCOVA). The covariates used for adjusted means were sex, age, residence area, income, occupation, drinking status, education, stress level, obesity, and physical activity.
2.3. Laboratory testing Blood samples were obtained in the morning following an overnight fast. The serum concentrations of glucose, high-density lipoprotein cholesterol (HDL), triglycerides (TG), aspartate transaminase (AST), and alanine transaminase (ALT) were measured using a Hitachi automatic analyzer 7600 (Tokyo, Japan). Lowdensity lipoprotein cholesterol (LDL) was calculated using the Friedewald equation [LDL ¼ total cholesterol e HDL e (TG/5.0)] if the TG concentration was not above 400 mg/dl. When the TG concentration was above 400 mg/dl, TG was measured directly using a Hitachi automatic analyzer 7600. All clinical analyses were performed by the Neodin Medical Institute, a laboratory certified by the Korean Ministry of Health and Welfare. 2.4. Assessment of nutrient intake All subjects were instructed to maintain their usual dietary habits prior to the assessment of dietary intake. Daily nutrient intake was measured using the 24-h recall method. The 24h dietary recalls were conducted through in-person interviews by trained dietary staff in mobile examination centers to explore food kinds and amounts that the subjects consumed for the past 24 h (midnight to midnight). Daily intake of calories and nutrients was calculated from the information of food intake acquired from interviewing using the Can-Pro 2.0 nutrient intake assessment software developed by the Korean Nutrition Society. Daily consumption of saturated, monounsaturated and polyunsaturated fatty acids were additionally estimated from the 24-h recall data by adding the data from fatty acid composition of foods tables into the nutrient data [23]. 2.5. Dietary assessment method and food grouping Dietary intake information was collected by administering a validated semi-quantitative food-frequency questionnaire to each participant. Food-frequency questionnaires used in KNHANES were developed and validated by the Ministry of Health and Welfare [24]. This questionnaire requested information regarding the participant's consumption of 63 food items. The participant's food intake frequency was quantified using nine categories: never or seldom, once a month, two to three times a month, one to two times a week, three to four times a week, five to six times a week, once a day, twice a day, and three times or more every day. Sixtythree food items were further categorized into 11 subgroups: grain 1 (rice, breads and noodles), grain 2 (cereals, rice cakes and potatoes), legumes, meat, fish, vegetables, fruit, milk, sugar, and other. Since KNHANES changed the data collection format for the
3. Results Subject characteristics by classification variables according to daily fat intake percentage are shown in Table 1. All of the classification variables were significantly different among groups, with significance levels of p < 0.01 for all variables except exercise and walking, for which the significance level was p < 0.05. As age increased, the proportion of participants reporting low fat intake (15.0%) increased significantly. The prevalence of metabolic syndrome was stable from 2007 to 2013, nor did any of the components of metabolic syndrome change, except the prevalence of diabetes, which was increased (Fig. 1). During the 2007e2013 time period, the percentage of people who consumed more than 25% of their calories in the form of fat gradually increased, and the prevalence of metabolic syndrome significantly declined according to daily fat intake (%) in the 40e49-, 50e59-, and 60-year age groups (Fig. 2). As age increased, fat intake decreased (Fig. 2). Adjusted ORs and 95% CI values were calculated for metabolic syndrome and its components according to daily fat intake percentages (units ¼ 5) as a continuous independent variable and according to the three categorized daily fat intake groups (15.0, 15.0e25.0, and 25.0%) after adjusting for covariates (Table 2) which were: sex, age, residence area, income, occupation, smoking and drinking status, education level, obesity, and physical activity. The adjusted ORs and 95% CI for metabolic syndrome after adjustment of covariates were 1.0696 (1.0434e1.0964) based on daily fat intake percentage (5% changes) as a continuous independent variable, and 1.2277 (1.0862e1.3877) for categorized daily fat intake analysis, indicating that 22.8% more people had metabolic syndrome in the low-fat (15.0%) compared with the high-fat-
Please cite this article in press as: Park S, et al., Very-low-fat diets may be associated with increased risk of metabolic syndrome in the adult population, Clinical Nutrition (2015), http://dx.doi.org/10.1016/j.clnu.2015.09.010
66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65
YCLNU2651_proof ■ 16 October 2015 ■ 4/9
4
S. Park et al. / Clinical Nutrition xxx (2015) 1e9
Table 1 General characteristics grouped by daily fat intake in the Korean adult population according to KNHANES 2007e2013. Fat intake (energy %)a
Classification
15.0 N (%) All Gender Age group
Residence area Income
Occupation
Smoking status
Drinking status
Education level
Obesity
Exercise Walk Year
Metabolic syndrome a b
Male Female 19e29 30e39 40e49 50e59 60e Urban Rural 1st Q 2nd Q 3rd Q 4th Q Clerical Manual Technical Unemployed Non smoker Past smoker Current smoker Non drinker Mild drinker Moderate drinker Heavy drinker Less than High School High School College Lean Normal Obese Yes No Yes No 2007 2008 2009 2010 2011 2012 2013 Yes No
16,502 6405 10,097 736 1877 2582 3521 7786 11,439 5063 4433 4226 3949 3606 4603 3746 1210 6943 10,221 3304 2977 6228 7026 1675 1573 11,258 2524 2720 595 10,370 5503 3437 13,065 6753 9749 1375 3004 3195 2413 2395 2211 1909 4641 11,861
(42.62) (39.67) (45.25) (19.12) (27.86) (39.65) (54.35) (70.75) (39.59) (54.57) (47.28) (43.3) (40.78) (38.55) (33.65) (60.68) (39.94) (47.3) (44.45) (43.95) (37.56) (53.51) (37.66) (40.43) (41.56) (56.31) (35.68) (26.58) (32.82) (42.41) (44.68) (41.73) (42.87) (42.54) (42.68) (45.89) (46.33) (46.15) (43.12) (40.75) (39.44) (38.69) (55.11) (39.49)
p valueb 15.0e25.0 N (%)
25.0 N (%)
12,120 5176 6944 1559 3018 2797 2208 2538 9868 2252 2625 2900 3103 3316 5260 1474 1153 4233 7120 2343 2657 3203 6321 1331 1265 5227 2668 4225 581 7768 3698 2590 9530 4764 7356 857 1906 2164 1869 1907 1751 1666 2268 9852
5381 2204 3177 1350 1610 1101 643 677 4577 804 1068 1330 1392 1515 2672 418 409 1882 3174 966 1241 1157 3051 579 594 1765 1215 2401 300 3475 1573 1196 4185 2200 3181 286 697 873 815 892 873 945 763 4618
(38.36) (40.53) (36.42) (43.14) (46.79) (43.29) (35.19) (22.93) (40.02) (31.82) (35.63) (37.38) (39.3) (41.55) (43.17) (28.9) (43.7) (34.61) (37) (38.3) (41.42) (32.87) (40.69) (40.59) (38.53) (31.77) (42.47) (45.58) (42.97) (38.5) (37.25) (37.73) (38.53) (37.55) (38.9) (39.51) (38.24) (36.64) (38.09) (39.06) (38.82) (38.69) (32.36) (39.87)
(19.02) (19.8) (18.32) (37.73) (25.35) (17.06) (10.46) (6.32) (20.39) (13.61) (17.09) (19.33) (19.92) (19.9) (23.18) (10.43) (16.36) (18.09) (18.56) (17.75) (21.03) (13.62) (21.65) (18.98) (19.91) (11.92) (21.85) (27.84) (24.2) (19.08) (18.07) (20.54) (18.6) (19.91) (18.42) (14.59) (15.43) (17.22) (18.79) (20.19) (21.74) (22.62) (12.53) (20.65)
0.01 0.01 0.01
0.01 0.01
0.01
0.01
0.01
0.01
0.01
0.05 0.05 0.01
0.01
Fat intake was calculated by the percentage of total energy intake. P value for Satterwaite Chisquare.
intake group (25.0%) (Table 2). In the analysis of components of metabolic syndrome as dependent variables, in the continuous variable analysis, the ORs for four components of metabolic syndrome were significantly influenced by daily fat intake, the exception being diabetes mellitus; when categorized daily fat intake was used, only three components (HDL, Triglyceride and blood pressure) had significant ORs. Next, ORs for low fat intake were calculated after adjusting for covariates according to classification variables using ordinal logistic regression analysis with three levels of the response variable (daily fat intake: 15.0, 15.0e25.0 and <25.0%) (Table 3). Among classification variables, age was significant predictor of low fat intake; as age increased, the prevalence of low fat intake also increased. On the other hand, the higher income and higher education level groups, past and current smokers, and those living in an urban area were significantly less likely to have a low fat intake than the reference groups. It is interesting that manual labor workers consumed less fat than clerical workers did when compared with unemployed subjects. The remaining classification
variables, including obesity, exercise and walk, and drinking status were not significantly associated with fat intake in the categorical analysis (see Table 4). Q1 To investigate the association of metabolic syndrome with daily fat intake calculated from 24-h recall and food groups obtained using the semi-quantitative food frequency questionnaire, adjusted ORs and 95% CI for low fat intake were calculated using ordinal logistic regression analysis according to 11 food groups after covariates adjustment. Grain groups 1 and 2 were significant predictors of low fat intake, whereas milk and sugar groups were significant predictors for not having low fat intake. Others food groups, such as legumes, meat, fish, vegetables, and fruits, were marginally significant predictors of high fat intake compared with reference groups, although the vegetable group showed inconsistent results. Finally, to clarify the association of nutrient intake according to daily fat intake percentage, the adjusted means and 95% CIs according to daily fat intake percentages were calculated by ANCOVA (Table 5) after covariate adjustment. As expected, the daily intake of macronutrients such as carbohydrates, protein and fats
Please cite this article in press as: Park S, et al., Very-low-fat diets may be associated with increased risk of metabolic syndrome in the adult population, Clinical Nutrition (2015), http://dx.doi.org/10.1016/j.clnu.2015.09.010
66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65
YCLNU2651_proof ■ 16 October 2015 ■ 5/9
S. Park et al. / Clinical Nutrition xxx (2015) 1e9
5
Fig. 1. Changes in the prevalence of metabolic syndrome and each component and in the percentage of people reporting 25% fat intake during 2007e2013. METS, the percentage of metabolic syndrome; WC, the percentage of 90 cm waist circumference; HDL, the percentage of <40 mg/dl serum HDL cholesterol; TG, <150 mg/dl serum triglyceride, BP, the percentage of systolic blood pressure 130 mmHg or diastolic blood pressure 85 mmHg; DM, the percentage of 100 mg/dl fasting blood glucose; Fat >25%, the percentage of >25% fat intake from total energy intake.
differed significantly among three fat-intake groups. Daily energy intake was higher as fat intake increased. Except for carbohydrates, mean values for nutrients were significantly lower in the low e as compared with the high-fat-intake group. The amount of each category of fatty acids (saturated, monounsaturated, and polyunsaturated) consumed from total fats was also significantly higher among all three groups: as total fat intake increased. The ratios of saturated, monounsaturated and polyunsaturated fatty acids were within the recommended range in the low-fat-intake group but the medium-fat and high-fat intake groups had lower ratios of PUFA intake than the low-fat-intake group and were lower than the ratio recommended for PUFA. Thus, a low fat intake (less than 15% fat) was associated with the higher incidence of metabolic syndrome regardless of the ratio of saturated, monounsaturated and polyunsaturated fatty acid. 4. Discussion Fat intake has often been targeted for reducing the prevalence of metabolic diseases, but this strategy has not decreased metabolic syndrome in the USA. Although the consumption of fat among Koreans has gradually increased, it is still much less than that of Americans in NHANES [25]. Data from this study of the Korean adult population can be used to examine the association of low dietary fat intake with the incidence of metabolic syndrome. Our data suggested that the prevalence of metabolic syndrome was significantly higher in the low-fat-intake group (15% of intake) compared with the high-fat-intake group (25%). Higher dietary fat intake was significantly associated with lower risk for four components of metabolic syndrome, the exception being high fasting blood glucose. The ratios of saturated, monounsaturated
and polyunsaturated fatty acids from total fat intake were within the recommended ranges regardless of different fat intake groups [19]. Interestingly, subjects in the low-fat group (15%) had much lower daily intake of energy (by 500 kcal) and of almost all nutrients except carbohydrates compared with the high-fat group (25%). These results suggest that metabolic syndrome may be related to sub-optimal intakes of nutrients other than carbohydrates in the Korean population. Metabolic syndrome is associated with major cardiovascular risk factors including insulin resistance, dyslipidemia, hypertension, nonalcoholic fatty liver disease, hyperuricemia, a prothrombotic state, and chronic inflammation [1]. Obesity is a welldocumented risk factor for metabolic syndrome. The prevention of metabolic syndrome can reduce the chance of developing cardiovascular diseases [1,2]. In NHANES I, II, III data, participants of both genders exhibited increased intake of calories in the form of fat, to about 33%, and of saturated fat, reaching approximately 11%, from 1971e1974 to 1999e2000 [15]. The intake of energy and in terms of calories and carbohydrates has increased. However, the overall trend in the US was an increased prevalence of obesity, but an unchanged prevalence of metabolic syndrome during this time period [13,14]. Thus, total energy intake is a key regulator of obesity, and the percentage of energy intake from of fat may affect the risk of metabolic syndrome independently from obesity. This present study demonstrated that subjects who consumed low-fat diets had increased likelihood of metabolic syndrome, although their total energy intake was lower than that of other subjects who consumed more. Additionally, the prevalence of metabolic syndrome was stable from 2007 to 2013, although the percentage of people who consumed more than 25% of calories from fat increased from 15 to 20%. Thus, the increase in fat intake among the Korea population
Please cite this article in press as: Park S, et al., Very-low-fat diets may be associated with increased risk of metabolic syndrome in the adult population, Clinical Nutrition (2015), http://dx.doi.org/10.1016/j.clnu.2015.09.010
66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65
YCLNU2651_proof ■ 16 October 2015 ■ 6/9
6
S. Park et al. / Clinical Nutrition xxx (2015) 1e9
Fig. 2. Prevalence of metabolic syndrome and each component in age category tertiles (40e49, 50e59, and 60 years old). METS, the percentage of metabolic syndrome; WC, the percentage of 90 cm waist circumference; HDL, the percentage of <40 mg/dl serum HDL cholesterol; TG, <150 mg/dl serum triglyceride, BP, the percentage of systolic blood pressure 130 mmHg or diastolic blood pressure 85 mmHg; DM, the percentage of 100 mg/dl fasting blood glucose.
may not lead to an increased risk of metabolic syndrome, but people who consume very little fat may be susceptible to metabolic syndrome. The optimal composition of marcronutrients in the diet is still controversial [11,16e18,26]. In terms of calories, fat intake is usually comparable to protein intake and opposite to carbohydrate intake [15,16]. High fat intake is believed to exacerbate obesity, metabolic syndrome, and certain cancers, even given constant caloric intake [11,27]. However, recent studies have shown that high-carbohydrate diets also increases the risk of metabolic syndrome. A recent meta-analysis in overweight and obese patients [28] demonstrated that low-fat diets (about 9.3% and 25e30% of total energy consumption from saturated fat and total fat, respectively) resulted in lower total cholesterol and LDL cholesterol in long-term randomized clinical trials compared with high-fat diets. However, low-fat diets may lead to increased circulating triglycerides and decreased HDL cholesterol [10,29]. In the present study, the Korean adults generally consumed low-fat diets, although fat intake has increased. When adults were divided into three categories by fat intake, adults in the lowest fat group were at greater risk of metabolic syndrome, except for blood glucose levels. These difference in results compared with previous studies may reflect a difference in the definition of fat percentage in the diet. In the present study, low- and high-fat diets were defined as <15% and >25% of energy intake, respectively, and the average intake of fat in the low-fat and high-fat groups constituted 15% and 33.5% of calories consumed. Thus, most of the adults in the high-fat-diet group in the present study consumed what the Schwingshack and Hoffmann study would have considered to be a low-fat-diet [28]. Thus, >15% dietary fat may be optimal to prevent metabolic syndrome.
Another meta-analysis study [29] showed the long-term (12 months) effects of low- and high-fat diets on serum lipid and glucose profiles in people with pre-diabetes and type 2 diabetes in randomized clinical trials. A high-fat diet was found to result in significant decreases in serum triglyceride and glucose levels in a fasting state and in diastolic blood pressure, as well as a significant increase in HDL-cholesterol levels. Thus, that study suggested that a high-fat diet may not be detrimental for managing blood glucose levels in pre-diabetic and type 2 diabetic patients. However, the present study demonstrated that the prevalence of diabetes, defined as an elevated fasting blood glucose level (100 mg/dl) or current anti-diabetic medication use, was not altered by dietary fat consumption. Additionally, unlike other components of metabolic syndrome, the prevalence of hyperglycemia continuously increased as the dietary fat consumption increased 2007 to 2013 in the present study. These results suggest that among Korean adults, fat intake of >25% of total calories may be detrimental to blood glucose regulation and increase the risk of type 2 diabetes. Furthermore, Korean pregnant women, the prevalence of gestational diabetes mellitus is associated with higher maternal weight gain at 24e28 weeks of gestation and is positively related to higher energy and fat intake, especially from saturated fat [11,12]. Therefore, more studies are needed to determine the optimal fat intake for preventing metabolic syndrome in the Korean population. A high-protein diet does not have a beneficial or detrimental effect in terms of weight management. Recent meta-analyses [30] have shown that neither low (about 15% of calories) nor high (25e30% of calories) protein in low-fat diets (20e30% of calories) has any effect on outcome markers for obesity, cardiovascular disease, or glycemic control in long-term randomized clinical trials. Thus, dietary protein content may not play a major role in
Please cite this article in press as: Park S, et al., Very-low-fat diets may be associated with increased risk of metabolic syndrome in the adult population, Clinical Nutrition (2015), http://dx.doi.org/10.1016/j.clnu.2015.09.010
66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65
YCLNU2651_proof ■ 16 October 2015 ■ 7/9
S. Park et al. / Clinical Nutrition xxx (2015) 1e9
Q3
Table 2 Adjusted odds ratios for metabolic syndrome and its components according to fat intake. Outcome
Classification of fat intake
Metabolic syndrome
Fat intake energy Fat intake 15.0% 15.0e25.0% 25.0% Fat intake energy Fat intake 15.0% 15.0e25.0% 25.0% Fat intake energy Fat intake 15.0% 15.0e25.0% 25.0% Fat intake energy Fat intake 15.0% 15.0e25.0% 25.0% Fat intake energy Fat intake 15.0% 15.0e25.0% 25.0% Fat intake energy Fat intake 15.0% 15.0e25.0% 25.0%
Waist circumference
Serum HDL
Serum triglyceride
Blood pressure
Diabetes mellitus
Odds ratio (95% CI)c
% (unit ¼ 5)a
1.0696 (1.0434e1.0964)
% (unit ¼ 5)
1.2277 (1.0862e1.3877) 1.0638 (0.931e1.2155) Ref (1.0)b 1.044 (1.0117e1.0773)
% (unit ¼ 5)
1.1424 (0.9848e1.3251) 1.0784 (0.9314e1.2486) Ref (1.0) 1.0574 (1.0359e1.0794)
% (unit ¼ 5)
1.1703 (1.0573e1.2954) 1.0297 (0.9321e1.1375) Ref (1.0) 1.0586 (1.0387e1.0788)
% (unit ¼ 5)
1.2336 (1.1292e1.3477) 1.0499 (0.9651e1.1421) Ref (1.0) 1.0441 (1.0207e1.0681)
% (unit ¼ 5)
1.2119 (1.0733e1.3685) 1.167 (1.0298e1.3223) Ref (1.0) 1.0139 (0.993e1.0353)
Table 3 Adjusted odds ratios for having low fat intake according to classification variables.
Gender Age group (yrs)
Income
Occupation
Education level
Smoking status
Drinking status
Obesity
Exercise
a
The adjusted odds ratio in continuous decrease of fat intake (energy %). b Reference group. c Adjusted for gender, age, residence area, income, occupation, smoking and drinking status, education, obesity, and physical activities.
Odds ratios (95% CI)b
Classification
Residence area
1.0295 (0.9298e1.1399) 0.9619 (0.8685e1.0653) Ref (1.0)
7
Walk
Male Female 19e29 30e39 40e49 50e59 60e Urban Rural 1st Q 2nd Q 3rd Q 4th Q Clerical Manual Technical Unemployed Less than High School High School College Non smoker Past smoker Current smoker Non drinker Mild drinker Moderate drinker Heavy drinker Lean Normal Obese Yes No Yes No
0.946 (0.863e1.037) Ref (1.0)a Ref (1.0) 1.739 (1.556e1.944) 2.596 (2.297e2.933) 3.953 (3.47e4.504) 6.839 (5.972e7.834) 0.802 (0.723e0.889) Ref (1.0) Ref (1.0) 0.892 (0.809e0.983) 0.876 (0.795e0.965) 0.818 (0.739e0.905) 0.806 (0.745e0.871) 1.279 (1.133e1.442) 0.938 (0.832e1.059) Ref (1.0) Ref (1.0) 0.821 (0.752e0.897) 0.667 (0.602e0.74) Ref (1.0) 0.863 (0.778e0.957) 0.861 (0.779e0.951) Ref (1.0) 0.857 (0.791e0.927) 0.933 (0.833e1.045) 1.041 (0.92e1.177) Ref (1.0) 0.997 (0.866e1.146) 0.967 (0.835e1.119) 0.964 (0.898e1.036) Ref (1.0) 1.033 (0.969e1.1) Ref (1.0)
a
Reference group. Adjusted for gender, age, residence area, income, occupation, smoking and drinking status, education, obesity, and physical activities. b
developing metabolic syndrome. Although protein intake of 0.826 g/kg body weight/day is recommended for adults [19], the actual protein intake in this study was greater than this recommendation because Koreans acquire protein from grains. The adults in a low-fat-diet group consumed protein much less than the other groups did, although the average consumption reached the recommended level. These results suggest that the protein intake in the low-fat group may not be sufficient and may also increase the risk for metabolic syndrome. The recommended intake of protein may not be sufficient for Korean adults when dietary patterns are considered. The low-fat diet may represent improper food intake and less variety of foods. The food frequency data showed that a higher intake of grain groups increased the risk of metabolic syndrome, but higher milk consumption was associated with a lower risk in the present study. Moreover, the proper intake of meat, fish, and fruit was related to a lower risk of metabolic syndrome. However, compared with deficient intake, proper intake of vegetables increased the risk of metabolic syndrome somewhat. These results indicate that a diet of mainly grain and vegetables, considered a Korean-style diet, may be associated with elevated risk of metabolic syndrome. A recent study [31] supported these observations: consuming a wide variety of healthful foods, as measured by the healthy food variety index, was associated with lower ORs for metabolic syndrome and hypertension, waist circumference, and fasting serum glucose levels in the US population based on NHANES 2003e2006 data. Furthermore, based on the KNHAES data, a balanced Korean diet is associated a lower OR for metabolic syndrome in women only and lower blood pressure in both genders when dietary patterns are categorized as a balanced Korean
Table 4 Adjusted odds ratio for having low fat intake according to food groups. Odds ratio (95% CI)b
Classification Grain group 1
Grain group 2
Legume group
Meat group
Fish group
Meat and fish group
Vegetable group
Fruits group
Milk group
Deficient Proper Excessive Deficient Proper Excessive Deficient Proper Excessive Deficient Proper Excessive Deficient Proper Excessive Deficient Proper Excessive Deficient Proper Excessive Deficient Proper Excessive Deficient Proper Excessive
Ref (1.0)a 1.138 (1.03e1.257) 1.189 (1.086e1.302) Ref (1.0) 1.054 (0.825e1.347) 1.762 (1.023e3.033) Ref (1.0) 0.874 (0.802e0.951) 0.977 (0.905e1.055) 1 (1e1) 0.859 (0.79e0.934) 1.106 (0.93e1.315) Ref (1.0) 0.698 (0.638e0.763) 0.86 (0.674e1.099) Ref (1.0) 0.857 (0.753e0.976) 0.919 (0.428e1.977) Ref (1.0) 1.13 (1.057e1.209) 0.973 (0.822e1.153) Ref (1.0) 0.87 (0.816e0.927) 0.962 (0.747e1.239) Ref (1.0) 0.678 (0.634e0.725) 0.431 (0.312e0.596)
a
Reference group. Adjusted for gender, age, residence area, income, occupation, smoking and drinking status, education, obesity, and physical activities. b
Please cite this article in press as: Park S, et al., Very-low-fat diets may be associated with increased risk of metabolic syndrome in the adult population, Clinical Nutrition (2015), http://dx.doi.org/10.1016/j.clnu.2015.09.010
66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 Q2 64 65
YCLNU2651_proof ■ 16 October 2015 ■ 8/9
8
S. Park et al. / Clinical Nutrition xxx (2015) 1e9
Table 5 Daily nutrient intake grouped by daily fat intake in KNHANES 2007e2013. Nutrients
Total energy (kcal) Protein (g) Carbohydrate (g) Dietary fiber (g) Total fats (g) Saturated fatty acid (SFA, g) Monounsaturated fatty acid (MUFA, g) Polyunsaturated fatty acid (PUFA, g) Ratio of SFA:MUFA:PUFA
Daily fat intake (energy%)
p value
15.0
15.0e25.0
25.0
1837 (1820e1854)a 59.8 (59.1e60.4) 328.0 (324.9e331.1) 7.182 (7.059e7.306) 21.5 (21.2e21.8) 5.92 (5.63e6.21) 6.11 (5.79e6.43) 5.98 (5.67e6.29) 1:1.03:1.01
2032 (2013e2051) 75.3 (74.5e76.2) 316.5 (313.7e319.3) 7.850 (7.700e8.000) 44.0 (43.6e44.4) 13.1 (12.7e13.5) 14.4 (14.0e14.8) 11.8 (11.4e12.2) 1:1.11:0.90
2338 (2304e2372) 93.4 (91.7e95.0) 294.3 (290.0e298.6) 7.809 (7.632e7.985) 82.0 (80.5e83.5) 25.3 (23.9e26.7) 29.4 (27.9e30.9) 20.0 (18.9e21.1) 1:1.16:0.79
<0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001
Adjusted for gender, age, residence area, income, occupation, smoking and drinking status, education, obesity, and physical activities. a Means (95% CI).
diet, unbalanced Korean diet, and semi-Western diet, using principal component analysis [32]. The women in the group who consumed a balanced Korean diet had higher intake of fat, protein, and other micronutrients such as vitamin C, vitamin A, and calcium but lower intake of carbohydrates. Thus, diets with low energy and low-fat contents may not be beneficial for decreasing the risk of metabolic syndrome. To the best of our knowledge, this study is the first to determine the positive association of low fat intake and metabolic syndrome in a large representative sample of the Korean population. However, this study has some limitations. First, this was a cross-sectional study, so the results do not represent causeeeffect relationships. Because people who had metabolic syndrome had lower energy intake and a low-fat diet compared with those who did not have this syndrome, our analysis is based on a negative association that requires clarification. Second, the fatty acid composition of fat consumed, i.e., saturated, monounsaturated, and polyunsaturated fatty acids, was not examined because it was not provided in the KNHANES data; however, the fatty acid composition may be more important for the prevalence of metabolic syndrome than just total fat itself [4]. Third, food intake could be under-reported knowingly or accidentally, despite the survey's being conducted by trained dieticians. Fourth, the usual nutrient intake including fat was determined by food intake based on 24-h recall data in KNHANES. This procedure may introduce some bias in the investigation of typical nutrient intake despite the skill of dieticians administering the measure, as some subjects may not accurately report their food intakes due to mistaken memories or other personal reasons. Additionally, food intake is quite different on weekdays than it is on weekends. Although the 3-day food record is the gold standard for determining typical intake levels [27], considering the expense and accuracy of self-recording food consumption, the 24-h recall can be an appropriate method for estimating actual and typical intakes. In conclusion, a diet of less than 15% fat intake increased the prevalence of metabolic syndrome despite the lower daily energy intake, by 500 kcal, in the adult population, and metabolic syndrome may be related to sub-optimal intakes of nutrients other than carbohydrates. The fatty acid composition of subjects with low fat dietary intakes in the adult population may not satisfy international PUFA recommendation for a lower risk of metabolic syndrome. Further studies are needed to identify how much fat intake, especially PUFA, is beneficial to prevent metabolic syndrome in adults. Conflict of interest None.
Acknowledgment S. P. and B.K.L. designed research and wrote the paper. B.K.L and J.A. conducted the statistical analysis. B.K.L. had primary responsibility for final content. All authors read and approved the final manuscript. References [1] Tchernof A. Visceral adipocyte and the metabolic syndrome. Nutr Rev 2007;65:S24e9. [2] Potenza MV, Mechanick JI. The metabolic syndrome: definition, global impact, and pathophysiology. Nutr Clin Pract 2009;24:560e77. [3] Kim WY, Kim JE, Choi YJ, Huh KB. Nutritional risk and metabolic syndrome in Korean type 2 diabetes mellitus. Asia Pac J Clin Nutr 2008;17:47e51. [4] Lottenberg AM, Afonso Mda S, Lavrador MS, Machado RM, Nakandakare ER. The role of dietary fatty acids in the pathology of metabolic syndrome. J Nutr Biochem 2012;23:1027e40. [5] Misra A, Singhal N, Khurana L. Obesity, the metabolic syndrome, and type 2 diabetes in developing countries: role of dietary fats and oils. J Am Coll Nutr 2010;29:289Se301S. [6] Park HS, Oh SW, Cho SI, Choi WH, Kim YS. The metabolic syndrome and associated lifestyle factors among South Korean adults. Int J Epidemiol 2004;33:328e36. [7] Korean Ministry of Health and Welfare. The Korean National Health Nutrition Examination Survey 1998. Seoul: Korean Ministry of Health and Welfare; 1999. [8] Korean National Statistical Office. 2000 report of statistics in mortality in Korean. Daejeon: Korean National Statistical Office; 2001. [9] Lim S, Shin H, Song JH, Kwak SH, Kang SM, Won Yoon J, et al. Increasing prevalence of metabolic syndrome in Korea: the Korean National Health and Nutrition Examination Survey for 1998e2007. Diabetes Care 2011;34: 1323e8. [10] Yang EJ, Chung HK, Kim WY, Kerver JM, Song WO. Carbohydrate intake is associated with diet quality and risk factors for cardiovascular disease in U.S. adults: NHANES III. J Am Coll Nutr 2003;22:71e9. [11] Park S, Kim MY, Baik SH, Woo JT, Kwon YJ, Daily JW, et al. Gestational diabetes is associated with high energy and saturated fat intakes and with low plasma visfatin and adiponectin levels independent of prepregnancy BMI. Eur J Clin Nutr 2013;67:196e201. [12] Park S, Kim MH, Kim SH. Early gestational weight gains within current recommendations result in increased risk of gestational diabetes mellitus among Korean women. Diabetes Metab Res Rev 2014;30:716e25. [13] Mozumdar A, Liguori G. Persistent increase of prevalence of metabolic syndrome among U.S. adults: NHANES III to NHANES 1999e2006. Diabetes Care 2011 Jan;34(1):216e9. [14] O'Neill S, O'Driscoll L. Metabolic syndrome: a closer look at the growing epidemic and its associated pathologies. Obes Rev 2015;16:1e12. [15] Centers for Disease Control and Prevention (CDC). Trends in intake of energy and macronutrients-United States, 1971e2000. MMWR Morb Mortal Wkly Rep 2004;53:80e2. [16] Vadiveloo M, Scott M, Quatromoni P, Jacques P, Parekh N. Trends in dietary fat and high-fat food intakes from 1991 to 2008 in the Framingham Heart Study participants. Br J Nutr 2014;111:724e34. [17] Fryar CD, Wright JD, Eberhardt MS, Dye BA. Trends in nutrient intakes and chronic health conditions among Mexican-American adults, a 25-year profile: United States, 1982e2006. Natl Health Stat Rep 2012;50:1e20. [18] Feldeisen SE, Tucker KL. Nutritional strategies in the prevention and treatment of metabolic syndrome. Appl Physiol Nutr Metab 2007;32:46e60. [19] Committee of Dietary reference intake in Korean Nutrition Society. Dietary reference intake for Koreans. Seoul: Korean Nutrition Society; 2008.
Please cite this article in press as: Park S, et al., Very-low-fat diets may be associated with increased risk of metabolic syndrome in the adult population, Clinical Nutrition (2015), http://dx.doi.org/10.1016/j.clnu.2015.09.010
66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18
YCLNU2651_proof ■ 16 October 2015 ■ 9/9
S. Park et al. / Clinical Nutrition xxx (2015) 1e9 [20] Kweon S, Kim Y, Jang MJ, Kim Y, Kim K, Choi S, et al. Data resource profile: the Korea National Health and Nutrition Examination Survey (KNHANES). Int J Epidemiol 2014;43:69e77. [21] Kanazawa M, Yoshiike N, Osaka T, Numba Y, Zimmet P, Inoue S. Criteria and classification of obesity in Japan and Asia-Oceania. World Rev Nutr Diet 2005;94:1e12. [22] World Health Organization regional office for the Western Pacific region, International Association for the Study of Obesity; International Obesity Task Force. The Asian-Pacific perspective: redefining obesity and its treatment. Sydney: Health Communications Australia; 2000. [23] Research Team: Department of Agrofood Resources. Standard food composition table. 7th version. Rural development administration. Wanju-gun: National Academy of Agricultural Science, Korea; 2007. [24] Korea Center of Disease and Control and Prevention by Korea Ministry of Health and Welfare. Users' guide for Korean National Health and Nutrition Examination Survey. Daejeon: Statistics Korea; 2011. [25] Cohen E, Cragg M, deFonseka J, Hite A, Rosenberg M, Zhou B. Statistical review of US macronutrient consumption data, 1965e2011: Americans have been following dietary guidelines, coincident with the rise in obesity. Nutrition 2015;31:727e32. [26] Ford ES, Capewell S. Trends in total and low-density lipoprotein cholesterol among U.S. adults: contributions of changes in dietary fat intake and use of cholesterol-lowering medications. PLoS One 2013;8:e65228.
9
[27] Thompson FE, Subar AF. Dietary assessment methodology. In: Coulston AM, Boushey CJ, Ferruzzi MG, editors. Nutrition in the prevention and treatment of disease. 3rd ed. San Diego: Academic Press; 2013. [28] Schwingshack L, Hoffmann G. Comparison of effects of long-term low-fat vs high-fat diets on blood lipid levels in overweight or obese patients: a systematic review and meta-analysis. J Acad Nutr Diet 2013;113: 1640e61. [29] Schwingshack L, Hoffmann G. Comparison of the long-term effects of high-fat v. low-fat diet consumption on cardiometabolic risk factors in subjects with abnormal glucose metabolism: a systematic review and meta-analysis. Br J Nutr 2014;111:2047e58. [30] Schwingshack L, Hoffmann G. Long-term effects of low-fat diets either low or high in protein on cardiovascular and metabolic risk factors: a systematic review and meta-analysis. Nutr J 2013;12:48. [31] Vadiveloo M, Parkeh N, Mattei J. Greater healthful food variety as measured by the US healthy food diversity index is associated with lower odds of metabolic syndrome and its components in US adults. J Nutr 2015;145: 564e71. [32] Oh HY, Kim MK, Lee M, Kim YO. Macronutrient composition and sodium intake of diet are associated with risk of metabolic syndrome and hypertension in Korean women. PLoS One 2013;8:e78088.
Please cite this article in press as: Park S, et al., Very-low-fat diets may be associated with increased risk of metabolic syndrome in the adult population, Clinical Nutrition (2015), http://dx.doi.org/10.1016/j.clnu.2015.09.010
19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36
YCLNU2651_proof ■ 16 October 2015 ■ 1/9
Clinical Nutrition xxx (2015) 1e9
Contents lists available at ScienceDirect
Clinical Nutrition journal homepage: http://www.elsevier.com/locate/clnu
Original article
Q5
Very-low-fat diets may be associated with increased risk of metabolic syndrome in the adult population
Q4
Sunmin Park a, 1, Jaeouk Ahn b, 1, Byung-Kook Lee c, d, * a
Department of Food and Nutrition, Institute of Basic Sciences, Hoseo University, Asan, South Korea Department of Medical IT Engineering, Soonchunhyang University, Asan, South Korea c Department of Preventive Medicine, Soonchunhyang University, Asan, South Korea d Chungju Medical Center, Chungju, Chungbuk, South Korea b
a r t i c l e i n f o
s u m m a r y
Article history: Received 12 June 2015 Accepted 30 September 2015
Background & aims: Although fat intake has often been targeted to decrease the prevalence of metabolic syndrome; however decreasing dietary fat intake has not had this result. We studied the association between fat intake and the prevalence of metabolic syndrome in adults using KNHANES 2007e2013 data, a representative sample of the non-institutionalized civilian population. Methods: This cross-sectional study included 34,003 Korean adults aged 19 years. Adjusted odds ratios (OR) for the components of metabolic syndrome were measured according to fat intake (15, 15e25, 25% of daily energy intake) while controlling for covariates that affect metabolic syndrome using linear and logistic regression analysis while incorporating the sample weights for the complex sample design of the survey. Results: Surprisingly, the prevalence of metabolic syndrome was significantly higher in the 15% fat intake group (OR ¼ 1.277), accompanied by lower daily energy intake compared to the reference group (25% fat intake). Higher daily fat intake was associated with significantly lower ORs for four components of metabolic syndrome, except diabetes mellitus, using continuous variable analysis, whereas only three serum components (serum HDL, serum triglyceride, and blood pressure) exhibited significantly higher ORs in the lowest tertile of dietary fat intake (15%) compared with the reference group (25% fat-intake tertile). Subjects in a low-fat intake group had about 5.4 g polyunsaturated fatty acid/day that did not meet the recommended intake. Consumption of grain groups was a significant predictor of low fat intake, whereas milk food groups were significant predictors of not having low fat intake. Subjects in the low-fat group (15%) had much lower daily energy intake, by 500 kcal, compared with subjects who consumed high-fat diets (25%). All nutrients except carbohydrates had significantly lower mean values in the low-fat-intake group as compared to the high-fat-intake group. Conclusions: Low fat intake, <15%, was associated with a higher incidence of metabolic syndrome in the adult population, despite the daily energy intakes being lower by 500 kcal; this may be related to lower intake of various nutrients other than carbohydrates. © 2015 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved.
Keywords: Metabolic syndrome Fat intake Carbohydrate intake Energy intake HDL
1. Introduction Metabolic syndrome is defined by the presence of related cardiovascular disease risk factors including: insulin resistance,
* Corresponding author. Department of Preventive Medicine, Soonchunhyang University, 22 Soonchunhyang-Ro Shinchang-Myun, Asan 336-745, South Korea. Tel.: þ82 10 5437 0531. E-mail address: [email protected] (B.-K. Lee). 1 Sunmin Park and Jaeouk Ahn are equally contributed to this work.
abdominal obesity, dyslipidemia, hypertension, and a proinflammatory state [1]. Metabolic syndrome has been linked to the development of type 2 diabetes mellitus, atherosclerosis, some cancers, and a profoundly increased risk of morbidity and mortality [2]. Lifestyle interventions remain the primary mode of therapy for metabolic syndrome. Some risk factors, including high-fat diet, inactivity and estrogen deficiency, are well characterized [3]. Dietary patterns are important modifiable factors that may be useful for preventing the development of metabolic syndrome. However, the relationship between the metabolic syndrome and dietary patterns has not been fully elucidated, although a high-fat diet,
http://dx.doi.org/10.1016/j.clnu.2015.09.010 0261-5614/© 2015 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved.
Please cite this article in press as: Park S, et al., Very-low-fat diets may be associated with increased risk of metabolic syndrome in the adult population, Clinical Nutrition (2015), http://dx.doi.org/10.1016/j.clnu.2015.09.010
55 56 57 58 59 60 61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65
YCLNU2651_proof ■ 16 October 2015 ■ 2/9
2
S. Park et al. / Clinical Nutrition xxx (2015) 1e9
which leads to obesity and dyslipidemia, is a widely accepted risk factor for metabolic syndrome [4,5]. The traditional Asian diet is characterized as high in carbohydrates, with an abundance of vegetables, and has been considered beneficial for preventing metabolic syndrome in the Asian population [5,6]. However, the Westernization of lifestyle and dietary patterns may result in increased prevalence of metabolic syndrome in Asian countries. Fat consumption rose remarkably, from 7.2% to 19.0% of total energy consumption, between 1969 and 1998 in Korea [7,8]. Although during that time period the prevalence of metabolic syndrome had not been measured in the population, this increase is believed have contributed to the incidence of metabolic syndrome components. Fat intake has not markedly increased in KNHANES data since 1998, remaining at about 17e19% of total energy intake, although some parts of population have markedly increased their fat intake [7,8]. Interestingly, the incidence of metabolic syndrome increased markedly in Korea, by 6.5%, between 1998 and 2007, whereas from 2008 to 2012 it increased slowly, by 1.1% [7e9]. These results have suggested that an increase in fat intake to an average of ~20% may not promote metabolic syndrome. Previous studies have demonstrated that high carbohydrate intake (>60% of energy) increases the risk of metabolic syndrome in middle-aged Korean type 2 diabetic women [3], and high-carbohydrate diets (>57.4% of energy in men and >59.1% of energy in women) are associated with a low serum HDLecholesterol concentration in US men and high serum triglyceride in US women [10]. However, pregnant Korean women have higher fat intake (about 28% of energy intake) during pregnancy, and women with higher fat intake are more likely to develop gestational diabetes [11,12]. Thus, the role of dietary fat consumption in the development of metabolic syndrome in Koreans is not clear. Furthermore, US NHANES data indicate that the prevalence of metabolic syndrome components including obesity, high blood pressure, dyslipidemia, and diabetes increased from 1982 to 2006 in adults [13,14]. However, the intake of energy, saturated fat, polyunsaturated fat, and cholesterol did not change markedly between 1988 and 2008 in US adults aged 20e74 years; indeed, it was higher during 1971e1980 than during 1988e2008 [15]. On the other hand, the prevalences of obesity and insulin resistance increased substantially over 17 years in association with increases in the percent of total fat and protein in the diets of adults aged 25 years in the Framingham Heart Study Offspring Cohort (1991e2008) [16]. Furthermore, there are ethnic differences in macronutrient intake, and these may exert different influences on the development in metabolic syndrome [17]. Thus, the amount of fat and carbohydrate intake that is beneficial for reducing metabolic syndrome remains unclear. However, in nutritional education, high fat intake is considered the major cause of metabolic diseases because it is associated with a higher incidence of metabolic syndrome in Western countries [18]. Some people in Korea try to consume food that is lower in fat, but they may not have consumed as much fat as they need. The Korean dietary reference intake (KDRI) recommends fat consumption of around 25% of energy intake [19]. Some people consume too little fat, far below the KDRI recommendation, which results in diets high in carbohydrates and low in proteins [7,8]. Asians, including Koreans, have historically consumed highcarbohydrate, low-fat diets. Researchers have considered that this dietary pattern may not be beneficial in reducing the risk of metabolic syndrome. Therefore, we hypothesized that different fat intakes modified the components of metabolic syndrome in Korean adults. We studied the association between fat intake and the prevalence of metabolic syndrome in adults 19 years of age using the KNHANES 2007e2013 data, a representative sample of the noninstitutionalized civilian population.
2. Methods 2.1. Design and data collection This study utilized data obtained from the Korea National Health and Nutrition Examination Survey (KNHANES) 2007e2013, which includes KNHANES IV (2007e2009), KNHANES V (2010e2012) and KNHANES VI (2013) surveys. KNHANES surveys are conducted annually using a rolling sampling design that involves a complex, stratified, multistage probability-cluster survey of a representative sample of the non-institutionalized civilian population in South Korea. The KNHANES is a large representative population study with rigorous quality controls. The survey is performed by the Korean Centers for Disease Control and Prevention and the Korean Ministry of Health and Welfare. It has three components: a health interview, a health examination, and a nutrition survey. The survey was approved by the Institutional Review Board of the Korean Centers for Disease Control and Prevention (approval nos. 200804EXP-01-C, 2009-01CON-03-2C, 2010-02CON-21-C and 201307CON-03-4C). The present cross-sectional analysis was restricted to adults 19 years of age who completed the health examination survey and the nutrition survey (n ¼ 34,003). Detailed descriptions of the design of the survey have been reported previously [20]. Briefly, the participants ages, education, smoking histories and alcohol intakes were obtained during the health interview. Height and weight measurements were performed, with the participants wearing light clothing and no shoes. Body mass index (BMI) was calculated as weight in kilograms divided by the square of the height in meters (kg/m2). Obesity was categorized into three groups according to the Asian obesity definition by recommended by International Obesity Task Force and the World Health Organization (WHO) Regional Office for the Western Pacific Region [21,22]: lean (BMI < 18.5), normal (18.5 BMI < 25), and obese (BMI 25). Age reported at the time of the health interview was categorized into five groups. Area of residence was categorized into urban (administrative divisions of a city) and rural areas (not classified as administrative divisions of a city). Income level was categorized into four quartile groups (1st Qe4th Q). Education level was categorized into three groups: below high school, high school, and college or higher. Occupation was categorized into four groups: clerical, manual, technical, and unemployed. Smoking status was divided into three categories: current smoker, past smoker and never-smoker. Smoking status was defined based on self-reported cigarette use: never-smokers had smoked less than 100 cigarettes in their lifetime; participants who had smoked 100 or more cigarettes were considered past or current smokers, based on current tobacco use. Alcohol consumption was assessed by asking the participants about their drinking behavior during the month prior to the interview, including their average frequency (days per month) of alcoholic beverage consumption and amount (in mL) of alcoholic beverages ingested on a single occasion. The responses were converted into the amount of pure alcohol (in grams) consumed per day. Alcohol consumption status was categorized into four groups according to average daily alcohol consumption: nondrinkers, and light (1e15 g), moderate (16e30 g), and heavy (>30 g) drinkers. Regular exercise was defined as regular exercising 30 min at a time at least five times per week, as moderate exercise activities (swimming slowly, playing doubles tennis or volleyball, and participating in occupational or recreational activities while carrying light objects), or for 20 min at a time at least three times per week in vigorous exercise activities (running, climbing, cycling fast, swimming fast, playing football, basketball, squash or
Please cite this article in press as: Park S, et al., Very-low-fat diets may be associated with increased risk of metabolic syndrome in the adult population, Clinical Nutrition (2015), http://dx.doi.org/10.1016/j.clnu.2015.09.010
66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65
YCLNU2651_proof ■ 16 October 2015 ■ 3/9
S. Park et al. / Clinical Nutrition xxx (2015) 1e9
3
singles tennis, jumping rope and participating in occupational or recreational activities while carrying heavy objects).
food frequency questionnaire (FFQ) in 2012, only 5 years' data (2007e2011) were used for dietary assessment and food grouping.
2.2. Definition of metabolic syndrome
2.6. Statistical analysis
Based on the 2005 revised National Cholesterol Education Program-Adult Treatment Panel III criteria and the Korean Society for the Study of Obesity criteria for waist circumference, metabolic syndrome was defined as the presence of three or more of the following: 1) elevated blood pressure (average systolic blood pressure 130 mmHg or diastolic blood pressure 85 mmHg) or current blood pressure medication use; 2) low HDL-cholesterol level (<40 mg/dl); 3) elevated serum TG level (150 mg/dl) or current anti-dyslipidemic medication use; 4) elevated fasting blood glucose level (100 mg/dl) or current anti-diabetic medication use; and 5) abdominal obesity (waist circumference 90 cm) [12,16,17].
Statistical analyses were performed using SAS software (version 9.4; SAS Institute, Cary, NC, USA) and SUDAAN (Release 11.0; Research Triangle Institute, Research Triangle Park, NC, USA), a software package that incorporates sample weights and adjusts analyses for the complex sample design of the survey. Survey sample weights were used in all analyses to produce estimates that were representative of the non-institutionalized civilian Korean population. Descriptive statistics of participants according to daily fat intake (%) were obtained by determining frequency distributions of categorical demographic variables; lifestyle factors and the presence of metabolic syndrome components, and statistical significances were determined using chi-squared tests. Adjusted odds ratios (ORs) and 95% confidence intervals (CI) for metabolic syndrome and its components according to daily fat intake (15.0, 15.0e25.0, <25.0%) were calculated using logistic regression analysis after covariate adjustment. Covariates were sex, age, residence area, occupation, income, education level, drinking status, obesity, and physical activity. Next, to evaluate the associations of selected study variables and 11 food intake groups obtained from the food frequency questionnaire with daily fat intake status, adjusted ORs for low fat intake (15.0%) were calculated using ordinal logistic regression analysis after covariate adjustment. Finally, adjusted means and 95% CIs of daily nutrient intakes according to daily fat intake (%) were calculated using analysis of covariance (ANCOVA). The covariates used for adjusted means were sex, age, residence area, income, occupation, drinking status, education, stress level, obesity, and physical activity.
2.3. Laboratory testing Blood samples were obtained in the morning following an overnight fast. The serum concentrations of glucose, high-density lipoprotein cholesterol (HDL), triglycerides (TG), aspartate transaminase (AST), and alanine transaminase (ALT) were measured using a Hitachi automatic analyzer 7600 (Tokyo, Japan). Lowdensity lipoprotein cholesterol (LDL) was calculated using the Friedewald equation [LDL ¼ total cholesterol e HDL e (TG/5.0)] if the TG concentration was not above 400 mg/dl. When the TG concentration was above 400 mg/dl, TG was measured directly using a Hitachi automatic analyzer 7600. All clinical analyses were performed by the Neodin Medical Institute, a laboratory certified by the Korean Ministry of Health and Welfare. 2.4. Assessment of nutrient intake All subjects were instructed to maintain their usual dietary habits prior to the assessment of dietary intake. Daily nutrient intake was measured using the 24-h recall method. The 24h dietary recalls were conducted through in-person interviews by trained dietary staff in mobile examination centers to explore food kinds and amounts that the subjects consumed for the past 24 h (midnight to midnight). Daily intake of calories and nutrients was calculated from the information of food intake acquired from interviewing using the Can-Pro 2.0 nutrient intake assessment software developed by the Korean Nutrition Society. Daily consumption of saturated, monounsaturated and polyunsaturated fatty acids were additionally estimated from the 24-h recall data by adding the data from fatty acid composition of foods tables into the nutrient data [23]. 2.5. Dietary assessment method and food grouping Dietary intake information was collected by administering a validated semi-quantitative food-frequency questionnaire to each participant. Food-frequency questionnaires used in KNHANES were developed and validated by the Ministry of Health and Welfare [24]. This questionnaire requested information regarding the participant's consumption of 63 food items. The participant's food intake frequency was quantified using nine categories: never or seldom, once a month, two to three times a month, one to two times a week, three to four times a week, five to six times a week, once a day, twice a day, and three times or more every day. Sixtythree food items were further categorized into 11 subgroups: grain 1 (rice, breads and noodles), grain 2 (cereals, rice cakes and potatoes), legumes, meat, fish, vegetables, fruit, milk, sugar, and other. Since KNHANES changed the data collection format for the
3. Results Subject characteristics by classification variables according to daily fat intake percentage are shown in Table 1. All of the classification variables were significantly different among groups, with significance levels of p < 0.01 for all variables except exercise and walking, for which the significance level was p < 0.05. As age increased, the proportion of participants reporting low fat intake (15.0%) increased significantly. The prevalence of metabolic syndrome was stable from 2007 to 2013, nor did any of the components of metabolic syndrome change, except the prevalence of diabetes, which was increased (Fig. 1). During the 2007e2013 time period, the percentage of people who consumed more than 25% of their calories in the form of fat gradually increased, and the prevalence of metabolic syndrome significantly declined according to daily fat intake (%) in the 40e49-, 50e59-, and 60-year age groups (Fig. 2). As age increased, fat intake decreased (Fig. 2). Adjusted ORs and 95% CI values were calculated for metabolic syndrome and its components according to daily fat intake percentages (units ¼ 5) as a continuous independent variable and according to the three categorized daily fat intake groups (15.0, 15.0e25.0, and 25.0%) after adjusting for covariates (Table 2) which were: sex, age, residence area, income, occupation, smoking and drinking status, education level, obesity, and physical activity. The adjusted ORs and 95% CI for metabolic syndrome after adjustment of covariates were 1.0696 (1.0434e1.0964) based on daily fat intake percentage (5% changes) as a continuous independent variable, and 1.2277 (1.0862e1.3877) for categorized daily fat intake analysis, indicating that 22.8% more people had metabolic syndrome in the low-fat (15.0%) compared with the high-fat-
Please cite this article in press as: Park S, et al., Very-low-fat diets may be associated with increased risk of metabolic syndrome in the adult population, Clinical Nutrition (2015), http://dx.doi.org/10.1016/j.clnu.2015.09.010
66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65
YCLNU2651_proof ■ 16 October 2015 ■ 4/9
4
S. Park et al. / Clinical Nutrition xxx (2015) 1e9
Table 1 General characteristics grouped by daily fat intake in the Korean adult population according to KNHANES 2007e2013. Fat intake (energy %)a
Classification
15.0 N (%) All Gender Age group
Residence area Income
Occupation
Smoking status
Drinking status
Education level
Obesity
Exercise Walk Year
Metabolic syndrome a b
Male Female 19e29 30e39 40e49 50e59 60e Urban Rural 1st Q 2nd Q 3rd Q 4th Q Clerical Manual Technical Unemployed Non smoker Past smoker Current smoker Non drinker Mild drinker Moderate drinker Heavy drinker Less than High School High School College Lean Normal Obese Yes No Yes No 2007 2008 2009 2010 2011 2012 2013 Yes No
16,502 6405 10,097 736 1877 2582 3521 7786 11,439 5063 4433 4226 3949 3606 4603 3746 1210 6943 10,221 3304 2977 6228 7026 1675 1573 11,258 2524 2720 595 10,370 5503 3437 13,065 6753 9749 1375 3004 3195 2413 2395 2211 1909 4641 11,861
(42.62) (39.67) (45.25) (19.12) (27.86) (39.65) (54.35) (70.75) (39.59) (54.57) (47.28) (43.3) (40.78) (38.55) (33.65) (60.68) (39.94) (47.3) (44.45) (43.95) (37.56) (53.51) (37.66) (40.43) (41.56) (56.31) (35.68) (26.58) (32.82) (42.41) (44.68) (41.73) (42.87) (42.54) (42.68) (45.89) (46.33) (46.15) (43.12) (40.75) (39.44) (38.69) (55.11) (39.49)
p valueb 15.0e25.0 N (%)
25.0 N (%)
12,120 5176 6944 1559 3018 2797 2208 2538 9868 2252 2625 2900 3103 3316 5260 1474 1153 4233 7120 2343 2657 3203 6321 1331 1265 5227 2668 4225 581 7768 3698 2590 9530 4764 7356 857 1906 2164 1869 1907 1751 1666 2268 9852
5381 2204 3177 1350 1610 1101 643 677 4577 804 1068 1330 1392 1515 2672 418 409 1882 3174 966 1241 1157 3051 579 594 1765 1215 2401 300 3475 1573 1196 4185 2200 3181 286 697 873 815 892 873 945 763 4618
(38.36) (40.53) (36.42) (43.14) (46.79) (43.29) (35.19) (22.93) (40.02) (31.82) (35.63) (37.38) (39.3) (41.55) (43.17) (28.9) (43.7) (34.61) (37) (38.3) (41.42) (32.87) (40.69) (40.59) (38.53) (31.77) (42.47) (45.58) (42.97) (38.5) (37.25) (37.73) (38.53) (37.55) (38.9) (39.51) (38.24) (36.64) (38.09) (39.06) (38.82) (38.69) (32.36) (39.87)
(19.02) (19.8) (18.32) (37.73) (25.35) (17.06) (10.46) (6.32) (20.39) (13.61) (17.09) (19.33) (19.92) (19.9) (23.18) (10.43) (16.36) (18.09) (18.56) (17.75) (21.03) (13.62) (21.65) (18.98) (19.91) (11.92) (21.85) (27.84) (24.2) (19.08) (18.07) (20.54) (18.6) (19.91) (18.42) (14.59) (15.43) (17.22) (18.79) (20.19) (21.74) (22.62) (12.53) (20.65)
0.01 0.01 0.01
0.01 0.01
0.01
0.01
0.01
0.01
0.01
0.05 0.05 0.01
0.01
Fat intake was calculated by the percentage of total energy intake. P value for Satterwaite Chisquare.
intake group (25.0%) (Table 2). In the analysis of components of metabolic syndrome as dependent variables, in the continuous variable analysis, the ORs for four components of metabolic syndrome were significantly influenced by daily fat intake, the exception being diabetes mellitus; when categorized daily fat intake was used, only three components (HDL, Triglyceride and blood pressure) had significant ORs. Next, ORs for low fat intake were calculated after adjusting for covariates according to classification variables using ordinal logistic regression analysis with three levels of the response variable (daily fat intake: 15.0, 15.0e25.0 and <25.0%) (Table 3). Among classification variables, age was significant predictor of low fat intake; as age increased, the prevalence of low fat intake also increased. On the other hand, the higher income and higher education level groups, past and current smokers, and those living in an urban area were significantly less likely to have a low fat intake than the reference groups. It is interesting that manual labor workers consumed less fat than clerical workers did when compared with unemployed subjects. The remaining classification
variables, including obesity, exercise and walk, and drinking status were not significantly associated with fat intake in the categorical analysis (see Table 4). Q1 To investigate the association of metabolic syndrome with daily fat intake calculated from 24-h recall and food groups obtained using the semi-quantitative food frequency questionnaire, adjusted ORs and 95% CI for low fat intake were calculated using ordinal logistic regression analysis according to 11 food groups after covariates adjustment. Grain groups 1 and 2 were significant predictors of low fat intake, whereas milk and sugar groups were significant predictors for not having low fat intake. Others food groups, such as legumes, meat, fish, vegetables, and fruits, were marginally significant predictors of high fat intake compared with reference groups, although the vegetable group showed inconsistent results. Finally, to clarify the association of nutrient intake according to daily fat intake percentage, the adjusted means and 95% CIs according to daily fat intake percentages were calculated by ANCOVA (Table 5) after covariate adjustment. As expected, the daily intake of macronutrients such as carbohydrates, protein and fats
Please cite this article in press as: Park S, et al., Very-low-fat diets may be associated with increased risk of metabolic syndrome in the adult population, Clinical Nutrition (2015), http://dx.doi.org/10.1016/j.clnu.2015.09.010
66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65
YCLNU2651_proof ■ 16 October 2015 ■ 5/9
S. Park et al. / Clinical Nutrition xxx (2015) 1e9
5
Fig. 1. Changes in the prevalence of metabolic syndrome and each component and in the percentage of people reporting 25% fat intake during 2007e2013. METS, the percentage of metabolic syndrome; WC, the percentage of 90 cm waist circumference; HDL, the percentage of <40 mg/dl serum HDL cholesterol; TG, <150 mg/dl serum triglyceride, BP, the percentage of systolic blood pressure 130 mmHg or diastolic blood pressure 85 mmHg; DM, the percentage of 100 mg/dl fasting blood glucose; Fat >25%, the percentage of >25% fat intake from total energy intake.
differed significantly among three fat-intake groups. Daily energy intake was higher as fat intake increased. Except for carbohydrates, mean values for nutrients were significantly lower in the low e as compared with the high-fat-intake group. The amount of each category of fatty acids (saturated, monounsaturated, and polyunsaturated) consumed from total fats was also significantly higher among all three groups: as total fat intake increased. The ratios of saturated, monounsaturated and polyunsaturated fatty acids were within the recommended range in the low-fat-intake group but the medium-fat and high-fat intake groups had lower ratios of PUFA intake than the low-fat-intake group and were lower than the ratio recommended for PUFA. Thus, a low fat intake (less than 15% fat) was associated with the higher incidence of metabolic syndrome regardless of the ratio of saturated, monounsaturated and polyunsaturated fatty acid. 4. Discussion Fat intake has often been targeted for reducing the prevalence of metabolic diseases, but this strategy has not decreased metabolic syndrome in the USA. Although the consumption of fat among Koreans has gradually increased, it is still much less than that of Americans in NHANES [25]. Data from this study of the Korean adult population can be used to examine the association of low dietary fat intake with the incidence of metabolic syndrome. Our data suggested that the prevalence of metabolic syndrome was significantly higher in the low-fat-intake group (15% of intake) compared with the high-fat-intake group (25%). Higher dietary fat intake was significantly associated with lower risk for four components of metabolic syndrome, the exception being high fasting blood glucose. The ratios of saturated, monounsaturated
and polyunsaturated fatty acids from total fat intake were within the recommended ranges regardless of different fat intake groups [19]. Interestingly, subjects in the low-fat group (15%) had much lower daily intake of energy (by 500 kcal) and of almost all nutrients except carbohydrates compared with the high-fat group (25%). These results suggest that metabolic syndrome may be related to sub-optimal intakes of nutrients other than carbohydrates in the Korean population. Metabolic syndrome is associated with major cardiovascular risk factors including insulin resistance, dyslipidemia, hypertension, nonalcoholic fatty liver disease, hyperuricemia, a prothrombotic state, and chronic inflammation [1]. Obesity is a welldocumented risk factor for metabolic syndrome. The prevention of metabolic syndrome can reduce the chance of developing cardiovascular diseases [1,2]. In NHANES I, II, III data, participants of both genders exhibited increased intake of calories in the form of fat, to about 33%, and of saturated fat, reaching approximately 11%, from 1971e1974 to 1999e2000 [15]. The intake of energy and in terms of calories and carbohydrates has increased. However, the overall trend in the US was an increased prevalence of obesity, but an unchanged prevalence of metabolic syndrome during this time period [13,14]. Thus, total energy intake is a key regulator of obesity, and the percentage of energy intake from of fat may affect the risk of metabolic syndrome independently from obesity. This present study demonstrated that subjects who consumed low-fat diets had increased likelihood of metabolic syndrome, although their total energy intake was lower than that of other subjects who consumed more. Additionally, the prevalence of metabolic syndrome was stable from 2007 to 2013, although the percentage of people who consumed more than 25% of calories from fat increased from 15 to 20%. Thus, the increase in fat intake among the Korea population
Please cite this article in press as: Park S, et al., Very-low-fat diets may be associated with increased risk of metabolic syndrome in the adult population, Clinical Nutrition (2015), http://dx.doi.org/10.1016/j.clnu.2015.09.010
66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65
YCLNU2651_proof ■ 16 October 2015 ■ 6/9
6
S. Park et al. / Clinical Nutrition xxx (2015) 1e9
Fig. 2. Prevalence of metabolic syndrome and each component in age category tertiles (40e49, 50e59, and 60 years old). METS, the percentage of metabolic syndrome; WC, the percentage of 90 cm waist circumference; HDL, the percentage of <40 mg/dl serum HDL cholesterol; TG, <150 mg/dl serum triglyceride, BP, the percentage of systolic blood pressure 130 mmHg or diastolic blood pressure 85 mmHg; DM, the percentage of 100 mg/dl fasting blood glucose.
may not lead to an increased risk of metabolic syndrome, but people who consume very little fat may be susceptible to metabolic syndrome. The optimal composition of marcronutrients in the diet is still controversial [11,16e18,26]. In terms of calories, fat intake is usually comparable to protein intake and opposite to carbohydrate intake [15,16]. High fat intake is believed to exacerbate obesity, metabolic syndrome, and certain cancers, even given constant caloric intake [11,27]. However, recent studies have shown that high-carbohydrate diets also increases the risk of metabolic syndrome. A recent meta-analysis in overweight and obese patients [28] demonstrated that low-fat diets (about 9.3% and 25e30% of total energy consumption from saturated fat and total fat, respectively) resulted in lower total cholesterol and LDL cholesterol in long-term randomized clinical trials compared with high-fat diets. However, low-fat diets may lead to increased circulating triglycerides and decreased HDL cholesterol [10,29]. In the present study, the Korean adults generally consumed low-fat diets, although fat intake has increased. When adults were divided into three categories by fat intake, adults in the lowest fat group were at greater risk of metabolic syndrome, except for blood glucose levels. These difference in results compared with previous studies may reflect a difference in the definition of fat percentage in the diet. In the present study, low- and high-fat diets were defined as <15% and >25% of energy intake, respectively, and the average intake of fat in the low-fat and high-fat groups constituted 15% and 33.5% of calories consumed. Thus, most of the adults in the high-fat-diet group in the present study consumed what the Schwingshack and Hoffmann study would have considered to be a low-fat-diet [28]. Thus, >15% dietary fat may be optimal to prevent metabolic syndrome.
Another meta-analysis study [29] showed the long-term (12 months) effects of low- and high-fat diets on serum lipid and glucose profiles in people with pre-diabetes and type 2 diabetes in randomized clinical trials. A high-fat diet was found to result in significant decreases in serum triglyceride and glucose levels in a fasting state and in diastolic blood pressure, as well as a significant increase in HDL-cholesterol levels. Thus, that study suggested that a high-fat diet may not be detrimental for managing blood glucose levels in pre-diabetic and type 2 diabetic patients. However, the present study demonstrated that the prevalence of diabetes, defined as an elevated fasting blood glucose level (100 mg/dl) or current anti-diabetic medication use, was not altered by dietary fat consumption. Additionally, unlike other components of metabolic syndrome, the prevalence of hyperglycemia continuously increased as the dietary fat consumption increased 2007 to 2013 in the present study. These results suggest that among Korean adults, fat intake of >25% of total calories may be detrimental to blood glucose regulation and increase the risk of type 2 diabetes. Furthermore, Korean pregnant women, the prevalence of gestational diabetes mellitus is associated with higher maternal weight gain at 24e28 weeks of gestation and is positively related to higher energy and fat intake, especially from saturated fat [11,12]. Therefore, more studies are needed to determine the optimal fat intake for preventing metabolic syndrome in the Korean population. A high-protein diet does not have a beneficial or detrimental effect in terms of weight management. Recent meta-analyses [30] have shown that neither low (about 15% of calories) nor high (25e30% of calories) protein in low-fat diets (20e30% of calories) has any effect on outcome markers for obesity, cardiovascular disease, or glycemic control in long-term randomized clinical trials. Thus, dietary protein content may not play a major role in
Please cite this article in press as: Park S, et al., Very-low-fat diets may be associated with increased risk of metabolic syndrome in the adult population, Clinical Nutrition (2015), http://dx.doi.org/10.1016/j.clnu.2015.09.010
66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65
YCLNU2651_proof ■ 16 October 2015 ■ 7/9
S. Park et al. / Clinical Nutrition xxx (2015) 1e9
Q3
Table 2 Adjusted odds ratios for metabolic syndrome and its components according to fat intake. Outcome
Classification of fat intake
Metabolic syndrome
Fat intake energy Fat intake 15.0% 15.0e25.0% 25.0% Fat intake energy Fat intake 15.0% 15.0e25.0% 25.0% Fat intake energy Fat intake 15.0% 15.0e25.0% 25.0% Fat intake energy Fat intake 15.0% 15.0e25.0% 25.0% Fat intake energy Fat intake 15.0% 15.0e25.0% 25.0% Fat intake energy Fat intake 15.0% 15.0e25.0% 25.0%
Waist circumference
Serum HDL
Serum triglyceride
Blood pressure
Diabetes mellitus
Odds ratio (95% CI)c
% (unit ¼ 5)a
1.0696 (1.0434e1.0964)
% (unit ¼ 5)
1.2277 (1.0862e1.3877) 1.0638 (0.931e1.2155) Ref (1.0)b 1.044 (1.0117e1.0773)
% (unit ¼ 5)
1.1424 (0.9848e1.3251) 1.0784 (0.9314e1.2486) Ref (1.0) 1.0574 (1.0359e1.0794)
% (unit ¼ 5)
1.1703 (1.0573e1.2954) 1.0297 (0.9321e1.1375) Ref (1.0) 1.0586 (1.0387e1.0788)
% (unit ¼ 5)
1.2336 (1.1292e1.3477) 1.0499 (0.9651e1.1421) Ref (1.0) 1.0441 (1.0207e1.0681)
% (unit ¼ 5)
1.2119 (1.0733e1.3685) 1.167 (1.0298e1.3223) Ref (1.0) 1.0139 (0.993e1.0353)
Table 3 Adjusted odds ratios for having low fat intake according to classification variables.
Gender Age group (yrs)
Income
Occupation
Education level
Smoking status
Drinking status
Obesity
Exercise
a
The adjusted odds ratio in continuous decrease of fat intake (energy %). b Reference group. c Adjusted for gender, age, residence area, income, occupation, smoking and drinking status, education, obesity, and physical activities.
Odds ratios (95% CI)b
Classification
Residence area
1.0295 (0.9298e1.1399) 0.9619 (0.8685e1.0653) Ref (1.0)
7
Walk
Male Female 19e29 30e39 40e49 50e59 60e Urban Rural 1st Q 2nd Q 3rd Q 4th Q Clerical Manual Technical Unemployed Less than High School High School College Non smoker Past smoker Current smoker Non drinker Mild drinker Moderate drinker Heavy drinker Lean Normal Obese Yes No Yes No
0.946 (0.863e1.037) Ref (1.0)a Ref (1.0) 1.739 (1.556e1.944) 2.596 (2.297e2.933) 3.953 (3.47e4.504) 6.839 (5.972e7.834) 0.802 (0.723e0.889) Ref (1.0) Ref (1.0) 0.892 (0.809e0.983) 0.876 (0.795e0.965) 0.818 (0.739e0.905) 0.806 (0.745e0.871) 1.279 (1.133e1.442) 0.938 (0.832e1.059) Ref (1.0) Ref (1.0) 0.821 (0.752e0.897) 0.667 (0.602e0.74) Ref (1.0) 0.863 (0.778e0.957) 0.861 (0.779e0.951) Ref (1.0) 0.857 (0.791e0.927) 0.933 (0.833e1.045) 1.041 (0.92e1.177) Ref (1.0) 0.997 (0.866e1.146) 0.967 (0.835e1.119) 0.964 (0.898e1.036) Ref (1.0) 1.033 (0.969e1.1) Ref (1.0)
a
Reference group. Adjusted for gender, age, residence area, income, occupation, smoking and drinking status, education, obesity, and physical activities. b
developing metabolic syndrome. Although protein intake of 0.826 g/kg body weight/day is recommended for adults [19], the actual protein intake in this study was greater than this recommendation because Koreans acquire protein from grains. The adults in a low-fat-diet group consumed protein much less than the other groups did, although the average consumption reached the recommended level. These results suggest that the protein intake in the low-fat group may not be sufficient and may also increase the risk for metabolic syndrome. The recommended intake of protein may not be sufficient for Korean adults when dietary patterns are considered. The low-fat diet may represent improper food intake and less variety of foods. The food frequency data showed that a higher intake of grain groups increased the risk of metabolic syndrome, but higher milk consumption was associated with a lower risk in the present study. Moreover, the proper intake of meat, fish, and fruit was related to a lower risk of metabolic syndrome. However, compared with deficient intake, proper intake of vegetables increased the risk of metabolic syndrome somewhat. These results indicate that a diet of mainly grain and vegetables, considered a Korean-style diet, may be associated with elevated risk of metabolic syndrome. A recent study [31] supported these observations: consuming a wide variety of healthful foods, as measured by the healthy food variety index, was associated with lower ORs for metabolic syndrome and hypertension, waist circumference, and fasting serum glucose levels in the US population based on NHANES 2003e2006 data. Furthermore, based on the KNHAES data, a balanced Korean diet is associated a lower OR for metabolic syndrome in women only and lower blood pressure in both genders when dietary patterns are categorized as a balanced Korean
Table 4 Adjusted odds ratio for having low fat intake according to food groups. Odds ratio (95% CI)b
Classification Grain group 1
Grain group 2
Legume group
Meat group
Fish group
Meat and fish group
Vegetable group
Fruits group
Milk group
Deficient Proper Excessive Deficient Proper Excessive Deficient Proper Excessive Deficient Proper Excessive Deficient Proper Excessive Deficient Proper Excessive Deficient Proper Excessive Deficient Proper Excessive Deficient Proper Excessive
Ref (1.0)a 1.138 (1.03e1.257) 1.189 (1.086e1.302) Ref (1.0) 1.054 (0.825e1.347) 1.762 (1.023e3.033) Ref (1.0) 0.874 (0.802e0.951) 0.977 (0.905e1.055) 1 (1e1) 0.859 (0.79e0.934) 1.106 (0.93e1.315) Ref (1.0) 0.698 (0.638e0.763) 0.86 (0.674e1.099) Ref (1.0) 0.857 (0.753e0.976) 0.919 (0.428e1.977) Ref (1.0) 1.13 (1.057e1.209) 0.973 (0.822e1.153) Ref (1.0) 0.87 (0.816e0.927) 0.962 (0.747e1.239) Ref (1.0) 0.678 (0.634e0.725) 0.431 (0.312e0.596)
a
Reference group. Adjusted for gender, age, residence area, income, occupation, smoking and drinking status, education, obesity, and physical activities. b
Please cite this article in press as: Park S, et al., Very-low-fat diets may be associated with increased risk of metabolic syndrome in the adult population, Clinical Nutrition (2015), http://dx.doi.org/10.1016/j.clnu.2015.09.010
66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 Q2 64 65
YCLNU2651_proof ■ 16 October 2015 ■ 8/9
8
S. Park et al. / Clinical Nutrition xxx (2015) 1e9
Table 5 Daily nutrient intake grouped by daily fat intake in KNHANES 2007e2013. Nutrients
Total energy (kcal) Protein (g) Carbohydrate (g) Dietary fiber (g) Total fats (g) Saturated fatty acid (SFA, g) Monounsaturated fatty acid (MUFA, g) Polyunsaturated fatty acid (PUFA, g) Ratio of SFA:MUFA:PUFA
Daily fat intake (energy%)
p value
15.0
15.0e25.0
25.0
1837 (1820e1854)a 59.8 (59.1e60.4) 328.0 (324.9e331.1) 7.182 (7.059e7.306) 21.5 (21.2e21.8) 5.92 (5.63e6.21) 6.11 (5.79e6.43) 5.98 (5.67e6.29) 1:1.03:1.01
2032 (2013e2051) 75.3 (74.5e76.2) 316.5 (313.7e319.3) 7.850 (7.700e8.000) 44.0 (43.6e44.4) 13.1 (12.7e13.5) 14.4 (14.0e14.8) 11.8 (11.4e12.2) 1:1.11:0.90
2338 (2304e2372) 93.4 (91.7e95.0) 294.3 (290.0e298.6) 7.809 (7.632e7.985) 82.0 (80.5e83.5) 25.3 (23.9e26.7) 29.4 (27.9e30.9) 20.0 (18.9e21.1) 1:1.16:0.79
<0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001
Adjusted for gender, age, residence area, income, occupation, smoking and drinking status, education, obesity, and physical activities. a Means (95% CI).
diet, unbalanced Korean diet, and semi-Western diet, using principal component analysis [32]. The women in the group who consumed a balanced Korean diet had higher intake of fat, protein, and other micronutrients such as vitamin C, vitamin A, and calcium but lower intake of carbohydrates. Thus, diets with low energy and low-fat contents may not be beneficial for decreasing the risk of metabolic syndrome. To the best of our knowledge, this study is the first to determine the positive association of low fat intake and metabolic syndrome in a large representative sample of the Korean population. However, this study has some limitations. First, this was a cross-sectional study, so the results do not represent causeeeffect relationships. Because people who had metabolic syndrome had lower energy intake and a low-fat diet compared with those who did not have this syndrome, our analysis is based on a negative association that requires clarification. Second, the fatty acid composition of fat consumed, i.e., saturated, monounsaturated, and polyunsaturated fatty acids, was not examined because it was not provided in the KNHANES data; however, the fatty acid composition may be more important for the prevalence of metabolic syndrome than just total fat itself [4]. Third, food intake could be under-reported knowingly or accidentally, despite the survey's being conducted by trained dieticians. Fourth, the usual nutrient intake including fat was determined by food intake based on 24-h recall data in KNHANES. This procedure may introduce some bias in the investigation of typical nutrient intake despite the skill of dieticians administering the measure, as some subjects may not accurately report their food intakes due to mistaken memories or other personal reasons. Additionally, food intake is quite different on weekdays than it is on weekends. Although the 3-day food record is the gold standard for determining typical intake levels [27], considering the expense and accuracy of self-recording food consumption, the 24-h recall can be an appropriate method for estimating actual and typical intakes. In conclusion, a diet of less than 15% fat intake increased the prevalence of metabolic syndrome despite the lower daily energy intake, by 500 kcal, in the adult population, and metabolic syndrome may be related to sub-optimal intakes of nutrients other than carbohydrates. The fatty acid composition of subjects with low fat dietary intakes in the adult population may not satisfy international PUFA recommendation for a lower risk of metabolic syndrome. Further studies are needed to identify how much fat intake, especially PUFA, is beneficial to prevent metabolic syndrome in adults. Conflict of interest None.
Acknowledgment S. P. and B.K.L. designed research and wrote the paper. B.K.L and J.A. conducted the statistical analysis. B.K.L. had primary responsibility for final content. All authors read and approved the final manuscript. References [1] Tchernof A. Visceral adipocyte and the metabolic syndrome. Nutr Rev 2007;65:S24e9. [2] Potenza MV, Mechanick JI. The metabolic syndrome: definition, global impact, and pathophysiology. Nutr Clin Pract 2009;24:560e77. [3] Kim WY, Kim JE, Choi YJ, Huh KB. Nutritional risk and metabolic syndrome in Korean type 2 diabetes mellitus. Asia Pac J Clin Nutr 2008;17:47e51. [4] Lottenberg AM, Afonso Mda S, Lavrador MS, Machado RM, Nakandakare ER. The role of dietary fatty acids in the pathology of metabolic syndrome. J Nutr Biochem 2012;23:1027e40. [5] Misra A, Singhal N, Khurana L. Obesity, the metabolic syndrome, and type 2 diabetes in developing countries: role of dietary fats and oils. J Am Coll Nutr 2010;29:289Se301S. [6] Park HS, Oh SW, Cho SI, Choi WH, Kim YS. The metabolic syndrome and associated lifestyle factors among South Korean adults. Int J Epidemiol 2004;33:328e36. [7] Korean Ministry of Health and Welfare. The Korean National Health Nutrition Examination Survey 1998. Seoul: Korean Ministry of Health and Welfare; 1999. [8] Korean National Statistical Office. 2000 report of statistics in mortality in Korean. Daejeon: Korean National Statistical Office; 2001. [9] Lim S, Shin H, Song JH, Kwak SH, Kang SM, Won Yoon J, et al. Increasing prevalence of metabolic syndrome in Korea: the Korean National Health and Nutrition Examination Survey for 1998e2007. Diabetes Care 2011;34: 1323e8. [10] Yang EJ, Chung HK, Kim WY, Kerver JM, Song WO. Carbohydrate intake is associated with diet quality and risk factors for cardiovascular disease in U.S. adults: NHANES III. J Am Coll Nutr 2003;22:71e9. [11] Park S, Kim MY, Baik SH, Woo JT, Kwon YJ, Daily JW, et al. Gestational diabetes is associated with high energy and saturated fat intakes and with low plasma visfatin and adiponectin levels independent of prepregnancy BMI. Eur J Clin Nutr 2013;67:196e201. [12] Park S, Kim MH, Kim SH. Early gestational weight gains within current recommendations result in increased risk of gestational diabetes mellitus among Korean women. Diabetes Metab Res Rev 2014;30:716e25. [13] Mozumdar A, Liguori G. Persistent increase of prevalence of metabolic syndrome among U.S. adults: NHANES III to NHANES 1999e2006. Diabetes Care 2011 Jan;34(1):216e9. [14] O'Neill S, O'Driscoll L. Metabolic syndrome: a closer look at the growing epidemic and its associated pathologies. Obes Rev 2015;16:1e12. [15] Centers for Disease Control and Prevention (CDC). Trends in intake of energy and macronutrients-United States, 1971e2000. MMWR Morb Mortal Wkly Rep 2004;53:80e2. [16] Vadiveloo M, Scott M, Quatromoni P, Jacques P, Parekh N. Trends in dietary fat and high-fat food intakes from 1991 to 2008 in the Framingham Heart Study participants. Br J Nutr 2014;111:724e34. [17] Fryar CD, Wright JD, Eberhardt MS, Dye BA. Trends in nutrient intakes and chronic health conditions among Mexican-American adults, a 25-year profile: United States, 1982e2006. Natl Health Stat Rep 2012;50:1e20. [18] Feldeisen SE, Tucker KL. Nutritional strategies in the prevention and treatment of metabolic syndrome. Appl Physiol Nutr Metab 2007;32:46e60. [19] Committee of Dietary reference intake in Korean Nutrition Society. Dietary reference intake for Koreans. Seoul: Korean Nutrition Society; 2008.
Please cite this article in press as: Park S, et al., Very-low-fat diets may be associated with increased risk of metabolic syndrome in the adult population, Clinical Nutrition (2015), http://dx.doi.org/10.1016/j.clnu.2015.09.010
66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18
YCLNU2651_proof ■ 16 October 2015 ■ 9/9
S. Park et al. / Clinical Nutrition xxx (2015) 1e9 [20] Kweon S, Kim Y, Jang MJ, Kim Y, Kim K, Choi S, et al. Data resource profile: the Korea National Health and Nutrition Examination Survey (KNHANES). Int J Epidemiol 2014;43:69e77. [21] Kanazawa M, Yoshiike N, Osaka T, Numba Y, Zimmet P, Inoue S. Criteria and classification of obesity in Japan and Asia-Oceania. World Rev Nutr Diet 2005;94:1e12. [22] World Health Organization regional office for the Western Pacific region, International Association for the Study of Obesity; International Obesity Task Force. The Asian-Pacific perspective: redefining obesity and its treatment. Sydney: Health Communications Australia; 2000. [23] Research Team: Department of Agrofood Resources. Standard food composition table. 7th version. Rural development administration. Wanju-gun: National Academy of Agricultural Science, Korea; 2007. [24] Korea Center of Disease and Control and Prevention by Korea Ministry of Health and Welfare. Users' guide for Korean National Health and Nutrition Examination Survey. Daejeon: Statistics Korea; 2011. [25] Cohen E, Cragg M, deFonseka J, Hite A, Rosenberg M, Zhou B. Statistical review of US macronutrient consumption data, 1965e2011: Americans have been following dietary guidelines, coincident with the rise in obesity. Nutrition 2015;31:727e32. [26] Ford ES, Capewell S. Trends in total and low-density lipoprotein cholesterol among U.S. adults: contributions of changes in dietary fat intake and use of cholesterol-lowering medications. PLoS One 2013;8:e65228.
9
[27] Thompson FE, Subar AF. Dietary assessment methodology. In: Coulston AM, Boushey CJ, Ferruzzi MG, editors. Nutrition in the prevention and treatment of disease. 3rd ed. San Diego: Academic Press; 2013. [28] Schwingshack L, Hoffmann G. Comparison of effects of long-term low-fat vs high-fat diets on blood lipid levels in overweight or obese patients: a systematic review and meta-analysis. J Acad Nutr Diet 2013;113: 1640e61. [29] Schwingshack L, Hoffmann G. Comparison of the long-term effects of high-fat v. low-fat diet consumption on cardiometabolic risk factors in subjects with abnormal glucose metabolism: a systematic review and meta-analysis. Br J Nutr 2014;111:2047e58. [30] Schwingshack L, Hoffmann G. Long-term effects of low-fat diets either low or high in protein on cardiovascular and metabolic risk factors: a systematic review and meta-analysis. Nutr J 2013;12:48. [31] Vadiveloo M, Parkeh N, Mattei J. Greater healthful food variety as measured by the US healthy food diversity index is associated with lower odds of metabolic syndrome and its components in US adults. J Nutr 2015;145: 564e71. [32] Oh HY, Kim MK, Lee M, Kim YO. Macronutrient composition and sodium intake of diet are associated with risk of metabolic syndrome and hypertension in Korean women. PLoS One 2013;8:e78088.
Please cite this article in press as: Park S, et al., Very-low-fat diets may be associated with increased risk of metabolic syndrome in the adult population, Clinical Nutrition (2015), http://dx.doi.org/10.1016/j.clnu.2015.09.010
19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36