A traditional Korean dietary pattern and metabolic syndrome abnormalities

Nutrition, Metabolism & Cardiovascular Diseases (2012) 22, 456e462 available at www.sciencedirect.com

journal homepage: www.elsevier.com/locate/nmcd

A traditional Korean dietary pattern and metabolic syndrome abnormalities Y. Song a, H. Joung b,* a

School of Human Ecology, The Catholic University of Korea, 43-1 Yeokgok2-dong, Wonmi-gu, Bucheon-si, Gyeonggi-do 420-743, Republic of Korea b Graduate School of Public Health, Seoul National University, San 56-1 Shillim-dong Kwanak-gu, Seoul 151-742, Republic of Korea Received 15 March 2010; received in revised form 30 August 2010; accepted 6 September 2010

KEYWORDS Dietary pattern; Metabolic syndrome; HDL-cholesterol; Korean

Abstract Background and aims: Using national data, we explored the relationship between dietary patterns and metabolic abnormalities to address how the traditional Korean diet, high in carbohydrate and low in animal fat with plenty of plant foods, has influenced metabolic abnormalities in the adult population. Methods and results: We examined cross-sectional associations between dietary patterns and the risk of metabolic abnormalities in 4,730 subjects aged 20 years or more using both health and dietary data from the 2005 Korean National Health and Nutrition Examination survey. Three evident dietary patterns were derived by cluster analysis: ‘Traditional’ (50.3% of total population), ‘Meat and Alcohol, (15.8%) and ‘Korean Healthy’ (33.9%). The ‘Traditional’ group was characterised by high consumptions of rice and kimchi, while the ‘Korean healthy’ group ate a modified Korean-style diet with various foods such as noodles, bread, eggs and milk, and the ‘Meat and Alcohol’ group had high consumptions of processed meat and alcohol. Compared with the ‘Traditional’ pattern, the ‘Meat and Alcohol’ pattern was associated with a 33% increased risk of having elevated blood glucose, a 21% increased risk of having elevated serum triglycerides and a 21% increased risk of having elevated blood pressure. However, the ‘Traditional’ pattern showed a 23% increased risk of having low high density lipoprotein (HDL)cholesterol compared with the other two patterns by logistics analysis. Conclusions: Fifty percent of the Korean adult population continues to follow a traditional dietary pattern, having beneficial effects with respect to some metabolic abnormalities. However, the high prevalence of low HDL-cholesterol, attributable to a high-carbohydrate diet, should be considered. ª 2010 Elsevier B.V. All rights reserved.

* Corresponding author. Tel.: þ82 2 740 8865; fax: þ82 2 745 9104. E-mail addresses: [email protected] (Y. Song), [email protected] (H. Joung). 0939-4753/$ - see front matter ª 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.numecd.2010.09.002

Korean dietary patterns and metabolic syndrome Since the World Health Organization (WHO) defined the cluster of metabolic derangements known as metabolic syndrome, numerous studies have been performed. The core components of metabolic syndrome are insulin resistance, impaired glucose tolerance, hypertension, dyslipidaemia, and central obesity, and these components as well as metabolic syndrome are reportedly related to increased risks of developing coronary heart disease, cancer, and even mortality [1e3]. To prevent or manage metabolic syndrome, it has been suggested that we need to understand lifestyle-associated risk factors and then modify them. According to Orchard et al. [4], 3-year cumulative incidences of metabolic syndrome were significantly reduced in a lifestyle intervention group compared with a placebo group, among people who had impaired glucose tolerance at baseline. Several lifestyle factors including a high body mass index (BMI), smoking, alcohol consumption, exercise, and eating habits have been found to influence metabolic syndrome abnormalities, and among dietary patterns, the Mediterranean diet and the Dietary Approaches to Stop Hypertension diet were reported to have a strong impact on metabolic syndrome [3,5e8]. Recent dietary studies have increasingly used dietary pattern approaches rather than the traditional focus on individual foods, nutrients or dietary components. Dietary pattern approaches are beneficial as they capture the complex nature of dietary intake and explore its relationship with health outcomes. Up to this date, many studies have reported associations between dietary patterns and metabolic syndrome [1,9e11]. Despite some inconsistencies in those findings, it is interesting to note that dietary patterns rich in whole-grains, legumes, vegetables and fish have favourable effects on metabolic abnormalities. On the other hand, so-called ‘Western’ patterns characterised by high fat foods have been shown to increase the risks of metabolic abnormalities such as type 2 diabetes and cardiovascular disease [12,13]. However, most previous studies on this issue were conducted in Western populations, and there have been only a few studies on Asian populations, where the prevalence of metabolic syndrome has steadily increased over the past decade [14,15]. Thus, the purpose of this study was to identify a posterior dietary pattern among Korean adults using cluster analysis and data from a National Health and Nutrition Examination Survey, as well as to explore the relationships between defined dietary patterns and metabolic syndrome.

Methods Study population This study was based on data obtained from the third Korean National Health and Nutrition Examination Survey (KNHANES III) of non-institutionalised Korean civilians in 2005. Details of the KNHANES performed in 2005 have been previously described [16]. In brief, KNHANES III consisted of the following four components: (1) a health Interview Survey, (2) a health behaviors survey, (3) a health

457 examination survey and (4) a nutrition survey. A total of 34,145 individuals from a stratified, multistage probability sampling design were selected for the Health Interview study. Among them, 5,481 subjects who were aged 20 years or more and who had participated in the Health Examination Survey as well as the Nutrition Survey were included in this study. We excluded those who reported implausibly low or high daily energy intakes (<500 kcal day1 or >5000 kcal day1), resulting in a final analytical sample of 4,731 subjects.

Health examination and dietary measurement Height, weight and waist circumference were obtained using standardised techniques and calibrated equipment. BMI was calculated by dividing weight by height squared. Blood pressure was measured by standard methods, using a sphygmomanometer with the subject in a sitting position. Three measurements were made on all subjects at 5-min intervals, and the average of the second and third measurements was used in the analysis. Blood samples were collected in the morning after having fasted for at least 8 h. Fasting glucose, total cholesterol, triglycerides and high density lipoprotein (HDL)-cholesterol were analysed in a central, certified laboratory. A general questionnaire was administered for basic demographic and health-related information. Socio-demographic factors such as age, gender, education and region and lifestyle factors such as smoking and physical activity were chosen as confounding factors [6]. Smoking status was attained by asking whether he/she currently smoked, and physical activity data were gathered by asking whether he/ she engaged in physical activity at least 3 days or more per week and lasting at least 20 min or more at moderate intensity over the previous week. Dietary intake was measured by the single 24-h dietary recall method. Trained staff instructed the respondents to recall and describe all the foods and beverages they had consumed in the previous day. Food models and measuring bowls, cups and spoons were used to assist in estimating portion sizes.

Definition of metabolic syndrome We applied the original definition of metabolic syndrome proposed by the National Cholesterol Education Program (NCEP) Adult Treatments Panel III. However, we used ethnicity-specific values for waist circumference as proposed by the International Diabetes Federation (IDF). Participants who presented three or more of the following five criteria were defined as having metabolic syndrome: central obesity (waist circumference 90 cm in men and 80 cm in women), hypertriglyceridaemia (150 mg dl1), low HDL-cholesterol (<40 mg/dl1 in men and <50 mg/dl1 in women), hypertension (130/85 mm Hg) and hyperglycaemia (fasting plasma glucose 110 mg/dl1) [17,18].

Dietary patterns Dietary data were collected by a 24-h recall, and the food data were categorised into 23 food groups based on

458 common groups classified in the Korean Nutrient Database to simplify the interpretation of components, and the percentage of total energy intake was determined from each food group. Grains and their products accounted for almost half of daily energy intake; hence, this food group was further divided into four subgroups to address the following types of staple foods: white rice, other grains, noodles and dumpling, and flour and bread. Kimchi (traditional fermented cabbage) was also separated into a single group because it is a traditional Korean side dish [19]. The dietary patterns were derived by cluster analysis using the k-means algorithm. A series of steps along with our earlier work were used to select the most suitable number of clusters for the analysis [19,20]. Finally, three clusters were examined for sensible patterns and labelled by descriptive names based on the predominant food groups. The Korean diet typically consists of rice, soup and side dishes with plenty of plant foods, and is characterised as a low-fat and high-vegetable diet [21,22]. Half of the subjects were assigned to a ‘Traditional’ dietary pattern, in which consumption of white rice accounted for 60% of total energy intake and the consumption of kimchi (fermented cabbage, one of the side dishes) was higher than in the other two groups. Then, 15.8% of subjects were assigned to a ‘Meat and Alcohol’ dietary pattern because they had a higher consumption of meat and alcohol. The other 33.8% of the subjects were assigned to a ‘Korean Healthy’ dietary pattern, which was based on a rice and vegetable diet but was characterised by a variety of food groups such as other grains, fruit, eggs, fish and milk and had appropriate ratios of energy from carbohydrate and fat compared with the dietary reference intakes for Koreans [23].

Statistical analysis All statistical analyses were conducted using SAS (release 9.1; SAS Institute, Cary, NC, USA). Basic characteristics were tested using chi-square tests according to the dietary pattern groups. The generalized linear model was used to test for significant differences in mean values by the dietary pattern groups for biochemical parameters and nutrient intakes. Logistic regression was used to calculate odds ratios (ORs) with 95% confidence intervals (CIs) for the metabolic syndrome traits. Because socio-demographic characteristic including age, gender, education, region and lifestyle characteristics including smoking and exercise were different across dietary pattern groups, all the variables were considered as confounding factors and were adjusted in all logistic regression models.

Results The key characteristics of the three dietary patterns and mean nutrient intakes are presented in Table 1. The ‘Traditional’ pattern had more than half of its percent daily energy intake solely from white rice, and vegetable and Kimchi consumptions were higher in this pattern than in the other two patterns. The ‘Meat and Alcohol’ pattern received 27% of energy from white rice, 22% of energy from meat and its products, and 11% of energy from alcohol. The ‘Korean Healthy’ pattern received 27% of energy from

Y. Song, H. Joung white rice, 10% from other grains, 14% from noodles and 7% from bread, which resulted in a total of 58% from grain products. Consumptions of fruit, eggs, fish, milk and oil were higher in the ‘Korean Healthy’ pattern than in the other two groups. Energy intake was significantly different according to the dietary pattern groups, and the ‘Meat and Alcohol’ pattern had the highest intake. Carbohydrate intake (% of energy) was 72% in the ‘Traditional’ pattern, 65% in the ‘Korean Healthy’ pattern and 53% in the ‘Meat and Alcohol’ pattern, while fat intake (% of energy) was 28% in the ‘Meat and Alcohol’, 20% in the ‘Korean Healthy’ and only 13% in the ‘Traditional’ dietary pattern groups. Calcium intake was highest in the ‘Korean Healthy’ pattern, and iron, vitamin A and vitamin C intakes were highest in the ‘Meat and Alcohol’ pattern. Tables 2 and 3 present demographic characteristics and metabolic syndrome components according to the dietary pattern groups. Members of the ‘Traditional’ pattern were more likely to be older, less educated, and residing in a rural area. Members of the ‘Meat and Alcohol’ pattern were more likely to be young, male, and current smokers, and members of the ‘Korean Healthy’ pattern were more likely to be female, smoke less, and be more physically active. BMI and waist circumference were significantly different by the dietary pattern groups after adjusting for age and gender. Serum triglyceride levels were slightly higher in the ‘Meat and Alcohol’ pattern and HDL-cholesterol levels were significantly lower in the ‘Traditional’ pattern, whereas serum fasting blood glucose levels were lowest in the ‘Korean Healthy’ pattern group. The multivariate-adjusted ORs (95% CI) for metabolic syndrome are presented in Table 4. Members of the ‘Meat and Alcohol’ pattern showed a 21% higher likelihood of having hypertriglyceridaemia (p Z 0.056), a 33% higher likelihood of elevated fasting blood glucose (p Z 0.04) and a 23% lower likelihood of having low HDL-cholesterol (p Z 0.003) compared with the ‘Traditional’ pattern. Members of the ‘Korean Healthy’ pattern showed a 23% lower likelihood of having low HDL-cholesterol (p Z 0.046). Other abnormalities were not associated with the dietary patterns. We applied other definitions of metabolic abnormalities as proposed by WHO, IDF and the updated ATP III, but no differences were found (data not shown).

Discussion Dietary patterns rich in whole-grains, fruits, vegetables and dairy foods have been suggested as having benefits against metabolic syndrome [1]. The Korean diet is traditionally high in carbohydrate, low in fat, and abundant in plant foods. In this study, three distinctive dietary patterns were identified among the adult Korean population using data from the recent Korean National Health and Nutrition Survey. Half of the population maintained a traditional dietary pattern with high consumptions of white rice and kimchi (fermented cabbage), whereas 15.8% indicated a ‘Meat and Alcohol’ pattern and the remaining 33.8% showed a ‘Korean Healthy’ pattern. Compared with the ‘Traditional’ pattern, the ‘Meat and Alcohol’ pattern was

Korean dietary patterns and metabolic syndrome Table 1

459

Mean food and nutrient intakes by dietary pattern groups among Korean adults.

Food groups (% energy) White rice Other grain Noodle & dumpling Flour & bread Vegetables Legumes Kimchi Fruits Meat & its products Eggs Fishes Milk & dairy products Oils Beverages Alcohols Nutrient Percent of energy (%) From carbohydrate From fat From protein Energy (kcal) Protein (g) Fat (g) Carbohydrate (g) Calcium (mg) Iron (mg) Vitamin A (R.E) Vitamin C (mg)

Traditional (n Z 2384)

Meat & Alcohol (n Z 748)

Korean Healthy (n Z 1599)

Mean

Mean

Mean

Std. Dev.

Std. Dev.

Std. Dev.

60.3 3.9 0.9 1.5 3.5 2.7 1.7 1.2 3.9 1.3 4.7 1.6 3.2 1.8 0.9

12.5 5.8 4.1 3.7 2.7 3.6 1.5 3.2 5.6 2.7 5.7 3.9 3.1 3.0 3.5

27.1 3.8 2.1 3.0 3.2 1.8 1.2 1.6 21.7 1.7 4.2 1.9 3.9 2.4 11.1

11.3 6.1 5.7 5.3 2.0 2.8 1.1 3.6 13.1 2.8 4.9 4.3 3.4 3.5 15.6

27.0 9.7 14.1 6.9 3.2 2.8 1.2 2.5 4.0 2.2 5.7 3.3 4.2 2.6 1.3

11.6 13.2 16.8 9.2 2.4 4.1 1.1 4.8 5.0 3.2 6.9 6.3 3.8 4.5 4.3

72.1 13.4 14.5 1805 65 27 315 525 14 799 94

8.0 6.0 3.6 641 31 18 106 345 9 834 77

52.7 28.0 19.2 2450 104 70 282 581 17 939 123

10.4 9.9 5.1 881 45 41 110 359 10 830 93

64.6 19.9 15.5 2091 80 46 331 619 15 869 118

9.0 7.6 4.6 752 37 27 124 407 9 827 102

All the values were significantly different by dietary pattern groups after adjusted for age and gender.

associated with increased risks of several metabolic abnormalities. However, the ‘Meat and Alcohol’ and ‘Korean Healthy’ patterns were associated with a lower risk of having low HDL-cholesterol compared with the ‘Traditional’ pattern group. The prevalence of metabolic syndrome among adults increased from 24% in 1998 to 28% in 2001, according to data from the KNHANES, and these data were not much lower than a prevalence of 34% according to US NHANES III conducted during 1999e2002 [14,24]. Although the traditional Korean diet has healthy elements, many researchers have suggested that rapid nutrition transitions and the adoption of a Western lifestyle with rapid economic growth have played a role in this increase with regard to the prevalence of metabolic syndrome. However, we found that half of the Korean adult population maintained a ‘Traditional’ dietary pattern and another 33.8% in the ‘Korean Healthy’ dietary pattern also based their eating on the traditional diet. A Western dietary pattern did not emerge in this study. Plausible explanations are that there are movements to keep healthful elements of the traditional Korean diet, and a Western-style diet is more likely to affect children and young adolescents rather than adults, who had already established their dietary habits before the Western lifestyle was introduced.

Instead, we found the ‘Meat and Alcohol’ pattern group members more likely to be male, middle-aged from 30 to 49 years, living in a metropolitan area and a current smoker. Alcohol consumption is popular among Korean adults, especially middle-aged men. In 1995, the 1-month prevalence of alcohol consumption was 63.1% for the Korean adult population, with 20% of all deaths for Koreans attributable to alcohol use [25]. Binge drinking has been a problem in Korean men and a recent study found that male binge drinkers in Korea had an increased risk of mortality, especially from total and haemorrhagic stroke [26]. This pattern group also showed higher intakes of energy and fat compared with the other two pattern groups, causing elevated serum triglycerides and elevated blood glucose. Several studies have indicated that dietary patterns dominated by red and processed meats have increased risks of coronary heart disease, diabetes and metabolic syndrome [10,12,13]. Alcohol consumption was also suggested to be associated with the risk of metabolic syndrome. A large cohort study conducted in 4,999 Swedish adults aged 45e68 years found that a dietary pattern dominated by cheese, cake and alcoholic beverages was associated with increased risks of hyperglycaemia and dyslipidaemia [9]. These findings are in accordance with our results.

460 Table 2

Y. Song, H. Joung Demographic characteristics by dietary pattern group. Traditional (n Z 2384)

Meat & Alcohol (n Z 748)

Korean Healthy (n Z 1599)

pa

Age group (%) 20e29 30e49 50e64 65 or more

7.5 38.1 28.9 25.5

17.4 58.2 17.8 6.7

15.1 55.2 20.5 9.3

0.0001

Gender (%) Male

40.7

55.6

36.8

0.0001

Education (%) Elementary Secondary College or more

37.0 43.1 19.8

12.3 48.3 39.4

14.0 47.2 38.8

0.0001

Region (%) Metropolitan City Rural

39.8 29.9 30.3

46.3 36.5 17.3

48.8 34.2 17.1

0.0001

19.0

27.6

16.8

0.0001

28.5

30.3

32.5

0.0001

Current smoking (%) Yes b

Physical activity (%) Yes a

p from chi-square test. b Physical activity was assigned as ‘yes’ if subjects engaged in physical activity at least 3 days or more per week and lasting at least 20 min or more at moderate intensity over the previous week.

One of the interesting findings in this study was the association of the dietary patterns with low HDL-cholesterol prevalence. Members of both the ‘Meat and Alcohol’ and ‘Korean Healthy’ patterns had significantly reduced risks of having low HDL-cholesterol compared with the ‘Traditional’ pattern. This may be explained by the nature of the highcarbohydrate and low-fat diet in the traditional Korean dietary pattern. According to the Dietary Reference Intakes (DRIs) for adults, the recommendation for total energy intake from carbohydrate is 45e65% in the US and 55e70% in Korea, based on the acceptable macronutrient adult distribution range (AMDR) [23]. In this study, the ‘Traditional’ dietary pattern group derived 72% of energy intake from carbohydrate, which exceeded the AMDR for Koreans. Using data from US NHANES III, Yang et al. [27] reported that

Table 3

a carbohydrate intake of over 60% of energy intake in US adults had a protective effect in terms of lowering BMI, but negative effects in terms of lowering HDL-cholesterol and increasing serum triglycerides. Further, based on data from Korean NHANES III, Park et al. [16] reported that a carbohydrate intake of over 70% of energy in Korean women was associated with low HDL-cholesterol. Samaha et al. [28] suggested that low-carbohydrate diets have more favourable effects on metabolic abnormalities, including serum triglycerides and HDL-cholesterol. Although the prevalence of having low HDL-cholesterol was considerably high, from 33% to 49% of adults aged 20 years or more, based on the first to the third Korean NHANES, carbohydrate intakes (% of energy) were similar according to a Korean NHANES report, 2006 and a high carbohydrate intake such as over 70% of

Metabolic syndrome components by dietary pattern group.

BMI (kg/m2) Waist circ. (cm) serum TG (mg/dl) HDL-cholesterol (mg/dl) Glucose (mg/dl) SBP (mm Hg) DBP (mm Hg)

Traditional (n Z 2384)

Meat & Alcohol (n Z 748)

Korean Healthy (n Z 1599)

Mean

Std. dev.

Mean

Std. dev.

Mean

Std. dev.

23.7 81.4 135.0 44.5 95.7 121.8 77.8

3.2 9.7 112.2 10.7 20.5 18.8 10.8

23.9 81.5 144.7 45.9 96.1 117.6 77.8

3.2 9.2 115.2 11.7 24.8 16.6 12.1

23.6 79.8 129.3 45.7 94.4 116.3 76.1

3.3 9.6 138.6 10.6 25.8 17.0 10.5

TG, triglyceride; glucose, fasting blood glucose; SBP/DBP, systolic/diastolic blood pressure. a All models were adjusted for age, gender, education, region, smoking, and physical activity.

pa

0.0196 0.0162 0.0959 0.0027 0.0004 0.2529 0.2381

Korean dietary patterns and metabolic syndrome Table 4

461

Odds Ratios (OR) for metabolic abnormalities by dietary patterns. Traditional

Meats & Alcohols

Korean Healthy

OR

OR

95% CI

95% CI

Abdominal obesity M > 90, F > 80

1.00

1.14

(0.94e1.38)

1.02

(0.88e1.18)

Hypertriglyceridemia 150 mg/dl

1.00

1.21

(1.00e1.47)**

1.06

(0.91e1.24)

Low HDL-cholesterol M < 40, F < 50 mg/dl

1.00

0.77

(0.65e0.92)*

0.87

(0.76e1.00)*

Elevated blood pressure 130/85 mm Hg

1.00

1.21

(0.99e1.47)

0.94

(0.81e1.11)

High fasting blood glucose 110 mg/dl

1.00

1.33

(1.01e1.75)*

1.02

(0.81e1.28)

Metabolic syndrome 3 or More

1.00

1.21

(0.92e1.58)

0.92

(0.75e1.13)

All logistic models were adjusted for age, gender, education, region, smoking, and physical activity (*p < 0.05, **p Z 0.056).

energy might be linked to a high prevalence of having low HDL-cholesterol in the Korean population. This should therefore be further explored. Nevertheless, it has been suggested that the traditional Korean diet has favourable effects on central obesity and serum triglycerides with regard to lower fat intake [20,21]. Another interesting finding was that the ‘Korean Healthy’ dietary pattern was based on the traditional Korean diet, rice and vegetables and was varied by noodles, bread, fruit, eggs and milk and dairy products, and carbohydrate intake was reduced to 65% of energy compared with 72% in the ‘Traditional’ pattern. While the ‘Korean Healthy’ pattern had protective effects on the prevalence of having low HDL-cholesterol levels, it had no significant associations with other metabolic abnormalities. Hence, as a modified Korean-style pattern, the ‘Korean Healthy’ pattern in this study might be favourable for addressing metabolic abnormalities among Korean adults. Thus, future studies are necessary to explore the unclear aspects of the Korean diet according to carbohydrate levels and their relationship to metabolic abnormalities. This study has several limitations. Our results alone cannot be directly generalized into the public setting due to the subjectivity of the dietary pattern technique. No single dietary variable can be considered solely responsible for the association of diet with the metabolic syndrome. This dietary pattern technique, however, was practical and useful to provide fundamental information on the relationships between a traditional Korean dietary pattern and the risk of metabolic syndrome at the population level. Thus, combining dietary pattern methods to capture overall diet quality as well as to refine quantitative dietary variables would help to better understand the relationships between diet and the metabolic syndrome. Further studies are necessary to explore the mechanisms of a high-carbohydrate diet on HDL-cholesterol levels and confirm the potential benefits of a Korean-style diet against the metabolic syndrome by using both types of dietary measurements. Another limitation was that we used data from a single 24-h recall, which might not represent usual intake. At the

population level, 24-h recalls can be used as a surrogate measure of usual intake. In addition, dichotomised variables for smoking and physical activity were used in this study, which would limit the nature of its own variables. Lastly, the cross-sectional design of our study limited causal inference between dietary factors and metabolic abnormalities. Thus, these results need to be confirmed by additional, longitudinal data. In conclusion, our findings suggest that a ‘Meat and Alcohol’ dietary pattern is negatively associated with metabolic abnormalities compared with a ‘Traditional’ pattern. Furthermore, a modified Korean-style, ‘Korean Healthy’ pattern that is moderately high in carbohydrate appears to be favourable against metabolic abnormalities among the Korean adult population.

Acknowledgements This work was supported by the Catholic University of Korea, Research Fund, 2009. None of authors had conflicts of interest to disclose.

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