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INTRODUCTION
In recent years, many Asian countries have seen a rapid westernization of their traditional dietary patterns, characterized by high intake levels of animal fats, refined sugar, and low vegetable intake, which has become associated with an increased risk of obesity and other chronic health conditions [1]. Similarly, South Korea has shown a large shift in the overall structure of its traditional dietary patterns in the past 3 decades, which has been associated with changes in disease patterns [2,3].
Traditionally, the common Korean meal type has been characterized by including rice and several smaller side dishes that were usually vegetable-based; the most popular dishes were cooked rice and noodles as the primary carbohydrate source, and cooked vegetables and a small serving of protein (meat, poultry, fish, egg, beans) as side dishes. Kim et al. [4] reported that traditional Korean diet, which was characterized by low fat intake and high vegetable consumption, has been associated with a low prevalence of chronic diseases in Korea. Song and Joung [5] further showed that the Korean traditional dietary patterns have been associated with a decreased incidence of metabolic abnormalities, such as high blood pressure and dyslipidemia. Favorable changes in cardiovascular risk factors have been reported by regular consumption of a Korean traditional diet for 12 wk in hypertensive and diabetic patients [6].
Despite the reported beneficial effects of a Korean traditional diet, within the past decade, there has been an increased adoption of nontraditional dietary practices, including selecting more westernized foods such as bread instead of rice. Breakfast has mostly been adapted to the westernized diet, whereas dinner has been maintained mostly as the traditional Korean dietary pattern [7]. In addition to the changed breakfast types, skipping breakfast has become a concern in Korea and worldwide [8,9,10]. Although many studies have emphasized the importance of eating breakfast [11,12,13,14] and shown it is an important determinant of a healthy lifestyle [15], those changes have primarily been observed in Korean and Chinese American cultures [7,16,17]. According to a report from the Korean National and Nutrition Examination Survey in 2010, 20.5% of Koreans skip breakfast [10]. Common reasons for skipping breakfast or having a westernized breakfast could include habitual oversleeping-which decreases the amount of time for breakfast in the morning-the increasing availability of 'convenience' foods such as bread because of the rapid development of the processed food industry, and the increasing professional and social participation of Korean women [11,18].
We hypothesize that Korean adults who have continued the traditional Korean breakfast of primarily rice with a variety of side dishes maintain better nutritional quality and health status than Korean adults eating 'convenient', nontraditional breakfasts or skipping breakfast altogether. In this study, we aimed to establish the relationship between daily nutrient intakes and health outcomes with dietary types at breakfast amongst Korean adults using the 2007-2009 Korean National Health and Nutrition Examination Survey (KNHANES).
SUBJECTS AND METHODS
Subjects
This study was based on data obtained from the 4th (2007-2009) KNHANES conducted by the Korean Centers for Disease Control and Korean Ministry of Health and Welfare [10]. The survey is a nationwide representative study using a stratified, multistage probability sampling design for the selection of household units. The sampling frame was based on the 2005 National Census Registry and 31,705 subjects aged ≥ 1 year were recruited.
The survey consisted of the following 4 components: the health interview survey, the health behavior survey, the health examination survey, and the nutrition survey. Among the 31,705 subjects, 24,871 (78.4%) participated in the survey; among those, 22,137 subjects participated in the nutrition survey. The inclusion criteria for our study was adults aged 20-64 years; the exclusion criteria were pregnant women and adults who could not be classified into the 5 major breakfast pattern groups we chose to observe. As a result, 11,801 subjects were selected for our analysis. The study was approved by the Korean Centers for Disease Control and Prevention Institutional Review Board.
Dietary intake
The diet in KNHANES was assessed based on 1-day food intake data collected using the 24-hr dietary recall method. Trained interviewers visited each household and instructed respondents to recall and describe the foods and beverages consumed over the previous 24 hr.
For the analysis, participants were divided into 5 groups based on their dietary breakfast types, which was determined from the 24-hr recalls: rice with 3 or more side dishes, rice with 0-2 side dishes, noodles, bread and cereal, and breakfast skipping. Three or more side dishes were used as a cut-off point for a balanced diet because 3 servings of meat, eggs, or beans and 7 servings of vegetables or side dishes (10 servings/d) are recommended daily in the Korean dietary guidelines [19]. This became 3 servings (1 serving of meat, eggs, or beans and 2 serving of vegetable dishes) when a total of 10 servings of side dishes were divided by 3 meals. Furthermore, using 3 dishes as a cut-off point, the number of breakfast groups was evenly distributed. In the 2 rice groups, side dishes included everything from soup and other dishes eaten with rice except kimchi; kimchi was excluded because most Korean people eat it at every meal and several variations in kimchi exist, so the number of kimchi servings was not considered to reflect a variety of vegetable side dishes or individual intake differences. Furthermore, kimchi intake is a controversial issue because of its high sodium content [20]; therefore, it was not included in the number of side dishes in terms of categorizing a variable diet. Breakfast types that could not be classified into the 5 breakfast pattern groups because there were only a few observations for the group (e.g., porridge) were excluded in the analysis.
Daily energy and nutrient intakes and nutrient density per 1,000 kcal during 24 hr were calculated and compared among breakfast pattern groups. The percentage of subjects whose nutrient intake was below the estimated average requirement standard for vitamin and minerals and the 75% of the estimated energy requirement (EER) for energy intake was calculated [19].
Anthropometric measurements and health examination survey
Height and weight were measured based on standard procedures from the 2007-2009 KNHANES (Ministry of Health and Welfare and the Korea Centers for Disease Control and Prevention) and body mass index (BMI). BMI was categorized using the Asia-Pacific standards for Asians: the cut-off point was BMI ≥ 25 kg/m2 (mild obesity). Waist circumference was measured using standardized techniques, with the cut-off points for abdominal obesity being ≥ 90 cm and ≥ 80 cm for men and women, respectively, based on the Asia-Pacific standards for Asians.
In our analysis, we used the criteria established by the Korean Society for the Study of Obesity based on the National Cholesterol Education Program Adult Treatment Panel III. Blood samples collected in the morning after fasting for at least 8 hr were analyzed and categorized: fasting plasma glucose ≥ 110 mg/dl for high blood glucose, triglycerides ≥ 150 mg/dl for high triglycerides, total cholesterol ≥ 200 mg/dl for high total cholesterol, high-density lipoprotein cholesterol (HDL-C) < 40 mg/dl in men and < 50 mg/dl in women for low HDL-C. Blood pressure was measured using a sphygmomanometer with the subject in a sitting position. Hypertension was defined as a systolic blood pressure ≥ 140 mm Hg and/or a diastolic blood pressure ≥ 90 mm Hg.
Participants were considered as having metabolic syndrome if at least 3 of the following 5 conditions were present based on criteria established by the National Cholesterol Education Program Adult Treatment Panel III: waist circumstance ≥ 90 cm in men and ≥ 80 cm in women, plasma glucose ≥ 110 mg/dl, serum triglyceride level ≥ 150 mg/dl, HDL < 40 mg/dl in men and < 50 mg/dl in women, and systolic and diastolic blood pressure ≥ 140/90 mmHg.
Income was divided by quartile and education was divided into 4 groups ≤ 6 years, 9 years, 12 years, and ≥ 16 years [10]. Smoking was divided into 3 groups; everyday, sometimes, and no smoking. Alcohol drinking was divided into drink ≥ 1 cup/mo and < 1 cup/mo; physical activity was regular if subjects did ≥ 30 min and ≥ 5 times/wk of walking/moderate physical activity or ≥ 20 min and ≥ 3 times/wk of severe activity.
Statistical analysis
All data were reported as mean ± standard error (SE) or as numbers and percentages. Categorical data were analyzed using the chi-square test; continuous data were analyzed using the analysis of covariance after adjusting for sex, age, income, education, smoking, drinking, and physical activity. Probability levels of P < 0.05 were considered to be statistically significant and exact P values are listed in the tables and text. Logistic regression was used to examine the relationship between biochemical risk factors associated with metabolic diseases and breakfast meal pattern adjusting for age and sex. All statistical analyses were performed by survey procedures to account for the complex sample design effect and appropriate sample weight using the SAS 9.2 statistical package.
RESULTS
Breakfast types
Table 1 shows general characteristics of study subjects. Of the 11,801 subjects, 35.53% (n = 4,193) were in the rice with 3 or more side dishes (Rice3+) group, 34.73% (n = 4,098) in the rice with 0-2 side dishes (Rice0-2) group, 1.56% (n = 184) in the noodle (Noodle) group, 6.56% (n = 774) in the bread and cereal (Bread) group, and 21.63% (n = 2,552) in the breakfast skipping (Skipping) group. The distribution of breakfast groups significantly differed by sex and age groups, with a higher percentage of women in the Rice3+ group and significantly more participants of older ages in both rice groups; in the other breakfast type groups, there were more participants of younger ages. Breakfast types were also significantly different by income, education, smoking, drinking, and physical activity.
Nutrient intakes
Tables 2 and 3 show total daily energy and nutrient intakes in which the percentages of nutrient intake are compared with Korean Recommended Nutrient Intake levels and nutrient density per 1,000 kcal. Fat intakes were significantly higher in the Bread and Noodle groups than in the other groups (P < 0.0001); sodium intake was the highest in the Noodle group (P < 0.0001). When the percentages of daily nutrient intakes are compared with the Korean Recommended Nutrient Intake levels, the Skipping group showed the lowest intake level and the Rice3+ group showed the highest intake level in both energy and nutrients. The Bread group showed the highest intake of calcium and riboflavin. Other than the Skipping group, the Rice 0-2 group showed a relatively low intake level of iron and vitamin A.
Nutrient density per 1,000 kcal showed that Rice3+ group had high nutrient density for most nutrients excluding total fat, carbohydrate, thiamin, and riboflavin, whereas the Rice0-2 and the Skipping groups showed low nutrient density for protein and the most vitamins and minerals. The Rice0-2 group showed the highest carbohydrate and lowest calcium, riboflavin, and vitamin C density level; the Noodle group had highest fat and iron densities. In the Bread group, the fat density as well as protein, calcium, riboflavin, niacin, and vitamin C densities were relatively high compared with other groups.
When the nutrient-deficient rates-the percentage of subjects whose nutrient intake was below the estimated average requirement for micronutrients-and the 75% of EER for energy intake for Koreans were compared among the 5 groups (Table 4), the Skipping group showed the highest rates for all nutrients. The rate was lowest in the Rice3+ group for energy, protein, iron, vitamin A, and vitamin C. For calcium and riboflavin, deficient rates were lowest in the Bread group and highest in the Rice0-2 and Skipping groups. The deficient rates for vitamins A and C were also relatively high in the Rice0-2 and Noodle groups.
When comparing the overconsumption rate for energy (> 125% EER), fat (≥ 25% of total energy from fat) and sodium (≥ 2,000 mg) were highest in the Noodle group. The fat overconsumption rate was highest in the Noodle, Bread, and Skipping groups, and lowest in the Rice3+ and Rice0-2 groups.
Risk factors of metabolic syndrome
Table 5 shows the risk of obesity, dyslipidemia, hypertension, high blood glucose, and metabolic syndrome for the 5 breakfast groups after controlling for potential confounding variables. When compared with the Rice3+ group, the odds ratios for the risk of obesity (BMI ≥ 25 kg/m2) and abdominal obesity (waist circumference ≥ 90 cm for men, ≥ 80 cm for women) was higher in the Skipping, Rice0-2, and Noodle groups. The odds for the risk of abdominal obesity in the Noodle group were 1.43 times greater than for the Rice3+ group. The risk of hypercholesterolemia was approximately 1.44 times higher, but the risk of hypertriglyceridemia was 36% lower in the Bread group when compared with the Rice3+ group. The risk of metabolic syndrome was also higher in the Rice0-2, Noodle, and Skipping groups with odds ratios of 1.23, 1.70, and 1.20, respectively, but lower in bread group with an odds ratio of 0.72.
DISCUSSION
Our study showed that among a sample size of 11,801 Korean adults aged 24-60 years, 70.26% ate rice with side dishes (the traditional meal type) for their breakfast, 21.63% skipped breakfast-with the highest skipping rate in those aged 20-34 years-and 8.12% followed other breakfast patterns (bread, noodles). We did find that in adults aged 20-29 and 30-39 years, 44.9% and 22.5% skipped breakfast, respectively, which was much higher than the 25.1% breakfast skippers in young American adults there were associated with low nutrient intakes, including calcium and riboflavin [21]. Our study also showed that the Skipping group showed poor daily nutrient intake with a high percentage of energy from fat and a higher risk of obesity and metabolic syndrome when compared with the Rice3+ group, as seen in similar studies that showed detrimental effects of skipping breakfast on cardiometabolic health [22,23,24,25,26]. However, despite those results, a recent study concluded that there was a lack of evidence for a causal relation between skipping breakfast and obesity, although an association was observed between them [27]. In an experiment of causal relation between breakfast and behaviors related to obesity, Leidy et al. suggested that the type of breakfast is also important, concluding that a high-protein breakfast reduced evening snacking compared with skipping breakfast, whereas a low-protein breakfast did not [28].
Our data agree with the results of other studies that studied the association of diet and disease patterns among Korean populations in which an association between a rice-based diet with a relatively low prevalence of obesity was shown [3,4,7]. However, we also found that the diversity of foods at breakfast even in rice-based, traditional breakfast is important to daily nutrient intake levels. Among those eating a rice-based breakfast, the Rice3+ group had higher daily nutrient intakes than other groups-especially in nutrients emphasized for Korea such as calcium and riboflavin-and a lower risk of obesity, abdominal obesity, and metabolic syndrome. Eating a rice-based meal with a few sides may lead to an increased consumption of rice instead of a variety of foods that can result in adverse health outcomes. Kim and colleagues reported that a rice-based, traditional dietary pattern as well as a high-fat, high-sweets, and coffee pattern could positively be associated with an increased risk of obesity in Korean [29]. Another study also reported that an unbalanced Korean diet with little variety was related to higher risk of metabolic syndrome and elevated blood pressure [20].
Another distinguishing result in our study was the positive association between noodles at breakfast and blood pressure. The Noodle group showed a high level of fat and sodium intake, with a higher risk of abdominal obesity, metabolic syndrome, and hypertension. The high sodium intake levels may be explained by the high sodium content of noodle soups, which may lead to a higher risk of hypertension and metabolic syndrome. Shin et al. reported the association between the increased risk of metabolic syndrome and instant noodle consumption as well, although they included only instant noodles, not all types of noodles [30].
The Bread breakfast group had the highest levels of calcium and riboflavin intake, but also had a high level of fat intake. This may have occurred in the Bread group because the foods often eaten with bread or cereal-such as milk, cheese, and processed meat-because Koreans may think bread or cereal mixes well with those foods that originated from western countries (bread and cereal are not traditional foods in Korea). The Bread group also showed a higher risk of hypercholesterolemia, as we expected; these results were similar in individuals who ate a bread-based diet for breakfast: they were more likely to have elevated serum total cholesterol levels [14]. However, in our study, the Bread group was not associated with the risk of obesity and metabolic syndrome. These results disagree with significant positive associations between western dietary patterns or oily food and serum triglyceride levels, blood pressure, abdominal obesity, and metabolic syndrome [31,32,33]. We believe that the reasons these did not lead to metabolic syndrome in the Bread group may result from the unexpectedly relatively lower risk for high blood triglycerides and low HDL levels. We also believe these results in the Bread group may be related to the relatively lower carbohydrate intake compared with carbohydrate intake in the other groups. Similar results were reported in other studies: that too much carbohydrate intake was significantly associated with higher serum triglyceride and low HDL in Korean adults [34,35]. Another study also showed an association with a lower risk of low HDL in women in the semi-western diet, characterized by a relatively high intake of meat and poultry [20].
One of the limitations of this study is that breakfast consumption type and daily nutrient intakes were estimated using a 24-hr dietary recall method, which may have resulted in the misclassification of usual dietary patterns by individuals because a single 24-hr dietary recall may not reflect the usual breakfast habits and food intakes of a population. Another limitation is that our study is a cross-sectional analysis, which allowed us to look at the association between breakfast types with biochemical and anthropometric indices, but limited us from making any conclusions of definitive causality and long-term health outcomes. However, despite these limitations, we found that breakfast plays an influential role in the Korean adult's overall nutritional status and that breakfast types may be a good indicator of the overall dietary and health status of an individual based on the differences in the daily nutrient intake levels and health status among the 5 breakfast groups.
A major strength of this study is that the subjects were selected to represent the general population; as a result, this reduces the errors of results from the bias of sample selection. Additionally, we were able to obtain useful information related to dietary types at breakfast, enabling us to adjust for related confounding variables including sex, age, income, education, smoking, drinking, and physical activity in contrast to many other studies that have primarily focused only on the importance of breakfast eating [36,37].
In conclusion, the traditional Korean, rice-based breakfast reflected the most desirable nutritional status and health outcomes when eaten with 3 or more side dishes, showing both the potential advantage of a rice-based diet in terms of nutritional content and the importance of food diversity. Our findings suggest that the Skipping group had poor daily nutrient intake patterns, whereas the Noodle breakfast group showed high fat and/or sodium intake and a higher risk of hypertension, or metabolic syndrome. This study suggests a need for increased nutrition education to help reduce the practice of skipping breakfast-and an increased need for strategies to effectively tackle the issue of balancing foods at meals.
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