**3. Results**

The general characteristics of the study population are presented in Table 1. The mean ages of the controls and students with ADHD were 9.1 and 9.0 years, respectively. The total energy intake was higher in controls than in students with ADHD (*p* = 0.008). Father's educational background and occupation significantly differed between ADHD students and controls (*p* < 0.001 and *p* = 0.001, respectively).


**Table 1.** General characteristics of study population 1 .


**Table 1.** *Cont.*

All analyses were performed with the data matched for age, sex, and dietary survey season.

1

PCA identified four major dietary patterns among the 32 food groups, and the associated factor loading scores with absolute values DUHVKRZQLQ7DEOH7KH³WUDGLWLRQDO´GLHWDU\SDWWHUQZDV characterized by high intakes of condiments, vegetables, tofu/soymilk, and mushrooms. The "seaweed-egg" dietary pattern included high intakes of seaweeds, fats/oils, sweets, and eggs. The "traditional-healthy" dietary pattern included high intakes of kimchi, grains, bonefish, and low intakes of fast foods and beverages. The "snack" dietary pattern was characterized by high intakes of snacks and processed meat and a low intake of noodles. Lean fish, other seafood, and yogurt were not listed due to their low factor loadings in all examined dietary patterns. Each dietary pattern explained 8.0%, 6.0%, 5.6%, and 5.4% of the variation in food intake, respectively.


**Table 2.** Factor loadings for the four major dietary patterns derived from principal components analysis with orthogonal rotation.


**Table 2.** *Cont.*

Factor loadings with absolute values ZHUHOLVWHGLQWKHWDEOHDPRQJIRRGJURXSs.

The distribution of characteristics by dietary pattern score tertiles is presented in Table 3. Increasing scores in the traditional and traditional-healthy patterns were correlated with a decreased percent energy from fat (*P* for trend = 0.001; *P* for trend <0.001, respectively), whereas the percent energy from carbohydrate increased as the score of the traditional-healthy pattern increased (*P* for trend <0.001). Fatty acids were significantly associated with dietary pattern scores. The traditional pattern score was associated with a high intake of total fatty acids; the seaweed-egg and traditional-healthy pattern scores were associated with high intakes of PUFAs and omega-3 fatty acids, whereas the snack pattern score was negatively associated with the intakes of total fatty acids, PUFAs, and MUFAs. Regarding mineral intake, calcium intake was positively associated with the scores of the traditional, traditional-healthy, and snack patterns, and iron was positively associated with the scores of the traditional and traditional-healthy patterns. Heavy metal exposure via food consumption was also assessed, and mercury was positively associated with the traditional, traditional-healthy, and snack patterns; lead was positively associated with the traditional and snack patterns.

The ORs and 95% CIs of ADHD were analyzed across the tertiles of dietary pattern scores (Table 4). The OR (95% CI) in the highest tertiles of the traditional dietary pattern compared to those in the lowest tertiles in crude model was 0.29 (0.13–0.64), but a significant association was not observed in multivariate model 2 (OR: 0.76, 95% CI: 0.26–2.24). The seaweed-egg pattern was not significantly associated with ADHD in any of the models. The snack pattern score was positively associated with the risk of ADHD, but a significant association was observed only in the second tertile in crude model and multivariate model 1. Students in the highest tertile of the traditional-healthy pattern score had an increased risk of ADHD in the multivariate-adjusted models when compared with those in the lowest tertile (OR (95% CI): 0.32 (0.13–0.82) in multivariate model 1; 0.31 (0.12–0.79) in multivariate model 2).





trend of nutrient and metal consumption was adjusted for total energy intake; PUFAs: Polyunsaturated fatty acids, MUFAs: Monounsaturated fatty acids.


**Table 4.** Distribution of characteristics by the tertiles of dietary pattern scores <sup>1</sup> .

1 All analyses were performed with the data matched for age, sex, and dietary survey season; <sup>2</sup> Adjusted for gestation age, birth weight, mother's age, birth order, father's education, and father's occupation; <sup>3</sup> Model 2 + additional adjustment for total energy intake, omega-3 fatty acids, lead, and mercury consumption; <sup>4</sup> Tertiles of dietary pattern scores; <sup>5</sup> Tests for trend were conducted by assigning the median value to each tertile of heavy metal intake as a continuous variable.

#### **4. Discussion**

The present study identified four dietary patterns. The traditional-healthy dietary pattern, characterized by high intakes of kimchi, grains, and bonefish, and low intakes of fast foods and beverages, was associated with lower odds having ADHD. Although the present study focused on dietary factors, significant associations with ADHD were found in father's education and occupation. Socioeconomic status of children is generally related to household income, and parent's educational background and occupation. Children from lower socioeconomic status are more likely diagnosed with ADHD than children from higher socioeconomic status in previous studies [14í@. Family income [14,15], parent's education [15–17] and occupation [15,16] were significantly associated with ADHD. Education status of mother was highly correlated with that of fathers in this study, and occupation of mother did not vary compared to that of father's. Thus, fathers' educational background and occupation were used as surrogate of socioeconomic status. As those variables were high associated with ADHD, we adjusted them for the analysis.

The role of diet in the behavior of children has been controversial, but associations between several nutritional factors and child behavior such as ADHD have been continually suggested [12,13]. Food additives, sugar, and aspartame are considered negative factors in the development of ADHD, and thus, dietary intervention studies with special diets, including additive-free and sugar elimination diets, have been conducted. A meta-analysis has reported that artificial food coloring is associated with childhood hyperactivity [18]. However, in a sugar elimination intervention study, there was no evidence that refined sugar affected child behavior [19–24].

The role of polyunsaturated fatty acids (PUFAs), particularly omega-3 fatty acids, in relation to neurodevelopmental disorders has been studied because omega-3 fatty acids play a critical role in brain development and function [25]. Children with ADHD have lower levels of omega-3 fatty acids, and the supplementation of omega-3 fatty acids can reduce the symptoms of ADHD in school-aged children and adolescents [26,27]. However, there was no clear evidence of improvement in ADHD symptoms with omega-3 supplementation in randomized controlled trials, but these findings could be the result of methodological problems [28,29]. The association between dietary pattern score and fatty acid intake was investigated in this study. The traditional, seaweed-egg, and traditional-healthy pattern scores were negatively associated with ADHD, although only the traditional-healthy pattern had a statistically significant association; moreover, they were positively associated with fatty acid intake. By contrast, the snack pattern score showed a positive association with ADHD and was negatively associated with the intake of total fatty acids, PUFAs, and MUFAs. However, additional adjustment for omega-3 fatty acid intake did not change the statistically significant association between the traditional-healthy dietary pattern and ADHD. Thus, the factors associated with the beneficial effects of a healthy dietary pattern might be complex.

Regarding mineral intake, calcium was positively associated with the scores of the traditional, traditional-healthy, and snack patterns, and iron was positively associated with the scores of the traditional and traditional-healthy patterns. Zinc was not associated with any of the four pattern scores. Iron deficiency may be associated with ADHD [30] because iron stores in the brain can influence dopamine-dependent functions [31,32]. A case-control study in India reported that the serum ferritin level was lower in children with ADHD [33], while another study found that ADHD symptoms in children with low serum ferritin levels were alleviated following iron supplementation [34]. In a 19-year follow-up study, the iron status of Costa Rican children was found to be associated with behavioral problems in adolescents [35]. The role of zinc nutrition in ADHD is not clear, but evidence suggests that zinc is beneficial in the treatment of children with ADHD [36,37]. Zinc deficiency is involved in dopamine transporter dysfunction [38], and intervention studies have found that zinc supplementation can reduce ADHD symptoms in children with low zinc levels [39–41]. Both, low iron and zinc levels have been associated with dopamine metabolism, and low levels of iron and zinc are involved in impaired dopamine transmission in subjects with ADHD [42–45].

Heavy metal exposure via food consumption was also investigated. Mercury was positively associated with the traditional, traditional-healthy, and snack patterns, and lead was positively associated with the traditional and snack patterns. The association between lead exposure and ADHD has been widely studied, and a meta-analysis has reported that lead exposure is positively associated with ADHD symptoms [46]. In a study with school-aged children living in two Romanian cities near a metal-processing plant, an association with ADHD was observed only for lead exposure, not aluminum or mercury exposure [47]. An association between the blood mercury level and ADHD in Chinese children in Hong Kong has been observed [48], but a significant association was not found in a cross-sectional study of Romanian children [47] or in a Children's Health and Environment Research (CHEER) study that surveyed elementary schools in six South Korean cities [49,50]. A more clear association with ADHD has been observed for lead exposure, even at low concentrations [49,50]. Prenatal mercury exposure is associated with an increased risk of neurobehavioral disorders, and lead exposure in childhood has been associated with ADHD [51]. In this study, lead and mercury consumption was positively correlated with the traditional-healthy dietary pattern, but it did not alter the beneficial effects of the traditional-healthy dietary pattern on ADHD.

Recently, associations between dietary patterns and ADHD have been examined in several cross-sectional studies [6,20,21]. One study, which included a population-based cohort of adolescents, reported that a Western-style dietary pattern, characterized by high intakes of fat, refined sugars, and sodium and low intakes of fiber, folate, and omega-3 fatty acids, was associated with increased odds of an ADHD diagnosis, whereas a healthy dietary pattern, with high intakes of fiber, folate, and omega-3 fatty acids, was not correlated with the diagnosis of ADHD [20]. In a study of adolescents in China, three major dietary patterns were identified, and dietary patterns characterized by a high intake of snacks or animal-derived foods were associated with higher odds for psychological symptoms [21]. In Iranian school-aged children, four major dietary patterns were identified. The higher scores of the dietary patterns associated with a high intake of sweets and fast food were associated with greater odds for having ADHD, but no significant association was observed for the healthy or Western dietary patterns [6]. In this study, traditional-healthy dietary pattern was positively associated with dietary factors, such as PUFAs and minerals that are known for beneficial effects on ADHD. Another beneficial effect of the traditional-healthy dietary pattern might be associated with the low fast food intake. Junk foods are generally high in fat, sugar, additives, artificial food colorings, and preservatives, which may negatively affect ADHD symptoms [52]. Overall, the traditional-healthy dietary pattern was associated with many dietary factors that affect childhood behavioral disorders, such as ADHD.

The present study has several limitations. As this was a case-control study, it is possible that dietary intake was affected by an individual's health status and social background. Thus, causal inference cannot be determined. Results could differ by ADHD types, but information about ADHD type was not gathered for subgroup analysis due to small sample size. However, such pattern analyses are useful to further understand the diet of ADHD children as a whole rather than classifying it by a single nutrient or food group.

#### **5. Conclusions**

The traditional-healthy dietary pattern, which is characterized by high intakes of kimchi, grains, and bonefish, and low consumption of fast foods and beverages, appears to be negatively associated with ADHD in school-aged Korean children.
