This study comprehensively investigated the influences of allergic diseases on children's EF difficulties, age-dependent EF development, and the relationship between EF and ADH problem. To the best of our knowledge, this was the first study to show that age-dependent EF development had different trajectories according to the allergic disease. In this study, children with a history of asthma or AR generally showed a higher level of EF difficulties. Previous studies have suggested that the release of inflammatory factors and cytokines in allergic diseases may alter the functioning of the prefrontal cortex and neurotransmitter systems, which play an important role in planning, organization, and behavior regulation [31], by causing neuronal damage, oxidative stress, blood brain barriers disruption, and neurotrophic factors [5, 32, 33]. In addition, the studies that investigated the psychological effects of allergic diseases suggested that the stress from children and parents due to hospitalization, school absence, and a need to avoid allergy triggers may lead to a child's behavioral problems [34]. Internalizing problems (e.g., depression, anxiety) associated with allergic diseases could also be the cause of behavioral difficulties [34]. However, unlike asthma and AR, the history related to AD did not associate with EF. This was similar to some previous studies [35, 36], including a study that investigated the relationship between allergic diseases and ADHD in Korean children [37], but different from other studies [38, 39].
One of the important results of this study showed that asthma is also related to a developmental trajectory of emotional regulation, not only increased the level of EF difficulties. In the case of AR and other EFs, there was no difference in the age-related trend of EF between allergic and non-allergic groups. However, in the case of asthma, the level of emotional control difficulty increased rapidly between the age of 8 and 9 compared to the group without asthma. The results of this study have an implication for the age at which allergic diseases influence EF, which is deeply related to a structural change in EF with age. Several critical studies focused on the structure of EF have found that it has a unitary structure before the age of 7 [40–42], while it changes to a multi-factor model in school-aged and adulthood [43, 44] as in Miyake, et al. [45]’s study. In this study, the fact that the children with asthma or AR showed higher level of EF difficulties in all sub-areas during the age of 7–10 implies that asthma and AR have primarily influenced the EF development before 7 years old, and because the structure of EF was unitary at that time, all sub-areas of EF were influenced. However, at the age of 8–9, after the structure of EF became a multi-factor model, asthma only affected individual factor, so only the developmental trajectory of emotional control has changed. In summary, the results of this study suggest that the age at which allergic diseases influence EF varies by the type of disease, and the developmental trajectory of EF varies depending on whether its structure is composed of single or multi-factor at that time.
In this study, the EF difficulties changed with age, and it generally showed a trend of peaked around the age of 8–9 and decreased around the age of 10. The strength of this study is that we annually investigated the changes in children's EF by sub-areas. Similar results were found in previous studies that examined the prevalence of ADHD by age [46, 47]. Interestingly, the developmental trajectories of behavior and emotional control were somewhat different. Unlike the other two EFs, the level of behavioral control difficulty tended to gradually decrease after the age of 7. These results support what previous studies argued that emotional and behavior regulation should be treated as two separate constructs [48]. To sum up the literatures assuming that self-regulation is a multidimensional structure, behavior and emotional regulation are related but have separate developmental trajectories [49].
Finally, this study suggested that allergic diseases could influence the relationship between EF and ADHD. Children with a history of asthma or AR showed a higher correlation between EF difficulties and CBCL’s ADH problem scale. Previous studies investigating the relationship between EF and sub-types of ADHD showed that EF deficits were more related to the symptoms of inattention (IA) than hyperactive-impulsivity (H-I) [15, 50]. However, conflicting results were found for differences between IA and combined type of ADHD [51]. Therefore, the higher correlation between ADH problem scale and EF, which has a strong association with IA symptoms, implies that asthma and AR are more associated with the ADHD-IA subtype rather than ADHD-HI. However, since subtypes of ADHD could be changed as children grow up [52], further studies are needed on which characteristics of certain subtype are associated with allergic diseases.
Limitations
There were several limitations in this study. The first was associated with a relatively small sample size of this study. For example, only 44 children scored a T score of 65 or higher on the ADH problem scale, which was the cut-off point of the borderline clinical range. This has resulted from the traits of PSKC which investigated a wide range of characteristics of children, parents, family, and school, not only on the variables of this study. To reduce errors that could be caused by small sample size, large-scale studies focused on allergic diseases, EF, and ADHD are needed in the future to verify the results of this study. In addition, oversimplification might have occurred during the dichotomization of the ADH problem scale according to the cutoff score. Therefore, in this study, the correlation between EF difficulties and ADH problem scale using raw scores was presented in a supplementary file (Table A1). Third, recall bias and response bias might have occurred in the process of parents responding to the items related to the child's behaviors and allergy history. In future studies, the use of structured clinical interviews or performance-based tests may ensure objectivity in measuring a child's characteristics. Nevertheless, in predicting ADHD symptoms in children, a previous study has reported that behavioral rating by parents was more useful than performance-based tests [53]. The fourth was the limitation related to the validity of the measurement tools used in this study. Although its validity has been proved [25], the sub-areas of EF in this study were somewhat different from the generally known core components of EF [45]. This limitation also occurred concerning the ADH problem scale. Therefore, consideration of these limitations is necessary when comparing the results of this study directly with other studies related to EF or ADHD. In addition, this study failed to account for variables such as a comorbid mental illness of children that could play a significant role in the relationship between allergic diseases and EF [34]. Therefore, it seems necessary to consider comorbid physical and mental illness of children and parents in further studies, and the results of this study may be strengthened or weakened accordingly. Finally, although this study showed longitudinal changes in EF according to allergic diseases, it does not explain the causal relationship between them. This was because this study did not include the history of allergic diseases after the age of 7, and accordingly, the results of this study do not imply that the diminish or treatment of allergic symptoms leads to EF improvement or ADHD treatment.