Executive Function Among Children and Adolescents With Primary Headache

Abstract

Background

Headache is the most common neurologic symptom among children and adolescents, with a point prevalence of 58%. Headache disorders, particularly migraine, are considered one of the most disabling conditions in childhood. Headaches may cause cognitive impairment; however, research on this symptom—particularly on its influence on executive functioning—remains limited. We aimed to examine the executive function among children and adolescents with primary headache disorder compared to controls. Determining executive problems is important, as it allows us to ensure appropriate support and intervention.

Methods

This cross-sectional case-control study was performed at the Department of Pediatrics and Adolescents Medicine, Copenhagen University Hospital, Herlev, Denmark. A total of 109 pediatric patients diagnosed with primary headache were recruited from the pediatric outpatient clinic, along with 112 controls without a headache diagnosis. Executive function was assessed using selected subtests from the Delis-Kaplan Executive Function System (D-KEFS): the Trail Making Test, the Figure Design Test, and the Verbal Fluency Test.

Results

Among the patients, 31 were diagnosed with migraine, 31 with tension-type headache, 31 with mixed headache, and 16 with unclassified headache. A significance level of P <.05 was applied. Patients with headache performed significantly worse than controls on the Trail Making Test (P = .015). No statistically significant differences in executive function were observed between the migraine and tension-type headache subgroups.

Among children with migraine, higher headache frequency was associated with poorer performance on the Verbal Fluency Test–Switching condition (P = .04). In children with mixed headache, higher headache frequency was similarly associated with poorer performance on the Trail Making Test–number-letter switching (P = .037).

Conclusion

We found a significant difference between the patient and control group in one of the subtests, suggesting that headache could be associated with poorer executive function. Future studies are needed to examine the causality of this association.

Keywords

adolescents children executive function migraine tension-type headache

Headache in children and adolescents is a major problem, which might affect attendance of school and other normal activities.^1,2 The prevalence of headache is nearly 58%, and specifically for migraine the prevalence is 7.7% in children and adolescents.^3–5

Furthermore, migraine represents the most significant neurologic cause of disability among children and adolescents.⁶

Although headache is one of the most common symptoms among children and adolescents—and one of the most common types of pain in childhood—its impact on cognitive function is not well understood, and the studies examining this topic are limited.⁷ Understanding whether headache affects cognitive performance is especially important when school attendance is compromised, as this could help guide optimal support strategies for affected children.

Some studies found that children with headache performed worse on verbal tasks than healthy controls.^8,9 One study reported that children with migraine made more errors and had poorer performance on a visual attention test than controls.¹⁰ Although some studies have explored cognitive functioning in children and adolescents with headache, the current study focuses specifically on executive functions, assessed using the Delis-Kaplan Executive Function System (D-KEFS). Although D-KEFS has previously been employed to evaluate executive functioning in children with epilepsy, to our knowledge, no prior studies have applied this instrument to investigate executive function in children and adolescents with headache.

The aim of this study was to examine the executive function among children and adolescents with the common types of primary headache, including both migraine and tension-type headache (TTH), compared with controls. Executive functions included cognitive processes such as planning, attention, language, problem solving, and cognitive flexibility.

Our hypothesis was that executive functions were affected in children and adolescents with headache regardless of the type of headache.

Methods

This cross-sectional case-control study was performed at the Pediatric Outpatient Clinic (POC) for headache at Herlev University Hospital, Denmark.

Participants

Between April 2019 and April 2021, all patients visiting the Pediatric Outpatient Clinic (POC) were invited to participate in the study. The only exclusion criterion was an inability to understand Danish, in order to prevent communication barriers.

Headache diagnosis was given by experienced neuropediatricians at the POC according to the International Classification of Headache Disorders, 3rd Edition (CHD-3), guidelines, and subsequently verified by the research team. Based on the final diagnosis, patients were categorized into one of 4 groups: (1) migraine (with or without aura), (2) TTH, (3) mixed headache, or (4) unclassified headache. Children with both migraine and TTH were assigned to the mixed headache group, and children with symptoms that did not fulfill any diagnostic criteria of the ICHD-3 guidelines were grouped in the unclassified category.

Healthy controls were recruited from schools located within the hospital's catchment area between November 2022 and January 2024. The aim was to include age-, sex-, and geographically matched controls. Inclusion criteria for controls were age between 6 and 19 years, no clinical diagnosis of headache, and no use of medication for headache. As with the patient group, individuals who could not understand Danish were excluded.

Materials and Procedures

Confounding Variables

The patients’ medical records were reviewed to collect data on age, sex, headache frequency, and the educational and work status of their parents.

Headache frequency was categorized as follows: daily (≥15 days per month), weekly (4-14 days per month), monthly (1-3 days per month), and less than monthly.

Parents’ educational and work status were used to determine socioeconomic status (SES), based on the classification by the Institute of Social Research. In this system, group 1 represents individuals with a high level of education, whereas group 5 includes unskilled workers.¹¹

Delis-Kaplan Executive Function System

The Delis-Kaplan Executive Function System (D-KEFS) is a collection of 9 independent tests designed to assess various components of executive functioning in both children and adults. In this study, we used 3 tests: The Trail making Test, the Verbal Fluency Test, and the Design Fluency Test.

The Trail Making Test consists of 5 conditions: (1) visual scanning, (2) number sequencing, (3) letter sequencing, (4) number-letter switching, and (5) motor speed. In the first mentioned condition, the examinees are asked to cross out all instances of the number 3 on a sheet. In the number sequencing condition, they must draw a connecting line for the numbers 1 to 16 in order. The third condition requires examinees to connect the letters from A to P in alphabetical order. For all 3 mentioned conditions, there are distractor numbers and/or letters on the examination sheet. The number-letter switching condition requires them to make a connecting line switching between numbers and letters: 1, A, 2, B, etc. In the last condition, the motor speed condition, examinees are told to connect the circles on the page by following the dotted line, as quickly as they can. The time it takes to finish each of the conditions is noted and called the raw score.

The Verbal Fluency Test also consists of 3 conditions: The first one is the letter fluency condition, where the examinees must generate as many words as possible starting with a specific first letter. In the second condition, the category fluency condition, participants were required to generate as many words as possible within a specific category. The last condition also requires generating words, but with the condition that the examinee must switch between two semantic categories, fruits and furniture: apple, table, banana, sofa etc.

The Design Fluency Test consists of 3 conditions: (1) filled dots, (2) empty dots only, and (3) switching. The first 2 conditions require the examinee to connect, respectively, filled dots and empty dots by only using 4 straight lines and make as many different designs as possible. For the last condition, they have to switch between filled and empty dots while connecting them with 4 straight lines. For the last 2 tests, the number of correct words/designs made in 60 seconds in each condition is noted (raw scores).

Raw scores from all test conditions were converted to age-normed scaled scores using normative data from a US sample of 1750 children and adults.^12,13 A scaled score between 7 and 13 is considered within the normal range, encompassing low average to high average performance.

The neuropsychological tests were administered by 3 different examiners. To minimize the risk of intertester bias, the exact same sentences were used during instruction of the tests, regardless of the examiner. Additionally, all the tests were conducted and scored following training and under the supervision of an experienced psychologist.

Statistical Methods

Descriptive statistics for both patients and controls and the statistical analysis were calculated using the SPSS software platform (version 29; IBM Corp). The data were normally distributed, except for socioeconomic status (SES) and the age of the control group.

To assess group differences, 2 sets of comparisons were performed: (1) between patients and controls, and (2) between patients with migraine and those with TTH. χ² tests were used for categorical variables, and a univariate general linear model was used for continuous variables. Age and sex were included as confounders in the general linear model analyses.

Additionally, the correlation between the executive function and headache frequency was examined separately within each headache category using general linear models, where age and sex again were included as confounders. Headache frequency was measured using categorical frequency variables (eg, once daily, once weekly, several times per week).

Ethics Statement

This study was approved by Health Research Ethics Committee (reference number: H19003374) and The Danish Data Protection Agency (reference number: VD-2019-222).

Results

A total of 109 children with a headache diagnosis and 112 control children were included in this study. Table 1 presents the cohort characteristics of the groups, stratified by headache diagnosis and by patient vs control status. Patients with migraine were younger than those with TTH, and a significant difference in sex distribution was observed between these 2 groups. However, no significant differences were found in SES.

Table 1.

Characteristics of Study Participants: Sex, Age, and Socioeconomic status.

Characteristics	Migraine(n = 31)	Tension-type headache(n = 31)	P ^a	Mixed headache(n = 31)	Unclassified headache(n = 16)	Allpatients(n = 109)	Control(n = 112)	P ^b
Sex			<.001^c					.438^c
Male, n (%)	20 (64.5)	5 (16.1)		10 (32.3)	9 (56,3)	44 (40.4)	51 (45.5)
Female, n (%)	11 (35.5)	26 (83.9)		21 (67.7)	7 (43,8)	65 (59.6)	61 (54.5)
Age, mean (SD) in patients and median (IQR) in healthy controls	12.4 (2.6)	15.1 (2.8)	<.001^d	14.9 (2.4)	12.5 (2.8)	13.9 (2.9)	11.5 (9.3-14.2)	<.001^d
SES, median (IQR)	2.0 (1.0-3.0)	2.0 (1.0-3.0)	.996^c	1.0 (1.0-2.0)	1.0 (1.0-2.0)	2.0 (1.0-3.0)	2.0 (1.0-2.0)	.612^c

Abbreviations: SES, socioeconomic status; TTH, tension-type headache.

The P values refer to the comparison between the migraine group and TTH group.

The P values refer to the comparison between “All patients” and the “Control” group.

Tested by χ² test.

Tested by 1-way analysis of variance.

When comparing patients and controls, the control group was significantly younger than the patient group. There were no significant differences in sex distribution or SES between these 2 groups.

Table 2 summarizes the results of the cognitive assessments using D-KEFS. The variables of executive function assessment by D-KEFS were normally distributed, and all the analyses were adjusted for both age and sex. Adjustment for socioeconomic status was not performed, as no statistically significant differences were observed between the patient and control groups. Patients performed significantly worse than controls on the Trail Making Test in the number-letter switching condition, with a mean score of 10.2 compared to 11.0 in the control group. No significant differences were observed between patients and controls on the Figure Design Test or the Verbal Fluency Test. Additionally, no significant differences were found between the migraine and TTH groups in any of the D-KEFS subtests.

Table 2.

Results of Executive Function Assessment by D-KEFS in Children and Adolescents with Headache and in Controls. Mean (SD) of the scaled scores of the 3 tests. The variables are normally distributed.

D-KEFS Variables	Migraine(n = 31)	Tension-type headache(n = 31)	Mixed headache(n = 31)	Unclassifiedheadache(n = 16)	Allpatients(n = 109)	Control(n = 112	P
Trailmaking, D-KEFS
Visual scanning	10.4 (2.1)	10.1 (2.4)	11.0 (2.1)	10.6 (2.0)	10.5 (2.2)	10.7 (2.6)	.554^e
Number sequencing	11.8 (2.0)	11.0 (2.3)	11.4 (2.5)	12.3 (1.9)	11.5 (2.3)	12.1 (1.8)	.095^e
Letter sequencing	10.7 (3.3)	10.7 (2.6)	14.3 (17.4)	10.8 (3.6)	11.7 (9.7)	11.9 (2.3)	.671^e
Number-letter switching	10.1 (2.5)	10.4 (2.1)	10.4 (2.2)	9.3 (2.7)	10.2 (2.3)	11.0 (2.4)	.015^e
Motor speed	13.5 (0.8)	12.8 (1.4)	12.8 (1.3)	13.4 (0.8)	13.0 (1.2)	13.2 (1.0)	.783^e
Figure design,D-KEFS
Filled dots	12.3 (3.4)	12.7 (2.9)	12.2 (3.0)	11.6 (3.0)	12.3 (3.1)	11.8 (2.6)	.349^e
Empty dots	12.5 (2.9)	11.7 (3.0)	11.7 (3.0)	11.0 (3.2)	11.8 (3.0)	11.8(2.7)	.682^e
Switching	11.7 (2.6)	12.8 (3.1)	12.4 (2.9)	11.7 (3.7)	12.2 (3.0)	12.6 (2.7)	.310^e
Verbal fluency,D-KEFS
Letter	9.2 (2.7)	9.7 (2.6)	10.0 (3.5)	9.1 (3.0)	9.5 (3.0)	9.4 (3.2)	.773^e
Category	12.0 (2.5)	12.1 (3.3)	11.3 (2.9)	12.3 (2.9)	11.9 (2.9)	12.5 (3.2)	.051^e
Switching	11.0 (2.4)	11.7 (2.8)	10.6 (3.0)	10.8 (1.6)	11.1 (2.6)	11.1 (2.8)	.974^e

Abbreviations: Delis-Kaplan Executive Function System.

Analysis of the relationship between executive function and headache frequency revealed no significant correlations, except for the outcome variable Verbal fluency–switching condition (P = .044) among patients with migraine, and the Trail Making–number-letter switching condition (P = .037) among patients with mixed headache.

Discussion

In this study, we examined the executive function in children and adolescents with a primary headache diagnosis compared with healthy controls. We found that children and adolescents with primary headache had poorer executive function according to the Trail Making Test than healthy controls. The difference was small, but statistically significant, even after adjustment for age and sex. Although it is difficult to determine with certainty whether the difference is clinically relevant, it is important to be aware that children with headache may have impaired executive functioning.

Furthermore, we did not find any statistically significant differences in performance on D-KEFS between the patients with migraine and the patients with TTH.

With increasing headache frequency, children with migraine performed significantly worse on the subtest Verbal Fluency–switching condition, and those with mixed headache showed poorer performance on the Trail Making Test–number-letter switching subtest.

Several studies have examined cognition in children and adolescents with headache; however, the number of studies focusing on executive functions remains limited. To our knowledge, no prior study has used D-KEFS as an assessment tool in this population.

Some studies have investigated differences in cognitive performance between children with migraine and those with TTH; however, the results remain contradictory.^8,9 Esposito et al⁸ found a lower verbal intelligence quotient (IQ) and a higher performance IQ in children with TTH compared with children with migraine without aura and healthy controls. In addition, they found that the migraine group tended to have lower perceptual organization ability than the other 2 groups. Compared with our study, Esposito et al used a broad measure for cognitive function (IQ), whereas we specifically have examined executive function. This could be a reason for the different results between the studies.

Waldie et al⁹ examined the association between headache and the cognitive function in a longitudinal cohort study of individuals born between April 1, 1972, and March 31, 1973, in New Zealand, who were examined psychologically and medically at different ages between age 3 and 26 years. Academic performance was estimated using total scores from New Zealand national examinations during the final 2 years of high school, while data on postschool academic qualifications were collected at age 26. The study found that patients with migraine had significantly poorer verbal abilities, which also negatively affected their academic performance, compared to those with TTH.

In a meta-analysis, Pizer et al¹⁴ aimed to evaluate whether neuropsychological functioning was impaired in pediatric populations with primary headaches compared to headache-free controls. The neuropsychological domains assessed included motor skills, executive functioning, learning and memory, language, processing speed, intelligence, and visuospatial/constructional abilities. Across the included studies, the analysis revealed significantly poorer neurocognitive performance in pediatric participants with migraine compared with non-headache controls. However, this effect was not observed among those with TTH. Another study by Margari et al¹⁵ aimed to evaluate potential deficits in nonverbal cognitive abilities—specifically memory and attention—in children and adolescents affected by migraine or TTH. The study included 35 patients aged 11-18 years with primary headache and 23 healthy control subjects, all assessed using the nonverbal Leiter-3 test. The findings indicated that headache-related disability had a significant impact on cognitive domains related to nonverbal memory and sustained attention.

Two other studies have shown decreased performance in Trail Making Test in children with migraine compared with healthy controls.^10,16

In these studies, a more traditional form of the Trail Making Test was used compared to the subtest in D-KEFS. The D-KEFS version of the Trail Making Test differs from the traditional form by having more interference stimuli and more trails. A recent study compared the older versions of Trail Making Test with newer ones, and it did not show a qualitative difference between them.¹⁷

In this study, the patients had poorer performance on condition 4 of the Trail Making Test. Condition 4 is the most important part of the D-KEFS Trail-Making Test because it examines cognitive flexibility, which is a classic executive function and is essential for skills such as multi-tasking, divided attention, and simultaneous processing. In everyday life, reduced cognitive flexibility can cause difficulties in academic and social functioning, for example, difficulties with planning, initiating, and completing the tasks; difficulties in processing information; and problems with teamwork.^18–20 If the executive function is impacted in children with headache, it is important to give them the right support to ensure the best opportunities for education and learning.

When examining the executive function in children and adolescents with headache, headache frequency is an important factor to consider. In our analysis, we examined whether headache frequency influenced executive function among every headache category. However, a statistically significant difference was observed only in the Verbal Fluency Test–switching (condition 3) within the migraine group, and in the Trail Making Test–number-letter switching (condition 4) among patients with mixed headache. The small sample size might be one of the reasons that we did not find any other statistically significant associations between executive function and headache frequency, and larger studies are needed in order to examine this further.

We found no significant differences in performance on the Verbal Fluency Test or the Figure Design Test between the patients with primary headache and controls. In contrast, a previous study involving adolescents with migraine reported reduced performance in the animal-naming category of the Verbal Fluency Test.¹⁶ To the best of our knowledge, no other studies have used Verbal Fluency and Figure Design tests in children with primary headache.

Although D-KEFS has not been used previously in studies examining executive function in children with primary headache, it has been used to examine executive function in children with epilepsy.^21–23 These studies showed that children with epilepsy had difficulties with executive functions and that D-KEFS was a reliable tool to assess executive function in this patient group and therefore we expect D-KEFS also to be a reliable tool in other neuropediatric patient populations.

Although our study and some other studies may indicate an association between headache in children and the executive function, it is not possible to infer causality. Future longitudinal studies are needed to examine this association and the causal relationship.

Strength and Limitations

This study has several strengths. Firstly, in this clinical cohort, the headache diagnosis was made by experienced neuropediatricians according to ICDH-III criteria and afterward verified by the research assistants.

Furthermore, the research assistants performing D-KEFS were trained and supervised by an experienced neuropsychologist.

A limitation of this study is its cross-sectional design, which does not make it possible to follow the individuals over time, and thereby conclude on the causality of the association between primary headache in children and the executive function. Furthermore, there is a risk of selection bias, because we included a patient group with children who have been referred to the hospital with headache, and they therefore may be more severely affected than children with headache who are not referred to a secondary clinic. Finally, although we attempted to age-match the patient and control groups, there was a statistically significant age difference between them. Although age was included as a confounder in the analyses, the possibility of residual confounding cannot be excluded.

Conclusion

Patients with headache had poorer performance than controls on one of the subtest of Delis-Kaplan Executive Function system (D-KEFS), suggesting reduced executive functioning, and no significant difference was found between children with migraine and children with TTH. Moreover, with increasing headache frequency, children with migraine performed significantly worse on the Verbal Fluency Test–switching condition, whereas children with mixed headache showed poorer performance on the Trail Making Test–number-letter switching subtest.

Future studies are needed to examine the causality of association between headache in children and executive function.

Supplemental Material

sj-docx-1-jcn-10.1177_08830738261424943 - Supplemental material for Executive Function Among Children and Adolescents With Primary Headache

Supplemental material, sj-docx-1-jcn-10.1177_08830738261424943 for Executive Function Among Children and Adolescents With Primary Headache by Zahraa Nima, Amalie Berring-Uldum and Nanette Mol Debes in Journal of Child Neurology

Footnotes

Acknowledgements

Not applicable.

ORCID iDs

Zahraa Nima

Amalie Berring-Uldum

Nanette Mol Debes

Ethical Considerations

This study was approved by Health Research Ethics Committee, reference number H19003374 and The Danish Data Protection Agency, reference number: VD-2019-222.

Consent to Participate

The patients and their parents were introduced to the project and informed of all aspects of the trial both at the POC and by an email with informational documents. Written consent from both parents were obtained before the examination day.

Consent for Publication

Not applicable.

Author Contributions

Zahraa Nima - Analysing the data, writing the article. Amalie Berring-Uldum - the study design, conducting it and analyzing data. Writing and supervision. Nanette Mol Debes - Writing and supervision.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

Declaration of Conflicting Interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Supplemental Material

Supplemental material for this article is available online.

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