Abstract
Post-traumatic headache is common after pediatric traumatic brain injury and affects thousands of children every year, but little is known about how headache affects recovery after traumatic brain injury in other symptom domains. We aimed to determine the association between headache and other common symptoms after pediatric traumatic brain injury and explore whether subjective complaints of headache are associated with objective deficits on specialized neurocognitive testing. We conducted a retrospective cohort study of children ages 3–19 years following traumatic brain injury with a completed Sports Concussion Assessment Tool (SCAT) questionnaire. Post-traumatic headache was defined by a score more than 2 on the SCAT question for headache and define headache groups for comparison. In our cohort, we analyzed data from the Delis-Kaplan Executive Function System and the Wechsler Abbreviated Scale of Intelligence, Second Edition (WASI-II). Headache was reported in 40 (33%) patients presenting for post-traumatic brain injury care among 121 pediatric traumatic brain injury patients and did not differ by injury severity. Median total SCAT symptom score in the headache group was 5-fold higher compared to patients without headache (median 45.5 vs 9; P < .001). Significantly lower-scaled scores in color naming, matrix reasoning, letter sequencing, and letter switching were also found in the headache group (all P ≤ .03). Our study shows that headache, as reported by patients on the SCAT, is associated with higher symptom scores in all other symptom domains, including sleep, mood, sensory, and cognitive. Headache was also associated with worse objective neurocognitive measures and may identify patients who could benefit from specialized follow-up care and management.
Keywords: cognition, concussion, headache, pediatric, outcome, traumatic brain injury, risk factor
Traumatic brain injury, defined as the alteration of brain function or brain pathology following external force, is a leading cause of long-term morbidity in children. More than 500 000 pediatric patients present to the emergency department for traumatic brain injury and 50 000 require hospitalization in the United States each year.1,2 From 2001 to 2012, the rate of emergency department visits for a diagnosis of traumatic brain injury or concussion more than doubled among children aged 19 years or younger.3 Traumatic brain injury leads to a range of long-term morbidities including physical, psychosocial, and neurocognitive deficits.4
Post-traumatic headache is one of the most common complaints following pediatric traumatic brain injury across all injury severities and may persist long term.5 Chronic headache in otherwise healthy children is an important morbidity to consider when providing care to patients because it interferes with school, social function, and parental productivity.6 It may be more relevant for consideration in children with traumatic brain injury who concurrently suffer functional and neurocognitive impairments related to direct brain injury. While some neurocognitive impairment after traumatic brain injury is related to location and severity of brain injury, even patients with mild traumatic brain injury and no identifiable brain injury on imaging suffer impairments in memory, attention, processing speed, language, and executive function that can persist for years and few effective interventions exist.7,8 Data are limited in pediatric post-traumatic headache as it relates to other morbidities including neurocognitive dysfunction, and whether headache treatments can modify other important morbidities following pediatric traumatic brain injury is unknown. Limited research has left clinicians without guidance on the identification and management of post-traumatic headache, which may have a key role in improving other outcomes.9,10
Our institution provides systematic care for children with traumatic brain injury including symptom evaluation and management through multidisciplinary concussion and pediatric neurocritical care programs.11,12 Both programs provide pediatric traumatic brain injury expertise that includes systematic symptom and comorbidity evaluations with medical and neuropsychological assessments. In this study, we evaluated post-traumatic headache in children presenting for post-traumatic brain injury evaluation and management. We aimed to determine the prevalence of headache, association between headache and other post-traumatic symptoms, and explore the relationship between headache and neurocognitive outcome. We hypothesized that post-traumatic headache after pediatric traumatic brain injury would be a prevalent morbidity that was associated with neurocognitive impairment regardless of traumatic brain injury severity.
Methods
Participants and Procedures
We conducted a retrospective cohort study of pediatric patients following traumatic brain injury to evaluate post-traumatic headache. The Oregon Health and Science University Institutional Review Board approved the study with a waiver of informed consent (IRB 17497). Consecutive children aged 3–19 years evaluated in the Oregon Health and Science University concussion program or in the pediatric neurocritical care program from March 2015 to January 2018 following a traumatic brain injury were included. Data were collected on the first outpatient visit to the clinics a median of 7 months after injury (interquartile range 3, 17 months).
Demographic information, injury characteristics, past medical histories, and radiology data were extracted from chart review. All severities of traumatic brain injury were included and defined by the Glasgow Coma Scale recorded at the time of injury (mild 13–15, mild complicated 13–15 with identified radiologic abnormality, moderate 9–12, and severe 3–8). Patients with mild traumatic brain injury and no radiologic abnormalities are termed concussion patients. Patients not evaluated at the time of initial injury were recorded as Glasgow Coma Scale score = 15, unless documented otherwise in the medical record. Our institution uses the PECARN guidelines13 when evaluating patients to determine need for head imaging after trauma. Intracranial injury (eg, hematoma or hemorrhage, contusion, axonal injury, edema) and skull fracture were recorded from radiologic data at the time of injury when available to distinguish mild and mild complicated injuries; all patients with moderate or severe traumatic brain injury had identified radiologic abnormalities. Prior head injury was documented from notes. Subconcussive head injury was defined as involvement in sports with potential for contact and in our cohort was was defined as involvement in football or soccer.
Measures
Post-traumatic headache was defined in this study as a self-reported score more than 2 on the Sports Concussion Assessment Tool (SCAT)14–16 for headache and was used to define headache groups for comparison. The SCAT is used routinely in both clinics to screen for traumatic brain injury–related symptoms. The SCAT symptom evaluation utilizes a self-report format to measure symptom severity scored from 0 to 6 on each item. Scores of 1 to 2 indicate mild, 3 to 4 moderate, and 5 to 6 severe symptoms. Patients were excluded from analysis if the SCAT form was missing or incomplete (n = 27/54 pediatric neurocritical care program patients and n = 76/170 concussion program patients).
Neuropsychological assessment is part of routine care in both Oregon Health and Science University programs and is conducted by the same neuropsychology team. We collected standardized scores for all neurocognitive assessments performed and compared between headache groups. Neurocognitive testing in the clinics utilizes a flexible battery approach, with age- and function-appropriate measures, so not all patients receive the same tests. The majority of patients are evaluated with the Delis-Kaplan Executive Function System (D-KEFS) and the Wechsler Abbreviated Scale of Intelligence, Second Edition (WASI-II); thus, we focused our evaluation of neurocognitive outcomes on the subset of patients undergoing these tests (n = 98).17–19 The Delis-Kaplan Executive Function System contains 9 separate tests (with multiple process levels), which measure a variety of different aspects of executive function in children aged ≥8 years. In our cohort, we analyzed data from the Delis-Kaplan Executive Function System verbal fluency test (ie, letter fluency and category fluency), colorword interference test (ie, color naming, word reading, and inhibition speed), and the trail making test (number sequencing, letter sequencing, and letter-number switching). From the WASI-II, we report the vocabulary (assessing verbal comprehension) and matrix reasoning (assessing nonverbal reasoning abilities) subtests in children ≥6 years, as well as the 2-subtest derived (hence abbreviated) Full Scale Intelligence Quotient. Testing was most often performed in clinic visits ≥6 months after injury, particularly for those with moderate or severe head injuries. Most patients without neurocognitive testing reported in the initial clinic visit (n = 23) were <6 months from injury (87%). Given constraints of Delis-Kaplan Executive Function System and WASI-II tests, patients undergoing neurocognitive testing were also older (median 14.8 vs 7.6 years), though testing was performed and reported for 1 patient <6 years of age.
Statistical Analysis
Categorical variables were reported as counts with percentages and continuous variables were reported as medians with interquartile range. Chi-square tests with Fisher exact correction as indicated were used for comparison of categorical variables between headache groups. Mann-Whitney U tests were performed for comparison of continuous variables between headache groups. Statistical analyses were performed using SPSS version 24. Significance was defined as P <.05, and all tests were 2-tailed.
Results
Traumatic Brain Injury Cohort
Following traumatic brain injury, 121 children were evaluated. Median time to outpatient assessment was 7 months after primary injury. Median age overall was 14.3 years, and 51% were male. Most patients (n = 106, 88%) had mild traumatic brain injury as defined by their Glasgow Coma Scale scores. Documented intracranial injury was found in 28 (23%) patients requiring hospitalization at the time of injury. Thirteen (46%) patients with intracranial injury had mild complicated traumatic brain injury. The most common mechanisms of injury included sports-related injury (44%), motor vehicle accidents (18%), and falls (14%). Comorbidities were found in 69 (57%) children in the overall cohort including psychiatric (n = 48, 40%), attention-deficit disorders (n = 21, 17%), and asthma (n = 11, 9%). Prior head injury (n = 49, 40%) and subconcussive injury risk (n = 24, 20%) were common.
Post-traumatic Headache
Headache was reported in 40 (33%) patients presenting for post-traumatic brain injury care. Table 1 presents the demographic characteristics of the traumatic brain injury cohort by headache group. No differences were found in the frequency of headache in the 2 clinics (P = .37). More females and those with Hispanic ethnicity or Medicaid insurance reported headaches, though differences did not reach statistical significance. Prior head injury and subconcussive head injury risk did not increase risk for post-traumatic headache. The frequency of chronic conditions overall was similar between headache groups (P = .39), though pre-existing psychiatric comorbidities were more common in the headache group (50%) versus patients without headache (35%; P = .1).
Table 1.
Demographic and Baseline Characteristics by Headache Group.a
| Headache negative (n = 81) | Headache positive (n = 40) | P value | |
|---|---|---|---|
| Median age in years (IQR) | 14.3 (11.1, 15.9) | 14.8 (11.3, 16) | .74 |
| Male | 44 (54) | 18 (45) | .34 |
| White race | 69 (85) | 30 (75) | .15 |
| Hispanic ethnicity | 9 (11) | 9 (23) | .07 |
| Medicaid insurance | 23 (28) | 17 (43) | .12 |
| Prior head injury | 30 (38) | 19 (48) | .29 |
| Subconcussive injury risk | 14 (17) | 10 (25) | .32 |
| Pre-existing comorbidity | 44 (54) | 25 (63) | .39 |
| Psychiatric | 28 (35) | 20 (50) | |
| Attention deficit | 17 (21) | 4 (10) | |
| Asthma | 6 (7) | 5 (13) | |
| History of special education or IEP | 10 (12) | 4 (10) | .70 |
Abbreviations: IEP, Individualized Education Program; IQR, interquartile range.
Unless otherwise noted, values are n (%).
Table 2 presents injury characteristics by headache group. No difference was found in Glasgow Coma Scale scores between groups, and headache was found in 33 patients with mild traumatic brain injury (35%), 2 with mild complicated traumatic brain injury (15%), 2 with moderate traumatic brain injury (29%), and 3 with severe traumatic brain injury patients (38%). Other injuries, such as extremity fractures, were more frequent in the headache group (23% vs 11%, P = .1). Headache risk was not increased among patients with documented intracranial injury by imaging, but notably some patient characteristics were different between those with intracranial injury versus concussion. Patients with intracranial injury (n = 28 mild complicated, moderate, severe traumatic brain injury) were more likely to present to care in the first 6 months after injury compared to concussion (81% vs 32%, P < .01). Patients with intracranial injury were less likely to have a comorbidity (15% vs 69%, P < .01) or a sports-related injury (11% vs 53%, P < .01).
Table 2.
Injury Characteristics by Headache Group.a
| Headache negative (n = 81) | Headache positive (n=40) | P-value | |
|---|---|---|---|
| Median GCS (IQR) | 15 (15, 15) | 15 (15, 15) | .92 |
| GCS group | .94 | ||
| Mild | 60 (74) | 33 (82) | |
| Mild complicated | 11 (14) | 2 (5) | |
| Moderate | 5 (6) | 2 (5) | |
| Severe | 5 (6) | 3 (8) | |
| Intracranial injury | 21 (26) | 7 (18) | .37 |
| Skull fracture | 12 (15) | 5 (13) | .73 |
| Mechanism of injury | .9 | ||
| Sports injury | 36 (44) | 17 (43) | |
| Motor vehicle accident | 15 (19) | 7 (18) | |
| Fall | 10 (12) | 7 (18) | |
| Otherb | 20 (25) | 9 (23) | |
| Loss of consciousness | 18 (22) | 9 (23) | .90 |
| Other injuriesc | 9 (11) | 9 (23) | .1 |
Abbreviations: GCS, Glasgow Coma Scale; IQR, interquartile range.
Unless otherwise noted, values are n (%).
Other includes: Auto-pedestrian/auto-bicycle, all-terrain vehicle accidents, bike/skateboard/scooter.
Other injuries included bone fractures, pulmonary contusions, liver and splenic lacerations.
Headache and Other Post-traumatic Morbidities
Headache was associated with significantly more subjective complaints of other symptoms after traumatic brain injury, including sleep, mood, sensory, and cognitive disturbances. Table 3 presents total SCAT score and SCAT symptom scores by headache group. Median total SCAT score in the headache group was 5-fold higher compared to patients without headache (median 45.5 [interquartile range 28, 68.5] vs 9 [interquartile range 3, 17]). One-quarter of patients in the headache group reported moderate or severe trouble falling asleep and half reported moderate to severe fatigue or low energy levels, whereas these symptoms were found in <10% of patients without headache. More than 25% of children in the headache group and <5% without headache reported at least moderate or severe sensitivity to light and noise. In regard to mood, 25% of the headache group reported moderate or severe disturbances, including feeling sad or anxious in contrast to <10% in those without headache. Further, moderate to severe difficulties with concentration and remembering were reported in more than 50% of patients with headache and in <10% of those without headache.
Table 3.
SCAT Scores by Headache Group.
| Headache negative, median (IQR) (n = 81) | Headache positive, median (IQR) (n = 40) | P value | |
|---|---|---|---|
| SCAT Total Score | 9 (3, 17) | 45.5 (28, 68.5) | <.001 |
| Symptom | |||
| Pressure in head | 0 (0, 1) | 2 (0, 3) | <.001 |
| Neck pain | 0 (0, 1) | 1 (0, 2.75) | .002 |
| Balance problems or dizzy | 0 (0, 0) | 1 (0, 2) | <.001 |
| Nausea/vomiting | 0 (0, 0) | 0 (0, 1) | <.001 |
| Vision problems | 0 (0, 0) | 1 (0, 3) | <.001 |
| Hearing problems | 0 (0, 0) | 0 (0, 2.75) | .009 |
| Do not feel right | 0 (0, 0) | 2.5 (1, 4) | <.001 |
| Feeling dinged | 0 (0, 0) | 1.5 (0, 3) | <.001 |
| Confusion | 0 (0, 0) | 1 (0, 3) | <.001 |
| Feeling slowed down | 0 (0, 1) | 1.5 (0, 3.75) | <.001 |
| Feeling in a fog | 0 (0, 0) | 2 (0, 3) | <.001 |
| Drowsiness | 0 (0, 1) | 2 (0, 4) | <.001 |
| Fatigue or low energy | 0 (0, 2) | 3 (1, 4.75) | <.001 |
| More emotional | 0 (0, 1) | 2 (0, 4) | <.001 |
| Irritable | 0 (0, 2) | 3 (0, 4) | <.001 |
| Difficulty concentrating | 0 (0, 1) | 3 (1, 4) | <.001 |
| Difficult remembering | 0 (0, 2) | 3 (1, 4.75) | <.001 |
| Sadness | 0 (0, 0) | 1 (0, 3) | <.001 |
| Nervous or anxious | 0 (0, 1) | 2 (0, 3.75) | <.001 |
| Trouble falling asleep | 0 (0, 1) | 2 (0, 4) | .001 |
| Sleeping more than usual | 0 (0, 1) | 0 (0, 3) | .015 |
| Sensitivity to light | 0 (0, 0) | 2 (0, 3) | <.001 |
| Sensitivity to noise | 0 (0, 0) | 2 (0, 4) | <.001 |
Abbreviations: IQR, interquartile range; SCAT, Sports Concussion Assessment Tool.
Objective neurocognitive testing broadly examining the cognitive domains of language, processing speed, intelligence, learned knowledge/memory, and executive function was performed on a subset of patients (n = 98; see Supplemental Table 1 for subgroup characteristics by headache group). Patients with headache had lower standardized scores in all neurocognitive tests, and statistically significant differences were found in some subdomains of the Delis-Kaplan Executive Function System and WASI-II batteries (Table 4). Median FSIQ score in the headache group (105; interquartile range 95, 117) was significantly below that of the patients without headache (117; interquartile range 104, 125; P < .01), as well as a similar pattern of significant group differences on the verbal (ie, vocabulary) and nonverbal (ie, matrix-reasoning) subtests that comprise the overall intelligence estimate (see Table 4). Significantly lower scaled scores regarding the Delis-Kaplan Executive Function System conditions of color naming, letter sequencing, and number-letter switching were also found in the headache group (all P ≤ .04) reflecting significant differences in processing speed and executive function between headache groups.
Table 4.
Neurocognitive Scaled Scores by Headache Group.
| Headache negative | Headache positive | ||||
|---|---|---|---|---|---|
| Neurocognitive test | Median score (IQR) | n (%) | Median score (IQR) | n (%) | P value |
| Color Namingb (n = 89) | 10.0 (8.0, 11.8) | 57 (64%) | 8.0 (6.0, 10.0) | 32 (36%) | .03 |
| Inhibition Speedb, d (n = 89) | 10.0 (7.3, 11.0) | 57 (64%) | 10.0 (7.0, 11.0) | 32 (36%) | .22 |
| Number Sequencingb (n = 95) | 10.5 (9.0, 13.0) | 62 (65%) | 10.0 (8.0, 12.0) | 33 (35%) | .14 |
| Letter Sequencingb (n = 95) | 12.0 (10.0, 13.0) | 62 (65%) | 10.0 (8.0, 12.0) | 33 (35%) | <.01 |
| Number-Letter Switchingb,d (n = 93) | 11.0 (9.0, 12.0) | 61 (66%) | 9.0 (7.0, 11.0) | 32 (34%) | .04 |
| Word Readinge (n = 89) | 11.0 (9.0, 12.0) | 57 (64%) | 9.0 (7.0, 11.0) | 32 (36%) | .1 |
| Full Scale IQc (n = 81) | 117.0 (104.3, 124.5) | 52 (64%) | 105.0 (95.0, 116.50) | 29 (36%) | <.01 |
| Matrix Reasoningc,d T-Score (n = 86) | 58.0 (53.3, 63.0) | 57 (66%) | 53.0 (47.50, 58.50) | 29 (33%) | .03 |
| Vocabularyc T-Score (n = 84) | 59.5 (51.5, 67.5) | 56 (67%) | 54.5 (47.5, 61) | 28 (33%) | .02 |
Abbreviations: IQ, intelligence quotient; IQR, interquartile range.
Testing Domains: (a = language, b = processing speed, c = intelligence, d = executive function, e = learned knowledge/memory).
Discussion
We found post-traumatic headache to be a prevalent morbidity in children who present for post-traumatic brain injury care, regardless of severity and characteristics of injury. In our study, post-traumatic headaches were found in one-third of patients at a median of 7 months after injury. Youth with post-traumatic headache also reported significantly more dysfunction with sleep, mood, sensory, and cognitive disturbances. Self-reported headache was associated with objectively worse neurocognitive function, particularly for tasks that tax processing speed abilities (see Table 4). Post-traumatic headache represents an important morbidity in pediatric traumatic brain injury patients that may compound other morbidities, offer a therapeutic target for other post-traumatic symptoms, and identify patients in need of formal neurocognitive testing.
Previous studies in adults and pediatrics have shown prevalence of post-traumatic headache to be anywhere from 9% to 44% at 3 months, 20% to 44% at 6 months, and 20% to 23% at 12 months, but have all used different methods for identifying headaches and ranges of time from injury.20–23 The largest study evaluating pediatric post-traumatic headache to date used a similar dichotomization of a single question to define headache and found a similar prevalence of headache, 42% at 3 months postinjury, and persistence of headache 12 months after injury.5 Our study adds to this literature showing a high prevalence and persistence of post-traumatic headache in the pediatric traumatic brain injury population. One-quarter of our patients with headache complained of moderate to severe sensitivity to light and noise, consistent with migraine headache features. Moderate to severe neck pain and pressure were also present in almost 25% of headache patients, consistent with tension headaches. Headache phenotypes are poorly defined in pediatric traumatic brain injury literature, though prior studies suggest migraine and tension are most common and consistent with our findings.21
Prior studies have identified several risk factors for post-traumatic headache, though findings are often inconsistent between studies.21 Females were more likely to endorse headache symptoms in prior studies,5,20,24,25 and older age has been associated with an elevated risk for post-traumatic headache.5,26 Our study did not find any statistically significant differences in risk for headache among the demographic and injury characteristics we evaluated. A recent systematic review of recovery after concussion noted inconsistencies when evaluating risk factors, and these differences may be due to variability in patient populations, definitions of headache, and variable time to evaluation after traumatic brain injury.27
Pre-existing conditions were found in more than half of the patients in our study, though no difference was found between headache groups. The most common comorbidities in our cohort included psychiatric, attention-deficit hyperactivity disorders (ADHD), and asthma. Previous studies in pediatric traumatic brain injury evaluating outcomes like neurocognitive function, sleep disturbances, and psychological disturbances have shown premorbid status to be a key risk factor determining outcome. A prior study in children evaluating post-traumatic headache found 51% had pre-existing headaches, 31% had migraine/probably migraine preinjury, and 56% had a family history of migraine.28 Preinjury parental factors were also associated with greater rates of post-traumatic headache in prior studies.26,29 We were unable to systematically assess pre-existing headache or family history with our study, and this may account for differences from prior studies.27 Further research is needed to determine if pre-existing comorbidities are driving the high prevalence of headaches found after pediatric traumatic brain injury to inform future intervention studies.
We did not find a difference in post-traumatic headache based on severity of primary traumatic brain injury measured by Glasgow Coma Scale, though patients with concussion versus intracranial injury had important differences, such as time to evaluation, frequency of pre-existing conditions, and mechanism of injury that may confound the association between headache and injury severity. Regardless of headache status, patients were more likely to present to care early after traumatic brain injury with the presence of radiographic intracranial injury versus concussion. Patients with concussion may present later to specialized care after referral from primary providers or related to persistence of symptoms, whereas patients with intracranial injury may present earlier because of presence of symptoms or direct referrals after hospitalization. Early intervention regardless of injury severity may prevent the evolution of secondary or tertiary injury factors that contribute to headache status. Although comorbidities were found in more than half of all patients, comorbidities were far less likely in patients with identifiable intracranial injury versus concussion. Mechanisms of injury also varied by the presence of intracranial injury, with sports-related injuries being more common in patients with concussion. Most studies to date have included only concussion patients or have stratified patients only by Glasgow Coma Scale scores.7 Although the presence of intracranial injury compared to concussion alone was not associated with increased risk of post-traumatic headache in our study, the differences in demographic characteristics between these 2 groups is an important consideration in future studies evaluating risk factors for post-traumatic headache.
Post-traumatic headache was associated with higher symptom scores in all other domains of the SCAT. It is unclear if headache drives development of other symptoms or is reflective of a common pathophysiology driving the development of all post-traumatic morbidities. Prior studies similarly show that these symptoms are highly inter-related and that headache may be a risk factor for persistence of postconcussive symptoms.27 One study in adult traumatic brain injury showed there was a relationship between headache, sleep problems, psychiatric symptoms, and dizziness on SCAT measures.30 Another study in adult patients with traumatic brain injury similarly showed that patients with post-traumatic headache had higher total symptom severity scores than the nonheadache group.31 Sleep, mood, and sensory disturbances after traumatic brain injury are all known morbidities, but it is unclear how headache impacts these symptoms in children. Headache may cause difficulty falling asleep, but sleep disturbances have also been associated with headache.32–34 Similarly, headache may cause anxiety or depressed mood by impairing quality of life or social function, but headache is also a known morbidity among patients with psychological disorders.35,36 Alternatively, traumatic brain injury, both through direct brain injury or secondary injury processes like inflammation, may be driving the development and persistence of all of the symptoms evaluated by SCAT, including headache. More research is needed to evaluate the relationship between headache and other post-traumatic symptoms to determine if treating headaches can improve other symptoms and lower the risk for persistence of postconcussive symptoms, or if targeting symptoms like sleep disturbances can improve headaches after traumatic brain injury.
Headache may be an important predictor of neurocognitive deficits after traumatic brain injury. Prior research on neurocognitive outcomes in pediatric traumatic brain injury have shown that young age at injury, lower premorbid developmental and academic achievement, and severity of injury increase risk of cognitive deficits, but have not evaluated headaches as a risk factor.37–41 We demonstrated that patients with headache had lowered neurocognitive performance among all of the commonly employed neuropsychological tests in our clinic, particularly in measures that tax processing speed abilities, but also subtests that have the highest factor loadings for overall intelligence estimates (ie, Full Scale Intelligence Quotient). The former finding is consistent with prior work,42 yet meta-analytic findings regarding intelligence after traumatic brain injury have demonstrated that Full Scale Intelligence Quotient impairments were absent for mild traumatic brain injury (compared to moderate/severe traumatic brain injury) in the subacute recovery phase, and only small intelligence impairments have been noted in the chronic recovery phase for mild traumatic brain injury. Further, adults with traumatic brain injury in the chronic recovery phase had larger intelligence differences than children who had sustained traumatic brain injury.43 Considering these meta-analytic findings, current significant differences in Full Scale Intelligence Quotient found between the headache and nonheadache group may reflect preinjury patient characteristics, including coping skills, which may mediate recovery from traumatic brain injury and reflect overall better health.27,44,45 In our study, the number of patients with a history of special education or individualized education programs was not statistically different between headache groups, but a comprehensive evaluation of premorbid status was not possible. Further, the possibility of preinjury population differences in cognitive performance underscores the importance of early evaluation to avoid the “good old days bias,”46 and early intervention to improve the trajectory of recovery. It is also possible that differences in cognitive performance between headache groups represent differences in severity of primary injury not captured by measures like Glasgow Coma Scale, ongoing secondary processes like inflammation, or are due to other post-traumatic symptom–related impairments in test performances.
Pain, including headache, may be particularly important in evaluations of neurocognitive outcomes in children with brain injury. Chronic pain and headaches outside of traumatic brain injury have been shown to reduce school performance and attendance, increase psychosocial comorbidities, and impair cognition.47–49 Additionally, avoidance of mental exertion following traumatic brain injury as it relates to headache has been shown to lower cognitive testing scores.50 Measures taxing processing speed abilities were particularly impaired with headache in our study and may reflect the effects of active pain during testing or avoidance of mental exertion as a perceived trigger. However, the global differences in cognitive performance between headache groups we found (considering trends toward significance in addition to significant group differences) suggests that headache may identify a group of patients at risk for post-traumatic cognitive impairment. Access to Pediatric Neuropsychology expertise is limited and often not provided as part of routine post-traumatic brain injury care, making screening tools valuable for clinicians to ensure high-risk patients access these services.51 This study provides preliminary evidence that the presence of headache, defined by SCAT score, may indicate which patients need specialized neurocognitive testing. Given the impact of neurocognitive deficits on learning and development in children, the relationship between post-traumatic headache and neurocognitive outcomes should be investigated because treatment for headaches could lead to improved cognitive performance after traumatic brain injury.
This study has limitations to consider including the retrospective design, use of SCAT to define headache, and use of a clinical sample from clinics providing post-traumatic brain injury care. The International Classification of Headache Disorders III-beta defines post-traumatic headache as onset of headache within 7 days of injury, but given the retrospective design of our study, timing of onset cannot be ensured.52 Additionally, SCAT data were missing or incomplete in the medical record for some patients evaluated after traumatic brain injury, which could contribute to selection bias. Further, although the original version of SCAT was not validated in pediatric patients, the child SCAT3 and SCAT3 have been validated in children aged 5–16 years and in non–sports injury concussions.53 The portion of the SCAT used in this study was limited to the symptom evaluation portion of the SCAT, which is very similar to that of the SCAT3. We chose to use SCAT scores given its widespread use, free availability to clinicians, and ease of administration.54 There are few headache-specific questionnaires available that have been validated in children or employed in pediatric traumatic brain injury populations. Our clinical sample may select patients with more post-traumatic symptoms overall as patients with milder or no symptoms may not complete a clinic visit. Although our clinics routinely assess some important comorbidities, preinjury headaches or family history of headache is not systematically assessed, which may be important when assessing risk of headache after traumatic brain injury in future work. Because of the retrospective nature of our study, preinjury cognitive testing scores were not obtained for comparison. Additionally, our study had a wide range of time to assessment, which likely affects our estimates of prevalence and risk factors. Our sample size was small, limiting our ability to detect potential differences between headache groups in some variables or to conduct rigorous multivariable adjustment when assessing risk for post-traumatic headache and the association between headache and neurocognitive outcomes. Nonetheless, our results show post-traumatic headache is an important morbidity that may be a useful predictor of important neurocognitive deficits requiring further research.
Conclusion
Post-traumatic headache is an important and persistent morbidity in pediatric traumatic brain injury patients, regardless of primary injury severity. Our study shows that headache, as reported by patients on the SCAT, is associated with higher symptom scores in all other post-traumatic symptom domains including sleep, mood, sensory, and cognitive. Headache was also associated with worse objective neurocognitive measures and may identify patients who could benefit from comprehensive cognitive evaluations. More studies are needed to define post-traumatic headache phenotype, determine effective headache interventions, and determine the impact of headache treatments on recovery from the multidimensional sequelae of pediatric traumatic brain injury.
Supplementary Material
Acknowledgments
Funding
The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: Dr Williams is supported by the Agency for Healthcare Research and Quality, grant number K12HS022981. The content is solely the responsibility of the authors and does not necessarily represent the official views of the Agency for Healthcare Research and Quality. Dr Piantino is supported by the National Heart, Lung, and Blood Institute grant number K12HL133115.
Footnotes
Supplemental Material
Supplemental material for this article is available online.
Declaration of Conflicting Interests
The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
References
- 1.Faul M, Xu L, Wald M, Coronado VG. Traumatic brain injury in the United States: emergency department visits, hospitalizations and deaths 2002–2006. Atlanta (GA): Centers for Disease Control and Prevention, National Center for Injury Prevention and Control; 2010. [Google Scholar]
- 2.Williams CN, Piantino J, McEvoy C, Fino N, Eriksson CO. The burden of pediatric neurocritical care in the United States. Pediatr Neurol. 2018;89:31–38. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Coronado VG, Haileyesus T, Cheng TA, et al. Trends in sports-and recreation-related traumatic brain injuries treated in US emergency departments: The National Electronic Injury Surveillance System–All Injury Program (NEISS-AIP) 2001–2012. J Head Trauma Rehabil. 2015;30(3):185–197. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Babikian T, Merkley T, Savage RC, Giza CC, Levin H. Chronic aspects of pediatric traumatic brain injury: review of the literature. J Neurotrauma. 2015;32(23):1849–1860. [DOI] [PubMed] [Google Scholar]
- 5.Blume HK, Vavilala MS, Jaffe KM, et al. Headache after pediatric traumatic brain injury: a cohort study. Pediatrics. 2012; 129(1):e31–39. [DOI] [PubMed] [Google Scholar]
- 6.Powers SW, Patton SR, Hommel KA, Hershey AD. Quality of life in childhood migraines: clinical impact and comparison to other chronic illnesses. Pediatrics. 2003;112(1, pt 1):e1–e5. [DOI] [PubMed] [Google Scholar]
- 7.Babikian T, Asarnow R. Neurocognitive outcomes and recovery after pediatric TBI: meta-analytic review of the literature. Neuropsychology. 2009;23(3):283–296. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Catroppa C, Anderson VA, Morse SA, Haritou F, Rosenfeld JV. Children’s attentional skills 5 years post-TBI. J Pediatr Psychol. 2007;32(3):354–369. [DOI] [PubMed] [Google Scholar]
- 9.Pinchefsky E, Dubrovsky AS, Friedman D, Shevell M. Part I—evaluation of pediatric post-traumatic headaches. Pediatr Neurol. 2015;52(3):263–269. [DOI] [PubMed] [Google Scholar]
- 10.Pinchefsky E, Dubrovsky AS, Friedman D, Shevell M. Part II—management of pediatric post-traumatic headaches. Pediatr Neurol. 2015;52(3):270–280. [DOI] [PubMed] [Google Scholar]
- 11.Gera G, Chesnutt J, Mancini M, Horak FB, King LA. Inertial sensor-based assessment of central sensory integration for balance after mild traumatic brain injury. Mil Med. 2018;183(suppl 1): 327–332. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Williams CN, Kirby A, Piantino J. If you build it, they will come: initial experience with a multi-disciplinary pediatric neurocritical care follow-up clinic. Children (Basel, Switzerland). 2017;4(9). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Kuppermann N, Holmes JF, Dayan PS, et al. Identification of children at very low risk of clinically-important brain injuries after head trauma: a prospective cohort study. Lancet (London, England). 2009;374(9696):1160–1170. [DOI] [PubMed] [Google Scholar]
- 14.McCrory P, Johnston K, Meeuwisse W, et al. Summary and agreement statement of the second international conference on concussion in sport, Prague 2004. Phys Sportsmed. 2005;33(4): 29–44. [DOI] [PubMed] [Google Scholar]
- 15.Schneider KJ, Emery CA, Kang J, Schneider GM, Meeuwisse WH. Examining Sport Concussion Assessment Tool ratings for male and female youth hockey players with and without a history of concussion. Br J Sports Med. 2010;44(15):1112–1117. [DOI] [PubMed] [Google Scholar]
- 16.Shehata N, Wiley JP, Richea S, Benson BW, Duits L, Meeuwisse WH. Sport concussion assessment tool: baseline values for varsity collision sport athletes. Br J Sports Med. 2009;43(10): 730–734. [DOI] [PubMed] [Google Scholar]
- 17.Cahill C A compendium of neuropsychological tests (3rd edition). Acta Neuropsychiatrica. 2007;19(3):219–219. [Google Scholar]
- 18.Canivez GL, Konold TR, Collins JM, Wilson G. Construct validity of the Wechsler Abbreviated Scale of Intelligence and Wide Range Intelligence Test: convergent and structural validity. School Psychol Q. 2009;24(4):252. [Google Scholar]
- 19.Delis DC, Kramer JH, Kaplan E, Holdnack J. Reliability and validity of the Delis-Kaplan Executive Function System: an update. J Int Neuropsychol Soc. 2004;10(2):301–303. [DOI] [PubMed] [Google Scholar]
- 20.Hoffman JM, Lucas S, Dikmen S, et al. Natural history of headache after traumatic brain injury. J Neurotrauma. 2011;28(9): 1719–1725. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Kacperski J, Hung R, Blume HK. Pediatric posttraumatic headache. Semin Pediatr Neurol. 2016;23(1):27–34. [DOI] [PubMed] [Google Scholar]
- 22.Kirk C, Nagiub G, Abu-Arafeh I. Chronic post-traumatic headache after head injury in children and adolescents. Dev Med Child Neurol. 2008;50(6):422–425. [DOI] [PubMed] [Google Scholar]
- 23.Walker WC, Seel RT, Curtiss G, Warden DL. Headache after moderate and severe traumatic brain injury: a longitudinal analysis. Arch Phys Med Rehabil. 2005;86(9):1793–1800. [DOI] [PubMed] [Google Scholar]
- 24.Bernard CO, Ponsford JA, McKinlay A, McKenzie D, Krieser D. Predictors of post-concussive symptoms in young children: injury versus non-injury related factors. J Int Neuropsychol Soc. 2016; 22(8):793–803. [DOI] [PubMed] [Google Scholar]
- 25.Berz K, Divine J, Foss KB, Heyl R, Ford KR, Myer GD. Sex-specific differences in the severity of symptoms and recovery rate following sports-related concussion in young athletes. Phys Sportsmed. 2013;41(2):58–63. [DOI] [PubMed] [Google Scholar]
- 26.Eisenberg MA, Andrea J, Meehan W, Mannix R. Time interval between concussions and symptom duration. Pediatrics. 2013; 132(1):8–17. [DOI] [PubMed] [Google Scholar]
- 27.Iverson GL, Gardner AJ, Terry DP, et al. Predictors of clinical recovery from concussion: a systematic review. Br J Sports Med. 2017;51(12):941–948. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Kuczynski A, Crawford S, Bodell L, Dewey D, Barlow KM. Characteristics of post-traumatic headaches in children following mild traumatic brain injury and their response to treatment: a prospective cohort. Dev Med Child Neurol. 2013;55(7):636–641. [DOI] [PubMed] [Google Scholar]
- 29.lsson KA, Lloyd OT, Lebrocque RM, McKinlay L, Anderson VA, Kenardy JA. Predictors of child post-concussion symptoms at 6 and 18 months following mild traumatic brain injury. Brain Inj. 2013;27(2):145–157. [DOI] [PubMed] [Google Scholar]
- 30.Tkachenko N, Singh K, Hasanaj L, Serrano L, Kothare SV. Sleep disorders associated with mild traumatic brain injury using sport concussion assessment tool 3. Pediatr Neurol. 2016;57:46–50.e41. [DOI] [PubMed] [Google Scholar]
- 31.Begasse de Dhaem O, Barr WB, Balcer LJ, Galetta SL, Minen MT. Post-traumatic headache: the use of the Sport Concussion Assessment Tool (SCAT-3) as a predictor of post-concussion recovery. J Headache Pain. 2017;18(1):60. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.Bruni O, Russo PM, Ferri R, Novelli L, Galli F, Guidetti V. Relationships between headache and sleep in a non-clinical population of children and adolescents. Sleep Med. 2008;9(5): 542–548. [DOI] [PubMed] [Google Scholar]
- 33.Dosi C, Figura M, Ferri R, Bruni O. Sleep and headache. Seminars in Pediatr Neurol. 2015;22(2):105–112. [DOI] [PubMed] [Google Scholar]
- 34.Holland PR. Headache and sleep: shared pathophysiological mechanisms. Cephalalgia. 2014;34(10):725–744. [DOI] [PubMed] [Google Scholar]
- 35.Kutuk MO, Tufan AE, Guler G, et al. Migraine and associated comorbidities are three times more frequent in children with ADHD and their mothers. Brain Dev. 2018;40:857–864. [DOI] [PubMed] [Google Scholar]
- 36.Torres-Ferrus M, Vila-Sala C, Quintana M, et al. Headache, comorbidities and lifestyle in an adolescent population (The TEENs Study). Cephalalgia. 2019;39(1):91–99. [DOI] [PubMed] [Google Scholar]
- 37.Anderson V, Catroppa C, Morse S, Haritou F, Rosenfeld J. Functional plasticity or vulnerability after early brain injury? Pediatrics. 2005;116(6):1374–1382. [DOI] [PubMed] [Google Scholar]
- 38.Anderson VA, Morse SA, Catroppa C, Haritou F, Rosenfeld JV. Thirty month outcome from early childhood head injury: a prospective analysis of neurobehavioural recovery. Brain. 2004; 127(pt 12):2608–2620. [DOI] [PubMed] [Google Scholar]
- 39.Ewing-Cobbs L, Barnes M, Fletcher JM, Levin HS, Swank PR, Song J. Modeling of longitudinal academic achievement scores after pediatric traumatic brain injury. Dev Neuropsychol. 2004; 25(1–2):107–133. [DOI] [PubMed] [Google Scholar]
- 40.Schachar R, Levin HS, Max JE, Purvis K, Chen S. Attention deficit hyperactivity disorder symptoms and response inhibition after closed head injury in children: do preinjury behavior and injury severity predict outcome? Dev Neuropsychol. 2004;25(1–2):179–198. [DOI] [PubMed] [Google Scholar]
- 41.Taylor HG, Yeates KO, Wade SL, Drotar D, Stancin T, Minich N. A prospective study of short- and long-term outcomes after traumatic brain injury in children: behavior and achievement. Neuropsychology. 2002;16(1):15–27. [DOI] [PubMed] [Google Scholar]
- 42.Karr JE, Areshenkoff CN, Garcia-Barrera MA. The neuropsychological outcomes of concussion: a systematic review of meta-analyses on the cognitive sequelae of mild traumatic brain injury. Neuropsychology. 2014;28(3):321–336. [DOI] [PubMed] [Google Scholar]
- 43.Konigs M, Engenhorst PJ, Oosterlaan J. Intelligence after traumatic brain injury: meta-analysis of outcomes and prognosis. Eur J Neurol. 2016;23(1):21–29. [DOI] [PubMed] [Google Scholar]
- 44.Kanazawa S Mind the gap . . . in intelligence: re-examining the relationship between inequality and health. Br J Health Psychol. 2006;11(pt 4):623–642. [DOI] [PubMed] [Google Scholar]
- 45.McNally KA, Bangert B, Dietrich A, et al. Injury versus noninjury factors as predictors of postconcussive symptoms following mild traumatic brain injury in children. Neuropsychology. 2013;27(1): 1–12. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 46.Brooks BL, Kadoura B, Turley B, Crawford S, Mikrogianakis A, Barlow KM. Perception of recovery after pediatric mild traumatic brain injury is influenced by the “good old days” bias: tangible implications for clinical practice and outcomes research. Arch Clin Neuropsychol. 2014;29(2):186–193. [DOI] [PubMed] [Google Scholar]
- 47.de Araújo CM, Barbosa IG, Lemos SMA, Domingues RB, Teixeira AL. Cognitive impairment in migraine: a systematic review. Dement Neuropsychol. 2012;6(2):74–79. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 48.Slover R, Neuenkirchen GL, Olamikan S, Kent S. Chronic pediatric pain. Adv Pediatr. 2010;57(1):141–162. [DOI] [PubMed] [Google Scholar]
- 49.Smith AP. Acute tension-type headaches are associated with impaired cognitive function and more negative mood. Front Neurol. 2016;7:42. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 50.Silverberg ND, Iverson GL, Panenka W. Cogniphobia in mild traumatic brain injury. J Neurotrauma. 2017;34(13):2141–2146. [DOI] [PubMed] [Google Scholar]
- 51.Dodd J, Hall T, Guilliams K, et al. Optimizing neurocritical care through the integration of neuropyschology. Pediatric Neurol. 2018;89:58–62. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 52.The International Classification of Headache Disorders, 3rd edition (beta version). Cephalalgia. 2013;33(9):629–808. [DOI] [PubMed] [Google Scholar]
- 53.Babl FE, Dionisio D, Davenport L, et al. Accuracy of components of SCAT to identify children with concussion. Pediatrics. 2017; 140(2). [DOI] [PubMed] [Google Scholar]
- 54.McCrory P, Meeuwisse W, Aubry M, et al. Consensus statement on concussion in sport—The 4th International Conference on Concussion in Sport held in Zurich, November 2012. Phys Ther Sport. 2013;14(2):e1–e13. [DOI] [PubMed] [Google Scholar]
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