Psychiatric outcomes after pediatric sports-related concussion

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  • 1 Departments of Surgery,
  • | 2 Pediatrics and Child Health,
  • | 3 Clinical Health Psychology, and
  • | 4 Psychiatry, and
  • | 5 Section of Neurosurgery, University of Manitoba;
  • | 6 Pan Am Concussion Program;
  • | 7 Childrens Hospital Research Institute of Manitoba; and
  • | 8 Canada North Concussion Network, Winnipeg, Manitoba, Canada
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OBJECT

The objectives of this study were twofold: 1) to examine the prevalence of emotional symptoms among children and adolescents with a sports-related concussion (SRC) who were referred to a multidisciplinary pediatric concussion program and 2) to examine the prevalence, clinical features, risk factors, and management of postinjury psychiatric outcomes among those in this clinical population.

METHODS

The authors conducted a retrospective chart review of all patients with SRC referred to a multidisciplinary pediatric concussion program between September 2013 and October 2014. Clinical assessments carried out by a single neurosurgeon included clinical history, physical examination, and Post-Concussion Symptom Scale (PCSS) scoring. Postinjury psychiatric outcomes were defined as a subjective worsening of symptoms of a preinjury psychiatric disorder or new and isolated suicidal ideation or diagnosis of a novel psychiatric disorder (NPD). An NPD was defined as a newly diagnosed psychiatric disorder that occurred in a patient with or without a lifetime preinjury psychiatric disorder after a concussion. Clinical resources, therapeutic interventions, and clinical and return-to-play outcomes are summarized.

RESULTS

One hundred seventy-four patients (mean age 14.2 years, 61.5% male) were included in the study. At least 1 emotional symptom was reported in 49.4% of the patients, and the median emotional PCSS subscore was 4 (interquartile range 1–8) among those who reported at least 1 emotional symptom. Overall, 20 (11.5%) of the patients met the study criteria for a postinjury psychiatric outcome, including 14 patients with an NPD, 2 patients with isolated suicidal ideation, and 4 patients with worsening symptoms of a preinjury psychiatric disorder. Female sex, a higher initial PCSS score, a higher emotional PCSS subscore, presence of a preinjury psychiatric history, and presence of a family history of psychiatric illness were significantly associated with postinjury psychiatric outcomes. Interventions for patients with postinjury psychiatric outcomes included pharmacological therapy alone in 2 patients (10%), cognitive behavioral therapy alone in 4 (20%), multimodal therapy in 9 (45%), and no treatment in 5 (25%). Overall, 5 (25%) of the patients with postinjury psychiatric disorders were medically cleared to return to full sports participation, whereas 5 (25%) were lost to follow-up and 9 (45%) remained in treatment by the multidisciplinary concussion program at the end of the study period. One patient who was asymptomatic at the time of initial consultation committed suicide.

CONCLUSIONS

Emotional symptoms were commonly reported among pediatric patients with SRC referred to a multidisciplinary pediatric concussion program. In some cases, these symptoms contributed to the development of an NPD, isolated suicidal ideation, and worsening symptoms of a preexisting psychiatric disorder. Future research is needed to clarify the prevalence, pathophysiology, risk factors, and evidence-based management of postinjury psychiatric outcomes after pediatric SRC. Successful management of these patients requires prompt recognition and multidisciplinary care by experts with clinical training and experience in concussion and psychiatry.

ABBREVIATIONS

ADHD = attention-deficit hyperactivity disorder; ICD-10 = International Classification of Diseases, 10th Revision; IQR = interquartile range; NOS = not otherwise specified; NPD = novel psychiatric disorder; OCD = obsessive-compulsive disorder; PCS = postconcussion syndrome; PCSS = Post-Concussion Symptom Scale; SRC = sports-related concussion; TBI = traumatic brain injury.

OBJECT

The objectives of this study were twofold: 1) to examine the prevalence of emotional symptoms among children and adolescents with a sports-related concussion (SRC) who were referred to a multidisciplinary pediatric concussion program and 2) to examine the prevalence, clinical features, risk factors, and management of postinjury psychiatric outcomes among those in this clinical population.

METHODS

The authors conducted a retrospective chart review of all patients with SRC referred to a multidisciplinary pediatric concussion program between September 2013 and October 2014. Clinical assessments carried out by a single neurosurgeon included clinical history, physical examination, and Post-Concussion Symptom Scale (PCSS) scoring. Postinjury psychiatric outcomes were defined as a subjective worsening of symptoms of a preinjury psychiatric disorder or new and isolated suicidal ideation or diagnosis of a novel psychiatric disorder (NPD). An NPD was defined as a newly diagnosed psychiatric disorder that occurred in a patient with or without a lifetime preinjury psychiatric disorder after a concussion. Clinical resources, therapeutic interventions, and clinical and return-to-play outcomes are summarized.

RESULTS

One hundred seventy-four patients (mean age 14.2 years, 61.5% male) were included in the study. At least 1 emotional symptom was reported in 49.4% of the patients, and the median emotional PCSS subscore was 4 (interquartile range 1–8) among those who reported at least 1 emotional symptom. Overall, 20 (11.5%) of the patients met the study criteria for a postinjury psychiatric outcome, including 14 patients with an NPD, 2 patients with isolated suicidal ideation, and 4 patients with worsening symptoms of a preinjury psychiatric disorder. Female sex, a higher initial PCSS score, a higher emotional PCSS subscore, presence of a preinjury psychiatric history, and presence of a family history of psychiatric illness were significantly associated with postinjury psychiatric outcomes. Interventions for patients with postinjury psychiatric outcomes included pharmacological therapy alone in 2 patients (10%), cognitive behavioral therapy alone in 4 (20%), multimodal therapy in 9 (45%), and no treatment in 5 (25%). Overall, 5 (25%) of the patients with postinjury psychiatric disorders were medically cleared to return to full sports participation, whereas 5 (25%) were lost to follow-up and 9 (45%) remained in treatment by the multidisciplinary concussion program at the end of the study period. One patient who was asymptomatic at the time of initial consultation committed suicide.

CONCLUSIONS

Emotional symptoms were commonly reported among pediatric patients with SRC referred to a multidisciplinary pediatric concussion program. In some cases, these symptoms contributed to the development of an NPD, isolated suicidal ideation, and worsening symptoms of a preexisting psychiatric disorder. Future research is needed to clarify the prevalence, pathophysiology, risk factors, and evidence-based management of postinjury psychiatric outcomes after pediatric SRC. Successful management of these patients requires prompt recognition and multidisciplinary care by experts with clinical training and experience in concussion and psychiatry.

Sports-related concussion (SRC) is a form of traumatic brain injury (TBI) that affects thousands of children and adolescents annually in Canada and the United States.42,51 The clinical presentation of pediatric SRC is highly individualized and often manifests as a combination of physical, cognitive, sleep, and emotional symptoms. Although many pediatric patients will recover to their neurological baseline within 1–4 weeks with an appropriate amount of physical and cognitive rest, 21%–73% of patients will experience symptoms that last longer than 1 month and will be diagnosed with postconcussion syndrome (PCS).1,2,5,6,11

Although the impact of pediatric SRC on physical and cognitive functioning has been well documented in previous clinical research studies,1,2,5–7,11,37,56 there has been little attention paid to the emotional and psychiatric manifestations of this condition. Previous studies have observed novel psychiatric disorders (NPDs) occurring in 10%–100% of children and adolescents with TBI of various severities, including personality changes, attention-deficit hyperactivity disorder (ADHD), behavioral disorders, depression, and anxiety disorders.4,21,22,26–28,30,31,33–36,49 Children and adolescents with psychiatric disorders are at risk for additional long-term comorbidities such as impaired school performance,9 social isolation,48 family dysfunction,55 substance abuse,45 and suicidal behavior.19 Successful management of isolated pediatric mood disorders requires a multidisciplinary approach that includes behavioral and pharmacological treatment options. Treatment of an NPD after TBI is more challenging and requires close collaboration between physicians with specialized clinical training and experience in TBI and psychiatry.22 Despite increased media and research attention surrounding the relationship between SRC, mood disorders, and suicide in professional athletes,12,14,15,17,40,46,50,52 there have been no clinical studies to examine postinjury psychiatric outcomes among an exclusive cohort of pediatric patients with SRC.

Accordingly, the aim of this study was twofold: 1) to examine the prevalence of emotional symptoms at initial consultation among children and adolescents with SRC who were referred to a multidisciplinary pediatric concussion program and 2) to examine the prevalence, clinical features, risk factors, and management of postinjury psychiatric disorders among those in this clinical population.

Methods

Research Design and Inclusion Criteria

A retrospective chart review was performed for all consecutive pediatric patients (aged 19 years or younger) referred to the Pan Am Concussion Program in Winnipeg, Manitoba, Canada, between September 1, 2013, and October 1, 2014. Patients referred with physician-diagnosed acute SRC or PCS secondary to an SRC or patients with a history of SRC and a new psychiatric condition potentially attributable to concussion history were included. This study was approved by the institutional ethics review board at the University of Manitoba.

Definitions

Sports-related concussion was defined according to the International Consensus on Concussion in Sport as an injury caused by the transmission of biomechanical forces to the brain that lead to clinical symptoms affecting multiple domains of physical, cognitive, sleep, and neurobehavioral functioning.38 For the purposes of this study, acute SRC was defined as a diagnosis of SRC less than 30 days from the time of injury. Similar to previous studies of pediatric SRC,6,8,10,11 we chose to define PCS according to the International Classification of Diseases, 10th Revision (ICD-10) criteria as the presence of 3 or more concussion symptoms for at least 1 month (30 days) after an SRC.3 Patients were classified as having fully recovered when they were able to tolerate full-time school, completed the graduated return-to-play protocol set forth by the International Consensus on Concussion in Sport, and no longer met the clinical criteria for vestibulo-ocular dysfunction.8

Mental health data were used to provide an assessment of each patient’s preinjury and postinjury status. Preinjury psychiatric disorder was defined as a self-reported physician-diagnosed psychiatric disorder that was present before any history of concussion or TBI. Previous neuropsychiatry literature has defined NPD as a newly diagnosed psychiatric disorder that occurred in a patient with or without a lifetime preinjury psychiatric disorder after TBI.22 In this case, a patient who has no preinjury psychiatric history can be diagnosed with an NPD after TBI. In addition, a patient with a previous psychiatric history (i.e., major depressive disorder) can be diagnosed with an NPD (i.e., generalized anxiety disorder) after TBI that was not present before the injury. A patient with a preinjury history of major depressive episode who develops a major depressive episode after TBI would not receive this classification. Therefore, for the purposes of this study, NPD was defined as a newly diagnosed psychiatric disorder that occurred in a patient with or without a lifetime preinjury psychiatric disorder after the patient’s most recent concussion. Depressive disorder was classified as a diagnosis of major depressive disorder, major depressive episode, depressive disorder not otherwise specified (NOS), dysthymia, or adjustment disorder with depressed mood. Anxiety disorder was classified as a diagnosis of generalized anxiety disorder, posttraumatic stress disorder, adjustment disorder with anxiety, separation anxiety disorder, or obsessive-compulsive disorder (OCD). For the purposes of this study, patients with a postinjury psychiatric outcome included any patient who developed an NPD, developed subjective worsening symptoms of a preinjury psychiatric disorder, or developed new and isolated suicidal ideation. Postinjury interventions were defined as interventions (medication, cognitive behavioral therapy, etc.) prescribed to a patient after the concussion.

Clinical Assessments

At the time of initial medical consultation, every patient completed a standardized data-collection form that included demographic data, sport played at the time of concussion, medical history, past concussion history, and family history. At the initial consultation, each patient also completed the Post-Concussion Symptom Scale (PCSS), an inventory that consists of 22 symptoms, classified as physical, cognitive, sleep, or emotional, that are rated on a 7-point (0–6) Likert scale with a maximum score of 132 (6 × 22). Every patient underwent a clinical history and physical examination by a single neurosurgeon. At the time of the study, a clinical neuropsychologist was not part of the on-site multidisciplinary concussion program. As such, computerized neurocognitive tools were not used as a supplemental tool to confirm the diagnosis of concussion in this cohort. Patients were seen in follow-up at 1- to 4-week intervals, depending on the severity of their symptoms, trajectory of recovery, and availability rather than according to a predesigned controlled research protocol. At each follow-up appointment, every patient completed the PCSS and underwent a clinical interview and follow-up physical examination, as medically indicated, by the neurosurgeon. In general, the patients were managed conservatively with physical and cognitive rest followed by gradual reintegration into full school and sporting activities. Patients who remained symptomatic at 1 month were considered for multidisciplinary management, which included referrals to experts in vestibular or cervical spine physiotherapy, exercise science, headache neurology, neuropsychology, and neuro-ophthalmology. The patients were screened for postinjury psychiatric outcomes by the neurosurgeon based on their PCSS score and clinical interview findings in the follow-up visits. Referrals to mobile crisis, adolescent psychiatry, and clinical neuropsychology were made as medically indicated by the neurosurgeon and not according to any preexisting standardized criteria. Neuroimaging studies were also performed as clinically indicated by the neurosurgeon and not according to any standardized criteria. Interventions were initiated by adolescent psychiatrists, pediatricians, or family medicine physicians.

Statistical Analysis

The distributions of baseline characteristics for the patients with SRC with and those without a postinjury psychiatric disorder were summarized using proportions for dichotomous/polytomous characteristics and means with standard deviations for continuous characteristics. If a continuous variable was not normally distributed, it was summarized by using the median and interquartile range (IQR). Dichotomous/polytomous clinical characteristics of those with and those without a postinjury psychiatric disorder were compared by using the chi-square test. Continuous clinical characteristics were compared by using the t-test. Statistical differences in medians were determined by using the Wilcoxon rank-sum test. For all statistical tests, a p value of < 0.05 was deemed statistically significant.

Results

Study Population

Between September 1, 2013, and October 1, 2014, 174 patients with SRC (mean age 14.2 years [SD 2.3], 61.5% male) who met the inclusion criteria for the study were evaluated at the multidisciplinary pediatric concussion program. Of these patients, 134 (77.0%) were classified as having acute SRC and 39 (22.4%) were classified as having PCS at the time of initial consultation. One patient was referred for consultation after a newly diagnosed psychiatric disorder that the referring physician suspected was partly attributable to concussion history. The median time from injury to initial consultation for all the patients was 9 days (IQR 6–27). For patients with acute SRC this time was 7 days (IQR 5–11), and for patients with PCS, 80 days (IQR 40–120). The median PCSS score for all the patients was 13 (IQR 4–29). The median PCSS score for patients with acute SRC was 11 (IQR 3–25), and for patients with PCS, it was 21 (IQR 10–43). Overall, hockey and soccer were the most commonly played sports at the time of injury. Additional characteristics among those who did and those who did not develop a psychiatric disorder are listed in Table 1.

TABLE 1.

Clinical characteristics of pediatric patients with SRC with or without a postinjury psychiatric disorder*

CharacteristicTotal (n = 174)Psychiatric OutcomeNo Psychiatric Outcomep Value
(n = 20)(n = 154)
Mean age in yrs (± SD)14.22 ± 2.3415.10 ± 1.8914.10 ± 2.370.073
Male107 (61.49)8 (40.00)99 (64.29)0.036
Medical history
 Previous concussion87 (50.00)10 (50.00)77 (50.00)1.00
 Migraine16 (9.20)2 (10.00)14 (9.09)0.895
 Preinjury psychiatric disorder23 (13.22)9 (45.00)14 (9.09)<0.001
 Family history of psychiatric disorders28 (16.09)8 (40.00)20 (12.99)0.002
 Missing1 (0.57)1 (0.65)
Loss of consciousness28 (16.09)2 (10.00)26 (16.88)0.431
Amnesia48 (27.59)6 (30.00)42 (27.27)0.811
Median initial PCSS score (IQR)13 (4–29)23 (13–57)11 (3–27)0.003
Median initial emotional PCSS subscore if score >0 (IQR)4 (1–8)9 (4–17)4 (1–7)0.003
 Sadness34 (19.54)9 (45.00)23 (14.94)0.001
  Missing4 (2.30)0 (0.00)4 (2.60)
 Nervousness35 (20.11)10 (50.00)25 (16.23)0.001
  Missing4 (2.30)0 (0.00)4 (2.60)
 Irritability72 (14.38)12 (60.00)60 (38.96)0.089
  Missing4 (2.30)0 (0.00)4 (2.60)
 More emotional50 (28.74)11 (55.00)39 (25.32)0.008
  Missing4 (2.30)0 (0.00)4 (2.60)
 Sport
  Hockey62 (35.63)9 (45.00)53 (34.42)
  Soccer32 (18.39)3 (15.00)29 (18.83)
  Football21 (12.07)1 (5.00)20 (12.99)
  Basketball13 (7.47)3 (15.00)10 (6.49)
  Baseball8 (4.60)0 (0.00)8 (5.19)
  Skiing/snowboarding6 (3.45)1 (5.00)5 (3.25)
  Volleyball6 (3.45)0 (0.00)6 (3.90)
  Ringette5 (2.87)0 (0.00)5 (3.25)
  Skating2 (1.15)1 (5.00)1 (0.65)
  Other19 (10.92)2 (10.00)17 (11.04)

Values are number (%) unless indicated otherwise.

A total of 86 patients had an initial emotional PCSS subscore of > 0 (14 with a psychiatric outcome and 72 with no psychiatric outcome).

Prevalence of Emotional Symptoms Among Pediatric Patients With SRC

Emotional symptoms reported at initial presentation by the patients using the PCSS included symptoms of sadness, nervousness, irritability, and “more emotional” rated on a 7-point Likert scale from 0 (no symptoms) to 6 (severe). As such, the minimal emotional PCSS subscore was 0, and the maximum was 24. At least 1 emotional symptom was reported by 58 patients (43.3%) with acute SRC, 28 (71.8%) with PCS, and 86 (49.4%) in the combined SRC group at initial presentation. The median emotional PCSS subscore was 0 (IQR 0–3) for patients with acute SRC, 4 (IQR 0–10) for patients with PCS, and 0 (IQR 0–4) for the combined SRC cohort. There was no difference between the median emotional PCSS subscores among patients with or those without a preexisting psychiatric disorder (p = 0.06) or family history of psychiatric illness (p = 0.33).

Preinjury Psychiatric Status

Medical histories of the patients with SRC in this study revealed that 87 patients (50%) reported at least 1 previous concussion, 16 (9.2%) had migraine or unspecified headaches, and 8 (4.6%) reported an unspecified learning disorder. Preinjury psychiatric disorders were reported by 23 patients (13.2%) with SRC, including ADHD (n = 14 [8.0%]), depressive disorders (n = 4 [2.3%]), anxiety disorders (n = 5 [2.9%]), and Tourette’s syndrome (n = 1 [0.6%]).

A family history of psychiatric illness was reported by 28 (16.1%) of the patients with SRC included in the study, and 8 patients (4.6%) with a family history also had a preinjury psychiatric disorder. A family history of psychiatric illness was significantly higher among patients included in the study with a preinjury psychiatric disorder than among those without a family history of psychiatric illness (p = 0.03). Clinical characteristics of pediatric patients with SRC with and those without a postinjury psychiatric disorder are summarized in Table 1.

Postinjury Psychiatric Outcomes and Interventions

Of the total sample (n = 174), 2 study patients (1.1%) were referred to mobile crisis, 16 (9.2%) to adolescent psychiatry, and 5 (2.9%) to clinical neuropsychology for psychiatric assessment (Table 2).

TABLE 2.

Psychiatric resource utilization, interventions, and clinical outcomes among pediatric patients with SRC

No. of Patients
Total (n = 174)w/ Psychiatric Disorder (n = 20)w/o Psychiatric Disorder (n = 154)
Novel psychiatric resource
 Mobile crisis220
 Clinical psychology440
 Clinical neuropsychology532
Psychiatry16151
Novel interventions for 20 patients w/ psychiatric outcomes
 Medication alone (new medications or increased dosages of existing medications)NA2NA
 CBT aloneNA4NA
 Multimodal therapyNA9NA
 NoneNA5NA
Outcome
 Returned to play1205115
 Remained in treatment20911
 Committed suicide110
 Lost to follow-up33528

CBT = cognitive behavioral therapy; NA = not applicable.

During the study period, 20 (11.5%) of 174 patients met the study criteria for a postinjury psychiatric disorder, including 14 patients diagnosed with an NPD, 2 diagnosed with novel and isolated suicidal ideation, and 4 who experienced subjective worsening symptoms of a preexisting psychiatric disorder (Table 3). Not including patients who were referred to the multidisciplinary concussion program because of a postinjury psychiatric disorder potentially related to concussion history, the prevalence of a postinjury psychiatric outcome in this study was 10.9%. Among the 20 patients with a postinjury psychiatric disorder, 10 (50%) had a history of preinjury psychiatric disorder and 8 (40%) had a family history of psychiatric illness. Of the 20 patients in this study who developed postinjury psychiatric disorders, 15 (75%) had 1 or 2 lifetime concussions, whereas 5 (25%) had a history of 3 or more lifetime concussions. Psychosocial stress was reported by 12 (60%) of the patients who developed postinjury psychiatric outcomes. In this study, 19 NPDs were diagnosed among 14 patients, including depressive disorders (n = 10 [52.6%]), anxiety disorders (n = 4 [21.1%]), major depression with secondary anxiety (n = 1 [5.3%]), ADHD (n = 1 [5.3%]), bipolar disorder (n = 1 [5.3%]), and substance abuse (n = 2 [10.5%]). All postinjury psychiatric disorders were diagnosed by an adolescent psychiatrist and/or a clinical neuropsychologist, except for 1 that was diagnosed by a sports medicine physician before referral to the multidisciplinary concussion program. All diagnoses were made during outpatient consultations, with the exception of 1 patient who required hospital admission for evaluation and stabilization for a new diagnosis of bipolar disorder and 1 patient diagnosed with adjustment disorder with depressed mood and substance abuse after hospital admission for a suicide attempt. At the time of the postinjury psychiatric outcome assessment, 18 (90%) of 20 patients also met the ICD-10 criteria for PCS. Interventions among the 20 patients with postinjury psychiatric outcomes included pharmacological therapy alone for 2 (10%) patients, cognitive behavioral therapy alone for 4 (20%), multimodal therapy for 9 (45%), and no treatment for 5 (25%). Novel pharmacological therapies used to treat postinjury psychiatric disorders in this cohort included antidepressants (10 patients), sleep medications (5 patients), stimulants (2 patients), mood stabilizers (1 patient), antianxiety medication (1 patient), and atypical antipsychotic medication (1 patient). A detailed summary of patients with postinjury psychiatric disorders is presented in Table 4.

TABLE 3.

Postinjury psychiatric outcomes in pediatric patients with SRC

Postinjury Psychiatric OutcomeNo.*
NPDs19
Novel depressive disorder10
 Major depressive disorder6
 Major depressive episode2
 Adjustment disorder w/ depressed mood2
Novel anxiety disorder4
 Generalized anxiety disorder1
 Separation anxiety disorder1
 Adjustment disorder w/ anxiety1
 Anxiety disorder NOS1
Other disorder5
 Bipolar disorder1
 Major depressive disorder w/ secondary anxiety1
 ADHD1
 Substance abuse2
Isolated suicidal ideation2
Subjective worsening symptoms of a preexisting psychiatric disorder4

There were 25 outcomes (in 20 patients).

These NPDs occurred in 14 patients.

TABLE 4.

Clinical details of pediatric patients with SRC and postinjury psychiatric outcomes

Age (yrs), SexNo. of Prev ConcussionsPreinjury StatusFam HxPS StressSportPCSS ScoresMet PCS CritImaging ResultNovel Resource(s)Postinjury Psych OutcomeNovel Interv(s)Clin Outcome
Psych HxPsych Interv(s)E, TIE*
15, M0NoneNoYesYesSoccer7, 2110YesCT: pst fossa arachnoid cystMobile crisis, psychiatryBipolar I disorderLithium, CBTRTP
14, F0Substance abuseNoNoYesSoccer3, 208YesMRI: complex pineal region cystMobile crisis, psychiatryMDDCBTLTF
18, F0NoneNoNoNoHockey1, 8NAYesMRI: normalVestibular therapyMDDAmitriptyline, desvenlafaxineRTP
18, F1NoneNoNoNoHockey4, 194YesNonePsychiatry, HA neurologyAdjustment disorder w/ anxietyCBTRIT
13, M3ADHDNoYesYesHockey0, 31NAYesNonePsychiatry, clin NSMDECitalopram, CBTLTF
14, F0NoneNoYesNoFigure skating3, 206YesNonePsychiatryAdjustment disorder w/ depressed mood, anxiety disorder NOSCitalopram, paroxetine, lorazepam, melatonin, CBTRIT
14, F0PTSDNoYesNoSynch swim24, 6424YesNonePsychiatryMDD w/ secondary anxietySertraline, melatonin, CBTRIT
19, F0NoneNoNoYesHockey13, 7518YesCT: skull fx; MRI: normalPsychiatry, clin NSMDDCBTRIT
16, F2MDENoNoYesSoccer12, 5012YesNoneClin NS, HA neurology, clin psychologyMDDQuetiapine, CBTLTF
16, F1Substance abuseNoNoYesFootball8, 5816YesMRI: normalPsychiatry, HA neurologyMDD, generalized anxiety disorder, ADHDFix, MP, melatonin, CBTRIT
15, F1ADHDMPYesNoHockey4, 496YesMRI: normalPsychiatry, clin NSSeparation anxiety, anxietyFix, trazadone, CBTRIT
14, F0NoneNoYesNoBasketball0, 12NAYesNonePsychiatryMDEFix, melatonin, CBTRIT
15, M0NoneNoYesYesBasketball0, 8NAYesNoneNoneMDD, substance abuseMP, flxLTF
16, M6NoneNoNoYesHockey0, 0NANoCT: normalPsychiatryAdjustment disorder w/ depressed mood, substance abuseNoneSuicide
14, M2NoneNoneNoYesHockey0, 251YesNoneNoneIsolated suicidal ideationNoneRTP
11, M0NoneNoYesYesHockey21, 8824YesMRI: normalPsychiatryIsolated suicidal ideationNoneLTF
15, F2Tourette’s syndrome, OCD, anxiety NOSRisperidone, flxNoYesBasketball17, 468YesMRI: normalPsychiatryWorsening OCD & anxiety Sx, new self-harm behaviorsIncreased fix, CBTRIT
14, M1ADHDNoNoNoSnow-boarding0, 21NAYesNoneNoneWorsening of ADHD SxNoneRTP
4, F1Depressive & anxiety disorderQuetiapine, sertraline, CBTNoYesDance15, 6911YesNonePsychiatry, clin NS, HA neurology, vestibular therapyWorsening depression & anxiety SxCBTRIT
17, M0ADHDNoNoNoneHockey8, 17NANoNoneNoneWorsening of ADHD SxNoneRTP

Clin = clinical; crit = criteria; E = emotional score; E, Tl = emotional & total initial score; fam = family; fix = fluoxetine; fx = fracture; HA = headache; Hx = history; interv = intervention; LTF = lost to follow-up; MDD = major depressive disorder; MDE = major depressive episode; MP = methylphenidate; NA = not available; NS = neuropsychology; prev = previous; PS = psychosocial; pst = posterior; PTSD = posttraumatic stress disorder; psych = psychiatric; RTP = returned to play; RIT = remained in treatment at time of writing; Sx = symptoms; synch swim = synchronized swimming.

At time of referral for psychiatric assessment (n = 24 patients).

At time of psychiatric assessment.

Return-to-Play Status Among Patients With Postinjury Psychiatric Outcomes

Overall, 5 (25%) of the 20 patients with postinjury psychiatric disorders were medically cleared to return to full sports participation, whereas 5 (25%) were lost to follow-up and 9 (45%) remained in treatment with the multidisciplinary concussion program at the end of the study period. One patient who was asymptomatic at the time of initial consultation committed suicide.

Discussion

In this study, we found that pediatric patients with SRC referred to our multidisciplinary pediatric concussion program commonly endorsed emotional symptoms at initial consultation. At least 1 emotional symptom was reported in 43% of the patients with acute SRC, 72% of the patients with PCS, and 49% of the combined cohort at initial presentation. In the vast majority of patients with acute SRC, emotional symptoms resolved along with physical, cognitive, and sleep-related symptoms, allowing for successful return to play. However, in a small proportion of patients, these symptoms worsened and negatively affected patient functioning. Studies evaluating the presence of individual concussion symptoms among pediatric patients with concussion at different time points of recovery and referral are rare. In 1 study conducted at a tertiary pediatric concussion clinic, emotional symptoms, including depression, frustration, irritability, and restlessness, were reported by 22.9%–27.7% of the patients evaluated less than 72 hours after injury.7 Emotional symptoms peaked 7 days after injury and decreased to 8.3%–14.7% among patients who remained symptomatic at 28 days. Together, these findings confirm that emotional symptoms are reported in a substantial proportion of pediatric patients with SRC, can fluctuate throughout the course of recovery, and can persist in selected individuals.

Ours is the first study to examine the prevalence, clinical features, risk factors, and management of postinjury psychiatric outcomes among pediatric patients with SRC referred to a multidisciplinary pediatric concussion program. In this study, 11.5% of the patients with SRC experienced a postinjury psychiatric outcome. Fourteen patients developed NPDs, 2 patients developed isolated suicidal ideation, and 4 additional patients experienced worsening symptoms of a preinjury psychiatric disorder. Previous work has suggested a significant association between TBI and psychiatric disorders in children and adolescents, with rates significantly higher than those observed among uninjured21,22,41,49 and orthopedically injured controls.32 Novel psychiatric disorders diagnosed among patients with TBI in these studies were heterogeneous and included depressive disorders, anxiety disorders such as generalized anxiety disorder, panic disorder, posttraumatic stress disorder, and OCD, somatoform disorder, ADHD, and behavioral disorders such as oppositional-defiant disorder and conduct disorder.4,21–23,26–28,30,34–36,49 Among the most common NPDs observed among prospective studies has been personality change resulting from a generalized medical condition, which has been diagnosed in up to 40% of pediatric patients after TBI but was not formally assessed in the present study.22,36 Clinical variables associated with the development of NPDs after pediatric TBI include history of preinjury psychiatric disorder, family history of psychiatric illness, severity of injury, low socioeconomic status, and preinjury adaptive and intellectual functioning.20,22,25,31,34,54 In addition, psychosocial stress and family functioning have also been identified as important factors that affect the risk of developing NPDs after pediatric TBI. In the present study, patients with SRC who developed a postinjury psychiatric outcome were significantly more likely to be female, to have a preinjury psychiatric disorder, and to have a family history of psychiatric illness.

Multiple concussions and repetitive subconcussive head injuries have been implicated as risk factors for the development of long-term neurological disorders such as depression, dementia, and other neurodegenerative conditions in professional athletes;14,18,40,47,52 however, their role in the development of postinjury psychiatric outcomes after pediatric SRC remains understudied. Of the 20 patients who developed postinjury psychiatric outcomes in this study, 75% had a history of 1 or 2 lifetime concussions, whereas 25% had a history of 3 or more lifetime concussions. Although injury severity has been identified as a key predictor of NPD development in the TBI literature,20,22,36 the severity of concussion is difficult to assess clinically among children and adolescents. The mean or median PCSS score has been used in previous pediatric SRC studies as a measure of concussion severity,8,10,43,44 whereas the use of the emotional PCSS subscore as a measure of psychological health has not been well studied. In this study, patients who reported sadness, nervousness, and feeling more emotional at initial presentation were more likely to develop postinjury psychiatric outcomes. In addition, higher initial PCSS and initial emotional PCSS scores were both associated with the development of a postinjury psychiatric outcome. Despite these findings, postinjury psychiatric outcomes did occur in patients who reported no emotional symptoms at initial presentation. In fact, in some cases, emotional PCSS subscores were not substantially elevated during follow-up appointments despite collateral clinical history indicating distressing symptoms of an underlying mood disorder or suicidal ideation. These findings suggest that symptom checklists are insufficient screening tools for postinjury psychiatric outcomes in children and adolescents with SRC and underscore the need for physicians to inquire about symptoms of depression and anxiety, as well as suicidal ideation, during the clinical evaluation irrespective of symptom inventory scores. Injury severity as measured by the initial PCSS score has also been associated with prolonged recovery and the development of PCS in pediatric SRC,8,10,43,44 which itself may play an important role in the development of psychiatric outcomes. In this study 90% of patients who developed postinjury psychiatric outcomes also met the ICD-10 criteria for PCS at the time of diagnosis. These findings suggest that children and adolescents who develop PCS should also be screened for psychiatric disorders and suicidal ideation.

Given the preinjury and postinjury rates of psychiatric disorders that can exist among pediatric patients with SRC, it is imperative that health care professionals caring for these patients have clinical training in mental health conditions that can potentially affect this population. Multidisciplinary pediatric concussion programs that offer specialized care for these patients should also have well-established partnerships with local mental health resources such as mobile crisis units, pediatric emergency departments, and adolescent psychiatry who can initiate prompt clinical treatment for these patients, especially in the setting of acutely worsening symptoms or suicidal ideation. Treatment options for postinjury psychiatric outcomes are often multimodal and include a combination of pharmacological and cognitive behavioral therapies. As demonstrated here, long-term follow-up by medical experts in TBI and psychiatry is often required.

Return-to-play status among pediatric patients with SRC who develop postinjury psychiatric outcomes is difficult to assess based on the results of this preliminary study. To help inform clinical decision making, future research is needed to evaluate whether the pathophysiological mechanisms that govern postinjury psychiatric outcomes are an expression of an unresolved TBI and thereby modify the risk of future concussion in patients returned to contact and collision sports. At present, there are no evidence-based guidelines directing return-to-play or retirement decision-making in patients who develop NPDs after SRC; as such, each patient must be managed on an individual basis taking into account previous concussion and psychiatric history, current symptoms, neuroimaging findings, and response to treatment.

Among the rare but most tragic of outcomes after pediatric SRC is suicide. Previous studies have suggested that adult13,53 and childhood survivors of TBI19 are at an elevated risk of suicidal behavior. Although some studies have demonstrated neuropathological findings of chronic traumatic encephalopathy among professional football players with a history of concussion and completed suicide,14,39,40,47 there have been no prospective population-based studies that have demonstrated a causal relationship between concussion and suicide,15 especially in children and adolescents. In many cases of suicide, comorbid psychiatric illness and psychosocial stress are often contributing factors. In the case of the 1 fatality secondary to suicide in the present study, the patient had a significant concussion history, was previously diagnosed with adjustment disorder with depressed mood after a hospital admission for a previous suicide attempt, and was experiencing a high level of psychosocial stress at the time of the completed suicide. An autopsy was not performed.

The results of the present study must be considered in light of several important limitations. First, we did not use a standardized psychiatric interview to provide comprehensive assessment of both preinjury and postinjury emotional symptoms and psychiatric disorders in all patients referred to the multidisciplinary concussion program. Among the patients referred to adolescent psychiatry, they all underwent formal assessments that included assessing preinjury and postinjury symptoms and psychiatric disorders; however, the incorporation of standardized instruments such as the Schedule for Affective Disorders and Schizophrenia for School-Aged Children, Present and Lifetime Version (K-SADS-PL), which has been used in previous studies,16,36 may have led to a more comprehensive assessment of preinjury and postinjury psychiatric disorders. Second, as mentioned, we did not use standardized instruments that assessed for personality change among those referred to adolescent psychiatry. Personality change accounts for a substantial proportion of NPDs detected in previous studies of psychiatric disorders after TBI.22,28,29,36 Although emotional lability, irritability, and apathy were endorsed among patients in this study, personality change disorders were not captured and likely lowered the prevalence of NPDs observed in this study. Third, studies have demonstrated that family functioning, socioeconomic status, and preinjury adaptive and intellectual function may contribute to the development of NPDs after pediatric TBI.22,24,32 These factors were also not assessed in this cohort of patients and should be considered in future studies. Fourth, although all the patients in this study were provided return-to-learn and return-to-play guidance, adherence to these recommendations was not assessed formally. It is possible that some patients were not compliant with these recommendations and that inadequate amounts of physical and cognitive rest contributed to the development of postinjury psychiatric outcomes in this study. Fifth, we examined the prevalence of emotional symptoms and NPDs among children and adolescents who were referred to a multidisciplinary pediatric concussion program, which in and of itself may have contributed to several limitations. Tertiary concussion clinics may include patients with more severe injuries who are more likely to develop long-term comorbidities associated with TBI, including PCS and psychiatric disorders. These clinics also experience high rates of patients who are lost to follow-up,8,44 which can have an impact on study results. In addition, patients are often evaluated at various levels of acuity and are seen in follow-up depending on the severity of their symptoms, trajectory of recovery, and availability and not according to a controlled research protocol. Most important is that the decision to refer any patient for neu-ropsychological or psychiatric assessment was based not on strict predetermined criteria but almost entirely on the clinical judgment of a neurosurgeon. As such, the findings of this study cannot be used to estimate the risk of developing a postinjury psychiatric outcome among a general population of pediatric patients with SRC. Finally, we did not compare emotional and psychiatric findings among pediatric patients with SRC with those of a control group or a population of patients who did not sustain TBI. Future prospective controlled studies are needed to confirm that postinjury psychiatric outcomes observed after SRC are attributable to TBI and not just injury alone.

Despite these methodological limitations, our study demonstrates that emotional symptoms are commonly reported at initial consultation among pediatric patients with SRC who are referred to a multidisciplinary pediatric concussion program. In most cases, these symptoms resolved and allowed for a successful return to sporting activities; however, in some cases, they worsened and led to the development of NPDs, isolated suicidal ideation, and worsening symptoms of a preexisting psychiatric disorder. Patients who are female, who report higher levels of emotional and total concussion symptoms at initial consultation, who have a preinjury and/or family history of psychiatric disorders, and who have PCS should be monitored closely for postinjury psychiatric outcomes. All patients with suspected postinjury psychiatric outcomes should be promptly referred to mental health professionals for multidisciplinary assessment, management, and follow-up. Future prospective studies using standardized psychiatric assessment tools that provide comprehensive assessment of preinjury and postinjury mental health, psychosocial stress, family functioning, and socioeconomic status are needed to establish the true risk of developing psychiatric disorders after an SRC. Until such data are available, clinical and return-to-play decision-making should be made on an individual basis by physicians and health care professionals who have had clinical training and experience with concussion, TBI, and psychiatry.

Acknowledgments

We thank the Pan Am Clinic Foundation and the Manitoba Health Research Council for their financial support of this study.

Author Contributions

Conception and design: Ellis, Ritchie, Russell. Acquisition of data: all authors. Analysis and interpretation of data: Ritchie, Koltek, Hosain, Chu, Selci, Russell. Drafting the article: Ellis, Russell. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Ellis.

References

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  • 1

    Babcock L, , Byczkowski T, , Wade SL, , Ho M, , Mookerjee S, & Bazarian JJ: Predicting postconcussion syndrome after mild traumatic brain injury in children and adolescents who present to the emergency department. JAMA Pediatr 167:156161, 2013

    • Search Google Scholar
    • Export Citation
  • 2

    Barlow KM, , Crawford S, , Stevenson A, , Sandhu SS, , Belanger F, & Dewey D: Epidemiology of postconcussion syndrome in pediatric mild traumatic brain injury. Pediatrics 126:e374e381, 2010

    • Search Google Scholar
    • Export Citation
  • 3

    Boake C, , McCauley SR, , Levin HS, , Contant CF, , Song JX, & Brown SA, et al.: Limited agreement between criteria-based diagnoses of postconcussional syndrome. J Neuropsychiatry Clin Neurosci 16:493499, 2004

    • Search Google Scholar
    • Export Citation
  • 4

    Brown G, , Chadwick O, , Shaffer D, , Rutter M, & Traub M: A prospective study of children with head injuries: III. Psychiatric sequelae Psychol Med 11:6378, 1981

    • Search Google Scholar
    • Export Citation
  • 5

    Burton LJ, , Quinn B, , Pratt-Cheney JL, & Pourani M: Headache etiology in a pediatric emergency department. Pediatr Emerg Care 13:14, 1997

    • Search Google Scholar
    • Export Citation
  • 6

    Corwin DJ, , Zonfrillo MR, , Master CL, , Arbogast KB, , Grady MF, & Robinson RL, et al.: Characteristics of prolonged concussion recovery in a pediatric subspecialty referral population. J Pediatr 165:12071215, 2014

    • Search Google Scholar
    • Export Citation
  • 7

    Eisenberg MA, , Meehan WP III, & Mannix R: Duration and course of post-concussive symptoms. Pediatrics 133:9991006, 2014

  • 8

    Ellis MJ, , Cordingley D, , Vis S, , Reimer K, , Leiter J, & Russell K: Vestibuloocular dysfunction in pediatric sports-related concussion. J Neurosurg Pediatr 18, 2015

    • Search Google Scholar
    • Export Citation
  • 9

    Fletcher JM: Adolescent depression: diagnosis, treatment, and educational attainment. Health Econ 17:12151235, 2008

  • 10

    Gibson S, , Nigrovic LE, , O’Brien M, & Meehan WP III: The effect of recommending cognitive rest on recovery from sport-related concussion. Brain Inj 27:839842, 2013

    • Search Google Scholar
    • Export Citation
  • 11

    Grubenhoff JA, , Deakyne SJ, , Brou L, , Bajaj L, , Comstock RD, & Kirkwood MW: Acute concussion symptom severity and delayed symptom resolution. Pediatrics 134:5462, 2014

    • Search Google Scholar
    • Export Citation
  • 12

    Guskiewicz KM, , Marshall SW, , Bailes J, , McCrea M, , Harding HP Jr, & Matthews A, et al.: Recurrent concussion and risk of depression in retired professional football players. Med Sci Sports Exerc 39:903909, 2007

    • Search Google Scholar
    • Export Citation
  • 13

    Harris EC, & Barraclough B: Suicide as an outcome for mental disorders. A meta-analysis Br J Psychiatry 170:205228, 1997

  • 14

    Hazrati LN, , Tartaglia MC, , Diamandis P, , Davis KD, , Green RE, & Wennberg R, et al.: Absence of chronic traumatic encephalopathy in retired football players with multiple concussions and neurological symptomatology. Front Hum Neurosci 7:222, 2013

    • Search Google Scholar
    • Export Citation
  • 15

    Iverson GL: Chronic traumatic encephalopathy and risk of suicide in former athletes. Br J Sports Med 48:162165, 2014

  • 16

    Kaufman J, , Birmaher B, , Brent D, , Rao U, , Flynn C, & Moreci P, et al.: Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): initial reliability and validity data. J Am Acad Child Adolesc Psychiatry 36:980988, 1997

    • Search Google Scholar
    • Export Citation
  • 17

    Kerr ZY, , Marshall SW, , Harding HP Jr, & Guskiewicz KM: Nine-year risk of depression diagnosis increases with increasing self-reported concussions in retired professional football players. Am J Sports Med 40:22062212, 2012

    • Search Google Scholar
    • Export Citation
  • 18

    Lehman EJ, , Hein MJ, , Baron SL, & Gersic CM: Neurodegenerative causes of death among retired National Football League players. Neurology 79:19701974, 2012

    • Search Google Scholar
    • Export Citation
  • 19

    Lewinsohn PM, , Rohde P, & Seeley JR: Psychosocial characteristics of adolescents with a history of suicide attempt. J Am Acad Child Adolesc Psychiatry 32:6068, 1993

    • Search Google Scholar
    • Export Citation
  • 20

    Luis CA, & Mittenberg W: Mood and anxiety disorders following pediatric traumatic brain injury: a prospective study. J Clin Exp Neuropsychol 24:270279, 2002

    • Search Google Scholar
    • Export Citation
  • 21

    Massagli TL, , Fann JR, , Burington BE, , Jaffe KM, , Katon WJ, & Thompson RS: Psychiatric illness after mild traumatic brain injury in children. Arch Phys Med Rehabil 85:14281434, 2004

    • Search Google Scholar
    • Export Citation
  • 22

    Max JE: Neuropsychiatry of pediatric traumatic brain injury. Psychiatr Clin North Am 37:125140, 2014

  • 23

    Max JE, , Castillo CS, , Robin DA, , Lindgren SD, , Smith WL Jr, & Sato Y, et al.: Posttraumatic stress symptomatology after childhood traumatic brain injury. J Nerv Ment Dis 186:589596, 1998

    • Search Google Scholar
    • Export Citation
  • 24

    Max JE, , Castillo CS, , Robin DA, , Lindgren SD, , Smith WL Jr, & Sato Y, et al.: Predictors of family functioning after traumatic brain injury in children and adolescents. J Am Acad Child Adolesc Psychiatry 37:8390, 1998

    • Search Google Scholar
    • Export Citation
  • 25

    Max JE, & Dunisch DL: Traumatic brain injury in a child psychiatry outpatient clinic: a controlled study. J Am Acad Child Adolesc Psychiatry 36:404411, 1997

    • Search Google Scholar
    • Export Citation
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