Pediatric Sports-Related Concussion: An Approach to Care

Abstract

Sports-related concussion (SRC) is a common sports injury in children and adolescents. With the vast amount of youth sports participation, an increase in awareness of concussion and evidence that the injury can lead to consequences for school, sports and overall quality of life, it has become increasingly important to properly diagnose and manage concussion. SRC in the student athlete is a unique and complex injury, and it is important to highlight the differences in the management of child and adolescent concussion compared with adults. This review focuses on the importance of developing a multimodal systematic approach to diagnosing and managing pediatric sports-related concussion, from the sidelines through recovery.

‘Ongoing neurodevelopment represents a particular challenge of concussion care in this age range, especially during adolescence, . . .’

Pathophysiology of Concussion

More than 44 million youth participate in sports annually with approximately 1.1 to 1.9 million sports-related concussions occurring annually in children younger than 18 years in the United States.^1-4 Sports-related concussion (SRC), as defined by the 5th International Conference on Concussion in Sport, is a mild traumatic brain injury (mTBI) caused by a direct blow to the head, face, neck, or elsewhere on the body, with an impulsive force transmitted to the head, resulting in the rapid onset of impairment of neurological function and a range of clinical signs and symptoms that may resolve spontaneously or, in up to 30% of pediatric cases,^5,6 become prolonged. ⁷ While our understanding of the pathophysiology of concussion continues to evolve, seminal work has elucidated the pathophysiology of concussion to be a complex multifactorial process. Current understanding is that biomechanical forces to the head induce axonal deformation and immediate changes at the cellular level, including ionic flux and glutamate release that leads to the metabolic mismatch of increased glucose demands and decreased cerebral blood flow.^7-10 This metabolic mismatch phase produces a vulnerable re-injury window. ⁹ Studies have shown that the greatest risk for concussion is a prior concussion, ¹⁰ with the greatest risk occurring in the first 10 days post-injury.^7,11,12 Preliminary evidence has shown the vulnerable window may be longer in duration in children compared with adults, highlighting the importance of proper concussion diagnosis and management in the pediatric athlete.^12,13

The following describes concussion evaluation and management best practices for children and youth with concussion. Ongoing neurodevelopment represents a particular challenge of concussion care in this age range, especially during adolescence, a time period of rapid change that also aligns with the highest incidence of concussion. As such, the effects of concussion on the various physiological systems may manifest differently across the pediatric age range. Most research has been conducted on collegiate and high school age with fewer studies in younger concussed children. This review highlights primary data in children, noting when developmental differences may alter the clinical approach.

Concussion Evaluation

Sports-related concussion in children and adolescents can occur in various settings such as sports practices or games, with the proportion of concussions from sports and recreation increasing across the pediatric age range. ¹⁴ Youth who experience any trauma to the head resulting in the new onset of signs and symptoms (described below) should be removed from play and assessed for a concussion immediately. The athlete must be removed from play until a concussion can be safely excluded. ¹⁵ Concussion symptoms may not develop immediately, and athletes may underreport symptoms due to fear of being removed from play^16,17; however, it is critical to identify a concussion as soon as possible and remove the player from play. Multiple studies have demonstrated concussed youth and collegiate players who were not removed from play exhibited greater symptom burden and took longer to recover than those who were removed immediately.^18-22 Timely removal of play is also important due to evidence of potential negative sequelae following an additional head impact acutely after a concussion. A study in young athletes found an additional head impact within the first 24 hours of injury produced greater symptom burden and prolonged recovery rates than those without an additional head impact. ²³

Sideline Assessment: Sport Concussion Assessment Tool (SCAT-5)

Sideline assessment tools, such as the widely used Sport Concussion Assessment Tool (SCAT-5), developed at the 5th International Consensus Conference on Concussion in Sport, have utility in the immediate initial evaluation of concussion by coaches, athletic trainers or parents on the sidelines. The SCAT-5^15,24 tool combines 5 steps covering multiple domains affected by concussion into one sideline tool. Step 1 establishes clinical information about the athlete, step 2 assesses symptom severity, step 3 involves cognitive screening by use of the Standardized Assessment of Concussion (SAC) to assess orientation, immediate memory, and concentration (repeating digits backward and months in reverse order), step 4 involves a neurological screen and balance assessment via the Modified Balance Error Scoring System (mBESS) test, and step 5 assesses delayed recall by repeating a set of 5 words used in the immediate memory portion of step 3. A similar version, the SCAT-5 Child is intended for use in children between ages 5 and 12 years and accounts for variances in developmental stage of the younger population. ²⁴ While youth with access to athletic trainers to perform sideline assessments have been found to have higher rates of concussion recognition, ²⁵ it is important to acknowledge the limitations of sidelines assessments. They have not been validated as a return to play tool and should not substitute for a thorough clinical examination by a physician. ¹⁵

Symptom Assessment

To date, concussion diagnosis remains clinical,^2,15 based on patient-reported symptom assessment and a clinical examination by a trained clinician, including physicians, nurse practitioners, and athletic trainers. ²⁵ Clinicians rely heavily on various validated concussion symptom scales such as the Post-Concussion Symptom Scale (PCSS) for children older than 11 years ² or the Post-Concussion Symptom Inventory (PCSI) which has child, teen and parent versions. ² A systematic approach to managing concussion symptoms would be to group them into the following domains: somatic, visio-vestibular, cognitive, mood, and sleep^26-30 as seen in Figure 1.

Figure 1.

Domains of concussion. ³⁰

Somatic symptoms can manifest as headache, fatigue, dizziness, sleep disturbances, and light and noise sensitivity. Vestibular symptoms may include dizziness, nausea, vertigo, or motion sensitivity, including motion sickness. Vision symptoms may present as headache, dizziness, blurred vision, diplopia, eye strain, eye pain, convergence insufficiency, and reading difficulties. Cognitive symptoms may include fogginess and difficulties with memory and/or concentration. Many symptoms of SRC are heterogeneous and non-specific, having the potential to be misleading during the diagnosis and management of concussion. ³¹ Because of the potential ambiguity of concussion symptoms, it is important to incorporate screening for anxiety and depression symptoms^32-35 into the symptom assessment to distinguish these possibly masked symptoms that may be otherwise attributed to aspects of life rather than to a concussion. It is essential for the clinician overseeing care of the pediatric athlete to screen for mood symptoms manifesting as nervousness, irritability and feelings of increased sadness to address potential anxiety and depression experienced by the child early in the concussion recovery process. Screening can be administered via validated questionnaires such as the Brief Symptom Inventory (BSI-18), ³⁶ Pediatric Quality of Life Questionnaire (PedsQL), ³⁷ or a detailed history from the pediatric patient. It is important to acknowledge that some of these domains will overlap in symptoms, deficits and targeted rehabilitation as seen in Table 1.

Table 1.

Concussion Symptoms and Management Based on Domain Dysfunction^78,128.

Affected domain	Symptoms	Targeted therapy
Somatic dysfunction	■ Headache ■ Fatigue ■ Dizziness ■ Light/noise sensitivity ■ Sleep disturbances	■ Aerobic exercise rehabilitation
Visio-vestibular dysfunction	■ Headache ■ Dizziness ■ Nausea	■ Vestibular rehabilitation ■ Vision rehabilitation
Cognitive dysfunction	■ Difficulty concentrating ■ Difficulty remembering ■ Fogginess	■ Return to learn ■ Return to appropriate age-related level of learning if the child is not in school ■ Speech therapy, occupational therapy
Mood dysfunction	■ Anxiety ■ Depression ■ Irritability ■ Nervousness	■ Psychologist for counseling ■ Medication if needed as second-line treatment
Sleep dysfunction	■ Drowsiness ■ Trouble falling asleep ■ Sleeping more than usual ■ Sleeping less than usual ■ Fatigue	■ Sleep hygiene ■ Melatonin supplementation

Sleep disturbances can be an underappreciated symptom in children and adolescents following concussion and remain poorly understood in the pediatric population.^38-41 Adequate amounts of sleep are necessary for maintenance of cognitive, physical, and mood functions. Physicians should be encouraged to include a sleep assessment into their clinical concussion evaluation. Sleep dysfunction commonly manifests as difficulties in falling asleep, staying asleep, waking up, sleeping more or less than before the concussion, daytime sleepiness, and fatigue. In young children, these changes in sleep patterns can commonly result in new napping behaviors which can further dysregulate proper sleep function. Two studies evaluating sleep after pediatric concussion found poor sleep quality to be strongly associated with greater concussion symptom severity and longer recovery times following SRC.^38,42 Similarly, a study looking at collegiate athletes found daytime sleepiness and insomnia to be a risk factor for SRC, ⁴³ further highlighting the need for sleep to be assessed and incorporated into treatment recommendations to ensure safe return to sport participation. Emphasizing the importance of proper sleep hygiene can improve these sleep disturbances. Decreasing naps, decreasing screen time to one hour before bed and increasing exercise are important aspects of proper sleep hygiene ⁴⁴ and can improve sleep quality. One exploratory study found brief cognitive behavioral intervention by use of scheduled activities and sleep hygiene relaxation to be promising in sleep rehabilitation after pediatric concussion. ⁴⁵ In addition, the use of melatonin supplementation is recommended for sleep dysfunction following concussion.^46,47 Studies have shown melatonin supplementation to improve sleep disturbances in adolescents suffering from sleep dysfunction, headaches, and anxiety after concussion.^39,46

Despite symptom assessment playing a crucial role in concussion evaluation, it is important to acknowledge concussion awareness and symptom reporting behaviors of pediatric athletes. Multiple studies have found young athletes to underreport symptoms after concussion, further emphasizing the importance of a targeted concussion clinical examination by a physician. A study in high school rugby players found that 80% failed to report their concussion or returned to play before full clinical recovery. ⁴⁸ Recent studies exploring reporting behaviors in high school and collegiate athletes found athletes did not report their SRC due to fear of removal from play, fear of repercussions from coaches, or a lack of recognition of the seriousness of the injury ⁴⁹ by the athlete, coaches, and parents.^17,50-54 There is, however, evidence that female high school athletes being more likely to report their SRC compared with their male counterparts, despite having similar awareness and knowledge of concussion symptoms. ⁴⁹

The Importance of a Medical History

In addition to categorizing the symptom profile, a detailed medical history is important to obtain. Previous concussion history, as well as specifics of those concussions, are important variables. The number of previous concussions^55,56 and having a concussion with symptoms lasting longer than a week have predicted longer recovery rates. ⁵ Research has shown youth who sustain a first concussion that has a long recovery (more than 30 days) and a high symptom burden (greater than 11 symptoms) are more likely to sustain a second injury. ¹⁰ Patients with pre-existing conditions are at risk for prolonged recovery rates. ³⁵ Those with psychological conditions such as anxiety and depression took longer to recover compared to those without these pre-existing conditions.^{5,35,55,57-59} Other studies have found female sex, ⁶⁰ pre-existing attention deficit hyperactivity disorder (ADHD), ⁶¹ sleep disturbances ⁶² or motion sickness^63,64 to be risk factors in children. ⁶¹ One pediatric targeted study found female sex, headaches, migraines, and a history of psychiatric conditions to significantly prolong recovery rates in children younger than 12 years. ⁶⁵ As such, thorough screening for pre-existing conditions (examples given in Table 2) is essential and can aid in concussion management by identifying children who may be susceptible to a prolonged recovery and require additional recovery support via targeted rehabilitation and/or specialist interventions. In addition to medical history, an injury history is important. This should include identification of the mechanism of injury and details surrounding the injury.

Table 2.

Pre-existing Conditions: Potential Risk for Prolonged Concussion Recovery ⁷⁸ .

Affected domain	Condition examples
Somatic dysfunction	Postural hypotension Postural orthostatic tachycardic syndrome (POTS)
Visio-vestibular	Vestibular: Motion sickness Visual: Amblyopia  Strabismus  History of eye surgery  Glasses  Convergence insufficiency (CI)  History of vision therapy
Cognitive	Attention-deficit disorder (ADD) Attention-deficit hyperactivity disorder (ADHD) Learning disorders, ie, dyslexia or processing delays
Mood	Anxiety Depression Bipolar disorder Obsessive-compulsive disorder (OCD) Oppositional defiant disorder (ODD)
Sleep	Insomnia

Concussion Physical Examination

Concussion physical examination should focus on assessing the autonomic, oculomotor, and vestibular systems seen in Table 3, as they are heavily interconnected and commonly affected after concussion.^15,66-69 Deficits in these systems commonly increase symptom burden and have implications for prolonged recovery rates. Autonomic nervous system dysfunction has been recognized as a result of pathophysiological changes following concussion.^70-76 Dysfunction can manifest in children and adolescents as reporting symptoms of fatigue, headache, “pressure in the head,” dizziness, light sensitivity, noise sensitivity, and exercise intolerance.^73,76-79 Clinical examination findings of cerebral blood flow (CBF) dysregulation may include elevated resting heart rate, orthostatic hypotension, and large reactive pupils. Studies have demonstrated CBF dysregulation, specifically decreased cerebral blood flow acutely after injury ¹³ is related to increased symptom severity^71,80 and decreased cognitive function. ⁷⁴

Table 3.

Key Components of the Concussion Physical Examination^78,128.

Targeted system	Physical examination assessment	Possible findings
Autonomic	■ Blood pressure and heart rate ■ Pupil examination	■ Increased heart rate ■ Orthostatic hypotension ■ Larger pupils ■ Exacerbation of symptoms
Visio-vestibular	■ Smooth pursuits ■ Saccadic function (horizontal and vertical directions) ■ Gaze stability/angular vestibular ocular reflex (VOR) (horizontal and vertical directions) ■ Vision motion sensitivity test ■ Near point of convergence ■ Monocular accommodation	■ Eyes slowing ■ Eyes watering ■ Eyes reddening ■ Eyes moving in circular motions when tracking ■ Exacerbation of symptoms
Vestibular balance	■ Dynamic tandem gait, eyes open/closed, forward/backward	■ Steps off mid-line ■ Body sway ■ Patient’s arms up as compensation mechanism ■ Exacerbation of symptoms

Oculomotor and vestibular deficits are common following pediatric concussion.^{27,66,68,81,82} Accumulating evidence suggests visio-vestibular dysfunction on clinical examination at initial presentation following SRC is associated with an increased risk of prolonged recovery and the development of post-concussion syndrome (PCS).^27,64,81,82 A previous study has shown 81% of pediatric patients diagnosed with a concussion had a vestibular abnormality, either in balance or vestibular ocular reflex (VOR) on initial clinical examination, prolonging their return to school and full clearance for sports. ²⁸ As such, a comprehensive visio-vestibular exam is essential to identify deficits after concussion.^15,83,84

Balance function can be assessed by use of a dynamic tandem gait task, instructing a child to walk heel-toe in a straight line forward and backward with eyes open and closed. Children older than 5 years are developmentally capable of performing dynamic tandem gait tasks.^24,85 A recent study provided further insight into which components of the tandem gait task are most sensitive for discriminating concussed adolescents from healthy controls. In particular, the most sensitive tandem gait component was backward eyes closed and the most specific was forward eyes open. Despite technological advances, device-based metrics of balance were not found to be more discriminatory than the commonly used mBESS (part of the SCAT-5 tool) and dynamic tandem gait. ⁸⁶

It is important to recognize the importance of incorporating a comprehensive visual examination beyond visual acuity into concussion management as it may have implications in the return to learn (RTL) process.^{26,29,84,87-91} In a cohort of symptomatic concussed adolescents, 69% were found to have a vision diagnosis after concussion and 46% were diagnosed with more than one vision diagnosis. ²⁹ Similarly, a recent study in elementary school-aged children found younger children report visio-vestibular symptoms at similar rates seen in adolescents. ⁶⁶ Oculomotor function is composed of smooth pursuits, saccades, vestibulo-ocular reflex, near point of convergence, monocular accommodation, and visual motion sensitivity.^78,89 Eye tracking is composed of both smooth pursuits and saccadic eye movements. Smooth pursuits allow for the ability to follow a moving object and can be assessed by instructing a child to follow the provider’s finger as it moves between both the right and left visual fields in a progressively more rapid manner. Saccadic eye movements, the rapid simultaneous eye movements of both eyes in the same direction to fixate on a target can be assessed by instructing a child to move both eyes between two ends of a fixed target. The provider should look for coordination and fluency of both eyes. Normal function of the vestibulo-ocular reflex coordinates head movement with eye movement, in order to provide clear vision during motion, which aids in maintaining balance. It can be assessed by instructing a child to fixate both eyes on a stationary object while being instructed to shake their head in pitch (vertical) and yaw (horizontal) directions. ⁹² Vision motion sensitivity refers to the feeling of increased dizziness and sense of disorientation with visio-vestibular motions. Children may experience symptom burden when exposed to visually stimulating environments, such as school hallways or the mall.^78,93

Convergence is a binocular visual function and allows for the ability to bring a fixed target in toward one’s nose, while accommodative amplitude is the ability to focus on an object from a distance. Convergence and monocular accommodation can both interfere with the ability to focus near when reading, especially with fine print, leading to headaches, diplopia, eye strain, and loss of place while reading. Both can be assessed by use of a near point rule (Gulden Ophthalmics). Convergence varies in each child but a receded near point of convergence is considered to be greater than 6cm from the nose. ⁹⁴ Studies have shown adolescents with convergence insufficiency are more likely to have balance abnormalities ⁹⁵ and prolonged recovery after SRC.^81,95 It is critical to recognize the significance that these functions have in carrying out daily functions. Subtle dysfunction can prolong recovery rates ⁶⁹ and have major implications for difficulties with the return to learn process, academic performance ⁸⁴ and return to sport participation, especially fast paced-contact sports/collision sports.

The Use of Imaging

Conventional imaging is still a common practice for head injuries diagnosed within the emergency department setting; however, it contributes little to concussion evaluation unless there is concern for a more serious brain injury such as intracranial bleeding or a structural lesion. In recent years, improvements have been made to decrease imaging rates for closed head injuries within emergency departments through the development and implementation of Pediatric Emergency Care Applied Research Network (PECARN) pediatric imaging guidelines to limit the use of computed tomography (CT) and its potentially harmful ionizing radiation exposure in children,^96-98 as noted in the Centers for Disease Control and Prevention (CDC) Pediatric mTBI Guideline, ⁹⁹ however, many children still receive imaging, indicating that more progress is still needed.^96,97,100 Most commonly, CT is used acutely when a child presents with loss of consciousness, repeated emesis, worsening of symptoms, neurological decline, and severe mental status impairment^15,101 after a head injury. These imaging guidelines were developed to supplement a detailed history surrounding the mechanism of injury and clinical presentation to determine if imaging is necessary to rule out a more serious brain injury. Children who continue to have persistent symptoms and neurocognitive decline following their concussion, should be considered for an MRI, a more costly scan and one used outside of the emergency setting, to rule out any structural anomalies or neoplasm of the brain that could be responsible for the child’s symptoms and deficits. Studies have shown significantly low incidence of children who had radiological findings such as skull fractures after concussion; however, it is important to acknowledge that their presence could contribute to longer recovery rates and influence the return to play protocol for some children. ¹⁰²

While concussion has been classified as an “invisible” brain injury, multiple studies exploring various emerging imaging modalities have provided insight into acute changes (structural, physiological, and metabolic) after concussion and have been found to have the ability to discriminate between concussed and healthy controls.^103,104 In recent years, the use of diffuse tensor imaging (DTI), functional magnetic resonance imaging (fMRI), magnetoencephalography (MEG), spectroscopy, perfusion imaging, positron emission tomography (PET), single photon emission computed tomography (SPECT), functional near-infrared spectroscopy (fNIRS), transcranial doppler (TCD), and transcranial magnetic stimulation (TMS) in mTBI have been explored, but remain limited,^105,106 especially in the pediatric population. DTI is a promising technique for evaluating the subtle structural brain alterations after concussion, providing an indirect method of examining white matter axonal and myelination changes. fMRI studies have provided insight into the coupling between cerebral blood flow and neuronal activation, yet they cannot decipher the mechanism for uncoupling (hemodynamic vs neuronal). ¹⁰⁶ On the contrary, the use of MEG has allowed for direct millisecond temporal measurements of electrical neural activity during rest and cognitive tasks. ¹⁰⁶ PET and SPECT are detailed nuclear modalities, but less commonly used in concussion for fear of increased radiation exposure and cost of each scan. ¹⁰⁷ While these modalities provide assessment of detailed structural and physiological changes, they are expensive and inaccessible to most clinicians and health care systems. As a result, there has been increased research investigating the use of more portable modalities such as fNIRS, a noninvasive device measuring hemoglobin changes. Literature has shown indications of decreased brain activation after concussion detected by fNIRS in both adults^108,109 and adolecents. ¹¹⁰ An additional imaging modality, TCD, is a noninvasive ultrasound technique, detecting microvasculature changes and subsequent cerebral blood flow dysregulation. A recent study did not find sex-based differences in TCD results and symptom burden report. ¹¹¹ CT, MRI, and TCD imaging modalities have been found to be the most useful in the clinical setting, yet it is important to acknowledge that no single imaging modality is diagnostic for concussion. ¹¹² Unlike the previously mentioned imaging modalities, neuromodulation via TMS has the potential to alter neuronal activity by delivering targeted magnetic pulses to produce neuronal depolarization. In its limited use, one study has used TMS to explore cortical excitation and inhibition after pediatric mTBI and found it be safe and well tolerated in the pediatric population. ¹¹³ Neuroimaging holds promise for imaging biomarker use; however, further exploration and validation of these imaging modalities is still needed, specifically in children and adolescents. ¹⁰⁶

Assessing for Neurocognitive Deficits

Literature has long shown cognitive dysfunction to be a challenging sequela following pediatric concussion. While adults require cognition to perform their daily jobs, the daily job of a child or adolescent is to attend school and obtain an education. The quality of academic work after concussion often declines, specifically with persistent cognitive dysfunction in the domains of concentration, attention span, memory, processing speeds and abstract thinking.^114,115 Children and adolescents often report headaches, difficulty remembering, difficulty with concentration, fogginess, inability to keep up with schoolwork, difficulty with following directions and the inability to complete school assignments accurately or in a timely fashion. Neurocognitive function acutely can be effectively assessed by symptom burden and school performance acutely after pediatric concussion. Furthermore, several computerized neurocognitive tests have been developed and are commonly incorporated into sports team pre-injury testing for athletes, assessing baseline symptoms, memory, concentration, and reaction times; areas commonly altered after concussion. Multiple factors, such as loud testing environment, mood, sleep deprivation, ⁶² hunger, or pre-existing medical conditions such as ADHD^116,117 and learning disabilities can influence testing outcomes negatively, skewing results and as such, should not replace appropriate concussion evaluation by a trained professional.

The Use of Serum Biomarkers

With concussion care trends following a more individualized approach in recent years, there has been evolving research around the investigation of serum protein biomarkers and their utility in concussion diagnosis and management. A recent review highlighted the limited scope of knowledge on fluid-based biomarkers specifically for children, indicating the need for more research. ¹¹⁸ Several specific biomarkers have been highlighted for their potential diagnostic and prognostic abilities in children and adults^119-125; however, to date, there is no serological test to confirm a concussion diagnosis. In 2018, the FDA approved the Banyan Brain Trauma Indicator test, which detects proteins such as ubiquitin C-terminal hydrolase L1 (UCH-L1) and glial fibrillary acidic protein (GFAP) following head injury; however, these proteins are not specific to concussion, but rather indicative of which patients may have intracranial lesions or intracranial hemorrhage, requiring imaging studies. ¹²⁵ The spectrin N-terminal fragment (SNTF) biomarker has been found to be increased following SRC in adult hockey players ¹²² and an indicative marker of persistent neurocognitive dysfunction following concussion. ¹²¹ While these biomarkers show promise in diagnostic and prognostic contributions, investigations are still preliminary and none have significant use in the clinical setting for pediatric concussion. Furthermore, the time course and relevance of these biomarkers for the pediatric population is understudied.

Concussion Management

Concussion management in the pediatric and adolescent athlete is not a single protocol or a “one size fits all” approach, but rather a multidimensional and interdisciplinary process, with current practices revolving around five essential affected domains: somatic, visio-vestibular, cognitive, mood, and sleep.^{26,78,126-128} Understanding that some of these domains will overlap in symptoms, deficits and targeted rehabilitation as seen in Table 1 is essential to properly manage pediatric concussion.

The Role of Physical and Cognitive Rest

The traditional recommendation for acute concussion management is physical and cognitive rest. Acute treatment for concussion includes modifications of cognitive and physical activity with relative rest, specifically in the first few days if a heavy symptom burden is experienced. Acute rest allows for physiologic recovery after the metabolic mismatch of concussion and can prevent further symptom exacerbation. Current guidelines recommend rest for the first 24 to 48 hours following the injury^15,129; however, the optimal duration of cognitive and physical rest is still not fully understood, but it is thought to be likely dependent on each child. Advances have been made in exploring the optimal duration of rest and there is evidence of prolonged rest being associated with an increased symptom burden and prolonged recovery rates in the pediatric population.^130-132 A randomized trial in children and young adults who were seen in an emergency department showed a group randomized to strict rest for 5 days reported higher total symptoms scores over ten days and prolonged recovery rates compared to those randomized to only 2 days of rest. ¹³⁰ Similarly, a larger multicenter study found pediatric patients who began physical activity within 7 days reported decreased post-concussion symptoms compared with those who did not. ¹³³ A similar study found a few days of rest after a concussion, allowing symptom burden to decrease, is generally sufficient for most children and adolescents, followed by the gradual return to cognitive and physical activities. ¹³⁴ Physical and cognitive rest often involves time away from school and sports, which has the potential to be socially isolating and academically detrimental if not properly managed. ¹³⁵ In recent years, the pendulum for physical and cognitive rest has swung from isolating children and adolescents in dark rooms for weeks at a time to the gradual return to activities and school as soon as tolerated. It is important to recognize that, while the use of guidelines is helpful in acute management, some children will require a longer rest period due to symptom burden acutely following concussion and the management plan should be individualized.

Aerobic Exercise

Aerobic exercise appears to play a significant role in the pathophysiology of autonomic function by improving cerebral flow regulation.^{67,74,76,136-138} Literature has shown evidence for the ability of controlled, graded subsymptom threshold, submaximal aerobic exercise in facilitating the recovery process after concussion by decreasing concussion symptom burden and improving recovery times.^{114,133,136,137,139-141} As examples of targeted rehabilitation with aerobic exercise, the Buffalo Concussion Treadmill Test (BCTT)^136,140-142 or Buffalo Concussion Bike Test (BCBT) ¹³⁸ are safe, well tolerated, graded exertion exercise tests, to identify autonomic and cerebral blood flow dysregulation. Studies have shown heart rate thresholds to be significantly lower in patients with prolonged recovery rates.^136,141 There is evidence that early controlled exercise does not adversely affect recovery,^137,142-144 but the role and exact timing of exercise introduction in the acute management of SRC is still not completely understood. Recent studies have provided evidence that adolescent athletes who exercised within days of injury recovered significantly faster than those who did not exercise or were prescribed a stretching prescription.^136,137 Controlled aerobic exercise has been found to accelerate return to school, decrease symptom burden, and improve psychological state. ¹⁴³

Return to Play

Return to play (RTP) varies tremendously in pediatric sport participants and must be an individualized process. Guidelines for RTP have been defined by the 5th International Conference on Concussion in Sport. ¹⁵ Readiness for return to play should be based on the physician’s discretion, assessing the athlete’s tolerance of exercise and targeted clinical examination findings. If persistent deficits in the visio-vestibular exam or gait assessment are noted, athletes should not be permitted to return to sports due to the increased risk of a subsequent concussion^11,127,145 or musculoskeletal injuries. ¹⁴⁶ Studies have shown the pediatric population experiences a longer recovery period compared with collegiate athletes, hence a conservative approach should be taken when making return to play decisions and assessing the younger athlete’s readiness to return to sport.^18,23

Current RTP recommendations from the 5th International Conference on Concussion in Sport¹⁵ support a graduated stepwise program. The 6-step RTP process involves the following: step 1—symptom limiting activities that do not provoke symptoms with the goal of reintroduction of school activities; step 2—light aerobic activity, i.e., walking or cycling on a stationary bike; step 3—sport-specific activities (no head impact activities), i.e., running; step 4—noncontact activity, i.e., drills and heavy resistance training; step 5—full contact practice following medical clearance; and step 6—full return to sport and normal game play. ¹⁵ Athletes should not be allowed to return to high-risk activities, contact or collision sports until the RTP process is completed successfully under the supervision of a trained professional. The student athlete may begin to advance through the 6-step RTP process once symptom-free, with one step completed every 24 hours as tolerated. If concussion-related symptoms occur during the stepwise advancement, the athlete should return to the previous asymptomatic level and re-attempt progression after being symptom-free for 24 hours on the previous step. ¹⁵

All 50 states have RTP laws ⁵⁰ ; however, it is important to recognize that they may not typically apply to younger children who do not play interscholastic sports. ¹⁴⁷ These students likely engage in recreational play and may participate in organized recreational or club sports outside the scholastic setting and thus, RTP decisions should still be considered for this young population.^14,66

It is important to recognize that a subset of athletes will suffer from persistent symptoms. While these patients may lack the readiness to participate in formal sports/contact sports, light aerobic exercise or activities with low risk for repeat injury as tolerated should be permitted once they are outside of the vulnerable acute post-injury phase. ⁹ As discussed earlier, exercise has been shown to decrease persistent concussion symptoms and decrease recovery time following concussion.^140,142,148 As prolonged inactivity has been shown to result in a higher symptom burden and prolonged recovery rates, limiting youth from safe, low-risk aerobic physical activities can be isolating for children during the recovery process.^130,132

Return to Learn

It is common for children and adolescents to experience difficulties with school re-entry following a concussion due to symptom burden.^135,149,150 Most children look physically normal after concussion, which belies the underlying neurologic dysfunction. Therefore, it is important to appreciate the importance of gradually returning the student into academics, even while still symptomatic. Concussion symptoms, visio-vestibular function, concentration, memory, and cognitive stamina all play a role in the challenges of the return to learn (RTL) process, as they may negatively affect school performance and should be considered when developing an academic accommodation plan.^{78,114,149,151} For example, saccadic dysfunction or convergence insufficiency may impede the child’s ability to return to full school workload (reading, taking notes in class, test taking) while vestibular deficits may prevent a child’s ability to tolerate a loud, busy school environment. ⁷⁸ Initially, the goal of school re-entry and RTL should be a gradual return to cognitive load. The student athlete should aim to attend essential classes as tolerated, slowly increasing time at school, progressing to full days and full academic load. School accommodations should be individualized and tailored to symptom burden and deficits experienced by the student and may include, but are not limited to, a limited number of classes, focusing on core subjects, preprinted school notes with a larger font size to minimize eye tracking and visual fatigue, extra time for tests/assignments and breaks for visual fatigue or symptom exacerbation. ⁷⁸ The clinician managing the child’s care should work closely with school personnel (i.e., school nurse, guidance counselor) to develop a plan that works for the student in the context of their particular school environment and needs.

Return to Drive

The leading cause of adolescent death in the United States is attributed to motor vehicle crashes. ¹⁵² Driving is a cognitively demanding task, requiring concentration, adequate reaction times and proper visual function, specifically eye tracking. These cognitive and visual function demands required for safe driving can commonly be altered following concussion. This is particularly concerning for young drivers for whom crash risks are great.^153-155 Previous studies have shown deficits in concentration, memory, processing speeds, and subsequent delayed reaction times to be common among adolescents after concussion.^156-158 These neurocognitive deficits and symptom burden in concussed adolescents can lead to suboptimal execution of driving. Furthermore, symptom burden, specifically light sensitivity, noise sensitivity, fatigue, sleep disturbances, ⁶² headaches, and nausea can pose challenges in driving for the adolescent, further affecting the driving task. RTL and RTP protocols have been developed to assist re-entry back into cognitively demanding environments such as school; however, there is a lack of return to drive protocols and this subject warrants further investigation.

Addressing Persistent Symptoms and Deficits

Children and adolescents generally recover from a concussion with a resolution of symptoms within four weeks.^5,159,160 In situations where symptoms and deficits persist, delaying recovery, it is recommended that the student athlete seek evaluation by a sports medicine physician or a physician with experience in managing pediatric SRC. About 30% of children and adolescents will exhibit persistent symptoms and deficits beyond the natural 3- to 4-week recovery period and will benefit from rehabilitation guided by a qualified physician.^5,161-163

Vision and Vestibular Therapy

The vestibular and visual systems are closely interconnected and dysfunction commonly persists in both systems after concussion. Persistent symptoms and deficits will commonly benefit from individualized and targeted vestibular therapy under the supervision of a trained physical therapist in vestibulopathies. ¹⁵ The main goal of therapy is patient-tailored vestibular exercise, aiming to re-establish the integration of the vestibular and visual systems necessary for daily function and sport participation, specifically fast-paced contact or collision sports.^164-166 Physicians treating children still experiencing symptoms and visio-vestibular deficits four weeks after concussion should consider referral to vestibular rehabilitation. Vestibular rehabilitation has historically been used for treatment of vertigo or motion sickness in adults and, more recently, has been used as a therapeutic intervention for vestibular symptoms and deficits following concussion.^92,167-171 Vestibular rehabilitation commonly consists of a customized therapy program targeting the use of specific exercises to improve dizziness, visual deficits, and balance function. Therapy should begin with the child receiving an initial evaluation to assess specific visio-vestibular system deficits, allowing the therapist to choose targeted therapeutic exercises for the child’s customized therapeutic rehabilitation program. Rehabilitation targets eye coordination and balance function, to improve habituation to motion stimuli in order to decrease symptom burden related to visio-vestibular deficits, specifically dizziness and headache. Each session is targeted at progression, safely increasing the difficulty of each exercise to gradually return the child to pre-injury function levels.

A subset of children and adolescents may require additional referral for vision rehabilitation for persistent visual symptoms and deficits. Trained developmental optometrists assess visual function and develop a customized neuro-optometric rehabilitation program. ⁹⁴ The American Optometric Association defines vision therapy as a sequence of neurosensory and neuromuscular activities individually prescribed and monitored by the doctor to develop, rehabilitate, and enhance visual skills and processing. ¹⁷² Following concussion, eye movements, convergence and accommodative amplitude are common targets for vision rehabilitation, which retrains the visual system to return the child to baseline visual function improving speed, accuracy and oculomotor functions. Research has shown binocular vision rehabilitation improves convergence in adults suffering from mTBI.^94,166,173 Similarly, recent data from adolescents showed improvement in convergence and accommodation with the utilization of vision rehabilitation as an intervention for common vision disorders after pediatric concussion.^87,94

Neuropsychological Intervention and Cognitive Therapy

Students who continue to experience persistent symptom burden, cognitive decline, and behavioral or emotional concerns beyond 4 weeks after injury may benefit from a formal neuropsychological evaluation by a trained neuropsychologist. Pediatric neuropsychologists are trained in assessing, diagnosing, supporting, and rehabilitating children with cognitive, learning, neurological, or psychiatric disorders. Neuropsychological evaluations consist of cognitive testing and a psychological evaluation. ¹⁷⁴ Commonly, a detailed clinical interview is performed followed by questionnaires, pencil and paper or computerized cognitive function testing, and validity testing.^174,175 Information gathered from these evaluations determines a child’s strengths and/or areas in need of improvement. Rehabilitation is achieved through the development of individualized and targeted strategies for the child to return to daily functions and school successfully.

When school re-entry with the use of accommodations is not sufficient for return to full cognitive workload, specifically with difficulties in concentration, following directions and memory, the pharmacological use of neurostimulants, i.e., methylphenidate, may be indicated.^78,176 A 2-year study found the use of methylphenidate to improve cognitive outcomes after TBI in adults ¹⁷⁷ ; however, its use in pediatric concussion is still not fully understood. Furthermore, in some circumstances, children and adolescents may benefit from the addition of formal cognitive occupational therapy or speech therapy interventions incorporated into their individualized rehabilitation. Occupational therapy rehabilitation is commonly used to improve patient outcomes in adults ¹⁷⁸ ; however, its use in pediatric concussion is still limited.

Persistent Mood Dysfunction

Assessment of emotional functioning is critical following pediatric concussion and should not be overlooked. Children and adolescents will commonly experience acute temporary symptoms associated with mood, such as irritability, sadness, nervousness, anger, or feeling more emotional during the recovery process. The subset of youth with persistent post-concussion symptoms often experience anxiety ¹⁷⁹ and depressed mood long term.^32,162,180 One third of adolescents up to a year following concussion experience anxiety. ¹⁸¹ Furthermore, research suggests that approximately 20% of collegiate athletes experience an increase in depressive symptoms after concussion, compared to 5% in a healthy control group. ¹⁸² A similar study found 50% of adolescents reported at least one mood symptom after SRC and one in ten met criteria for a post-injury psychiatric diagnosis after SRC. ³³

Successful management of youth suffering from mood dysfunction requires prompt recognition and multidisciplinary care by experts with clinical training in concussion, psychology, and/or psychiatry. If a child or adolescent screens positive for a mood dysfunction, incorporating a discussion about appropriate support systems with the child and parents is warranted. Psychological intervention, ¹⁸³ in the form of a school psychologist or formal therapy, may be necessary for children to cope with mood dysfunctions as well. ¹⁵ In addition, the use of exercise has been demonstrated to improve mental health outcomes for individuals suffering from depression, anxiety and stress and may be helpful in this population.^163,182 When psychological interventions are not sufficient, pharmacological interventions may be warranted as a second-line treatment option. A study in adults found those treated for depression immediately after concussion had significantly fewer follow-up visits for persistent symptoms, compared to those without pharmacological interventions. ¹⁸⁴

Centers for Disease Control and Prevention Pediatric Mild Traumatic Brain Injury Guideline

As previously discussed, pediatric concussion is complex and requires a multidisciplinary approach to provide optimal care for children, given its variability in presentation, management, and rehabilitation. To address this variability and unify concussion management standards, the CDC developed a pediatric mTBI guideline for providers managing pediatric concussion.^99,185 The CDC National Center for Injury Prevention and Control Board of Scientific Counselors, a federal advisory committee, established a Pediatric Mild Traumatic Brain Injury Guideline Workgroup, comprised of leading experts in the field of traumatic brain injury, to help develop the guideline.

The workgroup drafted recommendations based on the evidence that was obtained and assessed via a systematic review, as well as related evidence, scientific principles, and expert opinion. This information included selected studies published since the evidence review was conducted that were deemed by the workgroup to be relevant to the recommendations. The dates of the initial literature search were January 1, 1990, to November 30, 2012, and the dates of the updated literature search were December 1, 2012, to July 31, 2015.

The resulting evidence-based clinical care guideline on pediatric mTBI is designed for use in primary care and emergency settings. Studies have shown the most common points of entry into a healthcare system for a pediatric concussion evaluation to be these two settings^186,187 depending on the age of the child. The guideline was developed using a modified Grading of Recommendations, Assessment, Development and Evaluations (GRADE) methodology based on scientific literature published over a 25-year period (for all causes of pediatric mTBI).^99,185 It consists of 19 sets of clinical recommendations targeting diagnosis, prognosis, management and treatment of pediatric mTBI based on current evidence. Recommendations (most of which are reflected in this article) address the use of imaging and serum markers, assessment tools and prognosis, symptom scales, importance of a past medical history and previous concussion history, patient and family education, role of physical and cognitive rest, psychosocial and emotional support, return to school, and management of impairments that may occur following pediatric concussion.^99,185 Key recommendations can be seen in Table 4. The complete CDC Pediatric Mild Traumatic Brain Injury Guideline can be found on the CDC website at: https://www.cdc.gov/traumaticbraininjury/PediatricmTBIGuideline.html.

Table 4.

Centers for Disease Control and Prevention Pediatric Mild Traumatic Brain Injury (mTBI) Guideline Key Recommendations ⁹⁹ .

1. Do not routinely image patients to diagnose mTBI.

2. Use validated, age-appropriate symptom scales to diagnose mTBI.

3. Assess evidence-based risk factors for prolonged recovery.

4. Provide patients with instructions on return to activity customized to their symptoms.

5. Counsel patients to return gradually to non-sports activities after no more than 2-3 days of rest.

Conclusion

Diagnosis and management of pediatric sports-related concussion continues to evolve as advances continue, providing a better understanding of neurophysiological and neurobiological underpinnings of concussion and improving patient outcomes. Concussion management in the pediatric and adolescent population is unique and complex, requiring an approach that evaluates multiple domains. Initial assessments should be targeted, assessing the following core domains of concussion: somatic, visio-vestibular, cognitive, mood, and sleep. Effective management relies heavily on proper evaluation and appropriate, tailored rehabilitation of deficits in these domains. Emerging evidence points to the value of aerobic, vestibular and vision therapy and strategies to address persistent symptoms of cognitive and mood dysfunction. The goal of concussion management of pediatric student athletes is to return them to daily functions and academics, as well as potentially high-risk contact or collision sports, adding an additional layer of complexity to care. To help manage and organize the complexity of youth concussion management, the CDC developed the Pediatric Mild Traumatic Brain Injury (mTBI) Guideline consisting of 19 sets of clinical recommendations that cover diagnosis, prognosis, and management and treatment. These recommendations can be translated into local action plans implemented within health networks, school systems and athletic teams and leagues to ensure that, as concussion injuries occur, they are properly diagnosed, managed, and rehabilitated to ensure optimal safety and health outcomes for pediatric student athletes.