Office-based concussion evaluation, diagnosis, and management: pediatric

Office-based concussion evaluation, diagnosis, and management: pediatric

Handbook of Clinical Neurology, Vol. 158 (3rd series) Sports Neurology B. Hainline and R.A. Stern, Editors https://doi.org/10.1016/B978-0-444-63954-7...

244KB Sizes 0 Downloads 60 Views

Handbook of Clinical Neurology, Vol. 158 (3rd series) Sports Neurology B. Hainline and R.A. Stern, Editors https://doi.org/10.1016/B978-0-444-63954-7.00011-2 Copyright © 2018 Elsevier B.V. All rights reserved

Chapter 11

Office-based concussion evaluation, diagnosis, and management: pediatric HUGO PAQUIN1*, ALEX TAYLOR2, AND WILLIAM P. MEEHAN III3 Division of Pediatric Emergency Medicine, CHU Ste-Justine, Montreal, QC, Canada

1 2

Division of Neurology and Psychiatry, Boston Children’s Hospital, Boston, MA, United States 3

Division of Sports Medicine, Boston Children’s Hospital, Boston, MA, United States

Abstract More children and adolescents are participating in competitive sports than ever before, causing an overall increase in sport-related injuries. Concussion is a common injury in the pediatric population and its prevalence has increased with increased visibility and awareness. This chapter will discuss the clinical presentation, evaluation, and management of concussions sustained by pediatric athletes, while addressing the distinctive factors that pertain to this population. Management of concussion should be tailored to patients’ symptoms and should focus on an early and gradual return to both cognitive and noncontact low-risk physical activity. A multidisciplinary approach is often helpful in addressing more specific symptoms, which fall into the somatic, cognitive, vestibular, emotional, and sleep domains. A prolonged recovery is defined by symptoms lasting more than 4 weeks. Individualized return-to-play decisions should focus on the safety of the young athlete.

INTRODUCTION More children and adolescents are participating in competitive sports than ever before, causing an overall increase in sport-related injuries. Contact and collision sports, which have the highest incidence of concussion, are most commonly played by athletes under 19 years old (Gessel et al., 2007). With the increased awareness of concussion, in part due to increased media coverage, the numbers of patients with concussion presenting for care have increased substantially. In the United States, nearly half of the 1.2 million patients presenting to an emergency department, and 800,000 of those presenting to outpatient clinics with minor brain injury annually, are below 18 years old (Mannix et al., 2013). Between 2007 and 2013, pediatric healthcare visits for concussion and minor head injury increased more than fourfold (Taylor et al., 2015).

This chapter will discuss the clinical presentation, evaluation, and management of concussions sustained by pediatric athletes, addressing their distinctive factors.

HISTORY The presentation of concussion can be variable (McCrory et al., 2013) and its symptoms are nonspecific (Grady, 2010). Thus, the medical history is essential for establishing the diagnosis. Multiple assessment tools have been developed to guide the physician in collecting key elements of the concussion history and are available online (Gioia, 2012; CDC, 2016). Obtaining information from parents, teachers, and coaches may help clarify the history.

Mechanism As with any other trauma, clarifying the mechanism of the injury is important. Concussion results from trauma,

*Correspondence to: Dr. Hugo Paquin, Division of Pediatric Emergency Medicine, CHU Ste-Justine, 3175 Chemin de la C^ oteSainte-Catherine, Montreal (Qc) H3T 1C5, Canada. Tel: +1-514-972-2688, Fax: +1-514-345-2358, Email: [email protected]

108

H. PAQUIN ET AL.

most often to the head, although forces transmitted to the brain from blows delivered elsewhere on the body can result in a concussion (Master and Grady, 2012; McCrory et al., 2013). Characteristics of associated factors, such as height of fall, speed of impact, surface/object of collision, safety devices used, loss of consciousness, immediately evident bleeds or lacerations, and seizures, should be determined (Wing and James, 2013). It is important to record the date of injury, as the duration of symptoms may factor into future return-to-play decisions. In the case of recurrent concussions, the force of injury should be assessed, as a trend of concussions resulting from diminishing forces may also factor into return-to-play decisions.

Signs and symptoms Typical signs and symptoms of concussions are included in the Post-Concussion Symptom Scale, a widely used tool for diagnosing and monitoring concussion (Pardini et al., 2004; McCrory et al., 2017). Symptoms can be categorized in five general domains: somatic, vestibular, cognitive, emotional, and sleep. Asking directed questions to patients and their families is necessary to determine the presence of these symptoms, specifically in pediatric athletes who may be unaware their symptoms are due to a concussion or reluctant to report them even given potential consequences (McCrea et al., 2004; Karlin, 2011; Kerr et al., 2014). Occasionally, a young athlete will present with symptoms commonly observed in concussions, but without a clear mechanism. If there is no clear mechanism of injury, other etiologies, such as a primary headache disorder, mood disorder, or attention deficit disorder, should be sought and treated appropriately. Still, the physician may wish to be conservative in evaluating these patients, recommending removal from contact and other high-risk activities, and advising on return-to-play decisions to avoid additional injuries, worsening or prolonging symptoms, or placing the athlete at risk for second-impact syndrome. Furthermore, the expected course of a concussion should be one of gradual improvement. Steadily increasing symptoms should raise concern for other potential etiologies or psychosocial factors that may be complicating recovery.

SOMATIC SYMPTOMS Somatic symptoms are initially the most prevalent, with headaches very commonly reported following concussion. Other migraine-like symptoms may also be reported, such as nausea, vomiting (early), and sensitivity to light or noise, as well as neck pain. Among adolescent athletes, those with a high initial somatic symptom burden are more likely to have symptoms that persist beyond 28 days postinjury (Howell et al., 2016b).

VESTIBULAR SYMPTOMS Vestibular symptoms associated with concussions include dizziness, imbalance, and visual problems. Balance instability may be secondary to damaging the vestibular system in a concussion (Moran et al., 2015), and is most often evident in the early postinjury period (Guskiewicz et al., 2001; Hanson et al., 2014). More recently, visual complaints have been described in pediatric patients with concussion (Corwin et al., 2015). Such complaints, including blurred or double vision, eye fatigue, reading difficulties, and difficulty sustaining attention on a visual task, may particularly affect the student-athlete because of the amount of reading and visual tasks involved in schoolwork (Master et al., 2016). In a recent study involving 100 teenagers with a concussion, 69% had one or more of the following vision diagnoses: accommodative disorders (51%); convergence insufficiency (49%); and saccadic dysfunction (29%). In all, 46% of patients had more than one vision diagnosis (Master et al., 2016). Causes of posttraumatic dizziness include benign paroxysmal positional vertigo, central vestibular and/or peripheral vestibular dysfunction, neuro-ophthalmologic disorder, and proprioceptive dysfunction (Schneider et al., 2014). The Convergence Insufficiency Symptom Survey is a tool to assist in diagnosing these disorders in patients who have had a concussion (Borsting et al., 2003; Master et al., 2016).

COGNITIVE SYMPTOMS Given the high cognitive demands placed on studentathletes, it is not surprising that cognitive symptoms may be debilitating. Cognitive symptoms include impaired concentration or attention, memory deficits, and decreased executive function (Moran et al., 2015). Patients report difficulty thinking, concentrating, or remembering, in addition to confusion and feeling mentally foggy or slowed down. These symptoms may not be obvious at onset of diagnosis, but may appear as the patient returns to a learning environment.

EMOTIONAL SYMPTOMS Mood disruption is also frequently reported, with symptoms such as being more emotional, irritable, sad, anxious, or even depressed. Elevated levels of depression and anxiety among athletes following concussion are well reported (Kontos et al., 2012; McClain, 2015). The fear of school failure and the need for accommodations is an important source of worry for these children (Sady et al., 2011). Preinjury somatic symptoms are known to contribute to recovery (Nelson et al., 2016). Interestingly, emotional symptoms seem to play a larger role as recovery progresses, whereas somatic symptoms

OFFICE-BASED CONCUSSION EVALUATION, DIAGNOSIS, AND MANAGEMENT: PEDIATRIC 109 seem to decrease as recovery progresses, suggesting that, in some cases, emotional symptoms may be due to the restrictions based on activities or other factors as opposed to the pathophysiology of concussion itself (Eisenberg et al., 2014).

SLEEP SYMPTOMS Sleep disturbance is a common consequence of traumatic brain injury (Harmon et al., 2013; Phillips and Woessner, 2015). Patients may complain of either increased or decreased amounts of sleep, in addition to poor sleep quality. They may describe a delayed sleep phase, where the initiation of sleep is significantly later than the desired sleep time. This results in sleep latency, when the amount of time between lying down to sleep and falling asleep is longer than the normal 30 minutes. Sleep disturbances are important to address since they may also impact recovery and worsen other symptoms.

Potential indications for imaging Since concussion cannot be visualized on standard neuroimaging, routine imaging is not recommended. Imaging is indicated, however, when the clinician is concerned for a skull fracture or acute intracranial hemorrhage after a high-impact injury (Master and Grady, 2012), or when either the history or physical examination points to another potential cause of the athlete’s symptoms. A prediction rule to reduce the number of computed tomography (CT) scans in children older than 2 years old was developed by the Pediatric Emergency Care Applied Research Network (PECARN), and is meant to be applied in emergency department settings (Kuppermann et al., 2009). Two algorithms based on age separate patients in three categories: high-, intermediate-, or low-risk. A CT scan is recommended for high-risk patients, and no imaging for low-risk patients. The intermediate risk category suggests an observation period or a CT scan based on shared decision making and other external factors.

Prior concussions Obtaining a complete history of past concussions and their recovery time gives the clinician important information, including whether a patient had prior prolonged recovery or required medications or specific therapies. The ultimate number of concussions is one factor considered when making return-to-play decisions but no evidence-based protocol exists for these decisions as they are often multifactorial. Moreover, parents and patients may recollect undiagnosed events when a complete concussion history is taken.

Premorbid conditions Premorbid conditions, such as migraine headaches, attention deficit disorder, sleep disturbances, depression, anxiety, and other mood disorders, are associated with both symptoms and symptom duration after a concussion (Kutcher and Eckner, 2010). Given the importance of school in the pediatric athlete’s life, the presence of other conditions such as dyslexia, learning disability, amblyopia or strabismus, or other reading or visual tracking disorders should be determined, given their likely impact on functioning (Master and Grady, 2012; McCrory et al., 2013).

PHYSICAL EXAMINATION A thorough neurologic examination should be performed at the initial visit. The presence of focal neurologic deficits should prompt consideration of other potential etiologies and consideration of neuroimaging. While a gross neurologic screening examination will often be normal, deficits in coordination may be observed. Postural instability is common and can be detected by simple clinical tests such as the Balance Error Scoring System (Guskiewicz et al., 2001; McCrea et al., 2013). This test involves placing the patient in three different positions: double-leg stance; single-leg stance on the nondominant leg; and tandem stance with eyes closed and hands on hips for 20 seconds. An error is recorded each time athletes lift their hands off their hips, open their eyes, step, stumble, fall, remain out of the test position for more than 5 seconds, move hips into more than 30° of flexion or abduction, or lift their forefoot or heel. (Guskiewicz et al., 2001; Hanson et al., 2014) (see Chapter 8). For younger patients, having them perform heel–toe tandem gait forward and backward with eyes open and closed may be an alternative, with each variation adding a level of difficulty in maintaining balance. The physician should then be looking for truncal sway, wider-based gait, frank gait instability, rising of the arms, or full inability to perform a tandem gait (Master and Grady, 2012). Because of the increased incidence of vestibuloocular dysfunction, the physician should attempt to screen for such deficits. A vestibulo-ocular screen evaluates for nystagmus, saccades, vestibulo-ocular reflex, smooth pursuits, gaze stability, and convergence or accommodative insufficiency (Master and Grady, 2012). A study using a brief Vestibular Ocular Motor Screening assessment showed that this tool accurately distinguished pediatric patients (9–18 years old) with concussion who had symptoms of oculomotor impairment from uninjured controls (Mucha et al., 2014; Master et al., 2016). Smooth-pursuit evaluation may

110

H. PAQUIN ET AL.

cause concussed patients to become symptomatic, with the inability to track the examiner’s finger due to headaches, dizziness, or eye fatigue. Tearing may be seen in symptomatic patients, as well as jerky and interrupted eye movements. Similarly, vertical and horizontal saccade evaluation may show slowing, interruption, or circular tracking as opposed to sharper saccades. These deficits may well be associated with reading and school difficulties. Gaze stability evaluation should also attempt to generate the patient’s symptoms while the individual is performing the maneuver. Finally, convergence deficiency is shown by having a convergent point higher than the normal range, between 4 and 6 cm (Master and Grady, 2012). Evaluating the cervical spine is important, to rule out possible associated injury, but also to determine the contribution of cervical findings to the patient’s symptoms. Evaluation should include range of motion, which can be limited in the presence of a spasm or clinical concern of unstable injury. Part of the cervical evaluation should focus on the occipital nerve region, as tenderness at this region may lead to a diagnosis of occipital neuralgia or cervicogenic headaches (Dubrovsky et al., 2014).

MANAGEMENT Initial visit The first step in assessing patients with a possible concussion is to ensure their safety by identifying any associated unstable or emergent issues and addressing them appropriately. The initial management of concussions begins with removal from risk of additional trauma to the head and relative cognitive and physical rest for 48 hours (Master and Grady, 2012; McCrory et al., 2013, 2017). This brief period of rest represents a change from previous consensus recommendations. More strict rest for adolescents immediately after concussion offers no added benefit and may result in more severe and longer-lasting symptoms (Thomas et al., 2015). Complete rest until symptoms resolve is no longer recommended, as prolonged rest may predispose an individual to fatigue, depression, deconditioning, and disruption of cerebral blood flow regulation (Leddy et al., 2013; Tan et al., 2014). Therefore, most recent recommendations are to gradually resume nonrisk, noncontact physical activity, and cognitive activity after a brief period of rest (McCrory et al., 2017). Maintaining adequate hydration and nutrition will provide the energy sufficient for brain recovery, and limiting variations in blood pressure which can arise from orthostatic changes or dysautonomia following mild traumatic brain injury. For similar reasons, maintaining good sleep hygiene is important; sleep is not only restorative, but inadequate sleep may worsen symptoms of all

domains (Harmon et al., 2013; Garcia-Rodriguez and Thomas, 2014). Initial symptomatic care may involve the use of over-the-counter medications such as acetaminophen or ibuprofen, although many athletes do not find these medications helpful. More simple suggestions may also involve wearing sunglasses or earplugs for light and noise sensitivity. The avoidance of triggers should also be emphasized throughout recovery. Patients with a concussion should avoid alcohol consumption and narcotic pain medications after injury, because these medications themselves are associated with side-effects that may exacerbate concussion symptoms and their use may make it difficult to monitor and evaluate postconcussive symptoms.

COGNITIVE REST AND RETURN TO LEARN School-aged athletes are unique because their cognitive function is constantly being assessed and tested in school. Furthermore, their cognitive performance is graded, which can become part of their permanent academic records. Therefore, there is potential for greater secondary consequences of concussions sustained by children, which can be a source of great anxiety (Ewing-Cobbs et al., 2004; McCrory et al., 2004; Kirkwood et al., 2006). When discussing return-to-learn plans with patients and families, it is important to stress that cognitive activity is safe; symptoms may transiently increase with cognitive activity, but should return after breaks or periods of rest. Stages of “return to learn” have been suggested, consisting of a limited period of nonacademic activity at home, a limited period of academic work at home, partial school days with accommodations, full-day attendance with accommodations, and then removal of accommodations (DeMatteo et al., 2015). To support patients in returning to school, adequate documentation should be provided for school teachers and administrators (Arbogast et al., 2013). Indeed, written documentation removes the patient from academic decisions and puts the responsibility on the physician, who becomes an advocate for the patient’s recovery. Examples of accommodations include allowing written notes to be given to patients prior to class, allowing them breaks during class, allowing them more time to complete tests or assignments, and limiting or delaying scheduled examinations.

PHYSICAL REST AND RETURN-TO-PLAY DECISIONS Historically, a gradual return-to-play protocol was started in pediatric athletes only after all symptoms had fully resolved. Recent studies suggest that early initiation of nonrisk, noncontact physical activity is not detrimental to recovery and may hasten recovery. As the student progresses into the subacute healing phase, gradual

OFFICE-BASED CONCUSSION EVALUATION, DIAGNOSIS, AND MANAGEMENT: PEDIATRIC 111 reintroduction of well-supervised activity, even while symptomatic, may be appropriate as long as it does not exacerbate symptoms (Grady, 2010). Studies support this concept of permissive low-intensity, subsymptom exacerbation threshold exercising during the subacute phase, even while the patient is still symptomatic (Gagnon et al., 2009; Leddy et al., 2010; Howell et al., 2016a). Thus, after a period of rest, children and adolescents should be encouraged to participate in both cognitive and physical activity to a level that is tolerable and does not significantly worsen symptoms. Studies have found better concussion outcomes in recovering patients who were neither too underactive nor too overactive (Majerske et al., 2008; Brown et al., 2014; Gioia, 2015; Grool et al., 2016; Howell et al., 2016a;). As with a returnto-learn protocol, providing clear documentation for school teachers, athletic trainers, and coaches through a return-to-play protocol will support the patients in transitioning back to activity. The widely accepted Zurich and Berlin guidelines include a return-to-play protocol (McCrory et al., 2013, 2017) that progresses the athlete through six stages for a safe return to activities. From no activity or physical rest, the athlete then progresses to light aerobic exercise, moderate levels of sport-specific exercise, noncontact training drills, full-contact practice, and normal game play. Patients should be completely asymptomatic and should have achieved baseline functioning on all domains tested prior to the injury before returning to contact or collision sports.

Ancillary testing NEUROPSYCHOLOGIC EVALUATION Neuropsychologic evaluation yields data pertaining to cognitive, social, and emotional functioning to characterize brain–behavior relationships. Carefully interpreted, such data help to identify injury and noninjury-related factors that may contribute to neurocognitive dysfunction, and other commonly reported postconcussion symptoms. Findings also inform treatment plans that assist clinicians in making recommendations for safely returning school-age children to academics and sports. As such, neuropsychologic evaluation is a clinically useful tool for managing pediatric patients with concussion. Previous investigations indicate reduced neuropsychologic function immediately following injury. The areas identified as most vulnerable to injury include attention and executive function (e.g., speed of processing), new learning and memory, and reaction time. Primarily, decrements in these areas are thought to reflect brain dysfunction, which can occur even without selfreported symptoms (Fazio et al., 2007). Detecting dysfunction in pediatric patients is particularly important

because the developing brain may be more susceptible to reinjury during the acute recovery phase. Further, younger children may recover more slowly and be at risk for greater secondary effects, including academic and social stress.

MODELS FOR ASSESSMENT Different models of neuropsychologic assessment exist. In general, the model is determined by the phase of recovery: acute (3 days postinjury); subacute (4–30 days postinjury); prolonged or chronic (30 + days) (Kirkwood et al., 2008; McCrea et al., 2009). Acute Symptoms occurring in the hours or days following concussion preclude extensive neuropsychologic assessment and usually serve as the basis for initial management recommendations. Nonetheless, research supports the use of brief cognitive screens (e.g., Sport Concussion Assessment Tool) for diagnostic clarification and to help determine injury severity (McCrory et al., 2017). Subacute Neuropsychologic recovery typically parallels selfreported symptoms, with most individuals reporting spontaneous recovery in 7–10 days. However, several studies have indicated that subtle neurocognitive deficits may extend beyond self-reported symptoms and balance dysfunction (Belanger and Vanderploeg, 2005; Iverson et al., 2006; Broglio et al., 2007a; Fazio et al., 2007). As a result, an increasing number of organizations use neuropsychologic assessment to manage sport-related concussions, including obtaining preseason or “baseline” measures of function. This model allows athletes to serve as their own control and aids interpretation of data in light of pre-existing or contextual factors that may impact performance. A score significantly lower than baseline indicates ongoing dysfunction, whereas recovery is assumed when performance is comparable to preinjury levels. If no baseline data are available, results are compared to a normative sample of age-related peers. Because the cost and availability of trained neuropsychologists are prohibitive, computer- administered neurocognitive tests are frequently used. These allow entire teams to be tested in one session. Most programs offer several alternative forms, improving reliability with serial administrations. In addition, computerized assessment may provide a more accurate measurement of reaction time and speed of information processing. Conversely, some studies have raised concerns about the psychometric properties of computerized measures, particularly their test–retest reliability (Barr, 2001;

112

H. PAQUIN ET AL.

Randolph et al., 2005; Broglio et al., 2007b; Kirkwood et al., 2009). Further, there are currently no data demonstrating improved clinical outcomes or risk reduction with baseline testing (Randolph, 2011). Nonetheless, most experts support the use of neuropsychologic assessment in the management of sport-related concussion.

Prolonged/chronic symptoms The purpose of neuropsychologic assessment for patients with chronic symptoms after a concussion is to provide the referring clinician and patient with additional insight into injury and noninjury factors affecting recovery, as well as their impact on cognitive function. For example, symptoms of comorbidities, including sleep deprivation, deconditioning, emotional stress, and pain, closely resemble postconcussion symptoms and similarly influence health-related status and cognition (Iverson and Lange, 2011). Research also indicates that anxiety and depression, family functioning, caregiver adjustment, and pre-existing neurodevelopmental disorders (e.g., learning disability or attention deficit-hyperactivity disorder) are strong predictors of prolonged symptoms (Covassin et al., 2012; Ponsford et al., 2012; Yeates et al., 2012; Iverson et al., 2015; Bernard et al., 2016; Grubenhoff et al., 2016). Last, there is growing recognition that pediatric patients are susceptible to symptom magnification and suboptimal neuropsychologic performance following sport-related concussion (Kirkwood and Kirk, 2010; Kirkwood et al., 2014). Thus, validity testing is recommended practice, particularly in patients with prolonged recovery, because it helps to identify and target treatment of factors that cause noncredible symptoms (Brooks et al., 2015; Connery et al., 2016).

Neuropsychologic consultation as intervention Recent literature suggests neuropsychologic consultation is an effective intervention in and of itself. In a population of 8–17-year-old patients experiencing prolonged recovery from concussion, Kirkwood and colleagues (2016) found that self-report postconcussion symptoms decreased significantly at 1 week and 3 months relative to preinjury ratings after a 3-hour neuropsychologic consultation. In sum, neuropsychologic assessment is a clinically useful tool in diagnosing and managing sport-related concussion. It provides meaningful information to families and referring clinicians about the severity of injury, and it helps to identify and target treatment of noninjuryrelated factors to assist in making return-to-learn and return-to-play decisions.

PROLONGED SYMPTOMS Most athletes who sustain a concussion during high school sports will be completely symptom-free within a few weeks (Meehan et al., 2010, 2011). There are several risk factors associated with prolonged symptoms. In one study, high symptom scores at injury and initial visit, time to initial clinical presentation, presence of two or more previous concussions, and female sex were associated with prolonged concussion recovery, with 26.4% taking longer than 4 weeks to recover (Thomas et al., 2018). Another study created a 12-point risk score model, combining injury and noninjury factors. This included the variables of female sex, age of 13 years or older, physician-diagnosed migraine history, prior concussion with symptoms lasting longer than 1 week, headache, sensitivity to noise, fatigue, answering questions slowly, and four or more errors on the Balance Error Scoring System tandem stance (Zemek et al., 2016). It is possible, however, that prolonged duration of symptoms may not be attributable to concussion. Indeed, psychologic consequences of removal from validating life activities, combined with physical deconditioning, can contribute to the development and persistence of postconcussive symptoms (DiFazio et al., 2016). When assessing a patient with prolonged concussive symptoms, it is important to attempt to distinguish whether symptoms are attributable to a concussion from which the athlete is incompletely recovered, or an alternate cause. Symptoms may be secondary to excessive rest, isolation and frustration with slow recovery, exacerbation of premorbid conditions, or other etiologies. Given the wide range of possible symptoms, expanding the care of these children by involving multiple specialists may be helpful. For those who have been getting strict rest since the time of injury, gradual reintroduction of cognitive as well as nonrisk, noncontact physical activity may be helpful. In addition, the management of specific symptoms may help allow the athlete return to the activities of daily living until recovery is complete.

Managing headaches Headache is the most common symptom of concussion (Barlow et al., 2010; Meehan et al., 2010; Blume, 2015). When assessing a patient for persistent headaches, obtaining information about possible stressors, screening for mood disorders or cognitive difficulties, and asking about sleep quality, nutrition, and hydration may reveal factors that may worsen symptoms. A progressively worsening headache pattern, nocturnal awakening, Valsalva-induced headaches, or failure to respond to pharmacotherapy should prompt consideration of other potential etiologies and possible neuroimaging

OFFICE-BASED CONCUSSION EVALUATION, DIAGNOSIS, AND MANAGEMENT: PEDIATRIC 113 (Blume, 2015; Pinchefsky et al., 2015a). Adequate sleep, hydration, and nutrition, and leaving a proper amount of time for sleep should be encouraged. Physicians should also counsel about avoiding caffeine overconsumption, alcohol and drug consumption, stress management, and the minimization of known headache triggers (Pinchefsky et al., 2015b). Headache classification may help to guide therapy (Wilson and Krolczyk, 2006). For example, medications such as topiramate, amitriptyline, or cyproheptadine may be used for frequent headaches with migraine features, and physical therapy or peripheral nerve block for occipital or cervicogenic headaches. Headaches with a neuropathic pain component may be treated with gabapentin. Nonpharmacologic treatments such as relaxation, cognitive behavioral therapy, biofeedback, and acupuncture may be helpful (Eccleston et al., 2012; Nestoriuc et al., 2008), as may nutraceuticals such as riboflavin and magnesium. In a retrospective pediatric study, riboflavin was shown to decrease migraine attack and severity with doses at 200–400 mg/day. Also, a randomized controlled trial in children with primary headaches suggested that oral magnesium oxide may lead to a significant reduction in headache days and significantly lower headache severity (Wang et al., 2003; Condò et al., 2009). Medications for headache relief should be started at a low dose, increased slowly, and continued for at least 2 or 3 months before being abandoned as ineffective. Medication choice should be based on headache type, but also possible interactions or side-effects. Because many of these medications are not primarily used for concussion-related symptoms, they should be prescribed only by practitioners with expertise in managing chronic headaches or concussions. Consider referral to neurology for management if there is no improvement with initial therapies.

Managing vestibular symptoms: vestibular therapy Vestibular symptoms of concussion are prevalent among pediatric patients and can include dizziness, vertigo, and imbalance (Gottshall et al., 2003; Corwin et al., 2015). It is appropriate to refer patients with pronounced or persistent vestibular symptoms to an otolaryngologist or vestibular therapist for a more complete vestibular assessment and therapy. Vestibular rehabilitation can reduce dizziness and improve balance following mild traumatic brain injury (Alsalaheen et al., 2010; Schneider et al., 2014).

Managing visual symptoms Vision deficits following a concussion are common among those with prolonged concussion symptoms

(Master et al., 2016). Common visual complaints include blurry vision, difficulty focusing, difficulty reading for long periods of time, headaches, and eye strain. Convergence insufficiency and accommodation deficits are the most common vision diagnoses in those with prolonged symptoms of concussion. These diagnoses can be managed with visual rehabilitation therapy or correction of a refractive error, usually under the guidance of an optometrist or ophthalmologist. Other clinicians can help students with such symptoms by providing documentation of school-specific accommodations, such as visual breaks, audiobooks, oral teaching, large-font printed material, or preprinted notes (Master et al., 2012, 2016; Halstead et al., 2013).

Managing mood symptoms: counseling/ psychologic support Emotional symptoms become particularly prevalent in the population of patients with prolonged symptoms, and may contribute to the development of a new psychiatric disorder, act as a catalyst for underlying psychologic pre-existing morbidities, and even trigger suicidal ideation (Ellis et al., 2015). When detecting features of these diagnoses, it is important to consider referral to a mental health professional who can assist in the management of these patients, especially when medications might be considered.

Managing cognitive symptoms Cognitive symptoms in the student-athlete with a concussion are best managed by establishing academic accommodations that allow the student to keep up with schoolwork until full recovery is achieved. Several medications such as amantadine and methylphenidate have been studied to improve cognitive function in the setting of recovery from concussion and other forms of traumatic brain injury. Currently, their use in this setting is mostly off-label and not approved by the Food and Drug Administration. While there are some clinical data suggesting benefit, most studies are preliminary, with a small number of participants. Therefore, the decision to prescribe these medications should rest with those who commonly treat patients with concussions.

Managing sleep Sleep management is key because disordered sleeping following concussion can exacerbate symptoms. In the acute phase, the focus should be on adequate sleep hygiene (Harmon et al., 2013; Phillips and Woessner, 2015). In the subacute phase, sleep hygiene remains important. The introduction of aerobic exercise may contribute to better sleep. Medications, particularly those

114

H. PAQUIN ET AL.

with a low side-effect profile, such as melatonin, might be considered (Zemek et al., 2014). Benzodiazepines should be avoided because of their side-effect profile.

to make, and should only be made after discussions with the athlete and others important in the athlete’s life. Involvement of several specialists may be useful.

PREVENTION OF ADDITIONAL INJURIES

CONCLUSION

Currently, there is no proven way to prevent concussions from occurring during sports. Still, preliminary data suggest that there are several ways athletes might reduce their risk of sustaining sport-related concussions. To prevent secondary injuries in an athlete who is not fully recovered, education of coaches, athletic trainers, and others involved in sports might lead to increased recognition of concussion and a decreased risk of reinjury. There is no evidence that personal protective equipment such as helmets, headgear, mouth guards, or face shields decreases the relative risk of concussion in young athletes (Schneider et al., 2017). It is conceivable that athletes wearing protective equipment may compensate by playing more aggressively, and thus such equipment may increase the risk of concussion. However, personal protective headgear does decrease the risk of skull fractures, dental injuries, facial bone fractures, and other problems, and therefore should be worn and properly fitted by all athletes participating in sports that require them. Increased cervical muscle strength may reduce head acceleration at the time of impact, leading to the hypothesis that neck muscle strengthening may reduce concussion risk (Ommaya et al., 2002; Mihalik et al., 2010; Collins et al., 2014).

CONSIDERATIONS OF TIMING FOR RETURN TO PLAY OR RETIREMENT When considering the return to play of any athlete, the risks must be weighed against the benefits. The risks of reinjury must be considered, and will vary based on the nature of the sport, the athlete’s position, and how many sports the athlete participates in. Concerning components of a concussion history include: increasing duration of symptoms with subsequent injuries; decreasing amount of force required to produce concussion; multiple concussions sustained during the patient’s lifetime; more pronounced cognitive dysfunction with subsequent injuries; and more pertinent symptoms with successive injuries. After each concussion, these areas should be considered and discussed with the athlete and his or her family. The benefits of participating in the chosen sport should be weighed against the risks associated with exposing the athlete to the potential for additional injury. If, after considering all these factors, it is determined safe to return the athlete to sport, the physician should consider a longer symptom-free waiting period before returning the athlete to play. These decisions are difficult

Concussion is a common injury in pediatric athletes, and its prevalence has increased with increased visibility and awareness. Management of concussion should be tailored to a patient’s symptoms and should focus on an early and gradual return to both cognitive and noncontact, low-risk physical activity. A multidisciplinary approach is often helpful in addressing more specific symptoms. Individualized return-to-play decisions should focus on the safety of the young athlete.

FINANCIAL DISCLOSURE Dr. Meehan receives royalties from ABC-Clio Publishing for the sale of his book, Kids, Sports, and Concussion: A Guide for Coaches and Parents, and royalties from Wolters Kluwer (UpToDate author). Dr. Meehan’s research is funded, in part, by a grant from the National Football League Players Association and by philanthropic support from the National Hockey League Alumni Association.

REFERENCES Alsalaheen BA, Mucha A, Morris LO et al. (2010). Vestibular rehabilitation for dizziness and balance disorders after concussion. J. Neurol. Phys. Ther. JNPT 34: 87–93. Arbogast KB, McGinley AD, Master CL et al. (2013). Cognitive rest and school-based recommendations following pediatric concussion: the need for primary care support tools. Clin. Pediatr. (Phila.) 52: 397–402. Barlow KM, Crawford S, Stevenson A et al. (2010). Epidemiology of postconcussion syndrome in pediatric mild traumatic brain injury. Pediatrics 126: e374–e381. Barr WB (2001). Methodologic issues in neuropsychological testing. J. Athl. Train. 36: 297–302. Belanger HG, Vanderploeg RD (2005). The neuropsychological impact of sports-related concussion: a meta-analysis. J. Int. Neuropsychol. Soc. 11: 345–357. Bernard CO, Ponsford JA, McKinlay A et al. (2016). Predictors of post-concussive symptoms in young children: injury versus non-injury related factors. J. Int. Neuropsychol. Soc. JINS 22: 793–803. Blume HK (2015). Headaches after concussion in pediatrics: a review. Curr. Pain Headache Rep. 19: 42. Borsting EJ, Rouse MW, Mitchell GL et al. (2003). Validity and reliability of the revised convergence insufficiency symptom survey in children aged 9 to 18 years. Optom. Vis. Sci. Off. Publ. Am. Acad. Optom. 80: 832–838. Broglio SP, Macciocchi SN, Ferrara MS (2007a). Neurocognitive performance of concussed athletes when symptom free. J. Athl. Train. 42: 504–508.

OFFICE-BASED CONCUSSION EVALUATION, DIAGNOSIS, AND MANAGEMENT: PEDIATRIC 115 Broglio SP, Macciocchi SN, Ferrara MS (2007b). Sensitivity of the concussion assessment battery. Neurosurgery 60: 1050–1057. Brooks BL, Ploetz DM, Kirkwood MW (2015). A survey of neuropsychologists’ use of validity tests with children and adolescents. Child Neuropsychol. 53: 1–20. Brown NJ, Mannix RC, O’Brien MJ et al. (2014). Effect of cognitive activity level on duration of post-concussion symptoms. Pediatrics 133: e299–e304. CDC. (2016). Heads Up. Accessed 9 February 2017. Available online at: http://www.cdc.gov/headsup/index.html. Collins CL, Fletcher EN, Fields SK et al. (2014). Neck strength: a protective factor reducing risk for concussion in high school sports. J. Prim. Prev. 35: 309–319. Condo` M, Posar A, Arbizzani A et al. (2009). Riboflavin prophylaxis in pediatric and adolescent migraine. J. Headache Pain 10: 361–365. Connery AK, Peterson RL, Baker DA et al. (2016). The impact of pediatric neuropsychological consultation in mild traumatic brain injury: a model for providing feedback after invalid performance. Clin. Neuropsychol. 30: 579–598. Corwin DJ, Wiebe DJ, Zonfrillo MR et al. (2015). Vestibular deficits following youth concussion. J. Pediatr. 166: 1221–1225. Covassin T, Elbin RJIII, Larson E et al. (2012). Sex and age differences in depression and baseline sport-related concussion neurocognitive performance and symptoms. Clin. J. Sport Med. 22: 98–104. DeMatteo C, Stazyk K, Giglia L et al. (2015). A balanced protocol for return to school for children and youth following concussive injury. Clin. Pediatr. (Phila.) 54: 783–792. DiFazio M, Silverberg ND, Kirkwood MW et al. (2016). Prolonged activity restriction after concussion: are we worsening outcomes? Clin. Pediatr. (Phila.) 55: 443–451. Dubrovsky AS, Friedman D, Kocilowicz H (2014). Pediatric post-traumatic headaches and peripheral nerve blocks of the scalp: a case series and patient satisfaction survey. Headache J. Head Face Pain 54: 878–887. Eccleston C, Palermo TM, de C Williams AC et al. (2012). Psychological therapies for the management of chronic and recurrent pain in children and adolescents. Cochrane Database Syst. Rev. 12: CD003968. Eisenberg MA, Meehan WP, Mannix R (2014). Duration and course of post-concussive symptoms. Pediatrics 133: 999–1006. Ellis MJ, Ritchie LJ, Koltek M et al. (2015). Psychiatric outcomes after pediatric sports-related concussion. J. Neurosurg. Pediatr. 16: 709–718. Ewing-Cobbs L, Barnes M, Fletcher JM et al. (2004). Modeling of longitudinal academic achievement scores after pediatric traumatic brain injury. Dev. Neuropsychol. 25: 107–133. Fazio VC, Lovell MR, Pardini JE et al. (2007). The relation between post concussion symptoms and neurocognitive performance in concussed athletes. Neurorehabilitation 22: 207–216. Gagnon I, Galli C, Friedman D et al. (2009). Active rehabilitation for children who are slow to recover following sportrelated concussion. Brain Inj. 23: 956–964.

Garcia-Rodriguez JA, Thomas RE (2014). Office management of mild head injury in children and adolescents. Can. Fam. Physician Med. Fam. Can. 60 (523–531): e294–e303. Gessel LM, Fields SK, Collins CL et al. (2007). Concussions among United States high school and collegiate athletes. J. Athl. Train. 42: 495. Gioia GA (2012). Pediatric assessment and management of concussions. Pediatr. Ann. Thorofare 41: 198–203. Gioia GA (2015). Multimodal evaluation and management of children with concussion: using our heads and available evidence. Brain Inj. 29: 195–206. Gottshall K, Drake A, Gray N et al. (2003). Objective vestibular tests as outcome measures in head injury patients. The Laryngoscope 113: 1746–1750. Grady MF (2010). Concussion in the adolescent athlete/common lower extremity injuries in the skeletally immature athlete. Curr. Probl. Pediatr. Adolesc. Health Care 40: 154–169. Grool AM, Aglipay M, Momoli F et al. (2016). Association between early participation in physical activity following acute concussion and persistent postconcussive symptoms in children and adolescents. JAMA 316: 2504–2514. Grubenhoff JA, Currie D, Comstock RD et al. (2016). Psychological factors associated with delayed symptom resolution in children with concussion. J. Pediatr. 174: 27–32; e1. Guskiewicz KM, Ross SE, Marshall SW (2001). Postural stability and neuropsychological deficits after concussion in collegiate athletes. J. Athl. Train. Dallas 36: 263–273. Halstead ME, McAvoy K, Devore CD et al. (2013). Returning to learning following a concussion. Pediatrics 132: 948–957. Hanson E, Stracciolini A, Mannix R et al. (2014). Management and prevention of sport-related concussion. Clin. Pediatr. (Phila.) 53: 1221–1230. Harmon KG, Drezner JA, Gammons M et al. (2013). American Medical Society for Sports Medicine position statement: concussion in sport. Br J Sports Med 47: 15–26. Howell DR, Mannix RC, Quinn B et al. (2016a). Physical activity level and symptom duration are not associated after concussion. Am. J. Sports Med. 44: 1040–1046. Howell DR, O’Brien MJ, Beasley MA et al. (2016b). Initial somatic symptoms are associated with prolonged symptom duration following concussion in adolescents. Acta Paediatr. 105: e426–e432. Iverson GL, Lange RT (2011). The little black book of neuropsychology: a syndrome-based approach. In: MR Schoenberg, JG Scott (Eds.), Post-concussion syndrome. Springer, New York, pp. 745–763. Iverson GL, Brooks BL, Collins MW et al. (2006). Tracking neuropsychological recovery following concussion in sport. Brain Inj. BI 20: 245–252. Iverson GL, Silverberg ND, Mannix R et al. (2015). Factors associated with concussion-like symptom reporting in high school athletes. JAMA Pediatr. 169: 1–9. Karlin AM (2011). Concussion in the pediatric and adolescent population: “different population, different concerns”. PM R 3: S369–S379.

116

H. PAQUIN ET AL.

Kerr ZY, Register-Mihalik JK, Marshall SW et al. (2014). Disclosure and non-disclosure of concussion and concussion symptoms in athletes: review and application of the socio-ecological framework. Brain Inj. 28: 1009–1021. Kirkwood MW, Kirk JW (2010). The base rate of suboptimal effort in a pediatric mild TBI sample: performance on the Medical Symptom Validity Test. Clin. Neuropsychol. 24: 860–872. Kirkwood MW, Yeates KO, Wilson PE (2006). Pediatric sport-related concussion: a review of the clinical management of an oft-neglected population. Pediatrics 117: 1359–1371. Kirkwood MW, Yeates KO, Taylor HG et al. (2008). Management of pediatric mild traumatic brain injury: a neuropsychological review from injury through recovery brain injury. Psychology 22: 769–800. Kirkwood MW, Randolph C, Yeates KO (2009). Returning pediatric athletes to play after concussion: the evidence (or lack thereof) behind baseline neuropsychological testing. Acta Paediatr. Int. J. Paediatr. 98: 1409–1411. Kirkwood MW, Grubenhoff JA, Peterson RL et al. (2014). Postconcussive symptom exaggeration after pediatric mild traumatic brain injury. Pediatrics 133: 643–650. Kirkwood MW, Peterson RL, Connery AK et al. (2016). A pilot study investigating neuropsychological consultation as an intervention for persistent postconcussive symptoms in a pediatric sample. J. Pediatr. 169: 244–249; e1. Kontos AP, Covassin T, Elbin RJ et al. (2012). Depression and neurocognitive performance after concussion among male and female high school and collegiate athletes. Arch. Phys. Med. Rehabil. 93: 1751–1756. Kuppermann N, Holmes JF, Dayan PS et al. (2009). Identification of children at very low risk of clinicallyimportant brain injuries after head trauma: a prospective cohort study. The Lancet 374: 1160–1170. Kutcher JS, Eckner JT (2010). At-risk populations in sportsrelated concussion. Curr. Sports Med. Rep. 9: 16–20. Leddy JJ, Kozlowski K, Donnelly JP et al. (2010). A preliminary study of subsymptom threshold exercise training for refractory post-concussion syndrome. Clin. J. Sport Med. Off. J. Can. Acad. Sport Med. 20: 21–27. Leddy JJ, Cox JL, Baker JG (2013). Exercise treatment for postconcussion syndrome: a pilot study of changes in functional magnetic resonance imaging activation, physiology, and symptoms. J. Head Trauma Rehabil. 28: 241. Majerske CW, Mihalik JP, Ren D et al. (2008). Concussion in sports: postconcussive activity levels, symptoms, and neurocognitive performance. J. Athl. Train. 43: 265. Mannix R, O’Brien MJ, Meehan 3rd WP (2013). The epidemiology of outpatient visits for minor head injury: 2005 to 2009. Neurosurgery 73: 129–134; discussion 134. Master CL, Grady MF (2012). Office-based management of pediatric and adolescent concussion. Pediatr. Ann. 41: 1–6. Master CL, Gioia GA, Leddy JJ et al. (2012). Importance of “return-to-learn” in pediatric and adolescent concussion. Pediatr. Ann. Thorofare 41: 1–6. Master CL, Scheiman M, Gallaway M et al. (2016). Vision diagnoses are common after concussion in adolescents. Clin. Pediatr. (Phila.) 55: 260–267.

McClain R (2015). Concussion and trauma in young athletes: prevention, treatment, and return-to-play. Prim. Care 42: 77–83. McCrea M, Hammeke T, Olsen G et al. (2004). Unreported concussion in high school football players: implications for prevention. Clin. J. Sport Med. Off. J. Can. Acad. Sport Med. 14: 13–17. McCrea M, Iverson GL, McAllister TW et al. (2009). An integrated review of recovery after mild traumatic brain injury (MTBI): implications for clinical management. Clin. Neuropsychol. 23: 1368–1390. McCrea M, Iverson GL, Echemendia RJ et al. (2013). Day of injury assessment of sport-related concussion. Br. J. Sports Med. 47: 272–284. McCrory P, Collie A, Anderson V et al. (2004). Can we manage sport related concussion in children the same as in adults? Br. J. Sports Med. 38: 516–519. McCrory P, Meeuwisse WH, Aubry M et al. (2013). Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012. Br J Sports Med 47: 250–258. McCrory P, Meeuwisse W, Dvorak J et al. (2017). Consensus statement on concussion in sport – the 5th international conference on concussion in sport held in Berlin, October 2016. Br J Sports Med 51: 838–847. Meehan WP, d’Hemecourt P, Comstock RD (2010). High school concussions in the 2008-2009 academic year: mechanism, symptoms, and management. Am. J. Sports Med. 38: 2405–2409. Meehan WP, d’Hemecourt P, Collins CL et al. (2011). Assessment and management of sport-related concussions in United States high schools. Am. J. Sports Med. 39: 2304–2310. Mihalik JP, Blackburn JT, Greenwald RM et al. (2010). Collision type and player anticipation affect head impact severity among youth ice hockey players. Pediatrics 125: e1394–e1401. Moran B, Tadikonda P, Sneed KB et al. (2015). Postconcussive syndrome following sports-related concussion: a treatment overview for primary care physicians. South. Med. J. 108: 553–558. Mucha A, Collins MW, Elbin RJ et al. (2014). A brief vestibular/ocular motor screening (VOMS) assessment to evaluate concussions: preliminary findings. Am. J. Sports Med. 42: 2479–2486. Nelson LD, Tarima S, LaRoche AA et al. (2016). Preinjury somatization symptoms contribute to clinical recovery after sport-related concussion. Neurology 86: 1856–1863. Nestoriuc Y, Rief W, Martin A (2008). Meta-analysis of biofeedback for tension-type headache: efficacy, specificity, and treatment moderators. J. Consult. Clin. Psychol. 76: 379–396. Ommaya AK, Goldsmith W, Thibault L (2002). Biomechanics and neuropathology of adult and paediatric head injury. Br. J. Neurosurg. 16: 220–242. Pardini D, Stump J, Lovell M et al. (2004). The Post-concussion Symptom Scale (PCSS): a factor analysis. Br. J. Sports Med. 38: 661–662.

OFFICE-BASED CONCUSSION EVALUATION, DIAGNOSIS, AND MANAGEMENT: PEDIATRIC 117 Phillips S, Woessner D (2015). Sports-related traumatic brain injury. Prim. Care 42: 243–248. Pinchefsky E, Dubrovsky AS, Friedman D et al. (2015a). Part I – evaluation of pediatric post-traumatic headaches. Pediatr. Neurol. 52: 263–269. Pinchefsky E, Dubrovsky AS, Friedman D et al. (2015b). Part II – management of pediatric post-traumatic headaches. Pediatr. Neurol. 52: 270–280. Ponsford J, Cameron P, Fitzgerald M et al. (2012). Predictors of postconcussive symptoms 3 months after mild traumatic brain injury. Neuropsychology 26: 304–313. Randolph C (2011). Baseline neuropsychological testing in managing sport-related concussion: Does it modify risk? Curr. Sports Med. Rep. 10: 21–26. Randolph C, McCrea M, Barr WB (2005). Is neuropsychological testing useful in the management of sport-related concussion? J. Athl. Train. 40: 139–152. Sady MD, Vaughan CG, Gioia GA (2011). School and the concussed youth – recommendations for concussion education and management. Phys. Med. Rehabil. Clin. N. Am. 22: 701–719. Schneider KJ, Meeuwisse WH, Nettel-Aguirre A et al. (2014). Cervicovestibular rehabilitation in sport-related concussion: a randomised controlled trial. Br J Sports Med 48: 1294–1298. Schneider DK, Grandhi RK, Bansal P et al. (2017). Current state of concussion prevention strategies: a systematic review and meta-analysis of prospective, controlled studies. Br. J. Sports Med. 51: 1473–1482. Tan CO, Meehan WP, Iverson GL et al. (2014). Cerebrovascular regulation, exercise, and mild traumatic brain injury. Neurology 83: 1665–1672.

Taylor AM, Nigrovic LE, Saillant ML et al. (2015). Trends in ambulatory care for children with concussion and minor head injury from eastern Massachusetts between 2007 and 2013. J. Pediatr. 167: 738–744. Thomas DG, Apps JN, Hoffmann RG et al. (2015). Benefits of strict rest after acute concussion: a randomized controlled trial. Pediatrics 135: 213–223. Thomas DJ, Coxe K, Li H et al. (2018). Length of recovery from sports-related concussions in pediatric patients treated at concussion clinics. Clin. J. Sport Med. Off. J. Can. Acad. Sport Med. 28: 56–63. Wang F, Van Den Eeden SK, Ackerson LM et al. (2003). Oral magnesium oxide prophylaxis of frequent migrainous headache in children: a randomized, double-blind, placebo-controlled trial. Headache 43: 601–610. Wilson M-CB, Krolczyk SJ (2006). Pediatric post-traumatic headache. Curr. Pain Headache Rep. 10: 387–390. Wing R, James C (2013). Pediatric head injury and concussion. Emerg. Med. Clin. North Am., Pediatric Emergency Medicine 31: 653–675. Yeates KO, Taylor HG, Rusin J et al. (2012). Premorbid child and family functioning as predictors of post-concussive symptoms in children with mild traumatic brain injuries. Int J Dev Neurosci 30: 231–237. Zemek R, Duval S, DeMatteo C et al. (2014). Guidelines for diagnosing and managing pediatric concussion, Ontario Neurotrauma Foundation, Toronto, ON. Zemek R, Barrowman N, Freedman SB et al. (2016). Clinical risk score for persistent postconcussion symptoms among children with acute concussion in the ED. JAMA 315: 1014–1025.