3


Concussion Recognition, Diagnosis, and Acute Management

One of the first challenges in responding to sports-related concussions is to recognize that a player may have sustained a concussion and therefore should be removed from the activity for further evaluation. As discussed in Chapter 1, although previous generations of athletes were encouraged to “shake it off” and return to play, current guidelines (Halstead et al., 2010; Harmon et al., 2013; McCrory et al., 2013b) and most state laws (NCSL, 2013) require athletes to be removed from competition or practice if a concussion is suspected so that a more formal evaluation can be completed. In this chapter, the committee responds to the portions of its charge concerning cognitive, affective, and behavioral changes that can occur during the acute phase of concussion; hospital- and non-hospital-based diagnostic tools; and the treatment and management of sports concussion. The chapter provides an overview of concussion screening and diagnosis, including sideline assessments at the time of injury, subsequent clinical evaluation, and the use of evaluation tools such as symptom checklists, and neuropsychological testing. The chapter also reviews the signs and symptoms of concussions and various considerations pertaining to the acute management of concussion, including the reintegration of concussed individuals into academic and athletic activities.

SIDELINE ASSESSMENT

The assessment of an injured player is facilitated by the presence of a certified athletic trainer, team physician, or other health care provider at the venue (e.g., field, gymnasium, or rink) where the injury occurred. How-



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3 Concussion Recognition, Diagnosis, and Acute Management One of the first challenges in responding to sports-related concussions is to recognize that a player may have sustained a concussion and therefore should be removed from the activity for further evaluation. As discussed in Chapter 1, although previous generations of athletes were encouraged to “shake it off” and return to play, current guidelines (Halstead et al., 2010; Harmon et al., 2013; McCrory et al., 2013b) and most state laws (NCSL, 2013) require athletes to be removed from competition or practice if a concussion is suspected so that a more formal evaluation can be completed. In this chapter, the committee responds to the portions of its charge con- cerning cognitive, affective, and behavioral changes that can occur during the acute phase of concussion; hospital- and non-hospital-based diagnostic tools; and the treatment and management of sports concussion. The chap- ter provides an overview of concussion screening and diagnosis, including sideline assessments at the time of injury, subsequent clinical evaluation, and the use of evaluation tools such as symptom checklists, and neuro- psychological testing. The chapter also reviews the signs and symptoms of concussions and various considerations pertaining to the acute management of concussion, including the reintegration of concussed individuals into academic and athletic activities. SIDELINE ASSESSMENT The assessment of an injured player is facilitated by the presence of a certified athletic trainer, team physician, or other health care provider at the venue (e.g., field, gymnasium, or rink) where the injury occurred. How- 99

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100 SPORTS-RELATED CONCUSSIONS IN YOUTH ever, the vast majority of young athletes practice and play in circumstances where trained personnel are not routinely available to make sideline injury assessments, and the responsibility for determining whether to remove an athlete from play falls on coaches, parents, players, and, perhaps, officials. A further impediment to identification is that symptoms may not become apparent for several hours after injury, and one result of this is that a large number of concussions are not identified until 24 hours or more after the in- jury (Duhaime et al., 2012; McCrory et al., 2013b). The Centers for Disease Control and Prevention (CDC) Heads Up campaign is designed to educate coaches, parents, and athletes about the prevention and recognition of and response to concussions (CDC, 2012a). A central feature of the campaign is the dissemination of information about the signs and symptoms of concus- sion (see Table 3-1) along with the message that players suspected of having sustained a concussion should be removed from play for the remainder of the day, referred to a health care provider for evaluation, and not permit- ted to return to play until they have been cleared by a health professional trained in concussion diagnosis and management (CDC, 2012a). The sideline evaluation of a player’s symptoms may be complicated by the tendency of athletes to underreport their symptoms (Anderson et al., 2013; Dziemianowicz et al., 2012; McCrea et al., 2004). A 2004 study TABLE 3-1 Signs and Symptoms of Concussions Relevant to Sideline Assessment Signs Observed Symptoms Reported by Athlete • Appears dazed or stunned (such as glassy eyes) • Headache or “pressure” in head • Is confused about assignment or position • Nausea or vomiting • Forgets an instruction or play • Balance problems or dizziness • Is unsure of score or opponent • Double or blurry vision • Moves clumsily or has poor balance • Sensitivity to light or noise • Answers questions slowly • Feeling sluggish, hazy, foggy, or • Loses consciousness (even briefly) groggy • Shows mood, behavior, or personality changes • Concentration or memory problems • Cannot recall events prior to hit or fall • Confusion • Cannot recall events after hit or fall • Feeling more emotional, nervous, or anxious • Does not “feel right” or is “feeling down” SOURCE: Based on CDC, 2012b.

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CONCUSSION RECOGNITION, DIAGNOSIS, AND ACUTE MANAGEMENT 101 of high school football players found that 41 percent of subjects reported not wanting to leave the game as their reason for not reporting a possible concussion, and 66 percent said they did not report their symptoms because they did not think their injury was serious enough to warrant medical at- tention (McCrea et al., 2004).1 In a 2012 survey of high school football players, a majority indicated that it was “okay” to play with a concus- sion and said that they would “play through any injury to win a game,” despite being knowledgeable about the symptoms and dangers of concus- sions (Anderson et al., 2013; see also Coyne, 2013; Kroshus et al., 2013; Register-Mihalik et al., 2013a,c; Torres et al., 2013). In addition, concus- sion signs and symptoms may develop and evolve over time, particularly within the first hours following injury (Duhaime et al., 2012; McCrory et al., 2013b). The mantra for laypersons faced with a potentially concussed athlete is “when in doubt, sit them out”: If a player has received “a bump, blow, or jolt to the head or body” and exhibits or reports one or more of the signs or symptoms of concussion, the player may have sustained a concussion (CDC, 2012a). Appropriately trained personnel have a number of tools available for use in the initial assessment of an individual for a possible concussion (see, e.g., Table 3-2; Appendix C). The Standardized Assessment of Concussion (SAC) and the Sport Concussion Assessment Tool (SCAT) 3 or Child SCAT3 were developed for the sideline evaluation of potentially concussed athletes. The Military Acute Concussion Evaluation (MACE) is a screening tool used to assess service members involved in a potentially concussive event. Such tools as well as balance tests (see Table 3-2) may be used either by trained responders as part of an acute sideline or in-field assessment or by health care providers during subsequent clinical evaluation. It is important to note, however, that because of the natural evolution of concussions, not all concussed athletes will be identified at the time of (presumed) injury even when personnel trained in concussion recognition are present (McCrory et al., 2013b). Duhaime and colleagues (2012) found that 50 percent of a sample of collegiate athletes who sustained a diagnosed concussion (with athletic trainers present for all games and practices) did not experience an “immediate or near immediate” onset of symptoms. 1  The reasons for athletes not reporting concussion were not mutually exclusive. The subjects were asked to select all that applied.

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102 SPORTS-RELATED CONCUSSIONS IN YOUTH TABLE 3-2 Sideline Concussion Screening Tools Test Function Assessed Baseline Needed Glasgow Coma Scale (GCS) Degree of brain impairment No (Teasdale and Jennett, 1974) Standardized Assessment of Memory and attention Recommended Concussion (SAC) processes (McCrea, 2001; McCrea et al., 1998, 2000) Sport Concussion Assessment Compilation of: GCS, SAC, Recommended Tool (SCAT) 3 and Child BESS, symptom checklist, and SCAT3 neck evaluation (McCrory et al., 2013a,c) Military Acute Concussion Compilation of event history, Evaluation (MACE) symptom checklist, modified (DVBIC, 2012) SAC, neurological screening Balance Error Scoring System Central integration of Normative data (BESS) vestibular, visual, and available but baseline (Riemann et al., 1999) somatosensory information recommended Sensory Organization Test Central integration of (SOT) vestibular, visual, and (Neurocom, 2013) somatosensory information King-Devick Test Saccadic eye movements Recommended (Galetta et al., 2011) Clinical reaction time (RT clin) Reaction time Yes (Eckner et al., 2010, 2013) CLINICAL EVALUATION Concussion Diagnosis Given the absence of a diagnostic test or biomarker for concussion, the current cornerstone of concussion diagnosis is confirming the presence of a constellation of signs and symptoms after an individual has experienced a hit to the head or body. Symptoms are self-reported by the athlete, often using a symptom scale. Reliance on an athlete’s self-report of symptoms as a fundamental part of diagnosing a concussion is complicated by the sub- jective nature of the assessment and by the possibility of an athlete under- reporting the symptoms (Anderson et al., 2013; Dziemianowicz et al., 2012; McCrea et al., 2004). Using multiple evaluation tools, such as symptom

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CONCUSSION RECOGNITION, DIAGNOSIS, AND ACUTE MANAGEMENT 103 scales and checklists, balance testing, and neurocognitive assessments, may increase the sensitivity and specificity of concussion identification (Broglio et al., 2007b; Guskiewicz and Register-Mihalik, 2011; Harmon et al., 2013; Register-Mihalik et al., 2013b), and this is the current preferred method of diagnosing a concussion, although existing evidence is insufficient to deter- mine the best combination of measures (Giza et al., 2013). Traditional neuroimaging techniques, such as standard computed to- mography (CT) and magnetic resonance imaging (MRI) (see Box 3-1), are BOX 3-1 Imaging Techniques A number of imaging techniques have evolved for measuring the structure, function, and connectivity of the developing human brain in vivo. The most com- monly used techniques, which are briefly described below, vary in invasiveness (i.e., requirement of radioactive isotope, intravenous injection, or concentrated radiation).   Computed Tomography (CT) uses focused X-rays together with computer imaging technology to make three-dimensional pictures of the head and can detect skull fracture, hemorrhage, and swelling. Diffusion tensor imaging (DTI) noninvasively measures axonal microstructure based on diffusion of water molecules that are impeded by the orientation, my- elination, and regularity of fibers. The most common measures include water diffusion (mean diffusivity) and the directionality and strength of the diffusion (fractional anisotropy). Functional magnetic resonance imaging (fMRI) noninvasively measures changes in blood oxygenation in the brain that are assumed to reflect changes in neural activity. Activity is measured either while the individual is performing a task (task- based fMRI) to link brain activity with cognitive performance or while at rest (rest- ing state fMRI) to examine synchronous activity across brain regions. Magnetic resonance imaging (MRI) uses a magnetic field and pulses of radio wave energy to perturb water molecules in the brain to generate images of differ- ent types of brain tissue. This noninvasive technique is used to measure regional and whole brain volume and to identify brain lesions and bleeds. Magnetic resonance spectroscopy (MRS) uses signals from water molecules to measure concentrations of metabolites noninvasively. Single-photon emission computed (SPECT) and positron emission tomography (PET) measure cerebral metabolism and blood flow using intravenous injections of radioactive isotopes to construct pictures of functional processes of the brain, including glucose metabolism and blood flow.

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104 SPORTS-RELATED CONCUSSIONS IN YOUTH used to rule out more severe head and brain injuries, such as skull frac- tures and intracranial hemorrhages, as well as cerebral swelling that would require surgical intervention (Giza et al., 2013; McCrory et al., 2013b; Suskauer and Huisman, 2009). Because of its accessibility in the emer- gency room, CT is the most commonly used imaging technique for clinical assess­ ent of head trauma (Belanger et al., 2007; Toledo et al., 2012). CT m exposes the individual to radiation, which is an important consideration when evaluating youth. The American Academy of Neurology has recently recommended that CT not be used to evaluate suspected sports-related concussion in the absence of signs or symptoms of more serious traumatic brain injury (TBI) (Giza et al., 2013). Although MRIs avoid the use of ionizing radiation, instead using a magnetic field and pulses of radio wave energy to image different types of brain and body tissue, they too are of little diagnostic value for concussions per se, because structural imaging results are normal in concussions that are uncomplicated by skull fracture or hematoma. Newer imaging techniques (see Box 3-1), such as magnetic resonance spectroscopy, positron emission tomography, single-photon emission com- puted tomography, functional magnetic resonance imaging, and diffusion tensor imaging—which all can be used to track metabolic, blood flow, and axonal changes—build on animal work and clinical outcome measures in mild traumatic brain injury (mTBI). Although such techniques may be use- ful in the future for assessing sports-related concussions, at present they have not been validated for clinical use (Cubon et al., 2011; DiFiori and Giza, 2010; Jantzen et al., 2004; Koerte et al., 2012; Lovell et al., 2007; Vagnozzi et al., 2010; Virji-Babul et al., 2013). Signs and Symptoms The signs and symptoms of concussion reported within 1 to 7 days post injury (see Table 3-3) typically fall into four categories—physical (somatic), cognitive, emotional (affective), and sleep—and patients will experience one or more symptoms from one or more categories. A study of high school ath- letes found that female athletes reported more somatic symptoms (drowsi- ness and sensitivity to noise) while their male counterparts reported more cognitive symptoms (amnesia and confusion/disorientation), although the number of symptoms reported did not differ by sex (Frommer et al., 2011). Kontos and colleagues (2012) have reported a revised factor structure— cognitive-migraine-fatigue, affective, somatic, and sleep. In their study, high school athletes reported lower levels of the sleep symptom factor than did college athletes, and female athletes reported higher levels of the affective symptom factor than did their male counterparts. There were no age or sex differences for the other factors, and the interaction between age and sex

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CONCUSSION RECOGNITION, DIAGNOSIS, AND ACUTE MANAGEMENT 105 TABLE 3-3 Concussion Symptoms by Category Somatic Cognitive Emotional Sleep • Headache • Difficulty thinking • Irritability • Sleeping more • Fuzzy or blurry clearly • Sadness than usual vision • Feeling slowed • Feeling more • Sleeping less • Dizziness down emotional than usual • Fatigue • Difficulty • Nervousness or • Trouble falling • Drowsiness concentrating anxiety asleep • Sensitivity to light • Difficulty • Sensitivity to remembering new noise information • Balance problems • Nausea or vomiting (early on) SOURCE: CDC, 2013. was not significant (Kontos et al., 2012). It should be noted that the symp- toms reported differently by males and females in the Frommer study fell within a single factor in the structure presented by Kontos and colleagues. Clinical Assessment Because concussions can affect several aspects of brain function, a battery of tests is needed to assess and monitor a concussion. Relying on any one type of test for the ongoing monitoring of a concussed athlete and for making the decision to clear the athlete for activity risks an incomplete picture because the functions covered by each test recover at different rates (Ellemberg et al., 2009; Guskiewicz, 2011; Guskiewicz and Register- Mihalik, 2011). A comprehensive concussion assessment includes symptom scores, ob- jective measures of postural stability (Hunt et al., 2009), and cognitive testing as is often done with neuropsychological testing. Broglio and col- leagues (2007b) found that a complete battery of tests, including assessment of neurocognitive functioning, self-reported symptom assessments, and postural control evaluation, was more sensitive to concussions than was each test individually. The sensitivity of the complete battery ranged from 89 to 96 percent, with the tests detecting no impairment in the other 4 to 11 percent of athletes diagnosed with concussion. Register-Mihalik and colleagues (2013b) used a healthy sample of college football players to establish reliable change confidence intervals for common clinical concussion measures and applied the reliable change parameters to a sample of concussed players examined before and after

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106 SPORTS-RELATED CONCUSSIONS IN YOUTH injury. Outcome measures included symptom severity scores, Automated Neuropsychological Assessment Metrics (ANAM) computerized neuro- psychological battery throughput scores, and SOT composite scores. Con- cussed athletes (n=132) were assessed within 5 days of injury. Based on the percentage of athletes with reliable change scores below or above various confidence interval cutoffs (80 percent, 90 percent, 95 percent), they calcu- lated sensitivity and specificity based on the percent of cases that declined by more than the reliable change metric. At all three confidence intervals, individual tests and total battery scores exceeded 90 percent specificity, indi- cating that when there was either no change or an improvement, it was pre- dictive of the athlete not having a concussion. On the other hand, a decline in the scores was not predictive of having a concussion. Although having at least one score decline across the entire battery improved sensitivity, the sensitivity was still at 50 percent. The authors emphasize the importance of using a total battery in the assessment of concussion. In this particular battery, score declines did not predict concussions any better than chance. Symptom Assessment An athlete who has had a concussion often will complete a post- concussion symptom scale at each visit with his or her health care provider. These self-reports of symptoms not only provide information pertinent to concussion diagnosis but also serve as the foundation of monitoring recov- ery and decision making about the individual’s return to school and physi- cal activity. A variety of symptom checklists are available and are usually completed by the athlete with each symptom graded using a Likert scale (e.g., 0 is “not experiencing” and 6 is “most severe”), although a few use a “yes/no” classification (Valovich McLeod and Leach, 2012). The variety and psychometric properties of several commonly used symptom scales and checklists are discussed later in the chapter (see also Appendix C). Balance Testing The dizziness and balance disturbances reported following an impact to the head or body may result from disruption of the central integration of vestibular, visual, and somatosensory information. Postural instability has been seen in patients following mild, moderate, and severe TBI (Geurts et al., 1996), while Guskiewicz (2001) found balance disturbances in college athletes within 2 days following a concussion. Other researchers have cor- roborated these results, and the equilibrium of the athlete is now objectively tested as a part of an acute concussion evaluation (Cavanaugh et al., 2005; Covassin et al., 2012a; McCrea et al., 2003; Register-Mihalik et al., 2008) carried out using a tool such as the BESS or SOT, described in Appendix C.

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CONCUSSION RECOGNITION, DIAGNOSIS, AND ACUTE MANAGEMENT 107 Neuropsychological Testing Neuropsychological testing has become commonplace in the evalua- tion of concussed athletes. Traditionally neuropsychological tests have not been used to make diagnoses but rather to characterize cognitive function, testing memory, speed, and processing time. Although neuropsychological tests are able to detect cognitive changes in injured athletes, these tests are also sensitive to state effects which might include the symptoms associated with the injury (Fazio et al., 2007). A study by Van Kampen and colleagues (2006) demonstrated that neuropsychological testing improves diagnostic accuracy, particularly in ruling out a concussion if the test results are nor- mal or typical relative to an appropriate individual or group norm (base- line). However, questions have been raised about whether the presence of ongoing cognitive deficits in the absence of symptoms actually predicts any risk for youth in terms of recurrent injury or long-term functional deficits or, conversely, whether the resolution of cognitive deficits on neuropsycho- logical testing is helpful in predicting when it is safe for an athlete to return to full physical activity (Kirkwood et al., 2009). A full discussion of the use of neuropsychological testing in concussion diagnosis and management appears later in the chapter. Electroencephalography The electroencephalogram (EEG) provides a reading of the electrical activity on the scalp, which originates within the neurons (gray matter) that make up the surface of the brain. Quantitative EEG (QEEG) techniques record this EEG activity from large arrays of electrodes on the scalp and are effective in detecting changes in brain electrical processing following concussion (Gosselin et al., 2009) as well as after behavior deficits have disappeared (McCrea et al., 2010; Prichep et al., 2013). McCrea and col- leagues (2010) compared performance and QEEG measures on 28 high school and college athletes who experienced sports-related concussions with those recorded from 28 matched, uninjured controls. All underwent pre-season baseline testing on QEEG measures as well as on measures of concussive symptoms, postural stability, and cognitive functioning. Con- trols were matched to injured players based on their baseline tests. Clinical testing and QEEG were performed on the day of injury and were repeated 8 days and 45 days after injury. Although both groups performed identi- cally prior to injury, after injury the concussion group differed significantly from controls, exhibiting more severe levels of post-concussion behavior symptoms through day 3. Importantly, QEEG measures continued to show increasingly larger differences through day 8 even though no behavioral differences occurred after day 3, suggesting that abnormalities in brain

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108 SPORTS-RELATED CONCUSSIONS IN YOUTH function continued to increase for at least a week following injury, despite the absence of behavior impairments. Barr and colleagues (2012) reported similar results through 45 days post injury. QEEG was also much more effective in predicting when concussed athletes would be ready to return to play. Prichep and colleagues (2013) used a QEEG discriminant function algorithm based on frontal electrode sites to create a TBI Index of brain function that discriminated between those with mild (n=51) and those with moderate concussions (n=14) at 8 days and 45 days post injury. Only the QEEG index predicted return to play before 14 days post injury versus after 14 days post injury. Accuracy was 80 percent in both cases. Such re- sults suggest that QEEG techniques could provide a more effective means to identify athletes with impairments following concussion and to predict when they might more safely return to play. The event-related potential (ERP) is a portion of the continuous EEG signal, but it differs from the EEG in that the ERP is time-locked to the onset of a discrete stimulus. Upon onset, the EEG desynchronizes and pro- duces an electrical waveform composed of a series of positive and negative voltage fluctuations that can differ in their amplitude (in µV, or millionths of a volt) and latency (in milliseconds). Under most conditions, the ERP continues for approximately 500 to 1,200 milliseconds before it returns to the baseline EEG signal (Molfese et al., 2001). Researchers report numer- ous instances in which information obtained using ERPs converges with functional findings from fMRI, magnetoencephalography, near-infrared and PET techniques. The advantage of the ERP measure over most other imag- ing techniques is that it provides very rapid temporal information about the order in which different neural and cognitive processes occur. As Broglio and colleagues (2011) note, this tool has been successful in identifying relationships between brain-behavior measures in concussed versus non- concussed athletes. The most studied of the ERP components is the P300 or P3b component. Baillargeon and colleagues (2012) reported that this component is reliably smaller in children, adolescents, and adults who have experienced a concussion than in individuals who do not have a concussion. Importantly, as in the case of QEEG, ERP studies show that such differ- ences may continue even after other indications of concussive injury—such as behavior tests and somatic complaints—suggest recovery, indicating that persistent abnormalities in the P3b could reflect suboptimal compensation in concussed athletes. Thériault and colleagues (2009) suggest that if such effects persist, they may indicate that a concussed athlete is at increased risk for future concussions. Subsequent concussions also appear to alter brain responses. Thériault and colleagues (2011) identified impairments of working memory storage capacity that correlated with athletes’ history of concussions. Gosselin and colleagues (2012a) also recorded visual ERPs during a working memory task from 44 patients identified as having mTBI

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CONCUSSION RECOGNITION, DIAGNOSIS, AND ACUTE MANAGEMENT 109 (7 to 8 months post injury) and 40 control volunteers matched for age (19 to 41 years of age) and sex. They reported that the smaller amplitude ERPs correlated with slower reaction times and poorer working memory. Impor- tantly, results did not differ for the type of injury (e.g., sports concussion versus motor vehicle). There is some consensus in the literature that both QEEG and ERP procedures can detect differences in performance and neural responses in concussed versus non-concussed student athletes in high school and college even when behavior measures fail to do so. However, these findings are true for a relatively small set of tasks that assess a limited array of cogni- tive abilities. Use of a broader range of tasks that measure different aspects of cognitive processes is necessary to provide a comprehensive view of behaviors most likely affected and those more likely spared by concussion. Serum Biomarkers After a brain injury, proteins may leak from damaged cells into the cerebrospinal fluid, then cross the blood-brain barrier to enter into the bloodstream. Although research on serum brain biomarkers in adults with severe TBI dates back to the 1970s, research on serum biomarkers for milder TBI and in children has emerged in the last 15 years, and the lit- erature on biomarkers for mTBI or concussion in the pediatric population is very limited (Berger and Zuckerbraun, 2012). Potential roles for serum biomarkers in the diagnosis and management of sports-related head injury include (1) distinguishing individuals with a concussion from those with non-concussion head injury; (2) identifying individuals who may have a skull fracture or more severe intracranial injury (e.g., intracranial hemor- rhage, cerebral swelling); and (3) identifying those individuals who may be at risk for a prolonged recovery (Berger and Zuckerbraun, 2012). Three biomarkers in particular have emerged from the mTBI literature: S100B, neuron-specific enolase (NSE), and cleaved tau protein (CTP) (Berger and Zuckerbraun, 2012; Finnoff et al., 2011). S100B is a protein that is found in the brain and also in cartilage and skin. It originates in the glial cells, and plays a role in neuronal prolifera- tion, differentiation, regeneration, and apoptosis (Geyer et al., 2009). Geyer and colleagues (2009) examined S100B levels in 148 children ages 6 months to 15 years of age with either head injury alone or head injury accompanied by symptoms of mTBI. They found that S100B did not readily discriminate between the two groups. Other studies have found elevated S100B levels in uninjured adult marathon runners, adult ice hockey players, adult box- ers, and adult basketball players, which suggests that S100B is increased by extracranial release due to exercise (Hasselblatt et al., 2004; Otto et al., 2000; Stålnacke et al., 2003), which may limit its usefulness as a biomarker

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