Pediatrics

Concussion

OVERVIEW: What every practitioner needs to know

Are you sure your patient has concussion? What are the typical findings for this disease?

Concussion is a brain injury that is defined as a "complex pathophysiologic process affecting the brain, induced by traumatic biochemical forces." It commonly includes the following major features:

1. Concussion may be caused either by direct blow to the head, face, neck, or elsewhere on the body with an "impulsive" force transmitted to the head.

2. Concussion typically results in the rapid onset of short-lived impairment of neurologic function that resolves spontaneously. Signs and symptoms may develop minutes to hours after the injury occurs.

3. Concussion may result in neuropathological changes, but the acute clinical symptoms largely reflect a functional disturbance rather than a structural injury.

4. Concussion results in a graded set of clinical symptoms that may or may not involve loss of consciousness. Resolution of the clinical and cognitive symptoms typically follows a sequential course; however, it is important to note that in a small percentage of cases, postconcussive symptoms may be prolonged for weeks to months.

Loss of consciousness, amnesia, and tonic posturing or convulsions may be associated with the injury, but overall infrequently occur with a concussion (<10%) and are not essential for making the diagnosis of concussion.

Assessment of concussion involves both the clinician evaluating the patient for objective signs (e.g., imbalance or vomiting), as well as asking the patient about various symptoms (e.g., vision changes, mental fogginess). Typical concussion symptomatology can be broken down into four domains including physical, cognitive, emotional, and sleep (Table I).

Table I.

Signs and Symptoms of a Concussion
Physical Cognitive Emotional Sleep
Headache Feeling mentally “foggy” Irritability Drowsiness
Nausea Feeling slowed down Sadness Sleeping more than usual
Vomiting Difficulty concentrating More emotional Sleeping less than usual
Balance problems Difficulty remembering Nervousness Difficulty falling asleep
Visual problems Forgetful of recent information
Fatigue Confused about recent events
Sensitivity to light Answers questions slowly
Sensitivity to noise Repeats questions
Dazed or stunned

Many of these symptoms may be difficult to ascertain from younger children, in which case reliance on parental report of normalcy is important. The most common symptom of concussion in children is headache.

In addition to assessing signs and symptoms of concussion, it is important to obtain a detailed history, specifically inquiring about past concussions and exact mechanism of injury. Other useful information includes a personal and family headache history and psychiatric history, as these patients may be at more risk for significant and/or prolonged symptom burden. A complete physical examination should be performed, including vision, a full neurologic examination, and balance testing (e.g., Romberg, tandem gait). The physical exam is often normal, but clinical findings may include orthostatic tachycardia, poor balance, abnormal ocular convergence, tenderness to palpation of the occipital muscles, and an increase in symptoms with testing of the vestibulo-occular reflex. A Glasgow Coma Scale score of <13 at time of evaluation, a focal neurologic abnormality, or physical signs concerning for a skull fracture should raise concern for additional diagnoses/structural injury.

The Center for Disease Control and Prevention (CDC) leads the “Heads up" campaign (See Table II) to increase awareness of pediatric concussion in the United States. This site offers free online tools for medical providers to guide the assessment of concussion symptom burden and provides information on how to counsel schools and parents on returning children back to learn and to play:

Table II.

Centers for Disease Control and Prevention Resources
Topic Website
Heads Up Toolkit for High School Sports www.cdc.gov/concussion/HeadsUp/high_school.html
Heads Up Toolkit for Schools www.cdc.gov/concussion/HeadsUp/schools.html
Heads Up Toolkit for Physicians www.cdc.gov/concussion/HeadsUp/physicians_tool_kit.html

http://www.cdc.gov/headsup/providers/index.html

What other disease/condition shares some of these symptoms?

Depending on the acuity and severity of signs/symptoms of the patient, other conditions that share similar symptoms include intracranial hemorrhage or thrombus, mass lesion, atypical migraine, dehydration, anemia, overtraining, hypoglycemia, visual deficits, vestibular pathology, seizure, post-traumatic stress disorder, attention-deficit disorder, depression, and anxiety.

What are risk factors/modifiers for sports-related concussion?

In addition to any source of trauma, such as motor vehicle accident or fall, collision sports place the pediatric population at a higher risk for concussion. Football, hockey, lacrosse, basketball, rugby, snowboarding, cycling, and soccer have the strongest association with head injury. Most concussions occur due to player-to-player contact and certain positions are more likely to be associated with concussion than others.

Females appear to sustain more concussions, report more symptoms with a higher severity of symptoms, and for a longer duration than males in similar sports. Several theories postulate that this difference could be due to anatomic differences such as decreased head-neck segment mass in female athletes compared to male athletes, contributing to greater forces on the female brain. Investigations into the role of hormones and variations in blood flow between genders are on-going. At this time, it is unclear whether female gender itself is a true risk factor for concussion or whether the differences noted can be attributed to reporting variance.

Genetic predisposition for adverse outcomes associated with concussion are being investigated. Genetic markers (apolipoprotein E4, apolipoprotein E G-219T promoter gene), have been proposed to play a role in concussion outcome.

Sex, age, loss of consciousness at time of injury, and amnesia at time of injury were not associated with prolonged symptom duration. It appears that number and severity of symptoms play a larger role in predicting severity of injury than does presence or absence of amnesia.

The occurrence of convulsions at the time of injury does not predict concussion severity or recovery.

Previous history of concussion places an individual at 2-5 times higher risk for subsequent concussion, and thus timing of return to play is an important clinical decision to be made by a health care provider experienced in concussion management.

Age appears to affect the duration of recovery from concussion, but not the incidence. Younger athletes appear to suffer symptoms longer than older athletes, and they are more likely to suffer associated catastrophic injuries.

Mood disorders may complicate both the diagnosis and management of concussion, however, there is no evidence that pre-existing anxiety, depression, or irritability places an individual at higher risk for concussion.

It has been suggested that learning disabilities and attention disorders may be associated with protracted recovery from concussion, however this has not been well identified in the current literature. In addition, diagnoses of these conditions do not appear to parlay any added risk for the occurrence of concussion.

What laboratory studies should you request to help confirm the diagnosis? How should you interpret the results?

To date, there are no laboratory studies that will help confirm the diagnosis of concussion.

Would imaging studies be helpful? If so, which ones?

Head computed tomography (CT) or magnetic resonance imaging (MRI) is typically normal after concussion and therefore is not useful for its diagnosis or management. However, if cervical spine injury, skull fracture, or intracranial hemorrhage is suspected, appropriate imaging such as a head CT without contrast or cervical spine x-ray, should be performed.

Advanced MRI techniques such as as functional MRI, diffusion tensor imaging, and cerebral blood flow are increasingly involved in research applications regarding concussion, however, these are not a part of standard testing at the current time.

The following signs and symptoms should lead the provider to evaluate for more severe injury: severe headache not controlled with acetaminophen, focal seizures, focal neurologic deficits, bilateral parasthesias, repeated emesis, significant drowsiness or difficulty awakening, slurred speech, midline cervical tenderness, significant irritability, prolonged mental status changes, or worsening symptoms. The Pediatric Emergency Care Applied Research Network (PECARN) created and validated neuroimaging decision rule for pediatric TBI (Please refer to the head injury section for details) to identify children at low risk for a significant intracranial injury, and while this helps dictate the need to obtain neuroimaging in well-appearing head injured patients, it does not per se help with the diagnosis of concussion.

Confirming the diagnosis

Cognitive assessment tools (Table III) have been developed to measure symptoms in the athlete with suspected concussion; the most commonly known are the Standardized Assessment of Concussion (SAC), Balance Error Scoring System (BESS), and Sport Concussion Assessment Tool 2, SCAT 3 (Figure 1). The CDC has also adopted use of the Acute Concussion Evaluation. In the setting of significant signs of concussion, the SAC can be used to support the diagnosis of concussion. It has since been widely adopted as a means to assist in the ongoing evaluation of the postconcussive patient. For individuals under age 13, the Child SCAT 3 has been developed for a more age-appropriate evaluation.

Table III.

Cognitive Assessment Tools
Standardized Assessment of Concussion SAC
Balance Error Scoring System BESS
Sport Concussion Assessment Tool 3 SCAT3

Figure 1.

Sport Concussion Assessment Tool 2.

http://physicians.cattonline.com/resources/clinical-resources/

Neuropsychological testing has become a common adjunctive evaluation tool used to assess cognitive function before and after concussion. Although neuropsychological testing (both computerized and using pen and paper) is not independently diagnostic, it can be useful in the assessment of the recovering athlete who has had a concussion. Neuropsychological testing formatted in a computerized version is easily accessible and can be interpreted by experienced providers.

Familiar computerized tests for ages 13 and up include the ImPACT, ANAM (Automated Neuropsychological Assessment Metrics), CogState, Concussion Vital Signs, and HeadMinder (Table IV). Research performed by the test developers themselves has been more optimistic about the reliability of these tests than have nonbiased researchers; however, the formats have been implemented in many athletic programs across the nation. There has been recent speculation that neurocognitive recovery, as evidenced by these testing modalities, may be ongoing despite symptom resolution; whether or not this has clinical implications is yet to be determined.

Table IV.

Computerized Neuropsychological Testing
Internet Resources
CogState: www.cogstate.com
HeadMinder: www.headminder.com
ImPACT: www.impacttest.com
Automated Neuropsychological Assessment Metrics: www.armymedicine.army.mil/prr/anam.html

Pen-and-paper testing requires evaluation by a neuropsychologist, which may be difficult and more expensive given the limited number of these specialists. When available, testing with a neuropsychologist can be useful making recommendations for home and school in the concussed individual. In addition, those with worsening of a premorbid condition such as depression, anxiety or ADHD may benefit from formal neuropsychological testing.

If you are able to confirm that the patient has concussion, what treatment should be initiated?

Recommending both physical and cognitive rest, especially within the first 72 hours after injury, is imperative for proper concussion management. Sleep, proper nutrition and hydration, and reduction of stimulation are important in treatment and recovery. Younger athletes typically recover more slowly than collegiate or professional athletes. On average, high school students recover in 2 weeks, middle school students recover in 3 weeks and grade school students take an average of 4 weeks for their brain injury to resolve. Prolonged recovery may be secondary to failure to fully rest from both physical and cognitive activities. Cognitive stressors include attending school, reading, using computers, text messaging, loud music, and watching television or movies.

Physical and cognitive rest for the first few days after a concussion is the mainstay of treatment, but in general, rest should continue until the patient is asymptomatic while at rest, at which time physical and cognitive activities may be reintroduced in a stepwise fashion. To advance to the next step, the patient must be asymptomatic for the previous 24 hours. See Table V for graded rehabilitation table. There is no evidence-based research to support the use of medication in the treatment of concussion. Medication could mask the true symptoms of concussion or associated severe injury or could exacerbate intracranial hemorrhage. Thus, it has been argued that medication therapy should be avoided in the acute phase. Acetaminophen or ibuprofen may be used for relief of prolonged symptoms and is used to treat cervicogenic pain associated with a head injury.

Table V.

Graduated Return to Play Protocol
Rehabilitation Stage Functional Exercise at each stage of rehabilitation Objective
No activity Complete physical and cognitive rest Recovery
Light aerobic exercise Walking, swimming, or stationary cycling (intensity <70% maximum predicted heart rate); no resistance training Increase heart rate
Sport-specific exercise Skating drills in ice hockey, running drills in soccer; no head impact activities Add movement
Noncontact training drills Progression to more complex training drills (e.g., passing drills in football and ice hockey); may start progressive resistance training Exercise, coordination, and cognitive load
Full contact practice After medical clearance, participate in normal training activities Restore confidence, assessment of functional skills by coaching staff
Return to play Normal game play

Return to school should occur once symptoms have decreased to a tolerable level. Usually this occurs after 1-3 days of rest. The student should try a few hours of school and then increase time in school as symptoms will allow. Initially, the goal of school attendance is not to make up all of the work he or she missed while out, but to get used to being in a stimulating environment. The treating physician should provide a note to the student and help the family identify a point person at school that may help with return to learn. The point person may be a teacher, counselor, administrator, or school nurse. Table VI lists important adjustments needed at school for return to learn.

Table VI.

Postconcussion Symptom Scale
Headache 0 1 2 3 4 5 6
Nausea 0 1 2 3 4 5 6
Vomiting 0 1 2 3 4 5 6
Balance problems 0 1 2 3 4 5 6
Dizziness 0 1 2 3 4 5 6
Fatigue 0 1 2 3 4 5 6
Trouble falling to sleep 0 1 2 3 4 5 6
Excessive sleep 0 1 2 3 4 5 6
Loss of sleep 0 1 2 3 4 5 6
Drowsiness 0 1 2 3 4 5 6
Light sensitivity 0 1 2 3 4 5 6
Noise sensitivity 0 1 2 3 4 5 6
Irritability 0 1 2 3 4 5 6
Sadness 0 1 2 3 4 5 6
Nervousness 0 1 2 3 4 5 6
More emotional 0 1 2 3 4 5 6
Numbness 0 1 2 3 4 5 6
Feeling "slow" 0 1 2 3 4 5 6
Feeling "foggy" 0 1 2 3 4 5 6
Difficulty concentrating 0 1 2 3 4 5 6
Difficulty remembering 0 1 2 3 4 5 6
Visual problems 0 1 2 3 4 5 6

Clearance to return to play should be granted by a health care provider with experience in concussion management. Because of the significant variation in recovery duration, this decision should be based on the individual rather than on a standard rule. Return to play should not be granted until an athlete is symptom free at rest and during exertion. The athlete should not be taking any medication to control symptoms unless he or she was on medication prior to the concussion.

Neuropsychological testing is an objective measuring tool that may be helpful in the cognitive assessment of the athlete after concussion when addressing the decision of when to allow return to play and school. Table V gives a gradual schedule for returning to play. A 22-symptom postconcussion symptom scale may be used to follow the patient through recovery (Table VI). This scale has shown validity; however, its reliability has yet to be established.

Recovery is important. Secondary concussion in an athlete still recovering from intial concussion is thought to require less force than the initial trauma.

Return to learn and return to play may occur simultaneously, but a student should not be cleared for return to full contact sports until he or she is attending full days of school and performing at his or her preinjury level without return of concussion symptoms.

What about longer term treatment?

Approximately one-third of children and adolescents with concussion will continue to report significant symptoms at one month post-injury. Enough sleep, good hydration and nutrition and avoiding unnecessary stressors is important to help with recovery. If continued symptoms, a multi-disciplinary approach to evaluation and management may be beneficial, including neuropsychological testing by a trained neuropsychologist, cognitive therapy to work on coping mechanisms, neurorehabilitation, and a supervised progressive exercise program directed by a physical therapist. If a patient is having protracted symptoms that significantly affect daily life, than referral to a clinician that is knowledgeable and experienced in the assessment and management of pediatric concussion should be considered to discuss a possible trial of medication therapy.

The most commonly protracted physical symptom is headache, although sleep disturbances, depression, and attention issues have also been reported. Calcium channel blockers, amitriptyline, and topiramate have all been proposed as possible therapies for protracted headache, although there are no prospective studies to support their use or identify long-term effects of treatment. Melatonin may be offered to help with sleep disturbances, but only after ensuring good sleep hygiene has been implemented (a consistent and sufficient sleep schedule that eliminates all distractions/stimulations from the bedroom). Tricyclic antidepressants and serotonin reuptake inhibitors may be useful options in the treatment of traumatic brain injury–related depression. Studies investigating the role of neurostimulants (e.g., methylphenidate, amantadine) to combat persistent cognitive symptoms have resulted in mixed results. Anecdotal support for these medications exists; however, research is lacking.

What are the adverse effects associated with each treatment option?

Restriction of participation could lead to falling behind in school or missing an opportunity for a college athletic scholarship. Prolonged strict rest may exacerbate daily symptoms and slow recovery. A child who is used to being very active may become resentful of being excluded from sports. Social isolation may result from prolonged periods away from school and daily activities. Restricting the use of medication in the acute phase of injury may result in poor pain management for the concussive symptom of headache.

What are the possible outcomes of concussion?

Full recovery back to baseline is expected after a concussion. On average, high school students recover in 2 weeks, middle school in 3 weeks and grade schoolers in 4 weeks; however, some individuals may take months to recover. See the section on complications for further discussion.

What causes this disease and how frequent is it?

Cause of injury is discussed above.

It has been estimated that between 1.1 and 1.9 million recreation- and sports-related concussions occur every year in US children aged ≤18 years. Underreporting is a significant problem with this diagnosis; however, as education of families and coaches improves, awareness will increase and more patients will be properly diagnosed. For many, the myth that concussion requires loss of consciousness still exists. Awareness and education is the first step to proper management and prevention of both the injury itself and of poor outcomes associated with concussion.

The majority of sports-related concussion occurs in the pediatric and adolescent age groups due to greater participation in collision sports. Concussion accounts for up to 9% of all high school athletic injuries. Sports with the highest risk of concussion include football and ice hockey for boys and soccer and basketball for girls. The true incidence of pediatric concussion occurring in those younger than age 10 years is lacking, and further investigation is needed to establish evidence-based guidelines for this age group.

Genetic contributions are discussed in a previous section.

What are the pathophysiologic features of concussion?

Concussion is caused by acceleration-deceleration and rotational forces transmitted to the brain by a direct blow to the head or elsewhere on the body. This results in disruption of the neuronal membrane, with subsequent physiologic changes. Because of limited ability to research mild traumatic brain injury in the human, the pathophysiologic features of concussive injury have been principally studied in animals, often rodents.

According to the lateral fluid percussion model, there appears to be a primary insult followed by a secondary inflammatory reaction and resultant metabolic changes. Disruption of cell wall integrity by glutamate release after injury leads to sodium influx; the resultant potassium efflux potentiates suppression of neuronal activity by depolarization. N-methyl-d-aspartate receptor activation is responsible for further depolarization, ultimately causing an influx of calcium ions into the cells. All of this cellular derangement leads to mitochondrial calcium overloading and depletion of adenosine triphosphate, which in turns results in mitochondrial malfunction. This impaired function is responsible for inducing changes of membrane permeability causing organelle swelling and decreased blood flow. This "energy crisis" of a mismatch between increased energy demands and a decrease in cerebral blood flow can last up to weeks in children.

What complications might you expect from the disease or treatment of the disease?

Postconcussion syndrome: Most pediatric patients recover within 2 -4 weeks, although similar and/or additional concussive symptoms occur beyond this time frame in 30% of pediatric patients. Refer to Table I to review specific symptoms that may be present. The prevalence of true postconcussion syndrome (PCS) is not well reported in children, although one prospective study demonstrated that 10% of children were still symptomatic at 3 months post-injury.

Suffering from symptoms for an extended time may delay a return to work or play causing increased stress on the child and parent due to physical, social, and economic strains. In one study it appeared as though there could be lasting changes in visual processing up to 3 months after concussion in adolescents. Athletes with a remote history of multiple concussions were found to perform similarly on neuropsychological testing as those who suffered a concussion in the week before testing. This suggests potential persistent cognitive effects from concussion.

Grade point averages of athletes that have suffered two or more concussions in the past have been shown to be significantly lower than those of athletes who have not had concussions.

Post-traumatic encephalopathy: Research of concussion in mice has suggested that cognitive function recovers on the fourth day after injury, but that an accumulation of amyloid precursor protein is present beyond that, with observed axonal degeneration and disruption of axonal function lasting up to 14 days after injury. Chronic traumatic encephalopathy is a progressive neurodegenerative tauopathy caused by repeated concussive and subconcussive impacts. Neuropathologically, CTE is characterized by a distinctive pattern of extensive tau-immunoreactive inclusions scattered throughout the cerebral cortex in a patchy, superficial distribution, and grossly it is characterized by generalized atrophy and enlarged ventricles. CTE has been linked to either imitating, initiating or accelerating the molecular cascade involved in several degenerative diseases, including Alzheimer's disease, Parkinson's disease, and Amyotrophic Lateral Sclerosis. More research is needed to better understand the relationship between brain injury and these diseases.

Second impact syndrome occurs when an athlete with recent head injury sustains a second head injury before full recovery from symptoms of the first insult. It appears that the second insult leads to cerebral vascular congestion and edema; this injury is catastrophic, often fatal. In a review of the literature, of 17 published cases, 59% were football players and 100% were male, with a lag time from first to second concussion ranging from hours to weeks. All with poor outcomes were in children < 20 years of age. It remains uncertain whether the pathologic condition is caused by both reported insults or if the second insult is fully responsible for the cerebral changes.

Are additional laboratory studies available; even some that are not widely available?

No additional laboratory studies are known to be helpful. Tau exon 6, (S-100 calcium-binding protein) and glial fibrillary acid protein (GFAP) may be promising markers of injury, however, definitive association has yet to be determined.

How can concussion be prevented?

Avoidance of collision sports and activities that pose a high risk of physical trauma can minimize concussion risk. Use of helmets has been proved to reduce the incidence of concussion in skiing and snowboarding; however, further data to support the same effect in other high-risk sports is yet to be established. Soccer headbands have not been proven to reduce concussion risk. Neither generic nor custom-made mouthguards have been proved to reduce the risk of concussion. Development of break-away bases in baseball, implementation of rule changes in hockey and football, identifying high-risk positions and behaviors, use of full facial shield in ice hockey, and neck strengthening have all been proposed and/or implemented in an effort to prevent concussion.

What is the evidence?

Kirelik, SB, McAvoy, K.. "Acute Concussion Management with Remove-Reduce/Educate/Adjust-Accommodate/Pace (REAP)". J Emerg Med.. vol. 50. 2016 Feb. pp. 320-4.

Kacperski, J, Arthur, T.. "Management of post-traumatic headaches in children and adolescents". Headache. vol. 56. 2016 Jan. pp. 36-48.

Schneider, DK, Grandhi, RK, Bansal, P, Kuntz, GE, Webster, KE, Logan, K, Barber Foss, KD, Myer, GD.. "Current state of concussion prevention strategies: a systematic review and meta-analysis of prospective, controlled studies". Br J Sports Med.. 2016 Jun 1.

Myer, GD, Yuan, W, Barber Foss, KD, Thomas, S, Smith, D, Leach, J, Kiefer, AW, Dicesare, C, Adams, J, Gubanich, PJ, Kitchen, K, Schneider, DK, Braswell, D, Krueger, D, Altaye, M.. "Analysis of head impact exposure and brain microstructure response in a season-long application of a jugular vein compression collar: a prospective, neuroimaging investigation in American football". Br J Sports Med.. 2016 Jun 15.

Storey, EP, Master, SR, Lockyer, JE, Podolak, OE, Grady, MF, Master, CL.. "Near Point of Convergence after Concussion in Children". Optom Vis Sci.. 2016 Jul 6.

Rhine, T, Babcock, L, Zhang, N, Leach, J, Wade, SL.. "Are UCH-L1 and GFAP promising biomarkers for children with mild traumatic brain injury?". Brain Inj.. 2016 Jul 14. pp. 1-8.

Silverberg, ND, Iverson, GL, McCrea, M, Apps, JN, Hammeke, TA, Thomas, DG.. "Activity-Related Symptom Exacerbations After Pediatric Concussion". JAMA Pediatr.. 2016 Aug 1.

Howell, DR, Beasley, M, Vopat, L, Meehan, W.. "The effect of prior concussion history on dual-task gait following a concussion". J Neurotrauma.. 2016 Aug 19.

Elbin, RJ, Sufrinko, A, Schatz, P, French, J, Henry, L, Burkhart, S, Collins, MW, Kontos, AP.. "Removal From Play After Concussion and Recovery Time". Pediatrics. 2016 Aug 29. pp. e20160910.

Meehan, WP.. "Medical therapies for concussion". Clin Sports Med.. vol. 30. 2011 Jan. pp. 115-24.

(A review of therapies that may additional education, academic accommodations, physical therapy, cognitive rehabilitation, and medication for the management of concussive brain injury.)

Zemek, R, Barrowman, N, Freedman, SB. "Pediatric Emergency Research Canada (PERC) Concussion Team. Clinical risk score for persistent postconcussion symptoms among children with acute concussion in the ED". JAMA. vol. 315. 2016. pp. 1014-25.

(Prospective, multicenter cohort study that enrolled over 3000 young patients (aged 5-<18 years) who presented within 48 hours of an acute head injury at 1 of 9 pediatric emergency departments within the Pediatric Emergency Research Canada (PERC) network to derive and validate a clinical risk score to predict persistent postconcussion symptoms at 28 days post-injury.)

Boden, BP, Tacchetti, RL, Cantu, RC. "Catastrophic head injuries in high school and college players". Am J Sports Med. vol. 35. 2007. pp. 1075-81.

(This case series study is a level of evidence IV and represents a topic that needs further investigation. It attempts to prove that high school athletes suffer more catastrophic head injuries in comparison to collegiate athletes and that a good proportion of individuals that suffer catastrophic head injury were still suffering from a previous head injury. It questions an association between severity of injury and chronology of first insult in relationship to the second (same season or a previous season).

Colvin, AC, Mullen, J, Lovell, MR. "The role of concussion history and gender in recovery from soccer-related concussion". Am J Sports Med. vol. 37. 2009. pp. 1699-1704.

(This study was designed as a cohort study, with level of evidence II-2. The results suggested that athletes with a history of concussion (versus those without) and female soccer players (versus male soccer players) scored significantly worse on neuropsychological testing. The ImPACT test was used in this study.)

Davis, GA, Ierson, GL, Guskiewicz, KM. "Contributions of neuroimaging, balance testing, electrophysiology and blood markers to the assessment of sport-related concussion". Br J Sports Med. vol. 43. 2009. pp. i36-45.

(This review of recent literature highlights the need for further support of balance testing and can be used for an overview of neuroimaging and its role in concussion diagnosis and management.)

Dick, RW.. "Is there a gender difference in concussion incidence and outcomes?". Br J Sports Med. vol. 43. 2009. pp. i460-50.

(This review of 51 recent studies that have investigated sex differences in concussion indicates that there may be a difference in incidence between male and female athletes, with the latter having a higher incidence; however, the results are obscured by the possibility of reporting bias. The diagnosis of concussion is clinical and therefore relies on reporting by individuals; therefore, the possibility of reporting discrepancies is substantial.)

Field, M, Collins, MW, Lovell, MR. "Does age play a role in recovery of sports-related concussion? A comparison of high school and collegiate athletes". J Pediatr. vol. 142. 2003. pp. 546-53.

(This study [level of evidence II-3] reveals preliminary data suggesting a more protracted cognitive recovery in high school athletes versus collegiate athletes with concussion 3 days after injury, but not on initial evaluation after injury and not at days 5 or 7 after injury. Most of the participants were white, male, football and soccer athletes; therefore the information may not be generalizable to other sports and populations. In addition, the study is limited by its lack of blinding. Despite the limitations of this study, it suggests a statistical difference in recovery between age groups, at least in the populations studied. Most importantly, this study supports the need for further delineation of effects of concussion in each age group.)

Fung, M, Willer, B, Moreland, D. "A proposal for an evidence-based emergency department discharge form for mild traumatic brain injury". Brain Inj. vol. 20. 2006. pp. 889-94.

(This study compared multiple discharge forms with directions for signs and symptoms of hemorrhage after mild traumatic brain injury. It showed that many forms are confusing and not evidence based. Although this study reviewed adult charts, it highlights important considerations for discharge information across all populations, including pediatric populations.)

Harmon, KG, Drezner, JA, Gammons, M. "American Medical Society for Sports Medicine position statement: concussion in sport". Br J Sports Med. vol. 47. 2013. pp. 15-26.

(This position statement is a summary of the AMSSM's accepted approach to concussion diagnosis and management and also serves to note current research endeavours and clinical questions that remain unanswered.)

Jotwani, V, Harmon, KG.. "Postconcussion syndrome in athletes". Curr Sports Med Rep. vol. 9. 2010. pp. 21-6.

(This article is a review of the literature representing current and previous understanding of postconcussion syndrome. It summarizes the variable definitions and current arguments regarding the diagnosis of postconcussion syndrome and discusses the future directions for research.

Lovell, MR, Collins, MW, Iverson, GL.. "Recovery from mild concussion in high school athletes". J Neurosurg. vol. 98. 2003. pp. 296-301.

(At the time this study was performed, it was one of the first to investigate neuropsychological testing of high school athletes with concussion. Neuropsychological testing of high school athletes at baseline and after injury suggested statistically significant changes after mild traumatic brain injury in comparison to a control group. Athletes reported resolution of symptoms by the fourth day after injury; however, memory impairment was still noted on the seventh day after injury. Mental status change at the time of the injury appeared to be related to delayed cognitive recovery and resolution of symptoms. The duration of follow-up in this study was 7 days at which time there were still significant cognitive changes; continued follow-up and testing beyond 7 days would have facilitated more understanding of the functional recovery after concussion in high school athletes.)

McClincy, MP, Lovell, MR, Pardini, J. "Recovery from sports concussion in high school and collegiate athletes". Brain Inj. vol. 20. 2006. pp. 33-9.

(This study used neuropsychological testing to evaluate cognitive functioning in athletes who had concussions and revealed cognitive deficits up to 14 days after receiving the concussion. Effects of concussion appear to persist longer than symptoms, which raises questions about the appropriate duration of rest and whether return to play should be granted based on resolution of cognitive deficits rather than on resolution of symptoms at rest and during exertion. The most significant limitation of this study it its failure to apply the intention-to-treat principle; athletes who did not complete the full battery of three tests were not included. This limitation could allow for exaggeration of results. Continued efforts to elucidate the findings of this study are warranted.)

McCrea, M, Guskieqicz, K, Randolph, C. "Effects of a symptom-free waiting period on clinical outcome and risk of reinjury after sport-related concussion". Neurosurgery. vol. 65. 2009. pp. 876-83.

(This was a prospective, nonrandomized study with a large sample size of high school and collegiate athletes that investigated the influence of a symptom-free waiting period on outcome and risk of secondary injury after sports-related concussion. Significant influence was not identified.)

McCrory, P, Johnston, KM, Mohtadi, NG. "Evidence-based review of sport-related concussion: basic science". Clin J Sport Med. vol. 11. 2001. pp. 160-5.

(This review elucidates the pitfalls of the animal model and its application to the effect of concussion in the human brain. Exact simulation of the mechanism of concussive injury is difficult to achieve in the animal model, making applicability to a human model difficult.)

McCrory, P, Meeuwisse, W, Aubry, M. "Consensus statement on Concussion in Sport- 4th International Conference held in Zurich, November 2012". Br J Sport Med. vol. 47. 2013. pp. 250-258.

(This consensus statement by expert opinion [level of evidence III] is appropriate for guidance in the management of concussion in the pediatric population and specifically addresses concussion in sports in patients age 13 years and older. Data on younger patients is lacking and those patients should be managed more conservatively. This symposium was a formal consensus meeting that was held with the objective of providing balanced, objective, and knowledgeable guidance for management of concussion in this age group.)

McKee, AC, Cantu, RC, Nowinski, CJ. "Chronic traumatic encephalopathy in athletes: progressive tauopathy after repetitive head injury". J Neuropathol Exp Neurol. vol. 68. 2009. pp. 709-35.

(These new data could prove and clarify the understanding of the long-term effects of repeated mild traumatic brain injury but is still preliminary [level of evidence II-3]). Further research, with greater sample size will help to minimize confounding factors.)

"Heads Up: Facts for Physicians About Mild Traumatic Brain Injury (MTBI)".

(The information provided in this resource is helpful more for the outpatient physician; however, it contains a useful summary of the main diagnostic and management aspects of concussion. It is available for both youth and high school athletes. The CDC site also has links to written education for patients and families to take home.)

Additional References

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Ongoing controversies regarding etiology, diagnosis, treatment

Commonly debated topics regarding concussion include the role of neuropsychological testing in concussion management, the poorly understood pathologic characteristics of second-impact syndrome and its effect on the recommended management of head injury, the loosely defined nuances and medical management of postconcussion syndrome, the long-term effects of concussion on cognitive functioning and brain tissue, and the topics of return to play versus retirement in the athlete with multiple concussions. In general, given the paucity of research, a conservative approach should be adopted by care providers with respect to pediatric concussion management: "When in doubt, sit them out!"

**The original authors for this chapter were Drs. Teri McCambridge and Lindsay Jones. The chapter was revised by Drs. Tara Rhine and Kate Berz.

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