Abstract

Executive Summary Purpose of the Statement To provide an evidence-based, best practices summary to assist physicians with the evaluation and management of sports concussion. To establish the level of evidence, knowledge gaps, and areas requiring additional research. Importance of an AMSSM Statement Sports medicine physicians are frequently involved in the care of patients with sports concussion. Sports medicine physicians are specifically trained to provide care along the continuum of sports concussion from the acute injury to return-to-play decisions. The care of athletes with sports concussion is ideally performed by healthcare professionals with specific training and experience in the assessment and management of concussion. Competence should be determined by training and experience, not dictated by specialty. While this statement is directed toward sports medicine physicians, it may also assist other physicians and healthcare professionals in the care of patients with sports concussion. Definition Concussion is defined as a traumatically induced transient disturbance of brain function and involves a complex pathophysiologic process. Concussion is a subset of mild traumatic brain injury that is generally self-limited and at the less severe end of the brain injury spectrum. Pathophysiology Animal and human studies support the concept of postconcussive vulnerability, showing that a second blow before the brain has recovered results in worsening metabolic changes within the cell. Experimental evidence suggests the concussed brain is less responsive to usual neural activation, and when premature cognitive or physical activity occurs before full recovery the brain may be vulnerable to prolonged dysfunction. Incidence It is estimated as many as 3.8 million concussions occur in the US per year during competitive sports and recreational activities; however, as many as 50% of concussions may go unreported. Concussions occur in all sports with the highest incidence in football, hockey, rugby, soccer, and basketball. Risk Factors for Sports-related Concussion A history of concussion is associated with a higher risk of sustaining another concussion. A greater number, severity, and duration of symptoms after concussion are predictors of a prolonged recovery. In sports with similar playing rules, the reported incidence of concussion is higher in females than males. Certain sports, positions, and individual playing styles have a greater risk of concussion. Youth athletes may have a more prolonged recovery and are more susceptible to a concussion accompanied by a catastrophic injury. Preinjury mood disorders, learning disorders, attention deficit disorders (ADD/ADHD), and migraine headaches complicate diagnosis and management of concussion. Diagnosis of Concussion Concussion remains a clinical diagnosis ideally made by a healthcare provider familiar with the athlete and knowledgeable in the recognition and evaluation of concussion. Graded symptom checklists provide an objective tool for assessing a variety of symptoms related to concussions, while also tracking the severity of those symptoms over serial evaluations. Standardized assessment tools provide a helpful structure for the evaluation of concussion, although limited validation of these assessment tools is available. ‘Sideline’ Evaluation and Management Any athlete suspected of having a concussion should be removed from play and assessed by a licensed healthcare provider trained in the evaluation and management of concussion. Recognition and initial assessment of concussion should be guided by a symptom checklist, cognitive evaluation (including orientation, past and immediate memory, new learning, and concentration), balance tests, and further neurologic physical examination. While standardized sideline tests are a useful framework for examination, the sensitivity, specificity, validity, and reliability of these tests among different age groups, cultural groups, and settings is largely undefined. Their practical usefulness with or without an individual baseline test is also largely unknown. Balance disturbance is a specific indicator of concussion but is not very sensitive. Balance testing on the sideline may be substantially different than baseline tests because of differences in shoe/cleat type or surface, use of ankle tape or braces, or the presence of other lower extremity injury. Imaging is reserved for athletes where intracerebral bleeding is suspected. There is no same-day return to play for an athlete diagnosed with a concussion. Athletes suspected or diagnosed with concussion should be monitored for deteriorating physical or mental status. Neuropsychological Testing Neuropsychological tests are an objective measure of brain-behavior relationships and are more sensitive for subtle cognitive impairment than clinical exam. Most concussions can be managed appropriately without the use of neuropsychological testing. Computerized neuropsychological testing should be interpreted by healthcare professionals trained and familiar with the type of test and the individual test limitations, including a knowledgeable assessment of the reliable change index, baseline variability, and false positive and false negative rates. Paper and pencil neuropsychological tests can be more comprehensive, test different domains, and assess for other conditions that may masquerade as or complicate assessment of concussion. Neuropsychological testing should be used only as part of a comprehensive concussion management strategy and should not be used in isolation. The ideal timing, frequency, and type of neuropsychological testing have not been determined. In some cases, properly administered and interpreted neuropsychological testing provides added value to assess cognitive function and recovery in the management of sports concussions. It is unknown if use of neuropsychological testing in the management of sports concussion helps prevent recurrent concussion, catastrophic injury, or long-term complications. Comprehensive neuropsychological evaluation is helpful in the postconcussion management of athletes with persistent symptoms or complicated courses. Return to Class Students will require cognitive rest and may require academic accommodations such as reduced workload and extended time for tests while recovering from concussion. Return to Play Concussion symptoms should be resolved before returning to exercise. A return-to-play progression involves a gradual, step-wise increase in physical demands, sports-specific activities, and the risk for contact. If symptoms occur with activity, the progression should be halted and restarted at the preceding symptom-free step. Return to practice/play after concussion should occur only with medical clearance from a licensed healthcare provider trained in the evaluation and management of concussion. Short-term Risks of Premature Return to Play The primary concern with early return to play is decreased reaction time leading to increased risk of repeat concussion or other injury and prolongation of symptoms. Long-term Effects There is increasing concern that head impact exposure and recurrent concussions contribute to long-term neurological sequelae. Some studies have suggested an association between prior concussions and chronic cognitive dysfunction. Large-scale, epidemiological studies are needed to more clearly define risk factors and causation of any long-term neurological impairment. Disqualification from Sport There are no evidence-based guidelines for disqualifying/retiring an athlete from sport after concussion. Each case should be carefully deliberated and an individualized approach to determining disqualification taken. Education Greater efforts are needed to educate involved parties including athletes, parents, coaches, officials, school administrators, and healthcare providers to improve concussion recognition, management, and prevention. Physicians should be prepared to provide counseling regarding potential long-term consequences of concussion and recurrent concussion. Prevention Primary prevention of some injuries may be possible with modification and enforcement of the rules and fair play. Helmets, both hard (football, lacrosse, and hockey), and soft (soccer, rugby), are best suited to prevent impact injuries (fracture, bleeding, laceration, etc) but have not been shown to reduce the incidence and severity of concussions. There is no current evidence that mouth guards can reduce the severity of or prevent concussions. Secondary prevention may be possible by appropriate return-to-play management Legislation Legislative efforts provide a uniform standard for scholastic and nonscholastic sports organizations regarding concussion safety and management. Future Directions Additional research is needed to validate current assessment tools, delineate the role of neuropsychological testing, and improve identification of those at risk of prolonged postconcussive symptoms or other long-term complications. Evolving technologies for the diagnosis of concussion, such as newer neuroimaging techniques or biologic markers, may provide new insights into the evaluation and management of sports concussion. BACKGROUND AND PURPOSE The recognition and management of concussion in sport is an evolving and controversial topic with a myriad of groups and organizations producing statements and recommendations.1–6 The purpose of this statement is to provide an evidence-based, best practices summary to assist physicians with the evaluation and management of sports-related concussion and to establish the level of evidence, knowledge gaps, and areas requiring additional research. The American Medical Society for Sport Medicine (AMSSM) represents over 2100 nonsurgical sports medicine physicians who have completed additional training in sports medicine after a residency program in family medicine, internal medicine, pediatrics, emergency medicine, or physical medicine and rehabilitation, many of whom have extended expertise in concussion evaluation and management. Sports medicine physicians are frequently involved in the care of patients with sports concussion and are specifically trained to provide care along the continuum of sports concussion from the acute injury to return-to-play decisions. The care of athletes with sports-related concussions is ideally performed by healthcare professionals with specific training and experience in the assessment and management of concussion. Competence should be determined by training and experience, not dictated by specialty. While this statement is directed towards sports medicine-trained physicians, it may also be used by other physicians and healthcare professionals to improve the care of patients with sports-related concussion. Level of Evidence This statement uses the Strength of Recommendation Taxonomy (SORT) to grade recommendation based on athlete outcomes (Table 1).7TABLE 1: Strength-of-Recommendation Taxonomy (SORT)Definition of Concussion Concussion is defined as a traumatically induced transient disturbance of brain function and is caused by a complex pathophysiologic process. Concussions have also been referred to as mild traumatic brain injuries (MTBI). While all concussions are MTBIs, not all MTBIs are concussions. Concussions are a subset of mild traumatic brain injury on the less severe end of the brain injury spectrum and are generally self-limited in duration and resolution. Pathophysiology Concussions occur when linear and/or rotational forces are transmitted to the brain. Currently, there is no known biomechanical threshold for a clinical concussion. A demonstrated cellular process, the “neurometabolic cascade” underlying the clinical presentation of concussive injury, describes a complex cascade of ionic, metabolic, and pathophysiological events that is accompanied by microscopic axonal injury.8–10 This disruption of ionic balance and normal metabolism requires energy to reestablish homeostasis. However, the need for increased energy occurs in the presence of decreased cerebral blood flow and ongoing mitochondrial dysfunction, resulting in a mismatch of energy supply and demand.8,10,11 Until normal brain cellular function is restored, animal and human studies support the concept of increased postconcussive vulnerability, showing that a second injury before the brain has recovered results in worsening cellular metabolic changes and more significant cognitive deficits.8,9,11–16 Experimental evidence further suggests the concussed brain is less responsive to physiological neural activation.9,10 Thus, excessive cognitive or physical activity before full recovery may result in prolonged dysfunction. Some of these pathophysiological perturbations are more pronounced in youth, raising concerns that the immature brain may be even more susceptible to repeat concussion before full recovery.9 Reported Incidence of Sports-related Concussion Concussions occur commonly in helmeted and nonhelmeted sports, and recent data suggest a trend of increased annual concussion rates over the past decade.17,18 Reasons for the apparent increased incidence are unknown, but it is widely speculated to be a result of the emphasis on concussion education and awareness leading to increased identification and reporting.17,18 Despite the increased reported incidence of concussion in recent years, there has not been a corresponding increase in the incidence of sports-related catastrophic brain injuries such as subdural and epidural hematomas or malignant cerebral edema (ie, Second Impact Syndrome). The Centers for Disease Control and Prevention (CDC) estimates that between 1.6 and 3.8 million sports-related concussive injuries occur annually in the United States19 and account for 5% to 9% of all sport injuries.20,21 Thirty percent of all concussions in individuals between 5 to 19 years of age are sport related and result in a significant number of emergency room visits.6,22 The majority of concussions occurring in organized sports in the United States are sustained in football, wrestling, girls’ soccer, boys’ soccer, and girls’ basketball. 20,21,23,24 (Table 2) Competition concussion rates are consistently higher than practice rates, and in high school and college sports with the same rules (basketball and soccer) there is an increased incidence of concussion reported in female athletes. 20,23,25 Several studies contend the true incidence is likely higher than documented because many athletes fail to report concussions.26–28 With greater focus on concussion awareness and state legislation, the reported incidence is likely to continue to increase.TABLE 2: Concussion Rates Per 1000 Athlete ExposuresSigns and Symptoms There are many signs and symptoms that can be observed with a concussion (Table 3). Headache is the most common reported symptom, with dizziness the second most common.6,25,29,30 Loss of consciousness only occurs in about 10% of concussions.5,6,30–34 Several symptoms of concussion are nonspecific, eg, nausea, vomiting, and headache are a common presentation of acute gastroenteritis, and dizziness is a common symptom of acute cardiac compromise. Some symptoms overlap with other disorders such as sleep disturbances, depression, and attention deficit disorder and it is helpful to determine whether these symptoms were present prior to the injury. (C) In college athletes, 59% reported concussion-like symptoms in the prior year with no history of head injury, and 50% to 84% of high school athletes reported similar symptoms of concussion at baseline testing.34–36 There have been no consistently demonstrated differences in the symptoms reported between males and females.34–39TABLE 3: Signs and Symptoms of a ConcussionMost studies report that 80% to 90% of athletes will have symptom resolution by 7 days following their injury,6,25,29,32,39 although symptom resolution may not always indicate a full cognitive recovery as persistent deficits may be present on neuropsychological testing.32,40 However, the clinical importance of persistent neuropsychological testing changes in the absence of continued symptoms is unknown. Risk Factors/Modifiers for Sports-related Concussion A history of prior concussion, a greater number, severity or duration of symptoms after concussion, female sex, genetic predisposition, a history of a learning disorder, attention deficit disorder, migraines, or mood disorder, and playing certain positions have all been suggested to affect the risk of sustaining a concussion or having a more protracted course. Previous Concussion A history of concussion is associated with a 2 to 5.8 times higher risk of sustaining another concussion.24,38,41–46 Athletes with a prior history of concussion may also report more symptoms at baseline than those without a history of concussion.36,47–49 However, there is conflicting evidence on whether a prior concussion is associated with a prolonged recovery course.50,51 Lau found no difference in history of concussion and time to recovery, while Slobounov demonstrated significantly slower recovery rates of neurological functions after a second concussion.50,51 As with other sports injuries, the greatest risk factor for concussion is a previous concussion, and progressively prolonged symptoms with subsequent concussions is a concerning prognostic sign. Number, Severity, or Duration A greater number, severity, and duration of symptoms after concussion are predictors of a prolonged recovery.47,51–53 Specific signs or symptoms may also predict recovery time. Dizziness at the time of injury was found to be the greatest predictor in high school football players for a recovery taking longer than 21 days,50,54 and athletes who had more symptoms in the cognitive or migraine symptom clusters often required more recovery time.50 In rugby players, headaches lasting longer than 60 hours, 3 or more symptoms at initial presentation, and the presence of fatigue/tiredness/fogginess were associated with a longer recovery.29 Sex Recent data suggests that in sports with similar rules females sustain more concussions than their male counterparts.20,23,25,55,56 In addition, females experience or report a higher number and severity of symptoms as well as a longer duration of recovery than males in several studies.38,55–59 Decreased head-neck segment mass of females compared to male athletes may contribute to greater angular acceleration of the head after concussive impact as a mechanism for more severe injury.60 Estrogen and differential cerebral blood flow may also play a role in influencing concussion severity and outcome.15,61 Further study is needed to understand if sex is a risk factor for concussion and what mechanisms may account for it, or if sex is merely a predictor of symptom reporting.62 Age Youth athletes may have a more prolonged recovery and are more susceptible to concussion accompanied by catastrophic injury. The developing brain differs physiologically from the adult brain when comparing the brain water content, degree of myelination, blood volume, blood-brain barrier, cerebral metabolic rate of glucose, blood flow, number of synapses, and geometry and elasticity of the skull’s sutures.63 Developmentally younger brains have less established engrams and may have less cognitive reserve than more mature brains.9,64 This may account for the demonstrated increase in time to recovery from concussion seen in younger athletes.65–68 It is difficult to compare studies at different levels of play (high school, college, and professional) as longer recovery times could reflect differences in study methodology, in risk tolerance and return-to-play protocols, or all of the above. Recovery patterns have not been adequately studied in athletes less than 15 years old. Catastrophic injury is more likely in younger athletes and is hypothesized to be related to the physiologic differences between younger and older brains.69–71 Sport, Position, and Style of Play Certain sports, positions, and individual playing styles have a greater risk of concussion. The rate of concussion also varies by level of play. Position and style of play also appear to affect the risk of concussion. Mechanisms of concussive injury may vary based on the sport as well as the level of play. The most common mechanism of concussion is player-to-player contact.25 It is not surprising, therefore, that sports and positions involved in frequent collision impacts sustain more concussions. Studies on professional football players have shown that “backs” (quarterbacks, wide receivers, running backs, and defensive backs) have a 3 times greater risk of concussion than “linemen,”72 and kickoffs had a 4 times higher risk of concussion than rushing or passing plays.72 In high school football players, linebackers were the most commonly concussed on the defense and running backs on the offense. In soccer players, concussions most commonly occur from player contact both at the high school level and at the college level.73–75 At the high school level, 1 study demonstrated that 25.3% of concussions were associated with illegal activity. In a prospective study of college soccer players, the mechanism of concussion was again primarily player contact, and importantly none were related to purposeful heading.76 In hockey the most common mechanism of concussive injury is checking. Genetics Studies on the association between concussion and genetic polymorphisms such as APOE e4, APOE G-219T promoter, or tau exon 6 are limited by small sample sizes, limited sports populations, retrospective study design, use of self-reported concussion history, and a lack of control groups.77,78 Some studies have suggested potential associations, but methodological weaknesses do not support definitive conclusions. A study of college athletes showed prior self-reported concussion was associated with increased odds of having either 1 APOE e4 allele or at least 1 APOE G-219T ‘T’ allele. In other reports, a cross-sectional study showed college athletes with a self-reported history of concussion were 2.7 times as likely to have APOE promoter G-219T ‘TT’ genotype after controlling for various cofounders,77 and a small prospective cohort study showed no significant association between genotype and concussion risk.46 The largest prospective cohort study available (n = 234 athletes with 45 prospective concussions) showed no significant association between APOE, APOE G-219T, tau exon 6 Hist47Tyr, and Tau exon 6 Ser53Pro and concussion risk, although Tau exon 6 Ser53Pro was trending towards significance (P = 0.09).79 A large prospective cohort study of a representative athletic population that controls for athletic exposure, prior concussion history, and other predisposing factors is necessary to determine if polymorphisms confer an increased risk for concussion, more severe concussions, or delayed neurocognitive recovery. Mood Disorders Mood disorders, either preexisting or as a result of a concussive episode, complicate both diagnosis and management of concussion. Symptoms of anxiety, depression, or irritability occur in 17% to 46% of high school and college athletes and affect the brain’s mood centers including the hippocampus, amygdala, and prefrontal brain regions, which are also affected in concussion.80,81 There is no evidence that the preexistence of a mood disorder predisposes athletes to concussion. However, when evaluating an athlete it is often difficult to determine which symptoms preceded the concussion, which have been caused by the concussion, and which symptoms are worsened after the concussion. An increased incidence of depression has been associated with a history of concussion among retired boxers and professional football players; however, these retrospective studies relied on a self-reported history and did not control for other factors that may cause depression.42,82 Anxiety, depression, and other psychological impairments may also affect neuropsychological testing, either at baseline or at repeat testing, complicating test interpretation.83,84 Knowing preinjury mood status may be beneficial to the evaluation of athletes with subsequent injury. (C) Learning Disabilities and Attention Disorders As with other conditions which share common symptomatology with concussion, it is important to take learning disorders into account in both diagnosis and management of concussion. Preinjury learning disabilities and attention deficit disorders (ADD/ADHD) may be associated with increased cognitive dysfunction and prolonged recovery after concussion. Collins found that athletes with learning disabilities and a history of concussion did proportionally worse on selected paper and pencil neuropsychological testing than those without learning disabilities.85 In 108 athletes with concussion, Lau found there was no association between learning disability or attention deficit disorder and protracted recovery.54,86,87 Learning and attention disorders share common features of concussion, such as difficulty with memory, attention, and concentration, making the diagnosis and management in these individuals more challenging. Baseline neuropsychological testing scores are lower in those with learning and attention disabilities85,88 independent of concussion history making baseline testing more important in those with learning or attention disorders if neuropsychological testing is going to be used postinjury to assist in return-to-play decisions. Migraines A history of preexisting migraine headaches may be a risk factor for concussion and may be associated with prolonged recovery. 2.9% of NCAA college basketball athletes (0.9% of men and 4.4% of women) and 22% of Australian Rules football players report migraines meeting International Headache Society criteria for diagnosis compared to 10% of the general population.89–91 An association between concussion and preexisting migraine was shown in 1 retrospective population study,92 but no association between preexisting migraine and prolonged course of concussion has been demonstrated.54,86,87 Concussion can trigger a posttraumatic migraine, and athletes with postconcussion migraine usually have more symptoms and poorer performance on neuropsychological tests than athletes with other types of headache or no headache at all.93 In addition, Lau found that athletes (without preexisting diagnosis of migraines) who developed symptoms in the “migraine symptoms complex”, which included headaches, visual problems, dizziness, noise/light sensitivity, nausea/vomiting, balance problems, and numbness/tingling, had a more protracted recovery.54 Similar to mood, learning, and attention disorders, it is important to understand preinjury cognitive or psychological disorders in order to optimize management. Management of Concussion Preseason Preparation for the care of concussed athletes begins prior to any practice or competition with a preparticipation exam (PPE) and the development of an emergency action plan. (C) The preparticipation exam should include concussion-related questions including a past history of concussion (number, frequency, severity, and recovery) and the presence of mood, learning, attention, or migraine disorders.94 (C) This information can be used to assess risk and for historical reference in the case of injury. The exact role and impact on concussion management of baseline testing remains unclear, as no study has shown that use of these tests provides better short- or long-term outcomes for athletes with concussion. The preseason evaluation may also include baseline symptom scores, baseline balance testing, a baseline sideline evaluation tool (Sport Concussion Assessment Tool 2 [SCAT2], NFL Sideline Concussion Assessment Tool), and/or baseline computerized neuropsychological (NP) testing. This baseline testing may be more important in high-risk athletes with a prior history of concussion, with confounding conditions (learning disability, mood and attention disorders, migraine headaches) and sports with a higher incidence of concussion.95,96 (C) The reliability of preseason testing as a dependable baseline assessment to compare with postinjury testing performed weeks or months later is also controversial and for many tests unknown. While baseline testing is increasingly used in practice and may have a role in the preseason evaluation of high risk athletes, the role of baseline tests in other settings is unknown.97 (C) More research is needed to define which baseline tests should be performed and in which athletes. Preseason testing requires honest effort on the part of an athlete. Balance testing is time intensive, but can be done by nonphysician personnel. Computerized NP testing requires adequate resources and a quiet environment for best results, but can be done in large groups. Neuropsychological testing does require health professionals who are competent in test interpretation. On-Field Management The first step in assessing a collapsed athlete is the check for airway, breathing, and heart function, followed by a physical evaluation to exclude cervical spine injury and/or more serious brain injury. (C) If cervical spine injury cannot be eliminated, neck immobilization and immediate transfer emergency department capable of advanced neurological imaging and management of cervical trauma should follow. (C) Emergency transfer should also occur if there are signs of a more serious brain injury such as deteriorating mental status, focal neurological findings (abnormal or unequal pupil reaction, abnormalities with extra-ocular movements, abnormalities on a screening motor/sensory exam), or worsening of symptoms. (C) If cervical spine and more serious brain injury can be excluded with history and physical exam, then a more detailed history of injury and an examination that includes symptoms, cognitive and balance assessment, and ne

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