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Kevin M. Guskiewicz, PhD, ATC, FACSM; Scott L. Bruce, MS, ATC; Robert C. Cantu, MD, FACSM; Michael S. Ferrara, PhD, ATC; James P. Kelly, MD; Michael McCrea, PhD; Margot Putukian, MD, FACSM; and Tamara C. Valovich McLeod, PhD, ATC, CSCS, contributed to conception and design, acquisition and analysis and interpretation of the data; and drafting, critical revision, and final approval of the article.
Sport in today's society is more popular than probably ever imagined. Large numbers of athletes participate in a variety of youth, high school, collegiate, professional, and recreational sports. As sport becomes more of a fixture in the lives of Americans, a burden of responsibility falls on the shoulders of the various organizations, coaches, parents, clinicians, officials, and researchers to provide an environment that minimizes the risk of injury in all sports. For example, the research-based recommendations made for football between 1976 and 1980 resulted in a significant reduction in the incidence of fatalities and nonfatal catastrophic injuries. In 1968, 36 brain and cervical spine fatalities occurred in high school and collegiate football. The number had dropped to zero in 1990 and has averaged about 5 per year since then.1 This decrease was attributed to a variety of factors, including (1) rule changes, which have outlawed spearing and butt blocking, (2) player education about the rule changes and the consequences of not following the rules, (3) implementation of equipment standards, (4) availability of alternative assessment techniques, (5) a marked reduction in physical contact time during practice sessions, (6) a heightened awareness among clinicians of the dangers involved in returning an athlete to competition too early, and (7) the athlete's awareness of the risks associated with concussion.
Research in the area of sport-related concussion has provided the athletic training and medical professions with valuable new knowledge in recent years. Certified athletic trainers, who on average care for 7 concussive injuries per year,2 have been forced to rethink how they manage sport-related concussion. Recurrent concussions to several high-profile athletes, some of whom were forced into retirement as a result, have increased awareness among sports medicine personnel and the general public. Bridging the gap between research and clinical practice is the key to reducing the incidence and severity of sport-related concussion and improving return-to-play decisions. This position statement should provide valuable information and recommendations for certified athletic trainers (ATCs), physicians, and other medical professionals caring for athletes at the youth, high school, collegiate, and elite levels. The following recommendations are derived from the most recent scientific and clinic-based literature on sport-related concussion. The justification for these recommendations is presented in the summary statement following the recommendations. The summary statement is organized into the following sections: “Defining and Recognizing Concussion,” “Evaluating and Making the Return-to-Play Decision,” “Concussion Assessment Tools,” “When to Refer an Athlete to a Physician After Concussion,” “When to Disqualify an Athlete,” “Special Considerations for the Young Athlete,” “Home Care,” and “Equipment Issues.”
Perhaps the most challenging aspect of managing sport-related concussion is recognizing the injury, especially in athletes with no obvious signs that a concussion has actually occurred. The immediate management of the head-injured athlete depends on the nature and severity of the injury. Several terms are used to describe this injury, the most global being TBI, which can be classified into 2 types: focal and diffuse. Focal or posttraumatic intracranial mass lesions include subdural hematomas, epidural hematomas, cerebral contusions, and intracerebral hemorrhages and hematomas. These are considered uncommon in sport but are serious injuries; the ATC must be able to detect signs of clinical deterioration or worsening symptoms during serial assessments. Signs and symptoms of these focal vascular emergencies can include LOC, cranial nerve deficits, mental status deterioration, and worsening symptoms. Concern for a significant focal injury should also be raised if these signs or symptoms occur after an initial lucid period in which the athlete seemed normal.
Diffuse brain injuries can result in widespread or global disruption of neurologic function and are not usually associated with macroscopically visible brain lesions except in the most severe cases. Most diffuse injuries involve an acceleration-deceleration motion, either within a linear plane or in a rotational direction or both. In these cases, lesions are caused by the brain being shaken within the skull.4,5 The brain is suspended within the skull in cerebrospinal fluid (CSF) and has several dural attachments to bony ridges that make up the inner contours of the skull. With a linear acceleration-deceleration mechanism (side to side or front to back), the brain experiences a sudden momentum change that can result in tissue damage. The key elements of injury mechanism are the velocity of the head before impact, the time over which the force is applied, and the magnitude of the force.4,5 Rotational acceleration-deceleration injuries are believed to be the primary injury mechanism for the most severe diffuse brain injuries. Structural diffuse brain injury (diffuse axonal injury [DAI]) is the most severe type of diffuse injury because axonal disruption occurs, typically resulting in disturbance of cognitive functions, such as concentration and memory. In its most severe form, DAI can disrupt the brain-stem centers responsible for breathing, heart rate, and wakefulness.4,5
Cerebral concussion, which is the focus of this position statement, can best be classified as a mild diffuse injury and is often referred to as mild TBI (MTBI). The injury involves an acceleration-deceleration mechanism in which a blow to the head or the head striking an object results in 1 or more of the following conditions: headache, nausea, vomiting, dizziness, balance problems, feeling “slowed down,” fatigue, trouble sleeping, drowsiness, sensitivity to light or noise, LOC, blurred vision, difficulty remembering, or difficulty concentrating.6 In 1966, the Congress of Neurological Surgeons proposed the following consensus definition of concussion, subsequently endorsed by a variety of medical associations: “Concussion is a clinical syndrome characterized by immediate and transient impairment of neural functions, such as alteration of consciousness, disturbance of vision, equilibrium, etc, due to mechanical forces.”7 Although the definition received widespread consensus in 1966, more contemporary opinion (as concluded at the First International Conference on Concussion in Sport, Vienna, 20018) was that this definition fails to include many of the predominant clinical features of concussion, such as headache and nausea. It is often reported that there is no universal agreement on the standard definition or nature of concussion; however, agreement does exist on several features that incorporate clinical, pathologic, and biomechanical injury constructs associated with head injury:
Occasionally, players sustain a blow to the head resulting in a stunned confusional state that resolves within minutes. The colloquial term “ding” is often used to describe this initial state. However, the use of this term is not recommended because this stunned confusional state is still considered a concussion resulting in symptoms, although only very short in duration, that should not be dismissed in a cavalier fashion. It is essential that this injury be reevaluated frequently to determine if a more serious injury has occurred, because often the evolving signs and symptoms of a concussion are not evident until several minutes to hours later.
Although it is important for the ATC to recognize and eventually classify the concussive injury, it is equally important for the athlete to understand the signs and symptoms of a concussion as well as the potential negative consequences (eg, second-impact syndrome and predisposition to future concussions) of not reporting a concussive injury. Once the athlete has a better understanding of the injury, he or she can provide a more accurate report of the concussion history.
A forceful blow to the resting, movable head usually produces maximum brain injury beneath the point of cranial impact (coup injury). A moving head hitting an unyielding object usually produces maximum brain injury opposite the site of cranial impact (contrecoup injury) as the brain shifts within the cranium. When the head is accelerated before impact, the brain lags toward the trailing surface, thus squeezing away the CSF and creating maximal shearing forces at this site. This brain lag actually thickens the layer of CSF under the point of impact, which explains the lack of coup injury in the moving head. Alternatively, when the head is stationary before impact, neither brain lag nor disproportionate distribution of CSF occurs, accounting for the absence of contrecoup injury and the presence of coup injury.4,5
No scientific evidence suggests that one type of injury (coup or contrecoup) is more serious than the other or that symptoms present any differently. Many sport-related concussions are the result of a combined coup-contrecoup mechanism, involving damage to the brain on both the side of initial impact and the opposite side of the brain due to brain lag. Regardless of whether the athlete has sustained a coup, contrecoup, or combined coup-contrecoup injury, the ATC should manage the injury the same.
Three types of stresses can be generated by an applied force to injure the brain: compressive, tensile, and shearing. Compression involves a crushing force in which the tissue cannot absorb any additional force or load. Tension involves pulling or stretching of tissue, whereas shearing involves a force that moves across the parallel organization of the tissue. Brief, uniform compressive stresses are fairly well tolerated by neural tissue, but tension and shearing stresses are very poorly tolerated.4,9
Traditionally, computed tomography (CT) and magnetic resonance imaging (MRI) have been considered useful in identifying certain types of brain lesions; however, they have been of little value in assessing less severe head injuries, such as cerebral concussion, and contributing to the RTP decision. A CT scan is often indicated emergently if a focal injury such as an acute subdural or epidural bleed is suspected; this study easily demonstrates acute blood collection and skull fracture, but an MRI is superior at demonstrating an isodense subacute or chronic subdural hematoma that may be weeks old.10,11 Newer structural MRI modalities, including gradient echo, perfusion, and diffusion-weighted imaging, are more sensitive for structural abnormalities (eg, vascular shearing) compared with other diagnostic imaging techniques.10 Functional imaging technologies (eg, positron emission tomography [PET], single-photon emission computerized tomography [SPECT], and functional MRI [fMRI]) are also yielding promising early results and may help define concussion recovery.12 Presently, no neuroanatomic or physiologic measurements can be used to determine the severity of a concussion or when complete recovery has occurred in an individual athlete after a concussion.
Results from a thorough clinical examination conducted by both the ATC and the physician cannot be overlooked and should be considered very important pieces of the concussion puzzle. These evaluations should include a thorough history (including number and severity of previous head injuries), observation (including pupil responses), palpation, and special tests (including simple tests of memory, concentration, and coordination and a cranial nerve assessment). In many situations, a physician will not be present at the time of the concussion, and the ATC will be forced to act on behalf of the sports medicine team. More formal neuropsychological testing and postural-stability testing should be viewed as adjuncts to the initial clinical and repeat evaluations (see “Concussion Assessment Tools”). The ATC-physician team must also consider referral options to specialists such as neurologists, neurosurgeons, neuropsychologists, and neuro-otologists, depending on the injury severity and situation. Referrals for imaging tests such as CT, MRI, or electronystagmography are also options that sometimes can aid in the diagnosis and/or management of sport-related concussion but are typically used only in cases involving LOC, severe amnesia, abnormal physical or neurologic findings, or increasing or intensified symptoms.
The definition of concussion is often expanded to include mild, moderate, and severe injuries. Several early grading scales and RTP guidelines early were proposed for classifying and managing cerebral concussions.6,13–20 None of the scales have been universally accepted or followed with much consistency by the sports medicine community. In addition, most of these classification systems denote the most severe injuries as associated with LOC, which we now know is not always predictive of recovery after a brain injury.21,22 It is important for the ATC and other health care providers to recognize the importance of identifying retrograde amnesia and anterograde amnesia, LOC, and other signs and symptoms present and to manage each episode independently.
The ATC must recognize that no 2 concussions are identical and that the resulting symptoms can be very different, depending on the force of the blow to the head, the degree of metabolic dysfunction, the tissue damage and duration of time needed to recover, the number of previous concussions, and the time between injuries. All these factors must be considered when managing an athlete suffering from cerebral concussion.3 The 2 most recognizable signs of a concussion are LOC and amnesia; yet, as previously mentioned, neither is required for an injury to be classified as a concussion. A 2000 study of 1003 concussions sustained by high school and collegiate football players revealed that LOC and amnesia presented infrequently, 9% and 27% of all cases, respectively, whereas other signs and symptoms, such as headache, dizziness, confusion, disorientation, and blurred vision, were much more common.23 After the initial concussion evaluation, the ATC should determine whether the athlete requires more advanced medical intervention on an emergent basis or whether the team physician should be contacted for an RTP decision (Appendix B). It may be helpful if the injury is graded throughout the process, but this grading is likely to be more important for treating subsequent injuries than the current injury.
Most grading systems rely heavily on LOC and amnesia as indicators of injury severity. Recent research, however, suggests that these 2 factors, either alone or in combination, are not good predictors of injury severity. A number of authors have documented no association between brief (<1 minute) LOC and abnormalities on neuropsychological testing at 48 hours, raising concern for brief LOC as a predictor of recovery after concussion.8,22,24–27 Studies involving high school and collegiate athletes with concussion revealed no association between (1) LOC and duration of symptoms or (2) LOC and neuropsychological and balance tests at 3, 24, 48, 72, and 96 hours postinjury.21,28,29 In other words, athletes experiencing LOC were similar to athletes without LOC on these same injury-severity markers.
With respect to amnesia, the issue is more clouded because findings have been inconsistent. Several studies of nonathletes30–37 suggest that the duration of posttraumatic amnesia correlates with the severity and outcome of severe TBI but not with mild TBI or concussion.38–40 More contemporary studies of athletes with concussion are also clouded. Two unrelated, prospective studies of concussion suggest that the presence of amnesia best correlates with abnormal neuropsychological testing at 48 hours and with the duration and number of other postconcussion signs and symptoms.24,41 However, more recently, investigations of high school and collegiate athletes with concussion revealed no association between (1) amnesia and duration of symptoms or (2) amnesia and neuropsychological and balance tests at 3, 24, 48, 72, and 96 hours post-injury.21,28,29 Of importance in these studies is the significant association between symptom-severity score (within the initial 3 hours postinjury) and the total duration of symptoms (measured until asymptomatic). Although these findings suggest that initial symptom severity is probably a better indicator than either LOC or amnesia in predicting length of recovery, amnesia was recently found to predict symptom and neurocognitive deficits at 2 days postinjury.42 More research is needed in this area to help improve clinical decision making.
It has been suggested that LOC and amnesia, especially when prolonged, should not be ignored,43,44 but evidence for their usefulness in establishing RTP guidelines is scarce. Loss of consciousness, whether it occurs immediately or after an initially lucid interval, is important in that it may signify a more serious vascular brain injury. Other postconcussion signs and symptoms should be specifically addressed for presence and duration when the ATC is evaluating the athlete. Determining whether a cervical spine injury has occurred is also of major importance because it is often associated with head injury and should not be missed. If the athlete complains of neck pain or has cervical spine tenderness, cervical spine immobilization should be considered. If a cervical spine injury is ruled out and the athlete is taken to the sideline, a thorough clinical examination should follow, including a complete neurologic examination and cognitive evaluation. The ATC must note the time of the injury and then maintain a timed assessment form to follow the athlete's symptoms and examinations serially. It is often difficult to pay attention to the time that has passed after an injury. Therefore, it is important for one member of the medical team to track time during the evaluation process and record all pertinent information. After an initial evaluation, the clinician must determine whether the injured athlete requires more advanced medical intervention and eventually grade the injury and make an RTP decision that can occur within minutes, hours, days, or weeks of the injury.
There are currently 3 approaches to grading sport-related concussion. One approach is to grade the concussion at the time of the injury on the basis of the signs and symptoms present at the time of the concussion and within the first 15 minutes after injury. The American Academy of Neurology Concussion Grading Scale (Table (Table11)6 has been widely used with this approach. It permits the ATC to grade the injury primarily on the basis of LOC and to provide the athlete, coach, and parent with an estimation of injury severity. A disadvantage to this approach is that many injuries behave differently than expected on initial evaluation, potentially creating more difficulties with the athlete, coach, or parent and making the RTP decision more challenging. Another approach is to grade the concussion on the basis of the presence and overall duration of symptoms. This approach is best addressed using the Cantu Evidence-Based Grading Scale (Table (Table22),43 which guides the ATC to grade the injury only after all concussion signs and symptoms have resolved. This scale places less emphasis on LOC as a potential predictor of subsequent impairment and additional weight on overall symptom duration.3,43 Finally, a third approach to the grading-scale dilemma is to not use a grading scale but rather focus attention on the athlete's recovery via symptoms, neuropsychological tests, and postural-stability tests. This line of thinking is that the ATC should not place too much emphasis on the grading system or grade but should instead focus on whether the athlete is symptomatic or symptom free. Once the athlete is asymptomatic, a stepwise progression should be implemented that increases demands over several days. This progression will be different for athletes who are withheld for several weeks compared with those athletes withheld for just a few days. This multitiered approach was summarized and supported by consensus at the 2001 Vienna Conference on Concussion in Sport.8
The question raised most often regarding the concussion grading and RTP systems is one of practicality in the sport setting. Many clinicians believe that the RTP guidelines are too conservative and, therefore, choose to base decisions on clinical judgment of individual cases rather than on a general recommendation. It has been reported that 30% of all high school and collegiate football players sustaining concussions return to competition on the same day of injury; the remaining 70% average 4 days of rest before returning to participation.23 Many RTP guidelines call for the athlete to be symptom free for at least 7 days before returning to participation after a grade 1 or 2 concussion.6,13,15,17,43,44 Although many clinicians deviate from these recommendations and are more liberal in making RTP decisions, recent studies by Guskiewicz and McCrea et al21,29 suggest that perhaps the 7-day waiting period can minimize the risk of recurrent injury. On average, athletes required 7 days to fully recover after concussion. Same-season repeat injuries typically take place within a short window of time, 7 to 10 days after the first concussion,21 supporting the concept that there may be increased neuronal vulnerability or blood-flow changes during that time, similar to those reported by Giza, Hovda, et al45–47 in animal models.
Returning an athlete to participation should follow a progression that begins once the athlete is completely symptom free. All signs and symptoms should be evaluated using a graded symptom scale or checklist (described in “Concussion Assessment Tools”) when performing follow-up assessments and should be evaluated both at rest and after exertional maneuvers such as biking, jogging, sit-ups, and push-ups. Baseline measurements of neuropsychological and postural stability are strongly recommended for comparing with postinjury measurements. If these exertional tests do not produce symptoms, either acutely or in delayed fashion, the athlete can then participate in sport-specific skills that allow return to practice but should remain out of any activities that put him or her at risk for recurrent head injury. For the basketball player, this may include shooting baskets or participating in walk-throughs, and for the soccer player, this may include dribbling or shooting drills or other sport-specific activities. These restricted and monitored activities should be continued for the first few days after becoming symptom free. The athlete should be monitored periodically throughout and after these sessions to determine if any symptoms develop or increase in intensity. Before returning to full contact participation, the athlete should be reassessed using neuropsychological and postural-stability tests if available. If all scores have returned to baseline or better, return to full participation can be considered after further clinical evaluation. It is strongly recommended that after recurrent injury, especially within-season repeat injuries, the athlete be withheld for an extended period of time (approximately 7 days) after symptoms have resolved.
Sports medicine clinicians are increasingly using standardized methods to obtain a more objective measurement of postconcussion signs and symptoms, cognitive dysfunction, and postural instability. These methods allow the clinician to quantify the severity of injury and measure the player's progress over the course of postinjury recovery. An emerging model of sport concussion assessment involves the use of brief screening tools to evaluate postconcussion signs and symptoms, cognitive functioning, and postural stability on the sideline immediately after a concussion and neuropsychological testing to track recovery further out from the time of injury. Ultimately, these tests, when interpreted with the physical examination and other aspects of the injury evaluation, assist the ATC and other sports medicine professionals in the RTP decision-making process.
Data from objective measures of cognitive functioning, postural stability, and postconcussion signs and symptoms are most helpful in making a determination about severity of injury and postinjury recovery when preinjury baseline data for an individual athlete are available.3,8,24,29,41 Baseline testing provides an indicator of what is “normal” for that particular athlete while also establishing the most accurate and reliable benchmark against which postinjury results can be compared. It is important to obtain a baseline symptom assessment in addition to baseline cognitive and other ability testing. Without baseline measures, the athlete's postinjury performance on neuropsychological testing and other concussion assessment measures must be interpreted by comparison with available population normative values, which ideally are based on a large sample of the representative population. Normative data for competitive athletes on conventional (ie, paper-and-pencil) and computerized neuropsychological tests and other concussion assessment measures are now more readily available from large-scale research studies, but baseline data on an individual athlete still provide the greatest clinical accuracy in interpreting postinjury test results. When performing baseline testing, a suitable testing environment eliminates all distractions that could alter the baseline performance and enhances the likelihood that all athletes are providing maximal effort. Most important, all evaluators should be aware of a test's user requirements and be appropriately trained in the standardized instructions for test administration and scoring before embarking on baseline testing or adopting a concussion testing paradigm for clinical use.
Several models exist for implementing baseline testing. Ideally, preseason baseline testing is conducted before athletes are exposed to the risk of concussion during sport participation (eg, before contact drills during football). Some programs choose to conduct baseline testing as part of the preparticipation physical examination process. In this model, stations are established for various testing methods (eg, history collection, symptom assessment, neuropsychological testing, and balance testing), and athletes complete the evaluation sequence after being seen by the attending physician or ATC. This approach has the advantage of testing large groups of athletes in 1 session, while they are already in the mindset of undergoing a preseason physical examination. When preseason examinations are not conducted in a systematic group arrangement, alternative approaches can be considered. In any case, it is helpful to conduct all modules of baseline testing on players in 1 session to limit the complications of scheduling multiple testing times and to keep testing conditions constant for the athletes. One should allow adequate planning time (eg, 3 months) to implement a baseline testing module. Often this equates to conducting baseline testing for fall sports during the spring semester, before school is recessed for the summer. The benefits of interpreting postinjury data for an athlete after a concussion far outweigh the considerable time and human resources dedicated to baseline testing.
Collecting histories on individual athletes is also a vital part of baseline testing, especially in establishing whether the athlete has any history of concussion, neurologic disorder, or other remarkable medical conditions. Specifically with respect to concussion, it is important to establish (1) whether the player has any history of concussions and, if so, how many and (2) injury characteristics of previous concussions (eg, LOC, amnesia, symptoms, recovery time, time lost from participation, and medical treatment). For athletes with a history of multiple concussions, it is also important to clarify any apparent pattern of (1) concussions occurring as a result of lighter impacts, (2) concussions occurring closer together in time, (3) a lengthier recovery time with successive concussions, and (4) a less complete recovery with each injury. Documenting a history of attentional disorders, learning disability, or other cognitive development disorders is also critical, especially in interpreting an individual player's baseline and postinjury performance on neuropsychological testing. If resources do not allow for preseason examinations in all athletes, at least a concerted effort to evaluate those athletes with a previous history of concussion should be made because of the awareness of increased risk for subsequent concussions in this group.
Self-reported symptoms are among the more obvious and recognizable ways to assess the effects of concussion. Typical self-reported symptoms after a concussion include but are not limited to headache; dizziness; nausea; vomiting; feeling “in a fog”; feeling “slowed down”; trouble falling asleep; sleeping more than usual; fatigue; drowsiness; sensitivity to light or noise; unsteadiness or loss of balance; feeling “dinged,” dazed, or stunned; seeing stars or flashing lights; ringing in the ears; and double vision.8,26,48 Self-reported symptoms are referenced by many of the concussion grading scales.10,43,44,49 The presence of self-reported symptoms serves as a major contraindication for RTP, and, based on current recommendations, the athlete should be fully symptom free for at least 7 days at rest and during exertion before returning to play.43,44
A number of concussion symptom checklists43,50–52 and scales26,41,48,53 have been used in both research and clinical settings. A symptom checklist that provides a list of concussion-related symptoms allows the athlete to report whether the symptom is present by responding either “yes” (experiencing the symptom) or “no” (not experiencing the symptom). A symptom scale is a summative measure that allows the athlete to describe the extent to which he or she is experiencing the symptom. These instruments commonly incorporate a Likert-type scale that allows the player to rate the severity or frequency of postconcussion symptoms. These scores are then summed to form a composite score that yields a quantitative measure of overall injury severity and a benchmark against which to track postinjury symptom recovery. Initial evidence has been provided for the structural validity of a self-report concussion symptom scale.48 Obtaining a baseline symptom score is helpful to establish any preexisting symptoms attributable to factors other than the head injury (eg, illness, fatigue, or somatization). Serial administration of the symptom checklist is the recommended method of tracking symptom resolution over time (see Appendix A).
Cognitive screening instruments similar to the physician's mini mental status examination objectify what is often a subjective impression of cognitive abnormalities. Various methods have been suggested for a systematic survey of mental status and cognitive function in the athlete with a concussion. The SAC was developed to provide sports medicine clinicians with a brief, objective tool for assessing the injured athlete's mental status during the acute period after concussion (eg, sport sideline, locker room, and clinic).54 The SAC includes measures of orientation, immediate memory, concentration, and delayed recall that sum to 30 points.55 Lower scores on the SAC indicate more severe cognitive impairment. The SAC also includes assessments of strength, sensation, and coordination and a standard neurologic examination but should not replace the clinician's thorough physical examination or referral for more extensive neuropsychological evaluation when indicated. Information about the occurrence and duration of LOC and amnesia is also recorded on the SAC. Alternate forms of the SAC are available to minimize the practice effects during retesting. The SAC takes about 5 minutes to administer and should be used only after the clinician's thorough review of the training manual and instructional video on the administration, scoring, and interpretation of the instrument.
The SAC has demonstrated reliability29,55,56 and validity29,56,57 in detecting mental status changes after a concussion. Recent evidence suggests that a decline of 1 point or more from baseline classified injured and uninjured players with a level of 94% sensitivity and 76% specificity.56 The SAC is also sensitive to detecting more severe neurocognitive changes in injured athletes with LOC or amnesia associated with their concussions.57 The SAC is most useful in the assessment of acute cognitive dysfunction resulting from concussion, with sensitivity and specificity comparable with extensive neuropsychological testing batteries during the initial 2 to 3 days after concussion.29,58,59 As with neuropsychological testing, sensitivity and specificity of the SAC in concussion assessment are maximized when individual baseline test data are available.29,55,56,60
A number of postural-stability tests have been used to assess the effects of concussion in the clinical and laboratory settings. The Romberg and stork stand were basic tests used to assess balance and coordination. Riemann et al61–62 developed the Balance Error Scoring System (BESS) based on existing theories of posturography. The BESS uses 3 stance positions and tests on both a firm and a foam surface with the eyes closed (for a total of 6 trials). The administration and scoring procedures are found in several publications.61–63 The BESS has established good test-retest reliability and good concurrent validity when compared with laboratory forceplate measures52,62 and significant group differences, with an increased number of errors for days 1, 3, and 5 postinjury when compared with controls.52 Thus, the BESS can be used as a clinical measure in identifying balance impairment that could indicate a neurologic deficit.
The NeuroCom Smart Balance Master System (NeuroCom International, Clackamas, OR) is a forceplate system that measures vertical ground reaction forces produced by the body's center of gravity moving around a fixed base of support. The Sensory Organization Test (SOT, NeuroCom International) is designed to disrupt various sensory systems, including the visual, somatosensory, and vestibular systems. The SOT consists of 6 conditions with 3 trials per condition, for a total of 18 trials, with each trial lasting 20 seconds. The complete administration has been described previously.52,64 The SOT has produced significant findings related to the assessment of concussion recovery. In a sample of 36 athletes with concussion, the mean stability (composite score) and vestibular and visual ratios demonstrated deficits for up to 5 days postinjury.52 The greatest deficits were seen 24 hours postinjury, and the athletes with concussion demonstrated a gradual recovery during the 5-day period to within 6% of baseline scores. These results were confirmed by Peterson et al,65 who found that these deficits continued for up to 10 days after concussion. These findings reveal a sensory interaction problem from the effects of concussion with measurable changes in overall postural stability.
Neuropsychological testing has historically been used to evaluate various cognitive domains known to be preferentially susceptible to the effects of concussion and TBI. In recent years, neuropsychological testing to evaluate the effects of sport-related concussion has gained much attention in the sport concussion literature.20,21,26,29,48,52,58,59,65–69 The work of Barth et al,70 who studied more than 2000 collegiate football players from 10 universities, was the first project to institute baseline neuropsychological testing. Similar programs are now commonplace among many collegiate and professional teams, and interest is growing at the high school level. Several recent studies have supported the use of neuropsychological testing as a valuable tool to evaluate the cognitive effects and recovery after sport-related concussion,24,28,29,41,42,50–52,57,65,66,71–75 but its feasibility for sideline use is not likely realistic. As is the case with other concussion assessment tools, baseline neuropsychological testing is recommended, when possible, to establish a normative level of neurocognitive functioning for individual athletes.24,28,29,41,50–52,57–59,66,69,73–75 Baseline neuropsychological testing typically takes 20 to 30 minutes per athlete.
Before implementing a neuropsychological testing program, the ATC must consider several issues, including test-specific training requirements and methodologic issues, the practicality of baseline testing, the reliability and validity of individual tests comprising the test battery, and the protocol for interpretation of the postinjury test results. Barr76 provided an excellent review on the methodologic and professional issues associated with neuropsychological testing in sport concussion assessment. Most states require advanced training and licensure to purchase and use neuropsychological tests for clinical purposes. Neuropsychological tests are also copyright protected to prevent inappropriate distribution or use by unqualified professionals. At present, these requirements necessitate that a licensed psychologist, preferably one Board certified in clinical neuropsychology or with clinical experience in the evaluation of sport-related concussion, oversee and supervise the clinical application of neuropsychological testing for sport concussion assessment. These factors likely restrict how widely neuropsychological testing can be used to assess sport-related concussion, especially at the high school level and in rural areas where neuropsychologists are not readily available for consultation.
Neuropsychologists, ATCs, and sports medicine clinicians are faced with the challenge of designing a model that jointly upholds the testing standards of neuropsychology and meets the clinical needs of the sports medicine community without undue burden. The cost of neuropsychological testing, either conventional or computerized, is also a factor in how widely this method can be implemented, especially at the high school level. Consultation fees for the neuropsychologist can be considerable if work is not done on a pro bono basis, and some computerized testing companies charge a consulting fee for interpreting postinjury test results by telephone.
Although no clear indications exist as to which are the best individual neuropsychological tests to evaluate sport concussion, the use of multiple instruments as a “test battery” offers clinicians greater potential for recognizing any cognitive deficits incurred from the injury. A number of neuropsychological tests and test batteries have been used to assess sport-related concussion. Table Table33 provides a brief description of the paper-and-pencil neuropsychological tests commonly used by neuropsychologists in the assessment of sport concussion. Sport concussion batteries should include measures of cognitive abilities most susceptible to change after concussion, including attention and concentration, cognitive processing (speed and efficiency), learning and memory, working memory, executive functioning, and verbal fluency. Tests of attention and concentration50,52,74,77 and memory functioning41 have been reported as the most sensitive to the acute effects of concussion. The athlete's age, sex, primary language, and level of education should be considered when selecting a test battery.68
Recently, a number of computerized neuropsychological testing programs have been designed for the assessment of athletes after concussion. The Automated Neuropsychological Assessment Metrics (ANAM), CogSport, Concussion Resolution Index, and Immediate Postconcussion Assessment and Cognitive Testing (ImPACT) are all currently available and have shown promise for reliable and valid concussion assessment (Table (Table44).24,41,51,53,66,71,72,75,78–84 The primary advantages to computerized testing are the ease of administration, ability to baseline test a large number of athletes in a short period of time, and multiple forms used within the testing paradigm to reduce the practice effects. Collie et al71 summarized the advantage and disadvantages of computerized versus traditional paper-and-pencil testing.
As outlined, in the case of conventional neuropsychological testing, several of the same challenges must be addressed before computerized testing becomes a widely used method of sport concussion assessment. Issues requiring further consideration include demonstrated test reliability; validity, sensitivity, and specificity in the peer-reviewed literature; required user training and qualifications; the necessary role of the licensed psychologist for clinical interpretation of postinjury test results; hardware and software issues inherent to computerized testing; and user costs.71 Progress is being made on many of these issues, but further clinical research is required to provide clinicians with the most effective neuropsychological assessment tools and maintain the testing standards of neuropsychology.
Neuropsychological testing is not a tool that should be used to diagnose the injury (ie, concussion); however, it can be very useful in measuring recovery once it has been determined that a concussion has occurred. The point(s) at which postinjury neuropsychological testing should occur has been a topic of debate. A variety of testing formats has been used to evaluate short-term recovery from concussion.24,41,50,73,75,82 Two approaches are most common. The first incorporates neuropsychological testing only after the injured player reports that his or her symptoms are completely gone. This approach is based on the conceptual foundation that an athlete should not participate while symptomatic, regardless of neuropsychological test performance. Unnecessary serial neuropsychological testing, in addition to being burdensome and costly to the athlete and medical staff, also introduces practice effects that may confound the interpretation of performance in subsequent postinjury testing sessions.85 The second approach incorporates neuropsychological testing at fixed time points (eg, postinjury day 1, day 7, and so on) to track postinjury recovery. This approach is often appropriate for prospective research protocols but is unnecessary in a clinical setting when the player is still symptomatic and will be withheld from competition regardless of the neuropsychological test results. In this model, serial testing can be used until neuropsychological testing returns to normal, preinjury levels and the player is completely symptom free.
Measuring “recovery” on neuropsychological tests and other clinical instruments is often a complex statistical matter, further complicated by practice effects and other psychometric dynamics affected by serial testing, even when preinjury baseline data are available for individual athletes. The use of statistical models that empirically identify meaningful change while controlling for practice effects on serial testing may provide the clinician with the most precise benchmark in determining postinjury recovery, above and beyond the simple conclusion that the player is “back to baseline.” The complexity of this analysis is the basis for the neuropsychologist overseeing the clinical interpretation of test data to determine injury severity and recovery. Further research is required to clarify the guidelines for determining and tracking recovery on specific measures after concussion. The clinician should also be aware that any concussion assessment tool, either brief screening instruments or more extensive neuropsychological testing, comes with some degree of risk for false negatives (eg, a player performs within what would be considered the normal range on the measure before actually reaching a complete clinical recovery after concussion). Therefore, test results should always be interpreted in the context of all clinical information, including the player's medical history. Also, caution should be exercised in neuropsychological test interpretation when pre-injury baseline data do not exist. Numerous factors apart from the direct effects of concussion can influence test performance (Table (Table55).
Although most sport-related concussions are considered mild head injuries, the potential exists for complications and life-threatening injuries. Each ATC should be concerned about the potential for the condition of an athlete with a concussion to deteriorate. This downward trend can occur immediately (minutes to hours) or over several days after the injury. As discussed earlier, the spectrum of sport-related head injuries includes more threatening injuries, such as epidural and subdural hematomas and second-impact syndrome. Postconcussion syndrome, however, is a more likely consequence of a sport-related concussion. Not every sport-related concussion warrants immediate physician referral, but ATCs must be able to recognize those injuries that require further attention and provide an appropriate referral for advanced care, which may include neuroimaging. Serial assessments and physician follow-up are important parts of the evaluation of the athlete with a concussion. Referrals should be made to medical personnel with experience managing sport-related concussion. The ATC should monitor vital signs and level of consciousness every 5 minutes after a concussion until the athlete's condition stabilizes and improves. The athlete should also be monitored over the next few hours and days after the injury for delayed signs and symptoms and to assess recovery. Appendix B outlines scenarios that warrant physician referral or, in many cases, transport to the nearest hospital emergency department.
Return to participation after severe or repetitive concussive injury should be considered only if the athlete is completely symptom free and has a normal neurologic examination, normal neuropsychological and postural-stability examinations, and, if obtained, normal neuroimaging studies (ie, MRI with gradient echo). It may not be practical or even possible to use all these assessments in all athletes or young children, but a cautious clinical judgment should take into account all evaluation options. Each injured athlete should be considered individually, with consideration for factors including age, level of participation, nature of the sport (high risk versus low risk), and concussion history.
Standardized neuropsychological testing, which typically assesses orientation, immediate and delayed memory recall, and concentration may assist the ATC and physician in determining when to disqualify an athlete from further participation.60 Balance testing may provide additional information to assist the clinician in the decision-making process of whether to disqualify an individual after a concussion.52 When to disqualify the athlete is one of the most important decisions facing the ATC and team physician when dealing with an athlete suffering from a concussion. This includes not only when to disqualify for a single practice or event but also when to disqualify for the season or for a career.
The decision to disqualify an individual from further participation on the day of the concussive episode is based on the sideline evaluation, the symptoms the athlete is experiencing, the severity of the apparent symptoms, and the patient's past history.86 The literature is clear: any episode involving LOC or persistent symptoms related to concussion (headache, dizziness, amnesia, and so on), regardless of how mild and transient, warrants disqualification for the remainder of that day's activities.8,9,13,19,43,60,87 More recent studies of high school and collegiate athletes underscore the importance of ensuring that the athlete is symptom free before returning to participation on the same day; even when the player is symptom free within 15 to 20 minutes after the concussive episode, he or she may still demonstrate delayed symptoms or depressed neurocognitive levels. Lovell et al88 found significant memory deficits 36 hours postinjury in athletes who were symptom free within 15 minutes of a mild concussion. Guskiewicz et al21 found that 33% (10/30) of the players with concussion who returned on the same day of injury experienced delayed onset of symptoms at 3 hours postinjury, as compared with only 12.6% (20/ 158) of those who did not return to play on the same day of injury. Although more prospective work is needed in this area, these studies raise questions as to whether the RTP criteria for grade 1 (mild) concussions are conservative enough.
Guidelines from Cantu43 and the American Academy of Neurology6 both recommend termination of the season after the third concussion within the same season. The decision is more difficult if one of the injuries was more severe or was a severe injury resulting from a minimal blow, suggesting that the athlete's brain may be at particular risk for recurrent injury. In addition, because many athletes participate in year-round activities, once they are disqualified for the “season,” it may be difficult to determine at what point they can resume contact play. Other issues without clear-cut answers in the literature are when to disqualify an athlete who has not been rendered unconscious and whose symptoms cleared rapidly or one who suffered multiple mild to moderate concussions throughout the career and whether youth athletes should be treated differently for initial and recurrent concussive injuries.
When to disqualify an athlete for a career is a more difficult question to answer. The duration of symptoms may be a better criterion as to when to disqualify an athlete for the season or longer. Merril Hoge, Eric Lindros, Chris Miller, Al Toon, and Steve Young provide highly publicized cases of athletes sustaining multiple concussions with recurrent or postconcussion signs and symptoms that lasted for lengthy periods of time.43
Once an athlete has suffered a concussion, he or she is at increased risk for subsequent head injuries.21,43,86 Guskiewicz et al21,23 found that collegiate athletes had a 3-fold greater risk of suffering a concussion if they had sustained 3 or more previous concussions in a 7-year period and that players with 2 or more previous concussions required a longer time for total symptom resolution after subsequent injuries.21 Players also had a 3-fold greater risk for subsequent concussions in the same season,23 whereas recurrent, in-season injuries occurred within 10 days of the initial injury 92% of the time.21 In a similar study of high school athletes, Collins et al82 found that athletes with 3 or more prior concussions were at an increased risk of experiencing LOC (8-fold greater risk), anterograde amnesia (5.5-fold greater risk), and confusion (5.1-fold greater risk) after subsequent concussion. Despite the increasing body of literature on this topic, debate still surrounds the question of how many concussions are enough to recommend ending the player's career. Some research suggests that the magic number may be 3 concussions in a career.21,23,82 Although these findings are important, they should be carefully interpreted because concussions present in varying degrees of severity, and all athletes do not respond in the same way to concussive insults. Most important is that these data provide evidence for exercising caution when managing younger athletes with concussion and athletes with a history of previous concussions.
Many epidemiologic studies on concussion have focused on professional or collegiate athletes. However, this focus seems to now be shifting to the high school level and even to youth sports. Special consideration must be given to the young athlete. The fact that the brain of the young athlete is still developing cannot be ignored, and the effect of concussion on the developing brain is still not entirely understood. Even subtle damage may lead to deficits in learning that adversely influence development. Therefore, it has been suggested that pediatric athletes suffering a concussion should be restricted from further participation for the day and that additional consideration should be given as to when to return these individuals to activity.46
Recent epidemiologic investigations of head-injury rates in high school athletes have shown that 13.3% of all reported injuries in high school football affect the head and neck, whereas the numbers in other sports range from 1.9% to 9.5% in baseball and wrestling, respectively.89 Guskiewicz et al23 prospectively examined concussion incidence in high school and collegiate football players and found that the greatest incidence was at the high school level (5.6%), compared with the National Collegiate Athletic Association Division I (4.4%), Division II (4.5%), and Division III (5.5%).
Authors who have tracked symptoms and neuropsychological function after concussion suggest that age-related differences exist between high school and collegiate athletes with regard to recovery. Lovell et al41 reported that the duration of on-field mental status changes in high school athletes, such as retrograde amnesia and posttraumatic confusion, was related to the presence of memory impairment at 36 hours, 4 days, and 7 days postinjury as well as slower resolution of self-reported symptoms. These findings further emphasize the need to collect these on-field measures after concussion and to use the information wisely in making RTP decisions, especially when dealing with younger athletes. Field et al90 found that high school athletes who sustained a concussion demonstrated prolonged memory dysfunction compared with collegiate athletes who sustained a concussion. The high school athletes performed significantly worse on select tests of memory than age-matched control subjects at 7 days postinjury when compared with collegiate athletes and their age-matched control subjects. We hope these important studies and others will eventually lead to more specific guidelines for managing concussions in high school athletes.
Very few investigators have studied sport-related injuries in the youth population, and even fewer focused specifically on sport-related concussion. One group91 reported that 15% of the children (mean = 8.34 ± 5.31 years) who were admitted to hospitals after MTBI suffered from a sport-related mechanism of injury. Another group92 found that sport-related head injury accounted for 3% of all sport-related injuries and 24% of all serious head injuries treated in an emergency department. Additionally, sport-related concussion represented a substantial percentage of all head injuries in children under the age of 10 years (18.2%) and 10- to 14-year-old (53.4%) and 15- to 19-year-old (42.9%) populations.92 Thus, sport-related head injury has a relatively high incidence rate and is a significant public health concern in youth athletes, not just participants at higher competitive levels.
Although no prospective investigations in younger athletes (younger than 15 years old) have been undertaken regarding symptom resolution and cognitive or postural-stability recovery, Valovich McLeod et al93 recently determined the reliability and validity of brief concussion assessment tools in a group of healthy young athletes (9–14 years old). The SAC is valid within 48 hours of injury and reliable for testing of youths above age 5 years, but younger athletes score slightly below high school and collegiate athletes.55 This issue is remedied, however, if preseason baseline testing is conducted for all players and a preinjury baseline score established for each athlete against which changes resulting from concussion can be detected and other factors that affect test performance can be controlled. Users of standardized clinical tools should be aware of the effects of age and education on cognitive test performance and make certain to select the appropriate normative group for comparison when testing an injured athlete at a specific competitive level. Uncertainties about the effects of concussion on young children warrant further study.
Once the athlete has been thoroughly evaluated and determined to have sustained a concussion, a comprehensive medical management plan should be implemented. This plan should include frequent medical evaluations and observations, continued monitoring of postconcussion signs and symptoms, and postinjury cognitive and balance testing. If symptoms persist or worsen or the level of consciousness deteriorates at all after a concussion, neuroimaging should be performed. Although scientific evidence for the evaluation and resolution of the concussion is ample, specific management advice to be given to the athlete on leaving the athletic training room is lacking.94 Athletic trainers and hospital emergency rooms have created various home instruction forms, but minimal scientific evidence supports these instructions. However, despite these limitations, a concussion instruction form (Appendix C) should be given to the athlete and a responsible adult who will have direct contact with the athlete for the initial 24 hours after the injury. This form helps the companion to know what signs and symptoms to watch for and provides useful recommendations on follow-up care.
At this time, the clinician has no evidence-based pharmacologic treatment options for an athlete with a concussion.95 Most pharmacologic studies have been performed in severely head-injured patients. It has been suggested that athletes with concussion avoid medications containing aspirin or nonsteroidal anti-inflammatories, which decrease platelet function and potentially increase intracranial bleeding, mask the severity and duration of symptoms, and possibly lead to a more severe injury. It is also recommended that acetaminophen (Tylenol, McNeil Consumer & Specialty Pharmaceuticals, Fort Washington, PA) be used sparingly in the treatment of headache-like symptoms in the athlete with a concussion. Other substances to avoid during the acute postconcussion period include those that adversely affect central nervous function, in particular alcohol and narcotics.
Once it has been determined that a concussion has been sustained, a decision must be made as to whether the athlete can return home or should be considered for overnight observation or admission to the hospital. For more severe injuries, the athlete should be evaluated by the team physician or emergency room physician if the team physician is not available. If the athlete is allowed to return home or to the dormitory room, the ATC should counsel a friend, teammate, or parent to closely monitor the athlete. Traditionally, part of these instructions included a recommendation to wake up the athlete every 3 to 4 hours during the night to evaluate changes in symptoms and rule out the possibility of an intracranial bleed, such as a subdural hematoma. This recommendation has raised some debate about unnecessary wake-ups that disrupt the athlete's sleep pattern and may increase symptoms the next day because of the combined effects of the injury and sleep deprivation. It is further suggested that the concussed athlete have a teammate or friend stay during the night and that the athlete not be left alone. No documented evidence suggests what severity of injury requires this treatment. However, a good rule to use is if the athlete experienced LOC, had prolonged periods of amnesia, or is still experiencing significant symptoms, he or she should be awakened during the night. Both oral and written instructions should be given to both the athlete and the caregiver regarding waking.96 The use of written and oral instructions increases the compliance to 55% for purposeful waking in the middle of the night. In the treatment of concussion, complete bed rest was ineffective in decreasing postconcussion signs and symptoms.97 The athlete should avoid activities that may increase symptoms (eg, staying up late studying and physical education class) and should resume normal activities of daily living, such as attending class and driving, once symptoms begin to resolve or decrease in severity. As previously discussed, a graded test of exertion should be used to determine the athlete's ability to safely return to full activity.
Evidence is limited to support the best type of diet for aiding in the recovery process after a concussion. A cascade of neurochemical, ionic, and metabolic changes occur after brain injury.47 Furthermore, some areas of the brain demonstrate glycolytic increases and go into a state of metabolic depression as a result of decreases in both glucose and oxidative metabolism with a reduction in cerebral blood flow. Severely brain-injured subjects ate larger meals and increased their daily caloric intake when compared with controls.98 Although limited information is available regarding the recommended diet for the management of concussion, it is well accepted that athletes should be instructed to avoid alcohol, illicit drugs, and central nervous system medications that may interfere with cognitive function. A normal, well-balanced diet should be maintained to provide the needed nutrients to aid in the recovery process from the injury.
Although wearing a helmet will not prevent all head injuries, a properly fitted helmet for certain sports reduces the risk of such injuries. A poorly fitted helmet is limited in the amount of protection it can provide, and the ATC must play a role in enforcing the proper fitting and use of the helmet. Protective sport helmets are designed primarily to prevent catastrophic injuries (ie, skull fractures and intracranial hematomas) and are not designed to prevent concussions. A helmet that protects the head from a skull fracture does not adequately prevent the rotational and shearing forces that lead to many concussions.99
The National Collegiate Athletic Association requires helmets be worn for the following sports: baseball, field hockey (goalkeepers only), football, ice hockey, women's lacrosse (goalkeepers only), men's lacrosse, and skiing. Helmets are also recommended for recreational sports such as bicycling, skiing, mountain biking, roller and inline skating, and speed skating. Headgear standards are established and tested by the National Operating Committee on Standards for Athletic Equipment and the American Society for Testing and Materials.99
Efforts to establish and verify standards continue to be tested and refined, but rarely are the forces and conditions experienced on the field by the athletes duplicated. In addition to direction, speed, and amount of the forces delivered and received by the athlete, conditions not controlled in the testing process include weather conditions, changes in external temperatures and temperatures inside the helmet, humidity levels, coefficient of friction for the surfaces of the equipment and ground, and density of the equipment and ground. However, equipment that does meet the standards is effective in reducing head injuries.99
More recently, the issue of headgear for soccer players has received much attention. Although several soccer organizations and governing bodies have approved the use of protective headbands in soccer, no published, peer-reviewed studies support their use. Recommendations supporting the use and performance of headgear for soccer are limited by a critical gap in biomechanical information about head impacts in the sport of soccer. Without data linking the severity and type of impacts and the clinical sequelae of single and repeated impacts, specifications for soccer headgear cannot be established scientifically. These types of headgear may reduce the “sting” of a head impact, yet they likely do not meet other sports headgear performance standards. This type of headgear may actually increase the incidence of injury. Players wearing headgear may have the false impression that the headgear will protect them during more aggressive play and thereby subject themselves to even more severe impacts that may not be attenuated by the headgear.
The wearing of a mouth guard is thought by some to provide additional protection for the athlete against concussion by either reducing the risk of injury or reducing the severity of the injury itself.100 Mouth guards aid in the separation between the head of the condyle of the mandible and the base of the skull. It is thought that wearing an improperly fitted mouth guard or none at all increases this contact point. This theory, which is based on Newtonian laws of physics, suggests that the increased separation between 2 adjacent structures increases the time to contact, thus decreasing the amount of contact and decreasing the trauma done to the brain.100 However, no biomechanical studies support the theory that the increased separation results in less force being delivered to the brain.
High school football and National Collegiate Athletic Association football rules mandate the wearing of a mouth guard, but the National Football League rulebook does not require players to wear a mouth guard. The National Collegiate Athletic Association requires mouth guards to be worn by all athletes in football, field hockey, ice hockey, and lacrosse. Researchers101,102 have found no advantage in wearing a custom-made mouth guard over a boil-and-bite mouth guard to reduce the rise of cerebral concussion in athletes. However, ATCs and coaches should mandate the regular use of mouth guards because a properly fitted mouth guard, with no alterations such as cutting off the back part, is of great value in protecting the teeth and preventing fractures and avulsions that could require many years of expensive dental care.
We gratefully acknowledge the efforts of Kent Scriber, PhD, ATC; Scott Anderson, MS, ATC; Michael Collins, PhD; Vito A. Perriello, Jr, MD, PhD; Karen Johnston, MD, PhD; and the Pronouncements Committee in the preparation of this document.