Sport-related concussion is a common problem encountered by pediatricians and other primary care physicians. Assessment of concussion is based on clinical evaluation. The Zurich consensus statement provides a basic framework to guide concussion management decisions and recommends an individualized approach and the exercising of clinical judgment in return-to-play decisions. This article reviews practice aspects of concussion for the adolescent athletes who present in the primary care office or clinic setting.
Sport-related concussions are common in adolescents and can have significant acute and long-term adverse effects on the developing brain of the young athlete. This review discusses the practical aspects of sport-related concussions that are most relevant in the management of young athletes who present in the office. The Zurich consensus statement on concussion in sport provides a basic framework and a reference point for the evaluation and management of sport-related concussion in adolescents and adults. The Sport Concussion Assessment Tool 2 (SCAT2) ( Appendix 1 ), developed as part of the Zurich guidelines, provides a convenient and standard format for clinical evaluation and serial documentation of symptoms and examination findings of concussion. However, each athlete should be individually assessed, and clinical judgment ultimately supersedes in making management and return-to-play decisions.
Definition
In its practice parameter on concussion management in sports, the American Academy of Neurology defined concussion as a trauma-induced alteration in mental status that may or may not be associated with loss of consciousness. Confusion, loss of memory, and reduced speed of information processing, which may occur immediately or several minutes later, are considered to be the key features of concussion seen in most cases.
Concussion is defined by the Zurich consensus statement as a complex pathophysiological process affecting the brain, induced by traumatic biomechanical forces. Certain common clinical, pathologic, and biomechanical features of concussion that form the basis of this definition are listed in Box 1 .
- 1.
Concussion may be caused by a direct blow to the head, face, neck, or elsewhere on the body with impulsive force transmitted to the head.
- 2.
Concussion typically results in the rapid onset of short-lived impairment of neurologic function that resolves spontaneously.
- 3.
Concussion may result in neuropathological changes, but the acute clinical symptoms largely reflect a functional disturbance rather than structural injury.
- 4.
Concussion may result in a graded set of clinical syndromes that may or may not involve loss of consciousness. Resolution of the clinical and cognitive symptoms typically follows a sequential course; however, in a small percentage of cases, postconcussive symptoms may be prolonged.
- 5.
No abnormality on standard structural neuroimaging studies is seen in concussion.
Epidemiology
The Centers for Disease Control and Prevention, in the United States, reported 300,000 head injuries in a year in high-school sports, 90% of which are concussions. Reported incidence of concussions at high-school level is 0.14 to 3.66 concussions per 100 player seasons accounting from 3% to 5% of all sport-related injuries. Gessel and colleagues, using data from the High School Reporting Information Online and National Collegiate Athletic Association Injury Surveillance, reported that concussions represented 8.9% (n = 396) of all high-school athletic injuries and 5.8% (482) of all collegiate athletic injuries. The highest number of concussions has been reported in American football, followed by (in decreasing order of risk) ice hockey, soccer, wrestling, basketball, field hockey, baseball, and softball.
Symptoms and signs of concussion are often not recognized by the athlete or by medical personnel, and the athlete may fail to grasp the significance of head trauma and subsequent symptoms of concussion and not seek timely medical attention. Some athletes may not report symptoms or head injury for fear of being excluded from further sport participation. For these reasons it is generally accepted that the reported incidence of concussion is a gross underestimate.
Epidemiology
The Centers for Disease Control and Prevention, in the United States, reported 300,000 head injuries in a year in high-school sports, 90% of which are concussions. Reported incidence of concussions at high-school level is 0.14 to 3.66 concussions per 100 player seasons accounting from 3% to 5% of all sport-related injuries. Gessel and colleagues, using data from the High School Reporting Information Online and National Collegiate Athletic Association Injury Surveillance, reported that concussions represented 8.9% (n = 396) of all high-school athletic injuries and 5.8% (482) of all collegiate athletic injuries. The highest number of concussions has been reported in American football, followed by (in decreasing order of risk) ice hockey, soccer, wrestling, basketball, field hockey, baseball, and softball.
Symptoms and signs of concussion are often not recognized by the athlete or by medical personnel, and the athlete may fail to grasp the significance of head trauma and subsequent symptoms of concussion and not seek timely medical attention. Some athletes may not report symptoms or head injury for fear of being excluded from further sport participation. For these reasons it is generally accepted that the reported incidence of concussion is a gross underestimate.
Mechanism and pathophysiology
In addition to direct impact to the head or other parts of the body in contact or collision sports, concussion can also occur in noncontact sports as a result of sudden acceleration, deceleration, or rotational forces imparted to the brain. Thus, absence of a history of direct impact to the head or elsewhere on the body does not rule out the possibility of a concussion.
The biomechanics and pathophysiology of concussion have been elucidated by many investigators in animal models as well as in humans. Pathophysiology of concussion on a cellular level is characterized by disruption and increased permeability of neuronal cell membranes. This results in an efflux of potassium into extracellular spaces, resulting in a calcium-dependent release of excitatory amino acids, specifically glutamate. The increase in extracellular potassium triggers neuronal cell-membrane depolarization resulting in neuronal suppression. Sodium-potassium pump is activated to restore homeostasis. The increased cellular metabolic activity increases the need for energy and glucose, and leads to hyperglycolysis. To meet the increased metabolic demands in the brain, an increase in cerebral blood flow is expected; however, a decrease in cerebral blood flow is observed in concussive injury of the brain. A mismatch between metabolic demands and supply results in neuronal dysfunction that can last from 1 to 10 days or more following the concussion, during which time the brain is more vulnerable to further injury.
History
In the primary care setting the athlete with a concussion is seen in the office setting when they present for a follow-up of head injury and need a medical clearance to return to sport. On the other hand, some athletes may initially present with symptoms or signs of concussion several days or weeks after the head injury; many may not realize the significance of the initial symptoms and delay seeking medical attention or seek medical attention because of persistence or worsening or onset of new symptoms. Parents may first seek a pediatrician’s advice when they notice deterioration of academic performance and changes in behavior, mood, or personality in the athlete; in these cases a history of antecedent head trauma should be ascertained.
The athlete may give a history of direct blow to the head or other part of the body, a collision with another player, a fall to the ground, or being struck by an object such as a ball, puck, or a bat. There may not be any history of direct impact to the head or other part of the body, and concussion can result from indirect shearing or rotational forces imparted to the brain without direct impact. Not uncommonly, a teammate may notice that something is not right with the athlete and communicate that to the trainer on the sideline. The athletic trainer or the coach or, less commonly, a spectator may see a collision and observe that the player is confused, disoriented, and not able to execute tasks or follow commands as expected within the context of the play at the time.
The athlete with concussion may manifest any 1 or more of several symptoms or signs ( Table 1 ) ; some develop immediately after the injury to the brain, whereas others may be delayed for days or weeks. Because no single symptom or set of symptoms and signs is pathognomonic of concussion, and many symptoms are nonspecific in nature, a contemporaneous relationship between the time of initial head injury and subsequent development of symptoms and signs should be established based on history and examination. Several symptom checklists or scales are used in the evaluation of concussion; however, none is specifically validated for such use. SCAT2 includes one such symptom evaluation scheme. Increasing evidence suggests that concussion rating scales based on athlete self-report of multiple symptoms are a more reliable and practical way of detecting concussion and monitoring progress during the recovery phase.
| Mental status changes | Amnesia Confusion Disorientation Easily distracted Excessive drowsiness Feeing dinged, stunned, or foggy Impaired level of consciousness Inappropriate play behaviors Poor concentration and attention Seeing stars or flashing lights Slow to answer questions or follow directions |
| Physical or somatic | Ataxia or loss of balance Blurry vision Decreased performance or playing ability Dizziness Double vision Fatigue Headache Lightheadedness Nausea, vomiting Poor coordination Ringing in the ears Seizures Slurred, incoherent speech Vacant stare/glassy eyed Vertigo |
| Behavioral or psychosomatic | Emotional lability Irritability Low frustration tolerance Personality changes Nervousness, anxiety Sadness, depressed mood |
Details of any previous head injury should be ascertained. Detailed history should include the date of injury, symptoms or signs, recovery time, and results of any neuropsychological (NP) testing. If multiple concussions have occurred in the past, obtain similar details for each concussion and document the interval between successive concussions.
Review of systems
A relevant review of systems should include any known (preinjury) neurologic condition or learning disability, attention deficit/hyperactivity disorder, depression, academic function before and since the injury, use of drugs or performance-enhancing supplements, and use of therapeutic medications. Psychosocial history should assess the athlete’s interest in sports and any evidence of parental pressure to return to sport.
Neurologic examination
A complete neurologic examination is essential in the evaluation of athletes with concussion, with specific attention to speech, visual acuity, visual fields, ocular fundi, pupillary reaction, extraocular movements, muscle strength, deep-tendon reflexes, tandem gait, finger-nose test, pronator drift, and Romberg test. Postural stability has been shown to be a sensitive indicator of sensory-motor dysfunction in concussion. SCAT2 includes the Balance Error Scoring System to assess balance, and finger-to-nose task to assess coordination. Abnormal or focal findings on neurologic examination should prompt consideration of a focal intracranial pathology and emergent evaluation and management of the athlete. Findings on neurologic examination should be normal in athletes with concussion, other than the mental status or cognitive functions.
Cognitive function
Assessment of cognitive functions, assessed clinically or by formal NP tests (conventional or computer based), is an essential component of the evaluation of concussion. Cognitive function can be affected by many factors other than the effects of concussion, such as baseline (preinjury) intellectual ability, learning disability, attention deficit/hyperactivity disorder, substance abuse, level of education, cultural background, lack of sleep, fatigue, anxiety, age, and developmental stage. Cognitive assessment techniques should be appropriate for the athlete’s age, level of education, and developmental stage or maturity. SCAT2 provides a method or format for clinically assessing cognitive function. An athlete with concussion may continue to manifest somatic or behavioral symptoms even after resolution of cognitive deficits.
NP testing
Conventional (paper-and-pencil) or computer-based NP testing can be used to formally assess the cognitive functions ( Box 2 ) of athletes who have concussion. Conventional NP testing uses a battery of tests administered in 1 or more sessions (several hours) and interpreted by neuropsychologists. Conventional NP tests have not been traditionally designed or validated to assess athletes with sport-related concussion, cannot be easily adapted for mass application, and are expensive and labor intensive.
Amnesia after trauma
Attention span (focused, sustained, and visual)
Mental flexibility
Motor coordination
Motor speed
Orientation to person, place, and time
Processing speed
Reaction time
Verbal memory, immediate and delayed
Visual scanning
Computerized NP testing specifically designed to assess athletes with sport-related concussion is now being used at high-school, collegiate, and professional levels to obtain baseline as well as postconcussion NP profiles of athletes to monitor recovery. Some of the advantages of computerized testing include ease of administration, cost-effectiveness, and ease of interpretation. Examples of currently available computerized NP tests are listed in Box 3 . For interested physicians, detailed information on each of the tests is available at their Web sites.
Automated Neuropsychological Assessment Metrics (ANAM)
CogSport (formerly Concussion Sentinel)
Concussion Resolution Index (CRI)
Immediate Measurement of Performance and Cognitive Testing (ImPACT)
Standardized Assessment of Concussion (SAC) and its electronic version eSAC
It is possible to use NP testing to monitor an athlete’s recovery from a concussion, but data obtained from such tests after a concussion are most useful when compared with an injured athlete’s performance on those tests before injury (baseline profile model). This requires preparticipation baseline testing for all athletes in sports in which the risk of concussion is high. Computer-based tests make preparticipation testing more feasible by reducing the time involved in testing and by reducing observer bias in test results. These tests can also minimize the effect of repeated practice on an athlete’s performance on specific tests and detect attempts by an athlete to do poorly on baseline testing so that they will be more easily cleared to return to play after a concussion.
ANAM
The ANAM ( www.armymedicine.army.mil/prr/anam.html ) suite was developed primarily by the United States Department of Defense. The original purpose of ANAM was to assess how normal physical and cognitive performance might be affected by chemical warfare agents, and many of the component tests were taken from batteries of NP and psychomotor tests developed by different branches of the United States Armed Forces. However, ANAM has been used for evaluation of other types of injuries, including concussion in athletes. Retest reliability needed for baseline measurements has been studied, but ANAM scores do not measure or indicate return to baseline after a concussion.
CogSport
CogSport (CogState Limited: www.cogstate.com ; known in an earlier version as Concussion Sentinel) is a suite of 4 tests that measure psychomotor function, processing speed, visual attention, vigilance, visual learning, verbal learning, and memory. The suite is sensitive to cognitive changes seen in sport-related concussions compared with baseline performance, which is necessary for the evaluation of an athlete after concussion.
CRI
CRI (HeadMinder, Inc: www.headminder.com ) is a Web-based NP test that includes measures of cognitive functions related to postconcussion syndrome, including memory, reaction time, and speed of decision making and of information processing. As with several similar test suites, CRI was developed specifically to allow for comparison of an athlete’s baseline and postconcussion performance.
Immediate Postconcussion Assessment and Cognitive Testing (ImPACT)
ImPACT (ImPACT Applications, Inc: www.impacttest.com ; the acronym also stands for Immediate Measurement of Performance and Cognitive Testing) was the first test suite designed specifically to evaluate NP function in athletes, at baseline and after concussive injury, and is one of the most widely used test suites for evaluation of concussion in athletes, including professional players. ImPACT evaluates multiple neurocognitive skills, and assesses changes in processing speed as a test subject becomes fatigued. It can also vary stimuli randomly, which reduces the effect of practice on the athlete’s score, and can detect attempts by an athlete to reduce baseline performance deliberately so that postconcussion changes are masked.
SAC, eSAC
SAC ( www.csmisolutions.com ) is a brief examination intended for use at the sideline, and is based on the American Academy of Neurology’s 1997 Practice Parameter for management of sports-related concussion. The original SAC, which is still available, was a paper-and-pencil test that measures orientation, immediate and delayed memory, and concentration. Unlike other paper-and-pencil and performance tests, evaluation with SAC does not show a practice effect on repeated administration. An electronic version operating on handheld personal digital assistants is also available.
Validity of Computer-based NP Testing
The validity of computer-based NP testing in the evaluation of sport-related concussions remains a subject of intense debate and remains unsettled. Some investigators have questioned the value of baseline testing because of lack of clear evidence that such testing helps to positively affect the outcome of concussion. The performance of currently available NP tests for the evaluation of athletes after concussion seems to be variable, but better than pencil-and-paper tests. In one study, sensitivity of 2 different neurocognitive tests (CRI and ImPACT) to concussion were 78.6% and 79.2% respectively when used as the sole instrument for detection of concussion, compared with 43.5% for pencil-and-paper tests. When combined in a battery with reports of concussion-related symptoms (which had a stand-alone sensitivity of 68.0%), evaluation of postural control (stand-alone sensitivity 61.9%), and the pencil-and-paper tests, overall sensitivity ranged from 89% to 96%, suggesting that a battery of several tests including NP tests is preferable for detection of concussion effects.
Test-retest reliability has also been shown to be low to moderate over a 5- to 50-day interval between initial and later testing with ImPACT, CRI, and Concussion Sentinel. None of these tests reached the correlation coefficient of 0.75 considered acceptable for test-retest reliability. A head-to-head comparison of CogSport, ImPACT, and CRI showed significant but modest correlation in assessment of complex reaction time between ImPACT and CogSport and between ImPACT and CRI, but not between CogSport and CRI, and no significant correlation in assessment of memory indices between any pair of programs. This suggests that the same NP test suite needs to be used for baseline and postinjury evaluation. Self-reported previous histories of concussion do not correlate with performance on pencil-and-paper or computer-based NP tests.
One problem frequently encountered in concussion evaluation by comparison of baseline and postconcussion assessment is sandbagging, or performance deliberately reduced by an athlete during baseline testing with the intent of being able to return to play after a concussion without adequate recovery. Manual timing of an athlete during a paper-and-pencil test is difficult and may not have sufficient resolution to detect sandbagging. However, computer-based test suites can be designed to time tasks to high resolution, sometimes on the order of milliseconds, and tests can be designed to detect poor performance (ImPACT, in particular, contains tests that are intended to detect sandbagging); variability in time taken for a task, as well as in responses, is also associated with concussion.
Another issue is the effect of repeated practice on an athlete’s ability to perform tasks included in a test suite. Because paper-and-pencil tests are limited in their item variability, the practice effect is more pronounced with such tests, although one study showed little such effect with the SAC. Computer-based test suites can and should be designed so as to vary aspects of each individual test in the suite, and many of these tests, including ImPACT, CogState, and ANAM, provide for such variation.
Applications of Computer-based NP Testing
In the last 10 years NP evaluation of sports-related brain injury has become widespread. The management decisions in concussion should not be guided solely by the results of NP testing, and NP testing should be used as 1 tool in the overall assessment along with clinical evaluation. Such testing provides at least some objective data on cognitive function in concussion. Computer-based testing reduces interobserver variability in the gathering of test data and makes test results less dependent on the competence of test administrators. Accurate interpretation of the results of these tests requires knowledge of the tests used and of their limitations, in general use and with players in different sports, on different teams, and in different situations.
Adolescence is developmentally characterized by continued neurologic maturation associated with increased acquisition of neurocognitive abilities as well as rapid acquisition of new skills and knowledge. Therefore, continued improvement in measures of NP tests is expected through adolescence. A return to baseline NP profile may not necessarily indicate full recovery. This confounding factor should be taken into account in interpreting the results of NP tests in adolescents.
Brief mental status evaluations and assessments of cognitive function that can be administered easily on the sideline immediately after a head injury were among the initial applications of computer-based NP testing. Some of these tests, including SAC and ImPACT, were originally developed as pencil-and-paper tests; their adaptation to electronic testing increases precision, repeatability, and objectivity of test results while reducing the practice effect seen with repetitive administration of the same test items. In particular, the high precision of timing, to fractions of a second, possible in computer-based testing allows for better comparison of pre- and postconcussion performance and improved detection of subtle cognitive defects.
Another advantage of computer-based testing for evaluation of concussion is that the ability to test athletes without neuropsychologists having to administer the tests makes NP testing more accessible. Some of the available test suites, in particular ImPACT, can also detect sandbagging or other non–trauma-related changes in test performance, which is especially important during baseline testing.
Computer-based NP testing has been shown to provide valid and repeatable information on the effects of concussion on an athlete, and can be used in conjunction with baseline (before the season) test results to assess changes over time in cognitive functions. Formal NP testing is useful to delineate specific impairments in athletes who fail to recover as expected, or who deteriorate, or those who have had multiple concussions. NP testing can be useful in guiding the management of academic difficulties in children and adolescents. Computerized NP testing can be done on an individual basis in an office or clinic setting; however, in most communities it is done through the school system. Pediatricians are increasingly likely to see athletes who present with such baseline and postinjury test reports ( Fig. 1 ).
