Interest in sports concussion has grown widely in the last two decades among laypersons and medical professionals. Significant contributions of evidence-based research have led to a better understanding of this multifaceted, but still often elusive, injury. This information has transformed all aspects of concussion management, from on-field evaluation through return-to-play guidelines. The aim of this article is to highlight important research regarding predictors of outcome and treatment protocols. This research has been the basis of the paradigm shift from traditional concussion grading scales to individualized care. Today, concussion management requires a patient-centered approach with individualized assessment, including risk factor analysis, neurocognitive testing, and a thorough symptom evaluation.
CONCUSSION: DEFINITION, PATHOPHYSIOLOGY, AND PROGNOSIS
Without a universally accepted definition of concussion, understanding its subtleties has been difficult. Lack of consensus impedes "on-field" identification of injury, early management, and return-to-play recommendations. Although several academic organizations have proposed specific definitions over the years, a recent proposal by the U.S. Centers for Disease Control and Prevention (CDC) incorporates emerging research for a more comprehensive and individualized definition. The CDC defines mild traumatic brain injury (MTBI) or concussion as a complex pathophysiologic process affecting the brain, induced by traumatic biomechanical forces secondary to direct or indirect forces to the head. MTBI is caused by a jolt to the head or body that disrupts the function of the brain. This disturbance of brain function is typically associated with normal structural neuroimaging findings (i.e., CT scan, MRI). MTBI results in a constellation of physical, cognitive, emotional, and/or sleep-related symptoms and may or may not involve a loss of consciousness (LOC). Duration of symptoms is highly variable and may last from several minutes to days, weeks, months, or longer in some cases (7).
Noting that this disruption in brain function typically is associated with nonfocal exam findings and normal structural neuroimaging, this definition underscores important work by Giza and Hovda that finds metabolic changes in intra- and extra-cellular environments to be the basis of concussion pathophysiology. A detailed description of the pathophysiological basis of this injury is beyond the scope of this discussion; however, through animal models, these researchers have postulated that concussive trauma creates a "metabolic mismatch" between energy demand and energy supply, which may create cellular vulnerability and predispose to further injury (22). This model of neurologic vulnerability has clear implications for outcomes, return-to-play recommendations, and the potential additive effects of subsequent trauma.
Clinically, the effects of concussion upon the athlete have been well described in the literature. Four distinct symptom clusters mark the clinical presentation: cognitive (e.g., concentration and attention deficits, fogginess, feeling slowed down), somatic (e.g., headaches, dizziness, light and sound sensitivity), emotional (e.g., anxiety, sadness, irritability), and sleep-related (e.g., hypersomnia or insomnia) symptoms. For approximately 80% of individuals, these symptoms and the impairments noted on neurocognitive testing will resolve by 3 wk, as illustrated in Table 1 (12,48). For the remaining 20% of individuals, symptoms can last a month or longer and can occasionally preclude return to sports, school, or work. The research highlighted below has helped to advance our knowledge of predictive factors so that evidence-based judgments can be made about management and return to sport.
PREDICTORS OF OUTCOME AFTER CONCUSSION
Acute markers of injury have long been the basis for identification and classification of concussion. Thus, assessment of amnesia, LOC, and confusion has become the hallmark of sideline testing. The ability of these three markers to predict injury severity has been closely scrutinized, and data suggest that amnesia is the acute marker most predictive of injury severity and duration (6). This contradicts traditional concussion grading scales, which were heavily influenced by duration of LOC.
In a study of 47 concussed athletes, LOC predicted neither injury severity nor duration of symptoms; however, those athletes with evidence of posttraumatic amnesia (PTA) had significantly more symptoms, longer duration of symptoms, and more significant impairments on neurocognitive testing (18). The authors concluded that self-reported memory impairments at 24 h after injury were "robust indicators" of severity. These findings were corroborated by Collins et al. in a study of 78 high school and college athletes. Using neurocognitive testing and self-report of symptoms to measure severity of injury, the authors concluded that the presence of amnesia was the most predictive marker of concussion severity at 2 d post injury (11). More specifically, cognitively impaired athletes with pronounced post-concussive symptoms were more than 10 times more likely to have had retrograde amnesia and four times more likely to have had anterograde amnesia. LOC was again not shown to correlate with injury severity. Drake et al. examined the relationship between PTA and outcome using the Glasgow Coma Scale-Extended (GCS-E) in a concussed group of more than 350 military personnel (16). The GCS-E provides assessment of PTA, potentially making it more sensitive than the Glasgow Coma Scale, which has a ceiling effect in the assessment of mild traumatic brain injury. These investigators found that longer durations of PTA were associated with increased symptoms of dizziness, depression, and cognitive impairment.
The neurologic consequences of repeated head injury have been well documented among boxers, and long-term effects are recognized in soccer and football (24,32,33,42). In retired professional football players, Guskiewicz and colleagues found a significant increase in the prevalence of cognitive impairments among players with a reported history of three or more concussions (16). Of great concern is that the adverse sequelae of multiple concussions do not appear limited to athletes with years of concussive and subconcussive hits; rather, cumulative effects can be seen at any age.
Although several studies have shown that concussion history did not predict baseline performance upon computerized neurocognitive testing (3,8,27), there is mounting evidence that athletes with a history of concussion have longer recovery and are at increased risk for future injury. In studies of high school and collegiate athletes, those athletes with a history of three or more concussions had a more severe on-field presentation of concussion (12), were more likely to report headaches at baseline (41), were more vulnerable to subsequent injury than those with no concussion history (28), and were three times more likely to sustain an additional injury (25).
In their study of concussed collegiate athletes, Guskiewicz et al. also revealed an association between prolonged recovery and a history of three or more concussions, evidence recently corroborated (8,14,46). In one recent corroborating study, Covassin et al. found delayed recovery of verbal memory and reaction time in those athletes with only two or more prior concussions (41). Furthermore, Collins et al. found that among 400 collegiate football players, two or more previous concussions independently predicted long-term deficits of executive function, processing speed, and self-reported symptom severity (10).
Approximately 30 million children and adolescents participate in sports in the United States, and conservative estimates suggest concussion rates of 300,000 annually in this population (36). Traditional concussion grading scales and return-to-play guidelines do not distinguish treatment recommendations for adolescent, collegiate, or professional athletes, in effect treating all athletes similarly regardless of age. However, there is a growing body of research that suggests that children and adolescents are more vulnerable to the effects of concussion and should be managed more conservatively. In a direct comparison between collegiate and high school football and soccer players, Field et al. found that high school athletes took longer to recover their neurocognitive deficits when compared with matched collegiate athletes, findings which have been replicated (21,45). In a study comparing professional football players and high school athletes, again the younger athletes had prolonged impairments on neurocognitive testing (38).
Although it has been postulated that a "natural selection" bias may influence the results of these studies, age-related physiologic differences suggest that children have prolonged and diffuse cerebral swelling after traumatic brain injury with significant increases in sensitivity to glutamate, increasing their risk of secondary injury and second impact syndrome (5,35,39). This may account for the delayed recovery in younger athletes and the likelihood for more severe neurological damage if further injury occurs during the recovery period. These studies call attention to the need for more individualized, age-sensitive, concussion management that is not based upon standardized scales.
Title IX legislation has dramatically increased participation among women in sports over the last several decades. Despite this, research examining gender differences in concussion is limited, and prospective studies are needed to elucidate this further. Both estrogen and progesterone have been shown to have neuroprotective functions (43); however, a meta-analysis of 20 clinical outcomes after brain injury revealed that women had poorer outcomes across 85% of the variables used (19).
Initial study has been undertaken from several groups regarding gender differences upon baseline neurocognitive testing, and data are emerging. Female athletes have been found to perform significantly better on tests of verbal memory when compared with male athletes, and male athletes perform better on visual memory tests (2). Covassin et al. confirmed these findings using computerized neurocognitive testing and also reported that female athletes endorse a significantly higher number of baseline symptoms when compared to male athletes (15). Although there are multiple factors that may play a role in these differences in symptom reporting, including symptoms associated with menstrual cycles, this study further illustrates the importance of baseline testing for the individualized management of patients.
Headaches and Migrainous Symptoms
Headaches occur frequently after concussion, with an incidence up to 86% (26). Collins et al. found that high school athletes reporting headaches 7 d after injury had a significantly larger number of other post-concussive symptoms, slower reaction time, and impaired memory on neurocognitive testing (9). These athletes were also more likely to have three or four on-field markers of injury and mental status changes of 5 min or more after the acute injury. These findings have been replicated by Register-Mihalik et al., who revealed an increase in the incidence and severity of post-concussive symptoms among patients with headaches, as well as greater neurocognitive deficits on computerized neurocognitive testing (40). Mihalik et al. reported that athletes with migrainous symptoms (i.e., light and/or sound sensitivity, nausea, vomiting) have significantly greater neurocognitive deficits compared with athletes without posttraumatic migraines (37). These athletes were also compared with athletes with headaches without migrainous symptoms, and significant differences were seen between these groups as well. This suggests that migrainous symptoms may be more suggestive of poorer outcomes than headaches alone. Although the temporal relationship between the recovery of the headaches and improvement with neurocognitive testing was not evaluated, these findings suggest that post-concussive headaches, with migrainous symptoms more specifically, may mark incomplete recovery and should highlight the need for conservative management.
It has been observed that physical and cognitive exertion after concussion may delay recovery, and thus, rest has been advocated as the mainstay of primary management (34). Leddy and colleagues summarized the physiological dysfunction after concussion and asserted that exertion may place metabolic demands on the brain at a time when it is already compromised (30). Clinically, a recent retrospective study of 95 high school athletes found that athletes engaging in high levels of activity after concussion performed significantly worse on computerized neurocognitive testing (31). These findings underscore the importance of early injury identification and education regarding physical and cognitive rest, the hallmark of initial management. Cognitive rest, for example, may include having a student stay home from school or attend half-days of school in order to prevent cognitive over-exertion. While more investigation is needed in this area, these initial data suggest that specific graded exertional protocols guiding return to physical and cognitive activity are needed for concussion management.
NEW PARADIGMS FOR THE MANAGEMENT OF CONCUSSION
Arguably the most significant advancement in the field of concussion management has been the increasingly widespread use of neurocognitive testing. Computerized or traditional neurocognitive testing measuring domains such as verbal and visual memory, complex attention, reaction time, and processing speed have been found to be particularly helpful in the diagnosis and tracking of recovery when individual baseline testing is performed and compared with post-injury scores (17). Before implementation of neurocognitive testing, diagnosis of concussion relied solely upon symptom report from athletes, a population who often minimize complaints to return to the playing field sooner, possibly prematurely.
Computerized neurocognitive testing programs provide sensitive and specific objective data to quantify injury and track recovery (4,20,23,29,44,47). Van Kampen et al. compared baseline and post-injury results in a group of 122 athletes (47). These athletes were compared with a control sample of 70 athletes without concussions who underwent baseline testing followed by repeat testing in 1 wk to analyze test-retest fluctuations. In this study, 83% of athletes with concussions had significantly lower neurocognitive test scores when compared with their baseline scores. Using neurocognitive testing was nearly 20% more sensitive for detecting injury than symptom reporting alone. For the control group, none of the athletes reported symptoms and demonstrated poorer neurocognitive testing; this highlights the sensitivity and specificity for using neurocognitive testing with detailed medical interview to identify concussion. A similar recent study by Fazio et al. also demonstrated the "added value" of computerized neurocognitive testing in an athlete population (20). In this study, a large cohort of concussed athletes was tested within 7 d of concussive injury, and data were compared with a control group of athletes who did not sustain concussion. Results indicated that concussed athletes who denied subjective symptoms demonstrated significantly poorer performance than control subjects on all four summary scores of the computerized neurocognitive test battery (verbalmemory, visual memory, processing speed, and reaction time).
Computerized neurocognitive testing has many advantages when applied to the management of athletes, particularly student athletes. Preseason testing of large numbers of athletes can be accomplished with minimal human resources. Computerized databases allow results to be easily accessed when needed for comparison after injury and provide new avenues for research. Computerized test programs also have extensive normative data available for comparison when baseline data are not available for the athlete. Use of the computer allows for randomization of test stimuli to decrease "practice effects" and more sensitive measures of reaction time, to 1/100 of a second while traditional testing measures accuracy to 1-2 s. Sensitivity and specificity of computerized neurocognitive evaluation also is well established in multiple peer-reviewed studies (4,23,29,44).
In 2001, the first International Conference on Concussion in Sport underscored the importance of neurocognitive testing in the conference's summary and agreement statement (1). The group recommended that post-injury neurocognitive testing should be a "cornerstone" of injury assessment, management, and return-to-play decision making. Baseline neurocognitive testing was also recommended when possible, a recommendation that has been since implemented by several professional sporting leagues, as well as college and high school athletic associations. The recognition of the value of neurocognitive testing marked a significant shift from the standardized concussion grading scales and emphasized the need for an individualized approach from athletic trainers and medical professionals.
The International Conference on Concussion in Sport recommended another practice guideline that marked a clear departure from the traditional concussion scales. These return-to-play guidelines, presented in Table 2, also reflect the need for evidence-based, individualized concussion management for all athletes. The standard of care as now accepted for concussion management is that athletes meet three criteria before return to sport.
First, the athlete must be asymptomatic at rest before any return to activity. Comprehensive evaluation of symptoms, either in conjunction with computerized neurocognitive testing or separately through clinical interview, should be performed initially after injury and then serially throughout recovery. As symptom minimization may occur in this population, discussion regarding the importance of accurate symptom reporting should be carefully undertaken.
Second, the athlete must be asymptomatic with physical and cognitive exertion. After the athlete demonstrates being asymptomatic at rest, progressive return to activity can be initiated. As indicated in Table 2, the athlete should begin with light aerobic activity (e.g., walking or stationary bicycle), then progress to moderately exertional, sport-specific aerobic training (e.g., skating for hockey, running for soccer), and then finally to heavily exertional, noncontact training drills (e.g., weight training, sprints, positional maneuvers). If the athlete's symptoms return at any point, the athlete should return to the previous exertional level at which he or she was last asymptomatic. Cognitive exertion, in addition to physical exertion, must also be a key part of this protocol. School-related activities (e.g., test-taking, reading, and studying) also may exacerbate symptoms and require close monitoring. Only when student athletes meet both criteria, asymptomatic with physical and cognitive exertion, should return to sport be considered.
Finally, the athlete must have returned to baseline or normative values on neurocognitive testing. As noted previously, neurocognitive testing has become the cornerstone of concussion identification and management. With serial examinations after injury, recovery can be monitored closely. When scores return to baseline values (or in the absence of baseline tests, scores reach normative values), the athlete is deemed to have reached cognitive recovery.
These new evidence-based parameters for return-to-play have arguably become the standard of care for the management of concussion, buoyed by previously mentioned research regarding risk factors and prognostic indicators. Although neurocognitive testing is now more widely used and is helpful in studying predictors of outcome, the shift from traditional concussion grading scales to individualized care is still a new concept. Education of medical professionals, athletic trainers, athletes, coaches, and parents needs to remain a key focus of our efforts.
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