INTRODUCTION
Concussion is a major public health concern and is presently one of the least understood neurological injuries. An estimated 1.6 million to 3.8 million sport- and recreation-related brain injuries occur in the United States annually, and up to 75% are classified as mild.1 The Centers for Disease Control and Prevention describes mild traumatic brain injury (mTBI; which includes concussion) as a silent epidemic. Although research on concussion and mTBI has increased over the past decade, clinicians are confronted with several knowledge gaps in diagnosing and managing concussion/mTBI. First, current neuropsychological, behavioral, and standard neuroimaging tools lack adequate sensitivity to detect subtle changes in brain structure and function in many individuals, making the initial diagnosis of concussion difficult. Clinicians primarily rely on observable symptoms, and it has been difficult to establish direct links between these symptoms and the underlying changes in brain structure and function.2 While advanced diagnostic and imaging techniques exist and there is accumulating evidence in support of their efficacy for aggregate populations, there are many limitations in their application. Furthermore, a single tool for guiding concussion management on an individual basis has yet to be elucidated. Second, current recommendations for returning to normal activity are not based on strong scientific evidence.2 The summary statement of the 3rd International Conference on Concussion in Sport states that “the science of concussion is at early stages and, therefore, management and return to play decisions remain largely in the realm of clinical judgment on an individualized basis.”3 Consequently, individuals may return to normal activity well before full recovery has occurred, making them vulnerable to repeated trauma and susceptible to a higher risk of a second concussion 7 to 10 days after an initial concussion.4 Third, the clinical classification and symptoms are not directly correlated with the underlying neuropathology and, therefore, accurate diagnosis of the severity of injury and predictions regarding the long-term outcome are not possible.5 The aim of this article was to provide a critical review of current unifying themes in the concussion literature and an assessment of and recovery from concussion and discuss the implications for clinical practice.
CONCUSSION AND RISK FACTORS
Nature of Concussion
The term “concussion” has been the subject of much controversy both within the public domain and in the medical community. Concussion was generally considered to be less severe than an mTBI and as a result, athletes often returned to play or activity as early as 15 minutes following improvement of symptoms.6 In 2008, a consensus statement developed at the International Conference on Concussion in Sport in Zurich defined concussion as “a complex pathophysiological process affecting the brain, induced by traumatic biomechanical forces.”3 Furthermore, it stated that “concussion may result in neuropathological changes, but the acute clinical symptoms largely reflect a functional disturbance rather than a structural injury.” The representation of concussion as a “functional disturbance” reflected the limitations of traditional clinical neuroimaging, such as computed tomography and magnetic resonance imaging, which typically do not detect changes in brain structure following concussion.
Recent neuroimaging and behavioral studies are changing the definition of concussion. Conventional imaging modalities (ie, magnetic resonance imaging, computed tomography) have been shown to be sensitive to gross structural abnormalities such as fractures, lesions, or intracranial hemorrhage caused by traumatic brain injury (TBI). However, these standard neuroimaging techniques are of limited use for the detection of microscopic tissue damage that may be associated with mTBI and concussion. A number of more sensitive imaging techniques that may be of relevance for diagnostic use are becoming increasingly available. These include magnetic resonance spectroscopy, diffusion tensor imaging, transcranial magnetic stimulation, magnetoencephalography, electroencephalography, and functional magnetic resonance imaging (Table 1). Each of these modalities has shown promise in contributing to the diagnosis and prognosis of concussion, suggesting that the recovery may be more prolonged than previously thought. Also, these techniques have demonstrated that the effects of concussion are complex rather than simply being limited to physical and cognitive impairments and that these effects are influenced by specific risk factors.13–16 However, at this time, no one imaging modality is appropriate in guiding the individual management of concussion.
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Table 1: Summary of Common Imaging Approaches Applied in Concussion Research Studies
Sex
It has been shown that a greater number of concussions occur in males than in females,17,18 suggesting that males are at a higher risk of concussion than females. However, females report higher rates of concussion.19,20 The greater prevalence of concussion in males largely is explained by the greater proportion of males engaged in the specific sports and activities that have the highest incidence of concussion.19 Given females' increased frequency of concussion, gender is emerging as a potential risk factor for increased concussion incidence.21 Females suffering from concussions more frequently have cognitive impairments, report more symptoms, perform worse on neurocognitive testing, and thus are hypothesized to have worse postconcussion outcomes than males.19,22 It should be noted, however, that gender differences in reporting symptoms, seeking medical aid, and hiding injury need to be considered as potential limitations of these results.20,23
Age
While most adults generally show full recovery within 3 to 6 months following mTBI,24 little is known about the impact of concussion on the developing brain; however, it appears that children and adolescents take longer than adults to recover.25 Recently, Beauchamp et al26 have provided evidence suggesting that there may be observable changes in the brain up to 10 years following mTBI during childhood. It also has been suggested that younger children and adolescents suffer a greater number of concussions27 and report worse cognitive symptoms 1 year after concussion than adults.28 An inverse correlation between age and duration of recovery from memory-related symptoms was observed in a study examining the recovery times of adolescents and young adults who have sustained repeat sports-related concussions.29
Recent studies of TBI in adult humans and animals show that there are several factors that differentiate children and adolescents from adults. First, the pediatric skull is more compliant than the adult skull30 and is less resistant to mechanical forces resulting from primary and secondary injury,31 and therefore, the damage may potentially be greater in children/adolescents. Second, in TBI, there is evidence of a greater inflammatory response in pediatric populations compared with adults. The pathophysiology of this inflammatory response is not clear, but it appears that differences in glutamate receptor expression, increased vulnerability to oxidative stress, and cerebral blood flow dysregulation all play a role in the extent of injury.32–34 As glutamate receptors and cerebral blood flow dysregulation are also thought to play important roles in mTBI,35 the extent of injury in young populations may show a similar increase in physiological response as those currently noted with TBI. Third, the immature brain and developing neurons are highly susceptible to hypoxia, ischemia, and traumatic axonal injury.36,37 In a juvenile rodent model of repeated mTBI, increasing axonal injury and memory impairment were observed and may provide a new design to evaluate the susceptibility of the developing brain to repeated trauma.38 The frontal and temporal lobes appear to be the most vulnerable to injury; injury to these areas is associated with impairment of executive function, learning, memory, and behavioral disturbances.39–41 While the prevailing dogma was that the plasticity of the developing brain was somehow protective in children following brain injury, a recent review discussing the differences between pediatric and adult concussion42 highlights that psychosocial symptoms43 and impairments in visual processing44 may persist for a longer time in the pediatric population. It is important to note that many of these investigations were performed in more severe forms of TBI and caution should be exercised when extrapolating these findings to concussion.
Concussion History
Sustaining multiple or reoccurring concussions (≥3)45 increases the risk of long-term effects such as significant cognitive impairment46,47 and increases the likelihood of suffering a subsequent concussion.48,49 A history of multiple or subsequent concussions has been linked to cumulative effects, including prolonged recovery and increased symptoms.45 In a cohort of adolescent athletes, a history of 3 or more concussions was associated with an increased likelihood of loss of consciousness and anterograde amnesia after subsequent concussions.50 Repetitive head trauma has also been linked to chronic traumatic encephalopathy, which is a progressive deterioration of neural tissue leading to symptoms of dementia, memory loss, personality changes, depression, and motor impairments similar to those observed in Parkinson disease.51 Evidence of chronic traumatic encephalopathy has recently been found in several young college/high school athletes with no previously documented concussions (for review, see Schatz and Moserb52). This underscores the importance of understanding the effects of both concussion and subclinical repetitive head trauma on brain structure and function in an effort to minimize both the short- and long-term effects of these injuries.
Preexisting Neurological Conditions
Investigations are now emerging to explore existing diagnoses of migraines and learning disabilities as risk factors for concussion. Gordon et al17 found the Canadian Community Health Survey to expose an existing diagnosis of migraine headaches as a risk factor for sustaining concussions. The link between migraines and concussion deserves further exploration, as other factors may influence this potential relationship. Factors such as elite athletes' increased rates of migraines53 and increased exposure to head trauma, the difficulty in distinguishing the presentation of the 2 diagnoses, and a potential triggering of migraine by concussive impacts17 may all affect the link between these 2 conditions. Furthermore, initial evidence supports an extended recovery period for athletes with a history of migraines.54 Difficulties in learning, concentration, attention, and memory are common symptoms of concussion; therefore, individuals with learning disorders that exhibit these traits premorbidly may show an exacerbation of these traits following concussion.20,46 Furthermore, examinations of a population with learning disabilities may also complicate matters, as the neurocognitive concussion assessment tools have been validated for baseline with healthy controls, making it difficult to accurately apply in populations with learning disabilities, particularly if no baseline measurement is available.55
CONCUSSION ASSESSMENT
Sports-related concussions may cause impaired neurocognitive functioning,46 and there are a wide range of sideline assessment tools, neuropsychological test batteries, and other assessments tools used to evaluate postural stability, gaze, and attention by using dual-task paradigms after a suspected concussive event. In this section, we discuss the most widely used tools on the field and in clinical practice and comment on the strengths and weaknesses of each. The 3 most commonly used assessments for evaluating individuals with concussion are the Sideline Assessment of Concussion (SAC),56 the Sport Concussion Assessment Tool 2 (SCAT2),3 and the Immediate Post-Concussion Assessment and Cognitive Testing (ImPACT).57 The SAC and the SCAT2 are both sideline assessment tools. The ImPACT attempts to objectively measure the presence and severity of neurocognitive impairment. All have been recommended for use by the 3rd International Conference on Concussion in Sports.3
Standardized Assessment of Concussion
The SAC was originally developed to provide an objective method of immediately assessing the mental status of an individual with a suspected concussion.58 It is designed to act as a supplement to other diagnostic assessments. The 5- to 10-minute assessment involves a brief neuropsychological assessment and includes measures of orientation, immediate memory, concentration, and delayed recall.59 Previous studies have supported the validity,59,60 accuracy, and reliability of this tool as a test for determining the presence of concussion.61 However, this tool alone is not appropriate to make a return-to-play decision, and clinicians should interpret results with caution. In fact, Koscs et al61 suggest that clinicians should place less emphasis on the numerical SAC score and more emphasis on using the components of the SAC to evaluate neurocognition (ie, orientation, memory, and concentration) postconcussion.
Sport Concussion Assessment Tool 2
The SCAT2 is a standardized method of evaluating injured athletes (aged 10 years and older) for concussion and is one of the most widely used assessment tools. The SCAT2 is used for sideline and clinical assessment of concussion by determining a combination of scores from of a 22-item Postconcussion Symptom Scale (the number of symptoms and severity of symptoms, 6-point Likert scale), physical signs of loss of consciousness and/or balance problems, the Glasgow Coma Scale, the Maddock score (assessment of orientation), the SAC (orientation, immediate memory, concentration, and delayed recall), a modified Balance Error Scoring System, and a coordination examination (finger-to-nose).3
The advantage of the SCAT2 is that it enables the calculation of the SAC score and includes evaluations of symptoms, orientation, balance, and coordination. It may be possible to evaluate individual components of the test such as symptoms reported or balance and coordination to assess changes in specific domains. For example, Schneiders et al62 assessed the reliability of the motor performance component of the SCAT2 (ie, single-leg and tandem balance, finger-to-nose coordination) after a suspected concussion. They found an improvement in the subjects' performance in these motor tasks after exercise.62 These findings have implications for practicing clinicians to use components of the SCAT2 to reassess symptoms or specific performance during gradual return to physical activity. In addition, because the SCAT2 uses symptom scales to assess headache, depression, fatigue, and mood states, it could help guide clinician referrals, treatment, and management.63 Notably, healthy adolescent athletes have been shown to display significant interindividual variability in SCAT2 scores at baseline, and thus a SCAT2 assessment prior to play (eg, during an athlete's preseason) may be advisable.64 Both the SAC and the SCAT2 are primarily used to assess neurocognitive impairment and have not been validated for evaluating recovery from concussion.
Immediate Postconcussion Assessment and Cognitive Testing
The ImPACT is a computerized neuropsychological test battery designed to objectively measure a number of different aspects of cognitive function (including attention, working memory, reaction time, and nonverbal problem solving), as well as the severity of 22 concussion symptoms, using a 7-point Likert scale.65 A number of studies have been conducted to assess the sensitivity and reliability of this instrument for diagnosing concussion in a sports setting. Schatz et al66 suggested that the ImPACT is useful for assessing the neurocognitive and behavioral sequelae associated with concussion.66 They reported a sensitivity of 81.9% and a specificity of 89.4% in 72 concussed high school athletes, compared with 66 age- and education-matched controls with no history of concussion. In-depth neuropsychological testing provides a valuable assessment tool to detect neurocognitive impairments associated with concussion that may be present in people who are seemingly asymptomatic.4
CLINICAL MANAGEMENT
The current guidelines of concussion management emphasize physical and cognitive rest until symptoms improve or resolve, followed by a graded program of activity.3 These guidelines have not been based on research evidence but rather on consensus statements from leaders in the field of concussion.3,67 In fact, to date, there have been no randomized controlled human trials to evaluate the effects of rest versus exercise or an evaluation of specific intervention approaches. Furthermore, there are no reports in the literature documenting changes in the trajectory of recovery due to specific rehabilitation approaches.15
A further complication in determining the criteria for return to activity is the variability in symptoms across individuals. McCrea et al68 suggested that “rest” in the form of delaying return to competitive sports may be better served by a universal period of 7 to 10 days than by symptom monitoring, primarily to prevent the potential for reinjury. However, there is evidence that rest may exacerbate or even elicit concussion-like symptoms.69 In addition, there is literature showing that regular physical exercise alleviates many symptoms of associated health problems often linked to TBI, such as anxiety,70 depression, chronic fatigue, and chronic pain.69
While many studies support the idea that strenuous exercise should be avoided postconcussion,4,69 there are conflicting reports regarding whether light exercise that produces modest heart rate increases (eg, walking, swimming, or low-intensity cycling) may be beneficial or detrimental for neuropsychological function.61,71 Majerske et al72 observed poor performance on visual memory and reaction time in composite tests in athletes who engaged in either high-intensity physical activity (eg, return to full sports participation) or no physical activity postconcussion, compared with those performing intermediate levels of activity (ie, light exercise). However, Covassin et al71 were among the first to show impairment on the ImPACT verbal memory composite score, immediate memory, and delayed memory composite score following a
O2 max treadmill test in healthy individuals, suggesting that maximal exercise itself may be a principal cause of poor scores in neurological testing. Other research suggests that despite a difference in cardiovascular response, concussed athletes and their matched controls reported similar symptoms before and after exercise.73 Furthermore, Majerske et al72 reported that athletes with the highest performance on neurocognitive tests and lowest symptom scores engaged in intermediate levels of activity after concussion.
Findings from animal literature suggest that timing of engaging in physical activity is just as crucial to recovery as the intensity of that activity.74,75 In rats, after experimentally induced TBI, acute exercise prevented upregulation of brain plasticity–related proteins normally associated with exercise, compared with noninjured rats.74 Whereas, evidence of protein upregulation and greater recovery was shown when exercise delivery was delayed.75 These results require further investigation in humans but suggest that engaging in low or intermediate levels of activity postconcussion may not be detrimental and, depending on the timing of delivery, could potentially expedite recovery.
CLINICAL IMPLICATIONS
As the incidence of concussion continues to increase,4 a comprehensive understanding of the underlying neural substrates of injury and recovery is necessary to improve preventative strategies, develop evidence-based guidelines, and optimize management strategies. Concussion involves a spectrum of symptoms that often evolve over time. No single assessment tool has been shown to reliably capture all the motor and cognitive changes at the time of injury or to document the trajectory of recovery. Novel neuroimaging approaches in combination with clinical observation and concussion-specific assessment tools may provide different pieces of a complex puzzle about specific changes in the brain to precisely categorize the presence and severity of concussion, predict rate and extent of recovery, and evaluate the efficacy of therapeutic interventions aimed at reducing short- and long-term impairments.
Tools such as diffusion tensor imaging have the potential to provide a neural biomarker of concussion severity by characterizing microstructural changes in brain white matter. Consequently, this information may improve the understanding of brain injury and guide clinical management following concussion. Magnetoencephalography is increasingly becoming recognized as a powerful tool to evaluate the dynamics of brain activity and holds significant promise for understanding the relationship between functional and anatomical connectivity following brain injury. There is also increasing evidence that advanced functional neuroimaging methods like functional magnetic resonance imaging can provide more sensitive indications of underlying functional brain pathology even when individuals are clinically asymptomatic. An understanding of the overall risk factors for concussion/mTBI is also crucial for appropriate and timely diagnosis and management.
While neuroimaging may not be within the scope of current practice for many clinicians, diagnostic imaging is becoming more routine, and physical therapists are optimally positioned to interpret and evaluate this information and make recommendations to optimize functional recovery. It is important in the therapeutic management of concussion to use any available quantitative information from diagnostic imaging procedures and acute assessments of concussion status (eg, sideline concussion assessment tools) to aid physical therapists in their clinical assessment. Integrating these key sources of information will facilitate development of individualized plans of care aimed at ameliorating functional impairments and activity limitations.
Finally, recent research suggests clinical management of concussion should avoid strenuous exercise; however, intermediate levels of activity may not be harmful and could potentially accelerate recovery during a graded return to physical activity protocol. Clinicians should also remain aware of the potential effects strenuous exercise have on neurocognitive function in both healthy individuals and individuals with concussion and evaluate results obtained with neurocognitive tools accordingly.
SUMMARY
The increased incidence of sports-related concussions and the potential serious long-term consequences of injury on both the mature and developing brain have enormous clinical, societal, and economic impacts. Although there has been considerable media attention regarding the impact of concussion and the long-term implications associated with repeated head trauma, the science of concussion is still at an early stage. Clinicians who are informed of the latest research and have a broad understanding of the applications of novel and emerging imaging tools will be well positioned to understand the pathophysiology of concussion and develop effective clinical practice guidelines in the management of concussion.
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