Michael W. Collins PhD
Jamie E. Pardini PhD
Concussion, or mild traumatic brain injury (MTBI), is a topic that has received much recent attention in the field of sports medicine, both in national and international forums. By early estimates, the reported incidence of concussion in high school football players was approximately 19%, though a recently published study has shown a decreasing trend in concussion in football players, with a 4% reported incidence in 1999. However, given the significant variation in definitions and diagnostic criteria for concussion, the incidence of this injury is likely underestimated. Although most media coverage of the injury as a public health issue has focused on cases of professional athletes, it is high school and collegiate athletes who are at greatest risk and are most commonly seen in sports medicine clinics for evaluation of concussion.
Essentials of Diagnosis
General Considerations
One of the many problems in managing concussion in athletes is the lack of a universally accepted definition of concussion. Over the past 40 years, the most widely accepted definition has been the one proposed by the Committee on Head Injury Nomenclature of Neurological Surgeons in 1966. That committee defined concussion as “a clinical syndrome characterized by the immediate and transient post-traumatic impairment of neural function such as alteration of consciousness, disturbance of vision or equilibrium, etc., due to brain stem dysfunction.”
More recently, however, other definitions of concussion have been posed. Many clinicians and researchers currently use the definition of concussion proposed by the American Academy of Neurology (AAN): “Any trauma induced alteration in mental status that may or may not include a loss of consciousness.”
This definition was prompted by the belief of the AAN that the definition of the Committee on Head Injury Nomenclature may be too limiting, as the injury is not confined to the brain stem and may involve other brain structures (eg, cortical areas). This definition also served to emphasize the fact that concussion may occur with or without a loss of consciousness.
Bailes JE, Cantu RC: Head injury in athletes. Neurosurgery 2001;48:26.
Levy ML et al: Analysis and evolution of head injury in football. Neurosurgery 2004;55:649.
Lovell MR, Collins MW: Neuropsychological assessment of the head-injured professional athlete. In: Neurological Sports Medicine. Bailes JE, Day AL (editors). American Association of Neurological Surgeons, 2001.
Pathogenesis
Recent research into the subtle metabolic effects of concussion has led to increased understanding of its acute presentation and implications. Using a rodent concussion model, a process was elucidated whereby significant changes occur in the intracellular and extracellular environment of injured cells. These metabolic changes are the result of excitatory amino acid (EAA)-induced ionic shifts with increased Na/K-ATPase activation and resultant hyperglycolysis. Thus, there is a high demand for energy within the brain shortly after concussive injury. This process is accompanied by a decrease in cerebral blood flow that is not well understood. Decreased cerebral blood flow is hypothesized to be the
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result of an accumulation of endothelial Ca2+, which is thought to cause widespread cerebral neurovascular constriction. The resulting “metabolic mismatch” between energy demand and energy supply within the brain may propagate a cellular vulnerability that is particularly susceptible to even minor changes in cerebral blood flow, increases in intracranial pressure, and apnea. Animal models have indicated that this dysfunction can last up to 2 weeks or theoretically longer in the human model. Although the generalization of this theory of metabolic dysfunction to humans remains premature, it does raise important questions regarding the threat of vulnerability, how long it lasts, and if it is accompanied by identifiable markers of both injury and recovery.
Bergschneider M et al: Cerebral hyperglycolysis following severe human traumatic brain injury: a positron emission tomography study. J Neurosurg 2003;86:241.
Hovda DA et al: Neurobiology of concussion. In: Sports Related Concussion. Bailes JE et al (editors). Quality Medical Publishing, 1999.
Clinical Findings
Given the subtleties and variation in the presentation of a concussive injury, a thorough assessment of all signs and symptoms is crucial in making an accurate diagnosis of concussion. Following a concussion, athletes may present with only one symptom or a constellation of many postconcussion symptoms, any and all of which are important from a diagnostic and management standpoint. It should be stressed that sideline presentation may vary widely from athlete to athlete, depending on the biomechanical forces involved, an athlete's prior history of injury, and numerous other factors. To date, no individual sign or symptom of concern (eg, headache, anterograde amnesia, retrograde amnesia, and balance problems) has been proven to directly correlate with the severity of the concussion. There is speculation, as well as published data, that retrograde amnesia and/or posttraumatic amnesia may be better indicators of poor outcome, though stating this conclusively is premature. Table 8-1 summarizes common on-field signs and symptoms of concussion as presented on a commonly used sideline concussion card provided by the University of Pittsburgh Medical Center.
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Table 8-1. University of Pittsburgh Medical Center's sideline concussion card: signs and symptoms of concussion. |
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It is most helpful, though not always possible, to gain information on symptoms from multiple informants (athlete, athletic trainer, coach, teammates, parents) across multiple time points (eg, symptoms immediately following injury, a few hours later, at 24 hours, at 48 hours, etc). Multiple informants are useful, not only because a presenting amnesia and/or loss of consciousness may prevent athletes from accurately describing their own symptoms for a given period of time, but also because athletes may minimize, deny, or mask their symptoms, hoping to return to play more quickly.
Headache is the most commonly reported symptom of concussion and has been reported in up to 80% of affected athletes. However, the absence of headache does not preclude a diagnosis of concussion,
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highlighting the importance of a thorough assessment of all symptoms. Assessment of postconcussion headache may be complicated by the presence of musculoskeletal headaches and other preexisting headache syndromes (eg, migraine disorder or frequent stress headaches). However, any presentation of headache following a blow to the head or body should be managed with care.
Most frequently, a concussion headache is described as a sensation of pressure in the skull that may be localized to one region of the head or may be more generalized in nature. In some athletes (particularly athletes with a history of migraine), the headache may take the form of a vascular headache, may be unilateral, and is often described as throbbing or pulsing. Most commonly, postconcussion headache becomes worse with physical exertion. Thus, if the athlete's headache becomes worse during provocative exertional testing or return to play, postconcussion headache should be suspected and conservative management is indicated. Headaches due to concussion may not develop immediately after injury, and in fact may not develop until many hours after injury, again underscoring the need to assess symptoms at multiple time points postinjury.
Given the prevalence of headache with a concussive injury, the relation of this symptom to outcome has recently been examined. One study examined concussed high school athletes who reported headache versus those who did not at an assessment occurring approximately 1 week postinjury. Results indicated that athletes with headaches performed significantly worse on reaction time and memory measures on computerized neuropsychological testing, reported significantly more symptoms on the Post-Concussion Symptom Scale, and were more likely to have experienced an on-field anterograde amnesia than athletes without headaches. Another recent project examining headache type and outcome from concussion emphasizes the importance of proper assessment for the presence and type of postconcussion headache. Concussed athletes who present with no headaches (non-HA) or with headaches that do not meet the criteria for posttraumatic migraine (HA), and athletes who present with headaches that include symptoms of posttraumatic migraine (PTM) were compared on various postconcussion outcome measures. Overall, PTM athletes demonstrated the worst outcomes. Specifically, the PTM group (those reporting headache, nausea, and sensitivity to light and/or noise) demonstrated more pronounced cognitive deficits at postinjury testing than did either the HA or the non-HA group. The PTM group also demonstrated a greater departure from baseline neuropsychological testing scores than did either of the other headache groups. Thus, concussed athletes presenting with symptoms of posttraumatic migraines may need to be more conservatively managed than others, and may evidence more significant deficits and perhaps protracted recovery times.
Although headache following a concussion does not necessarily constitute a medical emergency, a severe or progressively worsening severe headache, particularly when accompanied by vomiting or rapidly declining mental status, may signal a life-threatening situation such as a subdural hematoma or intracranial bleed. This should prompt immediate transport to a hospital and imaging of the brain with computed tomography (CT) and/or magnetic resonance imaging (MRI).
In addition to headache, many other symptoms may emerge as the result of a concussive injury. Balance problems, lack of coordination, or dizziness may also be reported. Moreover, an athlete may report increased fatigue, feeling slowed down (cognitively or physically), or feeling lethargic. Fatigue is especially common in concussed athletes in the days following injury, and from a clinical perspective, seems to occur almost as frequently as headache. Athletes often report brief changes in vision as a result of concussion. These may include blurred vision, changes in peripheral vision, seeing “spots” or “lines,” and/or other visual disturbances. They may also report cognitive changes, including problems with attention, concentration, short-term memory, learning, and multitasking. These symptoms typically manifest after an athlete has returned to school or work. Changes in mental status such as confusion may also be reported by athletes, although because it is typically a readily observable phenomenon, it is reported most frequently and in better detail by others.
Another frequently reported symptom that has gained recent research attention is a reported sensation of feeling “foggy” following concussion. Specifically, a sample of concussed high school students who indicated feeling “foggy” on a symptom inventory were compared to concussed high school athletes who did not experience this sensation. Results indicated that the “foggy” group demonstrated significantly slower reaction times, attenuated memory performance, and slower processing speed via computerized neurocognitive testing. In addition, the “foggy” athletes also indicated a significantly higher number of other postconcussion symptoms when compared to the group who did not experience fogginess. The results of this study, like the studies examining posttraumatic migraines and headaches in general, reveal the potential importance of any reported or observed symptom in impacting the diagnosis and recovery time or in indicating the severity of the concussion.
Another commonly reported or observed symptom involves emotional changes. Most often, athletes will report increased irritability, or having a “shorter fuse.” However, other emotional changes may occur such as sadness/depression, nervousness/anxiety, or even (much less commonly) silliness or euphoria. Affect may be described by the athlete or parent as flattened or labile.
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Emotional changes may be very brief (eg, a linebacker bursts into tears for 30 seconds on the sideline) or may be prolonged in the case of a more significant injury (an athlete reports persistent depression).
Appropriate acute care and management of the concussed athlete begin with a detailed and accurate assessment of the severity of the injury. As with any serious injury, the first priority is always to evaluate the athlete's level of consciousness and ABCs (airway, breathing, and circulation). The attending medical staff must always be prepared with an emergency action plan in the event that the evacuation of a critically head- or neck-injured athlete is necessary. This plan should be familiar to all staff, be well delineated, and be frequently rehearsed.
Upon ruling out more severe injury via neurologic and clinical examination, the acute evaluation continues with assessment of concussion. First, the clinician should determine whether a loss of consciousness (LOC) has occurred. By definition, LOC represents a state of brief coma in which the eyes are typically closed and the patient is unresponsive to external stimuli. LOC is relatively rare and occurs in less than 10% of concussive injuries. Moreover, prolonged LOC (>1–2 minutes) in sports-related concussion occurs much less frequently. Athletes with LOC are typically unresponsive for only a brief period of time, sometimes only 1–2 seconds, which may at times make LOC difficult to diagnose, as it often takes medical personnel at least several seconds to reach the injured athlete. Any athlete with documented LOC should be managed conservatively and return to play is contraindicated.
Although many of the concussion grading and management scales rely heavily upon the presence or absence as well as on the duration of loss of consciousness, research has indicated that the brief losses of consciousness (less than 1 minute) typically associated with sports-related concussion may be unrelated to outcome, and that other markers, such as amnesia, may be more important in predicting outcome. Recent work with athletes has found no differences in acute recovery from concussion between those experiencing brief LOC and no LOC. Certainly, extended LOC (typically defined as greater than 1 minute) should warrant immediate neurologic evaluation.
A more common form of mental status change following concussion involves confusion and amnesia. Confusion (ie, disorientation), by definition, represents impaired awareness and orientation to surroundings, though memory systems are not directly affected. An athlete demonstrating postinjury confusion will typically appear stunned, dazed, or “glassy-eyed” on the sideline or playing field. In athletes who do not remove themselves from play confusion is often manifested by difficulty with appropriate play-calling, failure to correctly execute their positional assignment during play, or difficulty in communicating game information to teammates or coaches. Teammates are often the first to recognize that an athlete has been injured when the athlete begins demonstrating the above signs and has difficulty maintaining the flow of the game. On the sidelines, confused athletes may answer questions slowly or inappropriately, may ask “what is going on” or “what happened,” and may repeat things during evaluation. Some may be temporarily disoriented to time or place, and even, very rarely, to person (eg, not knowing coaches or teammates).
To properly assess the presence of confusion, medical personnel can ask the athlete simple orientation questions such as the date or the names of the stadium, city, and opposing team. Table 8-2 contains a list of orientation questions extracted from the University of Pittsburgh Medical Center's Concussion Card.
Amnesia is emerging as perhaps the most important sign to carefully assess following concussion (clearly, after more serious injuries have been ruled out). Amnesia due to concussion may present as retrograde amnesia (difficulty remembering events prior to the injury) or posttraumatic/anterograde amnesia (difficulty remembering events following the injury). Both forms of amnesia should be assessed thoroughly and taken very seriously in the evaluation and management of sport-related concussion. Athletes who present with one or both types of amnesia may initially have difficulty recalling large spans of time either before or after the injury (or both), though these larger periods of amnesia will frequently shrink as the injury becomes less acute. The presence of amnesia, even for only a few seconds, has been found to be predictive of postinjury cognitive deficits and postconcussion symptoms.
Posttraumatic amnesia and anterograde amnesia are synonymous terms that represent the duration of time between the head trauma (eg, an ice hockey player's forehead striking the boards) and the point at which the athlete reports a return of normal continuous memory functioning (eg, remembering the athletic trainer asking the athlete orientation questions in the locker room). On-field or sideline anterograde amnesia may be assessed through immediate and delayed (eg, 0, 5, 15 minute) recall for three words (eg, girl, dog, green), as detailed in Table 8-2 (University of Pittsburgh Medical Center Concussion Card Mental Status Testing).
At times, especially during an acute assessment, confusion and anterograde amnesia may be difficult to disentangle. It is important to remember that confusion is not associated with a loss of memory, whereas amnesia is present only with a loss of memory. This memory loss may span a few seconds, hours, and, less frequently in concussion, days. A practitioner may be unable to dissociate confusion and amnesia until the athlete's confusion
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has resolved, and he or she is better able to discuss actual memories surrounding the injury. Once the athlete is lucid, the practitioner may gain additional insight into any existing anterograde amnesia by asking the athlete to recall the events that occurred immediately following the trauma (eg, rising from the ground, walking/skating to the sideline, memory for any part of the game played or observed after the injury, memory for the score of the contest, and memory of the ride home). Anterograde amnesia is indicated by failure to remember any of the above (or similar) details.
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Table 8-2. University of Pittsburgh Medical Centers' sideline concussion card: acute (sideline or on-field) mental status testing. |
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Retrograde amnesia is the inability to recall events preceding a head trauma. To determine the presence and duration of retrograde amnesia, the patient should be questioned about events that occurred immediately before the concussion. Commonly used questions to assess retrograde amnesia are presented in Table 8-2. Medical personnel may ask the athlete to recall details of the actual injury (eg, seeing a linebacker charge toward him with his helmet down, then falling backward and striking the back of his head on the ground). Then, additional questions can probe events that are increasingly remote from the injury (eg, the score at the beginning of the first quarter, coming onto the field for stretching exercises, getting dressed in the locker room). The length of retrograde amnesia will typically “shrink” over time. As recovery occurs, the period of retrograde amnesia may contract from hours to several minutes or even seconds. However, by definition, a permanent loss of memory prior to the injury will remain. As with anterograde amnesia, even very brief retrograde amnesia may be considered pathognomonic and possibly linked to outcome in the form of protracted recovery, increased symptoms, etc.
Burgeoning data and studies emphasize that any athletes exhibiting a change in mental status (eg, confusion), posttraumatic/retrograde amnesia, and/or LOC be removed from and not be allowed to return to play, regardless of how long these symptoms take to “clear.”
Given that concussion is a metabolic and not a structural injury, traditional neurodiagnostic techniques such as the CT scan, MRI, or neurologic examination are almost always unremarkable following injury. Despite this fact, these techniques are invaluable in ruling out more serious pathology (eg, cerebral bleed or skull fracture) that may also occur with even seemingly mild head trauma. It is important to remember that a negative finding on a CT scan, MRI, etc does not rule out concussion, and
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should not be the basis for determining if an athlete is ready to return to play. Clinically, the sports medicine practitioner will likely encounter cases in which an athlete has been mistakenly returned to play based upon a negative CT and the athlete's assertion that he or she “feels fine.” These individuals may return days or weeks later with a second concussive injury that has resulted from seemingly minimal force and that typically requires much more time to resolve.
Despite the insensitivity of traditional neuroimaging in detecting concussion, there are many new neurodiagnostic techniques under investigation for their potential utility in identifying and/or managing concussion. Functional imaging and other techniques, though in early stages of development, may provide valuable information regarding concussion in the future. Techniques such as magnetoencephalography (MEG), functional magnetic resonance imaging (fMRI), positron emission tomography (PET), and the monitoring of brain electrophysiological activity through event-related potentials (ERPs) may provide additional insight into the physiology of injury and recovery, and may provide the foundation for the establishment of neurodiagnostic norms against which clinicians may accurately assess the severity of the concussion and the prognosis for recovery.
Perhaps the most important new development in the management of sports-related concussion is the recognition of neuropsychological or neurocognitive testing (synonymous terms) as a key element of the postconcussion evaluation process. Neurocognitive testing has contributed to the development of a more individualized and data-driven approach to the management of concussion. Neurocognitive testing was first used as a diagnostic tool in sports medicine in the mid-1980s within the context of a large multisite research project undertaken by Barth and his colleagues at the University of Virginia. The study demonstrated the utility of neuropsychological test procedures in documenting cognitive recovery within the first week following concussion. In the 1990s, a series of events shifted the use of neuropsychological testing in sports from the research to the clinical arena. First, concussive injuries in well-known professional athletes raised awareness and resulted in the implementation of baseline neuropsychological testing by a number of National Football League (NFL) teams. Similarly, after career-ending concussive injuries in athletes in the National Hockey League (NHL), the NHL mandated baseline neuropsychological testing for all athletes. In addition to the increased use of neuropsychological testing in professional sports, several large-scale studies of collegiate athletes were undertaken. These studies further demonstrated that neuropsychological testing yielded useful clinical information. Specifically, it allowed a baseline/postinjury analysis of the subtle aspects of cognitive function likely affected by concussive injury, thus providing objective data that could be used to make more informed decisions regarding return to play.
Neuropsychological testing of athletes participating in contact sport has been accomplished in two ways. In its early phases, and in many settings today, traditional neuropsychological testing (eg, paper and pencil testing) has been used to provide both baseline cognitive functioning levels and postinjury follow-up. However, as an increasing number of sports organizations recognized the utility of neuropsychological testing, many limitations to traditional testing procedures emerged. For example, traditional neuropsychological testing is quite time consuming and costly, making it difficult to implement in amateur (eg, high school) settings. Also, the availability of trained neuropsychologists to administer and interpret the tests is limited. Lastly, the majority of athletes participate in sports at the amateur, high school, and college levels, where traditional testing is often not practical, affordable, or possible. These limitations, as well as a continual increase in the number of sports organizations seeking neuropsychological testing as a key element in concussion management, led to the development and proliferation of computer-based neuropsychological testing procedures.
Computer-based neuropsychological testing procedures have a number of advantages and relatively few disadvantages when compared to more traditional testing procedures. First, the use of computers allows large numbers of student athletes to be evaluated with minimal manpower. For example, an entire football team may be baseline tested in one or two sessions in a school's computer laboratory. Second, data acquired through testing can be easily stored in a specific computer or computer network and can therefore be accessed at a later date (eg, following injury). Third, the use of the computer promotes a more accurate measurement of cognitive processes such as reaction time and information processing speed. In fact, computerized assessment allows response times that are accurate to 1/100 of a second to be evaluated, whereas the accuracy of traditional testing is only 1–2 seconds. This increased accuracy no doubt increases the validity of test results in detecting subtle changes in neurocognitive processes. Fourth, the utilization of the computer allows for the randomization of test stimuli, which should improve reliability across multiple administration periods, minimizing the “practice effects” that naturally occur with multiple exposures to the stimuli. These practice effects have clouded the interpretation of research studies and have also presented an obstacle for the clinician evaluating the true degree of neurocognitive deficit following injury. Lastly, computer-based approaches allow clinical information to be rapidly disseminated into a coherent clinical report that can be easily interpreted by the sports
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medicine clinician. In summary, there are many benefits derived from a computer-based approach insofar as the technology has appropriate sensitivity, reliability, and validity in measuring the subtle aspects of concussive injury.
Neurocognitive deficits resulting from concussion have been documented in many studies, and cognitive testing appears to be a highly valuable tool in documenting impairment or incomplete recovery from concussive injury. Neurocognitive deficits associated with concussion have also been documented in studies of collegiate and high school football players, amateur soccer players, and samples of athletes across multiple sports. Neurocognitive evaluation is a sensitive tool that may be utilized to assess the often subtle and potentially debilitating effects of concussive injury. Neurocognitive test data appear to provide objective, quantifiable, and individualized standards to better determine safe return to participation and overall management of the concussed athlete, and should therefore be considered a critical factor in the management of concussion.
Although neuropsychological testing is currently regarded as a gold standard in management of concussion, there are other measures that may be beneficial in the diagnosis and evaluation of concussion. The NeuroCom Smart Balance Master has been used to test for postural instability after mild head injury in an attempt to set the precedence for establishing recovery curves based on objective data. Concussed athletes exhibited increased postural instability for the first 3 days following injury. Balance testing or postural stability has recently been a popular topic among some clinicians, but current research in this area has been conducted with small sample sizes and has yet to be confirmed with larger groups of athletes.
Differential Diagnosis
The diagnosis of cerebral concussion can be a difficult process for many reasons. As previously mentioned, many differences exist in diagnostic criteria/classification, and there is a lack of one unified definition for the injury. In addition, there may be no direct or observed trauma to the head. Also, the concussed athlete often does not lose consciousness as a result of the injury. At times, an athlete may not immediately be aware that he or she has been injured. The injury may be very subtle and the athlete may not show any obvious signs of concussion such as disequilibrium, gross confusion, or obvious personality change. To further complicate the situation, athletes at all levels of competition may minimize or hide symptoms in an attempt to remain in the game, thus creating the potential for exacerbation of their injury. However, a clinical interview and thorough assessment of signs and symptoms will assist in making an accurate diagnosis.
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Treatment
Presently there are no curative medical treatments for concussion. This emphasizes the importance of early identification, evaluation, and management of a concussion and the resultant symptoms, as well as the prevention of additional injury or the exacerbation of a current injury through early return to physical exertion or early return to play. If a concussion does not resolve after a month or more, and/or postconcussion symptoms become unbearable and interfere with a patient's daily functioning, a physician may elect to treat the symptoms of concussion. For example, a patient with severe posttraumatic migrainous headaches may be treated with preventative (eg, Effexor, Wyeth Pharmaceuticals) or abortive (eg, Imitrex, GlaxoSmithKline) medication (or a combination of both). A patient troubled by significant
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dizziness, balance problems, or presyncopal symptoms may be referred for evaluation and treatment through a balance clinic or referred to a neurologist for further evaluation. If an athlete remains troubled by extreme fatigue or difficulties with attention, a physician may elect to try a stimulant or similar medication to alleviate those symptoms (eg, Strattera, Eli Lilly and Co.). In more severe cases of unremitting cognitive problems, a patient may be referred for cognitive rehabilitation. Although the treatment modalities described above my alleviate some of the symptoms related to concussion or mild traumatic brain injury, none has been demonstrated to “cure” the metabolic dysfunction of concussion.
Prognosis
As previously detailed, current research has yet to delineate the exact metabolic process of concussion in humans. However, the current model of the pathophysiology of concussion raises important clinical and research questions and considerations when attempting to determine the prognosis of injury. Based upon research findings thus far, it has been postulated that until metabolic dysfunction resulting from concussion is fully resolved, the injured person may be at significantly increased neurologic vulnerability if a second trauma (even minor) is sustained. In theory, sustaining a second head injury during a period of increased vulnerability with unresolved metabolic dysfunction has been linked to second impact syndrome.
Second impact syndrome has been previously reported in the literature and varying reports suggest that as many as 35 or more athletes in the past decade have succumbed to this syndrome. In all cases, athletes sustained an initial concussive injury, returned to sports or other activities, and sustained a second, typically milder, concussive injury. The second blow resulted in dysautoregulation, massive edema, uncal herniation, and coma, which is followed by death shortly after the blow. Morbidity is 100% in the case of second impact syndrome, whereas mortality is reported to occur in up to 50% of cases. To date, all reported cases of second impact syndrome have occurred in younger athletes, typically adolescent high school students. Theory posits that younger athletes may be more vulnerable to the dysautoregulation seen in this syndrome. Regardless, it appears that younger, “immature” brains may be more vulnerable to the devastating effects of this condition. Debate does surround this construct and whether an initial concussion is definitively required for second impact syndrome to occur.
Current clinical experience and research have suggested that proper management of concussion should lead to a good prognosis with minimal or no evidence of chronic or catastrophic brain dysfunction. Long-term deficits in the form of postconcussion syndrome have been observed from a single concussive event, though it is much more common in repetitive occurrences of concussion with poor management and premature return to play following an initial concussion. Postconcussion syndrome typically results in a constellation of somatic (eg, headaches, dizziness, balance deficits), cognitive (eg, deficits with memory, attention, executive dysfunction), personality (eg, depression, anxiety), and/or sleep disturbances (eg, difficulty initiating and maintaining sleep) that, though tacit, may be incapacitating and chronic. The duration of postconcussion syndrome is quite variable, though it has been observed to last months, or even years, in athletes. The true incidence of postconcussion syndrome in athletes remains unknown, though it is experientially relatively frequent, especially at the high school level of sport participation.
Medical professionals agree that allowing an athlete to participate in contact sports prior to complete recovery may greatly increase the risk of poor outcome, including chronic postconcussion syndrome or even catastrophic neurologic sequelae (as in cases of second impact syndrome). Thus, the most important step a practitioner can take toward a positive prognosis is proper assessment and management of concussion in the acute and follow-up stages of injury. A management protocol will be presented later in this chapter.
Management Guidelines
More than 20 concussion management guidelines have been published over the past 30 years, all of which were intended to assist physicians in determining both the severity of injury as well as when an athlete may return to play. Most were primarily developed by panels of experts in the field and are based on popular belief or clinical impressions. When using these guidelines, severity of injury was determined by an accompanying grading scale. In general, a Grade 1 concussion involves symptoms lasting 15–20 minutes or less; a Grade 2 concussion involves symptoms lasting longer than 15 or 20 minutes; and a Grade 3 concussion is typically any concussion involving loss of consciousness. However, perusal of the guidelines and grading scales reveals many differences of clinical opinion. The significant variations that can occur between scales, the fact that these scales are often based upon clinical impressions rather than research, as well as the multitude of guidelines that exist create confusion and debate among practitioners. Within this context, grading scales have helped in creating awareness of concussive injury and in establishing a nomenclature for classification. Although “grading scales” are appropriately being replaced with individualized management protocols (see above), they have played an important role in the “evolution” of proper management of concussion.
In 1999, the American Orthopaedic Society for Sports Medicine (AOSSM) published a report detailing
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the state of the current guidelines and establishing possible practical alternatives to the guideline system. Although the AOSSM guidelines did not differ substantially from prior grading systems and guidelines, this report stressed more individualized management of injury, rather than applying general standards and protocols (eg, grading systems) to all injuries.
In 2001, the Federation Internationale de Football Association (FIFA) in conjunction with the International Olympic Committee (IOC) and the International Ice Hockey Federation (IHF) assembled a group of physicians, neuropsychologists, and sports administrators in Vienna, Austria to explore methods of reducing morbidity and improve outcomes secondary to sports-related concussion. The agreement statement that arose from this meeting was published in 2002. Perhaps the most important agreement to emerge from the meeting was that none of the previously published concussion management guidelines was adequate to ensure proper management of every concussion. In their statement, the group emphasized the more individualized management and implementation of postinjury neuropsychological testing as a “cornerstone” of proper postinjury management and decisions involving return to play. A return-to-play protocol consistent with the Vienna group's recommendations will be elucidated later in this chapter.
In summarizing the evolution and current state of guidelines on the management of concussion, it is clear that these systems cannot be exclusively relied upon to make return to participation decisions. As previously stated, the number and variety of existing grading procedures, many with only subtle differences, can understandably create communication difficulties among medical personnel and others who manage concussed athletes. This lack of uniformity and lack of research reinforce current thinking that concussion is not a unitary phenomenon, and injured athletes must therefore be evaluated and managed on a case-by-case basis.
Return to Play
Once an athlete has sustained a concussion, the clinician must decide when the athlete may safely return to play. There is no simple evidence-based formula available to direct the clinician in this regard. The process may seem more ambiguous than many other decisions clinician may face, given the subtlety of the injury and the lack of research-grounded guidelines. Making the return to play decision is an individualized and dynamic process that should include evaluation of factors such as the severity of the injury (as measured by duration of loss of consciousness, amnesia, and confusion), the athlete's appraisal of the presence and intensity of symptoms (eg, headache, dizziness, visual changes), and, if available, the athlete's performance on neurocognitive testing. Importantly, a general awareness that symptoms of concussion may evolve over time and are also prone to worsen with exertion (ie, increased cerebral blood flow) is critical in helping to guide the clinician in establishing an assessment strategy. The one uniform agreement among experts is that any athlete known to be exhibiting signs or symptoms of concussive injury should not return to play, given the general issues surrounding increased neurological vulnerability to a second injury and that less biomechanical force may likely result in more severe postconcussion presentation.
In addition to signs and symptoms, there are many other factors that may play a role in an athlete's recovery trajectory, as well as in the decision as to when to return an athlete to participation in sports. Neuropsychological testing and continuing research have made it possible to identify individual factors that may play a role in the incidence, severity, and length of recovery regarding concussion.
In recent years, there has been an increase in the number of younger athletes who participate in sports. This influx of younger athletes focused attention on another limitation of grading scales, which is that most guidelines for return to play do not include or mention developmental considerations that are likely to be important when managing concussion, given that brain development continues throughout adolescence. Unfortunately, there has been no published research exploring the potential developmental differences in physiological recovery in the child or adolescent, though current theories are explored below. Recent research on cognitive recovery has demonstrated that high school athletes may recover more slowly than their collegiate counterparts, when recovery is defined as a return to baseline levels of cognitive functioning. Even in cases of very mild concussion or “bell ringers,” adolescent athletes were found to exhibit neuropsychological and symptom deficits for at least 7 days postinjury. These results are congruent with earlier studies showing age-based differences in recovery from concussion. Results from these age-specific research studies provide support for stopping all athletes under the age of 18 from participating in the athletic event in which they sustained a concussion, so that further evaluation can be undertaken (symptom inventories, cognitive testing, etc). Similar to this, recommendations from the Vienna meeting state that all athletes in whom concussion is diagnosed be removed from the playing contest. However, it should be noted that no prospective studies have examined the issue of mild concussion in college or professional-aged athletes. In addition, the overall risk/benefit analysis is likely to be different at different levels of competition. For example, professional athletes may be willing to assume greater risk through earlier return to play, given the
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obvious monetary and other considerations. Conversely, few parents would risk injury in a high school athlete, most of whom are unlikely to continue to compete beyond high school.
In addition to differences in cognitive recovery, age should be regarded as an important issue in management of concussion based on the fact that of the approximately 35 documented deaths related to second impact syndrome, the majority occurred in athletes between the ages of 13 and 18. Although no available research documents an age-based physiological or developmental vulnerability, many clinicians and researchers suspect that individuals who are younger, and therefore developmentally more immature, are at increased risk for second impact syndrome, and perhaps at risk for protracted recovery times following concussion.
One physiological theory exploring age-related differences is that children may undergo more prolonged and diffuse cerebral swelling after MTBI, which suggests that they may be at an increased risk for secondary intracranial hypertension and ischemia. This may also lead to a longer recovery period and could increase the likelihood of permanent or severe neurological deficit should reinjury occur during the recovery period. Another hypothesis is that the immature brain may be potentially 60 times more sensitive to glutamate-mediated N-methyl-D-aspartate (NMDA) excitotoxic brain injury. This hypersensitivity may render the child or adolescent more susceptible to the ischemic and injurious effects of EAA after MTBI.
As an alternative to theories of developmental vulnerability, the popular concept of cortical plasticity suggests that younger athletes should make a more complete recovery than their older counterparts. There has been clinical evidence of marked synaptic excess in children, relative to adults, which allows for neural pathway rerouting during recovery and functional plasticity in the developing brain. As time is not addressed in this theory, it may be assumed that a more complete recovery is possible due to the described plasticity, although it may take a longer period of time. Longitudinal and prospective studies examining the effects of age on outcome of sports concussion are currently underway and, in time, may elucidate this important clinical consideration.
Recent trends in sport participation have also indicated increased participation of girls and women. Thus, the issue of whether there are gender differences in incidence of concussion, recovery, and severity has become quite important. To date, very little research has specifically examined gender differences in MTBI. The majority of the published literature has focused on nonathletic populations (eg, accident victims) and on rodents. A recent meta-analysis of 8 studies and 20 outcome variables revealed that across 85% of those variables, outcome in women was worse. In studies unrelated to sports, findings have suggested that women with MTBI are more likely to report sleep disturbances and headaches up to a year after injury, may be less likely than men to be employed or in school 1 year after mild head injury, and suffer a significant decrease in grade point average (GPA) as compared to controls; there were no similar findings for men. Even when controlling for other demographic, premorbid, and event-related factors, most research to date has shown that women have worse outcomes than men after MTBI.
Although the literature on gender-based sports concussion is limited, a few studies have emerged. Barnes et al. retrospectively demonstrated that male elite soccer players suffered concussions of greater severity and were subject to a higher incidence of injury than were female elite soccer players. A prospective study involving 15 National Collegiate Athletic Association (NCAA) men's and women's soccer teams over two seasons revealed a similar incidence of concussion in men and women.
Although much of the available literature reveals poorer outcome among women suffering from MTBI, animal models suggest that female sex hormones may actually protect neurons in the brain following concussive injury. Progesterone is thought to reduce cerebral edema and potentially facilitate cognitive recovery, whereas studies of estrogen influence have yielded mixed results. One study has shown that estrogen plays a protective role in males while increasing mortality in females. Other research has demonstrated that estrogen can assist in maintaining normal cerebral blood flow and actually decrease mortality when administered acutely. All of the aforementioned research suggests there may be important gender differences impacting the incidence and severity of MTBI. More research in this area is necessary to accurately delineate the implications of such differences.
Learning disability (LD) refers to a heterogeneous group of disorders characterized by difficulties in the acquisition and use of listening, speaking, writing, reading, reasoning, or mathematical abilities and that is traditionally diagnosed in early childhood. The presence of a learning disability has been linked to lower baseline cognitive performance within a large, multiuniversity sample of football players. Learning-disabled football players who also reported a history of multiple concussions demonstrated reduced overall cognitive functioning when compared to athletes with multiple concussions who did not have a learning disability, and when compared to those with no history of concussion who had a learning disability, suggesting a potential additive effect. Therefore, knowing the educational history of athletes is important, as the presence of a learning disability certainly has the potential to complicate the
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diagnosis of concussion as well as the decision on return to play.
The potential contributing factor of a history of concussion to vulnerability to injury and to recovery is an often discussed topic in sports medicine, though consensus on this issue is elusive. Several studies suggest there may be cumulative detrimental effects of multiple concussions. These studies have typically examined cognitive impairment and neurological abnormalities in boxers. Lately, however, this topic has been of increasing concern among other athletic populations. In a study of almost 400 college football players, Collins and others discovered long-term subtle neurocognitive deficits in those suffering two or more concussions. Another study conducted by Matser and others similarly suggested that cumulative long-term consequences can be seen from repetitive blows to the head in professional soccer players. In another study Collins and colleagues found that high school and collegiate athletes suffering three or more concussions appear to be more vulnerable to subsequent injury than athletes with no history of injury. A study in 2004 by Iverson and others found baseline and postinjury deficits between amateur athletes with and without histories of concussion. Specifically, athletes with a history of concussion exhibited more symptoms of concussion at baseline (preinjury evaluation), scored lower on memory tests at 2 days postinjury, and were almost eight times more likely to demonstrate a significant drop in memory performance when compared to amateur athletes without a history of concussion. This accumulation of recent research points to likely cumulative effects of concussions; however, no currently reliable data are available to determine the number of concussions that should preclude return to participation or force retirement from sports. In addition, research has yet to determine the potential beneficial impact of properly managing each concussion prior to returning an athlete to play. Allowing a concussion to completely resolve through management according to Vienna conference-type recommendations (see below) may reduce the deleterious effects of multiple concussions.
American Academy of Neurology: Practice parameter: the management of concussion in sports (summary statement). Report of the Quality Standards Subcommittee. Neurology 1997;48:581.
Aubry M et al: Summary of the first international conference on concussion in sport. Clin J Sport Med 2002;12:6.
Bailes JE, Cantu RC: Head injury in athletes. Neurosurgery 2001;48(1):26.
Barnes BC et al: Concussion history in elite male and female soccer players. Am J Sports Med 1998;26:433.
Cantu RC: Posttraumatic retrograde and anterograde amnesia: pathophysiology and implications in grading and safe return to play. J Athletic Train 2001;36:244.
Collins MW et al: Relationship between concussion and neuropsychological performance in college football players. JAMA 1999;282:964.
Collins MW et al: Current issues in managing sports concussion. JAMA 1999;282:2283.
Collins MW et al: Cumulative effects of sports concussion in high school athletes. Neurosurgery 2002;51:1175.
Farace E, Alves W: Do women fare worse: a metaanalysis of gender differences in traumatic brain injury outcome. J Neurosurg 2000;93:539.
Field M et al: Does age play a role in recovery from sports-related concussion? A comparison of high school and collegiate athletes. J Pediatr 2003;142:546.
Grindel SH et al: The assessment of sports-related concussions: the evidence behind neuropsychological testing and management. Clin J Sport Med 2001;11:134.
Iverson GL et al: Cumulative effects of concussion in amateur athletes. Brain Injury 2004;18:433.
Lovell MR et al: Recovery from mild concussion in high school athletes. J Neurosurg 2003;98:296.
Lovell MR et al: Grade 1 or “ding” concussions in high school athletes. Am J Sports Med 2004;32:47.
Matser E et al: Neuropsychological impairment in amateur soccer players. JAMA 1999;282:971.
Roof RL, Hall ED: Estrogen-related gender differences in survival rate and cortical blood flow after impact acceleration head injury in rats. J Neurotrauma 2000;17:367.
Wojtys ED et al: Concussion in sports. Am J Sports Med 1999;27:676.
Concussion Management Model
Ideally, and if possible, a concussion management program for athletes should begin with baseline neurocognitive testing of athletes considered at high risk for concussion or mild traumatic brain injury. The definition of a “contact sport” varies from organization to organization, though it usually includes the sports of football, rugby, ice hockey, and soccer. Wrestling, field hockey, and basketball are also sports in which concussions are frequently seen. Even sports that do not seem to involve contact may on occasion lead to a concussive injury. In the sports of cheerleading, swimming, and diving, there have certainly been documented and sometimes severe cases of concussion. Baseline testing may also incorporate a baseline symptom report, such as the Post-Concussion Symptom Scale (see Table 8-3), to gain insight about an athlete's individual tendencies to report symptoms such as headache or attention problems when uninjured. Baseline testing is usually accomplished through the team athletic trainer or other athletic team staff. Once an athlete receives a valid baseline test, that test should serve for the tenure of the athlete's participation at that level of competition (eg, high school, college, professional levels).
It is also useful prior to the beginning of the season to educate athletes about sport-related concussion.
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Athletes at all levels should receive information about the common signs and symptoms of concussion, the variability in injury presentation, and the importance of reporting even a suspected concussion to the on-site medical personnel. In addition, either verbally or through educational materials, common myths about concussion should be dispelled (eg, athletes often believe that a concussion has not occurred if they do not experience loss of consciousness). In cases of child and adolescent athletes, the sports organization should attempt to educate parents and caregivers as well.
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Table 8-3. The postconcussion symptom scale. |
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Appropriate acute care of the concussed athlete begins an accurate assessment of the gravity of the situation. As with any assessment of a serious injury, the first priority is always to evaluate the athlete's level of consciousness and ABCs (airway, breathing, and circulation). The attending medical staff must always have an emergency action plan in the event that the evacuation of a critically head or neck-injured athlete is necessary. This plan should be familiar to all staff, be well delineated, and frequently rehearsed.
If concussion, without other brain injury, is suspected, the injured athlete should be administered a simple sideline mental status examination [eg, Standardized Assessment of Concussion (SAC) or University of Pittsburgh Medical Center (UPMC) On-Field Concussion Evaluation, see Table 8-2] to identify cognitive deficits and signs and symptoms of injury.
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Through this process, the clinician should document the presence and duration of loss of consciousness, amnesia, and confusion, as well as any other symptoms of concussion. Methods of assessing these symptoms have been described in the sections on “symptoms” and “signs” in this chapter.
A sideline assessment of cognitive functioning, signs, and symptoms should be completed even if the athlete asserts that he or she is “fine.” During the on-field examination, any overt neurologic/cognitive deficit or single sign or symptom of injury (eg, headache, confusion, balance problems, personality change) should preclude return of the athlete to participation for that contest, and signal the necessity of a more comprehensive examination. Serial evaluation and assessment of the athlete's status throughout the competition are important, especially as the presentation of concussion sequelae may be an evolving process. If there is resolution of all signs and symptoms (typically within 15 minutes) on a serial sideline examination as well as on exertion, returning the athlete to active participation that day may be a viable option. However, the risk–benefit ratio of returning younger athletes to play on the same day of competition should be carefully considered before a decision is made. Typically younger athletes, especially high school and below, are not returned to play during the same contest.
At present, prevailing standards of care require that an athlete satisfy three conditions before returning to play. From the standpoint of a sports medicine physician, the athlete should be asymptomatic at rest and during noncontact exertion before return to play is indicated. Once asymptomatic at rest, the athlete progresses through increasing noncontact physical exertion until he or she has demonstrated asymptomatic status with heavy noncontact physical exertion and noncontact sport-specific training. If there is access to cognitive/neuropsychological testing, the third Vienna conference criteria may be added whereby the athlete must exhibit intact cognitive functioning (ideally, through baseline-level performance on neurocognitive testing). Assessment of the three steps is reviewed below.
Separately or in conjunction with administration of a neurocognitive test battery, the athlete should complete a symptom inventory [such as the Postconcussive Symptom Scale (PCSS), see Table 8-3] or symptom interview both on the sideline (may be brief) and serially throughout recovery. Before progressing to any significant level of physical exertion, the athlete should report being asymptomatic at rest for at least 24 hours. If it is suspected that the athlete's report of asymptomatic status is false, a careful discussion of the importance of reporting all symptoms should be initiated. If there are others who present for evaluation with the athlete (parents, athletic trainers, teammates), asking these third party informants about the athlete's previous or current symptom complaints or signs of illness may be helpful.
An athlete who demonstrates asymptomatic status at rest should begin a graduated return to physical exertion prior to contact participation, as postconcussion difficulties may evolve with increased cerebral blood flow. The Vienna group has suggested a graduated protocol as outlined by Aubry et al. Briefly, an athlete successfully moves through the following exertional steps in 24-hour periods: (1) light aerobic exercise (walking, stationary biking), (2) sport-specific training (ice skating in hockey or running in soccer–typically moderately exertional), and (3) noncontact training drills (usually heavily exertional). Athletes whose previously resolved postconcussion symptoms reappear at any point during the graded return to physical exertion should return to the exertion level at which they were last asymptomatic. Clearly, prior history of concussion, outcome from previous concussion, as well as any suspected deception by the athlete in reporting symptoms may influence return to participation and management directives.
If an athlete has been excluded from competition and severe intracranial pathology has been ruled out, postinjury assessment in the form of neurocognitive evaluation may be used to help determine overall management and return-to-participation issues (even for those athletes who were initially cleared to play). An athlete's cognitive status can be determined by an objective neurocognitive evaluation. Cognitive recovery is achieved when the athlete's performance either returns to baseline levels or, in the absence of return to baseline, is consistent with premorbid estimates of functioning when the test data are compared to normative values (clinicians should utilize test batteries that have readily available athlete-specific norms).
As described above, a preseason or baseline neuropsychological assessment would be helpful in comparing postinjury functioning to “normal” functioning for the injured athlete. Many practitioners prefer to complete serial follow-up using computerized neuropsychological testing to gain insight into the extent and type of cognitive impairment created by the injury. The first test may be performed while the athlete is still symptomatic and then completed once the athlete is asymptomatic to gauge progress and ensure a return to baseline or premorbid expectations of cognitive functioning. Other practitioners prefer to conduct the test when the athlete is asymptomatic both at rest and with heavy noncontact exertion, prior to returning the athlete to any type of contact participation. This may maximize the chance that neuropsychological testing will need to be performed only once at follow-up.
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Athletes who are symptom free both at rest and with physical exertion, are within expected levels on cognitive testing (if available), and therefore are medically cleared may return to full-contact training and then to competition. Again, if any symptoms reemerge with return to contact participation, the athlete should return to noncontact physical activity.
Aubry M et al: Summary of the first international conference on concussion in sport. Clin J Sport Med 2002;12:6.
Bailes JE, Cantu RC: Head injury in athletes. Neurosurgery 2001;48(1):26.
Conclusions & Future Directions
The clinical management of concussion remains a topic of interest and of debate in the medical community. Science and theory of concussion management and return-to-play decisions are evolving rapidly, though there remains much to learn about both the short-and long-term consequences of injury. Clearly, the injury can have serious consequences, especially if not properly assessed, diagnosed, and managed. The realization that there is currently no one formula or guideline that can safely manage an injury as complex and multifaceted as concussion is perhaps the greatest breakthrough in research over the past decade.
As research continues to investigate the biomechanics, pathophysiology, and clinical course of sports-related concussion, management strategies will continue to evolve. Although the future of concussion management remains somewhat uncertain, emerging recommendations support individualized management of the injury through baseline testing, serial assessment of signs, symptoms, and cognitive function, and graduated return to exertion. Certainly, the practitioner must establish an absence of any clinical symptomology (at rest and exertion) as well as normal brain function prior to authorizing a return to play.