Epidemiology

Awareness of sports-related concussion has increased dramatically over the past decade and as public awareness has grown, there has been a corresponding increase in estimates of injuries. The Center for Disease Control recently revised their estimates from approximately 300,000 injuries per year during the 1990s to a current range of 1.6 to 2.3 million per year. Although there are several factors that explain this tenfold increase in injury prevalence, increased awareness at medical and public levels likely is responsible for increased identification and better reporting of injuries. Given this trend and the high probability that concussion still is under-reported, it is likely that increases in concussion rates over the next decade will continue to be seen.

Definitions of concussion

Definitions of traumatic brain injury (concussion) have undergone substantial change over the past 3 decades as understanding of the brain and its response to injury has continued to evolve. In 1966, the Committee on Head Injury Nomenclature of the Congress of Neurological Surgeons 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. For example, the American Academy of Neurology (AAN) defines concussion as:

“Any trauma induced alteration in mental status that may or may not include a loss of consciousness.”

Authors of the AAN definition believed that the Committee on Head Injury Nomenclature definition may have been too limiting, because other brain structures (eg, cortical areas) commonly are associated with concussion, and the injury is not limited to the brainstem. These guidelines also highlighted that concussion may occur with or without loss of consciousness (LOC).

Definitions of concussion

Definitions of traumatic brain injury (concussion) have undergone substantial change over the past 3 decades as understanding of the brain and its response to injury has continued to evolve. In 1966, the Committee on Head Injury Nomenclature of the Congress of Neurological Surgeons 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. For example, the American Academy of Neurology (AAN) defines concussion as:

“Any trauma induced alteration in mental status that may or may not include a loss of consciousness.”

Authors of the AAN definition believed that the Committee on Head Injury Nomenclature definition may have been too limiting, because other brain structures (eg, cortical areas) commonly are associated with concussion, and the injury is not limited to the brainstem. These guidelines also highlighted that concussion may occur with or without loss of consciousness (LOC).

The neurophysiology of concussion

Recent research into the subtle neurometabolic effects of concussion has led to new insights into the pathophysiology of concussion. This area of research was ushered in by Hovda and colleagues at UCLA in the 1990s. Using a rodent model, Hovda and colleagues described metabolic dysfunction that occurred at the intracellular and extracellular levels. They posited that these changes are the result of excitatory amino acid–induced ionic shifts with increased Na/K-ATPase activation and resultant hyperglycolysis. Thus, there is a high-energy demand within the brain shortly after concussive injury. Hovda and colleagues demonstrated further that hyperglycolysis is accompanied by decreased cerebral blood flow resulting in widespread cerebral neurovascular constriction. The resulting “metabolic mismatch” between energy supply and demand within the brain is postulated as leading to cellular vulnerability during the days to weeks after injury.

Given that concussion occurs on a physiologic rather than a structural level, traditional neurodiagnostic techniques (eg, CT scan, MRI, and neurologic examination) almost invariably are normal after concussive insult. It should be stressed, however, that these techniques are valuable in ruling out more serious pathology (eg, cerebral hematoma or skull fracture) that also may occur with head trauma.

Hovda and colleagues’ initial research was groundbreaking and led to an increased focus on the pathophysiology of this injury in human subjects. More recent research has examined the potential usefulness of functional MRI (fMRI) as a viable tool for the assessment of neural processes after concussion. The technology is based on the measurement of specific correlates of brain activation, such as cerebral blood flow and oxygenation. fMRI also has promoted the evaluation of specific neuropsychologic test paradigms through which cerebral blood flow changes can be linked to specific tests that measure memory and other cognitive processes. In addition, fMRI involves no exposure to radiation and can be used safely in children. Furthermore, repeat evaluations can be undertaken with minimal risk. This promotes the assessment of changes in neural substrata that may occur with mild concussion, permitting tracking of injured athletes throughout the recovery process. Potentially, one of the most important uses of fMRI scanning is the ability to provide validity data regarding the sensitivity and specificity of neuropsychologic testing for detection of subtle changes in brain function.

Although a promising tool, fMRI has yet to be implemented widely in clinical settings. Few laboratories actively are investigating the use of fMRI in sports-related head injury at present, although this likely will change within the next few years. Notably, Johnston and colleagues at McGill University in Montreal have developed an fMRI protocol that allows the assessment of several components of working memory. In the United States, my laboratory at the University of Pittsburgh represents one of only a handful of research programs structured to collect neuropsychologic and fMRI data in athletes. This multiyear, prospective study relies on the prior baseline neuropsychologic testing (Immediate Post-Concussion Assessment and Cognitive Testing [ImPACT]) of a large cohort (more than 3000) of male and female high school and college athletes. In the event of injury, the athletes undergo repeat testing within 24 to 72 hours and undergo fMRI scanning. An additional fMRI scan and ImPACT testing “in scanner” and “out of scanner” are completed as patients recover, allowing tracking of the correlation between fMRI and neuropsychologic testing. To date, more than 200 athletes have been evaluated within 1 week of injury and again after clinical recovery, and the group with the highest degree of abnormalities on fMRI has demonstrated a significantly longer time to clinical recovery (ie, symptom-free with normal neuropsychologic test performance).

On-field and sideline management of concussion

A concussion may occur without direct trauma to the head, and concussed athletes are rendered unconscious infrequently. In addition, athletes may be unaware that they are injured and may not show any obvious immediate signs or symptoms of injury, such as motor incoordination, gross confusion, or amnesia. To complicate the situation further, athletes at all levels of competition may minimize or hide symptoms in an attempt to prevent their removal from the game, creating the potential for re-injury, second concussion, and exacerbation of the original injury.

Initial sideline signs and symptoms of evaluation and return to play

Table 1 provides a summary of common on-field signs and symptoms of concussion. Sideline presentation may vary widely from athlete to athlete, depending on the biomechanical forces involved, athletes’ prior history of injury, and many other factors. In reviewing the common signs and symptoms of concussion, it is imperative to understand that an athlete may have only a few signs or symptoms of injury or a constellation of symptomatology. A thorough assessment of all common symptoms associated with concussion should be conducted for concussed athletes.

With regard to the frequency of postconcussion signs and symptoms, headache is the symptom reported most commonly, occurring in approximately 70% of concussed athletes. Although it is true that musculoskeletal headaches and other pre-existing headache syndromes may complicate the assessment of postconcussion headache, any presentation of headache after a blow to the head or body should be managed conservatively. Most frequently, a concussion headache is described as a sensation of pressure in the skull that most often is localized to the frontotemporal regions of the head. In some athletes (particularly migraineurs), a headache may be unilateral and often is described as throbbing or pulsating. A headache may not develop immediately after injury and may develop over the minutes, or even hours, after injury. It is not unusual for athletes initially to be pain-free, then wake the morning after with headache. Therefore, it is essential to question potentially concussed athletes regarding the development of symptoms beyond the first few minutes or hours after injury. It also is important to prompt family members to observe injured athletes for evolving signs of injury. Another common characteristic of postconcussion headache is that this type of headache often is made worse during physical and cognitive exertion. Athletes frequently report an exacerbation of symptoms after even minor increases in physical activity and after a return to school or activity. Although headache after a concussion does not necessarily constitute a medical emergency, a severe or progressively severe headache, particularly when accompanied by vomiting or rapidly declining mental status, may signal a life-threatening situation, such as a hematoma or intracranial bleed. This should prompt immediate transport to hospital and a CT scan of the brain.

Although headache is the most common symptom of concussion, concussion is possible without headache and other signs or symptoms of injury should be assessed and detailed carefully. For example, athletes often experience blurred vision, changes in peripheral vision, or other visual disturbance. Another common and disabling symptom is fatigue or sluggishness. Fatigue is prominent in concussed athletes especially during the days after injury and may be nearly as frequent as headache. In addition to these symptoms, cognitive or mental status changes commonly are seen immediately after injury. Athletes who have any degree of mental status change should be managed conservatively and a thorough discussion of these issues is warranted.

Initial evaluation of concussion and markers of injury

Appropriate care of a concussed athlete should begin with the initial on-field evaluation of the athlete ( Box 1 ). As with any serious injury, the first priority is evaluating an athlete’s level of consciousness and airway, breathing, and circulation. The attending medical staff must 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 medical staff, with each team member having a role that is defined in advance.

On ruling out more severe injury (eg, traumatic neck injury or acute neurosurgical emergency), the evaluation should continue with assessment of the concussion mental status of the injured athlete. First, a clinician should establish the presence of any LOC. By definition, LOC represents a state of brief coma in which an athlete is unresponsive to external stimuli and the eyes typically are closed. LOC is uncommon and occurs in less than 10% of concussive injuries. Furthermore, athletes who do experience LOC typically are unresponsive for only a brief period (usually seconds). Athletes who have documented LOC should be managed conservatively and return to play is contraindicated, particularly in younger athletes.

Although LOC is uncommon, confusion and amnesia are common sequelae of injury. Confusion (ie, disorientation), by definition, represents impaired awareness and orientation to surroundings and often manifests in athletes who have descriptions of appearing stunned, dazed, or glassy-eyed on the sideline. Confusion frequently presents as difficulties in appropriate play calling, answering questions slowly or inappropriately, or athletes repeating themselves during evaluation (perseveration). Teammates often are the first to recognize a confused athlete during difficulties with running plays or completing assignments. To assess the presence of confusion properly, simple orientation questions can be asked (eg, name, current stadium, city, opposing team, and current month and day).

A careful evaluation of amnesia is of particular importance in the diagnosis and management of concussed athletes. Amnesia may be associated with loss of memory for events preceding (retrograde) or after injury (posttraumatic). Retrograde amnesia is defined as the inability to recall events occurring during the period immediately preceding trauma. To assess on-field retrograde amnesia properly, athletes may be asked questions pertaining to details occurring just before the trauma that caused the concussion. Simple questions posed to an athlete, such as recollection of details of the injury, are a good starting point ( Box 2 ). From the point of injury, an evaluator should ask probing questions in an attempt to ascertain the last formed memory before injury. The length of retrograde amnesia typically shrinks over time but an athlete often never regains all of the lost information.

Posttraumatic amnesia typically is represented by the length of time between trauma (eg, helmet-to-helmet contact) and the point at which an individual regains normal continuous memory functioning (eg, standing on the sideline after the hit). As outlined in Table 1 , on-field posttraumatic amnesia may be assessed through immediate and delayed (eg, 0-, 5-, and 15-minute) memory for three words (eg, girl, dog, and green). In addition, simply asking an athlete to recall specific events that occurred immediately after a trauma is useful (eg, memory of returning to sideline, memory for subsequent plays, and memory of later parts of contest). Any failure to recall these events properly is indicative of posttraumatic amnesia. The presence of posttraumatic amnesia is highly predictive of postinjury neurocognitive and symptom deficit.

The return-to-play decision-making process

Return-to-Play Guidelines

During the past 30 years, more than 20 concussion management guidelines have been published with the intent of providing guidance and direction for sports medicine practitioners in making complex return-to-play decisions. The authors of each of these guidelines provided an accompanying grading scale designed to reflect and characterize the severity of an injury. Although these guidelines no doubt have resulted in improved care of athletes, these multiple directives have created significant confusion and sparked almost continuous debate. A historical review of all past and current concussion guidelines is beyond the scope of this article; however, brief review is provided.

Cantu originally proposed a grading scale and management guidelines based on clinical experience. Cantu was careful to emphasize, however, that these guidelines were intended to supplement rather than replace clinical judgment. The original Cantu guidelines allowed return to play the day of injury if an athlete were symptom-free at rest and after physical exertion. For athletes who experienced any LOC (eg, grade 3 concussion), a restriction of contact for 1 month was recommended. Athletes who suffered a grade 2 concussion were allowed to return to play in 2 weeks, if asymptomatic for a period of 7 days.

The Colorado guidelines were published in 1991 after the death of a high school athlete from second impact syndrome and were drafted under the auspices of the Colorado Medical Society. These guidelines allowed for same-day return to play if symptoms cleared within 20 minutes of injury. For more severe injury (grade 3 concussion), these guidelines recommended immediate transport to a hospital for further evaluation. These guidelines later were revised under the sponsorship of the AAN. The AAN guidelines allowed return to competition the same day of injury if an athlete’s signs and symptoms cleared within 15 minutes of injury. Grade 2 concussions were managed in a manner similar to that of the Colorado guidelines, with return to competition within 1 week, if asymptomatic.

More recently, Cantu has amended his guidelines to emphasize the duration of posttraumatic symptoms in grading the severity of the concussion and making return-to-play decisions. Grade 1 concussion was redefined by an absence of LOC and postconcussion signs or symptoms lasting fewer than 30 minutes. Same-day return to competition was allowed only if athletes were completely asymptomatic after the injury.

Concussion management guidelines reached their zenith of popularity during the 1980s and 1990s; in the late 1990s, sports medicine practitioners and organizations began to question the empiric basis of these guidelines. This trend prompted the American Orthopaedic Society for Sports Medicine (AOSSM) to sponsor a workshop with the purpose of re-evaluating guidelines and establishing practical alternatives. The AOSSM guidelines were the first to emphasize more individualized management of injury rather than applying general standards and protocols.

A particularly important development took place in 2002 under the auspices of the Fédération Internationale de Football Association in conjunction with the International Olympic Committee and the International Ice Hockey Federation. The organizers of this meeting assembled a group of physicians, neuropsychologists, and sports administrators in Vienna, Austria, to continue to explore methods of reducing morbidity secondary to sports-related concussion. The deliberations that took place during this meeting led to the publication of a document outlining recommendations for diagnosis and management of concussion in sports. One of the most important conclusions of this meeting was that none of the previously published concussion management guidelines was adequate to assure proper management of every concussion. Although a complete discussion of these recommendations is beyond the scope of this article, the group emphasized the implementation of postinjury neuropsychologic testing as a cornerstone of proper postinjury management and return-to-play decision making. A second meeting of this group took place in Prague in 2004, and they continued to promote a return-to-play protocol that was based on assessment of signs and symptoms of injury. This statement also continued to avoid the numeric grading system but did suggest the possible classification of concussions as being simple or complex in nature. Although this classification system has yet to be validated, simple concussions were defined as concussions that were followed by improvement within 10 days of injury and not accompanied by convulsions or other obvious signs of brain injury. In addition, athletes who had a past history of concussion automatically were classified as having complex injuries. In contrast, complex concussions were described as taking more than 10 days to recover, being accompanied by convulsions or occurring within the context of a history of multiple injuries.

To date, there has only one study that has investigated the validity of the simple- complex dichotomy. The investigation by Iverson used cognitive function scores in four categories (verbal memory, visual memory, reaction time, and processing speed) and symptoms provided by the ImPACT test battery to investigate the clinical usefulness of the new classification system. Iverson found that within 72 hours of injury, high school athletes who had complex concussions performed worse than baseline on three of four cognitive composite scores (visual memory, processing speed, and reaction time) than those who had simple concussions. Furthermore, the study found that patients who had complex concussions were more likely to report a total symptom score of 40 or greater on the postconcussion scale (a self-report symptom inventory) ( Table 2 ). Iverson suggested that low composite scores in two or three of the aforementioned cognitive tests may be indicative of a complex concussion or slower recovery.

Table 2

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