Concussion and Brain Injury

Among the wide range of injuries that occur in the sports arena, traumatic brain injury (TBI) is a health problem that has garnered increasing public awareness during recent years. This heightened interest has been largely driven by intense media exposure, as well as the retirement of prominent professional athletes with cognitive and behavioral dysfunction purportedly representing lingering sequelae of brain injury. Player safety concerns have become an area of special focus for professional leagues, such as the National Football League (NFL) and National Hockey League (NHL), as well as organizations such as the International Olympic Committee and the National Collegiate Athletic Association (NCAA), with a resulting impact on collegiate, high school, and recreational sports.

Key to a discussion of sports brain injury is an understanding of the terminology applied to the topic. TBI is an umbrella term that encompasses a range of clinical labels that vary based on severity. Mild traumatic brain injury (mTBI) involves an impact to or acceleration/deceleration of the head resulting in at least a temporary alteration in consciousness or loss of consciousness (LOC) of less than 20 minutes, a Glasgow Coma Scale score of 13 to 15, and no findings on neuroimaging. mTBI is alternately referred to as mild head injury, minor head injury, and concussion . The vast majority of brain injuries sustained by athletes are mild events that would be considered concussions ; moderate, severe, and penetrating traumatic brain injuries are less common. For practical purposes, in this chapter mTBI, mild head injury, and concussion are considered synonymous, and the term concussion is used throughout this chapter.

The intent of this chapter is to provide a resource for the clinician on the diagnosis and management of sports concussion. A brief historical context for the issue of sports concussion, relevant definitions, and epidemiology are presented; the clinical presentations that can occur after a concussive blow are also reviewed, and a clear concussion management and return-to-play (RTP) decision-making process is given.

Background

Concussion is not a modern phenomenon. Numerous references to cranial injury can be found in ancient medical reports and mythological literature by such figures as Hippocrates and Homer. The recognition of concussion as a separate entity from more severe head injuries was made as far back as the first century AD by Rhazes, an Arabian physician who described concussion as an abnormal physiologic state lacking gross traumatic brain lesions. Modern-day literature, however, has predominately focused on moderate to severe brain injuries, with relatively little attention given to mild brain injuries, whether sports-related or not.

The topic of concussion began to be taken seriously by medical science in the 1980s, when clinical and epidemiologic studies received media attention in a Wall Street Journal article, “Silent Epidemic: Head Injuries Often Difficult to Diagnose, Get Rising Attention.” The growing consensus that mild head injury was in fact not innocuous was based on the identification of neuropsychological deficits in problem solving, attention, and memory lasting up to 3 months after a trauma was sustained. In addition, primate studies documented histologic evidence of axonal shear and strain during experimentally induced acceleration-deceleration mild head injury.

Because the study of concussion does not lend itself to randomized controlled trials, significant strides were made when Barth and colleagues turned to the collegiate sports arena to address the problem of finding adequate control subjects and accounting for the effects of premorbid functioning in the study of concussion. The sporting venue provided a large number of potential participants who were likely to experience mild acceleration-deceleration head trauma. Data from 10 universities showed that athletes who sustained a concussion had neurocognitive deficits at 24 hours and 5 days after concussion but recovered by the 10th day, a recovery curve that has been replicated by other studies. This seminal study set the methodologic standard for baseline and serial neuropsychological testing as the best way to determine the effect of concussion, and this approach of using individual athletes as their own controls and as a model for understanding brain injury in general was termed the Sports as a Laboratory Assessment Model (SLAM). The SLAM approach helped establish concussion as a sports medicine issue with broader implications for mTBI in other areas (e.g., motor vehicle accidents).

Definition of Concussion

As noted at the outset of this chapter, a widely varying set of terms and defining parameters exist for the topic of sport related concussion (SRC), and this lack of clarity and consistency has hampered the study of concussion to a significant degree. The two most common definitions used in sports concussion research are from the American Academy of Neurology (AAN) Practice Parameters and the Concussion in Sports Group (CISG; commonly referred to as the Vienna, Prague, Zurich, and Berlin Conferences). In 1997 the AAN defined concussion as an altered mental state that may or may not include LOC. Four years later, the CISG group proposed that concussion is a “complex pathophysiologic process affecting the brain, induced by traumatic biomechanical forces,” and included common features of concussion that incorporate clinical, pathologic, and biomechanical constructs to supplement the definition. This definition was updated in 2017 to state “Sport related concussion is a traumatic brain injury induced by biomechanical forces,” with common features including “1. SRC may be caused either by a direct blow to the head, face, neck, or elsewhere on the body with an ‘impulsive’ force transmitted to the head; 2. SRC typically results in the rapid onset of short-lived impairment of neurologic function that resolves spontaneously. However, in some cases, signs and symptoms evolve over a number of minutes to hours; 3. SRC may result in neuropathologic changes, but the acute clinical signs and symptoms largely reflect a functional disturbance rather than a structural injury and, as such, no abnormality is seen on standard structural neuroimaging studies; 4. SRC results in a range of clinical signs and symptoms that may not involve loss of consciousness. Resolution of the clinical and cognitive features typically follows a sequential course. However, in some cases symptoms may be prolonged.”

This definition largely reaffirms that established by the prior Consensus Conferences in Zurich and reflects the current trend toward emphasizing the biomechanical force, time course of symptoms, and the functional nature of the injury, as opposed to the structural emphasis used in more severe forms of TBI.

Epidemiology

The Centers for Disease Control and Prevention estimates that approximately 1.6 to 3.0 million sports-related concussions among high school students will be reported each year in the United States, and during the past decade, emergency department visits for sports concussions among children and adolescents increased by 60%. Such estimates likely underestimate the actual occurrence, given that many leagues lack the medical oversight to identify concussions. Recent studies suggest that 8.9% of all high school athletic injuries were concussions, and estimates for collegiate sports range from 5% to 18%, with more than 52,000 concussions reported between the academic years beginning in 2009–2013. The incidence of sports concussion is expected to continue to rise in part because of the increase in sports participation by both male and female athletes at the collegiate and high school levels, but also because of increased knowledge, detection, and reporting of the injury, including the adoption of sports injury surveillance systems.

Pathophysiology

A full discussion of the pathophysiology underlying concussion is beyond the scope of this chapter. The interested reader is referred to the work of Giza and Hovda for a thorough understanding of the topic. In brief, concussion occurs as a result of linear and rotational accelerations and decelerations to the brain and is thought to cause a multifactorial neurometabolic cascade of physiologic changes. This process begins with cell body expulsion of sodium and potassium into the intracellular space and an influx of calcium, as well as mild edema and a resultant decrease in cerebral blood flow in the setting of initial hyperglycolysis. As glucose is consumed and blood flow is limited, a state of hypoglycolysis ensues, which slows the neurochemical return to homeostasis. This dysautoregulation in addition to axonal injury, impaired neurotransmission, and protease activation leading to cell death explain how clinical signs of brain dysfunction can be observed in the absence of readily detectable physical damage. This cascade begins within minutes of the injury and can be active for several weeks.

Clinical Presentation

When the question is raised as to why concussion in sports represents an important problem that must be identified, the answer lies in the known consequences demonstrated by concussed athletes, who may present with acute, catastrophic, lingering, or long-term sequelae.

Although it is controversial and rare, a potentially catastrophic outcome from concussion termed second impact syndrome (SIS) is sometimes manifested. This most severe consequence of concussion was part of the initial impetus for a formalized approach to concussion management and RTP criteria. First described in detail in 1984, the syndrome is said to occur when a second concussion is sustained before the symptoms of the first have fully resolved. The second impact may appear minor and may not occur on the same day. The athlete may not initially appear injured but may collapse and lose consciousness shortly after the event, with respiratory failure, coma, and even death possibly ensuing. Underlying the SIS phenomena is the notion that the brain appears to have a decreased threshold for sustaining a concussion of any severity with each subsequent trauma. The pathophysiology behind SIS is not fully understood, but it has been suggested that the subclinical edema and increased intracranial pressure from the first concussive impact make the brain successively more vulnerable to the second impact through autodysregulation and subsequent vascular engorgement. This condition manifests as malignant cerebral edema and herniation of the uncus or the cerebellar tonsils through the foramen magnum, resulting in brainstem failure. However, recent systematic reviews of the literature regarding this syndrome found a dearth of high quality literature, unclear actual mortality rates (though nearly all studies said the rate was “high”), and “severe lack of definitive structure” as to what signs and symptoms are associated with it, leading the authors to conclude “SIS is not a credible, literature supported diagnosis.”

Persistent symptoms (also known as postconcussive syndrome or PCS) may remain after a sports concussion is sustained and reflect a failure of normal clinical recovery. Most concussed athletes demonstrate gradual, spontaneous recovery, generally within 2 to 10 days after injury, consistent with laboratory animal studies showing short-lived effects of concussion, and with meta-analytic studies demonstrating no evidence of impairment beyond 3 months. However, the fact that some people experience persistent sequelae has been recognized for quite some time. For example, at 3-month follow-up, 34% of an mTBI clinical (nonsports) sample had not yet returned to work, and 24% demonstrated measurable neurocognitive deficits. The Fourth International Conference of Concussion in Sport defined prolonged recovery as symptom persistence greater than 10 to 14 days from injury for adults and greater than 4 weeks in children; however, the definitions used in the literature vary from 10 days to more than 2 months. Persistent symptoms can include neurologic symptoms such as headache, dizziness, and nausea; cognitive deficits, such as impaired attention, slowed mental processing, and memory dysfunction; and emotional or psychological disruption, including depression or irritability. It is important to note that the presence of one or more of these symptoms after a concussion is sustained in an athlete is not diagnostic of delayed recovery, since such symptoms are extremely common in a host of other conditions. For example, PCS type symptomatology has been demonstrated in 81% of subjects in a chronic pain sample with no history of concussion. As such, the clinician may find the identification of persistent symptoms difficult. One challenge is that the athlete may present with vague, subjective symptoms that are nonspecific. Issues of effort and secondary gain may also be a contributing factor in some cases. Furthermore, the differential diagnosis often includes mood and anxiety disorders, as well as sleep disruption, which can lead to or mimic PCS symptoms. Neuropsychological assessment can be quite useful in this situation, because objective evaluation can help parse out the factors contributing to the athlete's atypical presentation. Structural imaging (MRI and CT) are of limited value in evaluation of these patients and advanced techniques such as fMRI, diffusion tensor imaging, MR spectroscopy, and quantitative EEG have unclear clinical significance.

In addition to the clinical presentations of SIS and PCS, a third potential clinical presentation known as chronic traumatic encephalopathy (CTE) can occur after multiple concussions. This outcome appears to be dose-related long-term response of repeated concussions and subconcussive blows and has been studied in groups of retired football, rugby, and boxing athletes. The combination of repetitive sports head injury–related damage with that of age-related neuronal loss may result in the development of clinical signs of CTE, often appearing years after the end of the athlete's career. Though the diagnosis of CTE is based on neuropathologic evidence collected postmortem, its clinical course can be characterized by long-term deficits in executive functioning, processing speed, verbal learning, and visual memory; motor impairments, including impaired coordination, spasticity, and parkinsonism; as well as behavioral problems such as emotional dysregulation and disinhibition. Referred to as “dementia pugilistica” in early literature, CTE in its advanced stage can be clinically indistinguishable from other advanced dementias. Neuropathologically, CTE is a progressive tauopathy with gliosis and neurofibrillary tangles, as well as common gross elements of reduced brain weight, enlarged ventricles, volume loss in the corpus callosum, cavum septum pellucidum, and scarring and neuronal loss of the cerebellar tonsils. The pathology of CTE has been most frequently demonstrated in the brains of professional athletes and can be widespread throughout the brain given the nonfocal nature of repeated head trauma. Similarly, elevated tau protein levels have been detected in the plasma of both injured and noninjured contact athletes relative to non-athlete controls with increased tau levels corresponding to delayed return to sport. Although long-term deficits in the form of persistent symptoms can manifest after a single concussive blow, it is generally assumed that a concussed athlete can expect a favorable prognosis if the injury is safely managed. The risk of outcomes such as SIS, persistent symptoms, and CTE can be significantly reduced with proper concussion identification, examination, and intervention.

Examination

The goal of sports concussion examination is to identify the concussion, assess the injury, determine its effects, and devise appropriate interventions. The traditional approach to this task involved simply gauging the signs and symptoms of the concussion and their resolution over time. Many different classification schemes for concussion exist, and definitions and criteria continue to evolve. Historically, the two most widely used systems for grading concussion were those proposed by the AAN in 1997 and Cantu in 2001. These systems used three grades to represent mild, moderate, and severe concussion based on the clinical presentation of the athlete and placed considerable emphasis on LOC (AAN) or posttraumatic amnesia (PTA; Cantu) as severity indicators. Despite early TBI literature showing that coma duration is an important predictor of outcome, more recent studies have found that the relationship between LOC and injury outcome in the realm of mTBI and sports concussion is less certain. Concussion grading systems are now considered obsolete, and an individualized approach to concussion diagnosis and management is favored, consistent with the CISG guidelines.

Although monitoring subjective symptoms is an important aspect of concussion management, it cannot be the sole means of gauging effect and recovery. It is now understood that fewer than half of concussed athletes spontaneously report their symptoms, citing doubt that the injury was severe, not wanting to leave the game, or general lack of awareness about concussion as reasons for not reporting. For these and other reasons, the modern model for concussion examination, outlined by the CISG Conferences, emphasizes an individualized approach that incorporates neurocognitive evaluation. Several computer-administered measures (outlined later) are validated for the assessment of concussion sequelae. The standard practice has evolved to include such standardized tools in both preseason and postinjury assessment. Current guidelines recommend that athletes not resume a gradual progression of activity until their concussion symptoms have remitted. Thus neurocognitive testing has become a valuable tool in identifying subtle cognitive symptoms and their resolution.

Baseline (Preseason) Assessment

Baseline neuropsychological assessments have been advocated by some authors and increased in popularity with the development of computerized tests in the 1990s. Advocates of preseason testing point out the results of any evaluation vary based on many factors other than the actual injury, including intelligence and cultural background, learning disabilities, and previous concussion history. This situation applies to neurologic findings as well; for example, up to 20% of athletes normally experience a headache while in the midst of competition, and approximately 3% of the healthy population exhibit pupillary asymmetry. Erroneous conclusions about the cognitive and neurologic state of an athlete may be drawn without an awareness of these baseline characteristics. However, other authors have shown these tests may have poor test-retest reliability, vary between group and individual administration or alternate forms, suffer from measurement errors, and may not offer an improvement over postinjury testing alone (when compared with normative data as opposed to individualized preseason baseline). Routine mandatory preseason baseline neurocognitive testing is not recommended by either the Berlin conference or the American Medical Society of Sports Medicine guidelines.

Neurocognitive baselines may be obtained for athletes with the use of computerized methods in an individual or group setting with a trained examiner. Several tools are available for the specific purpose of assessing concussion severity and resolution. These tools include the Automated Neuropsychological Assessment Metrics ; the Immediate Post-concussion Assessment and Cognitive Testing (ImPACT Applications Inc., Pittsburgh, PA) ; the Concussion Resolution Index (HeadMinder Inc., New York, NY) ; and the Computerized Cognitive Assessment Tool (Axon Sports [formerly CogSport], Wausau, WI). The Automated Neuropsychological Assessment Metrics measures processing speed, resistance to interference, and working memory. The Immediate Post-concussion Assessment and Cognitive Testing tool was developed specifically for athletes, and assesses reaction time and a range of attentional and memory skills, accompanied by a self-report postconcussion scale. The Concussion Resolution Index is a web-based set of cognitive tasks that measure simple and complex reaction time, attention, memory, and cognitive processing speed. Axon is also an Internet-based system and includes eight tasks designed to sample a range of cognitive functions.

Sideline Assessment

The first step in the assessment of concussion is to recognize that a concussion may have occurred. It is important to remember that signs and symptoms may be delayed or rapidly changing in the acute phase, and injured athletes may exhibit no obvious indications that they are concussed. Therefore sideline assessment is warranted for any athlete who has received a significant blow to the head or an athlete who does not appear to “be him or herself” in response to a lesser degree of contact. This assessment involves evaluation of the athlete both on the field, or more commonly on the sideline, as well as in a controlled environment such as the locker room, and usually is conducted by a physician or a certified athletic trainer with expertise in concussion evaluation and management.

An obvious goal of the sideline assessment is to determine if the athlete has signs that signal the presence of severe intracranial or spinal cord injury and whether transport to a medical facility is required. Once this determination is made, any individual should be removed from the field for further assessment. Classic signs such as LOC, retrograde amnesia, or frank neurologic deficit may be helpful but are absent in a minority of injured athletes.

In general, the sideline evaluation should assess for signs of confusion, loss of balance, headache, dizziness, and slowed responding, in addition to informal cranial nerve, motor, sensory, and reflex testing and, importantly, cognitive screening. For athletes with no obvious acute symptoms, physical maneuvers such as push-ups or jumping jacks can help determine whether concussive signs or symptoms develop with exertion and resultant increased intracranial pressure. Sideline assessment should also incorporate a mental status examination that targets orientation, concentration, and memory. Notably, standard orientation questions (time, place, person) have been shown to be unreliable following a sports injury relative to memory assessment. Concentration may be gauged by tasks such as repeating strings of three to five digits both forward and backward, serial subtraction of numbers, or repeating a well-known verbal sequence such as months of the year or days of the week backward. Memory can be informally and qualitatively assessed by recall of three items at different intervals after the injury or repeating assignments of a number of previous plays.

Although these informal methods of sideline assessment are helpful, a standardized approach is preferable. A number of standardized methods for determining the severity of a concussion and the initial symptoms have been developed for use in the sideline evaluation of athletes. The Concussion Recognition Tool 5 (CRT5) was developed by the CISG as a pocket guide for nonmedically trained personnel to identify SRC as well as guide removal from play decisions. The Standardized Assessment of Concussion (SAC) is a 5-minute measure administered by a trained physician or athletic trainer and includes five orientation questions, a five-word learning test, reciting digits backward, reciting the months of the year in reverse, and delayed word recall. The SAC provides a 30-point composite score to gauge neurocognitive function and also includes a standard neurologic screening, exertional maneuvers, and means of assessing LOC and PTA. Normative data for comparison are also available. The SAC is available in paper form and a pocket-card format, and has been adapted for use with smartphone technology. The Balance Error Scoring System is an objective measure of postural stability for use on the sideline. The 5-minute procedure requires the injured athlete to maintain three stances (double, single, and tandem) for 20 seconds with the eyes closed and both hands on his or her hips. Scoring is based on six types of errors over six test trials. The Standardized Concussion Assessment Tool (SCAT5) is another standardized tool that incorporates elements of the aforementioned SAC and a graded rating of common physical and cognitive signs and symptoms. Recently revised to the fifth version, the test battery takes 10 minutes to administer and updates the widely used SCAT3. This test has also been developed into a pediatric version (Child SCAT5) for use in children age 5 to 12. The Berlin Conference recommended use of the SCAT5 and Child SCAT5 for sideline concussion assessment. The tool is easily accessible online and may be freely copied for distribution to individuals, teams, groups, and organizations.

After a sideline evaluation, any athlete considered to have sustained a concussion should be removed from the sporting environment and undergo a multimodal medical evaluation with a more detailed neuropsychological assessment. The concussed player should not be allowed to return to play (RTP) the day of injury. Serial exams should be conducted over the first few hours after injury to monitor for signs of deterioration. Finally, to provide an objective basis for detecting the effects of the concussion, the athlete should undergo postinjury neurocognitive assessment. This brief repeat evaluation can occur within 24 to 48 hours after the suspected concussion if the athlete appears to be symptom free. This aspect of concussion management may provide increased sensitivity for identifying cognitive impairment resulting from concussion when physical symptoms are limited or resolved. However, conducting the brief repeat evaluation 7 days after the injury has been found to provide more unique information regarding impairment than routine assessment conducted relatively close in time to the sideline assessment.

Comprehensive Assessment

In the case of a single uncomplicated concussion or subconcussive event, it is generally anticipated that the athlete will experience full resolution of symptoms within the 2- to 14-day natural recovery curve. In cases with an atypical presentation, a more comprehensive evaluation may be necessary. Athletes with preexisting or comorbid conditions (e.g., learning or attention disorders, depression, or substance abuse), those who report or demonstrate a slower than expected recovery, or those who have sustained multiple previous concussions should be considered for expanded assessment. In these situations, a referral for comprehensive outpatient neuropsychological evaluation is indicated, which includes a clinical interview, record review, and objective testing of aptitude and cognitive functioning, and provides individualized recommendations for the athlete and relevant treatment providers. In addition, further medical assessment may be warranted for atypical concussion cases (e.g., neuroophthalmology).

Imaging

Acute evaluation of concussion may incorporate at least one form of brain imaging. Computed tomography is an appropriate choice to rule out the presence of intracranial hemorrhage and skull fracture, and is the imaging option of choice for concussion evaluation in most emergency departments. Magnetic resonance imaging (MRI) with an angiogram can be obtained if carotid dissection or stroke is suspected, and MRI studies may also identify a diffuse injury such as axonal shearing.

It is important to emphasize that most concussions are unlikely to produce observable signs upon testing with these traditional radiologic techniques. Advanced diagnostics such as functional MRI, diffusion tensor imaging, MR spectroscopy, fluid biomarkers, and genetic testing are, at present, only practical and widely available in the research setting and are of uncertain clinical utility. Although structural neuroimaging continues to rule out the presence of serious pathology that would be beyond that of a mild concussive injury, brain imaging is less relevant in the context of typical concussion management.

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