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Laskowitz D, Grant G, editors. Translational Research in Traumatic Brain Injury. Boca Raton (FL): CRC Press/Taylor and Francis Group; 2016.

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Translational Research in Traumatic Brain Injury.

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Chapter 2Sport-Related Traumatic Brain Injury

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INTRODUCTION

Sport-related traumatic brain injuries (TBIs) have received significant media coverage in recent years, in part due to an increased body of scientific literature and growing concern surrounding their long-term effects. The major focus is centered on concussions, which are believed to account for 80% of TBI-related visits to emergency departments.1 With the development and application of advanced concussion assessment tools, including neuropsychological testing, neuroimaging, and balance and gait assessments, there is a rising tide of data that is driving changes in clinical practices and management of concussed patients. In this chapter, we explore the major features of sport-related TBI, with a special emphasis on concussions. This overview will cover definitions of the injury, pathophysiology, biomechanics, epidemiology, clinical management, and future directions in research. The details of each of these sections are taken from the most current and impactful literature in the field; this includes both primary research as well as expert opinion and consensus and position statements of major societies and organizations imparting meaningful guidance to clinicians and healthcare professionals. These include the American Academy of Neurology,2 American Academy of Pediatrics,3 American Medical Society for Sports Medicine,4 National Athletic Trainers’ Association,5 and the 4th International Conference on Concussion in Sport.6 Furthermore, we present commentary on this literature that is meant to highlight the difficulties of translational research in the field and project the trajectory of the sport-related concussion field in the coming years.

DEFINITIONS AND NOMENCLATURE

To answer the question “what is a concussion?” we must first discuss the recent history of the term and how it has changed over time.* Although medical descriptions of concussion, or commotio cerebri, date back to the Corpus Hippocraticum, there has been considerable difficulty in establishing a universal definition of concussion for decades. Several classification and grading schemes811 were used with no consensus as to which classification scheme was most appropriate or useful. This created a problem of inconsistency of definition in the field of concussion research; however, many of these definitions have common elements. Nearly all grading/classification systems use the presence and duration of loss of consciousness and post-traumatic amnesia as major criteria for diagnosis and stratification into varying levels of severity. The ability to predict prognosis following concussion based on post-traumatic amnesia and loss of consciousness has proven difficult and the use of such classification systems has significantly dropped. In sports injury research, a widely used definition has been put forth by the International Conference on Concussion in Sport (ICCS). In the most recent 2012 consensus statement, the authors defined concussion as “a complex pathophysiological process affecting the brain, induced by biomechanical forces.”6 While the description goes on to describe concussion as involving neuropathological changes, the authors emphasize that the acute clinical symptoms reflect a functional disturbance rather than a structural injury. A striking feature of the ICCS definition is the lack of a specific description of a clinical presentation; this was intentional as the nature of concussive injury varies widely, as will be discussed in the succeeding section.

Of note, concussion has often been referred to as a “mild TBI” in a large volume of research literature. Although some authors draw distinctions between the terms,4 they are often considered synonymous. The term “concussion” has gained favor over mild TBI because of the concern that “mild” TBI may give the impression that the injury does not have serious sequelae.6 Contrariwise, the authors of one study examining the connotations of the term “concussion” as applied to pediatric patients suggests that clinicians often use “concussion” rather than “mild TBI” to convey to parents that their child’s injury is transient and without long-term sequelae.12 Whichever term is used, it is generally accepted that concussion is a serious injury that requires early recognition and proper management.

SIGNS AND SYMPTOMS

The common signs and symptoms of concussion are listed in Table 2.1 and generally fall into four domains: physical, cognitive, emotional, and sleep related.1320 The specific set of symptoms experienced by a given patient can vary, but generally headache, dizziness, feeling “slowed down,” and fatigue are the most commonly reported symptoms.16,19,21,22 The presence of any of these symptoms following a blow to the head (or body in the case of a whiplash mechanism of injury) is sufficient to diagnose concussion. A meta-analysis of postinjury follow-up studies of concussed athletes showed that neurocognitive performance and balance decrease, and self-reported symptoms increase on initial evaluation.23 Caution is advised, however, against using any one measure to diagnose concussion. A multimodal approach assessing balance, neurocognitive function, and self-reported symptoms, with comparisons to baseline measures, is the preferred method for evaluating suspected concussion cases. We will examine several assessment instruments later in this chapter.

TABLE 2.1

TABLE 2.1

Common Signs and Symptoms of Concussion

Concussion is a subset of TBI distinct from moderate and severe forms in that it typically does not result in an extended period of loss of consciousness. Clinicians often use the Glasgow Coma Scale (GCS) to distinguish between mild, moderate, and severe TBI, with lower scores indicating a deeper loss of consciousness.24 Concussions are generally defined by GCS scores between 13 and 15.* Loss of consciousness and post-traumatic amnesia were once erroneously considered “conditio sine qua non” with regard to diagnosing a concussion.26 Recent evidence, however, suggests loss of consciousness occurs in less than 10% of sport-related injuries and post-traumatic amnesia between 25% and 30% of cases.16,17,27 This is a major point of misunderstanding among athletes, coaches, and parents, as well as clinicians.

The natural history of concussion is variable, but most individuals become asymptomatic in 7 to 10 days.27,29 Neuropsychological performance may be decreased beyond when the athlete no longer reports symptoms,27,3035 though the clinical significance of this finding is unclear. Interestingly, for self-reported symptoms, rate of symptom resolution is correlated to number of assessments given,23 possibly indicating a role for repeated assessments; this phenomenon is not observed with neurocognitive performance, though balance assessments show a learning effect in healthy individuals.36,37 Symptom exacerbation can occur during physical and/or cognitive exertion, and thus rest for both domains is recommended in the acute setting. The role of rest is unclear as symptoms persist outside of the typical recovery timeframe of 1 to 2 weeks.

PATHOPHYSIOLOGY

Determining the pathophysiological underpinnings of the symptoms of concussion is a major focus in concussion research. Animal models of mild TBI have elucidated a metabolic cascade of events in the acute phase following injury. A large potassium efflux occurs, coinciding with a diffuse release of glutamate.38 This is believed to be caused by a large number of indiscriminant depolarizations at the time of injury, likely due to sheer and strain forces on neurons. The ionic imbalance is restored through the action of K+/Na+ pumps, which require adenosine triphosphate (ATP), the primary energy substrate in the brain. Evidence suggests that action potentials and postsynaptic effects of glutamate account for as much as 80% of base rate energy metabolism in the cerebral cortex.39,40 Thus, indiscriminate neuronal firing and release of glutamate after concussion creates a massive rise in brain energy demand. This large energy demand coincides with a decrease in cerebral blood flow, leading to an imbalance between cerebral glucose metabolism and perfusion.4143 It is important to note that these mechanisms have not been extensively studied in human subjects. However, studies using proton magnetic resonance spectroscopy have found neurometabolite alterations indicative of neural damage and distress following sport-related concussion.44,45

Advanced neuroimaging of concussive injury is a growing field within sport-related concussion research. Routine neuroimaging studies, including magnetic resonance imaging (MRI) and cranial tomography (CT), are typically normal in the majority of concussed patients,46,47 leading many to call concussion a functional rather than structural injury. However, using more advanced MRI imaging protocols, particularly diffusion tensor imaging (DTI), microscopic disruptions in white matter tracts can be visualized.4852 Differences in image acquisition (including scanner type, time to scan following injury) and study design (voxel-versus tract-based versus region of interest analyses) have complicated synthesizing the results from DTI studies. Additionally, some studies have demonstrated no changes in white matter integrity following sport-related concussion.53 A meta-analysis by Aoki et al., showed that the most consistent changes occurred in the corpus callosum and were unrelated to time following injury.54 Specifically, two major metrics of white matter integrity were noted to change: fractional anisotropy (FA) decreased while mean diffusivity (MD) increased. Functional MRI (fMRI) and electroencephalography (EEG) have been useful in determining functional network changes following concussion. Resting state fMRI has shown changes in the default mode network, a neuronal network involved in non-task-related cognition.5558 Task-based fMRI studies have shown changes in both episodic59 and working memory57 networks. EEG studies have demonstrated differences following concussion,6065 with one well-designed, prospective study showing changes at 12 months following injury;66 however, there are no signature patterns on EEG that can be used to definitively diagnose concussion.

BIOMECHANICS

Linear and rotational head accelerations are hypothesized to be the primary risk factors for concussion during an impact. Both direct and inertial (i.e., whiplash) loading of the head may result in linear and rotational head acceleration. Head acceleration induces strain patterns in brain tissue, which may cause injury. Current science has not identified an exact threshold for concussive injury, and direct measurement of brain dynamics during impact is extremely difficult in humans. Head acceleration, on the other hand, can be more readily measured; its relationship to severe brain injury has been postulated and tested for more than 50 years. Both linear and rotational acceleration of the head play important roles in producing diffuse injuries to the brain. However, the relative contributions of these accelerations to specific injury mechanisms have not been conclusively established. The numerous mechanisms theorized to result in brain injury have been evaluated in cadaveric and animal, surrogate,67 and computer68,69 models. Prospective clinical studies combining head impact biomechanics and clinical outcomes have been relatively void in the literature.

Our ongoing studies at the University of North Carolina involving collegiate and high school football players employs a real-time helmet accelerometer data collection methodology to better understand the biomechanics of concussion. Our findings suggest a higher propensity of top-of-the-head impacts and a higher relative risk of concussion for those impacts. In one of our published papers, six of thirteen concussions occurred from impacts to the top of the head, which is in contrast to four, two, and one concussions occurring to the front, right, and back, respectively (Figure 2.1).70 These findings suggested that football players are concussed by head impacts occurring at a wide range of magnitudes (60.51 to 168.71 g linear acceleration), and that clinical measures of acute symptom severity, balance, and neuropsychological function, all appear to be largely independent of impact magnitude and location. There was no relationship between impact magnitude or location, and clinical outcomes of symptomatology, balance, or neuropsychological performance. The concussions sustained as a result of lower end magnitudes presented with just as many clinical deficits as those with higher end magnitudes. Thus, despite the literature suggesting that high magnitudes of head impact, particularly with high angular acceleration, result in more serious clinical outcomes in cases of moderate or severe TBI,71,72 the magnitude and location do not predict clinical recovery in cases of sport-related concussion.

FIGURE 2.1. Helmet accelerometer data showing location and magnitude of impact leading to concussion in cohort of collegiate American football players.

FIGURE 2.1

Helmet accelerometer data showing location and magnitude of impact leading to concussion in cohort of collegiate American football players. (From Guskiewicz, K.M. et al., Neurosurgery 61(6): 1244–1252, 2007.)

Concussions are often referred to structurally as “diffuse axonal injuries” and result in some degree of functional impairment, but differ from more moderate to severe TBI in that the impairment is transient in nature. Diffuse axonal injury, in addition to linear coup-contrecoup mechanisms of injury, can result in disruption to centers of the brain responsible for breathing, heart rate, and consciousness, but more typically result in memory loss, cognitive deficits, balance disturbances, and a host of other somatic symptoms. In the context of sport concussion, the term impact typically denotes an injurious blow that makes direct contact with the head. An indirect impact typically refers to an impact that sets the head in motion without directly striking it. Direct head impacts in sport range from helmet-to-helmet collisions, striking an opponent’s head with a stick, or being struck in the head by a projectile (e.g., soccer ball, hockey puck). Indirect impacts are most commonly caused by tackling or body checking, and are the result of abruptly stopping an opponent’s body from traveling in the direction in which it was originally moving. Direct and indirect impacts are traditionally linear (translational) or angular (rotational) in nature. In real-world activities, there is usually some combination of both linear and angular accelerations associated with direct and indirect impacts.

Many factors are thought to play a role in the body’s ability to dissipate head impact forces including individual differences in cerebrospinal fluid levels and function, vulnerability to brain tissue injury, relative musculoskeletal strengths and weaknesses, and the anticipation of an oncoming direct or indirect impact. Few studies have investigated the influence of cervical musculature on head impact biomechanics, and in general, increased cervical strength and muscle size has not been shown to reduce head acceleration and therefore prevent concussion.73,74 However, a recent study by Schmidt et al.75 observed that greater cervical muscle stiffness and angular displacement following perturbation reduces an athlete’s odds of sustaining higher magnitude impacts. Therefore, suggesting that improving the cervical muscles’ ability to quickly contract may be more important than overall muscle strength.

EPIDEMIOLOGY

An estimated 1.6 million to 3.8 million sport-related concussions occur in the United States annually,76 with an estimated 10 million all-cause TBIs occurring globally each year.77 As many as 50% of these sport-related concussions go unreported.78 The factors contributing to the underreporting of concussive injury are multifactorial and include gaps in knowledge concerning concussion symptoms, beliefs that the injury is not serious, and unwillingness to be removed from competition.78,79 Despite this underreporting, concussion incidence rates have been increasing in the past two decades.80,81 This may be due, in part, to increased awareness of the signs and symptoms of concussion and the growing concern over their long-term effects leading to increased reporting. A national study of TBIs with loss of consciousness indicated that 20% were attributed to sports and recreational activities.33 Within this sport-related sample (~300,000 total TBIs), 34% did not see a physician and 55% received only outpatient care (including emergency department visits). It is a major concern that concussions without major symptoms, such as loss of consciousness, may go unrecognized and unmanaged. It should be noted that there are barriers to obtaining high-quality epidemiological data about concussion incidence. In addition to underreporting, there is a lack of a widely used surveillance system in youth sports. Furthermore, very little information exists concerning sports below the high school level.

Nevertheless, concussion is a concern at every competitive level in contact sports.29,8284 Organized team sports account for approximately half of emergency department (ED) visits for concussion in the 14- to 18-year-old age range.81 The youth sports accounting for the greatest number of concussions are football, wrestling, girls’ soccer, boys’ soccer, and girls’ basketball.8587 Girls are reported to have a greater incidence of concussions when compared to boys playing similar sports.85,8789 The reasons for this gender disparity are unknown, but may include differences in cervical neck muscle strength, greater tendency to report symptoms in females, or due to the nature of female versions of the sports themselves.*

Of particular concern is football, which not only has one of the highest rates of concussion but also the largest participation.91 Highlighting the commonality of concussion in football, in the National Football League (NFL) a concussion occurs almost every other game (incidence of 0.41 per game92). In a 2007 study of 2552 retired NFL players, over 60% reported one or more concussions in their playing career with 24% reporting three or more concussions.93 Recurrent injury is not unique to football; evidence indicates that athletes with a history of concussion are at increased risk (as high as three-to fivefold greater risk) of additional concussions in the future.83,84,9496

EVALUATION

The evaluation of concussion should rely on a detailed history of injury and subjective symptomatology, physical exam, and objective assessment tools of cognitive functioning and balance. The immediate focus of the initial postinjury evaluation is on ruling out more serious injury to neurological structures; these include intracerebral, epidural, subdural, and subarachnoid hemorrhages; skull fractures; and cervical spine injury. Such injuries are emergencies that require immediate medical attention and intervention. The major concerning symptoms are alterations in consciousness, neck pain, loss of sensation or motor control, and abnormal posturing. Two major items of importance in the history of present illness include loss of consciousness and presence of post-traumatic amnesia as these predict presence of neurocranial abnormalities on cranial tomography.26 Beyond general impressions of consciousness, the physical exam should include a full neurological examination of the 12 cranial nerves, extremity strength, and fine touch sensation as these can be useful to further rule out focal deficits following injury. Additionally, previous history of concussion, history of neurological or psychological disorders, and family history of migraines and headaches may predict a worse prognosis.97

Once more serious injuries have been ruled out, definitive diagnosis of concussion relies on self-reported symptoms and objective measures of cognitive functioning and balance. As noted earlier, symptoms may vary but are commonly described as feeling dazed or “in a fog” and with a headache of variable intensity. Concussed patients may be slow to answer questions, repeat questions on answering, or have difficulty orienting to their surroundings. The standard assessment of concussion (SAC) is a well-developed tool for assessing acute cognitive functioning immediately postinjury with 94% sensitivity in detecting concussion.31,32,98,99 The SAC contains general questions concerning alertness and tasks to assess memory formation, delayed recall, and attention. The Balance Error Scoring System (BESS) is a useful instrument to assess balance immediately postinjury.100,101 The BESS involves scoring athletes’ ability to hold three different static stances (double leg, single leg, and tandem stance), first on a hard surface and then on a foam pad, each for 20 seconds (Figure 2.2). The SAC and BESS can be easily deployed on the sideline for immediate objective information regarding the mental status of athletes suspected of having a concussion. When used in combination with a graded symptom checklist, this multimodal approach to concussion management has been found to be very sensitive to diagnosing and tracking recovery following the injury.27,29,30 Figure 2.3 shows typical recovery curves of a graded symptom checklist, SAC, and BESS.

FIGURE 2.2. Demonstration of static stances comprising the Balance Error Scoring System (BESS).

FIGURE 2.2

Demonstration of static stances comprising the Balance Error Scoring System (BESS). The test begins with panel (a) and moves to panel (f) with each stance held for 20 seconds.

FIGURE 2.3. Typical recovery curves of serial assessments of symptoms, cognitive performance, and balance following a sport-related concussion.

FIGURE 2.3

Typical recovery curves of serial assessments of symptoms, cognitive performance, and balance following a sport-related concussion. (From McCrea, M. et al., JAMA 290(19): 2556–2563, 2003).

More detailed investigation into cognitive functioning is useful to track recovery and influence return-to-play decisions. Computerized neuropsychological testing systems, such as ImPACT (ImPACT Applications, Inc.; Pittsburgh, Pennsylvania), CNS-Vital Signs (CNS Vital Signs, LLC; Morrisville, North Carolina), Axon Sports (Axon Sports, LLC; Wausau, Wisconsin), combine a variety of paper-and-pencil tests into a single battery with rapid interpretation of results. These batteries give information across a broad range of cognitive domains including memory, attention, reaction time, processing speed, psychomotor speed, and fine motor coordination. The domains that are most sensitive to concussion are delayed memory, memory acquisition, and global cognitive functioning.33 Using baseline results and reliable change indices, trained clinicians can determine when cognitive functioning has returned to baseline levels. Caution is advised in the use of neuropsychological testing in making decisions regarding return-to-play.102 Although they are highly sensitive to mild cognitive dysfunction, they lack requisite specificity to be considered a diagnostic tool. Additionally, the domains computerized neuropsychological batteries seek to measure (as listed earlier) are inherently unstable, they can be affected by external factors (drugs, disease states, time of day) and internal factors (motivation, fatigue, mood, level of alertness).103 However, several of these tests have demonstrated reliability and can be considered a useful tool in the trained clinician’s armamentarium.103,104

Additionally, postural control and balance can be assessed in finer detail using NeuroCom (NeuroCom Inc.; Clackamas, Oregon) force plate-based technology. Specifically the Sensory Organization Test (SOT) is useful to isolate and measure the function of different domains including vestibular, visual, somatosensory, and preferential balance. SOT scores are decreased acutely following concussion and improve over the course of several days.100,101 Additionally, the SOT can be useful in determining what balance systems, if any, are affected in patients experiencing prolonged recovery. The affected systems can be targeted using either visual or vestibular rehabilitation. As with any injury, full consideration of all patient information should be the basis of management decisions, particularly in regard to the concussed athlete. Neither cognitive performance nor balance is sufficient in determining treatment or return-to-play decisions.

A relatively new domain of interest in initial concussion evaluations and tracking recovery is the oculomotor system. Disruptions in visual performance have been noted following blast-related mild TBI in military service members.105 One instrument designed to probe these deficits is the King-Devick test. This test requires the subject to read aloud a string of numbers across several test cards as quickly as possible, which requires both saccadic eye movements and rapid processing of information. Some studies have shown promise in detecting head trauma and concussion,106,107 whereas an emergency department study did not support its use.108 Further validation and development of the instrument is needed, but there is promise that the King–Devick test will become another useful tool for clinicians facing a concussed athlete.

Last, gait tasks have become increasingly popular due to the known deficits in balance following concussion. By assessing gait, the clinician can see an athlete perform a dynamic and more functionally relevant task than quiet standing or stance-holding as required by the SOT and BESS, respectively. Studies assessing gait postconcussion have found observable deficits.109112 Cantena et al. recommend pairing a gait task with an attentional task to obviate deficits in gait.113115 Such dualtask paradigms are being studied both for concussion evaluation as well as rehabilitation.116119 To date, there are no definitive studies supporting the use of dual-task rehabilitation programs in sport-related concussion.

TREATMENT

Cognitive and physical rest is considered the cornerstone of concussion management.24,6 The extent and duration of rest to maximize benefit is unclear, as only a scarcity of studies address the relationship between activity level after concussion and recovery of concussed athletes; however, they corroborate the principle of rest as an acute treatment.120122 The recommendation for rest is primarily based on an absence of literature surrounding interventions that may reduce risk of prolonged symptoms or improve recovery.3,123 Based on anecdotal evidence, the general recommendation is for complete rest in the immediate postinjury phase for 2 to 3 days followed by a gradual increase in activity as tolerated. For an athlete, this means temporary withdrawal from practice and reductions in cognitive activities (e.g., scholastic work, reading, cellular phone use). As symptoms abate, a progressive, stepwise return-to-play protocol is followed that increases physical activity until full participation can be resumed.

There are concerns regarding the immediate management and return-to-play decisions surrounding youth athletes. Many states have passed legislation that requires immediate removal from play, evaluation by a medical professional, and no same day return-to-play under any circumstance.124 For many years, sports concussion literature highlighted second-impact syndrome (SIS) as a potentially lethal consequence of concussion mismanagement.125,126 This catastrophic consequence is described as a loss of autoregulation of cerebral blood flow and thought to be the result of an impact occurring to an athlete while they are still symptomatic following an initial head injury. This second impact does not need to be severe enough to cause a second concussion, but can trigger a sequence of events that leads to nearly 50% mortality and 100% morbidity. However, the fact remains that SIS is a poorly understood phenomenon, due in large part to the rarity of its occurrence with only 35 probable cases identified in a 23-year period.127,128 If the risk of SIS is directly tied to concussive injury, one might expect a greater number of cases given the large number of estimated unreported concussions and the potential for athletes to receive impacts to the head following an unreported concussion.

Regardless of SIS, there are reasons to keep athletes from returning to play while they are symptomatic. Pediatric patients are slower to recover from injury than adults.129,130 It is generally accepted that there is unnecessary risk to returning an athlete to play before they are evaluated and cleared by a medical professional. There is a lack of understanding concerning the long-term effects of concussion, particularly where the developing brain is concerned. As previously mentioned, with symptom resolution typically occurring within 1 to 2 weeks, the time course for recovery from concussion is relatively rapid when compared to musculoskeletal injuries that can take weeks or months to heal. In the end, there should be no rush to return an athlete who may suffer from symptom exacerbation and an increased risk of suffering an additional injury. The focus of care should of course be on the general health and well-being of the athlete, not the rapidity of their return-to-play. Particular concern is warranted in the case of recurrent concussion suffered in the context of sports. When an athlete presents with repeat sport-related concussions, clinicians should engage in a frank discussion of risks versus reward with respect to continued participation in their sport.

FUTURE DIRECTIONS IN RESEARCH

Because of the dynamic and interdisciplinary nature of sport-related concussion, there are a large number of research areas and topics that are being aggressively pursued. While each of these avenues of research contributes to our understanding of the nature of the injury, there is a shortlist of priority areas that require meticulous, well-designed studies to move the field forward and make impactful change. These include the long-term effects of concussion, developing the clinical utility of neuroimaging, determining the effect of subconcussive impacts on the developing brain, improving clinical management practices, and making youth sports safer. We will now discuss some of the ongoing studies addressing these issues and the gaps in knowledge that are yet to be addressed.

While relatively few studies have examined the long-term effects of recurrent, sport-related concussion, several concerning trends have emerged, including increased risk of depression,93 cognitive impairment,131,132 earlier onset Alzheimer’s disease,42 dementia,133 and neurodegenerative cause of death.134 Despite these clinical observations, little is known about the neurophysiological changes associated with recurrent concussions and their impact on neurodegenerative disease. Recently, an association between repetitive head trauma and the development of chronic traumatic encephalopathy (CTE) has been proposed.135138 CTE is described as a neurodegenerative disease, distinguishable from Alzheimer’s disease and other forms of dementia on the basis of postmortem neuropathology. Histological studies on the brains of deceased contact athletes and military veterans have shown several characteristic findings such as a distinct pattern of hyperphosphorylated tau, reduction in total brain weight, and enlargement of ventricles.510

The clinical presentation of CTE consists of memory problems, executive dysfunction, and behavioral and personality changes, among others.137 However, it should be noted that clinical descriptions of CTE are based on informant interviews of deceased patients with CTE confirmed on postmortem histopathology. In vivo evidence of CTE is limited and further study is needed to understand the role of recurrent concussions on neurodegenerative disease. As such, CTE is a controversial diagnosis that is not universally accepted as a distinct pathology due to the largely nonspecific clinical descriptions and lack of clear diagnostic criteria.132 Nevertheless, preliminary results of a recent study demonstrate the presence of tau deposits in symptomatic retired football players distributed in a pattern consistent with autopsy studies.139 Additionally, in a mouse model that expresses human tau isoforms, repetitive mild TBI resulted in greater hyperphosphorylated tau deposition; however the authors noted that it did not follow the pattern described in CTE.140 Whether CTE is a distinct pathology, neurodegenerative disease is a major concern for retired athletes and military veterans. The controversy surrounding CTE highlights our need for structured, prospective investigations of the linkages between neurodegenerative disease and repetitive head trauma.

A major issue in studying the long-term effects of concussion is that the neuroimaging modalities by which we can study the structure and function of the brain in vivo are not yet perfected. Most imaging studies have used a concussed group with comparisons made to a matched control group, often with a small number of subjects (less than 20). Using a single scan, cross-sectional, group approach makes voxelwise analyses troublesome. Within the concussed group, the location of neuronal injury must occur in an approximately identical location in the brain for all the subjects in order to detect a significant difference between patient and the control groups. Given that the nature of concussive injury is heterogeneous based on the mechanics of the injury itself, more sophisticated analytic techniques are needed to adequately assess neuronal injury using imaging. Studies that compare concussed individuals to their preinjury scans are ideal, however, exceedingly difficult to perform, not in small part due to the large number of subjects that would need to be enrolled and the high cost of the scans. Regardless, such prospective investigation is needed to advance the utility of neuroimaging after concussion. Thus far, the clinical application of neuroimaging in concussion is underdeveloped. While CT is useful in ruling out more serious injury, there is little more to recommend imaging following concussion. To translate advanced neuroimaging to the clinic, e.g., DTI, susceptibility weighted imaging, or quantitative EEG, a large atlas of normative data would be needed across a wide range of ages. Injuries would need to be well characterized and studied across several time-points. Once these studies have been performed, the field can address the questions surrounding diagnostic sensitivity and specificity and prognostic ability of neuroimaging.

An interest in subconcussive head impacts has emerged in recent years following reports of CTE pathology in concussion naïve patients. Subconcussive impacts refer to head impacts sustained during collision sports that do not result in clinically apparent symptoms. Prospective study of repetitive subconcussive impacts is more easily implemented because investigators need not wait for concussion cases to present. Bazarian et al. has used DTI to study college football players across a single season and found greater changes in diffusion metrics in those athletes exposed to repetitive head impacts as compared to noncollision sport controls.141,142 Many of these changes persisted to six months following cessation of collision-sport activity. The findings of the Bazarian et al. studies are worrying, though preliminary. It is unclear whether the observed changes are deleterious or perhaps adaptive, given that in some regions there were increases in white matter integrity (increased FA) and others in which decreases were noticed (reduced FA). These changes were, for the most part, not strongly correlated to changes in neuropsychological testing, indicating that the neuroanatomical changes are clinically undetectable. Other studies employing a similar design found differences in diffusion metrics in club soccer players143 and college football and ice hockey players.144

Aside from imaging, another helpful tool to investigators seeking to further study the effects of subconcussive impacts is accelerometer technology. Helmeted sports, such as football, ice hockey, and lacrosse, have been studied using accelerometers embedded in the helmet; these systems provide information on the linear and rotational accelerations of the helmet and head during impact. Studies utilizing helmet accelerometers have improved our understanding of the in-game risk factors involved in concussive injury including position, sport, and event type (game versus practice).70,145,146 Furthermore, these systems have been used to determine the biomechanics of concussive injury, though no definitive threshold of head acceleration to predict concussion has been found.147 Studying the biomechanics of head impacts in youth sports has implications on practice structure, rule revisions, and coaching proper form and technique.148,149

In addition to research, accelerometer systems have clinical utility. Our group has used accelerometer systems as a way to monitor athletes during games and practices, and check in with those athletes who experience impacts that are above a cutoff magnitude. This practice has a caveat in that smaller impacts can still cause concussion, and thus, the clinical staff must be vigilant. Another use for the accelerometers entails behavioral correction of athletes who display “poor” head impact profiles (i.e., numerous high magnitude impacts, particularly to the crown of the head) that may be predictive of improper technique. Newer acceleration systems have been developed, such as intraoral devices and adhesive patches that can be applied directly to the head. These systems, though new and in need of validation, allow researchers to study nonhelmeted sports that convey a high concussion risk (e.g., soccer), and may be a more accurate method for directly measuring head acceleration. This will enable a finer, more resolved method to studying youth sports and informing decisions to improve safety and reduce concussion risk.

Although prevention is certainly a major goal in reducing the burden of sport-related concussions, improving management and clinical decision-making is equally important. In approximately 10% of sport-related concussion cases, symptoms persist beyond the normal window of recovery, and can last for weeks or months.29,95 Although definitions of postconcussion syndrome (PCS) vary depending on the source and there is no universally accepted definition of the syndrome, the common feature of the definitions of PCS is the continued experience of symptoms elicited from the initial injury. The World Health Organization’s International Statistical Classification of Diseases (10th revision) definition has a sensitivity and specificity of 73% and 61%, respectively, at one month postinjury.150

PCS is poorly understood, as are the risk factors associated with the condition. Initial self-reported symptom severity, prolonged headache, and concentration deficits have been associated with prolonged recovery.14 Corroborating some of these findings, a 10-year, controlled study of adolescent athletes found that presence of unconsciousness, post-traumatic amnesia, and symptom severity were most strongly associated with prolonged recovery.29,151 However, neither loss of consciousness nor amnesia are associated with greater deficits or slower recovery of objective measures of postural stability and neurocognitive function.101 Whether previous concussion history is predictive of developing PCS on repeat injury is in question as contradicting results exist across studies.152,153 Some evidence suggests that involvement in litigation or workers’ compensation may increase the severity and duration of concussion symptoms.22,154 Recent evidence suggests a role for a prescribed regimen of exercise155158 and/or cervicovestibular rehabilitation159 for treatment of patients with PCS. However, there is concern that reactive intervention may not be optimal and that earlier interventions, before PCS is diagnosed, are warranted. An obstacle to improving acute care of sport-related concussions lies in the fact that the vast majority of injuries self-resolve without observable, lasting impairments. Thus, the objective for interventions acutely following concussion should be to reduce the risk of developing PCS, which as described, is understudied.

CONCLUSION

There has been quite an evolution with respect to concussion management over the last two decades. Much of this can be attributed to research that has advanced our understanding of the biomechanics, pathophysiology, and recovery patterns associated with concussion. This evolution has brought technology and objective testing methods to the forefront of concussion management. Additionally, greater emphasis on education and awareness has certainly played a major part in helping to recognize and effectively manage these injuries. One of the greatest influences that clinicians can have in preventing sport-related concussion, and catastrophic outcomes, is to educate athletes, coaches, and parents about the dangers of playing while symptomatic following a concussion. Reports of the cumulative effects of multiple concussions, as well as the potential for multiple head impacts to affect long-term cognitive health, should lead clinicians to rethink their approach to managing concussion.

Contemporary methods of concussion assessment, involving the use of symptom checklists, neuropsychological testing, and postural stability/balance testing, are indicated for any athlete suspected of having sustained a concussion. Clinicians working with high-risk sports should conduct baseline assessments, including neuropsychological and postural stability tests, prior to the start of the season. Testing should also be conducted following exertional activities that are typically performed prior to a full return to activity. Most important, clinicians must recognize that the recovery and return-to-play considerations involve many factors. More recent research aimed at identifying biomarkers for determining the potential risk factors that predict symptom onset and progression of neurodegenerative disease in athletes who have played contact sports will eventually bring advanced technologies such as neuroimaging and blood biomarkers to our toolbox. With these new tools comes the promise of improving patient outcomes and maximizing safety for athletes with regard to their mental and cognitive health and longevity.

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Footnotes

*

For a thorough discussion of the history and evolution of our understanding of head injury and concussion, we refer readers to the excellent review provided by McCrory and Berkovic, 2001.7

*

It should be noted that the GCS was not intended to supplant a full neurological examination. However, serial evaluations of the GCS can be useful as the progression of scores can be used to predict prognoses (i.e., a high GCS score staying high or a low score becoming high are scenarios indicative of a good prognosis).25

As exemplified in a New England Journal of Medicine article in 2007 where the authors erroneously stated: “Concussion refers to an immediate and transient loss of consciousness accompanied by a brief period of amnesia after a blow to the head.”28

*

For instance, in ice hockey, females tend to get concussed more frequently than males. One possible explanation is that checking is disallowed in women’s hockey, and thus, players may not anticipate contact as often as male skaters.90

© 2016 by Taylor & Francis Group, LLC.
Bookshelf ID: NBK326721PMID: 26583180

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