Handbook of Clinical Neurology, Vol. 127 (3rd series) Traumatic Brain Injury, Part I J. Grafman and A.M. Salazar, Editors © 2015 Elsevier B.V. All rights reserved

Chapter 10

Acute sports-related traumatic brain injury and repetitive concussion KEVIN M. GUSKIEWICZ1* AND STEVEN P. BROGLIO2 Matthew Gfeller Sport-Related TBI Research Center, Department of Exercise and Sport Science, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA

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NeuroSport Research Laboratory, Michigan NeuroSport, School of Kinesiology, University of Michigan, Ann Arbor, MI, USA

INTRODUCTION Concussion is the most common neurologic injury occurring in sports and recreational activities, with an estimated 1.8–3.6 million cases each year (Langlois et al., 2006). Concussions can occur at all levels of athletic participation, in both contact and noncontact sports. However, contact sports such as football, soccer, wrestling, and lacrosse have higher concussion incidence rates compared to noncontact sports (Gessel et al., 2007; National Collegiate Athletic Association (NCAA) 2007; Lincoln et al., 2011). Concussions typically carry no outwardly visible signs, leaving approximately half of them unreported to coaches, parents, and medical professionals (McCrea et al., 2004). This is concerning because athletes who do not report concussions and return to play increase their risk of a recurrent and possibly catastrophic injury (McCrea et al., 2004). While the incidence varies widely between sports (National Collegiate Athletic Association (NCAA) 2007), in some sports (e.g., women’s ice hockey) the incidence of concussion may exceed that of all other injuries (Agel et al., 2007). Regardless of the setting, sports medicine clinicians must be prepared to manage these complex and somewhat misunderstood injuries, which have been labeled by the US Centers for Disease Control and Prevention as a “hidden epidemic.” Developing and instituting a concussion policy and management protocol constitutes the first step in properly treating the athlete suspected of sustaining a concussion, which should be backed by proper planning and practice of the on-field management strategy.

The potential for long-term effects of repetitive concussion has also been recognized (Bailes and Hudson, 2001; Macciocchi et al., 2001; Guskiewicz et al., 2005, 2007a; De Beaumont et al., 2009; Broglio et al., 2012; Kerr et al., 2012; Ford et al., 2013; Hart et al., 2013; Randolph et al., 2013) and there are increasing concerns about the limited ability to identify and treat these neurologic conditions in an attempt to slow or stop the progression in former athletes. Therefore, the term “ding” or “bell ringer” is discouraged for describing concussion and/or repetitive subconcussive head insults, because it does not convey the appropriate injury severity and need for medical care. The 4th International Conference on Concussion in Sport’s consensus group removed the classification of mild traumatic brain injury for concussion, and defined sport concussion as a brain injury involving a complex pathophysiologic process affecting the brain, induced by biomechanical forces (McCrory et al., 2013). According to the consensus group, several common features that incorporate clinical, pathologic, and biomechanical injury constructs that may be utilized in defining the nature of a concussive head injury include: 1.

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Concussion 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. Concussion typically results in the rapid onset of short-lived impairment of neurologic function that resolves spontaneously. However in some cases, symptoms and signs may evolve over a number of minutes to hours.

*Correspondence to: Kevin M. Guskiewicz, PhD, ATC, 209 Fetzer Hall, CB#8700, University of North Carolina Chapel Hill, Chapel Hill, NC 27599-8700, USA. Tel: +1-919-962-5175, Fax: +1-919-962-0409, E-mail: [email protected]

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K.M. GUSKIEWICZ AND S.P. BROGLIO Concussion may result in neuropathologic changes, but the acute clinical symptoms largely reflect a functional disturbance rather than a structural injury and, as such, no abnormality is seen in concussion on standard structural neuroimaging studies. Concussion results in a graded set of clinical symptoms that may or may not involve loss of consciousness. Resolution of the clinical and cognitive symptoms typically follows a sequential course. However, it is important to note that in some cases symptoms may be prolonged (McCrory et al., 2013).

Others have emphasized that the injury involves a temporary alteration in brain function which can present with a spectrum of postconcussive symptoms best categorized as somatic (headache, sensitivity to light or noise, balance problems, etc.), cognitive (concentration problems and memory impairment), or neurobehavioral (sleep disorders, fatigue, sadness, etc.) (Piland et al., 2006). Only about 10% of concussions will involve a loss of consciousness and less than one-third will involve amnesia (Guskiewicz et al., 2003; McCrea et al., 2005; Broglio and Guskiewicz, 2009; Guskiewicz and Broglio, 2011). Acute evaluation of concussions should focus on ruling out life-threatening or more severe injuries, such as a cervical spine injury or an intracranial hematoma. Once life-threatening injuries are ruled out, the evaluation should involve repeated evaluations on a multitude of measures, beginning with a sideline evaluation and continuing throughout full recovery. The majority of acute concussions will resolve within 7–10 days, but a small number can take longer (McCrea et al., 2005; Giza et al., 2013; McCrory et al., 2013). Unfortunately, there is no way to predict how long it will take an individual to recover from a concussion, but one group reported on field dizziness to be linked to a protracted recovery (Lau et al., 2011). Others (McCrea et al., 2005) identified acute injury characteristics of unconsciousness and amnesia as increasing the risk of a high school and collegiate athlete requiring longer than the typical 7 day window to achieve a full recovery. More severe injuries were also associated with more severe and longer lasting symptoms, cognitive impairment, and balance deficits. Failing to achieve a complete recovery within the first week postinjury was the factor most strongly associated with persistent symptoms 45–90 days postinjury. These findings underscore the importance of utilizing a multifaceted approach to evaluating concussion. This approach should include a thorough clinical evaluation, assessment of the patient’s signs and symptoms, measures of balance, and cognitive function. These should be tracked closely for the first several days postinjury to identify whether the athlete may be on a more

protracted recovery course (Guskiewicz et al., 2004; McCrea et al., 2005; Broglio and Guskiewicz, 2009; McCrory et al., 2013; Guskiewicz and Broglio, 2011; Broglio et al., 2014). Current standards recommend testing athletes on these measures prior to athletic participation, in order to serve as a baseline for comparison, in the event that the athlete sustains a concussion (Guskiewicz et al., 2004; Broglio and Guskiewicz, 2009; McCrory et al., 2013; Guskiewicz and Broglio, 2011; McCrory et al., 2013; Broglio et al., 2014). Several concussion grading scales were previously recommended for the management of concussion in the 1980s and 1990s; however, more contemporary practice guidelines do not recommend their use. Instead, these guidelines recommended a multimodal approach of tracking the presence and severity of all clinical symptoms, cognitive function, and balance as part of a comprehensive assessment and management strategy (Giza et al., 2013; McCrory et al., 2013; Broglio et al., 2014). These practice guidelines recommend that once the athlete is asymptomatic and exhibiting normal cognitive and balance function, the use of a graduated return to play progression should be implemented into the management plan. This involves first utilizing light aerobic exercises, followed by more provocative and sport-specific exercises over the course of several days to help determine when the player may be ready for a full return to participation. The focus of this chapter will be on the pathophysiology, evaluation, and potential long-term sequelae of sport-related TBI and repetitive concussion.

PATHOPHYSIOLOGY OF SPORTSRELATED TRAUMATIC BRAIN INJURY Sports-related TBI is caused by a sudden acceleration or deceleration of the head can result in compressive, shear, and tensile stress to cerebral tissue, leading to a diffuse injury from a linear and/or rotational acceleration. Acceleration-deceleration injuries usually occur when an individual is moving and comes into contact with a moving opponent, or in some cases a stationary object. These injuries cause shifting of cerebral tissue within the cranium, which may cause microscopic tearing of small vessels and capillaries, resulting in localized bleeding and hematoma formation (Bailes and Cantu, 2001). Brain injuries that occur in sport can be classified as either focal or diffuse. Focal brain injuries usually result from a direct blow that causes damage to cerebral substances and vessels, typically resulting in macroscopic lesions such as cortical or subcortical brain contusions and intracerebral hematomas (Bailes and Cantu, 2001) such as subdural or epidural hematomas. These severe injuries occur infrequently in sports, but when they do

ACUTE SPORTS-RELATED TRAUMATIC BRAIN INJURY AND REPETITIVE CONCUSSION 159 they can result in a fatality if the blood is not quickly EVALUATION OFACUTE SPORTSevacuated and the pressure on the brain not relieved RELATED TRAUMATIC BRAIN INJURY quickly. Diffuse brain injuries vary in intensity from A careful and well planned on-field and sideline assessmild to severe, and are often caused by rotational forces ment of concussion can be the difference between a from a direct or indirect blow. Diffuse injuries often good and bad outcome when managing TBI. In most result in shearing of white matter within the cortex to cases, the sideline assessment serves as a triage for the midbrain and brainstem, and are often not visible determining if a TBI has occurred, and if so, establishes in diagnostic images (Bigler et al., 2000; Bailes and a benchmark for determining the severity and potentially Cantu, 2001). Concussions are considered mild traucatastrophic condition could be developing. Given the matic brain injuries, and are considered diffuse axonal aforementioned description as “a complex pathophysioinjuries. A more serious type of traumatic brain injury, logical process affecting the brain, induced by traumatic but fortunately very rare, is that of diffuse cerebral biomechanical forces” (McCrory et al., 2013), concusedema. It involves diffuse swelling of the brain caused sions can evolve into something more serious if signs by a disruption of the blood flow through the brain. In and symptoms go undetected or are ignored. While these this situation, the injured brain is unable to self-regulate are very rare events (subdural and epidural hematomas or control the amount of blood pooling within the cereor diffuse cerebral edema) they must always be at the bral vessels. The rapid swelling of the brain often leads to forefront of the clinician’s mind. These conditions brainstem herniation and death most often occurs in should be suspected with a rapid worsening of symptoms patients with immature brains (12 professional bouts), and a clinical diagnosis of chronic traumatic encephalopathy. ApoE4 genotype, particularly in conjunction with increasing age (as a surrogate for exposure to repeated mTBI), was also associated with greater cognitive impairment in professional football players (Kutner et al., 2000). Other studies using a retrospective health questionnaire of 2552 retired professional football athletes revealed a fivefold risk of mild cognitive impairment diagnosis and self-reported memory problems following a history of three or more concussions (Guskiewicz et al., 2005). Although this study did not detect a direct association with Alzheimer’s disease (AD), an earlier onset of AD in the football retiree population was shown, relative to the general adult male population (age-adjusted prevalence ratio for AD ¼ 1.37 [95% CI 0.98–1.56]). In another study using the same health survey, the researchers revealed a threefold lifetime risk of depression in the retired professional football players with three or more prior concussions (Guskiewicz et al., 2007a).

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Other studies have identified an association between prior concussions and chronic cognitive dysfunction (Collins et al., 1999; Shuttleworth-Edwards, 2008; Thornton et al., 2008; Preiss-Farzanegan et al., 2009) but others have contradicted these findings, suggesting that there is no association (Broglio et al., 2006; Collie et al., 2006; Bruce and Echemendia, 2009). Several case reports or case studies which have identified the presence of tauopathy in former athletes (Omalu et al., 2005; McKee et al., 2009, 2010; Gavett et al., 2010; Omalu et al., 2010a, b, c) have suggested that there could be a cause and effect relationship between repetitive head trauma and the tau protein deposits found in the brains of former athletes on autopsy (i.e., chronic traumatic encephalopathy), but to date there are no prospective studies that have linked this condition to repetitive head trauma in athletes. The exact role of head impact exposure is not fully understood, and future research must consider how the athlete’s brain may differ from normal brain aging. There are many behavioral and environmental factors (sedentary lifestyle, excessive alcohol intake, smoking, prior recreational and occupational hazards, which can also negatively influence the aging brain (Broglio et al., 2012). Regardless, there is sufficient research to support the notion that the histopathologic features of dementia-related syndromes, as well as depression, may be initiated by repetitive head trauma and diagnosed concussions in athletes playing contact sports. Clinicians should counsel athletes, parents, and coaches about the potential dangers and long-term consequences of repetitive head trauma and consider early disqualification for those athletes with recurrent concussion.

CONCLUSION Sport-related traumatic brain injury has received significant attention in recent years, and clinicians can benefit from the evolution of new technologies and objective testing methods to help in the management of acute concussion. Concussive injury, which involves a temporary alteration in brain function, must be assessed serially over several days in order to ensure full recovery prior to returning to activity. Perhaps the greatest influence clinicians can have in preventing concussion, or at least preventing catastrophic outcome, is to educate athletes, coaches, and parents about the dangers of playing while symptomatic following a concussion, and to understand the potential cumulative effects of repetitive trauma. Contemporary methods of concussion assessment, involving the use of symptom checklists, neuropsychological testing, and postural stability testing, are

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indicated for any athlete suspected of having sustained a concussion, and research has shown the utility of these when incorporated into a systematic sideline and clinical assessment. Special tests for mental status and postural stability, along with reports of concussion-related symptoms, can provide the objective information that supports the clinical examination. Throughout the evaluation process the clinician should inquire about the development, presence, and intensity, or return of concussion-related symptoms. In no instance should an athlete be returned to play if they report any symptoms consistent with concussion, substantiating the dictum “when in doubt, sit them out” (Cantu, 2007).

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Acute sports-related traumatic brain injury and repetitive concussion.

Concussions are described as functional, not structural injuries, and therefore cannot be easily detected through standard diagnostic imaging. The vas...
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