http://informahealthcare.com/bij ISSN: 0269-9052 (print), 1362-301X (electronic) Brain Inj, 2015; 29(2): 276–282 ! 2015 Informa UK Ltd. DOI: 10.3109/02699052.2014.965216
REVIEW
Sports concussion assessment and management: Future research directions Michael McCrea1,2, Donna K. Broshek3, & Jeffrey T. Barth3 Departments of Neurosurgery and Neurology, Medical College of Wisconsin, Milwaukee, WI, USA, 2Clement Zablocki VA Medical Center, Milwaukee, WI, USA, and 3Department of Psychiatry and Neurobehavioral Sciences, University of Virginia School of Medicine, Charlottesville VA, USA Brain Inj 2015.29:276-282. Downloaded from informahealthcare.com by Kainan University on 04/10/15. For personal use only.
1
Abstract
Keywords
Over the past 2 decades, major progress has been achieved toward advancing the translational science of sport-related concussion (SRC), paving the way for evidence-based guidelines for injury diagnosis, evaluation and management. Several key empirical questions on the basic and clinical science of SRC, however, remain unanswered. The aim of this summary article is to highlight gaps in the existing science of SRC and to propose a platform for the next generation of SRC research. The article is framed around addressing two key questions that have major significance to protecting the health and safety of athletes affected by SRC, including: (a) Who is at risk of slow recovery or poor outcome after SRC, and why? (b) How does one modify the risks of slow recovery and poor outcome after SRC? Another aim of this article is to stimulate thought among researchers who will carry the science of SRC into the future, including neuropsychology leaders in the field. Implications for the broader science of traumatic brain injury are also discussed.
Neuropsychology, research, sports concussion
Introduction Over the past 2 decades, enormous strides have been made toward advancing the basic and clinical science of sportrelated concussion (SRC). In doing so, a new evidence base now informs on the magnitude of the problem, including large scale epidemiologic studies indicating the frequency of concussion in contact and collision sports at all competitive levels. There is now a new understanding of the defining characteristics of concussion, on which current definitions of injury and diagnostic criteria are based [1–4]. Several large prospective studies have described the true natural history of acute clinical effects and recovery, including detailed evidence on the time course in recovery of symptoms, cognitive functioning, balance and other functional capacities in athletes affected by SRC [5–8]. From the basic science arena, major scientific breakthroughs have shed light on the underlying pathophysiology of concussion, which in turn has implications for understanding of the time course of physiological effects and recovery after injury [9].
Correspondence: Michael McCrea, PhD, Professor & Director of Brain Injury Research, Departments of Neurosurgery and Neurology, Medical College of Wisconsin, 9200 W. Wisconsin Avenue, Milwaukee, WI 53226, USA. Tel: 414-955-7302. Fax: 414-955-0115. E-mail: [email protected]
History Received 21 April 2014 Revised 13 June 2014 Accepted 18 June 2014 Published online 10 October 2014
These research advances have directly impacted the development of evidence-based, best practice guidelines for the diagnosis, assessment and management of SRC, including protocols that drive the decision-making process on an athlete’s fitness to return to participation after concussion. In essence, translational research over the past 20 years has delivered several key findings that to a large extent take the guess work out of concussion management and provide the clinician with parameters for best practice. The sports concussion research model has proven incredibly valuable in that regard. The first prospective neurocognitive study of SRC introduced the Sports as a Laboratory Assessment Model (SLAM) which utilized a pre-season baseline and sequential post-concussion brief neurocognitive testing protocol which allowed individualized assessment of acute concussion effects and recovery curves [10]. Since then, neuropsychologists in particular have made major contributions to advancing scientific understanding of SRC, developing international guidelines for best practice in the clinical evaluation and management of SRC and guiding educational campaigns geared at the prevention of SRC. While research over the past 20 years has significantly advanced the basic and clinical science of SRC, several key empirical questions remain unanswered. The most pressing questions emanate from concerns about the risk for poor outcome after SRC, either in the form of complicated recovery during the acute and sub-acute phase, or the
Future research directions
Brain Inj 2015.29:276-282. Downloaded from informahealthcare.com by Kainan University on 04/10/15. For personal use only.
DOI: 10.3109/02699052.2014.965216
potential for long-term neurologic consequences associated with exposure to SRC and repetitive head impact exposure in contact and collision sports. The aim of this summary article is to highlight gaps in the existing science of SRC and to propose a platform for the next generation of SRC research. The authors have elected to frame the discussion of future directions around two key questions that have major clinical and translational significance to protecting the health and safety of athletes affected by SRC, including: Who is at risk of slow recovery or poor outcome after SRC and why? How does one modify the risks of slow recovery and poor outcome after SRC? Although this article is geared to stimulate thought among researchers who will carry the science of SRC into the future, including neuropsychology leaders in the field, it certainly is not intended to represent an exhaustive agenda for the broader science of traumatic brain injury.
Who is at risk of slow recovery or poor outcome after SRC and why? Several prospective studies over the past 2 decades have demonstrated that concussion is typically followed by a gradual, uncomplicated course of clinical recovery [5–8]. Large, prospective studies have plotted the continuous time course of clinical recovery in symptoms, cognitive functioning and postural stability after concussion, indicating that most athletes follow a gradual course of recovery in symptoms, cognitive functioning and postural stability over 1–2 weeks after concussion (Figure 1) [7, 11]. Recent research suggests, however, that more severe grades of injury or the presence of select comorbidities (e.g. history of depression, anxiety, migraine headaches) may result in symptoms and functional deficits that persist beyond the typical 7–10 day window after concussion [12] and that the
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risk of repeat concussion is highest during that same 7–10 day timeframe [13]. Further, recent studies indicate that abnormalities on advanced imaging and electrophysiological testing are detectable in athletes who otherwise report a complete symptom recovery and perform normally on clinical measures (e.g. cognitive and balance testing) after SRC [8, 14, 15]. Similar findings have been reported from studies of nonsports related mTBI, including findings of abnormalities on advanced neuroimaging that persist beyond the point of clinical recovery [16]. These findings fuel the critical concern that a window of cerebral vulnerability (WoCV) extends beyond the point of clinical recovery after mTBI, when the brain remains physiologically-compromised and at heightened risk of repetitive injury. Recent scientific breakthroughs begin to converge around an integrated model of clinical and physiological recovery, as illustrated in Figure 2. This model proposes a progression of recovery, characterized by (a) an acute period of clinical signs (e.g. symptoms, functional abilities) and concurrent physiologic dysfunction, followed by (b) persistent physiological dysfunction in the post-acute period (after resolution of clinical signs of injury) and, finally, (c) complete clinical and physiological recovery. In this model, the intermediate period of recovery is often characterized as a compensatory or over-excitatory phase, when the brain requires more neuronal resources and expends more metabolic energy to perform at the same standard as the healthy brain. This is also the period during which athletes typically begin the progression back to play, even when experiencing low-grade symptoms. In a clinical setting, understanding the natural time course of physiological recovery after mTBI has enormous implications. Risk prevention-based return to activity decisionmaking would ideally be based on more objective markers of both clinical and physiological recovery, indicating that the window of cerebral vulnerability has elapsed and the athlete is safe to resume activity without undue risk.
Figure 1. Symptom, cognitive and balance recovery in collegiate athletes.
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Figure 2. Integrated model of clinical and physiological recovery after concussion.
To better inform ultimate understanding of the risks associated with sport-related concussion, this study proposes three main areas of scientific inquiry that it is believed are both germane to the topic and achievable in the near future. Specifically, researchers are charged with empirically addressing the following key questions: How do injury dynamics and acute injury characteristics predict recovery? What is the influence of individual factors and vulnerabilities on recovery and outcome? What are the short-term and long-range health effects of repetitive head impact exposure through routine participation in contact and collision sports? How do injury dynamics and acute injury characteristics predict recovery? Over the past 2 decades, more has arguably been learned about the acute effects and early recovery course after SRC than any other specific topic area relevant to concussion. Still, key questions remain unanswered about the relative importance of acute injury variables in predicting short-term recovery and long-term outcome. Although classic characteristics of unconsciousness, post-traumatic amnesia and neurologic signs (e.g. pupil asymmetry) have proven of limited value in differentiating grades of injury and predicting postinjury outcome, new lines of research on injury biomechanics, clinical characterization and evaluation methods have been fruitful. New technologies now allow one to study the biomechanics of concussion by way of in vivo, real-time analysis. Future research applying head impact sensor technologies can inform on the influence of kinetics and kinematics on injury risk, characterization and recovery. In
addition to studying single concussive impacts, these technologies will also provide a wealth of information on short- and long-term health risks associated with repetitive, low-grade (sub-concussive) head impact exposure from routine participation in contact and collision sports. Similarly, important work over the last decade has positioned one to implement advanced neuroimaging and biological markers of concussion into the sports concussion research model. Great advances have been made in understanding the clinical, biomechanical and neurobiological effects of concussion in athletes, civilians and military service members. In large part, however, these efforts have focused on a single mTBI ‘marker’ for diagnosis and narrow measurement of recovery. Studies have mainly concentrated on a singular area of interest (e.g. neurocognitive testing). Few studies have fused the complete array of diagnostic technologies and broad based outcome measures available into a unified, prospective study design. As a result, an integrated neurobiopsychosocial model of mTBI is yet to be achieved. Ideally, future studies will investigate the correlation between multi-dimensional predictor and outcome variables associated with mTBI from a fully neurobiopsychosocial perspective in a common injured sample and single study design (see Figure 3). This work will also enable a longitudinal perspective on factors that influence both short-range and long-term outcomes after SRC. What is the influence of individual factors and vulnerabilities on recovery and outcome? Even when the characteristics of injury appear consistent across athletes, it is widely recognized that recovery and outcome can be influenced by variables specific to the
Future research directions
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DOI: 10.3109/02699052.2014.965216
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Figure 3. Neurobiopsychosocial model of concussion.
individual athlete. These factors may include demographic (e.g. age, gender, race), participation (e.g. sport, level of participation, etc.), health history (e.g. prior concussion history, co-morbid conditions), neurodevelopmental (e.g. history of attention deficit disorder or learning disability, etc.) and psychological factors (e.g. stress and resilience levels, etc.). While a small number of studies have investigated the influence of single factors on recovery and outcome, most studies have not had large enough sample sizes to investigate the complex interaction across multiple variable domains. As a result, a multi-dimensional understanding of risk has not yet been achieved. Ideally, future studies would provide larger samples and include common data elements to more systematically study the collective pool of risk factors. To that end, large, multi-centre collaborative efforts that enable data sharing will be essential. What are the short-term and long-range effects of repetitive head impact exposure? There are also emerging concerns about the potential longterm risks associated with mTBI, particularly in the setting of repetitive mTBI or sub-concussive head impact exposure. Beyond post-concussion syndrome, chronic risks include cumulative cognitive impairment, neurodegenerative disease and chronic traumatic encephalopathy (CTE). In this regard, military service members and athletes participating in contact and collision sports who are known to have a high incidence of mTBI or concussion are considered at highest risk. Studies focused on a comprehensive understanding of factors contributing to the risk of CTE and the development of
practical methods (imaging and fluid biomarkers) for diagnosing this disorder in living humans have the potential to move SRC research forward and positively impact medical and public policy. Research is needed to elucidate the role of impact and acceleration forces, age, gender, substance use and other psychosocial and health variables, as well as the influence of genetic factors. In addition to the concerns about the effects of concussive events, there is increasing concern and speculation about the potential negative health effects of repetitive, low-grade (subconcussive or non-concussive) head impact exposure experienced by athletes through routine participation in contact and collision sports. These concerns are fuelled in part by a series of individual case studies of former professional athletes who reportedly have followed a mid-life course of cognitive decline thought to be associated with their prior participation in collision sports, some reportedly with no documented instances of diagnosed concussion. More recently, a small number of studies have also suggested the potential for changes in brain structure and function associated with repetitive, sub-concussive head impact exposure and the absence of diagnosed concussion. The implications of these findings to the competitive sporting environment and larger society are monumental. That is, it is one thing if one is faced with developing strategies to reduce the risks associated with concussive injury, but an entirely new and daunting challenge if one is faced with developing strategies to reduce or completely eliminate head impact exposure from common contact and collision sports. Large, prospective studies are required to more definitively determine the short-term and long-range
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influence of head impact exposure on the health of athletes who compete in contact and collision sports at all competitive levels.
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How does one modify risks of slow recovery and poor outcome after SRC? In hopes of driving scientific discoveries that result in evidence-based injury prevention strategies, this study proposes three main areas of scientific inquiry that have immediate, translational relevance to the clinical setting and to protecting the health and safety of athletes. Specifically, it is recommended that the following key questions be studied further: How do current methods for injury diagnosis and assessment modify risk? How do current approaches to concussion management and return to play modify risk? What is the efficacy of specific treatment interventions and rehabilitation methods? How do current methods for injury diagnosis and assessment modify risk? The last 20 years could be characterized as the ‘scientific and standardization movement’ in SRC. That is, there has been an explosion of applied clinical research focused on concussion definition, diagnosis, assessment and management. These studies have significantly informed understanding of the defining characteristics of concussion, while also driving evidence-based approaches to the diagnosis and assessment of SRC. At the same time, a proliferation has been seen in the development of clinical tools intended for the assessment of athletes affected by SRC. Clinicians now have available a combination of brief screening tools appropriate for use in the rapid evaluation of athletes on the sideline, as well as more sophisticated tools intended to measure an athlete’s level of clinical recovery and fitness to return to participation after SRC. Building on the rich history of traditional neuropsychological testing, there are now many computerized neurocognitive assessment tools commercially available and in use in a sports medicine setting. Likewise, standardized approaches to clinical balance testing are commonly employed by sports medicine clinicians. Innovative approaches to multimodal testing now commonly integrate the assessment of postconcussive symptoms, cognitive functioning, postural stability and other functional abilities susceptible to the effects of SRC. More recently, researchers are exploring the prospects of physiological and biological testing in the acute clinical setting to assist in the diagnosis and assessment of SRC. A large body of literature has reported on the reliability, validity and clinical utility of the various concussion assessment tools commonly used by clinicians. In essence, great strides have been made in demonstrating the value of many of these clinical tools, enabling a more accurate and wellcharacterized assessment of the athlete during the acute phase. There is little research, however, focused on the predictive validity of concussion assessment tools and the influence these tools have in protecting athletes from further risk after SRC. In addition, concerns have been
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raised about who interprets the results of these various evaluative tools and how. The next generation of research should focus on how results from early clinical assessments can more specifically drive injury management strategies that facilitate recovery, reduce complications and prevent risk of re-injury. Ideally, based on current international consensus guidelines, these efforts would focus on the collective value of the multi-dimensional assessment battery to determine how this approach maximizes the sensitivity, specificity and predictive validity of SRC assessment strategies. It has become increasingly clear from prior research that single domain approaches to concussion assessment fall short in this regard and that the multi-dimensional approach will perform better in the context of what is known to be a highly heterogeneous injury. Specific prospects for future research might include the following: What is the best combination of clinical tools that provides the greatest sensitivity and specificity in detecting the immediate effects of sport-related concussion and enables an accurate diagnosis on the sports sideline? How do results from these clinical tools predict an athlete’s recovery and risk of post-injury complication or re-injury? How do results from early clinical assessments drive specific injury management strategies and return to play decision-making by clinicians? What is the best combination of clinical tools to most accurately measure an athlete’s eventual level of recovery and fitness to return to participation after SRC? What is the added value of baseline testing in evaluating and managing individual athletes after SRC? How do specific clinical tools perform with and without the availability of pre-injury baseline data in determining an athlete’s level of recovery and fitness to return to participation? How might head impact sensor technologies provide additional information over and above clinical assessment measures and assist in the diagnosis and characterization of SRC? What is the feasibility and clinical utility of using biological metrics (e.g. blood biomarkers) to assist in the acute diagnosis of concussion in a clinical setting (i.e. sports sideline)? What is the added value of these biomarkers over and above the multi-dimensional clinical approach? To what extent are the time courses of clinical and physiological recovery after SRC overlapping? If there is indeed an extended window of physiological recovery beyond the time point of typical clinical recovery, what are the clinical implications for injury management strategies? How do current approaches to concussion management and return to play modify risk? A point of maturity in the science has been reached such that there is a great deal of international consensus that rest and graded exertion are the cornerstones of concussion management. All consensus guidelines agree that no athlete who continues to experience or report any signs or symptoms of concussion should return to participation. The recommended
Future research directions
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DOI: 10.3109/02699052.2014.965216
approach to injury management is that the athlete observe a brief period of rest to facilitate early recovery and that the athlete first re-engage in light intensity, non-contact physical exercise prior to being cleared for full participation in sport-specific activities [2]. Recommended protocols call for the athlete to gradually increase the intensity and duration of aerobic exercise over a period of several days, as tolerated without any worsening or exacerbation of post-concussive symptoms. Once the athlete is able to tolerate high intensity, non-contact exertion, they then resume sport-specific activities and eventually return to unrestricted participation in contact and collision sports. This approach has been generally well received by the clinical community and has greatly simplified the landscape of injury management after SRC. The next frontier is to conduct prospective studies to determine the clinical efficacy of current day concussion management strategies, how they prevent post-injury complications and reduce the risk of repeat injury, particularly during the early window of recovery after SRC. To the extent that it is ethical from a human research safety standpoint, future studies should explore the benefits of the rest and graded exertion approach to injury management. Specific lines of scientific inquiry could involve the following: What is the optimal period of rest to facilitate recovery and minimize risk of re-injury after SRC? What is the specific type of rest that provides the greatest benefit (e.g. physical, cognitive, combined)? How should return to school and academics be considered in the context of rest and graded activity protocols? How does the introduction of ‘active rehabilitation’ positively or negatively affect the athlete’s response to rest and graded exertion? How do individual factors affect an athlete’s response to rest and graded activity? Is there a one size fits all solution to rest and graded activity or is there added benefit to a customized approach based on individual factors? Similarly, how do protocols for rest and graded exertion perform at different age and competition levels? Can a single protocol be applied across all competitive levels or are there nuances that should prompt consideration based on the athlete’s level and intensity of competition? What are the most effective injury management strategies for athletes who fail to progress through the common protocol of rest and graded activity? What is the efficacy of specific treatment interventions and rehabilitation methods? Beyond the scope of conventional concussion assessment and management, future research should explore new frontiers in treatment interventions to facilitate recovery and prevent poor outcome after SRC. Although a number of treatment and rehabilitation modalities (e.g. vestibular therapy, multi-modal rehabilitation, cognitive behavioural therapy, pharmacologic agents) are often employed in various clinical settings, the efficacy of these methods remains unclear, particularly with regard to SRC. As new and innovative treatment approaches become available, research should allow for clinical trials on the comparative efficacy of these interventions, ideally in a
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randomized design against current standard of care (i.e. rest and graded exertion). Similarly, the future should also bring greater emphasis on the development of strategies to reduce or prevent the incidence of SRC in contact and collision sports. A multidimensional approach to injury prevention that dually focuses on changes in policy, protective equipment and the culture of sports is likely to be more effective than any singular solution. Collectively, scientific, multi-disciplinary advances that drive evidence-based approaches to injury assessment, diagnosis, treatment and prevention are in the best interest of protecting the health of young athletes and preserving the richness of competitive sports.
Conclusion Over the past 2 decades, major advances have been realized toward a greater scientific understanding of SRC. There is now a more robust evidence base on the acute clinical effects and natural history of recovery that drive consensus guidelines for the diagnosis, evaluation and management of SRC. As a result of the work over the past 20 years, researchers are now positioned to conduct more sophisticated and comprehensive investigations of the physiological effects and recovery course after SRC. The advent of sophisticated neuroimaging technologies and other biological markers will fuel more advanced studies on the basic science of concussion. As such, future research should focus on enabling a dual understanding of the true natural history of both clinical and physiological recovery after SRC. These new lines of research will not only have direct relevance to injury management and prevention in sports, but will ultimately have translational significance to other populations at risk of concussion, including civilians and military service members.
Declaration of interest The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
References 1. Giza CC, Kutcher JS, Ashwal S, Barth J, Getchius TS, Gioia GA, Gronseth GS, Guskiewicz K, Mandel S, Manley G, McKeag DB, Thurman DJ, Zafonte R. Summary of evidence-based guideline update: Evaluation and management of concussion in sports: report of the Guideline Development Subcommittee of the American Academy of Neurology. Neurology 2013;80:2250–2257. 2. McCrory P, et al. Consensus statement on concussion in sport: The 4th International Conference on Concussion in Sport held in Zurich, November 2012. British Journal of Sports Medicine 2013; 47:250–258. 3. Harmon KG, et al. American medical society for sports medicine position statement: concussion in sport. Clinical Journal of Sport Medicine 2013;23:1–18. 4. Broglio SP, et al. National athletic trainers’ association position statement: Management of sport concussion. Journal of Athletic Training 2014;49:245–265. 5. McCrea M, et al. An integrated review of recovery after mild traumatic brain injury (MTBI): Implications for clinical management. Clinical Neuropsychology 2009;23:1368–1390. 6. Belanger HG, Vanderploeg RD. The neuropsychological impact of sports-related concussion: A meta-analysis. Journal of the International Neuropsychological Society 2005;11:345–357. 7. McCrea M, et al. Acute effects and recovery time following concussion in collegiate football players: The NCAA Concussion
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M. McCrea et al. Study. Journal Of The American Medical Association 2003;290: 2556–2563. McCrea M, et al. Acute effects and recovery after sport-related concussion: A neurocognitive and quantitative brain electical activity study. Journal of Head Trauma Rehabilitation 2010;25: 283–292. Giza CC, Hovda DA. The neurometabolic cascade of concussion. Journal of Athletic Training 2001;36:228–235. Barth JT, et al. Mild head injury in sports: Neuropsychological sequelae and recovery of function. In: Levin H, Eisenberg J, Benton A, editors. Mild head injury. Oxford Press: New York; 1989. p 257–275. McCrea M. Mild traumatic brain injury and post-concussion syndrome: The new evidence base for diagnosis and treatment. Oxford Press: New York; 2007.
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12. McCrea M, et al. Incidence, clinical course, and predictors of prolonged recovery time following sport-related concussion in high school and college athletes. Journal of the International Neuropsychological Society 2013;19:22–33. 13. Guskiewicz KM, et al. Cumulative effects associated with recurrent concussion in collegiate football players: The NCAA Concussion Study. Journal of The American Medical Association 2003;290: 2549–2555. 14. Barr WB, et al. Measuring brain electrical activity to track recovery from sport-related concussion. Brain Injury 2012;26:58–66. 15. Hammeke T, et al. Acute and subacute changes in neural activation during recovery from sport-related concussion. Journal of International Neuropsychological Society 2013;19:863–872. 16. Mayer AR, et al. A prospective diffusion tensor imaging study in mild traumatic brain injury. Neurology 2010;74:643–650.
REVIEW
Sports concussion assessment and management: Future research directions Michael McCrea1,2, Donna K. Broshek3, & Jeffrey T. Barth3 Departments of Neurosurgery and Neurology, Medical College of Wisconsin, Milwaukee, WI, USA, 2Clement Zablocki VA Medical Center, Milwaukee, WI, USA, and 3Department of Psychiatry and Neurobehavioral Sciences, University of Virginia School of Medicine, Charlottesville VA, USA Brain Inj 2015.29:276-282. Downloaded from informahealthcare.com by Kainan University on 04/10/15. For personal use only.
1
Abstract
Keywords
Over the past 2 decades, major progress has been achieved toward advancing the translational science of sport-related concussion (SRC), paving the way for evidence-based guidelines for injury diagnosis, evaluation and management. Several key empirical questions on the basic and clinical science of SRC, however, remain unanswered. The aim of this summary article is to highlight gaps in the existing science of SRC and to propose a platform for the next generation of SRC research. The article is framed around addressing two key questions that have major significance to protecting the health and safety of athletes affected by SRC, including: (a) Who is at risk of slow recovery or poor outcome after SRC, and why? (b) How does one modify the risks of slow recovery and poor outcome after SRC? Another aim of this article is to stimulate thought among researchers who will carry the science of SRC into the future, including neuropsychology leaders in the field. Implications for the broader science of traumatic brain injury are also discussed.
Neuropsychology, research, sports concussion
Introduction Over the past 2 decades, enormous strides have been made toward advancing the basic and clinical science of sportrelated concussion (SRC). In doing so, a new evidence base now informs on the magnitude of the problem, including large scale epidemiologic studies indicating the frequency of concussion in contact and collision sports at all competitive levels. There is now a new understanding of the defining characteristics of concussion, on which current definitions of injury and diagnostic criteria are based [1–4]. Several large prospective studies have described the true natural history of acute clinical effects and recovery, including detailed evidence on the time course in recovery of symptoms, cognitive functioning, balance and other functional capacities in athletes affected by SRC [5–8]. From the basic science arena, major scientific breakthroughs have shed light on the underlying pathophysiology of concussion, which in turn has implications for understanding of the time course of physiological effects and recovery after injury [9].
Correspondence: Michael McCrea, PhD, Professor & Director of Brain Injury Research, Departments of Neurosurgery and Neurology, Medical College of Wisconsin, 9200 W. Wisconsin Avenue, Milwaukee, WI 53226, USA. Tel: 414-955-7302. Fax: 414-955-0115. E-mail: [email protected]
History Received 21 April 2014 Revised 13 June 2014 Accepted 18 June 2014 Published online 10 October 2014
These research advances have directly impacted the development of evidence-based, best practice guidelines for the diagnosis, assessment and management of SRC, including protocols that drive the decision-making process on an athlete’s fitness to return to participation after concussion. In essence, translational research over the past 20 years has delivered several key findings that to a large extent take the guess work out of concussion management and provide the clinician with parameters for best practice. The sports concussion research model has proven incredibly valuable in that regard. The first prospective neurocognitive study of SRC introduced the Sports as a Laboratory Assessment Model (SLAM) which utilized a pre-season baseline and sequential post-concussion brief neurocognitive testing protocol which allowed individualized assessment of acute concussion effects and recovery curves [10]. Since then, neuropsychologists in particular have made major contributions to advancing scientific understanding of SRC, developing international guidelines for best practice in the clinical evaluation and management of SRC and guiding educational campaigns geared at the prevention of SRC. While research over the past 20 years has significantly advanced the basic and clinical science of SRC, several key empirical questions remain unanswered. The most pressing questions emanate from concerns about the risk for poor outcome after SRC, either in the form of complicated recovery during the acute and sub-acute phase, or the
Future research directions
Brain Inj 2015.29:276-282. Downloaded from informahealthcare.com by Kainan University on 04/10/15. For personal use only.
DOI: 10.3109/02699052.2014.965216
potential for long-term neurologic consequences associated with exposure to SRC and repetitive head impact exposure in contact and collision sports. The aim of this summary article is to highlight gaps in the existing science of SRC and to propose a platform for the next generation of SRC research. The authors have elected to frame the discussion of future directions around two key questions that have major clinical and translational significance to protecting the health and safety of athletes affected by SRC, including: Who is at risk of slow recovery or poor outcome after SRC and why? How does one modify the risks of slow recovery and poor outcome after SRC? Although this article is geared to stimulate thought among researchers who will carry the science of SRC into the future, including neuropsychology leaders in the field, it certainly is not intended to represent an exhaustive agenda for the broader science of traumatic brain injury.
Who is at risk of slow recovery or poor outcome after SRC and why? Several prospective studies over the past 2 decades have demonstrated that concussion is typically followed by a gradual, uncomplicated course of clinical recovery [5–8]. Large, prospective studies have plotted the continuous time course of clinical recovery in symptoms, cognitive functioning and postural stability after concussion, indicating that most athletes follow a gradual course of recovery in symptoms, cognitive functioning and postural stability over 1–2 weeks after concussion (Figure 1) [7, 11]. Recent research suggests, however, that more severe grades of injury or the presence of select comorbidities (e.g. history of depression, anxiety, migraine headaches) may result in symptoms and functional deficits that persist beyond the typical 7–10 day window after concussion [12] and that the
277
risk of repeat concussion is highest during that same 7–10 day timeframe [13]. Further, recent studies indicate that abnormalities on advanced imaging and electrophysiological testing are detectable in athletes who otherwise report a complete symptom recovery and perform normally on clinical measures (e.g. cognitive and balance testing) after SRC [8, 14, 15]. Similar findings have been reported from studies of nonsports related mTBI, including findings of abnormalities on advanced neuroimaging that persist beyond the point of clinical recovery [16]. These findings fuel the critical concern that a window of cerebral vulnerability (WoCV) extends beyond the point of clinical recovery after mTBI, when the brain remains physiologically-compromised and at heightened risk of repetitive injury. Recent scientific breakthroughs begin to converge around an integrated model of clinical and physiological recovery, as illustrated in Figure 2. This model proposes a progression of recovery, characterized by (a) an acute period of clinical signs (e.g. symptoms, functional abilities) and concurrent physiologic dysfunction, followed by (b) persistent physiological dysfunction in the post-acute period (after resolution of clinical signs of injury) and, finally, (c) complete clinical and physiological recovery. In this model, the intermediate period of recovery is often characterized as a compensatory or over-excitatory phase, when the brain requires more neuronal resources and expends more metabolic energy to perform at the same standard as the healthy brain. This is also the period during which athletes typically begin the progression back to play, even when experiencing low-grade symptoms. In a clinical setting, understanding the natural time course of physiological recovery after mTBI has enormous implications. Risk prevention-based return to activity decisionmaking would ideally be based on more objective markers of both clinical and physiological recovery, indicating that the window of cerebral vulnerability has elapsed and the athlete is safe to resume activity without undue risk.
Figure 1. Symptom, cognitive and balance recovery in collegiate athletes.
Brain Inj 2015.29:276-282. Downloaded from informahealthcare.com by Kainan University on 04/10/15. For personal use only.
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Figure 2. Integrated model of clinical and physiological recovery after concussion.
To better inform ultimate understanding of the risks associated with sport-related concussion, this study proposes three main areas of scientific inquiry that it is believed are both germane to the topic and achievable in the near future. Specifically, researchers are charged with empirically addressing the following key questions: How do injury dynamics and acute injury characteristics predict recovery? What is the influence of individual factors and vulnerabilities on recovery and outcome? What are the short-term and long-range health effects of repetitive head impact exposure through routine participation in contact and collision sports? How do injury dynamics and acute injury characteristics predict recovery? Over the past 2 decades, more has arguably been learned about the acute effects and early recovery course after SRC than any other specific topic area relevant to concussion. Still, key questions remain unanswered about the relative importance of acute injury variables in predicting short-term recovery and long-term outcome. Although classic characteristics of unconsciousness, post-traumatic amnesia and neurologic signs (e.g. pupil asymmetry) have proven of limited value in differentiating grades of injury and predicting postinjury outcome, new lines of research on injury biomechanics, clinical characterization and evaluation methods have been fruitful. New technologies now allow one to study the biomechanics of concussion by way of in vivo, real-time analysis. Future research applying head impact sensor technologies can inform on the influence of kinetics and kinematics on injury risk, characterization and recovery. In
addition to studying single concussive impacts, these technologies will also provide a wealth of information on short- and long-term health risks associated with repetitive, low-grade (sub-concussive) head impact exposure from routine participation in contact and collision sports. Similarly, important work over the last decade has positioned one to implement advanced neuroimaging and biological markers of concussion into the sports concussion research model. Great advances have been made in understanding the clinical, biomechanical and neurobiological effects of concussion in athletes, civilians and military service members. In large part, however, these efforts have focused on a single mTBI ‘marker’ for diagnosis and narrow measurement of recovery. Studies have mainly concentrated on a singular area of interest (e.g. neurocognitive testing). Few studies have fused the complete array of diagnostic technologies and broad based outcome measures available into a unified, prospective study design. As a result, an integrated neurobiopsychosocial model of mTBI is yet to be achieved. Ideally, future studies will investigate the correlation between multi-dimensional predictor and outcome variables associated with mTBI from a fully neurobiopsychosocial perspective in a common injured sample and single study design (see Figure 3). This work will also enable a longitudinal perspective on factors that influence both short-range and long-term outcomes after SRC. What is the influence of individual factors and vulnerabilities on recovery and outcome? Even when the characteristics of injury appear consistent across athletes, it is widely recognized that recovery and outcome can be influenced by variables specific to the
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Figure 3. Neurobiopsychosocial model of concussion.
individual athlete. These factors may include demographic (e.g. age, gender, race), participation (e.g. sport, level of participation, etc.), health history (e.g. prior concussion history, co-morbid conditions), neurodevelopmental (e.g. history of attention deficit disorder or learning disability, etc.) and psychological factors (e.g. stress and resilience levels, etc.). While a small number of studies have investigated the influence of single factors on recovery and outcome, most studies have not had large enough sample sizes to investigate the complex interaction across multiple variable domains. As a result, a multi-dimensional understanding of risk has not yet been achieved. Ideally, future studies would provide larger samples and include common data elements to more systematically study the collective pool of risk factors. To that end, large, multi-centre collaborative efforts that enable data sharing will be essential. What are the short-term and long-range effects of repetitive head impact exposure? There are also emerging concerns about the potential longterm risks associated with mTBI, particularly in the setting of repetitive mTBI or sub-concussive head impact exposure. Beyond post-concussion syndrome, chronic risks include cumulative cognitive impairment, neurodegenerative disease and chronic traumatic encephalopathy (CTE). In this regard, military service members and athletes participating in contact and collision sports who are known to have a high incidence of mTBI or concussion are considered at highest risk. Studies focused on a comprehensive understanding of factors contributing to the risk of CTE and the development of
practical methods (imaging and fluid biomarkers) for diagnosing this disorder in living humans have the potential to move SRC research forward and positively impact medical and public policy. Research is needed to elucidate the role of impact and acceleration forces, age, gender, substance use and other psychosocial and health variables, as well as the influence of genetic factors. In addition to the concerns about the effects of concussive events, there is increasing concern and speculation about the potential negative health effects of repetitive, low-grade (subconcussive or non-concussive) head impact exposure experienced by athletes through routine participation in contact and collision sports. These concerns are fuelled in part by a series of individual case studies of former professional athletes who reportedly have followed a mid-life course of cognitive decline thought to be associated with their prior participation in collision sports, some reportedly with no documented instances of diagnosed concussion. More recently, a small number of studies have also suggested the potential for changes in brain structure and function associated with repetitive, sub-concussive head impact exposure and the absence of diagnosed concussion. The implications of these findings to the competitive sporting environment and larger society are monumental. That is, it is one thing if one is faced with developing strategies to reduce the risks associated with concussive injury, but an entirely new and daunting challenge if one is faced with developing strategies to reduce or completely eliminate head impact exposure from common contact and collision sports. Large, prospective studies are required to more definitively determine the short-term and long-range
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influence of head impact exposure on the health of athletes who compete in contact and collision sports at all competitive levels.
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How does one modify risks of slow recovery and poor outcome after SRC? In hopes of driving scientific discoveries that result in evidence-based injury prevention strategies, this study proposes three main areas of scientific inquiry that have immediate, translational relevance to the clinical setting and to protecting the health and safety of athletes. Specifically, it is recommended that the following key questions be studied further: How do current methods for injury diagnosis and assessment modify risk? How do current approaches to concussion management and return to play modify risk? What is the efficacy of specific treatment interventions and rehabilitation methods? How do current methods for injury diagnosis and assessment modify risk? The last 20 years could be characterized as the ‘scientific and standardization movement’ in SRC. That is, there has been an explosion of applied clinical research focused on concussion definition, diagnosis, assessment and management. These studies have significantly informed understanding of the defining characteristics of concussion, while also driving evidence-based approaches to the diagnosis and assessment of SRC. At the same time, a proliferation has been seen in the development of clinical tools intended for the assessment of athletes affected by SRC. Clinicians now have available a combination of brief screening tools appropriate for use in the rapid evaluation of athletes on the sideline, as well as more sophisticated tools intended to measure an athlete’s level of clinical recovery and fitness to return to participation after SRC. Building on the rich history of traditional neuropsychological testing, there are now many computerized neurocognitive assessment tools commercially available and in use in a sports medicine setting. Likewise, standardized approaches to clinical balance testing are commonly employed by sports medicine clinicians. Innovative approaches to multimodal testing now commonly integrate the assessment of postconcussive symptoms, cognitive functioning, postural stability and other functional abilities susceptible to the effects of SRC. More recently, researchers are exploring the prospects of physiological and biological testing in the acute clinical setting to assist in the diagnosis and assessment of SRC. A large body of literature has reported on the reliability, validity and clinical utility of the various concussion assessment tools commonly used by clinicians. In essence, great strides have been made in demonstrating the value of many of these clinical tools, enabling a more accurate and wellcharacterized assessment of the athlete during the acute phase. There is little research, however, focused on the predictive validity of concussion assessment tools and the influence these tools have in protecting athletes from further risk after SRC. In addition, concerns have been
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raised about who interprets the results of these various evaluative tools and how. The next generation of research should focus on how results from early clinical assessments can more specifically drive injury management strategies that facilitate recovery, reduce complications and prevent risk of re-injury. Ideally, based on current international consensus guidelines, these efforts would focus on the collective value of the multi-dimensional assessment battery to determine how this approach maximizes the sensitivity, specificity and predictive validity of SRC assessment strategies. It has become increasingly clear from prior research that single domain approaches to concussion assessment fall short in this regard and that the multi-dimensional approach will perform better in the context of what is known to be a highly heterogeneous injury. Specific prospects for future research might include the following: What is the best combination of clinical tools that provides the greatest sensitivity and specificity in detecting the immediate effects of sport-related concussion and enables an accurate diagnosis on the sports sideline? How do results from these clinical tools predict an athlete’s recovery and risk of post-injury complication or re-injury? How do results from early clinical assessments drive specific injury management strategies and return to play decision-making by clinicians? What is the best combination of clinical tools to most accurately measure an athlete’s eventual level of recovery and fitness to return to participation after SRC? What is the added value of baseline testing in evaluating and managing individual athletes after SRC? How do specific clinical tools perform with and without the availability of pre-injury baseline data in determining an athlete’s level of recovery and fitness to return to participation? How might head impact sensor technologies provide additional information over and above clinical assessment measures and assist in the diagnosis and characterization of SRC? What is the feasibility and clinical utility of using biological metrics (e.g. blood biomarkers) to assist in the acute diagnosis of concussion in a clinical setting (i.e. sports sideline)? What is the added value of these biomarkers over and above the multi-dimensional clinical approach? To what extent are the time courses of clinical and physiological recovery after SRC overlapping? If there is indeed an extended window of physiological recovery beyond the time point of typical clinical recovery, what are the clinical implications for injury management strategies? How do current approaches to concussion management and return to play modify risk? A point of maturity in the science has been reached such that there is a great deal of international consensus that rest and graded exertion are the cornerstones of concussion management. All consensus guidelines agree that no athlete who continues to experience or report any signs or symptoms of concussion should return to participation. The recommended
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approach to injury management is that the athlete observe a brief period of rest to facilitate early recovery and that the athlete first re-engage in light intensity, non-contact physical exercise prior to being cleared for full participation in sport-specific activities [2]. Recommended protocols call for the athlete to gradually increase the intensity and duration of aerobic exercise over a period of several days, as tolerated without any worsening or exacerbation of post-concussive symptoms. Once the athlete is able to tolerate high intensity, non-contact exertion, they then resume sport-specific activities and eventually return to unrestricted participation in contact and collision sports. This approach has been generally well received by the clinical community and has greatly simplified the landscape of injury management after SRC. The next frontier is to conduct prospective studies to determine the clinical efficacy of current day concussion management strategies, how they prevent post-injury complications and reduce the risk of repeat injury, particularly during the early window of recovery after SRC. To the extent that it is ethical from a human research safety standpoint, future studies should explore the benefits of the rest and graded exertion approach to injury management. Specific lines of scientific inquiry could involve the following: What is the optimal period of rest to facilitate recovery and minimize risk of re-injury after SRC? What is the specific type of rest that provides the greatest benefit (e.g. physical, cognitive, combined)? How should return to school and academics be considered in the context of rest and graded activity protocols? How does the introduction of ‘active rehabilitation’ positively or negatively affect the athlete’s response to rest and graded exertion? How do individual factors affect an athlete’s response to rest and graded activity? Is there a one size fits all solution to rest and graded activity or is there added benefit to a customized approach based on individual factors? Similarly, how do protocols for rest and graded exertion perform at different age and competition levels? Can a single protocol be applied across all competitive levels or are there nuances that should prompt consideration based on the athlete’s level and intensity of competition? What are the most effective injury management strategies for athletes who fail to progress through the common protocol of rest and graded activity? What is the efficacy of specific treatment interventions and rehabilitation methods? Beyond the scope of conventional concussion assessment and management, future research should explore new frontiers in treatment interventions to facilitate recovery and prevent poor outcome after SRC. Although a number of treatment and rehabilitation modalities (e.g. vestibular therapy, multi-modal rehabilitation, cognitive behavioural therapy, pharmacologic agents) are often employed in various clinical settings, the efficacy of these methods remains unclear, particularly with regard to SRC. As new and innovative treatment approaches become available, research should allow for clinical trials on the comparative efficacy of these interventions, ideally in a
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randomized design against current standard of care (i.e. rest and graded exertion). Similarly, the future should also bring greater emphasis on the development of strategies to reduce or prevent the incidence of SRC in contact and collision sports. A multidimensional approach to injury prevention that dually focuses on changes in policy, protective equipment and the culture of sports is likely to be more effective than any singular solution. Collectively, scientific, multi-disciplinary advances that drive evidence-based approaches to injury assessment, diagnosis, treatment and prevention are in the best interest of protecting the health of young athletes and preserving the richness of competitive sports.
Conclusion Over the past 2 decades, major advances have been realized toward a greater scientific understanding of SRC. There is now a more robust evidence base on the acute clinical effects and natural history of recovery that drive consensus guidelines for the diagnosis, evaluation and management of SRC. As a result of the work over the past 20 years, researchers are now positioned to conduct more sophisticated and comprehensive investigations of the physiological effects and recovery course after SRC. The advent of sophisticated neuroimaging technologies and other biological markers will fuel more advanced studies on the basic science of concussion. As such, future research should focus on enabling a dual understanding of the true natural history of both clinical and physiological recovery after SRC. These new lines of research will not only have direct relevance to injury management and prevention in sports, but will ultimately have translational significance to other populations at risk of concussion, including civilians and military service members.
Declaration of interest The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
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