Review Article
Sports Concussion Management: Part I Thomas R. Terrell, MD, MPhil, Timothy Nobles, BA, Brianna Rader, Kenneth Bielak, Irfan Asif, MD, Robert Casmus, BA, Jamie Yeager, BS, and Reem Hussein, BA Abstract: Concussion is a popular clinical topic that has been the subject of unprecedented recent media coverage. As concerns about the potential short- and long-term implications of repetitive head injury in sports such as football continue to mount, the proper clinical management of concussion seems to increase in importance. The days of ignoring the ‘‘ding’’ on the sideline are definitely over. A series of updated clinical evaluation and management recommendations from international experts are highlighted in this review. The clinical presentation of an acute concussion, both the typical and more subtle variations, may be evaluated with new validated sideline evaluation tools (eg, Sports Concussion Assessment Tool 2). In addition, the role of computerized neuropsychological and balance testing in the acute and ongoing evaluation are discussed, along with how they contribute to the return-to-play decision. Same-day return to play is outdated, and the relative insensitivity of current neuroimaging modalities to demonstrate structural damage is highlighted. New therapeutic interventions such as amantadine and cognitive rest may improve recovery time. The appropriate management of concussion typically results in a normal functional and neurocognitive outcome. The recommendations in this article may guide clinicians, with varying degrees of prior experience managing concussion, to increase the likelihood of an excellent outcome. Key Words: concussion, minimal traumatic brain injury, postconcussion syndrome, return-to-play
From the University of Tennessee Graduate School of Medicine, Knoxville, the Department of Physical Education and Athletics, Catawba College, Salisbury, North Carolina, and the East Tennessee State University School of Medicine, Johnson City. Reprint requests to Dr Thomas R. Terrell, Associate Professor, Department of Family Medicine, University of Tennessee Graduate School of Medicine, 1924 Alcoa Hwy, U-71, Knoxville, TN 37920. Email: [email protected] This article has been developed as a Journal CME Activity by the Southern Medical Association. Visit http://sma.inreachce.com to view instructions, documentation, and the complete necessary steps to receive CME credit for reading this article. Fees may apply. CME credit will be available for 2 years after date of publication. T.R.T. received grant funding from the National Operating Committee on Standards for Athletic Equipment, the American Medical Society for Medicine Foundation, and the University of Tennessee Physician’s Medical Education Research Fund. The opinions expressed in this article are those of the authors and not those of these organizations. The authors have no financial relationships to disclose and no conflicts of interest to report. Accepted February 19, 2013. Copyright * 2014 by The Southern Medical Association
MD, MBA,
S
port-related concussion is one of the most pressing issues in sports medicine and has received unprecedented recent media attention. A total of 1.6 to 3.8 million concussions occur in sports and recreational activities annually in the United States. The significant variability in the concussion rates reported in the literature1 and, in particular, the significant recent increase, may occur as the result of the historical underreporting of concussions; one study showed that less than half of US football players report their concussions2 and that they believe they are impervious to significant injury.3 This underreporting led to underestimates of prevalence in older data.4 The most likely cause for the increased recent prevalence stems from the increased awareness by athletes about the importance of concussion coupled with improved detection methods. Finally, the true rate may have increased, owing to changes in the game. Concussions and their improved detection and management have become the focus of attention of several international consensus conferences,5 the National Football League, the National College Athletics Association (NCAA), state legislative bodies, and the US Congress.5Y10 Several high-profile deaths attributed to improper concussion management have raised this issue to a high level of professional and public scrutiny,11 and the primary care physician is expected to follow the latest clinical management guidelines.
Key Points & Concussion is a functional disturbance and not a structural problem; therefore, clinical imaging does not add to management. & Validated acute concussion tools such as the Sports Concussion Assessment Tool 2, the postconcussion symptom score, and the Balance Error Scoring system postural evaluation provide additional objective information that aids in assessment. & A patient with an acute concussion is not to return to any physical activity on the day of the injury, and may require serial neurocognitive testing and the use of other tools to determine the appropriate point at which return to some exercise may occur. & The clinical management of acute concussion includes an enhanced focus on ‘‘cognitive rest’’ to enhance the speed and completeness of recovery.
0038-4348/0Y2000/107-115 DOI: 10.1097/SMJ.0000000000000063
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Concussion management has changed because of a number of research advances, including several validated sideline evaluation tools5 and computerized neuropsychological testing that allow a more objective evaluation of these sometimes subtle injuries. In the past, the clinician was limited to the sideline and mental status examination to evaluate an athlete with acute concussion.12 The prevention of a catastrophic outcome, such as second impact syndrome (SIS), remains the preeminent goal of proper management. SIS is a typically fatal complication that occurs in individuals with concussions who sustain additional head trauma before completely recovering from an initial concussion.13 In theory, SIS occurs because of the loss of normal cerebral autoregulation, leading to brain stem herniation and death.13 This article presents an updated review of ways to diagnose and manage a suspected concussion. We discuss the clinical evaluation and use of neuroimaging and neuropsychological testing, new sideline tools, and the latest return-to-play (RTP) guidelines.
Definition The Consensus Statement on Concussion in Sport (4th edition) provides the most up-to-date concussion definition and discusses the latest guidelines.5 Concussion is defined as a transient neurological event that occurs following a blow to or twisting of the head and may be characterized by confusion, disorientation, and retrograde (RGA) or anterograde (posttraumatic) amnesia. Headache, dizziness, fogginess, visual changes, fatigue, and nausea often occur (Table 1).14,15 Several characteristics of a concussive head injury include the following5: 1. Concussion may be caused by a direct blow to the head, face, neck, or elsewhere on the body, with an impulsive force transmitted to the head. 2. Concussion typically results in the rapid onset of short-lived impairment of neurologic function that resolves spontaneously. 3. Concussion may result in neuropathological changes, but the acute clinical symptoms largely reflect a functional disturbance rather than a structural injury. 4. 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; in a small percentage of cases, postconcussion symptoms (PCSs) may be prolonged.
Anterograde amnesia (PTA) is characterized by a significant impairment in new learning. RGA for events that occurred before the concussive event is a measure of a more severe concussion. A study by Cantu first emphasized the importance of PTA and RGA in grading concussion severity.16
Sideline Evaluation and Treatment Any individual who sustains a blow to the head and experiences any of the symptoms listed in Table 1 may have sustained a concussion. The acute evaluation focuses on determining whether a concussion or an epidural or a subdural
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Table 1. Symptoms experienced by athletes with concussion Loss of consciousness
Headache
Confusion
Pressure in head
Posttraumatic amnesia/retrograde amnesia
Vomiting
Disorientation Dizziness
Nausea Feeling as though ‘‘in a fog’’
Difficulty concentrating
Slurred speech
Difficulty remembering
‘‘Don’t feel right’’
Visual changes Balance problems Sensitivity to light or noise
Drowsiness Trouble falling asleep Nervous or anxious
Feeling slowed down
More emotional
Personality changes Fatigue or low energy
Irritability Sadness
hematoma has occurred. An on-the-field assessment includes the evaluation and management of the ABCsVAssess the situation, Be alert for signs and symptoms, Contact a healthcare professionalVbefore cognitive function is evaluated.17 After the ABCs, the mental status and focused neurological examinations are completed. Loss of consciousness carries with it the potential for an occult cervical spine (c-spine) injury; thus, precautionary c-spine immobilization is imperative in this setting. After loss of consciousness, if the athlete regains consciousness and lucidity and the physician reliably may assess for c-spine tenderness without the confounding nature of distracting pain or altered mental status, then the c-spine may be cleared. If not, then full c-spine immobilization and emergency transport for radiological evaluation is mandatory. Vital signs are monitored every 15 to 30 minutes until the athlete becomes asymptomatic. The athlete must never be left unsupervised. A stepwise approach to sideline evaluation includes the following: assess the general level of consciousness and mental status; determine the mechanism of injury and obtain clinical history from the patient and others (eg, athletic trainers, teammates); inquire about prior concussions, their severity, and timing; conduct a neurological examination by assessing mental status, cranial nerves, pupillary response, motor strength, Romberg test, and cerebellar examination; administer the Sports Concussion Assessment Tool 2 (SCAT 2; Fig. [note that the SCAT3 is the current document, which is discussed in Part II])18; and compare with any baseline scores, if available. Neuroimaging of the brain after a concussion rarely is abnormal, but it is often obtained to rule out a more serious injury. The American College of Emergency Physicians’ guidelines for ordering computed tomography (CT) scans for acute concussion19 include a prolonged disturbance of the unconscious state, a focal neurological deficit, or worsening acute symptoms.17 In addition, one may consider obtaining a CT if there are symptoms or signs of an altered sensorium suggestive * 2014 Southern Medical Association
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Fig. Sports Concussion Assessment Tool 2 (SCAT2). Validated concussion assessment instrument developed by the Third International Conference on Concussion in Sports, Zurich, 2008. Reproduced from British Journal of Sports Medicine, McCrory P, Meeuwisse WH, Johnston K, et al. 43, i76Yi84, 2009, with permission from BMJ Publishing Group Ltd. Southern Medical Journal
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Fig. (continued)
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Fig. (continued) Southern Medical Journal
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of an intracranial injury (eg subdural hematoma, epidural hematoma). The modality of choice to rule out acute intracranial injury is the noncontrast CT. Concussion is a functional disturbance rather than a structural one, and for this reason, the vast majority of CT scans on athletes with acute concussion are normal.5 A nonemergent CT scan may be indicated if PCSs worsen in the days following the injury or magnetic resonance imaging (MRI; our preference) if they persist 2 to 3 weeks after the injury. The recommendation to order an MRI is based on expert opinion, unsupported by any prospective or comparative studies. More sophisticated diffusion tensor-weighted MRI imaging20 is available at research centers, but the proper clinical interpretation and application of this type of imaging is premature. The use of functional MRI and positron emission tomography/ CT scans is limited by cost and access.21
Concussion Assessment Tools A number of validated concussion assessment tools have been developed to aid in concussion evaluation. Ultimately, concussion remains a clinical diagnosis; however, the Standardized Assessment of Concussion (SAC) has some utility in confirming an acute concussion.22 The SCAT2,5 used for injured athletes ages 10 years or older, and the SAC5,22 are validated tests to identify, diagnose, and study recovery after a concussion. They are easy to use and recognized internationally. The SCAT2, a composite of four previously validated subtests, is administered acutely and serially every few days to objectively study concussion resolution. The SCAT2 includes Maddocks Questions to assess orientation and understanding. In addition, the SAC22 tests orientation, immediate memory, concentration, and delayed recall. Finally, the Balance Error Scoring System is a validated sideline balance examination that measures equilibrium.16 It is important to obtain baseline scores for these measures to facilitate the interpretation of postconcussion results.
Neuropsychological Testing Neuropsychological (NP) testing is an objective measurement of different cognitive domains and distinctive types of cognitive function.23 The validated software most commonly used for group testing includes HeadMinder (New York, NY),24,25 ImPACT (ImPACT Applications, Pittsburgh, PA),26,27 ANAM (Vista Life Sciences, Washington, DC),28 and Cogstate/Axon (New Haven, CT).29 These programs assist athletic trainers and physicians in studying postconcussion neurocognitive recovery.5,12,14,23 Typically, collision/contact athletes (eg, football players) complete a baseline normal NP test during the preseason that is compared, if an acute concussion occurs, with postconcussion testing to evaluate neurocognitive performance and recovery over time.23 The software provides results in a format that is conducive to understanding when a return to baseline has occurred. Controversy remains as to whether NP
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testing improves clinical management or outcomes for concussed athletes; however, some asymptomatic postconcussion patients have persistently abnormal NP testing, despite appearing to be recovered. These cases further support the need for NP testing.30,31
Chronic Traumatic Encephalopathy Chronic traumatic encephalopathy (CTE) is a progressive neurodegenerative disease formerly called dementia pugilistica. A number of autopsy-proven cases in former professional collision-sport athletes32Y36 and a high school athlete37 have stimulated considerable concern and research. The clinical manifestations of CTE include progressive symptoms of memory loss; difficulty with planning, organization, and judgment, coupled with having a ‘‘short fuse;’’ mood disturbances; inappropriate behavior; and drug use.32,33 Participation in a prolonged career in collision sports causes a threefold increase in the risk of developing neurodegenerative conditions.38 Although the precise pathological mechanisms that link repeated head injuries to neurofibrillary tangles are unknown, they may involve a series of diffuse axonal injuries set in motion by the initial trauma and aggravated by subsequent mild traumatic injuries.32 CTE is characterized by tau neurofibrillary tangles, neuropil threads, and glial tangles that are found in the medial temporal lobe, often in greater densities than that seen in severe Alzheimer disease, the diencephalon, basal ganglia, and brainstem.32 Ongoing research is focused on defining the amount, mechanism, and type of cumulative brain trauma that may lead to CTE and any potential predisposing genetic/other risk factors.32,33
PCS PCS has no universally accepted definition; however, in general, it involves at least three of the following symptoms: headache, dizziness, fatigue, irritability, impaired memory and concentration, insomnia, and light sensitivity,39 which may persist for months to years. PCS typically resolves with prolonged rest. Proper management of acute concussion and the RTP decision is critical to reduce the risk of PCS. NCAA restrictions on the neurostimulant Adderall make amantadine more attractive as a medication to treat PCS. Subsymptom exercise treadmill testing is being studied as a treatment modality for refractory PCS.40,41
Management of Acute Concussion The clinician has a challenging responsibility in managing acute concussion, the severity of which is typically unknown initially. There is no universal guideline on how to treat each concussion42; each should be managed on a case-by-case basis.43,44 The Consensus Statement on Concussion in Sport,5 however, does provide some general guidance: athletes with symptoms should be removed from play and no athlete with symptoms, at rest or with exertion, should continue to play. The caveat we would add is that CT scan is helpful in instances in which the severity of the injury is unknown. * 2014 Southern Medical Association
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The sine qua non of management is to withhold an athlete with a concussion from exercise activity until symptoms are fully resolved at rest and following an exercise challenge. Several concussion symptoms overlap with other disorders, including headache from an effort headache,45 dehydration, an underlying premorbid migraine, or other disorders, thus creating diagnostic difficulties.
RTP Decisions Perhaps the most challenging decision to make is when it is safe for an athlete with a recent concussion to RTP. RTP on the same day as the acute concussion is no longer recommended because research shows incomplete neurocognitive recovery in asymptomatic acutely concussed patients and because of the risk of life-threatening SIS.30,31 An incompletely recovered athlete with a concussion who sustains a second concussion is at greater risk of prolonged recovery and/or a more severe concussion with prolonged recovery, RGA or PTA, and PCS.5,46,47 To even consider RTP, first the athlete must be asymptomatic at rest. Second, the athlete should be fully recovered neurocognitively, as measured by SCAT2, SAC, and preferably postconcussion NP testing (or most commonly, a combination of several of these measures), before being cleared to start an exercise challenge test.17,46,47 The limitations of these instruments are considerable. The SCAT2 is not validated as a composite tool, and the utility of NP testing is affected by the quality of the baseline test with which the postconcussion test is compared. Commonly used validated instruments include the SAC, the ImPACT postconcussion self-reported symptom score,26 and NP testing with HeadMinder,24 ImPACT,26,27 or Axon/Cogsport.29 The sensitivity of ImPACT is 82% and specificity is 89%, with strong intercorrelations among HeadMinder, ImPACT, and Axon/ Cogsport on subscales such as processing speed and reaction time, but not within the memory domain.48 These factors combine to make RTP a complicated decision. Same-day RTP, even following a successful exercise challenge that provoked no symptoms, is no longer allowed based on the recommendations from the American Medical Society for Sports Medicine concussion position statements.49 Recently concussed NCAA athletes may have persistent neurocognitive deficits (ImPACT score abnormal in one-third of asymptomatic athletes) despite symptom recovery.50 In addition, a study of high school football documented cognitive impairment without clinically diagnosed concussion.31 How to fully interpret this study and its impact on clinical management is evolving, but cautious RTP is the norm. Some clinicians are using graduated exercise on a treadmill to rehabilitate patients who have sustained a concussion or those with PCS. The authors suggest that an abnormal heart rate response to exercise may be treated with a gradual progressive increase in treadmill exercise intensity, although the need remains for prospective Southern Medical Journal
outcome studies comparing different protocols for concussion groups.40
Cognitive Rest The symptomatic athlete with acute concussion benefits from a period of cognitive rest that includes restriction from schoolwork, extensive reading, texting, loud environments, and playing video games.51 Bed rest is unnecessary and may actually be harmful.52 The limited research suggests that the ideal amount of cognitive rest remains to be determined.53,54 Proper management of the academic demands on a concussed patient is critical for normal recovery.
Pharmacological Interventions in Concussion Clinicians may use pharmacological therapy to treat acute and persistent symptoms. No effective pharmacological treatment speeds recovery from traumatic brain injury (TBI).55 Clinicians experienced in concussion management may prescribe medications that modify the underlying pathophysiology of the concussion, the goal being to shorten symptom duration. Tylenol or nonsteroidal anti-inflammatory drugs are helpful for acute postconcussion headache, but they may lead to rebound headache and are not recommended.56 Medications also may treat associated sleep dysfunction, headaches arising from cognitive fatigue, persistent dizziness, and attention difficulties. The use of sleeping agents such as melatonin, trazodone, or nonbenzodiazepine sleeping agents such as zolpidem or tricyclic antidepressants is permitted, but benzodiazepines should be avoided because of potential memory impairment.57Y59 Neurobehavioral symptoms may be treated with medication. Amantadine has been proven effective in improving arousal in severe TBI cases60 and has been studied in sports concussion.61 Some studies show that it improves executive function in pediatric patients,62 but other small studies show no improvement in the NP scores of subjects taking amantadine versus placebo.63 Typically, a 3-week trial of amantadine is adequate to determine its efficacy. Neurostimulants such as methylphenidate have been proven by randomized controlled trials to assist in TBI treatment,64 particularly in treating deficits in attention and speed of processing and general cognitive functioning65; however, some studies have shown them to be ineffective.66 They should be considered carefully on a caseby-case basis. If the athlete is an NCAA player, the organization must be notified in writing of any stimulant use because stimulants are banned substances.67 For depression that develops following TBI, the use of selective serotonin reuptake inhibitors such as sertraline68 is beneficial, according to Meehan and colleagues.69
RTP NP may provide additional objective data to help clinicians evaluate postconcussion neurocognitive recovery and to recommend appropriate timing for safe RTP.70 The ultimate utility
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Table 2. Concussion modifier Factors
Modifier
Symptoms
Number Duration (910 d) Severity Prolonged loss of consciousness (91 min)
Signs
Amnesia Sequelae
Concussive convulsions
Temporal
Frequency: repeated concussions over time Timing: injuries close together in time Recency: recent concussion or TBI
Threshold
Repeated concussions occurring with progressively less impact force or slower recovery after each successive concussion
Age
Child and adolescent (younger than 18 y)
Comorbidities and premorbidities
Migraine Depression or other mental health disorders Attention-deficit/hyperactivity disorder Learning disabilities Sleep disorders
Medication
Psychoactive drugs Anticoagulants
Behavior
Dangerous style of play
Sport
High-risk activity Contact and collision sport High sporting level
TBI, traumatic brain injury. Data adapted from BMJ Publishing Group Ltd.5
of NP in assisting clinicians in making final RTP decisions remains subject to debate, although the Zurich statement made it clear that NP testing should be understood as a clinical decisionmaking tool to be used in conjunction with numerous clinical domains and investigational results.5 When the concussed
patient becomes asymptomatic, he or she should undergo a postconcussion NP test. If the postconcussion NP scores are within 1 standard deviation of baseline, then it may be safe from a neurocognitive recovery standpoint to recommend the graduated exercise progression protocol that is successfully completed before RTP. Consideration of clinical parameters always is crucial, and NP testing should not be used in isolation to decide upon RTP. Research also supports NP testing. For instance, some studies demonstrate that asymptomatic athletes with recent concussion may show persistent neurocognitive deficits that extend several days or weeks.31,50 RTP guidelines continue to become more conservative. Additional factors to consider when weighing the safe RTP include whether the subject has any history of concussion modifiers5 (Table 2) that may prolong recovery time or has sustained several concussions in the preceding weeks or months. Finally, a history of severe concussion with a prolonged recovery time of 92 months or of multiple severe concussions are scenarios that dictate a more conservative approach to RTP. Once postconcussion symptoms have resolved, the athlete must successfully complete a sequential, graduated exercise program in a 5- to 7-day period before he or she may be cleared for RTP (Table 3).5 This approach should reduce the risk associated with premature return to activity.71 Of particular importance, if any symptoms recur during the exercise challenge, the athlete should stop at this level of activity and not resume activity until he or she is asymptomatic for 24 hours.5 The athlete should then step down to a lower level of physical activity and restart the process. After one successful day at that exercise activity level, the patient may advance to a more intensive form of exercise. The graduated exercise challenge may be managed effectively by athletic trainers under the direction of a medical provider. Studies on the adherence to published RTP guidelines show that compliance is not always high. Athletic trainers reporting on the Internet on concussed high school athletes showed that compliance with RTP guidelines was not attained
Table 3. Graduated return-to-play protocol Rehabilitation stage
Functional exercise at each rehabilitation stage
Objective of each stage
1: No activity
Complete physical and cognitive rest
Recovery
2: Light aerobic exercise
Walking, swimming, or stationary cycling, keeping intensity 970% maximum predicted heart rate
Increase heart rate
3: Sport-specific exercise
No resistance training Skating drills in ice hockey, running drills in soccer
Add movement
No head-impact activities 4: Noncontact training drills
Progression to more complex training drills (eg, passing drills in football and ice hockey)
Exercise, coordination, and cognitive load
May start progressive resistance training 5: Full contact practice
Following medical clearance, participate in normal training activities
6: Return to play
Normal game play
Restore confidence and assess functional skills by coaching staff
Data adapted from BMJ Publishing Group Ltd.5
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in 40% of cases.72 Another study showed that 78% of rugby players with concussions did not receive any RTP guidelines.73
Children and Adolescents RTP decisions are much more conservative for concussed athletes in elementary and middle school because their brains are still developing. They should be held out of any physical activity until they are asymptomatic at rest for at least 1 week.74
Multiple Concussions The management of individuals who sustain multiple concussions in a given year is a complicated process because of the absence of prospective outcome data on which to rely to develop evidence-based guidelines. The classic Cantu RTP recommendations, following a single concussion or multiple concussions in the same year, remain the mainstay of treatment.75 We suggest discussing these cases with a primary care sports medicine physician, neurologist, or neurosurgeon who specializes in sports concussion. No arbitrary number of concussions has been established after which an athlete should stop participating in all collision sports. It is important to carefully evaluate the severity of each individual concussion, any secondary modifying factors, and formal pencil-and-paper neuropsychological testing rather than focusing solely on the total number of historical concussions. A family conference involving the key parties may be helpful to make these difficult decisions. Clinicians must consider having discussions with recurrently concussed athletes on modification to a noncollision sport or even retirement.76
SIS SIS occurs when an individual who has recently sustained a head injury but has not recovered completely from it experiences an additional, typically milder, head injury that leads to a life-threatening syndrome. The person with SIS typically collapses, experiencing dilated pupils and labored respirations as the cerebellum herniates through the foramen magnum; typically, 50% of individuals with SIS die.13,77 A group of researchers in Australia question the existence of SIS,78 but it is fully accepted as a clinical entity in most of the world.
Conclusions The Appendix provides a summary of educational resources for concussion management. Legislation (eg, the Zackery Lystedt law) that requires a physician or designee (usually an athletic trainer) to clear any concussed athlete before RTP has been passed by 940 states.79 Some investigators are studying whether genetic factors may increase concussion risk. A cross-sectional study of 178 college athletes showed a 2.7-fold increased risk of self-reported prior concussion for participants with the APOE G-219T TT genotype.80 Additional discussion of this work and other current research on concussion appears in the second article of this series (see page 126). Southern Medical Journal
The dissemination of new scientific research on concussion has increased dramatically in recent years. Consequently, the practicing clinician has more research-derived clinical guidelines for the management of concussion and a more extensive set of sideline and bedside evaluation tools. A proper assessment of acute symptoms, supplemented by sideline tools such as the SCAT2, SAC, and NP testing, provides more extensive information with which a physician may make clinical decisions. The expansion of baseline and postconcussion NP testing provides an objective evaluation of neurocognitive recovery that supplements the more subjective follow-up of self-reported symptom resolution. Concerns about the timing of full neurocognitive recovery that may follow symptom resolution have eliminated the practice of same-day RTP following concussion; however, a timely RTP is still possible for asymptomatic patients who pass a graduated exercise challenge protocol.
Acknowledgments The authors thank Victoria Coy and Gregory Nichols for assistance in the preparation of the article.
Appendix: Concussion Management Resources & Acute Concussion Evaluation (ACE) Care Plan: http:// www.cdc.gov/concussion/HeadsUp/physicians_tool_kit.html. & American Medical Society for Sports Medicine position statement: See Reference 15. & American Medical Society for Sports Medicine Webinar on concussion: http://www.amssm.org/AMSSMNewsConcussionWebinar.php. & Heads Up Concussion in Youth Sports Concussion Toolkit: Includes free coaches training for youth sports (http://www. cdc.gov/concussion/HeadsUp/physicians_tool_kit.html). & www.Boksmart.com: Developed by South African physicians to educate teenage rugby players, coaches, and parents. Compulsory biennial online training required of coaches/ referees. & Hockey Canada Concussion App for iPhone: http://www. hockeycanada.ca/en-ca/Hockey-Programs/Safety/ Concussions.aspx. & Cantu R, Hyman M. Concussions and Our Kids. Boston: Houghton Mifflin Harcourt; 2012.
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4. Delaney J, Lacroix VJ, Leclerc S, et al. Concussions among university football and soccer players. Clin J Sports Med 2002;12:331Y338. 5. McCrory P, Meeuwisse WH, Aubry M, et al. Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012. Br J Sports Med 2013;47:250Y258. 6. Guskiewicz KM, McCrea M, Marshall SW, et al. Cumulative effects associated with recurrent concussion in collegiate football players: the NCAA Concussion Study. JAMA 2003;290:2549Y2555. 7. Ellenbogen RG, Berger MS, Batjer HH. The National Football League and concussion: leading a culture change in contact sports. World Neurosurg 2010;74:560Y565. 8. Jaffee MS, Helmick KM, Girard PD, et al. Acute clinical care and care coordination for traumatic brain injury within Department of Defense. J Rehabil Res Dev 2009;46:655Y666. 9. Gavett BE, Stern RA, McKee AC. Chronic traumatic encephalopathy: apotential late effect of sport-related concussive and subconcussive head trauma. Clin Sports Med 2011;30:179Y188. 10. Vecsey G. College athletes move concussions into the courtroom. New York Times 2011:B14. 11. Latimer P. Schools adjust to new N.C. concussion law. http://www. starnewsonline.com/article/20110702/ARTICLES/110709944. Published July 2, 2011. Accessed August 4, 2012. 12. Terrell TR. Concussion in athletes. South Med J 2004;97:837Y842. 13. Cantu RC. Second-impact syndrome. Clin Sports Med 1998;17:37Y44. 14. Scorza KA, Raleigh MF, O’Connor FG. Current concepts in concussion: evaluation and management. Am Fam Physician 2012;85:123Y132. 15. Harmon KG, Drezner J, Gammons M, et al. American Medical Society for Sports Medicine position statement: concussion in sport. Clin J Sport Med 2013;23:1Y18. 16. Cantu RC. Posttraumatic retrograde and anterograde amnesia: pathophysiology and implications in grading and safe return to play. J Athl Train 2001;36:244Y248. 17. Buzzini SR, Guskiewicz KM. Sport-related concussion in the young athlete. Curr Opin Pediatr 2006;18:376Y382. 18. Guskiewicz KM. Assessment of postural stability following sport-related concussion. Curr Sports Med Rep 2003;2:24Y30. 19. Jagoda AS, Bazarian JJ, Bruns JJ Jr, et al. Clinical policy: neuroimaging and decision making in adult mild traumatic brain injury in the acute setting. Ann Emerg Med 2008;52:714Y748. 20. Van Boven RW, Harrington GS, Hackney DB, et al. Advances in neuroimaging of traumatic brain injury and posttraumatic stress disorder. J Rehabil Res Dev 2009;46:717Y757. 21. Clark CM, Schneider JA, Bedell BJ. Use of florbetapir-PET for imaging beta-amyloid pathology. JAMA 2011;305:275Y283. 22. McCrea M. Standardized mental status testing on the sideline after sportrelated concussion. J Athl Train 2001;36:274Y279. 23. Johnson EW, Kegel NE, Collins MW. Neuropsychological assessment of sport-related concussion. Clin Sports Med 2011;30:73Y88. 24. Erlanger DM, Feldman DJ, Kutner KC. HeadMinder: Concussion Resolution Index (CRI): Professional Manual. New York, HeadMinder, 2002. 25. Erlanger DM, Kaushik T, Broshek D, et al. Development and validation of a web-based screening tool for monitoring cognitive status. J Head Trauma Rehabil 2002;17:458Y476. 26. Lovell MR, Iverson GL, Collins MW, et al. Measurement of symptoms following sports-related concussion: reliability and normative data for the post-concussion scale. Appl Neuropsychol 2006;13:166Y174. 27. Iverson GL, Lovell MR, Collins MW. Validity of ImPACT for measuring processing speed following sports-related concussion. J Clin Exp Neuropsychol 2005;27:683Y689. 28. Cernich A, Reeves D, Sun W, et al. Automated neuropsychological assessment metrics sports medicine battery. Arch Clin Neuropsychol 2007;22:S101YS114. 29. Collie A, Maruff, P, McStephen M, et al. Cogsport, in Echemendia RJ (ed): Sports Neuropsychology: A Clinical Primer. New York, Guilford Press, 2005:71Y84.
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30. Iverson GL, Brooks BL, Collins MW, et al. Tracking neuropsychological recovery following concussion in sport. Brain Inj 2006;20:245Y252. 31. Talavage TM, Nauman E, Breedlove EL, et al. Functionally-detected cognitive impairment in high school football players without clinicallydiagnosed concussion. J Neurotrauma 2013; [Epub ahead of print]. 32. McKee AC, Cantu RC, Nowinski CJ, et al. Chronic traumatic encephalopathy in athletes: progressive tauopathy after repetitive head injury. J Neuropathol Exp Neurol 2009;68:709Y735. 33. McKee AC, Stern RA, Nowinski CJ, et al. The spectrum of disease in chronic traumatic encephalopathy. Brain 2013;136:43Y64. 34. Omalu BI, Fitzsimmons RP, Hammers J, et al. Chronic traumatic encephalopathy in a professional American wrestler. J Forensic Nurs 2010;6: 130Y136. 35. Omalu BI, DeKosky ST, Hamilton RL, et al. Chronic traumatic encephalopathy in a National Football League player: part II. Neurosurgery 2006;59:1086Y1093. 36. Omalu BI, DeKosky ST, Minster RL, et al. Chronic traumatic encephalopathy in a National Football League player. Neurosurgery 2005;57: 128Y134. 37. Schwarz A. Concussion trauma risk seen in amateur athlete. New York Times 2009:B14. 38. Lehman EJ, Hein MJ, Baron SL, et al. Neurodegenerative causes of death among retired National Football League players. Neurology 2012;79:1970Y1974. 39. King NS. Post-concussion syndrome: clarity amid the controversy? Br J Psychiatry 2003;183:276Y278. 40. Leddy JJ, Sandhu H, Sodhi V, et al. Rehabilitation of concussion and postconcussion syndrome. Sports Health 2012;4:147Y154. 41. Leddy JJ, Kozlowski K, Donnelly JP, et al. A preliminary study of subsymptom threshold exercise training for refractory post-concussion syndrome. Clin J Sport Med 2010;20:21Y27. 42. McKeag DB. Understanding sports-related concussion: coming into focus but still fuzzy. JAMA 2003;290:2604Y2605. 43. Stricker PR, Moriarity J, O’Connor FG. Concussion. N Engl J Med 2007;356:1787Y1788. 44. Putukian M. The acute symptoms of sport-related concussion: diagnosis and on-field management. Clin Sports Med 2011;30:49Y61. 45. McCrory P. Recognizing exercise-related headache. Phys Sportsmed 1997;25:33Y43. 46. Poirier MP. Concussions: assessment, management, and recommendations for return to activity. Clin Pediatr Emerg Med 2003;4:179Y185. 47. Putukian M, Aubry M, McCrory P. Return to play after sports concussion in elite and non- elite athletes? Br J Sports Med 2009;43:i28Yi31. 48. Shatz P, Putz BO. Cross-validation of measures used for computer-based assessment of concussion. Appl Neuropsychol 2006;13:151Y159. 49. Herring SA, Cantu RC, Guskiewicz KM, et al. Concussion (mild traumatic brain injury) and the team physician: a consensus statementV2011 update. Med Sci Sports Exerc 2011;43:2412Y2422. 50. Broglio SP, Macciocchi SN, Ferrara MS. Neurocognitive performance of concussed athletes when symptom free. J Athl Train 2007;42:504Y508. 51. Valovich McLeod TC, Gioia GA. Cognitive rest: the often neglected aspect of concussion management. Athletic Ther Today 2010;15:1Y3. 52. de Kruijk JR, Leffers P, Meerhoff S, et al. Effectiveness of bed rest after mild traumatic brain injury: a randomised trial of no versus six days of bed rest. J Neurol Neurosurg Psychiatry 2002;73:167Y172. 53. Valentine V, Logan K. Cognitive rest in concussion management. Am Fam Physician 2012;85:100Y101. 54. Moser RS, Glatts C, Schatz P. Efficacy of immediate and delayed cognitive and physical rest for treatment of sports-related concussion. J Pediatr 2012;161:922Y926. 55. Beauchamp K, Mutlak H, Smith WR, et al. Pharmacology of traumatic brain injury: where is the ‘‘golden bullet’’? Mol Med 2008;14:731Y740. 56. Lenaerts ME, Couch JR. Posttraumatic headache. Curr Treat Options Neurol 2004;6:507Y517.
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57. Samantaray S, Das A, Thakore NP, et al. Therapeutic potential of melatonin in traumatic central nervous system injury. J Pineal Res 2009;47: 134Y142. 58. Rao V, Rollings P. Sleep disturbances following traumatic brain injury. Curr Treat Options Neurol 2002;4:77Y87. 59. Arciniegas DB, Anderson CA, Topkoff J, et al. Mild traumatic brain injury: a neuropsychiatric approach to diagnosis, evaluation and treatment. Neuropsychiatr Dis Treat 2005;1:311Y327. 60. Giacino JT, Whyte J, Bagiella E, et al. Placebo-controlled trial of amantadine for severe traumatic brain injury. N Engl J Med 2012;366:819Y826. 61. Reddy CC, Collins M, Lovell M, et al. Amantadine treatment on symptoms and neurocognitive performance among adolescents following sportsrelated concussion. J Head Trauma Rehabil 2013;28:260Y265. 62. Kraus MF, Smith GS, Butters M, et al. Effects of the dopaminergic agent and NMDA receptor antagonist amantadine on cognitive function, cerebral glucose metabolism and D2 receptor availability in chronic traumatic brain injury: a study using positron emission tomography (PET). Brain Inj 2005;19:471Y479. 63. Schneider WN, Drew-Cates J, Wong TM, et al. Cognitive and behavioural efficacy of amantadine in acute traumatic brain injury: an initial doubleblind placebo-controlled study. Brain Inj 1999;13;863Y872. 64. Sivan M, Neumann V, Kent R, et al. Pharmacotherapy for treatment of attention deficits after non-progressive acquired brain injury. A systematic review. Clin Rehabil 2010;24:110Y121. 65. Neurobehavioral Guidelines Working Group, Warden DL, Gordon B, et al. Guidelines for pharmacologic treatment of neurobehavioral sequelae of traumatic brain injury. J Neurotrauma 2006;23:1468Y1501. 66. Chew E, Zafonte RD. Pharmacologic management of neurobehavioral disorders following traumatic brain injuryVa state-of-the-art review. J Rehabil Res Dev 2009:46:851Y879. 67. National Collegiate Athletic Association. NCAA banned drug list. http:// www.ncaa.org/wps/wcm/connect/public/NCAA/Health+and+Safety/Drug+ Testing/Resources. Published January 4, 2013. Accessed December 17, 2013.
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68. Fann JR, Uomoto JM, Katon WJ. Cognitive improvement with treatment of depression following mild traumatic brain injury. Psychosomatics 2001;42:48Y54. 69. Meehan WP 3rd. Medical therapies for concussion. Clin Sports Med 2011;30:115Y124 70. Echemendia RJ, Iverson GL, McCrea M, et al. Role of neuropsychologists in the evaluation and management of sport-related concussion: an inter-organization position statement. Arch Clin Neuropsychol 2012;27: 119Y122. 71. Schnadower D, Vazquez H, Lee J, et al. Controversies in the evaluation and management of minor blunt head trauma in children. Curr Opin Pediatr 2007;19:258Y264. 72. Yard EE, Comstock RD. Compliance with return to play guidelines following concussion in US high school athletes, 2005Y2008. Brain Inj 2009;23:888Y898. 73. Hollis SJ, Stevenson MR, McIntosh AS, et al. Compliance with return-toplay regulations following concussion in Australian schoolboy and community rugby union players. Br J Sports Med 2012;46:735Y740. 74. Purcell L. What are the most appropriate return-to-play guidelines for concussed child athletes? Br J Sports Med 2009;43:i51Yi55. 75. Cantu RC. Guidelines for return to contact sports after a cerebral concussion. Phys Sportsmed 1986;14:75Y83. 76. Bailes JE, Cantu RC. Head injury in athletes. Neurosurgery 2001;48:26Y45. 77. Wetjen NM, Pichelmann MA, Atkinson JL. Second impact syndrome: concussion and second injury brain complications. J Am Coll Surg 2010;211: 553Y557. 78. McCrory P, Davis G, Makdissi M. Second impact syndrome or cerebral swelling after sporting head injury. Curr Sports Med Rep 2012;11:21Y23. 79. Legislative actions dealing with concussion policy in the United States. http://www.sportsconcussions.org/links/law-and-policy.html. Accessed November 1, 2012. 80. Terrell TR, Bostick RM, Abramson R, et al. APOE, APOE promoter, and Tau genotypes and risk for concussion in college athletes. Clin J Sport Med 2008;18:10Y17.
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Sports Concussion Management: Part I Thomas R. Terrell, MD, MPhil, Timothy Nobles, BA, Brianna Rader, Kenneth Bielak, Irfan Asif, MD, Robert Casmus, BA, Jamie Yeager, BS, and Reem Hussein, BA Abstract: Concussion is a popular clinical topic that has been the subject of unprecedented recent media coverage. As concerns about the potential short- and long-term implications of repetitive head injury in sports such as football continue to mount, the proper clinical management of concussion seems to increase in importance. The days of ignoring the ‘‘ding’’ on the sideline are definitely over. A series of updated clinical evaluation and management recommendations from international experts are highlighted in this review. The clinical presentation of an acute concussion, both the typical and more subtle variations, may be evaluated with new validated sideline evaluation tools (eg, Sports Concussion Assessment Tool 2). In addition, the role of computerized neuropsychological and balance testing in the acute and ongoing evaluation are discussed, along with how they contribute to the return-to-play decision. Same-day return to play is outdated, and the relative insensitivity of current neuroimaging modalities to demonstrate structural damage is highlighted. New therapeutic interventions such as amantadine and cognitive rest may improve recovery time. The appropriate management of concussion typically results in a normal functional and neurocognitive outcome. The recommendations in this article may guide clinicians, with varying degrees of prior experience managing concussion, to increase the likelihood of an excellent outcome. Key Words: concussion, minimal traumatic brain injury, postconcussion syndrome, return-to-play
From the University of Tennessee Graduate School of Medicine, Knoxville, the Department of Physical Education and Athletics, Catawba College, Salisbury, North Carolina, and the East Tennessee State University School of Medicine, Johnson City. Reprint requests to Dr Thomas R. Terrell, Associate Professor, Department of Family Medicine, University of Tennessee Graduate School of Medicine, 1924 Alcoa Hwy, U-71, Knoxville, TN 37920. Email: [email protected] This article has been developed as a Journal CME Activity by the Southern Medical Association. Visit http://sma.inreachce.com to view instructions, documentation, and the complete necessary steps to receive CME credit for reading this article. Fees may apply. CME credit will be available for 2 years after date of publication. T.R.T. received grant funding from the National Operating Committee on Standards for Athletic Equipment, the American Medical Society for Medicine Foundation, and the University of Tennessee Physician’s Medical Education Research Fund. The opinions expressed in this article are those of the authors and not those of these organizations. The authors have no financial relationships to disclose and no conflicts of interest to report. Accepted February 19, 2013. Copyright * 2014 by The Southern Medical Association
MD, MBA,
S
port-related concussion is one of the most pressing issues in sports medicine and has received unprecedented recent media attention. A total of 1.6 to 3.8 million concussions occur in sports and recreational activities annually in the United States. The significant variability in the concussion rates reported in the literature1 and, in particular, the significant recent increase, may occur as the result of the historical underreporting of concussions; one study showed that less than half of US football players report their concussions2 and that they believe they are impervious to significant injury.3 This underreporting led to underestimates of prevalence in older data.4 The most likely cause for the increased recent prevalence stems from the increased awareness by athletes about the importance of concussion coupled with improved detection methods. Finally, the true rate may have increased, owing to changes in the game. Concussions and their improved detection and management have become the focus of attention of several international consensus conferences,5 the National Football League, the National College Athletics Association (NCAA), state legislative bodies, and the US Congress.5Y10 Several high-profile deaths attributed to improper concussion management have raised this issue to a high level of professional and public scrutiny,11 and the primary care physician is expected to follow the latest clinical management guidelines.
Key Points & Concussion is a functional disturbance and not a structural problem; therefore, clinical imaging does not add to management. & Validated acute concussion tools such as the Sports Concussion Assessment Tool 2, the postconcussion symptom score, and the Balance Error Scoring system postural evaluation provide additional objective information that aids in assessment. & A patient with an acute concussion is not to return to any physical activity on the day of the injury, and may require serial neurocognitive testing and the use of other tools to determine the appropriate point at which return to some exercise may occur. & The clinical management of acute concussion includes an enhanced focus on ‘‘cognitive rest’’ to enhance the speed and completeness of recovery.
0038-4348/0Y2000/107-115 DOI: 10.1097/SMJ.0000000000000063
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Concussion management has changed because of a number of research advances, including several validated sideline evaluation tools5 and computerized neuropsychological testing that allow a more objective evaluation of these sometimes subtle injuries. In the past, the clinician was limited to the sideline and mental status examination to evaluate an athlete with acute concussion.12 The prevention of a catastrophic outcome, such as second impact syndrome (SIS), remains the preeminent goal of proper management. SIS is a typically fatal complication that occurs in individuals with concussions who sustain additional head trauma before completely recovering from an initial concussion.13 In theory, SIS occurs because of the loss of normal cerebral autoregulation, leading to brain stem herniation and death.13 This article presents an updated review of ways to diagnose and manage a suspected concussion. We discuss the clinical evaluation and use of neuroimaging and neuropsychological testing, new sideline tools, and the latest return-to-play (RTP) guidelines.
Definition The Consensus Statement on Concussion in Sport (4th edition) provides the most up-to-date concussion definition and discusses the latest guidelines.5 Concussion is defined as a transient neurological event that occurs following a blow to or twisting of the head and may be characterized by confusion, disorientation, and retrograde (RGA) or anterograde (posttraumatic) amnesia. Headache, dizziness, fogginess, visual changes, fatigue, and nausea often occur (Table 1).14,15 Several characteristics of a concussive head injury include the following5: 1. Concussion may be caused by a direct blow to the head, face, neck, or elsewhere on the body, with an impulsive force transmitted to the head. 2. Concussion typically results in the rapid onset of short-lived impairment of neurologic function that resolves spontaneously. 3. Concussion may result in neuropathological changes, but the acute clinical symptoms largely reflect a functional disturbance rather than a structural injury. 4. 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; in a small percentage of cases, postconcussion symptoms (PCSs) may be prolonged.
Anterograde amnesia (PTA) is characterized by a significant impairment in new learning. RGA for events that occurred before the concussive event is a measure of a more severe concussion. A study by Cantu first emphasized the importance of PTA and RGA in grading concussion severity.16
Sideline Evaluation and Treatment Any individual who sustains a blow to the head and experiences any of the symptoms listed in Table 1 may have sustained a concussion. The acute evaluation focuses on determining whether a concussion or an epidural or a subdural
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Table 1. Symptoms experienced by athletes with concussion Loss of consciousness
Headache
Confusion
Pressure in head
Posttraumatic amnesia/retrograde amnesia
Vomiting
Disorientation Dizziness
Nausea Feeling as though ‘‘in a fog’’
Difficulty concentrating
Slurred speech
Difficulty remembering
‘‘Don’t feel right’’
Visual changes Balance problems Sensitivity to light or noise
Drowsiness Trouble falling asleep Nervous or anxious
Feeling slowed down
More emotional
Personality changes Fatigue or low energy
Irritability Sadness
hematoma has occurred. An on-the-field assessment includes the evaluation and management of the ABCsVAssess the situation, Be alert for signs and symptoms, Contact a healthcare professionalVbefore cognitive function is evaluated.17 After the ABCs, the mental status and focused neurological examinations are completed. Loss of consciousness carries with it the potential for an occult cervical spine (c-spine) injury; thus, precautionary c-spine immobilization is imperative in this setting. After loss of consciousness, if the athlete regains consciousness and lucidity and the physician reliably may assess for c-spine tenderness without the confounding nature of distracting pain or altered mental status, then the c-spine may be cleared. If not, then full c-spine immobilization and emergency transport for radiological evaluation is mandatory. Vital signs are monitored every 15 to 30 minutes until the athlete becomes asymptomatic. The athlete must never be left unsupervised. A stepwise approach to sideline evaluation includes the following: assess the general level of consciousness and mental status; determine the mechanism of injury and obtain clinical history from the patient and others (eg, athletic trainers, teammates); inquire about prior concussions, their severity, and timing; conduct a neurological examination by assessing mental status, cranial nerves, pupillary response, motor strength, Romberg test, and cerebellar examination; administer the Sports Concussion Assessment Tool 2 (SCAT 2; Fig. [note that the SCAT3 is the current document, which is discussed in Part II])18; and compare with any baseline scores, if available. Neuroimaging of the brain after a concussion rarely is abnormal, but it is often obtained to rule out a more serious injury. The American College of Emergency Physicians’ guidelines for ordering computed tomography (CT) scans for acute concussion19 include a prolonged disturbance of the unconscious state, a focal neurological deficit, or worsening acute symptoms.17 In addition, one may consider obtaining a CT if there are symptoms or signs of an altered sensorium suggestive * 2014 Southern Medical Association
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Fig. Sports Concussion Assessment Tool 2 (SCAT2). Validated concussion assessment instrument developed by the Third International Conference on Concussion in Sports, Zurich, 2008. Reproduced from British Journal of Sports Medicine, McCrory P, Meeuwisse WH, Johnston K, et al. 43, i76Yi84, 2009, with permission from BMJ Publishing Group Ltd. Southern Medical Journal
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Fig. (continued)
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Fig. (continued) Southern Medical Journal
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of an intracranial injury (eg subdural hematoma, epidural hematoma). The modality of choice to rule out acute intracranial injury is the noncontrast CT. Concussion is a functional disturbance rather than a structural one, and for this reason, the vast majority of CT scans on athletes with acute concussion are normal.5 A nonemergent CT scan may be indicated if PCSs worsen in the days following the injury or magnetic resonance imaging (MRI; our preference) if they persist 2 to 3 weeks after the injury. The recommendation to order an MRI is based on expert opinion, unsupported by any prospective or comparative studies. More sophisticated diffusion tensor-weighted MRI imaging20 is available at research centers, but the proper clinical interpretation and application of this type of imaging is premature. The use of functional MRI and positron emission tomography/ CT scans is limited by cost and access.21
Concussion Assessment Tools A number of validated concussion assessment tools have been developed to aid in concussion evaluation. Ultimately, concussion remains a clinical diagnosis; however, the Standardized Assessment of Concussion (SAC) has some utility in confirming an acute concussion.22 The SCAT2,5 used for injured athletes ages 10 years or older, and the SAC5,22 are validated tests to identify, diagnose, and study recovery after a concussion. They are easy to use and recognized internationally. The SCAT2, a composite of four previously validated subtests, is administered acutely and serially every few days to objectively study concussion resolution. The SCAT2 includes Maddocks Questions to assess orientation and understanding. In addition, the SAC22 tests orientation, immediate memory, concentration, and delayed recall. Finally, the Balance Error Scoring System is a validated sideline balance examination that measures equilibrium.16 It is important to obtain baseline scores for these measures to facilitate the interpretation of postconcussion results.
Neuropsychological Testing Neuropsychological (NP) testing is an objective measurement of different cognitive domains and distinctive types of cognitive function.23 The validated software most commonly used for group testing includes HeadMinder (New York, NY),24,25 ImPACT (ImPACT Applications, Pittsburgh, PA),26,27 ANAM (Vista Life Sciences, Washington, DC),28 and Cogstate/Axon (New Haven, CT).29 These programs assist athletic trainers and physicians in studying postconcussion neurocognitive recovery.5,12,14,23 Typically, collision/contact athletes (eg, football players) complete a baseline normal NP test during the preseason that is compared, if an acute concussion occurs, with postconcussion testing to evaluate neurocognitive performance and recovery over time.23 The software provides results in a format that is conducive to understanding when a return to baseline has occurred. Controversy remains as to whether NP
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testing improves clinical management or outcomes for concussed athletes; however, some asymptomatic postconcussion patients have persistently abnormal NP testing, despite appearing to be recovered. These cases further support the need for NP testing.30,31
Chronic Traumatic Encephalopathy Chronic traumatic encephalopathy (CTE) is a progressive neurodegenerative disease formerly called dementia pugilistica. A number of autopsy-proven cases in former professional collision-sport athletes32Y36 and a high school athlete37 have stimulated considerable concern and research. The clinical manifestations of CTE include progressive symptoms of memory loss; difficulty with planning, organization, and judgment, coupled with having a ‘‘short fuse;’’ mood disturbances; inappropriate behavior; and drug use.32,33 Participation in a prolonged career in collision sports causes a threefold increase in the risk of developing neurodegenerative conditions.38 Although the precise pathological mechanisms that link repeated head injuries to neurofibrillary tangles are unknown, they may involve a series of diffuse axonal injuries set in motion by the initial trauma and aggravated by subsequent mild traumatic injuries.32 CTE is characterized by tau neurofibrillary tangles, neuropil threads, and glial tangles that are found in the medial temporal lobe, often in greater densities than that seen in severe Alzheimer disease, the diencephalon, basal ganglia, and brainstem.32 Ongoing research is focused on defining the amount, mechanism, and type of cumulative brain trauma that may lead to CTE and any potential predisposing genetic/other risk factors.32,33
PCS PCS has no universally accepted definition; however, in general, it involves at least three of the following symptoms: headache, dizziness, fatigue, irritability, impaired memory and concentration, insomnia, and light sensitivity,39 which may persist for months to years. PCS typically resolves with prolonged rest. Proper management of acute concussion and the RTP decision is critical to reduce the risk of PCS. NCAA restrictions on the neurostimulant Adderall make amantadine more attractive as a medication to treat PCS. Subsymptom exercise treadmill testing is being studied as a treatment modality for refractory PCS.40,41
Management of Acute Concussion The clinician has a challenging responsibility in managing acute concussion, the severity of which is typically unknown initially. There is no universal guideline on how to treat each concussion42; each should be managed on a case-by-case basis.43,44 The Consensus Statement on Concussion in Sport,5 however, does provide some general guidance: athletes with symptoms should be removed from play and no athlete with symptoms, at rest or with exertion, should continue to play. The caveat we would add is that CT scan is helpful in instances in which the severity of the injury is unknown. * 2014 Southern Medical Association
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The sine qua non of management is to withhold an athlete with a concussion from exercise activity until symptoms are fully resolved at rest and following an exercise challenge. Several concussion symptoms overlap with other disorders, including headache from an effort headache,45 dehydration, an underlying premorbid migraine, or other disorders, thus creating diagnostic difficulties.
RTP Decisions Perhaps the most challenging decision to make is when it is safe for an athlete with a recent concussion to RTP. RTP on the same day as the acute concussion is no longer recommended because research shows incomplete neurocognitive recovery in asymptomatic acutely concussed patients and because of the risk of life-threatening SIS.30,31 An incompletely recovered athlete with a concussion who sustains a second concussion is at greater risk of prolonged recovery and/or a more severe concussion with prolonged recovery, RGA or PTA, and PCS.5,46,47 To even consider RTP, first the athlete must be asymptomatic at rest. Second, the athlete should be fully recovered neurocognitively, as measured by SCAT2, SAC, and preferably postconcussion NP testing (or most commonly, a combination of several of these measures), before being cleared to start an exercise challenge test.17,46,47 The limitations of these instruments are considerable. The SCAT2 is not validated as a composite tool, and the utility of NP testing is affected by the quality of the baseline test with which the postconcussion test is compared. Commonly used validated instruments include the SAC, the ImPACT postconcussion self-reported symptom score,26 and NP testing with HeadMinder,24 ImPACT,26,27 or Axon/Cogsport.29 The sensitivity of ImPACT is 82% and specificity is 89%, with strong intercorrelations among HeadMinder, ImPACT, and Axon/ Cogsport on subscales such as processing speed and reaction time, but not within the memory domain.48 These factors combine to make RTP a complicated decision. Same-day RTP, even following a successful exercise challenge that provoked no symptoms, is no longer allowed based on the recommendations from the American Medical Society for Sports Medicine concussion position statements.49 Recently concussed NCAA athletes may have persistent neurocognitive deficits (ImPACT score abnormal in one-third of asymptomatic athletes) despite symptom recovery.50 In addition, a study of high school football documented cognitive impairment without clinically diagnosed concussion.31 How to fully interpret this study and its impact on clinical management is evolving, but cautious RTP is the norm. Some clinicians are using graduated exercise on a treadmill to rehabilitate patients who have sustained a concussion or those with PCS. The authors suggest that an abnormal heart rate response to exercise may be treated with a gradual progressive increase in treadmill exercise intensity, although the need remains for prospective Southern Medical Journal
outcome studies comparing different protocols for concussion groups.40
Cognitive Rest The symptomatic athlete with acute concussion benefits from a period of cognitive rest that includes restriction from schoolwork, extensive reading, texting, loud environments, and playing video games.51 Bed rest is unnecessary and may actually be harmful.52 The limited research suggests that the ideal amount of cognitive rest remains to be determined.53,54 Proper management of the academic demands on a concussed patient is critical for normal recovery.
Pharmacological Interventions in Concussion Clinicians may use pharmacological therapy to treat acute and persistent symptoms. No effective pharmacological treatment speeds recovery from traumatic brain injury (TBI).55 Clinicians experienced in concussion management may prescribe medications that modify the underlying pathophysiology of the concussion, the goal being to shorten symptom duration. Tylenol or nonsteroidal anti-inflammatory drugs are helpful for acute postconcussion headache, but they may lead to rebound headache and are not recommended.56 Medications also may treat associated sleep dysfunction, headaches arising from cognitive fatigue, persistent dizziness, and attention difficulties. The use of sleeping agents such as melatonin, trazodone, or nonbenzodiazepine sleeping agents such as zolpidem or tricyclic antidepressants is permitted, but benzodiazepines should be avoided because of potential memory impairment.57Y59 Neurobehavioral symptoms may be treated with medication. Amantadine has been proven effective in improving arousal in severe TBI cases60 and has been studied in sports concussion.61 Some studies show that it improves executive function in pediatric patients,62 but other small studies show no improvement in the NP scores of subjects taking amantadine versus placebo.63 Typically, a 3-week trial of amantadine is adequate to determine its efficacy. Neurostimulants such as methylphenidate have been proven by randomized controlled trials to assist in TBI treatment,64 particularly in treating deficits in attention and speed of processing and general cognitive functioning65; however, some studies have shown them to be ineffective.66 They should be considered carefully on a caseby-case basis. If the athlete is an NCAA player, the organization must be notified in writing of any stimulant use because stimulants are banned substances.67 For depression that develops following TBI, the use of selective serotonin reuptake inhibitors such as sertraline68 is beneficial, according to Meehan and colleagues.69
RTP NP may provide additional objective data to help clinicians evaluate postconcussion neurocognitive recovery and to recommend appropriate timing for safe RTP.70 The ultimate utility
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Table 2. Concussion modifier Factors
Modifier
Symptoms
Number Duration (910 d) Severity Prolonged loss of consciousness (91 min)
Signs
Amnesia Sequelae
Concussive convulsions
Temporal
Frequency: repeated concussions over time Timing: injuries close together in time Recency: recent concussion or TBI
Threshold
Repeated concussions occurring with progressively less impact force or slower recovery after each successive concussion
Age
Child and adolescent (younger than 18 y)
Comorbidities and premorbidities
Migraine Depression or other mental health disorders Attention-deficit/hyperactivity disorder Learning disabilities Sleep disorders
Medication
Psychoactive drugs Anticoagulants
Behavior
Dangerous style of play
Sport
High-risk activity Contact and collision sport High sporting level
TBI, traumatic brain injury. Data adapted from BMJ Publishing Group Ltd.5
of NP in assisting clinicians in making final RTP decisions remains subject to debate, although the Zurich statement made it clear that NP testing should be understood as a clinical decisionmaking tool to be used in conjunction with numerous clinical domains and investigational results.5 When the concussed
patient becomes asymptomatic, he or she should undergo a postconcussion NP test. If the postconcussion NP scores are within 1 standard deviation of baseline, then it may be safe from a neurocognitive recovery standpoint to recommend the graduated exercise progression protocol that is successfully completed before RTP. Consideration of clinical parameters always is crucial, and NP testing should not be used in isolation to decide upon RTP. Research also supports NP testing. For instance, some studies demonstrate that asymptomatic athletes with recent concussion may show persistent neurocognitive deficits that extend several days or weeks.31,50 RTP guidelines continue to become more conservative. Additional factors to consider when weighing the safe RTP include whether the subject has any history of concussion modifiers5 (Table 2) that may prolong recovery time or has sustained several concussions in the preceding weeks or months. Finally, a history of severe concussion with a prolonged recovery time of 92 months or of multiple severe concussions are scenarios that dictate a more conservative approach to RTP. Once postconcussion symptoms have resolved, the athlete must successfully complete a sequential, graduated exercise program in a 5- to 7-day period before he or she may be cleared for RTP (Table 3).5 This approach should reduce the risk associated with premature return to activity.71 Of particular importance, if any symptoms recur during the exercise challenge, the athlete should stop at this level of activity and not resume activity until he or she is asymptomatic for 24 hours.5 The athlete should then step down to a lower level of physical activity and restart the process. After one successful day at that exercise activity level, the patient may advance to a more intensive form of exercise. The graduated exercise challenge may be managed effectively by athletic trainers under the direction of a medical provider. Studies on the adherence to published RTP guidelines show that compliance is not always high. Athletic trainers reporting on the Internet on concussed high school athletes showed that compliance with RTP guidelines was not attained
Table 3. Graduated return-to-play protocol Rehabilitation stage
Functional exercise at each rehabilitation stage
Objective of each stage
1: No activity
Complete physical and cognitive rest
Recovery
2: Light aerobic exercise
Walking, swimming, or stationary cycling, keeping intensity 970% maximum predicted heart rate
Increase heart rate
3: Sport-specific exercise
No resistance training Skating drills in ice hockey, running drills in soccer
Add movement
No head-impact activities 4: Noncontact training drills
Progression to more complex training drills (eg, passing drills in football and ice hockey)
Exercise, coordination, and cognitive load
May start progressive resistance training 5: Full contact practice
Following medical clearance, participate in normal training activities
6: Return to play
Normal game play
Restore confidence and assess functional skills by coaching staff
Data adapted from BMJ Publishing Group Ltd.5
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in 40% of cases.72 Another study showed that 78% of rugby players with concussions did not receive any RTP guidelines.73
Children and Adolescents RTP decisions are much more conservative for concussed athletes in elementary and middle school because their brains are still developing. They should be held out of any physical activity until they are asymptomatic at rest for at least 1 week.74
Multiple Concussions The management of individuals who sustain multiple concussions in a given year is a complicated process because of the absence of prospective outcome data on which to rely to develop evidence-based guidelines. The classic Cantu RTP recommendations, following a single concussion or multiple concussions in the same year, remain the mainstay of treatment.75 We suggest discussing these cases with a primary care sports medicine physician, neurologist, or neurosurgeon who specializes in sports concussion. No arbitrary number of concussions has been established after which an athlete should stop participating in all collision sports. It is important to carefully evaluate the severity of each individual concussion, any secondary modifying factors, and formal pencil-and-paper neuropsychological testing rather than focusing solely on the total number of historical concussions. A family conference involving the key parties may be helpful to make these difficult decisions. Clinicians must consider having discussions with recurrently concussed athletes on modification to a noncollision sport or even retirement.76
SIS SIS occurs when an individual who has recently sustained a head injury but has not recovered completely from it experiences an additional, typically milder, head injury that leads to a life-threatening syndrome. The person with SIS typically collapses, experiencing dilated pupils and labored respirations as the cerebellum herniates through the foramen magnum; typically, 50% of individuals with SIS die.13,77 A group of researchers in Australia question the existence of SIS,78 but it is fully accepted as a clinical entity in most of the world.
Conclusions The Appendix provides a summary of educational resources for concussion management. Legislation (eg, the Zackery Lystedt law) that requires a physician or designee (usually an athletic trainer) to clear any concussed athlete before RTP has been passed by 940 states.79 Some investigators are studying whether genetic factors may increase concussion risk. A cross-sectional study of 178 college athletes showed a 2.7-fold increased risk of self-reported prior concussion for participants with the APOE G-219T TT genotype.80 Additional discussion of this work and other current research on concussion appears in the second article of this series (see page 126). Southern Medical Journal
The dissemination of new scientific research on concussion has increased dramatically in recent years. Consequently, the practicing clinician has more research-derived clinical guidelines for the management of concussion and a more extensive set of sideline and bedside evaluation tools. A proper assessment of acute symptoms, supplemented by sideline tools such as the SCAT2, SAC, and NP testing, provides more extensive information with which a physician may make clinical decisions. The expansion of baseline and postconcussion NP testing provides an objective evaluation of neurocognitive recovery that supplements the more subjective follow-up of self-reported symptom resolution. Concerns about the timing of full neurocognitive recovery that may follow symptom resolution have eliminated the practice of same-day RTP following concussion; however, a timely RTP is still possible for asymptomatic patients who pass a graduated exercise challenge protocol.
Acknowledgments The authors thank Victoria Coy and Gregory Nichols for assistance in the preparation of the article.
Appendix: Concussion Management Resources & Acute Concussion Evaluation (ACE) Care Plan: http:// www.cdc.gov/concussion/HeadsUp/physicians_tool_kit.html. & American Medical Society for Sports Medicine position statement: See Reference 15. & American Medical Society for Sports Medicine Webinar on concussion: http://www.amssm.org/AMSSMNewsConcussionWebinar.php. & Heads Up Concussion in Youth Sports Concussion Toolkit: Includes free coaches training for youth sports (http://www. cdc.gov/concussion/HeadsUp/physicians_tool_kit.html). & www.Boksmart.com: Developed by South African physicians to educate teenage rugby players, coaches, and parents. Compulsory biennial online training required of coaches/ referees. & Hockey Canada Concussion App for iPhone: http://www. hockeycanada.ca/en-ca/Hockey-Programs/Safety/ Concussions.aspx. & Cantu R, Hyman M. Concussions and Our Kids. Boston: Houghton Mifflin Harcourt; 2012.
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