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Sports-Related Concussion
Abstract: Concussion is a common injury that emergency medicine physicians will be called upon to evaluate. A comprehensive history and physical examination, cognitive evaluation, and balance testing are important in the assessment of a head injury. Assessment tools have been developed and are widely available. Their inclusion in the initial evaluation of suspected concussion may aid diagnosis and management. Athletes should never be allowed to return to play on the same day they suffer a concussion. Follow-up with a primary care physician, sports medicine specialist, or neurologist is recommended before return to play. Accurate anticipatory guidance has been shown to be beneficial in concussion recovery and can be instituted in the emergency department setting. Familiarity with legislation within your state is important in understanding the regulations for medical clearance for return to play for competitive athletes.
Sports-Related Concussion Bradley C. Weinberger, MD, Susannah M. Briskin, MD
C
oncussion is a form of mild traumatic brain injury (TBI) that results when a direct blow to the head, neck, face, or elsewhere on the body produces biomechanical forces that are subsequently transmitted to the brain. It usually results in rapid onset of signs, symptoms, and neurologic impairment, which typically resolve spontaneously. Although the pathophysiology of concussion is not yet completely understood, it is currently theorized to be a functional disturbance that is due to a complex metabolic cascade that occurs within the brain as a result of trauma. Typically, no structural disturbance can be visualized on advanced imaging. 1,2 Resolution of signs and symptoms occurs in less than 10 days for 80% to 90% of individuals who suffer a concussion. However, children and adolescents are more likely to have a delayed recovery beyond 10 days. 3
Keywords: head injury; mild traumatic brain injury; adolescents; athletes
Division of Pediatric Sports Medicine, Rainbow Babies and Children's Hospital, University Hospitals Case Medical Center, Cleveland, OH. Reprint requests and correspondence: Susannah Briskin, MD, c/o Jill Walker, UH Solon Medical Center, Solon Centre Pointe, 34055 Solon Rd, Suite 202, Solon, OH 44139. [email protected] (B.C. Weinberger), [email protected] (S.M. Briskin) 1522-8401/$ - see front matter © 2013 Elsevier Inc. All rights reserved.
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EPIDEMIOLOGY Each year an estimated 1.6 to 3.8 million sports-related concussions occur in the United States, with most individuals not seeking medical care. 4 Within the last decade, there has been a 62% increase in the number of children and adolescents presenting to an emergency department (ED) for sports- and recreation-related TBI. 5 Media attention and improved awareness and recognition of concussion have likely contributed to a dramatic increase in the number of individuals presenting for medical evaluation and management of suspected head injuries. From 1997 to 2008, Lincoln et al 6 collected data showing an overall annual increase in concussion rate of 16.5% in high school athletes. At the high school level, the overall concussion rate is 2.4 to 2.5 per 10 000 athletic exposures (AEs). An AE is defined as 1 athlete participating in 1 practice or competition. 6,7 Marar et al 7 studied high school athletes across all sports and found consistently higher concussion rates in competition than in practices. Overall, boys have a total concussion rate almost 2 times that of girls (3.1 vs 1.6 per 10 000 AEs). This is because essentially only boys play football, which is the sport that accounts for the largest number of
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concussions. However, in gender comparable sports (ie, boy's vs girl's soccer), girls have a total concussion rate almost 2 times that of boys, 1.7 vs 1.0 per 10 000 AEs (Table 1). 7
DIAGNOSIS The 4th International Conference on Concussion in Sport was held in Zurich in November 2012, and proceedings from this meeting have been published in both the Clinical Journal of Sports Medicine and the British Journal of Sports Medicine and represent a revision and update of the recommendations developed following the 1st (Vienna 2001), 2nd (Prague 2004), and 3rd (Zurich 2008) International Consensus Conferences. These most recent guidelines are commonly referred to as the Zurich guidelines. From these meetings, the following consensus definition of concussion was established: concussion is a brain injury and is defined as a complex pathophysiological process affecting the brain, induced by biomechanical forces. Several common features that incorporate clinical, pathologic, and biomechanical injury constructs that may be used in defining the nature of a concussive head injury include the following: 1. Concussion may be caused either by a direct blow to the head, face, neck, or elsewhere on the body with an “impulsive” force transmitted to the head. 2. Concussion typically results in the rapid onset of short-lived impairment of neurologic function that resolves spontaneously. How-
TABLE 1. Concussion rates in high school athletics. 6,7 Sport
Rate per 10 000 Athletic Exposures
Football Boys' ice hockey Boys' lacrosse Girls' lacrosse Girls' soccer Boys' wrestling Girls' field hockey Girls' basketball Boys' soccer Boys' basketball Girls' softball Boys' baseball
6.0-6.4 5.4 3.0-4.0 2.0-3.5 3.4-3.5 1.7-2.2 1.0-2.2 1.6-2.1 1.7-1.9 1.0-1.6 1.1-1.6 0.5
ever, in some cases, symptoms and signs may evolve over a number of minutes to hours. 3. Concussion may result in neuropathological changes, but the acute clinical symptoms largely reflect a functional disturbance rather than a structural injury, and as such, no abnormality is seen on standard structural neuroimaging studies. 4. Concussion results in a graded set of clinical symptoms that may or may not involve loss of consciousness (LOC). Resolution of the clinical and cognitive symptoms typically follows a sequential course. However, it is important to note that, in some cases, symptoms may be prolonged.1 It is important to note that the diagnosis of concussion is clinical and relies on patient-reported symptoms. Physical examination frequently reveals deficits in balance and cognitive function; however, it may also be normal. Because of their limited clinical utility in predicting prognosis, previously published concussion grading scales were abandoned in 2008. 8
SYMPTOMS The symptoms of concussion are numerous and can be grouped into 4 categories: physical, cognitive, emotional, and sleep (Table 2). The most commonly reported symptom in concussion is headache, with dizziness as the next most common. 9,10 Headache is frequently bilateral but may be unilateral and is often exacerbated by bright light and loud noise. Loss of consciousness only occurs in 10% of concussions but, when prolonged, may indicate a need for neuroimaging to rule out structural injury. 7,10 The presence of amnesia, which may be either retrograde (preceding the injury) or anterograde (after the injury), may be predictive of longer recovery time. 11,12 Dizziness at the time of injury and total number and severity of symptoms have also been associated with prolonged recovery. 9,13 Cognitive impairment after concussion may be dramatic but is more commonly subtle. Athletes may be confused about recent events, answer questions slowly, or may even repeat questions. Sleep disturbance is common in concussion, although athletes will typically complain of fatigue and sleeping more than usual acutely after concussion. 11 Athletes often have difficulty recognizing concussion symptoms and, therefore, may be less likely to accurately report probable concussion. In the acute stage, concussion should be seen as an evolving injury. Symptom onset may not occur or be
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TABLE 2. Signs and symptoms of sport-related concussion. 1 Physical
Cognitive
Headache
Feeling mentally “foggy” Feeling slowed down Difficulty concentrating Difficulty remembering Forgetful of recent information Confused about recent events Answers questions slowly Repeats questions
Nausea Vomiting Balance problems Dizziness Visual problems Fatigue Sensitivity to light Sensitivity to noise Numbness/ tingling Dazed Stunned
Emotional Irritability
Sleep Drowsiness
Sadness
Sleeping more than usual More Sleeping less emotional than usual Nervousness Difficulty falling asleep
Data from Br J Sports Med 2013;47(5):250-8.
recognized for several hours or days after the injury, thereby making concussion recognition challenging. 8,14 In addition, athletes may be likely to ignore the symptoms of concussion. A 2004 study of high school football players found less than half of all probable concussions were reported in a given season. Reasons for not reporting included a desire to avoid restriction from sports, a self-judgment that symptoms were not severe enough to warrant attention, and a lack of awareness that symptoms indicate a probable concussion. 15 Symptom scales (Figure 1) allow patients to grade symptom severity. More importantly, athletes are more likely to report symptoms when completing a symptom scale than when asked via interview; hence, use of a symptom scale appears to improve diagnostic accuracy.
ASSESSMENT Any athlete suspected of suffering a concussion should be removed from the field of play and assessed, ideally, by a health care professional with experience in concussion management. 16 Any athlete found
unconscious after head or neck trauma should be assumed to have a cervical spine injury, and neck stabilization should be maintained until cleared. In this case, the initial evaluation should focus on the athlete's airway, breathing and circulatory function, and evaluation for cervical spine injury. Emergency transfer is indicated if a cervical spine injury cannot be excluded or if there are signs of a more serious neurologic injury (eg, focal neurologic examination, Glasgow Coma Score [GCS] ≤ 14, etc). 16 For less emergent injuries, the athlete can undergo serial examinations on the sideline or, if no health care provider is available for assessment, referred urgently for evaluation. The evaluation of an athlete with a possible concussion in the ED should include a comprehensive history and head/neck and neurologic examination, including mental status, cognitive function and balance, and determination of the need for neuroimaging. 16 A number of sideline assessment tools have been developed to allow a standardized approach to concussion evaluation and are frequently used in the office setting. The Standardized Assessment of Concussion (SAC) is a tool that measures cognitive function by evaluating orientation, memory (immediate and delayed), and concentration (see Appendix). It is worth noting that traditional orientation questions (eg, person, place, time) have been shown to be unreliable in sports-related concussion. 17,18 Although the SAC has shown good sensitivity and specificity in the diagnosis of concussion in older teenagers and young adults, its validity has not been demonstrated in younger children. 11,19 Ideally, athletes undergo preseason testing to obtain baseline SAC scores. In 1 study of high school football players, the average baseline score of nonconcussed controls was 25.6 of a possible total score of 30. 18 After a suspected concussion, athletes are retested, and the results, compared to their baseline. In a study of high school and collegiate athletes, a decline of 1 point or greater from baseline resulted in a sensitivity of 94% and specificity of 76% for concussion diagnosis. 20 In adults presenting to the ED with head injury, the SAC appears to be sensitive in concussion diagnosis. 21 However, a recent study of pediatric ED patients found a graded symptom checklist to be more sensitive than the SAC in concussion diagnosis. 22 Although SAC scores trended lower for concussed patients, the difference was not significant. Of note, SAC scores for nonconcussed controls younger than 12 years were significantly lower (age 9-11 years: SAC, 22.7; age 6-8 years: SAC 17.7) than those typically seen in nonconcussed high school athletes. 22
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Figure 1. Postconcussion Symptom Scale.
The Balance Error Scoring System (BESS) is a validated tool for measuring postural stability, which is frequently impaired in those with concussions. The patient is timed in 3 different stances (double leg, single leg, and tandem) for 20 seconds each on both a flat surface and a piece of mediumdensity foam. The total number of errors (eg, lifting hands off hips, stumbles, eye openings, etc) is summed to provide an overall score, which can be compared to a patient's baseline, if available, or published norms (11.0 + 5.1 for adults and 17.6 + 7.5 for children 10-17 years old). 23-25 The modified BESS eliminates the foam portion of the test and is often used on the sidelines or in office or ED settings. Overall, balance tends to recover quickly, typically within 3 to 7 days of injury. 23 The Sports Concussion Assessment Tool 3 (SCAT3) was released in the most recent Zurich statement and consists of a graded symptom checklist, the GCS, the Maddocks Questions, the SAC, and the BESS. The Maddocks questions (Table 3) have been shown to be more sensitive than standard questions of orientation (eg, What is your name?
What day is it?) in identifying possible concussion in the sports setting. 17 For the first time, the 2012 Zurich consensus statement included a Child-SCAT3 to aid in the assessment of concussion in children ages 5 to 12 years. 1 It includes a child and parent report of symptoms as well as a more basic version of the SAC and BESS. The SCAT3 is designed to be easy to administer with completion in 10 minutes or less.
TABLE 3. Maddocks questions from SCAT3/Child-SCAT3. Modified Maddocks Score What venue are we at today? Which half is it now? Who scored last in this match? What team did you play last week/game? Did your team win the last game?
Child-Maddocks Score Where are we at now? Is it before or after lunch? What did you have last lesson/class? What is your teacher’s name?
Data from Br J Sports Med 2013;47(5):250-258.
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Both versions of the SCAT3 are freely available to download (see Appendix). The inclusion of multiple assessment tools in the SCAT3 may increase the sensitivity and specificity of concussion diagnosis; however, there have not yet been any studies to validate it for diagnosing concussion. 16 Emerging tools in the assessment of concussion include quantitative electroencephalogram, functional neuroimaging (including functional magnetic resonance imaging, magnetoencephalography, and positron emission technology), and head impact sensors. Although some of these technologies show promise, their clinical utility has yet to be established. 26 Therefore, at this time, diagnosis remains a clinical one, supported by history, a comprehensive physical examination, and added assessments of cognitive function and balance.
NEUROIMAGING Neuroimaging is typically normal, and therefore, not indicated in most athletes with concussion. It should be reserved for those patients suspected of having a more severe head injury. 1,27 Computed tomography (CT) is more sensitive than magnetic resonance imaging in the identification of skull fracture and intracerebral hemorrhage or contusion in the first few days after injury. Magnetic resonance imaging is more helpful in the identification of preexisting pathology (eg, Chiari malformation, arteriovenous malformation, etc) that could cause worsening or prolonged symptoms. 16 The decision of whether a patient with an acute brain injury requires neuroimaging can be a difficult one. A recent prospective cohort study by the Pediatric Emergency Care Applied Research Network attempted to identify clinical factors associated with a low risk of clinically important traumatic brain injury (TBI) in children with head trauma. For children age 2 years and older, the following factors were identified as predictive of a low risk of structural brain injury: normal mental status, no LOC, no vomiting, nonsevere injury mechanism, no signs of basilar skull fracture, and no severe headache. This prediction rule demonstrated sensitivity of 96.8% and a negative predictive value of 99.95%. Altered mental status, GCS of 14 or less, and signs of a basilar skull fracture were most predictive of clinically important TBI (4.3% risk). Computed tomography was recommended for patients presenting with any of those predictors (Table 4). Observation without CT was recommended for those patients with a history of LOC, vomiting, severe mechanism of injury, or severe headache with normal mental status and no signs of basilar skull fracture. 28 If imaging is not obtained,
TABLE 4. Clinical predictors of clinically important TBI (indications for obtaining CT). CT Recommended GCS ≤ 14 Other signs of altered mental status Agitation Somnolence Repetitive questioning Slow response to verbal communication Signs of basilar skull fracture Battle's sign: retroauricular bruising Raccoon eyes: periorbital bruising Hemotympanum CSF otorrhea or rhinorrhea
Observation History of LOC History of vomiting
Severe mechanism of injury
Severe headache Data from Lancet 2009;374:1160-70.
anticipatory guidance should be given before discharge regarding symptoms and signs concerning intracranial bleeding, including worsening mental status or headache and persistent vomiting, which warrant return to the ED for re-evaluation.
MANAGEMENT Following initial evaluation, the implementation of cognitive and physical rest is considered the “cornerstone” of concussion management. 1 Physical rest is recommended to avoid symptom exacerbation and prolongation and to minimize the risk of a second head injury. If a second head injury is sustained before symptoms associated with the first have fully cleared, there is a risk for diffuse cerebral swelling, a rare condition that is more common in children than in adults and frequently fatal. Physical rest includes not only organized sports activities but also any activity or exercise that elevates the heart rate or poses risk of additional head injury. Cognitive rest includes time off from school or work, no homework or reading, no screen time (eg, television, computers, video games, smart phones), and increased rest or sleep. Evidence for these recommendations is limited, although a recent study of high school and collegiate athletes demonstrated the efficacy of physical and cognitive rest in the resolution of symptoms and cognitive dysfunction. 29 Although most athletes recover from concussion in 1 to 2 weeks, studies have shown longer recovery times in younger vs older athletes. 8,30 School-aged athletes often need academic accommodations in
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place when they return to school (eg, extra time to complete tests/assignments, preferential seat placement in class, avoidance of computer screens, note taker, reduced workload). 31 Medications may be used to manage postconcussive signs and symptoms when prolonged, although evidence supporting their usage is limited. In the acute setting, acetaminophen may be recommended for headache, although typically is not effective for concussion headaches. Nonsteroidal anti-inflammatory drugs and aspirin are not recommended due to the theoretical risk for bleeding. 16 Chronic postconcussion symptoms typically targeted for pharmacologic therapy include nausea, sleep disturbance, chronic headache, depression and anxiety (antidepressants), and cognitive dysfunction (stimulants). A recent survey of pediatric providers found that most (89%) of the respondents used medications to manage concussed patients with prolonged symptoms. Nonprescription medications, specifically acetaminophen, nonsteroidal anti-inflammatory drugs, and melatonin, were most frequently used, whereas prescription medications, including antidepressants and stimulants, were used less frequently. 32 In general, narcotic use should be avoided as it makes it challenging to properly assess the mental status of the concussed individual.
Return to Activity The most recent Zurich guidelines recommend that return to play after concussion should be individualized to the athlete and his or her particular injury. 16 No athlete with a suspected concussion should be allowed to return the same day. Return-to-play protocols should only begin when athletes are symptom free at rest for a minimum of 24 hours and have a normal physical examination, and when cognitive function has returned to baseline. It is recommended that no child or adolescent athlete attempts a return to organized sports until they have returned to full participation in school successfully. 1 Determination of when an athlete may return to activity requires follow-up with the primary care physician, sports medicine physician, or neurologist with experience in managing concussions. 16 Because it is impossible to predict how long an individual's symptoms will last, an exact time frame for return to play cannot be given in the ED. Follow-up also provides an opportunity for education regarding concussion prevention and typical recovery patterns, which may reduce anxiety and aid symptom resolution. 33 In some cases, computerized neuropsychological testing may be performed at the follow-up visit to
determine whether cognitive function has normalized; however, it has not been shown to be useful in the ED setting in predicting recovery. 34,35 A typical return-to-play protocol is listed in Table 5. Athletes follow a stepwise, progressive increase in the amount and intensity of exercise; any return of symptoms leads to a stop in the progression and a return to the stage at which they were last symptom free. Return to practice or competition should only occur after final clearance by a health care provider with experience in managing concussions. 1 Returnto-play protocols may need to be lengthened for the pediatric athlete. 36
PREVENTION Protective Equipment Helmets are a crucial part of protective equipment in many sports. Within alpine sports and bicycle riding, helmets have been proven to reduce moderate to severe brain injuries. 37-39 In American football, the hard shell helmet design was initially developed to decrease the force of a strong linear acceleration that was thought to put an individual at risk for skull fractures and cerebral bleeds. 40 However, there is a lack of clinical evidence to prove that helmets can reduce the risk of concussion. Although laboratory studies show that impact forces to the brain can be reduced with some
TABLE 5. Return-to-play protocol. 1 Rehabilitation Stage Day 1: Light aerobic exercise Day 2: Sportspecific exercise Day 3: Noncontact training drills Day 4: Fullcontact practice Day 5: Return to play
Exercise Aerobic exercise HR b 70% maximum Running drills in football Passing drills in soccer
Objective Increase HR Add movement Exercise, coordination, and cognitive load
Normal training Restores confidence, activities, resistance allows evaluation by training coaching staff Competition
Return-to-play protocol may begin after patient has been symptom free for at least 24 hours and physical and neurocognitive examinations are normal. If symptoms recur, patient should rest for a minimum of 24 hours and until symptoms are resolved before reattempting that day's activity. Data from Br J Sports Med 2013;47(5):250-8.
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headgear and helmets, there is no evidence to prove a reduction in concussion incidence. 1 Although linear forces can cause a concussion, it is the angular forces to the head that produce rotational acceleration, which is thought to be the primary mechanism of injury for concussion. 41 Mouthguards are frequently worn protective gear in many sports. There is strong evidence that wearing a mouthguard decreases the risk of suffering dental trauma; however, there is a paucity of data to support wearing a mouthguard to decrease concussion risk or severity. 42
Rule Changes Several sports-governing bodies have implemented rule changes to eliminate or decrease specific contact that may place an individual at greater risk for suffering a concussion. Identification of an injury mechanism that increases concussion risk is the initial step in deciding how to formulate rule changes. For instance, youth hockey studies have shown that athletes were more likely to suffer a concussion in leagues where body checking was permitted. 43,44 Subsequently, USA Hockey and Hockey Canada have both raised their minimum body checking age to 13 years old. 45 Similarly, in 2012, Pop Warner football began limiting the amount of contact in practices and eliminating all head-on, full-speed tackling drills after research demonstrated that second graders take more than 100 hits to the head during a football season, some with a force equal to concussion-inducing impacts that were measured in adults. 46,47 In 2011, the National Football League changed its kickoff rule by moving the spot of the kickoff 5 yards closer to the opposite goal line. The following season, the number of concussions during kickoffs fell from 35 to 20, a decline of 43%. 48
LEGISLATION Legislation aimed at improving concussion education and identification began in the State of Washington in May 2009 when the Zachary Lystedt Law was passed. The law was named after a 13-yearold football player who sustained a head injury and returned to play in the same game. He subsequently developed recurrent intracerebral hemorrhages and required emergency surgery. Zachary's injury resulted in significant neurologic injury and disabilities. 49 As of May 2013, 48 states plus the District of Columbia have passed concussion legislation. Although variation exists state to state, most states incorporate the 3 main principles of legislation set forth by the Lystedt Law (no concussion legislation
as of yet in Mississippi, legislation in Wyoming does not incorporate the tenets of the Lystedt Law). These include (1) education for youth athletes and their parents, (2) removal of an athlete from sports if they appear to have suffered a concussion, and (3) evaluation and written clearance of that athlete by a licensed health care professional before their return to play. 50 State-specific information can be found at www.nflevolution.com. The effects of the concussion legislation on concussion rates are not yet clear. However, studies about the free online educational CDC “Heads Up” program (see Appendix) have demonstrated improved concussion knowledge among high school coaches and improved concussion management by physicians. 51-53
SUMMARY Concussion is a common injury that ED physicians will be called upon to evaluate. A comprehensive history, physical examination, cognitive evaluation, and balance testing are important in assessing an individual with a head injury. Initial treatment for a concussion is physical and cognitive rest until symptoms are significantly improved. Athletes should never be allowed to return to play on the same day they suffer a concussion. Follow-up with a primary care physician, sports medicine specialist, or neurologist with experience in managing concussions is recommended before return to activity. A formal return-to-play progression should not begin until an athlete is asymptomatic for a minimum of 24 hours. Familiarity with legislation within your state is important for understanding the necessary rules for clearance for return to play for athletes.
APPENDIX SAC link: http://www.ncbi.nlm.nih.gov/pmc/articles/ PMC155418/ SCAT3 links: http://bjsm.bmj.com/content/47/5/259.full.pdf http://bjsm.bmj.com/content/47/5/263.full.pdf Child SCAT3 CDC “Heads Up” Program: http://www.cdc.gov/concussion/HeadsUp/youth.html BESS link: http://www.sportsconcussion.com/pdf/ management/BESSProtocolNATA09.pdf
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42. Labella CR, Smith BW, Sigurdsson A. Effect of mouthguards on dental injuries and concussions in college basketball. Med Sci Sports Exerc 2002;34:41–4. 43. Macpherson A, Rothman L, Howard A. Body-checking rules and childhood injuries in ice hockey. Pediatrics 2006;117: e143–7. 44. Emery CA, Kang J, Shrier I, et al. Risk of injury associated with body checking among youth ice hockey players. JAMA 2010;303:2265–72. 45. The Globe and Mail. Hockey Canada's older bodychecking age sends a message that children's safety is paramount. Available at: http://www.theglobeandmail.com/commentary/ editorials/hockey-canadas-older-bodychecking-age-sends-amessage-that-childrens-safety-is-paramount/article 12174920/. Accessed June 14, 2013. 46. The New York Times. Trying to reduce head injuries, youth football limits practices. Available at: http://www.nytimes.com/ 2012/06/14/sports/pop-warner-football-limits-contact-inpractices.html?_r=0. Accessed June 14, 2013. 47. Daniel RW, Rowson S, Duma SM. Head impact exposure in youth football. Ann Biomed Eng 2012;40:976–81.
48. The Washington Post. Concussions in NFL down from last season because of kickoff rule change, study finds. Available at: http://articles.washingtonpost.com/2012-08-07/sports/ 35494074_1_kickoff-rule-concussions-nfl-players. Accessed September 5, 2013. 49. Adler RH. Youth sports and concussions: preventing preventable brain injuries. One client, one cause, and a new law. Phys Med Rehabil Clin N Am 2011;22:721–8, ix. 50. NFL Evolution. Concussion Legislation by State. Available at: http://www.nflevolution.com/article/Concussion-Legislationby-State?ref=767. Accessed June 14, 2013. 51. Covassin T, Elbin RJ, Sarmiento K. Educating coaches about concussion in sports: evaluation of the CDC's “Heads Up: concussion in youth sports” initiative. J Sch Health 2012;82:233–8. 52. Sarmiento K, Mitchko J, Klein C, et al. Evaluation of the centers for disease control and prevention's concussion initiative for high school coaches: “Heads Up: concussion in high school sports”. J Sch Health 2010;80:112–8. 53. Chrisman SP, Schiff MA, Rivara FP. Physician concussion knowledge and the effect of mailing the CDC's “Heads Up” toolkit. Clin Pediatr 2011;50:1031–9.
Sports-Related Concussion Bradley C. Weinberger, MD, Susannah M. Briskin, MD
C
oncussion is a form of mild traumatic brain injury (TBI) that results when a direct blow to the head, neck, face, or elsewhere on the body produces biomechanical forces that are subsequently transmitted to the brain. It usually results in rapid onset of signs, symptoms, and neurologic impairment, which typically resolve spontaneously. Although the pathophysiology of concussion is not yet completely understood, it is currently theorized to be a functional disturbance that is due to a complex metabolic cascade that occurs within the brain as a result of trauma. Typically, no structural disturbance can be visualized on advanced imaging. 1,2 Resolution of signs and symptoms occurs in less than 10 days for 80% to 90% of individuals who suffer a concussion. However, children and adolescents are more likely to have a delayed recovery beyond 10 days. 3
Keywords: head injury; mild traumatic brain injury; adolescents; athletes
Division of Pediatric Sports Medicine, Rainbow Babies and Children's Hospital, University Hospitals Case Medical Center, Cleveland, OH. Reprint requests and correspondence: Susannah Briskin, MD, c/o Jill Walker, UH Solon Medical Center, Solon Centre Pointe, 34055 Solon Rd, Suite 202, Solon, OH 44139. [email protected] (B.C. Weinberger), [email protected] (S.M. Briskin) 1522-8401/$ - see front matter © 2013 Elsevier Inc. All rights reserved.
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EPIDEMIOLOGY Each year an estimated 1.6 to 3.8 million sports-related concussions occur in the United States, with most individuals not seeking medical care. 4 Within the last decade, there has been a 62% increase in the number of children and adolescents presenting to an emergency department (ED) for sports- and recreation-related TBI. 5 Media attention and improved awareness and recognition of concussion have likely contributed to a dramatic increase in the number of individuals presenting for medical evaluation and management of suspected head injuries. From 1997 to 2008, Lincoln et al 6 collected data showing an overall annual increase in concussion rate of 16.5% in high school athletes. At the high school level, the overall concussion rate is 2.4 to 2.5 per 10 000 athletic exposures (AEs). An AE is defined as 1 athlete participating in 1 practice or competition. 6,7 Marar et al 7 studied high school athletes across all sports and found consistently higher concussion rates in competition than in practices. Overall, boys have a total concussion rate almost 2 times that of girls (3.1 vs 1.6 per 10 000 AEs). This is because essentially only boys play football, which is the sport that accounts for the largest number of
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concussions. However, in gender comparable sports (ie, boy's vs girl's soccer), girls have a total concussion rate almost 2 times that of boys, 1.7 vs 1.0 per 10 000 AEs (Table 1). 7
DIAGNOSIS The 4th International Conference on Concussion in Sport was held in Zurich in November 2012, and proceedings from this meeting have been published in both the Clinical Journal of Sports Medicine and the British Journal of Sports Medicine and represent a revision and update of the recommendations developed following the 1st (Vienna 2001), 2nd (Prague 2004), and 3rd (Zurich 2008) International Consensus Conferences. These most recent guidelines are commonly referred to as the Zurich guidelines. From these meetings, the following consensus definition of concussion was established: concussion is a brain injury and is defined as a complex pathophysiological process affecting the brain, induced by biomechanical forces. Several common features that incorporate clinical, pathologic, and biomechanical injury constructs that may be used in defining the nature of a concussive head injury include the following: 1. Concussion may be caused either by a direct blow to the head, face, neck, or elsewhere on the body with an “impulsive” force transmitted to the head. 2. Concussion typically results in the rapid onset of short-lived impairment of neurologic function that resolves spontaneously. How-
TABLE 1. Concussion rates in high school athletics. 6,7 Sport
Rate per 10 000 Athletic Exposures
Football Boys' ice hockey Boys' lacrosse Girls' lacrosse Girls' soccer Boys' wrestling Girls' field hockey Girls' basketball Boys' soccer Boys' basketball Girls' softball Boys' baseball
6.0-6.4 5.4 3.0-4.0 2.0-3.5 3.4-3.5 1.7-2.2 1.0-2.2 1.6-2.1 1.7-1.9 1.0-1.6 1.1-1.6 0.5
ever, in some cases, symptoms and signs may evolve over a number of minutes to hours. 3. Concussion may result in neuropathological changes, but the acute clinical symptoms largely reflect a functional disturbance rather than a structural injury, and as such, no abnormality is seen on standard structural neuroimaging studies. 4. Concussion results in a graded set of clinical symptoms that may or may not involve loss of consciousness (LOC). Resolution of the clinical and cognitive symptoms typically follows a sequential course. However, it is important to note that, in some cases, symptoms may be prolonged.1 It is important to note that the diagnosis of concussion is clinical and relies on patient-reported symptoms. Physical examination frequently reveals deficits in balance and cognitive function; however, it may also be normal. Because of their limited clinical utility in predicting prognosis, previously published concussion grading scales were abandoned in 2008. 8
SYMPTOMS The symptoms of concussion are numerous and can be grouped into 4 categories: physical, cognitive, emotional, and sleep (Table 2). The most commonly reported symptom in concussion is headache, with dizziness as the next most common. 9,10 Headache is frequently bilateral but may be unilateral and is often exacerbated by bright light and loud noise. Loss of consciousness only occurs in 10% of concussions but, when prolonged, may indicate a need for neuroimaging to rule out structural injury. 7,10 The presence of amnesia, which may be either retrograde (preceding the injury) or anterograde (after the injury), may be predictive of longer recovery time. 11,12 Dizziness at the time of injury and total number and severity of symptoms have also been associated with prolonged recovery. 9,13 Cognitive impairment after concussion may be dramatic but is more commonly subtle. Athletes may be confused about recent events, answer questions slowly, or may even repeat questions. Sleep disturbance is common in concussion, although athletes will typically complain of fatigue and sleeping more than usual acutely after concussion. 11 Athletes often have difficulty recognizing concussion symptoms and, therefore, may be less likely to accurately report probable concussion. In the acute stage, concussion should be seen as an evolving injury. Symptom onset may not occur or be
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TABLE 2. Signs and symptoms of sport-related concussion. 1 Physical
Cognitive
Headache
Feeling mentally “foggy” Feeling slowed down Difficulty concentrating Difficulty remembering Forgetful of recent information Confused about recent events Answers questions slowly Repeats questions
Nausea Vomiting Balance problems Dizziness Visual problems Fatigue Sensitivity to light Sensitivity to noise Numbness/ tingling Dazed Stunned
Emotional Irritability
Sleep Drowsiness
Sadness
Sleeping more than usual More Sleeping less emotional than usual Nervousness Difficulty falling asleep
Data from Br J Sports Med 2013;47(5):250-8.
recognized for several hours or days after the injury, thereby making concussion recognition challenging. 8,14 In addition, athletes may be likely to ignore the symptoms of concussion. A 2004 study of high school football players found less than half of all probable concussions were reported in a given season. Reasons for not reporting included a desire to avoid restriction from sports, a self-judgment that symptoms were not severe enough to warrant attention, and a lack of awareness that symptoms indicate a probable concussion. 15 Symptom scales (Figure 1) allow patients to grade symptom severity. More importantly, athletes are more likely to report symptoms when completing a symptom scale than when asked via interview; hence, use of a symptom scale appears to improve diagnostic accuracy.
ASSESSMENT Any athlete suspected of suffering a concussion should be removed from the field of play and assessed, ideally, by a health care professional with experience in concussion management. 16 Any athlete found
unconscious after head or neck trauma should be assumed to have a cervical spine injury, and neck stabilization should be maintained until cleared. In this case, the initial evaluation should focus on the athlete's airway, breathing and circulatory function, and evaluation for cervical spine injury. Emergency transfer is indicated if a cervical spine injury cannot be excluded or if there are signs of a more serious neurologic injury (eg, focal neurologic examination, Glasgow Coma Score [GCS] ≤ 14, etc). 16 For less emergent injuries, the athlete can undergo serial examinations on the sideline or, if no health care provider is available for assessment, referred urgently for evaluation. The evaluation of an athlete with a possible concussion in the ED should include a comprehensive history and head/neck and neurologic examination, including mental status, cognitive function and balance, and determination of the need for neuroimaging. 16 A number of sideline assessment tools have been developed to allow a standardized approach to concussion evaluation and are frequently used in the office setting. The Standardized Assessment of Concussion (SAC) is a tool that measures cognitive function by evaluating orientation, memory (immediate and delayed), and concentration (see Appendix). It is worth noting that traditional orientation questions (eg, person, place, time) have been shown to be unreliable in sports-related concussion. 17,18 Although the SAC has shown good sensitivity and specificity in the diagnosis of concussion in older teenagers and young adults, its validity has not been demonstrated in younger children. 11,19 Ideally, athletes undergo preseason testing to obtain baseline SAC scores. In 1 study of high school football players, the average baseline score of nonconcussed controls was 25.6 of a possible total score of 30. 18 After a suspected concussion, athletes are retested, and the results, compared to their baseline. In a study of high school and collegiate athletes, a decline of 1 point or greater from baseline resulted in a sensitivity of 94% and specificity of 76% for concussion diagnosis. 20 In adults presenting to the ED with head injury, the SAC appears to be sensitive in concussion diagnosis. 21 However, a recent study of pediatric ED patients found a graded symptom checklist to be more sensitive than the SAC in concussion diagnosis. 22 Although SAC scores trended lower for concussed patients, the difference was not significant. Of note, SAC scores for nonconcussed controls younger than 12 years were significantly lower (age 9-11 years: SAC, 22.7; age 6-8 years: SAC 17.7) than those typically seen in nonconcussed high school athletes. 22
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Figure 1. Postconcussion Symptom Scale.
The Balance Error Scoring System (BESS) is a validated tool for measuring postural stability, which is frequently impaired in those with concussions. The patient is timed in 3 different stances (double leg, single leg, and tandem) for 20 seconds each on both a flat surface and a piece of mediumdensity foam. The total number of errors (eg, lifting hands off hips, stumbles, eye openings, etc) is summed to provide an overall score, which can be compared to a patient's baseline, if available, or published norms (11.0 + 5.1 for adults and 17.6 + 7.5 for children 10-17 years old). 23-25 The modified BESS eliminates the foam portion of the test and is often used on the sidelines or in office or ED settings. Overall, balance tends to recover quickly, typically within 3 to 7 days of injury. 23 The Sports Concussion Assessment Tool 3 (SCAT3) was released in the most recent Zurich statement and consists of a graded symptom checklist, the GCS, the Maddocks Questions, the SAC, and the BESS. The Maddocks questions (Table 3) have been shown to be more sensitive than standard questions of orientation (eg, What is your name?
What day is it?) in identifying possible concussion in the sports setting. 17 For the first time, the 2012 Zurich consensus statement included a Child-SCAT3 to aid in the assessment of concussion in children ages 5 to 12 years. 1 It includes a child and parent report of symptoms as well as a more basic version of the SAC and BESS. The SCAT3 is designed to be easy to administer with completion in 10 minutes or less.
TABLE 3. Maddocks questions from SCAT3/Child-SCAT3. Modified Maddocks Score What venue are we at today? Which half is it now? Who scored last in this match? What team did you play last week/game? Did your team win the last game?
Child-Maddocks Score Where are we at now? Is it before or after lunch? What did you have last lesson/class? What is your teacher’s name?
Data from Br J Sports Med 2013;47(5):250-258.
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Both versions of the SCAT3 are freely available to download (see Appendix). The inclusion of multiple assessment tools in the SCAT3 may increase the sensitivity and specificity of concussion diagnosis; however, there have not yet been any studies to validate it for diagnosing concussion. 16 Emerging tools in the assessment of concussion include quantitative electroencephalogram, functional neuroimaging (including functional magnetic resonance imaging, magnetoencephalography, and positron emission technology), and head impact sensors. Although some of these technologies show promise, their clinical utility has yet to be established. 26 Therefore, at this time, diagnosis remains a clinical one, supported by history, a comprehensive physical examination, and added assessments of cognitive function and balance.
NEUROIMAGING Neuroimaging is typically normal, and therefore, not indicated in most athletes with concussion. It should be reserved for those patients suspected of having a more severe head injury. 1,27 Computed tomography (CT) is more sensitive than magnetic resonance imaging in the identification of skull fracture and intracerebral hemorrhage or contusion in the first few days after injury. Magnetic resonance imaging is more helpful in the identification of preexisting pathology (eg, Chiari malformation, arteriovenous malformation, etc) that could cause worsening or prolonged symptoms. 16 The decision of whether a patient with an acute brain injury requires neuroimaging can be a difficult one. A recent prospective cohort study by the Pediatric Emergency Care Applied Research Network attempted to identify clinical factors associated with a low risk of clinically important traumatic brain injury (TBI) in children with head trauma. For children age 2 years and older, the following factors were identified as predictive of a low risk of structural brain injury: normal mental status, no LOC, no vomiting, nonsevere injury mechanism, no signs of basilar skull fracture, and no severe headache. This prediction rule demonstrated sensitivity of 96.8% and a negative predictive value of 99.95%. Altered mental status, GCS of 14 or less, and signs of a basilar skull fracture were most predictive of clinically important TBI (4.3% risk). Computed tomography was recommended for patients presenting with any of those predictors (Table 4). Observation without CT was recommended for those patients with a history of LOC, vomiting, severe mechanism of injury, or severe headache with normal mental status and no signs of basilar skull fracture. 28 If imaging is not obtained,
TABLE 4. Clinical predictors of clinically important TBI (indications for obtaining CT). CT Recommended GCS ≤ 14 Other signs of altered mental status Agitation Somnolence Repetitive questioning Slow response to verbal communication Signs of basilar skull fracture Battle's sign: retroauricular bruising Raccoon eyes: periorbital bruising Hemotympanum CSF otorrhea or rhinorrhea
Observation History of LOC History of vomiting
Severe mechanism of injury
Severe headache Data from Lancet 2009;374:1160-70.
anticipatory guidance should be given before discharge regarding symptoms and signs concerning intracranial bleeding, including worsening mental status or headache and persistent vomiting, which warrant return to the ED for re-evaluation.
MANAGEMENT Following initial evaluation, the implementation of cognitive and physical rest is considered the “cornerstone” of concussion management. 1 Physical rest is recommended to avoid symptom exacerbation and prolongation and to minimize the risk of a second head injury. If a second head injury is sustained before symptoms associated with the first have fully cleared, there is a risk for diffuse cerebral swelling, a rare condition that is more common in children than in adults and frequently fatal. Physical rest includes not only organized sports activities but also any activity or exercise that elevates the heart rate or poses risk of additional head injury. Cognitive rest includes time off from school or work, no homework or reading, no screen time (eg, television, computers, video games, smart phones), and increased rest or sleep. Evidence for these recommendations is limited, although a recent study of high school and collegiate athletes demonstrated the efficacy of physical and cognitive rest in the resolution of symptoms and cognitive dysfunction. 29 Although most athletes recover from concussion in 1 to 2 weeks, studies have shown longer recovery times in younger vs older athletes. 8,30 School-aged athletes often need academic accommodations in
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place when they return to school (eg, extra time to complete tests/assignments, preferential seat placement in class, avoidance of computer screens, note taker, reduced workload). 31 Medications may be used to manage postconcussive signs and symptoms when prolonged, although evidence supporting their usage is limited. In the acute setting, acetaminophen may be recommended for headache, although typically is not effective for concussion headaches. Nonsteroidal anti-inflammatory drugs and aspirin are not recommended due to the theoretical risk for bleeding. 16 Chronic postconcussion symptoms typically targeted for pharmacologic therapy include nausea, sleep disturbance, chronic headache, depression and anxiety (antidepressants), and cognitive dysfunction (stimulants). A recent survey of pediatric providers found that most (89%) of the respondents used medications to manage concussed patients with prolonged symptoms. Nonprescription medications, specifically acetaminophen, nonsteroidal anti-inflammatory drugs, and melatonin, were most frequently used, whereas prescription medications, including antidepressants and stimulants, were used less frequently. 32 In general, narcotic use should be avoided as it makes it challenging to properly assess the mental status of the concussed individual.
Return to Activity The most recent Zurich guidelines recommend that return to play after concussion should be individualized to the athlete and his or her particular injury. 16 No athlete with a suspected concussion should be allowed to return the same day. Return-to-play protocols should only begin when athletes are symptom free at rest for a minimum of 24 hours and have a normal physical examination, and when cognitive function has returned to baseline. It is recommended that no child or adolescent athlete attempts a return to organized sports until they have returned to full participation in school successfully. 1 Determination of when an athlete may return to activity requires follow-up with the primary care physician, sports medicine physician, or neurologist with experience in managing concussions. 16 Because it is impossible to predict how long an individual's symptoms will last, an exact time frame for return to play cannot be given in the ED. Follow-up also provides an opportunity for education regarding concussion prevention and typical recovery patterns, which may reduce anxiety and aid symptom resolution. 33 In some cases, computerized neuropsychological testing may be performed at the follow-up visit to
determine whether cognitive function has normalized; however, it has not been shown to be useful in the ED setting in predicting recovery. 34,35 A typical return-to-play protocol is listed in Table 5. Athletes follow a stepwise, progressive increase in the amount and intensity of exercise; any return of symptoms leads to a stop in the progression and a return to the stage at which they were last symptom free. Return to practice or competition should only occur after final clearance by a health care provider with experience in managing concussions. 1 Returnto-play protocols may need to be lengthened for the pediatric athlete. 36
PREVENTION Protective Equipment Helmets are a crucial part of protective equipment in many sports. Within alpine sports and bicycle riding, helmets have been proven to reduce moderate to severe brain injuries. 37-39 In American football, the hard shell helmet design was initially developed to decrease the force of a strong linear acceleration that was thought to put an individual at risk for skull fractures and cerebral bleeds. 40 However, there is a lack of clinical evidence to prove that helmets can reduce the risk of concussion. Although laboratory studies show that impact forces to the brain can be reduced with some
TABLE 5. Return-to-play protocol. 1 Rehabilitation Stage Day 1: Light aerobic exercise Day 2: Sportspecific exercise Day 3: Noncontact training drills Day 4: Fullcontact practice Day 5: Return to play
Exercise Aerobic exercise HR b 70% maximum Running drills in football Passing drills in soccer
Objective Increase HR Add movement Exercise, coordination, and cognitive load
Normal training Restores confidence, activities, resistance allows evaluation by training coaching staff Competition
Return-to-play protocol may begin after patient has been symptom free for at least 24 hours and physical and neurocognitive examinations are normal. If symptoms recur, patient should rest for a minimum of 24 hours and until symptoms are resolved before reattempting that day's activity. Data from Br J Sports Med 2013;47(5):250-8.
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headgear and helmets, there is no evidence to prove a reduction in concussion incidence. 1 Although linear forces can cause a concussion, it is the angular forces to the head that produce rotational acceleration, which is thought to be the primary mechanism of injury for concussion. 41 Mouthguards are frequently worn protective gear in many sports. There is strong evidence that wearing a mouthguard decreases the risk of suffering dental trauma; however, there is a paucity of data to support wearing a mouthguard to decrease concussion risk or severity. 42
Rule Changes Several sports-governing bodies have implemented rule changes to eliminate or decrease specific contact that may place an individual at greater risk for suffering a concussion. Identification of an injury mechanism that increases concussion risk is the initial step in deciding how to formulate rule changes. For instance, youth hockey studies have shown that athletes were more likely to suffer a concussion in leagues where body checking was permitted. 43,44 Subsequently, USA Hockey and Hockey Canada have both raised their minimum body checking age to 13 years old. 45 Similarly, in 2012, Pop Warner football began limiting the amount of contact in practices and eliminating all head-on, full-speed tackling drills after research demonstrated that second graders take more than 100 hits to the head during a football season, some with a force equal to concussion-inducing impacts that were measured in adults. 46,47 In 2011, the National Football League changed its kickoff rule by moving the spot of the kickoff 5 yards closer to the opposite goal line. The following season, the number of concussions during kickoffs fell from 35 to 20, a decline of 43%. 48
LEGISLATION Legislation aimed at improving concussion education and identification began in the State of Washington in May 2009 when the Zachary Lystedt Law was passed. The law was named after a 13-yearold football player who sustained a head injury and returned to play in the same game. He subsequently developed recurrent intracerebral hemorrhages and required emergency surgery. Zachary's injury resulted in significant neurologic injury and disabilities. 49 As of May 2013, 48 states plus the District of Columbia have passed concussion legislation. Although variation exists state to state, most states incorporate the 3 main principles of legislation set forth by the Lystedt Law (no concussion legislation
as of yet in Mississippi, legislation in Wyoming does not incorporate the tenets of the Lystedt Law). These include (1) education for youth athletes and their parents, (2) removal of an athlete from sports if they appear to have suffered a concussion, and (3) evaluation and written clearance of that athlete by a licensed health care professional before their return to play. 50 State-specific information can be found at www.nflevolution.com. The effects of the concussion legislation on concussion rates are not yet clear. However, studies about the free online educational CDC “Heads Up” program (see Appendix) have demonstrated improved concussion knowledge among high school coaches and improved concussion management by physicians. 51-53
SUMMARY Concussion is a common injury that ED physicians will be called upon to evaluate. A comprehensive history, physical examination, cognitive evaluation, and balance testing are important in assessing an individual with a head injury. Initial treatment for a concussion is physical and cognitive rest until symptoms are significantly improved. Athletes should never be allowed to return to play on the same day they suffer a concussion. Follow-up with a primary care physician, sports medicine specialist, or neurologist with experience in managing concussions is recommended before return to activity. A formal return-to-play progression should not begin until an athlete is asymptomatic for a minimum of 24 hours. Familiarity with legislation within your state is important for understanding the necessary rules for clearance for return to play for athletes.
APPENDIX SAC link: http://www.ncbi.nlm.nih.gov/pmc/articles/ PMC155418/ SCAT3 links: http://bjsm.bmj.com/content/47/5/259.full.pdf http://bjsm.bmj.com/content/47/5/263.full.pdf Child SCAT3 CDC “Heads Up” Program: http://www.cdc.gov/concussion/HeadsUp/youth.html BESS link: http://www.sportsconcussion.com/pdf/ management/BESSProtocolNATA09.pdf
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