GENERAL SCIENTIFIC SESSION 1 GENERAL SCIENTIFIC SESSION 1
Return to Play: A Question of Balance Richard G. Ellenbogen, MD Department of Neurological Surgery, University of Washington School of Medicine, Harborview Medical Center, Seattle, Washington Correspondence: Richard G. Ellenbogen, MD, FACS, Professor and Chair, Department of Neurological Surgery, Harborview Medical Center, 325, 9th Ave, Box 359924, Seattle, WA. E-mail: [email protected] Copyright © 2015 by the Congress of Neurological Surgeons.
The 2014 CNS Annual Meeting presentation on which this article is based is available at http://bit.ly/1Hkja8F.
CLINICAL NEUROSURGERY
I
t is reassuring to witness the academic interest, clinical activity, and passion of neurological surgeons for sports medicine issues such as return to play after concussion. The concussion issue in sports had been a perfect storm of activity in the media and with our families. Neurological surgeons have been and remain on the front lines of traumatic brain injury (TBI) prevention and treatment. The spectrum of TBI, from mild to severe, still requires a commitment from many of our practices and on-call hospital/community duties. However, concussion, which is on the milder end of the spectrum in TBI, recently received a more significant share of our neurological surgery bandwidth. Nevertheless, the concussion field is not simply owned by one specialty; it is a public health issue for many healthcare providers and a public health challenge for the entire world. The World Health Organization predicts that by 2020 TBI will be one of the leading causes of death and morbidity of all ages. It is currently one of the leading causes of mortality and disability of adolescents worldwide.1 In the United States, TBI accounts for approximately 30% of all traumatic deaths.2 The “perfect storm” is a reference to the combination of somber medical reports we have witnessed over the past decade. It is an amalgamation of events including a larger-thanexpected segment of our wounded soldiers returning from Iraq and Afghanistan with TBI and posttraumatic stress disorder, elite athletes suffering concussions with prolonged absences, and youth student athletes suffering tragic and preventable TBIs that have attracted enormous press coverage. Although sports concussions make up only a small fraction of the TBI events in the United States, their high profile has become a lightning rod for action in terms of prevention and management. The epidemiology shows that the majority of TBIs in the United States occur from falls, motor vehicle accidents, assaults, and being struck by an object. In fact, in children, .50% of TBIs are caused by falls.3 The Centers for Disease Control and Prevention (CDC) statistics from 5 years ago estimated that 248418 children (#19 years of age) were treated in the emergency departments of US hospitals
for concussion from sports-related injuries. That is a 57% rise in injuries reported over the preceding decade. It is now estimated that as a result of improved education and reporting, 1.6 to 3.8 million children perhaps suffer a concussion at a sports-related activity. The number is uncertain because many families do not seek or require medical attention and evaluation in an emergency department after the suspected injury.4 In my practice, one of the most common concerns of a parent after a child sustains a concussion is the safety of specific sports-related activity. It is easy to show parents the plethora of peer-reviewed literature that demonstrates that the benefits of exercise and organized sports activities are vast. However, that sentiment provides little comfort after a concussion is confirmed. Parents are often incredulous when I show epidemiology statistics that the risk of TBI for their children is much greater outside an organized sports activity. If statistics were purely the driving force of this vigorous focus on safety, then issues related to riding a bicycle, riding in a car, and running on the playground should receive attention equal to that focused on organized sports-related activity. Fortunately, this sports-related focus has had a salutary effect on our youth. It has helped make our beloved organized and intramural sports safer for our student athletes. It is estimated that over 26 million US students (,17 years of age) play some form of a sport in an organized or intermittent fashion. An espnW Aspen Institute Project Play Survey conducted in September 2014 of 1511 households showed that the overriding parental concerns of sports for their children were safety (87.9%), quality or behavior of coaches (81.5%), cost (70.3%), the time commitment required (67.9%), and the emphasis on winning over having fun (66.1%). The number 1 concern of parents is the risk of concussion over joint, bone, or other bodily injuries. Although .80% of parents would let their children play sports, parents had concerns about concussion in 2 sports in particular. The survey showed that parents would consider restricting their child’s participation in football
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(82.3%) and soccer (20.3%) over other sports on the basis of concern for the risk of concussion. So, we as neurological surgeons have more work to do to help make sports safer.5 One of the ramifications of this healthy national emphasis on sports safety has been that the legislatures and governors of 50 states have wisely and rapidly passed some form of youth concussion legislation protecting youth athletes during 2009 to 2014. These laws generally contain some elements of 3 guiding principles: education of the student athletes and their parents on the diagnosis and risk factors for concussion, barring a student athlete from return to play during the same game or practice after a suspected concussion, and ensuring that no student athlete returns to play without clearance by a healthcare provider who is an expert at this process. On May 14, 2009, Washington State Governor Christine Gregoire passed the first sports concussion safety legislation in the United States, the Zackery Lystedt Law (House Bill 1824; Figure 1). Several states quickly followed that legislative pathway. Zackery Lystedt, the resilient 14-year-old student who suffered a devastating, nonfatal TBI in a football game in Washington State, was a lightning rod and symbol for change for parents, student athletes, youth advocates, and legislators. The National Football League (NFL) built and financially supported a coalition to pass this legislation state by state with a wide range of healthcare providers and sports associations. This coalition included, and at times was energized by, US neurological surgeons to successfully pass this legislation. The need for legislation over just education was based on the fact that each school district throughout our country could interpret
sports-related rules as it wished, and thus there was no “stickiness” to the education or school district rules on sports safety. Although they may have been effective in some locales, they were simply ineffective in creating a much needed culture change in the United States. Washington State was the first state to pass legislation protecting the student athlete. The Brain Injury Association of Washington and its lobbyist built a coalition of interested parties, including the CDC, the Department of Defense, the Seattle Seahawks, secondary insurers, hospitals, physicians, athletic trainers, soccer associations, and legislators, to ensure that the rules had the gravitas of a law behind the laudable concept and school district guidelines.6 With the focus now firmly on concussion awareness and the impact of the legislation on sports health and safety, what can we as neurosurgeons use to guide us? First, the signs and symptoms guide us as we care for these student athletes on the field and after their injury in terms of return to play management. Headaches are the most common symptom reported after a suspected concussion, followed by dizziness, balance, and visual complaints or signs. Only 10% of all athletes are noted to suffer a loss of consciousness with their concussion. There is a wide range of presentation and recovery patterns, and $80% of athletes have their symptoms resolve within 7 days after the injury. However, a National Collegiate Athletic Association concussion study showed that full cognitive recovery, postural stability, and symptom recovery could take $90 days in a small set of the athletes.7 One of the greatest risk factors for an athlete to suffer a concussion remains a previous concussion. Selected athletes
FIGURE 1. Zackery Lystedt Law (House Bill 1824) signing on May 14, 2009, in Olympia, Washington. Foreground left to right: Jay Rodne, Fifth District, State Representative, Washington (Republican) and House Bill 1824 Sponsor; Governor Christine Gregoire; Mercedes Lystedt (mother); Zackery Lystedt; Victor Lystedt (father); and Richard Adler, JD, Brain Injury Association of Washington president.
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RETURN TO PLAY
with a previous concussion have 2 times the risk of having symptoms last longer than 1 week.8 In addition, studies seem to demonstrate that in comparable sports, female athletes experience a higher rate of concussion (1.7) and experienced longer duration to recovery than male athletes9,10 for unclear reasons. A recurrent concussion is associated with a prolonged recovery compared with a single incident, especially in high school athletes.11 In addition, the severity burden of the symptom complex after a concussion is a predictor of a prolonged recovery.7,8 Immediate postconcussion signs and symptoms that have occurred in our student athletes with prolonged recovery run a spectrum and include confusion, loss of consciousness, posttraumatic amnesia, lack of balance, dizziness, visual problems, personality changes, fatigue, and postinjury cognitive disturbances. According to the data from the University of Pittsburgh Medical Center concussion program, dizziness at the time of injury was the single major symptom associated with protracted recovery (odds ratio, 6.34).12 One of the most challenging aspects of any concussion practice is the treatment of athletes who have pre-existing conditions such as mood disorders, anxiety, depression, attention deficit–hyperactivity disorder, attention deficit disorder, risk-taking behavior, and migraine. In our practice, each of these pre-existing conditions has been intermittently associated with a prolonged recovery. In addition, it has resulted in a tailored approach to rehabilitative therapy. We partner with a neurology headache specialist for athletes whose headaches have been especially resistant to standard medical therapies and rehabilitation medicine physicians to manage active therapies such as balance, cognitive, and vestibular therapy. The school issues are managed on a caseby-case basis by a skilled and experienced team. This multidisciplinary approach often requires every member to include social workers, educational specialists, physicians, nurses, and the athletic trainers. Fortunately, certified athletic trainers are assigned to each high school in Seattle. The athletic trainers provide an invaluable service and are an insightful and protective liaison between the student athlete and parents, healthcare professionals, and teachers. They help inform all parties on appropriate return to play decisions. Our concussion team’s desire for athletic trainers in all schools on the basis of their overwhelming benefit is currently impractical because of the economic realities to accomplish this goal. Regardless, for youth athletes in 2015, in terms of return to play, it is not only the law but also safer to hold an athlete out of play or practice until cleared by a healthcare professional and a measured return to play exercise regimen is completed. Recent controversy has centered on when is it best to return a student athlete to play. The 2 schools of thought include are active rehabilitation and prolonged cognitive rest. For the past several years, most clinicians have recommended cognitive and activity rest until major symptom abatement has permitted the student to comfortably return to a graduated return to play program. This has translated into limited computer/game screen time and a time-limited excuse from schoolwork for many students. This approach is based on empirical practice, not
CLINICAL NEUROSURGERY
validated randomized trials. Those who argue for active rehabilitation of concussed student athletes while still mildly symptomatic argue that every concussion is different and needs a tailored treatment. The argument for specific therapies is that the 10% to 20% who do not improve in the first week after injury may benefit from this approach. The theory is one can successfully rehabilitate specific dysfunctions with the appropriate vestibular, visual, or cognitive therapies. The best practice for return to play after a concussion is evolving, and the active rehabilitation and cognitive rest concepts are hypotheses that have yet to be subjected to a randomized or a case-control trial. Until that time, most patients will likely receive treatment based on the best practice of their clinicians and/or concussion clinic. There are 5 lessons I learned in our work with the all-volunteer NFL, Head, Neck and Spine Medical Committee. These are lessons that informed and improved our previous practice and can be extrapolated for use in student athletes. Admittedly, the impressive economic resources that the NFL possesses and has applied to professional player health and safety are simply not practical at the amateur level. In addition, the professional on-field experience and entertainment goals are arguably disparate from those of the amateur levels.13 However, some of the most basic and scientifically validated principles championed by the NFL for concussion are economically viable at every level of amateur sports and applicable for both sexes. The principles are essential elements in our current student athlete return to play protocols. 1. Preseason: The exact role of and which preseason baseline neuropsychological or cognitive tests are best for an athlete have not been settled. However, some sort of baseline testing for the student athlete merits attention. Suffice it to say that the logical value of preseason testing is that it provides a baseline with which to compare postinjury performance. Some schools perform ImPACT testing, a commercially available computer-based neuropsychological performance test that is good for measuring reaction times.14 The utility of a baseline test such as ImPACT is that it gives a more precise assessment of clinical deterioration, improvement, and full recovery after the concussive event than simple clinical impressions. A person experienced in interpreting the results is essential. Tailored pen and paper neuropsychological tests administered by experienced neuropsychologists provide an exceptionally detailed insight into baseline cognitive function and postinjury status, and some view them as a gold standard in terms of measuring that cognitive functioning. Again, such tests are not budget neutral, despite their apparent value, because they require experienced interpretation. The Sports Concussion Assessment Tool 3 is a revision of the previous International Consensus Conferences on Concussion in Sports. The 2012 Zurich Consensus, which produced the document called Sports Concussion Assessment Tool 3, applied scientific principles in a consensus-based approach that is used worldwide for preinjury and postinjury assessment of athletes.15 It was sponsored by worldwide professional sports organizations such as the Fédération Internationale de
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Football Association, International Rugby Board, International Independent Hockey League, International Olympic Committee, Fédération Equestre Internationale. It uses cognitive, memory, coordination, balance, symptoms, signs (neurological examination and Glasgow Coma Scale) and other clinically relevant or validated tools to assess an athlete in a precise and reproducible manner. It is free, can be downloaded online, and takes about 20 minutes to perform by almost any sideline personnel, coach, athletic trainer, or trained parent. Training sideline personnel to perform the examination is cost-effective and easy.16 2. Education: The value of education for the athlete cannot be underestimated nor its full effect measured accurately in such a short time since the enactment of concussion legislation. The first act of the NFL Head, Neck and Spine Committee was the construction of a poster with the CDC and NFL Players Association that hangs in the locker room of every team.17 It provides accurate information on the signs, symptoms, and risks of concussion and the importance of timely investigation of any suspected head injuries. The poster was so successful that the CDC adapted the language for that poster, and it is now used for youth athletes (Figure 2).18 We can surmise that the rise in concussion reports nationwide is likely due in part to the ability of the coaches, referees, athletic trainers, lay person, parents, and athletes to recognize, diagnose, and treat an injured athlete. The CDC has championed the art and science of communicating its expansive concussion education portfolio. The CDC offerings are both broad and engaging. One of the most powerful tools that the CDC possesses for clinicians is the CDC online clinician training that helps healthcare professionals hone their skills on diagnosis, management, and return to play (http://www.cdc.gov/concussion/headsup/clinicians/). It has been a required exercise for sports physicians, school nurses, and concussion clinic personnel throughout the country. Every one of the students, physicians, and nurses we partner with have completed the short but illuminating Web-based course.19 3. Rules: Rules matter. Regardless of a student athlete’s style, from rule breaker to rule obeyer, the design of fair and effective sports rules helps to level the playing field and to improve player health and safety. It is an art supported by data-driven science. The fact that the NFL has kept data and film on almost every on-field event for .3 decades has helped the NFL Competition Committee design effective rules to protect the players and the game. Fortunately, because amateur sports do not enjoy that same wealth of data collection that professional sports is afforded, there is a trickle-down effect of rule creation and rule-enforced behavior from professional to youth sports. Rules, like laws, are effective because there is both a protective underpinning to their rationale derived by data and a punitive aspect to their violation. The NFL and NFL Players Association have agreed to the strictest practice regimen in
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any elite sport. The NFL permits no more than 14 full-contact practices once the regular season begins. The rationale is that, if contact in practice is limited during the regular season, the risk of concussion at practice is much lower than during games. This approach has been proven effective. Subsequent to the NFL rule changes, Pop Warner was the first youth football organization to limit contact in practice in 2013.20 Another example of effective rule changes in the NFL occurred when the NFL Competition Committee moved up the restraining line for kickoffs 4 years ago. The rationale was that the kickoff and kickoff return, with very fast, powerful athletes running at each other, produced a concussion risk that could be ameliorated and lowered. The result was fewer kickoff returns and more touchbacks. The direct concussion reduction reward was that for the past 3 consecutive years, the NFL has witnessed a dramatic .30% decrease in concussions on the kickoff and return. Intentional head-to-head contact, one of the prime causes of concussion in all sports at all levels, was studied in the NFL. It was determined that there would be penalties or fines for such events to athletes judged causing them. The result was a drop in the number of such events. Amateur and professional sports worldwide benefit from collecting data and subsequently analyzing the data to find opportunities to make specific play safer. When thoughtful rules are proposed, executed, and enforced, sports become safer and players suffer fewer injuries. 4. Sideline diligence: The sideline is the place to enhance the safety of the game in the most obvious and effective ways. On any given game day in any NFL city, there are .20 healthcare professionals on the field. They include team sports medicine physicians, orthopedic surgeons, professional athletic trainers, unaffiliated neurological surgeons, and emergency medicine physicians prepared to intubate any seriously injured player or fan. Arguably, an NFL sideline is one of the safest places in the United States to suffer an injury, especially a TBI. However, once we step away from the elite levels of sports, the on-field intensity and depth of medical expertise drop precipitously. Comparing concussion care in a professional or elite-level game with a rural high school game naturally invites a false comparison and should be avoided for reasons that may threaten the existence of amateur sports. Nevertheless, there are several concussion care tenets that should be followed, regardless of level of play, geographic location, and resources. “If in doubt, sit them out.” This adage is timeless and priceless for the health of all athletes. Any athlete suspected of suffering a concussion should be immediately removed from play and assessed by a licensed healthcare provider trained in the evaluation and management of concussion. Health and safety concerns always trump competitive concerns in every player, practice, and game. In rural, urban, and impoverished regions short on physicians and athletic trainers, the sideline expert may be
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RETURN TO PLAY
FIGURE 2. Centers for Disease Control and Prevention poster for concussion awareness for youth athletes (http://www.cdc.gov/headsup/ pdfs/highschoolsports/nfl_youngathleteposter_concussion_a-must_read_for_young_athletes.pdf).18
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ELLENBOGEN
TABLE. Graduated Return to Playa Rehabilitation Stages
Clinical Objective
Physical and cognitive rest according to postinjury condition
Improvement of symptoms and recovery of cognitive and physical function
Light activity
Walking, swimming, or stationary bike; avoid resistance training Running, skating, biking, or swimming drills; avoid head impact Progression to more complex training drills, sport specific; start progressive resistance training Resume normal activity only after medical clearance Normal game/competition
Increase heart rate and advance activity
Sports-specific activity Noncontact drills Full contact Return to play a
Functional Exercise
No activity (rest)
Add movement and check symptoms Exercise, coordination, balance; endurance without symptoms To restore confidence and assess functional/sports skills Prevent next injury/sustain health
A suggested return to play graduated exercise regimen.
a parent, nurse, emergency medical technician, certified coach, or equivalently trained personnel entrusted and empowered to act on behalf of the student athlete to remove the athlete when a suspected concussion is observed. Recognition and initial assessment of a suspected concussion may take place in the framework of the Sports Concussion Assessment Tool 3 or any equivalent sideline test. Because ,10% of concussed athletes suffer a loss of consciousness, the symptom checklist, orientation, memory, concentration, cognitive, and neurological evaluations are paramount. The initial questions should not be “Are you OK?” Concussed players do not know when they are disoriented, and a natural response of “yes” may simply be a reflection of the desire to stay in the game. The Maddocks questions remain the best initial and most reliable adjunct with the sideline examination.21 The Maddocks questions are the following: 1. At what venue/game are we today? 2. Which half or quarter is it now? 3. Who scored last in this game? 4. Who did you play last week? 5. Did your team win the last game? The Maddocks questions require memory and cognitive/ executive function skills to answer correctly. The false-negative rate of an initial Maddocks test is low (15%). The specificity, sensitivity, and validity of the sideline tests are different among different age groups and not fully defined for each level of play or cultural nuances. The sideline tests are best used in concert with similar baseline examinations for comparison.22 Imaging is rarely necessary except in athletes in whom an intracranial bleed is suspected. Athletes suspected of or diagnosed with a concussion can evolve in their symptoms, and they need to be observed for deteriorating neurological status. The athlete suspected of a concussion and cleared of the diagnosis also should be watched periodically because concussion symptoms can evolve over time after an initial appearance of wellness. 5. Return to Play: Finally, an athlete should never be discharged from the emergency department or physician office back to
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play. Return to play principles include gradual return and a coordinated, step-wise regimented exercise process that is supervised (Table). If symptoms recur with activity, the exercise progression should be slowed and restarted at the preceding symptom-free step. The return to play process should occur only after medical clearance by a healthcare professional trained in the management of concussion. The long-term effects of repeated exposure to head impacts and premature return to play are potential long-term neurological sequelae that are being defined by current and future scientific studies. There are no evidence-based guidelines for retiring an athlete from a sport after a concussion. In addition, return to play of an athlete after a craniotomy or after incidental discovery magnetic resonance of an anatomic condition such as an arachnoid cyst or Chiari malformation is complex and highly subjective. The results of a recent survey sent to neurological surgeons caring for athletes who presented with structural neurosurgical lesions (both operative and nonoperative lesions) were fascinating. Approximately 94% of athletes returning to play with nonoperative lesions suffered no reported clinical sequelae. Not surprisingly, nonsurgical and 81% of surgical respondents required deficit resolution before clearing their patients for return to play. The conclusion is that each concussion and each anatomic variant must receive individualized attention by an expert. It must be evaluated in the context of the patient’s desire and willingness to return to play, risk threshold, balance between quality of life and safety, and current scientific evidence or lack thereof.23
CONCLUSION We have come a long way in a short period of time in terms of protecting and managing youth athletes with concussion. A perfect storm of events has focused our attention and clinical and scientific efforts on improvements in this complex, evolving field.
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Disclosures Dr Ellenbogen serves as a volunteer for the NFL Head, Neck and Spine Medical Committee. The author has no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article.
REFERENCES 1. Hyder AA, Wunderlich CA, Puvanachandra P, Gururaj G, Kobusingye OC. The impact of traumatic brain injuries: a global perspective. NeuroRehabilitation. 2007; 22(5):341-353. 2. Faul M, Xu L, Wald M, Coronado V. Traumatic Brain Injury in the United States: Emergency Department Visits, Hospitalizations, and Deaths. Atlanta, GA: Centers for Disease Control and Prevention, National Center for Injury Prevention and Control; 2010. 3. Centers for Disease Control and Prevention. Injury prevention & control: traumatic brain injury. Available at: http://www.cdc.gov/traumaticbraininjury/ data/dist_ed.html. Accessed February 24, 2014. 4. Centers for Disease Control and Prevention. Nonfatal traumatic brain injuries related to sports and recreation activities among persons aged #19 years—United States, 2001-2009. MMWR Morb Mortal Wkly Rep. 2011;60(39):1337-1342. 5. EspnW/Aspen Institute EspnW/Aspen Institute Project Play Survey of Parents on Youth Sports Issues. Available at: http://aspenprojectplay.org/sites/default/files/ espnw-Aspen%20Institute%20Project%20Play%20Survey%20of%20Parents% 20on%20youth%20sports%20issues.pdf. 6. Ellenbogen RG. Concussion advocacy and legislation: a neurological surgeon’s view from the epicenter. Neurosurgery. 2014;75(suppl 4):S122-S130. 7. McCrea M, Guskiewicz KM, Marshall SW, et al. Acute effects and recovery time following concussion in collegiate football players: the NCAA Concussion Study. JAMA. 2003;290(19):2556-2563. 8. Chrisman SP, Rivara FP, Schiff MA, Zhou C, Comstock RD. Risk factors for concussive symptoms 1 week or longer in high school athletes. Brain Inj. 2013; 27(1):1-9. 9. Marar M, McIlvain NM, Fields SK, Comstock RD. Epidemiology of concussions among United States high school athletes in 20 sports. Am J Sports Med. 2012;40 (4):747-755.
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10. Colvin AC, Mullen J, Lovell MR, West RV, Collins MW, Groh M. The role of concussion history and gender in recovery from soccer-related concussion. Am J Sports Med. 2009;37(9):1699-1704. 11. Castile L, Collins CL, McIlvain NM, Comstock RD. The epidemiology of new versus recurrent sports concussions among high school athletes, 2005-2010. Br J Sports Med. 2012;46(8):603-610. 12. Lau BC, Kontos AP, Collins MW, Mucha A, Lovell MR. Which on-field signs/ symptoms predict protracted recovery from sport-related concussion among high school football players? Am J Sports Med. 2011;39(11):2311-2318. 13. National Football League. 2014 Health & Safety Report. Available at: www. nflevolution.com/healthandsafetyreport/. Accessed 2014. 14. Iverson GL, Lovell MR, Collins MW. Interpreting change on ImPACT following sport concussion. Clin Neuropsychol. 2003;17(4):460-467. 15. 2013 Concussion in Sport Group. Sport concussion assessment tool, 3rd edition. Br J Sports Med. 2013;47:259-262. 16. 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(5):250-258. 17. Centers for Disease Control and Prevention. Poster. Available at: http://www.cdc. gov/headsup/pdfs/highschoolsports/nfl_youngathleteposter_concussion_a-must_ read_for_young_athletes.pdf. Accessed April 8, 2015. 18. CDC. Concussion. Available at: http://www.cdc.gov/headsup/pdfs/highschoolsports/ nfl_youngathleteposter_concussion_a-must_read_for_young_athletes.pdf. Accessed April 8, 2015. 19. CDC. Available at: http://www.cdc.gov/concussion/HeadsUp/clinicians/index. html. Accessed April 8, 2015. 20. Pop Warner Little Scholars. Official Rule Book. Available at: http://www. popwarner.com/forms/rules.htm. Accessed 2014. 21. Maddocks DL, Dicker GD, Saling MM. The assessment of orientation following concussion in athletes. Clin J Sport Med. 1995;5(1):32-35. 22. Giza CC, Kutcher JS, Ashwal S, et al. Summary of evidence-based guideline update: evaluation and management of concussion in sports: report of the Guideline Development Subcommittee of the American Academy of Neurology. Neurology. 2013;80(24):2250-2257. 23. Saigal R, Batjer HH, Ellenbogen RG, Berger MS. Return to play for neurosurgical patients. World Neurosurg. 2014;82(3-4):485-491.
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Copyright © Congress of Neurological Surgeons. Unauthorized reproduction of this article is prohibited
Return to Play: A Question of Balance Richard G. Ellenbogen, MD Department of Neurological Surgery, University of Washington School of Medicine, Harborview Medical Center, Seattle, Washington Correspondence: Richard G. Ellenbogen, MD, FACS, Professor and Chair, Department of Neurological Surgery, Harborview Medical Center, 325, 9th Ave, Box 359924, Seattle, WA. E-mail: [email protected] Copyright © 2015 by the Congress of Neurological Surgeons.
The 2014 CNS Annual Meeting presentation on which this article is based is available at http://bit.ly/1Hkja8F.
CLINICAL NEUROSURGERY
I
t is reassuring to witness the academic interest, clinical activity, and passion of neurological surgeons for sports medicine issues such as return to play after concussion. The concussion issue in sports had been a perfect storm of activity in the media and with our families. Neurological surgeons have been and remain on the front lines of traumatic brain injury (TBI) prevention and treatment. The spectrum of TBI, from mild to severe, still requires a commitment from many of our practices and on-call hospital/community duties. However, concussion, which is on the milder end of the spectrum in TBI, recently received a more significant share of our neurological surgery bandwidth. Nevertheless, the concussion field is not simply owned by one specialty; it is a public health issue for many healthcare providers and a public health challenge for the entire world. The World Health Organization predicts that by 2020 TBI will be one of the leading causes of death and morbidity of all ages. It is currently one of the leading causes of mortality and disability of adolescents worldwide.1 In the United States, TBI accounts for approximately 30% of all traumatic deaths.2 The “perfect storm” is a reference to the combination of somber medical reports we have witnessed over the past decade. It is an amalgamation of events including a larger-thanexpected segment of our wounded soldiers returning from Iraq and Afghanistan with TBI and posttraumatic stress disorder, elite athletes suffering concussions with prolonged absences, and youth student athletes suffering tragic and preventable TBIs that have attracted enormous press coverage. Although sports concussions make up only a small fraction of the TBI events in the United States, their high profile has become a lightning rod for action in terms of prevention and management. The epidemiology shows that the majority of TBIs in the United States occur from falls, motor vehicle accidents, assaults, and being struck by an object. In fact, in children, .50% of TBIs are caused by falls.3 The Centers for Disease Control and Prevention (CDC) statistics from 5 years ago estimated that 248418 children (#19 years of age) were treated in the emergency departments of US hospitals
for concussion from sports-related injuries. That is a 57% rise in injuries reported over the preceding decade. It is now estimated that as a result of improved education and reporting, 1.6 to 3.8 million children perhaps suffer a concussion at a sports-related activity. The number is uncertain because many families do not seek or require medical attention and evaluation in an emergency department after the suspected injury.4 In my practice, one of the most common concerns of a parent after a child sustains a concussion is the safety of specific sports-related activity. It is easy to show parents the plethora of peer-reviewed literature that demonstrates that the benefits of exercise and organized sports activities are vast. However, that sentiment provides little comfort after a concussion is confirmed. Parents are often incredulous when I show epidemiology statistics that the risk of TBI for their children is much greater outside an organized sports activity. If statistics were purely the driving force of this vigorous focus on safety, then issues related to riding a bicycle, riding in a car, and running on the playground should receive attention equal to that focused on organized sports-related activity. Fortunately, this sports-related focus has had a salutary effect on our youth. It has helped make our beloved organized and intramural sports safer for our student athletes. It is estimated that over 26 million US students (,17 years of age) play some form of a sport in an organized or intermittent fashion. An espnW Aspen Institute Project Play Survey conducted in September 2014 of 1511 households showed that the overriding parental concerns of sports for their children were safety (87.9%), quality or behavior of coaches (81.5%), cost (70.3%), the time commitment required (67.9%), and the emphasis on winning over having fun (66.1%). The number 1 concern of parents is the risk of concussion over joint, bone, or other bodily injuries. Although .80% of parents would let their children play sports, parents had concerns about concussion in 2 sports in particular. The survey showed that parents would consider restricting their child’s participation in football
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(82.3%) and soccer (20.3%) over other sports on the basis of concern for the risk of concussion. So, we as neurological surgeons have more work to do to help make sports safer.5 One of the ramifications of this healthy national emphasis on sports safety has been that the legislatures and governors of 50 states have wisely and rapidly passed some form of youth concussion legislation protecting youth athletes during 2009 to 2014. These laws generally contain some elements of 3 guiding principles: education of the student athletes and their parents on the diagnosis and risk factors for concussion, barring a student athlete from return to play during the same game or practice after a suspected concussion, and ensuring that no student athlete returns to play without clearance by a healthcare provider who is an expert at this process. On May 14, 2009, Washington State Governor Christine Gregoire passed the first sports concussion safety legislation in the United States, the Zackery Lystedt Law (House Bill 1824; Figure 1). Several states quickly followed that legislative pathway. Zackery Lystedt, the resilient 14-year-old student who suffered a devastating, nonfatal TBI in a football game in Washington State, was a lightning rod and symbol for change for parents, student athletes, youth advocates, and legislators. The National Football League (NFL) built and financially supported a coalition to pass this legislation state by state with a wide range of healthcare providers and sports associations. This coalition included, and at times was energized by, US neurological surgeons to successfully pass this legislation. The need for legislation over just education was based on the fact that each school district throughout our country could interpret
sports-related rules as it wished, and thus there was no “stickiness” to the education or school district rules on sports safety. Although they may have been effective in some locales, they were simply ineffective in creating a much needed culture change in the United States. Washington State was the first state to pass legislation protecting the student athlete. The Brain Injury Association of Washington and its lobbyist built a coalition of interested parties, including the CDC, the Department of Defense, the Seattle Seahawks, secondary insurers, hospitals, physicians, athletic trainers, soccer associations, and legislators, to ensure that the rules had the gravitas of a law behind the laudable concept and school district guidelines.6 With the focus now firmly on concussion awareness and the impact of the legislation on sports health and safety, what can we as neurosurgeons use to guide us? First, the signs and symptoms guide us as we care for these student athletes on the field and after their injury in terms of return to play management. Headaches are the most common symptom reported after a suspected concussion, followed by dizziness, balance, and visual complaints or signs. Only 10% of all athletes are noted to suffer a loss of consciousness with their concussion. There is a wide range of presentation and recovery patterns, and $80% of athletes have their symptoms resolve within 7 days after the injury. However, a National Collegiate Athletic Association concussion study showed that full cognitive recovery, postural stability, and symptom recovery could take $90 days in a small set of the athletes.7 One of the greatest risk factors for an athlete to suffer a concussion remains a previous concussion. Selected athletes
FIGURE 1. Zackery Lystedt Law (House Bill 1824) signing on May 14, 2009, in Olympia, Washington. Foreground left to right: Jay Rodne, Fifth District, State Representative, Washington (Republican) and House Bill 1824 Sponsor; Governor Christine Gregoire; Mercedes Lystedt (mother); Zackery Lystedt; Victor Lystedt (father); and Richard Adler, JD, Brain Injury Association of Washington president.
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with a previous concussion have 2 times the risk of having symptoms last longer than 1 week.8 In addition, studies seem to demonstrate that in comparable sports, female athletes experience a higher rate of concussion (1.7) and experienced longer duration to recovery than male athletes9,10 for unclear reasons. A recurrent concussion is associated with a prolonged recovery compared with a single incident, especially in high school athletes.11 In addition, the severity burden of the symptom complex after a concussion is a predictor of a prolonged recovery.7,8 Immediate postconcussion signs and symptoms that have occurred in our student athletes with prolonged recovery run a spectrum and include confusion, loss of consciousness, posttraumatic amnesia, lack of balance, dizziness, visual problems, personality changes, fatigue, and postinjury cognitive disturbances. According to the data from the University of Pittsburgh Medical Center concussion program, dizziness at the time of injury was the single major symptom associated with protracted recovery (odds ratio, 6.34).12 One of the most challenging aspects of any concussion practice is the treatment of athletes who have pre-existing conditions such as mood disorders, anxiety, depression, attention deficit–hyperactivity disorder, attention deficit disorder, risk-taking behavior, and migraine. In our practice, each of these pre-existing conditions has been intermittently associated with a prolonged recovery. In addition, it has resulted in a tailored approach to rehabilitative therapy. We partner with a neurology headache specialist for athletes whose headaches have been especially resistant to standard medical therapies and rehabilitation medicine physicians to manage active therapies such as balance, cognitive, and vestibular therapy. The school issues are managed on a caseby-case basis by a skilled and experienced team. This multidisciplinary approach often requires every member to include social workers, educational specialists, physicians, nurses, and the athletic trainers. Fortunately, certified athletic trainers are assigned to each high school in Seattle. The athletic trainers provide an invaluable service and are an insightful and protective liaison between the student athlete and parents, healthcare professionals, and teachers. They help inform all parties on appropriate return to play decisions. Our concussion team’s desire for athletic trainers in all schools on the basis of their overwhelming benefit is currently impractical because of the economic realities to accomplish this goal. Regardless, for youth athletes in 2015, in terms of return to play, it is not only the law but also safer to hold an athlete out of play or practice until cleared by a healthcare professional and a measured return to play exercise regimen is completed. Recent controversy has centered on when is it best to return a student athlete to play. The 2 schools of thought include are active rehabilitation and prolonged cognitive rest. For the past several years, most clinicians have recommended cognitive and activity rest until major symptom abatement has permitted the student to comfortably return to a graduated return to play program. This has translated into limited computer/game screen time and a time-limited excuse from schoolwork for many students. This approach is based on empirical practice, not
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validated randomized trials. Those who argue for active rehabilitation of concussed student athletes while still mildly symptomatic argue that every concussion is different and needs a tailored treatment. The argument for specific therapies is that the 10% to 20% who do not improve in the first week after injury may benefit from this approach. The theory is one can successfully rehabilitate specific dysfunctions with the appropriate vestibular, visual, or cognitive therapies. The best practice for return to play after a concussion is evolving, and the active rehabilitation and cognitive rest concepts are hypotheses that have yet to be subjected to a randomized or a case-control trial. Until that time, most patients will likely receive treatment based on the best practice of their clinicians and/or concussion clinic. There are 5 lessons I learned in our work with the all-volunteer NFL, Head, Neck and Spine Medical Committee. These are lessons that informed and improved our previous practice and can be extrapolated for use in student athletes. Admittedly, the impressive economic resources that the NFL possesses and has applied to professional player health and safety are simply not practical at the amateur level. In addition, the professional on-field experience and entertainment goals are arguably disparate from those of the amateur levels.13 However, some of the most basic and scientifically validated principles championed by the NFL for concussion are economically viable at every level of amateur sports and applicable for both sexes. The principles are essential elements in our current student athlete return to play protocols. 1. Preseason: The exact role of and which preseason baseline neuropsychological or cognitive tests are best for an athlete have not been settled. However, some sort of baseline testing for the student athlete merits attention. Suffice it to say that the logical value of preseason testing is that it provides a baseline with which to compare postinjury performance. Some schools perform ImPACT testing, a commercially available computer-based neuropsychological performance test that is good for measuring reaction times.14 The utility of a baseline test such as ImPACT is that it gives a more precise assessment of clinical deterioration, improvement, and full recovery after the concussive event than simple clinical impressions. A person experienced in interpreting the results is essential. Tailored pen and paper neuropsychological tests administered by experienced neuropsychologists provide an exceptionally detailed insight into baseline cognitive function and postinjury status, and some view them as a gold standard in terms of measuring that cognitive functioning. Again, such tests are not budget neutral, despite their apparent value, because they require experienced interpretation. The Sports Concussion Assessment Tool 3 is a revision of the previous International Consensus Conferences on Concussion in Sports. The 2012 Zurich Consensus, which produced the document called Sports Concussion Assessment Tool 3, applied scientific principles in a consensus-based approach that is used worldwide for preinjury and postinjury assessment of athletes.15 It was sponsored by worldwide professional sports organizations such as the Fédération Internationale de
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Football Association, International Rugby Board, International Independent Hockey League, International Olympic Committee, Fédération Equestre Internationale. It uses cognitive, memory, coordination, balance, symptoms, signs (neurological examination and Glasgow Coma Scale) and other clinically relevant or validated tools to assess an athlete in a precise and reproducible manner. It is free, can be downloaded online, and takes about 20 minutes to perform by almost any sideline personnel, coach, athletic trainer, or trained parent. Training sideline personnel to perform the examination is cost-effective and easy.16 2. Education: The value of education for the athlete cannot be underestimated nor its full effect measured accurately in such a short time since the enactment of concussion legislation. The first act of the NFL Head, Neck and Spine Committee was the construction of a poster with the CDC and NFL Players Association that hangs in the locker room of every team.17 It provides accurate information on the signs, symptoms, and risks of concussion and the importance of timely investigation of any suspected head injuries. The poster was so successful that the CDC adapted the language for that poster, and it is now used for youth athletes (Figure 2).18 We can surmise that the rise in concussion reports nationwide is likely due in part to the ability of the coaches, referees, athletic trainers, lay person, parents, and athletes to recognize, diagnose, and treat an injured athlete. The CDC has championed the art and science of communicating its expansive concussion education portfolio. The CDC offerings are both broad and engaging. One of the most powerful tools that the CDC possesses for clinicians is the CDC online clinician training that helps healthcare professionals hone their skills on diagnosis, management, and return to play (http://www.cdc.gov/concussion/headsup/clinicians/). It has been a required exercise for sports physicians, school nurses, and concussion clinic personnel throughout the country. Every one of the students, physicians, and nurses we partner with have completed the short but illuminating Web-based course.19 3. Rules: Rules matter. Regardless of a student athlete’s style, from rule breaker to rule obeyer, the design of fair and effective sports rules helps to level the playing field and to improve player health and safety. It is an art supported by data-driven science. The fact that the NFL has kept data and film on almost every on-field event for .3 decades has helped the NFL Competition Committee design effective rules to protect the players and the game. Fortunately, because amateur sports do not enjoy that same wealth of data collection that professional sports is afforded, there is a trickle-down effect of rule creation and rule-enforced behavior from professional to youth sports. Rules, like laws, are effective because there is both a protective underpinning to their rationale derived by data and a punitive aspect to their violation. The NFL and NFL Players Association have agreed to the strictest practice regimen in
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any elite sport. The NFL permits no more than 14 full-contact practices once the regular season begins. The rationale is that, if contact in practice is limited during the regular season, the risk of concussion at practice is much lower than during games. This approach has been proven effective. Subsequent to the NFL rule changes, Pop Warner was the first youth football organization to limit contact in practice in 2013.20 Another example of effective rule changes in the NFL occurred when the NFL Competition Committee moved up the restraining line for kickoffs 4 years ago. The rationale was that the kickoff and kickoff return, with very fast, powerful athletes running at each other, produced a concussion risk that could be ameliorated and lowered. The result was fewer kickoff returns and more touchbacks. The direct concussion reduction reward was that for the past 3 consecutive years, the NFL has witnessed a dramatic .30% decrease in concussions on the kickoff and return. Intentional head-to-head contact, one of the prime causes of concussion in all sports at all levels, was studied in the NFL. It was determined that there would be penalties or fines for such events to athletes judged causing them. The result was a drop in the number of such events. Amateur and professional sports worldwide benefit from collecting data and subsequently analyzing the data to find opportunities to make specific play safer. When thoughtful rules are proposed, executed, and enforced, sports become safer and players suffer fewer injuries. 4. Sideline diligence: The sideline is the place to enhance the safety of the game in the most obvious and effective ways. On any given game day in any NFL city, there are .20 healthcare professionals on the field. They include team sports medicine physicians, orthopedic surgeons, professional athletic trainers, unaffiliated neurological surgeons, and emergency medicine physicians prepared to intubate any seriously injured player or fan. Arguably, an NFL sideline is one of the safest places in the United States to suffer an injury, especially a TBI. However, once we step away from the elite levels of sports, the on-field intensity and depth of medical expertise drop precipitously. Comparing concussion care in a professional or elite-level game with a rural high school game naturally invites a false comparison and should be avoided for reasons that may threaten the existence of amateur sports. Nevertheless, there are several concussion care tenets that should be followed, regardless of level of play, geographic location, and resources. “If in doubt, sit them out.” This adage is timeless and priceless for the health of all athletes. Any athlete suspected of suffering a concussion should be immediately removed from play and assessed by a licensed healthcare provider trained in the evaluation and management of concussion. Health and safety concerns always trump competitive concerns in every player, practice, and game. In rural, urban, and impoverished regions short on physicians and athletic trainers, the sideline expert may be
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FIGURE 2. Centers for Disease Control and Prevention poster for concussion awareness for youth athletes (http://www.cdc.gov/headsup/ pdfs/highschoolsports/nfl_youngathleteposter_concussion_a-must_read_for_young_athletes.pdf).18
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TABLE. Graduated Return to Playa Rehabilitation Stages
Clinical Objective
Physical and cognitive rest according to postinjury condition
Improvement of symptoms and recovery of cognitive and physical function
Light activity
Walking, swimming, or stationary bike; avoid resistance training Running, skating, biking, or swimming drills; avoid head impact Progression to more complex training drills, sport specific; start progressive resistance training Resume normal activity only after medical clearance Normal game/competition
Increase heart rate and advance activity
Sports-specific activity Noncontact drills Full contact Return to play a
Functional Exercise
No activity (rest)
Add movement and check symptoms Exercise, coordination, balance; endurance without symptoms To restore confidence and assess functional/sports skills Prevent next injury/sustain health
A suggested return to play graduated exercise regimen.
a parent, nurse, emergency medical technician, certified coach, or equivalently trained personnel entrusted and empowered to act on behalf of the student athlete to remove the athlete when a suspected concussion is observed. Recognition and initial assessment of a suspected concussion may take place in the framework of the Sports Concussion Assessment Tool 3 or any equivalent sideline test. Because ,10% of concussed athletes suffer a loss of consciousness, the symptom checklist, orientation, memory, concentration, cognitive, and neurological evaluations are paramount. The initial questions should not be “Are you OK?” Concussed players do not know when they are disoriented, and a natural response of “yes” may simply be a reflection of the desire to stay in the game. The Maddocks questions remain the best initial and most reliable adjunct with the sideline examination.21 The Maddocks questions are the following: 1. At what venue/game are we today? 2. Which half or quarter is it now? 3. Who scored last in this game? 4. Who did you play last week? 5. Did your team win the last game? The Maddocks questions require memory and cognitive/ executive function skills to answer correctly. The false-negative rate of an initial Maddocks test is low (15%). The specificity, sensitivity, and validity of the sideline tests are different among different age groups and not fully defined for each level of play or cultural nuances. The sideline tests are best used in concert with similar baseline examinations for comparison.22 Imaging is rarely necessary except in athletes in whom an intracranial bleed is suspected. Athletes suspected of or diagnosed with a concussion can evolve in their symptoms, and they need to be observed for deteriorating neurological status. The athlete suspected of a concussion and cleared of the diagnosis also should be watched periodically because concussion symptoms can evolve over time after an initial appearance of wellness. 5. Return to Play: Finally, an athlete should never be discharged from the emergency department or physician office back to
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play. Return to play principles include gradual return and a coordinated, step-wise regimented exercise process that is supervised (Table). If symptoms recur with activity, the exercise progression should be slowed and restarted at the preceding symptom-free step. The return to play process should occur only after medical clearance by a healthcare professional trained in the management of concussion. The long-term effects of repeated exposure to head impacts and premature return to play are potential long-term neurological sequelae that are being defined by current and future scientific studies. There are no evidence-based guidelines for retiring an athlete from a sport after a concussion. In addition, return to play of an athlete after a craniotomy or after incidental discovery magnetic resonance of an anatomic condition such as an arachnoid cyst or Chiari malformation is complex and highly subjective. The results of a recent survey sent to neurological surgeons caring for athletes who presented with structural neurosurgical lesions (both operative and nonoperative lesions) were fascinating. Approximately 94% of athletes returning to play with nonoperative lesions suffered no reported clinical sequelae. Not surprisingly, nonsurgical and 81% of surgical respondents required deficit resolution before clearing their patients for return to play. The conclusion is that each concussion and each anatomic variant must receive individualized attention by an expert. It must be evaluated in the context of the patient’s desire and willingness to return to play, risk threshold, balance between quality of life and safety, and current scientific evidence or lack thereof.23
CONCLUSION We have come a long way in a short period of time in terms of protecting and managing youth athletes with concussion. A perfect storm of events has focused our attention and clinical and scientific efforts on improvements in this complex, evolving field.
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Disclosures Dr Ellenbogen serves as a volunteer for the NFL Head, Neck and Spine Medical Committee. The author has no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article.
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10. Colvin AC, Mullen J, Lovell MR, West RV, Collins MW, Groh M. The role of concussion history and gender in recovery from soccer-related concussion. Am J Sports Med. 2009;37(9):1699-1704. 11. Castile L, Collins CL, McIlvain NM, Comstock RD. The epidemiology of new versus recurrent sports concussions among high school athletes, 2005-2010. Br J Sports Med. 2012;46(8):603-610. 12. Lau BC, Kontos AP, Collins MW, Mucha A, Lovell MR. Which on-field signs/ symptoms predict protracted recovery from sport-related concussion among high school football players? Am J Sports Med. 2011;39(11):2311-2318. 13. National Football League. 2014 Health & Safety Report. Available at: www. nflevolution.com/healthandsafetyreport/. Accessed 2014. 14. Iverson GL, Lovell MR, Collins MW. Interpreting change on ImPACT following sport concussion. Clin Neuropsychol. 2003;17(4):460-467. 15. 2013 Concussion in Sport Group. Sport concussion assessment tool, 3rd edition. Br J Sports Med. 2013;47:259-262. 16. 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(5):250-258. 17. Centers for Disease Control and Prevention. Poster. Available at: http://www.cdc. gov/headsup/pdfs/highschoolsports/nfl_youngathleteposter_concussion_a-must_ read_for_young_athletes.pdf. Accessed April 8, 2015. 18. CDC. Concussion. Available at: http://www.cdc.gov/headsup/pdfs/highschoolsports/ nfl_youngathleteposter_concussion_a-must_read_for_young_athletes.pdf. Accessed April 8, 2015. 19. CDC. Available at: http://www.cdc.gov/concussion/HeadsUp/clinicians/index. html. Accessed April 8, 2015. 20. Pop Warner Little Scholars. Official Rule Book. Available at: http://www. popwarner.com/forms/rules.htm. Accessed 2014. 21. Maddocks DL, Dicker GD, Saling MM. The assessment of orientation following concussion in athletes. Clin J Sport Med. 1995;5(1):32-35. 22. Giza CC, Kutcher JS, Ashwal S, et al. Summary of evidence-based guideline update: evaluation and management of concussion in sports: report of the Guideline Development Subcommittee of the American Academy of Neurology. Neurology. 2013;80(24):2250-2257. 23. Saigal R, Batjer HH, Ellenbogen RG, Berger MS. Return to play for neurosurgical patients. World Neurosurg. 2014;82(3-4):485-491.
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