User login
Concussions in American Football
Football is an important component of American culture, with approximately 3 million youth athletes, 1.1 million high school athletes, and 100,000 college athletes participating each year.1 Participation in football provides athletes with physical, social, psychological, and academic benefits. Despite these benefits, widespread focus has been placed on the safety of football due to the risk for sport-related concussion (SRC) and potentially long-term effects; however, little recognition has been given to the advancements in concussion management across time and occurrence of concussions during most life activities. Although it is reasonable for concerns to be presented, it is important to better understand SRC and the current factors leading to prolonged recoveries, increased risk for injury, and potentially long-term effects.
What Is a Concussion?
Concussions occur after sustaining direct or indirect injury to the head or other parts of the body, as long as the injury force is transmitted to the head. Athletes often experience physical, cognitive, emotional, and sleep-related symptoms post-concussion secondary to an “energy crisis” within the brain.2 The energy crisis occurs as the result of transient neurological dysfunction triggered by changes in the brain (eg, release of neurotransmitters, impaired axonal function).2,3 Concussion is undetectable with traditional imaging; however, advanced imaging techniques (eg, diffuse tensor imaging) have shown progress in assessing axonal injury.3 Symptom duration post-concussion is highly variable due to individual differences; a recent study showed recovery took 3 to 4 weeks for memory and symptoms.4,5
Previous Concussion Management
Identification techniques and return-to-play guidelines for concussion have significantly changed across time. In the past, concussion grading scales were utilized for diagnosis and return to play was possible within the same contest.6,7 It has since been recognized that initial concussion severity makes it difficult to predict recovery.3 For example, research revealed memory decline and increased symptoms 36 hours post-injury for athletes with a grade 1 concussion (ie, transient confusion, no loss of consciousness, concussion symptoms or mental status changes that resolve within 15 minutes of injury) compared to baseline.7 Another study found duration of mental status changes to be related to slower symptom resolution and memory impairment 36 hours to 7 days post-injury.6 Consequently, return to play within the same contest was likely too liberal. Guidelines today recommend immediate removal from play with suspected SRC. Nevertheless, the “play through pain” culture has led athletes to continue playing after SRC, contributing to prolonged recoveries and potentially long-term effects.
Current Concussion Management: Continued Concerns and Areas of Improvement
Despite increased awareness of concussions, recent estimates revealed high rates (ie, 27:1 ratio for general players) of underreporting in college football, particularly amongst offensive linemen.8 Researchers have studied recovery implications for remaining in play, with one study revealing a 2.2 times greater risk for prolonged recovery in college athletes with delayed vs immediate removal.9 Another similar study discovered an 8.8 times greater risk for prolonged recovery in adolescent and young adult athletes not removed vs removed from play.10 Further analysis found remaining in play to be the greatest risk factor for prolonged recovery compared to other previously studied risk factors (eg, age, sex, posttraumatic migraine).10 Additionally, significant differences in neurocognitive data were seen between the “removed” and “not removed” groups for verbal memory, visual memory, processing speed, and reaction time at 1 to 7 days and 8 to 30 days.10 The recovery implications of remaining in play and the additional risk for second impact syndrome (SIS), or repeat concussion when recovering from another injury, emphasizes the need for further education efforts amongst athletes to encourage immediate reporting of injury.11
Sideline Assessment
Sideline assessment has become a vital component of concussion management to rule out concussion and/or significant injury other than concussion. Assessment should include observation, cognitive/balance testing, neurologic examination, and possible exertion testing to ensure a comprehensive evaluation of all areas of potential dysfunction.12 Indications for emergency department evaluation include suspicion for cervical spine injury, intracranial hemorrhage, or skull fracture as well as prolonged loss of consciousness, high-risk mechanisms, posttraumatic seizure(s), and/or significant worsening of symptoms.12
Observation
On the sideline, it is important to identify any immediate signs of injury (ie, loss of consciousness, anterograde/retrograde amnesia, and disorientation/confusion). Since immediate signs are not always present, it is important to be aware of the most commonly reported symptoms, including headache, difficulty concentrating, fatigue, drowsiness, and dizziness.13 If symptoms are not reported by the athlete, balance problems, lack of coordination, increased emotionality, and difficulty following instructions may be observed during play.12
On-Field Assessment
Cognitive and balance testing are essential in determining if an athlete has sustained a concussion. Immediate declines in memory, concentration abilities, and balance abilities are common. Given limitations in administering long testing batteries on the sideline, brief standardized tests such as the Standardized Assessment of Concussion (SAC), Balance Error Scoring System (BESS), and Sport Concussion Assessment Tool (SCAT) are commonly utilized. Identification of cognitive and/or balance abnormalities can help the athlete recognize deficits following injury.12 Balance problems are experienced due to abnormalities in sensory organization and generally resolve during the acute recovery period.14,15 Cognitive difficulties typically persist longer than balance problems, though duration varies widely.
Neurologic Evaluation
A neurologic evaluation including cranial nerve testing and evaluation of motor-sensory function (ie, assessment for the strength and sensation of upper and lower extremities) is important to identify focal deficits (ie, sensation changes, loss of fine motor control) indicative of serious intracranial pathology.12 Additionally, clinicians have suggested inclusion of vestibular and oculomotor assessments due to frequent dysfunction post-concussion.12,15,16 Examination of the vestibular/oculomotor systems through tools such as the Vestibular/Ocular Motor Screening (VOMS) assessment (assesses both the vestibular and oculomotor systems) and King-Devick Test (primarily assesses saccadic eye movements) can elicit symptoms that may not present immediately. If assessment appears normal, exertion testing can be utilized to determine if symptoms are provoked through physical exercise that should include cardio, dynamic, and sport-specific activities to stress the vestibular system.12
Risk Factors for Injury and Prolonged Recovery
Medical professionals must consider the presence of risk factors when managing concussion in order to make appropriate treatment recommendations and return-to-play decisions. Research has demonstrated the role of female gender, learning disability, attention-deficit/hyperactivity disorder, psychiatric history, young age, motion sickness, sleep problems, somatization, concussion history, on-field dizziness, posttraumatic migraine, and fogginess in increased risk for injury and/or prolonged recovery.17-25 Additionally, athletes with ongoing symptoms from a previous injury are at risk for sustaining another injury.
Acute Home Concussion Management
Although strict rest has been recommended post-concussion, recent research evaluating strict rest vs usual care for adolescents revealed greater symptom reports and longer recovery periods for the strict rest group.26 Based on these findings and emphasis for regulation within the migraine literature (due to the common pathophysiology between migraine and concussion27), we recommend that athletes follow a regulated daily schedule post-concussion including: 1) regular sleep-wake schedule with avoidance of naps, 2) regular meals, 3) adequate fluid hydration, 4) light noncontact physical activity (ie, walking, with progressions recommended by a physician), and 5) stress management techniques. Use of these strategies immediately can help in preventing against increased symptoms and stress, and decreases the need for medication in select cases. Additionally, over-the-counter medications should be limited to 2 to 3 doses per week to avoid rebound headaches.28
In-Office Concussion Management
Athletes diagnosed with SRC will experience different symptoms based on the injury mechanism, risk factors, and management approach. Comprehensive evaluation should include assessment of risk factors, injury details, symptoms, neurocognitive functioning, vestibular/oculomotor dysfunction, tolerance of physical exertion, balance functioning, and cervical spine integrity (if necessary).29,30 Due to individual differences and the heterogeneous symptom profiles, concussion management must move beyond a “one size fits all” approach to avoid nonspecific treatment strategies and consequently prolonged recoveries.29 Clinicians and researchers at University of Pittsburgh Medical Center have identified 6 concussion clinical profiles (ie, vestibular, ocular, posttraumatic migraine, cervical, anxiety/mood, and cognitive/fatigue) that are generally identifiable 48 hours after injury.29,30 Identification of the clinical profile(s) through a comprehensive evaluation guides the development of individualized treatment plans and targeted rehabilitation strategies.29,30
Vestibular. The vestibular system is responsible for stabilizing vision while the head moves and balance control.15 Athletes can experience central and/or peripheral vestibular dysfunction to include benign paroxysmal positional vertigo (BPPV), visual motion sensitivity, vestibular ocular reflex impairment, and balance impairment.30,31 Symptoms typically include dizziness, impaired balance, blurry vision, difficulty focusing, and environmental sensitivity.15,29,30 Potential treatment options include vestibular rehabilitation, exertion therapy, and school/work accommodations.
Ocular. The oculomotor system is responsible for control of eye movements. Athletes can experience many different posttraumatic vision changes, including convergence problems, eye-tracking difficulties, refractive error, difficulty with pursuits/saccades, and accommodation insufficiency. Symptoms typically include light sensitivity, blurred vision, double vision, headaches, fatigue, and memory difficulties.15,29,30 Potential treatment options include vision therapy, vestibular rehabilitation, and school/work accommodations.32
Posttraumatic Migraine. Headache, the most common post-concussion symptom, can persist and meet criteria for posttraumatic migraine (ie, unilateral headache with accompanying nausea and/or photophobia and phonophobia).29,30,33 Implementation of a routine schedule, daily physical activity, exertion therapy, pharmacologic intervention, and school/work accommodations are potential treatment options.
Cervical. The cervical spine can be injured during whiplash-type injuries. Therefore, determining the location, onset, and typical exacerbations of pain can be helpful in identifying cervical involvement.29,30 Symptoms typically include headaches, neck pain, numbness, and tingling. Evaluation and therapy by a certified physical therapist and pharmacologic intervention (eg, muscle relaxants) are potential treatment options. 29,30
Anxiety/Mood. Anxiety, or worry and fear about everyday situations, is common post-concussion and can sometimes be related to ongoing vestibular impairment. Symptoms typically include ruminative thoughts, avoidance of specific situations, hypervigilance, feelings of being overwhelmed, and difficulty falling asleep.29,30 Potential treatment options include implementation of a routine schedule, exposure to provocative situations, psychotherapy, pharmacologic intervention, and school/work accommodations.34
Cognitive/Fatigue. A global concussion factor (including cognitive, fatigue, and migraine symptoms) has been identified within 1 to 7 days of injury. Although this factor of symptoms generally resolves during the acute recovery period, it persists in select cases.13 Symptoms typically include fatigue, decreased energy levels, nonspecific headaches, potential sleep disruption, increased symptoms towards the end of the day, difficulty concentrating, and increased headache with cognitive activities.29,30,35 Routine schedule, daily physical activity, exertion therapy, pharmacologic intervention (eg, amantadine), and school/work accommodations are potential treatment options.30
Conclusion
Advancements in SRC management warrant change in the conversations regarding concussion in football. Specifically, conversations should address the current understanding of concussion and improvements in the safety of football through stricter concussion guidelines, detailed sideline evaluations, recognition of risk factors, improved acute management, and identification of concussion profiles that help to direct individualized treatment plans and targeted rehabilitation strategies. The biggest concerns related to concussions in football include underreporting of injury, premature return to play, and receiving routine rather than individualized treatment. Therefore, to further improve the safety of football and management of concussion it is essential that future efforts focus on the following 6 areas:
Education: Improved understanding of concussion is imperative to reducing poor outcomes and widespread concerns.
Immediate reporting: Reporting of concussion must be expected and encouraged through consistent responses by coaches to reduce underreporting and fear of reporting in athletes.
Prevention techniques: Athletes must be taught proper form and playing techniques to reduce the risk for concussion. Proper form and technique should be incentivized.
Targeted treatment: Individualized treatment plans and targeted rehabilitation strategies must be developed based on the identified clinical profile(s) to avoid nonspecific treatment recommendations.
Multidisciplinary treatment teams: Given the heterogeneous symptoms profiles and need for care provided by different medical specialties, multidisciplinary teams are essential.
Remain current: With the progress in understanding concussion, providers must remain vigilant of future advances in concussion management to further improve the safety of football.
Am J Orthop. 2016;45(6):352-356. Copyright Frontline Medical Communications Inc. 2016. All rights reserved.
1. Dompier TP, Kerr ZY, Marshall SW, et al. Incidence of concussion during practice and games in youth, high school, and collegiate American football players. JAMA Pediatrics. 2015;169(7):659-665.
2. Giza C, Hovda D. The new neurometabolic cascade of concussion
3. Barkhoudarian G, Hovda DA, Giza CC. The molecular pathophysiology of concussive brain injury - an update. Phys Med Rehabil Clin N Am. 2016;27:373-393.
4. Henry L, Elbin R, Collins M, Marchetti G, Kontos A. Examining recovery trajectories after sport-related concussion with a multimodal clinical assessment approach. Neurosurgery. 2016;78(2):232-241.
5. McCrory P, Meeuwisse WH, Aubry M, et al. Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012. Brit J Sports Med. 2013;47(5):250-258.
6. Lovell MR, Collins MW, Iverson GL, et al. Recovery from mild concussion in high school athletes. J Neurosurg. 2003;98(2):296-301.
7. Lovell MR, Collins MW, Iverson GL, Johnston KM, Bradley JP. Grade 1 or “ding” concussions in high school athletes. Am J Sports Med. 2004;32(1):47-54.
8. Baugh CM, Kroshus E, Daneshvar DH, Filali NA, Hiscox MJ, Glantz LH. Concussion management in United States college sports: compliance with National Collegiate Athletic Association concussion policy and areas for improvement. Am J Sports Med. 2015;43(1):47-56.
9. Asken BM, McCrea MA, Clugston JR, Snyder AR, Houck ZM, Bauer RM. “Playing through it”: Delayed reporting and removal from athletic activity after concussion predicts prolonged recovery. J Athl Train. 2016;51(4):329-335.
10. Elbin RJ, Sufrinko A, Schatz P, et al. Athletes that continue to play with concussion demonstrate worse recovery outcomes than athletes immediately removed from play. J Pediatr. In press.
11. Signoretti S, Lazzarino G, Tavazzi B, Vagnozzi R. The pathophysiology of concussion. PM R. 2011;3(10 Suppl 2):S359-S368.
12. Bloom J, Blount JG. Sideline evaluation of concussion. UpToDate. 2016. http://www.uptodate.com/contents/sideline-evaluation-of-concussion. Accessed July 13, 2016.
13. Kontos AP, Elbin RJ, Schatz P, et al. A revised factor structure for the post-concussion symptom scale: baseline and postconcussion factors. Am J Sports Med. 2012;40(10):2375-2384.
14. Guskiewicz KM, Ross SE, Marshall SW. Postural stability and neuropsychological deficits after concussion in collegiate athletes. J Athl Train. 2001;36(3):263.
15. Mucha A, Collins MW, Elbin R, et al. A brief Vestibular/Ocular Motor Screening (VOMS) assessment to evaluate concussions preliminary findings. Am J Sports Med. 2014;42(10):2479-2486.
16. Bloom J. Vestibular and ocular motor assessments: Important pieces to the concussion puzzle. Athletic Training and Sports Health Care. 2013;5(6):246-248.
17. Covassin T, Elbin R, Harris W, Parker T, Kontos A. The role of age and sex in symptoms, neurocognitive performance, and postural stability in athletes after concussion. Am J Sports Med. 2012;40(6):1303-1312.
18. Kontos A, Sufrinko A, Elbin R, Puskar A, Collins M. Reliability and associated risk factors for performance on the Vestibular/Ocular Motor Screening (VOMS) tool in healthy collegiate athletes. Am J Sports Med. 2016;44(6):1400-1406.
19. Guskiewicz KM, McCrea M, Marshall SW, et al. Cumulative effects associated with recurrent concussion in collegiate football players: the NCAA Concussion Study. JAMA. 2003;290(19):2549-2555.
20. Lau B, Lovell MR, Collins MW, Pardini J. Neurocognitive and symptom predictors of recovery in high school athletes. Clin J Sport Med. 2009;19(3):216-221.
21. 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.
22. Mihalik JP, Register-Mihalik J, Kerr ZY, Marshall SW, McCrea MC, Guskiewicz KM. Recovery of posttraumatic migraine characteristics in patients after mild traumatic brain injury. Am J Sports Med. 2013;41(7):1490-1496.
23. Covassin T, Moran R, Elbin RJ. Sex differences in reported concussion injury rates and time loss from participation: An update of the National Collegiate Athletic Association injury surveillance program from 2004-2005 through 2008-2009. J Athl Train. 2016;51(3):189-194.
24. Root JM, Zuckerbraun NS, Wang L, et al. History of somatization is associated with prolonged recovery from concussion. J Pediatr. 2016;174:39-44.
25. Sufrinko A, Pearce K, Elbin RJ, et al. The effect of preinjury sleep difficulties on neurocognitive impairment and symptoms after sport-related concussion. Am J Sports Med. 2015;43(4):830-838.
26. Thomas DG, Apps JN, Hoffmann RG, McCrea M, Hammeke T. Benefits of strict rest after acute concussion: a randomized controlled trial. Pediatrics. 2015;135(2):213-223.
27. Choe M, Blume H. Pediatric posttraumatic Headache: a review. J Child Neurol. 2016;31(1):76-85.
28. Tepper SJ, Tepper DE. Breaking the cycle of medication overuse. Cleve Clin J Med. 2010;77(4):236-242.
29. Collins M, Kontos A, Reynolds E, Murawski C, Fu F. A comprehensive, targeted approach to the clinical care of athletes following sport-related concussion. Knee Surg Sports Traumatol Arthrosc. 2014;22(2):235-246.
30. Reynolds E, Collins MW, Mucha A, Troutman-Ensecki C. Establishing a clinical service for the management of sports-related concussions. Neurosurgery. 2014;75 Suppl 4:S71-S81.
31. Broglio SP, Collins MW, Williams RM, Mucha A, Kontos AP. Current and emerging rehabilitation for concussion: a review of the evidence. Clin Sports Med. 2015;34(2):213-231.
32. Master C, Scheiman M, Gallaway M, et al. Vision diagnoses are common after concussion in adolescents. Clin Pediatr (Phila). 2016;55(3):260-267.
33. Headache Classification Committee of the International Headache Society (IHS). The international classification of headache disorders, 3rd edition (beta version). Cephalalgia. 2013;33(9):629-808.
34. Kontos A, Deitrick JM, Reynolds E. Mental health implication and consequences following sport-related concussion. Brit J Sports Med. 2016;50(3):139-140.
35. Kontos AP, Covassin T, Elbin R, Parker T. Depression and neurocognitive performance after concussion among male and female high school and collegiate athletes. Arch Phys Med Rehabil. 2012;93(10):1751-1756.
Football is an important component of American culture, with approximately 3 million youth athletes, 1.1 million high school athletes, and 100,000 college athletes participating each year.1 Participation in football provides athletes with physical, social, psychological, and academic benefits. Despite these benefits, widespread focus has been placed on the safety of football due to the risk for sport-related concussion (SRC) and potentially long-term effects; however, little recognition has been given to the advancements in concussion management across time and occurrence of concussions during most life activities. Although it is reasonable for concerns to be presented, it is important to better understand SRC and the current factors leading to prolonged recoveries, increased risk for injury, and potentially long-term effects.
What Is a Concussion?
Concussions occur after sustaining direct or indirect injury to the head or other parts of the body, as long as the injury force is transmitted to the head. Athletes often experience physical, cognitive, emotional, and sleep-related symptoms post-concussion secondary to an “energy crisis” within the brain.2 The energy crisis occurs as the result of transient neurological dysfunction triggered by changes in the brain (eg, release of neurotransmitters, impaired axonal function).2,3 Concussion is undetectable with traditional imaging; however, advanced imaging techniques (eg, diffuse tensor imaging) have shown progress in assessing axonal injury.3 Symptom duration post-concussion is highly variable due to individual differences; a recent study showed recovery took 3 to 4 weeks for memory and symptoms.4,5
Previous Concussion Management
Identification techniques and return-to-play guidelines for concussion have significantly changed across time. In the past, concussion grading scales were utilized for diagnosis and return to play was possible within the same contest.6,7 It has since been recognized that initial concussion severity makes it difficult to predict recovery.3 For example, research revealed memory decline and increased symptoms 36 hours post-injury for athletes with a grade 1 concussion (ie, transient confusion, no loss of consciousness, concussion symptoms or mental status changes that resolve within 15 minutes of injury) compared to baseline.7 Another study found duration of mental status changes to be related to slower symptom resolution and memory impairment 36 hours to 7 days post-injury.6 Consequently, return to play within the same contest was likely too liberal. Guidelines today recommend immediate removal from play with suspected SRC. Nevertheless, the “play through pain” culture has led athletes to continue playing after SRC, contributing to prolonged recoveries and potentially long-term effects.
Current Concussion Management: Continued Concerns and Areas of Improvement
Despite increased awareness of concussions, recent estimates revealed high rates (ie, 27:1 ratio for general players) of underreporting in college football, particularly amongst offensive linemen.8 Researchers have studied recovery implications for remaining in play, with one study revealing a 2.2 times greater risk for prolonged recovery in college athletes with delayed vs immediate removal.9 Another similar study discovered an 8.8 times greater risk for prolonged recovery in adolescent and young adult athletes not removed vs removed from play.10 Further analysis found remaining in play to be the greatest risk factor for prolonged recovery compared to other previously studied risk factors (eg, age, sex, posttraumatic migraine).10 Additionally, significant differences in neurocognitive data were seen between the “removed” and “not removed” groups for verbal memory, visual memory, processing speed, and reaction time at 1 to 7 days and 8 to 30 days.10 The recovery implications of remaining in play and the additional risk for second impact syndrome (SIS), or repeat concussion when recovering from another injury, emphasizes the need for further education efforts amongst athletes to encourage immediate reporting of injury.11
Sideline Assessment
Sideline assessment has become a vital component of concussion management to rule out concussion and/or significant injury other than concussion. Assessment should include observation, cognitive/balance testing, neurologic examination, and possible exertion testing to ensure a comprehensive evaluation of all areas of potential dysfunction.12 Indications for emergency department evaluation include suspicion for cervical spine injury, intracranial hemorrhage, or skull fracture as well as prolonged loss of consciousness, high-risk mechanisms, posttraumatic seizure(s), and/or significant worsening of symptoms.12
Observation
On the sideline, it is important to identify any immediate signs of injury (ie, loss of consciousness, anterograde/retrograde amnesia, and disorientation/confusion). Since immediate signs are not always present, it is important to be aware of the most commonly reported symptoms, including headache, difficulty concentrating, fatigue, drowsiness, and dizziness.13 If symptoms are not reported by the athlete, balance problems, lack of coordination, increased emotionality, and difficulty following instructions may be observed during play.12
On-Field Assessment
Cognitive and balance testing are essential in determining if an athlete has sustained a concussion. Immediate declines in memory, concentration abilities, and balance abilities are common. Given limitations in administering long testing batteries on the sideline, brief standardized tests such as the Standardized Assessment of Concussion (SAC), Balance Error Scoring System (BESS), and Sport Concussion Assessment Tool (SCAT) are commonly utilized. Identification of cognitive and/or balance abnormalities can help the athlete recognize deficits following injury.12 Balance problems are experienced due to abnormalities in sensory organization and generally resolve during the acute recovery period.14,15 Cognitive difficulties typically persist longer than balance problems, though duration varies widely.
Neurologic Evaluation
A neurologic evaluation including cranial nerve testing and evaluation of motor-sensory function (ie, assessment for the strength and sensation of upper and lower extremities) is important to identify focal deficits (ie, sensation changes, loss of fine motor control) indicative of serious intracranial pathology.12 Additionally, clinicians have suggested inclusion of vestibular and oculomotor assessments due to frequent dysfunction post-concussion.12,15,16 Examination of the vestibular/oculomotor systems through tools such as the Vestibular/Ocular Motor Screening (VOMS) assessment (assesses both the vestibular and oculomotor systems) and King-Devick Test (primarily assesses saccadic eye movements) can elicit symptoms that may not present immediately. If assessment appears normal, exertion testing can be utilized to determine if symptoms are provoked through physical exercise that should include cardio, dynamic, and sport-specific activities to stress the vestibular system.12
Risk Factors for Injury and Prolonged Recovery
Medical professionals must consider the presence of risk factors when managing concussion in order to make appropriate treatment recommendations and return-to-play decisions. Research has demonstrated the role of female gender, learning disability, attention-deficit/hyperactivity disorder, psychiatric history, young age, motion sickness, sleep problems, somatization, concussion history, on-field dizziness, posttraumatic migraine, and fogginess in increased risk for injury and/or prolonged recovery.17-25 Additionally, athletes with ongoing symptoms from a previous injury are at risk for sustaining another injury.
Acute Home Concussion Management
Although strict rest has been recommended post-concussion, recent research evaluating strict rest vs usual care for adolescents revealed greater symptom reports and longer recovery periods for the strict rest group.26 Based on these findings and emphasis for regulation within the migraine literature (due to the common pathophysiology between migraine and concussion27), we recommend that athletes follow a regulated daily schedule post-concussion including: 1) regular sleep-wake schedule with avoidance of naps, 2) regular meals, 3) adequate fluid hydration, 4) light noncontact physical activity (ie, walking, with progressions recommended by a physician), and 5) stress management techniques. Use of these strategies immediately can help in preventing against increased symptoms and stress, and decreases the need for medication in select cases. Additionally, over-the-counter medications should be limited to 2 to 3 doses per week to avoid rebound headaches.28
In-Office Concussion Management
Athletes diagnosed with SRC will experience different symptoms based on the injury mechanism, risk factors, and management approach. Comprehensive evaluation should include assessment of risk factors, injury details, symptoms, neurocognitive functioning, vestibular/oculomotor dysfunction, tolerance of physical exertion, balance functioning, and cervical spine integrity (if necessary).29,30 Due to individual differences and the heterogeneous symptom profiles, concussion management must move beyond a “one size fits all” approach to avoid nonspecific treatment strategies and consequently prolonged recoveries.29 Clinicians and researchers at University of Pittsburgh Medical Center have identified 6 concussion clinical profiles (ie, vestibular, ocular, posttraumatic migraine, cervical, anxiety/mood, and cognitive/fatigue) that are generally identifiable 48 hours after injury.29,30 Identification of the clinical profile(s) through a comprehensive evaluation guides the development of individualized treatment plans and targeted rehabilitation strategies.29,30
Vestibular. The vestibular system is responsible for stabilizing vision while the head moves and balance control.15 Athletes can experience central and/or peripheral vestibular dysfunction to include benign paroxysmal positional vertigo (BPPV), visual motion sensitivity, vestibular ocular reflex impairment, and balance impairment.30,31 Symptoms typically include dizziness, impaired balance, blurry vision, difficulty focusing, and environmental sensitivity.15,29,30 Potential treatment options include vestibular rehabilitation, exertion therapy, and school/work accommodations.
Ocular. The oculomotor system is responsible for control of eye movements. Athletes can experience many different posttraumatic vision changes, including convergence problems, eye-tracking difficulties, refractive error, difficulty with pursuits/saccades, and accommodation insufficiency. Symptoms typically include light sensitivity, blurred vision, double vision, headaches, fatigue, and memory difficulties.15,29,30 Potential treatment options include vision therapy, vestibular rehabilitation, and school/work accommodations.32
Posttraumatic Migraine. Headache, the most common post-concussion symptom, can persist and meet criteria for posttraumatic migraine (ie, unilateral headache with accompanying nausea and/or photophobia and phonophobia).29,30,33 Implementation of a routine schedule, daily physical activity, exertion therapy, pharmacologic intervention, and school/work accommodations are potential treatment options.
Cervical. The cervical spine can be injured during whiplash-type injuries. Therefore, determining the location, onset, and typical exacerbations of pain can be helpful in identifying cervical involvement.29,30 Symptoms typically include headaches, neck pain, numbness, and tingling. Evaluation and therapy by a certified physical therapist and pharmacologic intervention (eg, muscle relaxants) are potential treatment options. 29,30
Anxiety/Mood. Anxiety, or worry and fear about everyday situations, is common post-concussion and can sometimes be related to ongoing vestibular impairment. Symptoms typically include ruminative thoughts, avoidance of specific situations, hypervigilance, feelings of being overwhelmed, and difficulty falling asleep.29,30 Potential treatment options include implementation of a routine schedule, exposure to provocative situations, psychotherapy, pharmacologic intervention, and school/work accommodations.34
Cognitive/Fatigue. A global concussion factor (including cognitive, fatigue, and migraine symptoms) has been identified within 1 to 7 days of injury. Although this factor of symptoms generally resolves during the acute recovery period, it persists in select cases.13 Symptoms typically include fatigue, decreased energy levels, nonspecific headaches, potential sleep disruption, increased symptoms towards the end of the day, difficulty concentrating, and increased headache with cognitive activities.29,30,35 Routine schedule, daily physical activity, exertion therapy, pharmacologic intervention (eg, amantadine), and school/work accommodations are potential treatment options.30
Conclusion
Advancements in SRC management warrant change in the conversations regarding concussion in football. Specifically, conversations should address the current understanding of concussion and improvements in the safety of football through stricter concussion guidelines, detailed sideline evaluations, recognition of risk factors, improved acute management, and identification of concussion profiles that help to direct individualized treatment plans and targeted rehabilitation strategies. The biggest concerns related to concussions in football include underreporting of injury, premature return to play, and receiving routine rather than individualized treatment. Therefore, to further improve the safety of football and management of concussion it is essential that future efforts focus on the following 6 areas:
Education: Improved understanding of concussion is imperative to reducing poor outcomes and widespread concerns.
Immediate reporting: Reporting of concussion must be expected and encouraged through consistent responses by coaches to reduce underreporting and fear of reporting in athletes.
Prevention techniques: Athletes must be taught proper form and playing techniques to reduce the risk for concussion. Proper form and technique should be incentivized.
Targeted treatment: Individualized treatment plans and targeted rehabilitation strategies must be developed based on the identified clinical profile(s) to avoid nonspecific treatment recommendations.
Multidisciplinary treatment teams: Given the heterogeneous symptoms profiles and need for care provided by different medical specialties, multidisciplinary teams are essential.
Remain current: With the progress in understanding concussion, providers must remain vigilant of future advances in concussion management to further improve the safety of football.
Am J Orthop. 2016;45(6):352-356. Copyright Frontline Medical Communications Inc. 2016. All rights reserved.
Football is an important component of American culture, with approximately 3 million youth athletes, 1.1 million high school athletes, and 100,000 college athletes participating each year.1 Participation in football provides athletes with physical, social, psychological, and academic benefits. Despite these benefits, widespread focus has been placed on the safety of football due to the risk for sport-related concussion (SRC) and potentially long-term effects; however, little recognition has been given to the advancements in concussion management across time and occurrence of concussions during most life activities. Although it is reasonable for concerns to be presented, it is important to better understand SRC and the current factors leading to prolonged recoveries, increased risk for injury, and potentially long-term effects.
What Is a Concussion?
Concussions occur after sustaining direct or indirect injury to the head or other parts of the body, as long as the injury force is transmitted to the head. Athletes often experience physical, cognitive, emotional, and sleep-related symptoms post-concussion secondary to an “energy crisis” within the brain.2 The energy crisis occurs as the result of transient neurological dysfunction triggered by changes in the brain (eg, release of neurotransmitters, impaired axonal function).2,3 Concussion is undetectable with traditional imaging; however, advanced imaging techniques (eg, diffuse tensor imaging) have shown progress in assessing axonal injury.3 Symptom duration post-concussion is highly variable due to individual differences; a recent study showed recovery took 3 to 4 weeks for memory and symptoms.4,5
Previous Concussion Management
Identification techniques and return-to-play guidelines for concussion have significantly changed across time. In the past, concussion grading scales were utilized for diagnosis and return to play was possible within the same contest.6,7 It has since been recognized that initial concussion severity makes it difficult to predict recovery.3 For example, research revealed memory decline and increased symptoms 36 hours post-injury for athletes with a grade 1 concussion (ie, transient confusion, no loss of consciousness, concussion symptoms or mental status changes that resolve within 15 minutes of injury) compared to baseline.7 Another study found duration of mental status changes to be related to slower symptom resolution and memory impairment 36 hours to 7 days post-injury.6 Consequently, return to play within the same contest was likely too liberal. Guidelines today recommend immediate removal from play with suspected SRC. Nevertheless, the “play through pain” culture has led athletes to continue playing after SRC, contributing to prolonged recoveries and potentially long-term effects.
Current Concussion Management: Continued Concerns and Areas of Improvement
Despite increased awareness of concussions, recent estimates revealed high rates (ie, 27:1 ratio for general players) of underreporting in college football, particularly amongst offensive linemen.8 Researchers have studied recovery implications for remaining in play, with one study revealing a 2.2 times greater risk for prolonged recovery in college athletes with delayed vs immediate removal.9 Another similar study discovered an 8.8 times greater risk for prolonged recovery in adolescent and young adult athletes not removed vs removed from play.10 Further analysis found remaining in play to be the greatest risk factor for prolonged recovery compared to other previously studied risk factors (eg, age, sex, posttraumatic migraine).10 Additionally, significant differences in neurocognitive data were seen between the “removed” and “not removed” groups for verbal memory, visual memory, processing speed, and reaction time at 1 to 7 days and 8 to 30 days.10 The recovery implications of remaining in play and the additional risk for second impact syndrome (SIS), or repeat concussion when recovering from another injury, emphasizes the need for further education efforts amongst athletes to encourage immediate reporting of injury.11
Sideline Assessment
Sideline assessment has become a vital component of concussion management to rule out concussion and/or significant injury other than concussion. Assessment should include observation, cognitive/balance testing, neurologic examination, and possible exertion testing to ensure a comprehensive evaluation of all areas of potential dysfunction.12 Indications for emergency department evaluation include suspicion for cervical spine injury, intracranial hemorrhage, or skull fracture as well as prolonged loss of consciousness, high-risk mechanisms, posttraumatic seizure(s), and/or significant worsening of symptoms.12
Observation
On the sideline, it is important to identify any immediate signs of injury (ie, loss of consciousness, anterograde/retrograde amnesia, and disorientation/confusion). Since immediate signs are not always present, it is important to be aware of the most commonly reported symptoms, including headache, difficulty concentrating, fatigue, drowsiness, and dizziness.13 If symptoms are not reported by the athlete, balance problems, lack of coordination, increased emotionality, and difficulty following instructions may be observed during play.12
On-Field Assessment
Cognitive and balance testing are essential in determining if an athlete has sustained a concussion. Immediate declines in memory, concentration abilities, and balance abilities are common. Given limitations in administering long testing batteries on the sideline, brief standardized tests such as the Standardized Assessment of Concussion (SAC), Balance Error Scoring System (BESS), and Sport Concussion Assessment Tool (SCAT) are commonly utilized. Identification of cognitive and/or balance abnormalities can help the athlete recognize deficits following injury.12 Balance problems are experienced due to abnormalities in sensory organization and generally resolve during the acute recovery period.14,15 Cognitive difficulties typically persist longer than balance problems, though duration varies widely.
Neurologic Evaluation
A neurologic evaluation including cranial nerve testing and evaluation of motor-sensory function (ie, assessment for the strength and sensation of upper and lower extremities) is important to identify focal deficits (ie, sensation changes, loss of fine motor control) indicative of serious intracranial pathology.12 Additionally, clinicians have suggested inclusion of vestibular and oculomotor assessments due to frequent dysfunction post-concussion.12,15,16 Examination of the vestibular/oculomotor systems through tools such as the Vestibular/Ocular Motor Screening (VOMS) assessment (assesses both the vestibular and oculomotor systems) and King-Devick Test (primarily assesses saccadic eye movements) can elicit symptoms that may not present immediately. If assessment appears normal, exertion testing can be utilized to determine if symptoms are provoked through physical exercise that should include cardio, dynamic, and sport-specific activities to stress the vestibular system.12
Risk Factors for Injury and Prolonged Recovery
Medical professionals must consider the presence of risk factors when managing concussion in order to make appropriate treatment recommendations and return-to-play decisions. Research has demonstrated the role of female gender, learning disability, attention-deficit/hyperactivity disorder, psychiatric history, young age, motion sickness, sleep problems, somatization, concussion history, on-field dizziness, posttraumatic migraine, and fogginess in increased risk for injury and/or prolonged recovery.17-25 Additionally, athletes with ongoing symptoms from a previous injury are at risk for sustaining another injury.
Acute Home Concussion Management
Although strict rest has been recommended post-concussion, recent research evaluating strict rest vs usual care for adolescents revealed greater symptom reports and longer recovery periods for the strict rest group.26 Based on these findings and emphasis for regulation within the migraine literature (due to the common pathophysiology between migraine and concussion27), we recommend that athletes follow a regulated daily schedule post-concussion including: 1) regular sleep-wake schedule with avoidance of naps, 2) regular meals, 3) adequate fluid hydration, 4) light noncontact physical activity (ie, walking, with progressions recommended by a physician), and 5) stress management techniques. Use of these strategies immediately can help in preventing against increased symptoms and stress, and decreases the need for medication in select cases. Additionally, over-the-counter medications should be limited to 2 to 3 doses per week to avoid rebound headaches.28
In-Office Concussion Management
Athletes diagnosed with SRC will experience different symptoms based on the injury mechanism, risk factors, and management approach. Comprehensive evaluation should include assessment of risk factors, injury details, symptoms, neurocognitive functioning, vestibular/oculomotor dysfunction, tolerance of physical exertion, balance functioning, and cervical spine integrity (if necessary).29,30 Due to individual differences and the heterogeneous symptom profiles, concussion management must move beyond a “one size fits all” approach to avoid nonspecific treatment strategies and consequently prolonged recoveries.29 Clinicians and researchers at University of Pittsburgh Medical Center have identified 6 concussion clinical profiles (ie, vestibular, ocular, posttraumatic migraine, cervical, anxiety/mood, and cognitive/fatigue) that are generally identifiable 48 hours after injury.29,30 Identification of the clinical profile(s) through a comprehensive evaluation guides the development of individualized treatment plans and targeted rehabilitation strategies.29,30
Vestibular. The vestibular system is responsible for stabilizing vision while the head moves and balance control.15 Athletes can experience central and/or peripheral vestibular dysfunction to include benign paroxysmal positional vertigo (BPPV), visual motion sensitivity, vestibular ocular reflex impairment, and balance impairment.30,31 Symptoms typically include dizziness, impaired balance, blurry vision, difficulty focusing, and environmental sensitivity.15,29,30 Potential treatment options include vestibular rehabilitation, exertion therapy, and school/work accommodations.
Ocular. The oculomotor system is responsible for control of eye movements. Athletes can experience many different posttraumatic vision changes, including convergence problems, eye-tracking difficulties, refractive error, difficulty with pursuits/saccades, and accommodation insufficiency. Symptoms typically include light sensitivity, blurred vision, double vision, headaches, fatigue, and memory difficulties.15,29,30 Potential treatment options include vision therapy, vestibular rehabilitation, and school/work accommodations.32
Posttraumatic Migraine. Headache, the most common post-concussion symptom, can persist and meet criteria for posttraumatic migraine (ie, unilateral headache with accompanying nausea and/or photophobia and phonophobia).29,30,33 Implementation of a routine schedule, daily physical activity, exertion therapy, pharmacologic intervention, and school/work accommodations are potential treatment options.
Cervical. The cervical spine can be injured during whiplash-type injuries. Therefore, determining the location, onset, and typical exacerbations of pain can be helpful in identifying cervical involvement.29,30 Symptoms typically include headaches, neck pain, numbness, and tingling. Evaluation and therapy by a certified physical therapist and pharmacologic intervention (eg, muscle relaxants) are potential treatment options. 29,30
Anxiety/Mood. Anxiety, or worry and fear about everyday situations, is common post-concussion and can sometimes be related to ongoing vestibular impairment. Symptoms typically include ruminative thoughts, avoidance of specific situations, hypervigilance, feelings of being overwhelmed, and difficulty falling asleep.29,30 Potential treatment options include implementation of a routine schedule, exposure to provocative situations, psychotherapy, pharmacologic intervention, and school/work accommodations.34
Cognitive/Fatigue. A global concussion factor (including cognitive, fatigue, and migraine symptoms) has been identified within 1 to 7 days of injury. Although this factor of symptoms generally resolves during the acute recovery period, it persists in select cases.13 Symptoms typically include fatigue, decreased energy levels, nonspecific headaches, potential sleep disruption, increased symptoms towards the end of the day, difficulty concentrating, and increased headache with cognitive activities.29,30,35 Routine schedule, daily physical activity, exertion therapy, pharmacologic intervention (eg, amantadine), and school/work accommodations are potential treatment options.30
Conclusion
Advancements in SRC management warrant change in the conversations regarding concussion in football. Specifically, conversations should address the current understanding of concussion and improvements in the safety of football through stricter concussion guidelines, detailed sideline evaluations, recognition of risk factors, improved acute management, and identification of concussion profiles that help to direct individualized treatment plans and targeted rehabilitation strategies. The biggest concerns related to concussions in football include underreporting of injury, premature return to play, and receiving routine rather than individualized treatment. Therefore, to further improve the safety of football and management of concussion it is essential that future efforts focus on the following 6 areas:
Education: Improved understanding of concussion is imperative to reducing poor outcomes and widespread concerns.
Immediate reporting: Reporting of concussion must be expected and encouraged through consistent responses by coaches to reduce underreporting and fear of reporting in athletes.
Prevention techniques: Athletes must be taught proper form and playing techniques to reduce the risk for concussion. Proper form and technique should be incentivized.
Targeted treatment: Individualized treatment plans and targeted rehabilitation strategies must be developed based on the identified clinical profile(s) to avoid nonspecific treatment recommendations.
Multidisciplinary treatment teams: Given the heterogeneous symptoms profiles and need for care provided by different medical specialties, multidisciplinary teams are essential.
Remain current: With the progress in understanding concussion, providers must remain vigilant of future advances in concussion management to further improve the safety of football.
Am J Orthop. 2016;45(6):352-356. Copyright Frontline Medical Communications Inc. 2016. All rights reserved.
1. Dompier TP, Kerr ZY, Marshall SW, et al. Incidence of concussion during practice and games in youth, high school, and collegiate American football players. JAMA Pediatrics. 2015;169(7):659-665.
2. Giza C, Hovda D. The new neurometabolic cascade of concussion
3. Barkhoudarian G, Hovda DA, Giza CC. The molecular pathophysiology of concussive brain injury - an update. Phys Med Rehabil Clin N Am. 2016;27:373-393.
4. Henry L, Elbin R, Collins M, Marchetti G, Kontos A. Examining recovery trajectories after sport-related concussion with a multimodal clinical assessment approach. Neurosurgery. 2016;78(2):232-241.
5. McCrory P, Meeuwisse WH, Aubry M, et al. Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012. Brit J Sports Med. 2013;47(5):250-258.
6. Lovell MR, Collins MW, Iverson GL, et al. Recovery from mild concussion in high school athletes. J Neurosurg. 2003;98(2):296-301.
7. Lovell MR, Collins MW, Iverson GL, Johnston KM, Bradley JP. Grade 1 or “ding” concussions in high school athletes. Am J Sports Med. 2004;32(1):47-54.
8. Baugh CM, Kroshus E, Daneshvar DH, Filali NA, Hiscox MJ, Glantz LH. Concussion management in United States college sports: compliance with National Collegiate Athletic Association concussion policy and areas for improvement. Am J Sports Med. 2015;43(1):47-56.
9. Asken BM, McCrea MA, Clugston JR, Snyder AR, Houck ZM, Bauer RM. “Playing through it”: Delayed reporting and removal from athletic activity after concussion predicts prolonged recovery. J Athl Train. 2016;51(4):329-335.
10. Elbin RJ, Sufrinko A, Schatz P, et al. Athletes that continue to play with concussion demonstrate worse recovery outcomes than athletes immediately removed from play. J Pediatr. In press.
11. Signoretti S, Lazzarino G, Tavazzi B, Vagnozzi R. The pathophysiology of concussion. PM R. 2011;3(10 Suppl 2):S359-S368.
12. Bloom J, Blount JG. Sideline evaluation of concussion. UpToDate. 2016. http://www.uptodate.com/contents/sideline-evaluation-of-concussion. Accessed July 13, 2016.
13. Kontos AP, Elbin RJ, Schatz P, et al. A revised factor structure for the post-concussion symptom scale: baseline and postconcussion factors. Am J Sports Med. 2012;40(10):2375-2384.
14. Guskiewicz KM, Ross SE, Marshall SW. Postural stability and neuropsychological deficits after concussion in collegiate athletes. J Athl Train. 2001;36(3):263.
15. Mucha A, Collins MW, Elbin R, et al. A brief Vestibular/Ocular Motor Screening (VOMS) assessment to evaluate concussions preliminary findings. Am J Sports Med. 2014;42(10):2479-2486.
16. Bloom J. Vestibular and ocular motor assessments: Important pieces to the concussion puzzle. Athletic Training and Sports Health Care. 2013;5(6):246-248.
17. Covassin T, Elbin R, Harris W, Parker T, Kontos A. The role of age and sex in symptoms, neurocognitive performance, and postural stability in athletes after concussion. Am J Sports Med. 2012;40(6):1303-1312.
18. Kontos A, Sufrinko A, Elbin R, Puskar A, Collins M. Reliability and associated risk factors for performance on the Vestibular/Ocular Motor Screening (VOMS) tool in healthy collegiate athletes. Am J Sports Med. 2016;44(6):1400-1406.
19. Guskiewicz KM, McCrea M, Marshall SW, et al. Cumulative effects associated with recurrent concussion in collegiate football players: the NCAA Concussion Study. JAMA. 2003;290(19):2549-2555.
20. Lau B, Lovell MR, Collins MW, Pardini J. Neurocognitive and symptom predictors of recovery in high school athletes. Clin J Sport Med. 2009;19(3):216-221.
21. 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.
22. Mihalik JP, Register-Mihalik J, Kerr ZY, Marshall SW, McCrea MC, Guskiewicz KM. Recovery of posttraumatic migraine characteristics in patients after mild traumatic brain injury. Am J Sports Med. 2013;41(7):1490-1496.
23. Covassin T, Moran R, Elbin RJ. Sex differences in reported concussion injury rates and time loss from participation: An update of the National Collegiate Athletic Association injury surveillance program from 2004-2005 through 2008-2009. J Athl Train. 2016;51(3):189-194.
24. Root JM, Zuckerbraun NS, Wang L, et al. History of somatization is associated with prolonged recovery from concussion. J Pediatr. 2016;174:39-44.
25. Sufrinko A, Pearce K, Elbin RJ, et al. The effect of preinjury sleep difficulties on neurocognitive impairment and symptoms after sport-related concussion. Am J Sports Med. 2015;43(4):830-838.
26. Thomas DG, Apps JN, Hoffmann RG, McCrea M, Hammeke T. Benefits of strict rest after acute concussion: a randomized controlled trial. Pediatrics. 2015;135(2):213-223.
27. Choe M, Blume H. Pediatric posttraumatic Headache: a review. J Child Neurol. 2016;31(1):76-85.
28. Tepper SJ, Tepper DE. Breaking the cycle of medication overuse. Cleve Clin J Med. 2010;77(4):236-242.
29. Collins M, Kontos A, Reynolds E, Murawski C, Fu F. A comprehensive, targeted approach to the clinical care of athletes following sport-related concussion. Knee Surg Sports Traumatol Arthrosc. 2014;22(2):235-246.
30. Reynolds E, Collins MW, Mucha A, Troutman-Ensecki C. Establishing a clinical service for the management of sports-related concussions. Neurosurgery. 2014;75 Suppl 4:S71-S81.
31. Broglio SP, Collins MW, Williams RM, Mucha A, Kontos AP. Current and emerging rehabilitation for concussion: a review of the evidence. Clin Sports Med. 2015;34(2):213-231.
32. Master C, Scheiman M, Gallaway M, et al. Vision diagnoses are common after concussion in adolescents. Clin Pediatr (Phila). 2016;55(3):260-267.
33. Headache Classification Committee of the International Headache Society (IHS). The international classification of headache disorders, 3rd edition (beta version). Cephalalgia. 2013;33(9):629-808.
34. Kontos A, Deitrick JM, Reynolds E. Mental health implication and consequences following sport-related concussion. Brit J Sports Med. 2016;50(3):139-140.
35. Kontos AP, Covassin T, Elbin R, Parker T. Depression and neurocognitive performance after concussion among male and female high school and collegiate athletes. Arch Phys Med Rehabil. 2012;93(10):1751-1756.
1. Dompier TP, Kerr ZY, Marshall SW, et al. Incidence of concussion during practice and games in youth, high school, and collegiate American football players. JAMA Pediatrics. 2015;169(7):659-665.
2. Giza C, Hovda D. The new neurometabolic cascade of concussion
3. Barkhoudarian G, Hovda DA, Giza CC. The molecular pathophysiology of concussive brain injury - an update. Phys Med Rehabil Clin N Am. 2016;27:373-393.
4. Henry L, Elbin R, Collins M, Marchetti G, Kontos A. Examining recovery trajectories after sport-related concussion with a multimodal clinical assessment approach. Neurosurgery. 2016;78(2):232-241.
5. McCrory P, Meeuwisse WH, Aubry M, et al. Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012. Brit J Sports Med. 2013;47(5):250-258.
6. Lovell MR, Collins MW, Iverson GL, et al. Recovery from mild concussion in high school athletes. J Neurosurg. 2003;98(2):296-301.
7. Lovell MR, Collins MW, Iverson GL, Johnston KM, Bradley JP. Grade 1 or “ding” concussions in high school athletes. Am J Sports Med. 2004;32(1):47-54.
8. Baugh CM, Kroshus E, Daneshvar DH, Filali NA, Hiscox MJ, Glantz LH. Concussion management in United States college sports: compliance with National Collegiate Athletic Association concussion policy and areas for improvement. Am J Sports Med. 2015;43(1):47-56.
9. Asken BM, McCrea MA, Clugston JR, Snyder AR, Houck ZM, Bauer RM. “Playing through it”: Delayed reporting and removal from athletic activity after concussion predicts prolonged recovery. J Athl Train. 2016;51(4):329-335.
10. Elbin RJ, Sufrinko A, Schatz P, et al. Athletes that continue to play with concussion demonstrate worse recovery outcomes than athletes immediately removed from play. J Pediatr. In press.
11. Signoretti S, Lazzarino G, Tavazzi B, Vagnozzi R. The pathophysiology of concussion. PM R. 2011;3(10 Suppl 2):S359-S368.
12. Bloom J, Blount JG. Sideline evaluation of concussion. UpToDate. 2016. http://www.uptodate.com/contents/sideline-evaluation-of-concussion. Accessed July 13, 2016.
13. Kontos AP, Elbin RJ, Schatz P, et al. A revised factor structure for the post-concussion symptom scale: baseline and postconcussion factors. Am J Sports Med. 2012;40(10):2375-2384.
14. Guskiewicz KM, Ross SE, Marshall SW. Postural stability and neuropsychological deficits after concussion in collegiate athletes. J Athl Train. 2001;36(3):263.
15. Mucha A, Collins MW, Elbin R, et al. A brief Vestibular/Ocular Motor Screening (VOMS) assessment to evaluate concussions preliminary findings. Am J Sports Med. 2014;42(10):2479-2486.
16. Bloom J. Vestibular and ocular motor assessments: Important pieces to the concussion puzzle. Athletic Training and Sports Health Care. 2013;5(6):246-248.
17. Covassin T, Elbin R, Harris W, Parker T, Kontos A. The role of age and sex in symptoms, neurocognitive performance, and postural stability in athletes after concussion. Am J Sports Med. 2012;40(6):1303-1312.
18. Kontos A, Sufrinko A, Elbin R, Puskar A, Collins M. Reliability and associated risk factors for performance on the Vestibular/Ocular Motor Screening (VOMS) tool in healthy collegiate athletes. Am J Sports Med. 2016;44(6):1400-1406.
19. Guskiewicz KM, McCrea M, Marshall SW, et al. Cumulative effects associated with recurrent concussion in collegiate football players: the NCAA Concussion Study. JAMA. 2003;290(19):2549-2555.
20. Lau B, Lovell MR, Collins MW, Pardini J. Neurocognitive and symptom predictors of recovery in high school athletes. Clin J Sport Med. 2009;19(3):216-221.
21. 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.
22. Mihalik JP, Register-Mihalik J, Kerr ZY, Marshall SW, McCrea MC, Guskiewicz KM. Recovery of posttraumatic migraine characteristics in patients after mild traumatic brain injury. Am J Sports Med. 2013;41(7):1490-1496.
23. Covassin T, Moran R, Elbin RJ. Sex differences in reported concussion injury rates and time loss from participation: An update of the National Collegiate Athletic Association injury surveillance program from 2004-2005 through 2008-2009. J Athl Train. 2016;51(3):189-194.
24. Root JM, Zuckerbraun NS, Wang L, et al. History of somatization is associated with prolonged recovery from concussion. J Pediatr. 2016;174:39-44.
25. Sufrinko A, Pearce K, Elbin RJ, et al. The effect of preinjury sleep difficulties on neurocognitive impairment and symptoms after sport-related concussion. Am J Sports Med. 2015;43(4):830-838.
26. Thomas DG, Apps JN, Hoffmann RG, McCrea M, Hammeke T. Benefits of strict rest after acute concussion: a randomized controlled trial. Pediatrics. 2015;135(2):213-223.
27. Choe M, Blume H. Pediatric posttraumatic Headache: a review. J Child Neurol. 2016;31(1):76-85.
28. Tepper SJ, Tepper DE. Breaking the cycle of medication overuse. Cleve Clin J Med. 2010;77(4):236-242.
29. Collins M, Kontos A, Reynolds E, Murawski C, Fu F. A comprehensive, targeted approach to the clinical care of athletes following sport-related concussion. Knee Surg Sports Traumatol Arthrosc. 2014;22(2):235-246.
30. Reynolds E, Collins MW, Mucha A, Troutman-Ensecki C. Establishing a clinical service for the management of sports-related concussions. Neurosurgery. 2014;75 Suppl 4:S71-S81.
31. Broglio SP, Collins MW, Williams RM, Mucha A, Kontos AP. Current and emerging rehabilitation for concussion: a review of the evidence. Clin Sports Med. 2015;34(2):213-231.
32. Master C, Scheiman M, Gallaway M, et al. Vision diagnoses are common after concussion in adolescents. Clin Pediatr (Phila). 2016;55(3):260-267.
33. Headache Classification Committee of the International Headache Society (IHS). The international classification of headache disorders, 3rd edition (beta version). Cephalalgia. 2013;33(9):629-808.
34. Kontos A, Deitrick JM, Reynolds E. Mental health implication and consequences following sport-related concussion. Brit J Sports Med. 2016;50(3):139-140.
35. Kontos AP, Covassin T, Elbin R, Parker T. Depression and neurocognitive performance after concussion among male and female high school and collegiate athletes. Arch Phys Med Rehabil. 2012;93(10):1751-1756.