PERSPECTIVE
Principles for return to learn after concussion
Return to Learn after Concussion
The 2012 Zurich Consensus Statement (1) recommends a graduated protocol for return to play following concussion, beginning with rest and followed by increasing levels of physical activity. With the growing recognition that both physical and mental exertion can aggravate concussion symptoms (2,3) and perhaps prolong recovery (4,5), the Zurich statement also highlights the importance of cognitive rest and the need to limit exertion with activities of daily living that may exacerbate symptoms. In children and adolescents, this would include the modification of school attendance and activities to avoid provocation of symptoms. Thus, it is important to consider developing principles and guidance for resuming academic activities after concussion. Research on the academic effects of concussion has generally shown no adverse long-term outcomes (6,7). In most cases, concussion symptoms and cognitive difficulties will improve in a matter of days (8). However, problems can persist for weeks or months, causing significant academic disruption. There are limited empirical data specifically addressing the academic effects of concussion. Medical professionals who diagnose and treat concussion will often make recommendations to a student’s school so as to try to reduce symptoms and foster optimal recovery. A number of authors have developed recommendations for academic re-entry and accommodations after concussion (4,9–14) and the Centers for Disease Control and Prevention offers ‘Heads Up for Schools’ materials with concussion information and practical guidance (http://www.cdc.gov/concussion/ HeadsUp/schools.html). There is emerging consensus on the optimal process for return to school, but still a lack of research. Teachers and other school staff are ultimately responsible for implementing any recommendations, and for ensuring that the recovering student’s needs are considered and addressed. We propose the following principles and practical guidance, in the hope that this will stimulate discussion and encourage empirical study of best practices. There are several graduated return to learn protocols in the literature that are analogous to the Zurich graduated return to play protocol. The Oregon Center for Applied Science has a six step protocol with two home steps and four school steps (15). Halstead et al. (14) recommend that a student stay home from school until able to tolerate 30–45 min of cognitive
1286
activity, at which point a gradual return to school is suggested. Master et al. propose a six step plan that includes: a prescription for physical and cognitive rest, a gradual reintroduction of cognitive activity, homework at home before schoolwork at school, school re-entry, gradual reintegration into school and full return to school. They introduce the concept of subsymptom threshold for cognitive activity and the strategy of pacing, or gradually increasing cognitive activity while staying below the student’s symptom threshold (9). In this article, we build on their plan and attempt to integrate aspects of other return to learn approaches. While a standard graduated protocol may work well for return to play, as students return to learn after a concussion a more flexible approach may be needed for each individual student. We summarise relevant background literature in Data S1. We propose principles based on this background literature. These principles are meant to help inform the adjustment of an individual student to his/ her particular school environment. We then present an initial approach to be further developed and refined and discuss the emerging consensus on return to learn. As can be seen in Data S1, the current literature is suggestive of a complex and dynamic set of injury mechanisms at work in the brain after concussion associated with a window of dysfunction and increased vulnerability. In the context of sports, there has been a heightened focus on minimising the risk of more severe injury and symptoms by removing the athlete from play until recovery is complete. However, in the academic context, removing students from school until they are recovered is not practical. In this sense, the pressure to keep going in school after concussion may actually be greater than the pressure to return to play. There is growing attention to the academic effects of concussion in the literature and emerging agreement on some guiding principles for return to learn.
Guiding principles for return to learn after concussion
•
During recovery, avoid re-injury and over-exertion both at home and at school.
ª 2014 John Wiley & Sons Ltd Int J Clin Pract, November 2014, 68, 11, 1286–1288. doi: 10.1111/ijcp.12517
Perspective
•
Immediately after concussion, a limited period of complete rest (physical and mental) is recommended until the most significant symptoms have resolved (this may help shorten recovery time and reduce risk for persistent symptoms). • As symptoms improve, gradually increase cognitive activity and environmental stimulation. • Stay below the individual student’s ‘symptom threshold,’ as overdoing it mentally (thinking, stress, stimulation) can aggravate symptoms and may complicate recovery. • Pace activities by limiting cognitive exertion and including rest breaks before reaching the student’s symptom threshold. • Adapt the school environment and academic demands (accommodations) to facilitate a gradual increase in school activity while staying below the symptom threshold. • Recognise that the student’s cognitive functioning may be impaired, including slowed processing, trouble concentrating, memory problems and limited mental stamina. • A team-based approach is best, with collaboration between the student and family, healthcare professionals and school staff. • Maintaining academic progress and recovering from concussion can be conflicting goals, so students need help to reduce academic demands and stress and to set the conditions for optimal recovery.
The Return to Learn Process A step by step plan for return to learn has advantages in providing a consistent yet flexible approach for parents, health professionals and school personnel that could be adopted across various schools. Unfortunately, this approach could also lead to fitting an individual student into each step rather than using the guidelines as a starting point to develop an individualised plan for facilitating a particular student’s return to school. Alternatives to the limitations of a linear step by step approach are available in the literature (10,11,14,16). Principles for return to learn can integrate these approaches and contribute to developing an individualised plan for a particular student’s recovery from concussion. Tables 1–3 and additional discussion of Table 1 are included in Data S2. Table 1 proposes three phases (ABC) for return to learn. Progression through these phases involves a gradual increase in activity while attempting to remain below the student’s ‘symptom threshold’. This threshold is based on the length of time and the intensity of cognitive activity, other activity and environmental stimulation ª 2014 John Wiley & Sons Ltd Int J Clin Pract, November 2014, 68, 11, 1286–1288
that results in an exacerbation of symptoms (9,17). ‘Pacing’ of activity can include rest breaks at home or in school before the student reaches a symptom threshold (e.g. a rest break could be built into the students schedule for 5–15 min every 30–45 min, or at home a rest break at 80% of the time it takes for symptom exacerbation). Use of the SCAT3 (http:// bjsm.bmj.com/content/47/5/259.full.pdf) or Child SCAT3 (ages 5–12; http://bjsm.bmj.com/content/47/ 5/263.full.pdf) Symptom Evaluation, or another symptom scale, is recommended as a way to monitor symptoms (1). A form such as that included in the REAP guidelines (http://www.rockymountain hospitalforchildren.com/sports-medicine/concussionmanagement/reap-guidelines.htm) can be sent to school with the student. Most students recovering from concussion will immediately benefit from a core group of accommodations, listed in Table 2. As time goes on, accommodations can (and should) be adjusted more to fit the individual student’s needs. Table 3 presents examples of typical symptoms during each phase and more specific examples of physical, cognitive and academic activities, as well as academic accommodations that may be useful with these symptoms. A ‘symptom wheel’ approach may be helpful in tailoring accommodations to fit the student’s needs http://www.naspon line.org/publications/cq/40/6/return-to-learning.aspx. The REAP guidelines (Reduce-Educate-Accommodate-Pace) for returning to school after concussion noted above reflect the above literature and emphasise the importance of teamwork among parents, school athletic and academic professionals and medical professionals. Additional guidance for return to learn is available in the literature (9,18). The purpose of the phase ABC approach presented in Table 1 is to propose general principles, to be further developed in the literature, for implementing a consistent yet flexible approach to returning individual students to school after a concussion. It must be emphasised again that this approach is aimed primarily at those students who will have a typical recovery from concussion in 1–2 weeks. When symptoms are more severe or prolonged, return to learn recommendations are best developed in the context of an individualised and comprehensive management plan put together by concussion specialists in conjunction with the school team. Also, while early intervention and reassurance can help to optimise recovery, over-reacting may sometimes be problematic, too, such as ‘cocooning’ a child or keeping children out of school longer than necessary. One of the most challenging aspects of managing the return to school after concussion is the dynamic and variable nature of the symptoms and of recovery. This
1287
1288
Perspective
can be quite vexing to students, parents and teachers trying to figure out what kinds of supports are needed and for how long. Regular meetings between parents and school staff will help in making adjustments to the return to learn plan as recovery progresses and also help to avoid either over- or under-serving the student. Middle and high school students can be included in these meetings as well. A Case Example presented in Data S3 may help to illustrate some of these issues.
Summary There is a rapidly growing knowledge base on concussion, particularly regarding what is now understood to be multiple injury pathways and recovery trajectories. While resolution of symptoms is most often complete within 2 weeks, recovery can take longer, especially in children and adolescents. There is growing attention to return to learn but no consensus yet or accepted guidelines. We have proposed a set of principles, a graduated return to learn protocol, and a set of core academic accommodations that is informed by the broader concussion literature as well as the work of others who have written on this topic. The evidence base remains limited in this area but the time may be ripe for an organisation such as the
References 1 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): 250–8. 2 Gioia G, Vaughan C, Reesman J et al. Characterizing post-concussion exertional effects in the child and adolescent (abstract). J Int Neuropsychol Soc 2010; 16(S1): 178. 3 Majerske CW, Mihalik JP, Ren D et al. Concussion in sports: postconcussive activity levels, symptoms, and neurocognitive performance. J Athletic Training 2008; 43(3): 265. 4 Sady MD, Vaughan CG, Gioia GA. School and the concussed youth-recommendations for concussion education and management. Phys Med Rehabil Clin N Am 2011; 22(4): 701. 5 Brown NJ, Mannix RC, O’Brien MJ, Gostine D, Collins MW, Meehan WP. Effect of cognitive activity level on duration of post-concussion symptoms. Pediatrics 2014; 133(2): e299–e304. 6 Light RAR, Satz P, Zaucha K, McCleary C, Lewis R. Mild closed-head injury in children and adolescents: behavior problems and academic outcomes. J Consult Clin Psychol 1998; 66(6): 1023–9. 7 Satz PZK, McCleary C, Light R, Asarnow R, Becker D. Mild head injury in children and adolescents: a review of studies. Psychol Bull 1997; 122(2): 107–31. 8 Kirkwood MW, Yeates KO, Taylor HG, Randolph C, McCrea M, Anderson VA. Management of pediatric mild traumatic brain injury: a neuropsychological review from injury through recovery. Clin Neuropsychol 2008; 22(5): 769–800.
National Collaborative on Children’s Brain Injury, which is comprised of leading paediatric brain injury experts from medical and academic communities, to form a consensus for return to learn after concussion. J. G. Baker,1 B. P. Rieger,2 K. McAvoy,3 J. J. Leddy,4 C. L. Master,5 S. J. Lana,6 B. S. Willer7 1 School of Social Work, Nuclear Medicine, Orthopaedics and Sports Medicine, University at Buffalo, Buffalo, NY, USA 2 Physical Medicine and Rehabilitation, Upstate Concussion Center, SUNY Upstate Medical University, Syracuse, NY, USA 3 Center for Concussion, Rocky Mountain Youth Hospital for Children, Denver, CO, USA 4 Orthopaedics and Sports Medicine, University at Buffalo, Buffalo, NY, USA 5 Department of Surgery and Pediatrics, The Children’s Hospital of Philadelphia, Philadelphia, PA, USA 6 Department of Pediatrics, University at Buffalo, Buffalo, NY, USA 7 Department of Psychiatry, University at Buffalo, Buffalo, NY, USA Correspondence to: John G. Baker, PhD, School of Social Work, 219 Parker Hall, University at Buffalo, Buffalo, NY 14214, USA Tel.: + 716 838 5889, x165 Fax: + 716 838 4918 Email:
[email protected]
9 Master CL, Gioia GA, Leddy JJ, Grady MF. Importance of ‘Return-to-Learn’ in pediatric and adolescent concussion. Pediatr Ann 2012; 41(9): 1–6. 10 McAvoy K. Providing a continuum of care for concussoin using existing educational frameworks. Brain Inj Prof [Internet] 2012; 9(1): 26–7. http://is suu.com/bipmagazine/docs/bip30?mode=window& viewMode=doublePage. 11 McAvoy K. Return to learning: going back to school following a concussion. Communique 2012; 40(6): http://www.nasponline.org/publications/cq/ 40/6/return-to-learning.aspx. 12 McGrath N. Supporting the student-athlete’s return to the classroom after a sport-related concussion. J Athletic Training 2010; 45(5): 492. 13 Valovich McLeod TC, Gioia GA. First words-cognitive rest: the often neglected aspect of concussion management. Athletic Ther Today 2010; 15(2): 1. 14 Halstead ME, McAvoy K, Devore CD et al. Returning to learning following a concussion. Pediatrics 2013; 132(5): 948–57. 15 Oregon Center for Applied Science I. Concussion Management Policy and Resource Handbook. http:// orcas-sportsconc2.s3.amazonaws.com/files/A_CMTH andbook.pdf, (accessed 2013). 16 McAvoy K. (2009) REAP the benefits of good concussion management. Centennial, CO: Rocky Mountain Sports Medicine Institute Center for Concussion. http://issuu.com/healthone/docs/reap_april_2011 (accessed 2013). 17 Gagnon I, Galli C, Friedman D, Grilli L, Iverson GL. Active rehabilitation for children who are slow
to recover following sport-related concussion. Brain Inj 2009; 23(12): 956–64. 18 Rieger BP. Suggestions for facilitating return to learn after concussion. Brain Inj Prof [Internet] 2012; 9(1): 22–4. http://issuu.com/bipmagazine/ docs/bip30?mode=window&viewMode=doublePage (accessed 2013).
Acknowledgements We thank the following organisations for financial support: The Robert Rich Family Foundation, Program for Understanding Childhood Concussion and Stroke, Buffalo Bills (Ralph Wilson) Team Physician Fund and the Buffalo Sabres Foundation.
Disclosure The authors report no known conflicts of interest.
Supporting Information Additional Supporting Information may be found in the online version of this article: Data S1. Background literature. Data S2. Tables 1–3 and Discussion. Data S3. Case example. Paper received March 2014, accepted July 2014
ª 2014 John Wiley & Sons Ltd Int J Clin Pract, November 2014, 68, 11, 1286–1288
Supplemental Online Content 1 Background Literature Immediately after a concussion there is a neurometabolic cascade of brain neurochemical changes that produces an initial hyper-‐metabolic state as the brain attempts to restore homeostasis. This is followed by a state of metabolic depression as cerebral blood flow declines and brain energy demand exceeds supply (1). This may explain why some symptoms are delayed in onset or worsen over time (2), and why some students report symptom resolution before they demonstrate physical and cognitive homeostasis (3). It is important to consider that students who are asymptomatic at rest can become symptomatic during physical or cognitive exertion and may have difficulty performing physical and cognitive tasks (2). For example, Maugans et al. (4) found that alterations in cerebral blood flow lasted 14 days for 73% and at least 30 days for 36% of a sample of 11 to 15 year old athletes with concussion versus controls. Cognitive activity level has been shown to affect the duration of symptoms among a pediatric sample with sport related or similar concussion (5). Nonetheless, questions have been raised in the literature regarding whether absolute rest is advisable for longer than 3 days after concussion (6). In addition to physiological dysfunction, cervical injury and vestibular and oculomotor dysfunction may lead to difficulty with cognition and resuming school-‐related activity. A cervical injury, if not properly treated, may result in prolonged symptoms such as headache, dizziness, and difficulty with concentration and memory that may be confused with concussion symptoms (7-‐9). Vestibular and oculomotor dysfunction will also require
specialized treatment and specific academic accommodations (10-‐15). Sleep disturbance, common to concussion, may also affect many other aspects of recovery (16-‐18).
A basis for prolonged cognitive difficulties focusing more on injury to individual
neurons can also be found in recent literature (19). Animal models support a role for dynamic stretch of neurons causing rupture of axon microtubules that affects axon transport, leading to swelling, protein accumulation, and ultimately axon degeneration. Imaging studies have found white matter damage during the acute phase of concussion (1 to 6 days post injury) and at follow-‐up around 6 months later among college football players using diffusion tensor imaging (DTI) (20). Other studies have found white matter DTI changes after concussion, and even after subconcussive hits from playing football or hockey among high school (21) and college (22) student athletes. These types of white matter changes appear to reflect microstructural changes to neurons (23-‐25). Associations between DTI changes and decreased reaction time have been found (26), that may help to explain slowed information processing after concussion. Nonetheless questions have been raised regarding the potential clinical applications of these types of findings on DTI imaging (27). Functional MRI (fMRI) imaging studies have found unique individual patterns of abnormal activation after concussion. These patterns have been interpreted to reflect a compensatory mechanism whereby the brain allocates additional processing resources to accomplish a task. While performance may remain average for a period of time, these compensatory mechanisms may contribute to fatigue, slow and inefficient information processing, and other symptoms over an extended period of cognitive activity (28-‐32). A symptom threshold using length of time to symptom exacerbation has been suggested for
cognitive activity (33). This symptom threshold is analogous to the heart rate threshold used for exercise rehabilitation (34). Pilot data suggest that almost one fourth (24%) of a sample of 50 students ages 13 to19, who successfully completed exercise treadmill testing and return to play, may experience problems in school that they didn’t experience before their concussion (35). A recent survey found that while many primary care providers were aware of the importance of cognitive rest after concussion, many fewer actually made a written recommendation for cognitive rest (36). A common problem observed by those working with students recovering from concussion—but one that has not yet been specifically addressed in the research literature—is the effect of academic stress on symptoms and recovery. Especially in cases of prolonged or complicated recovery, students must often cope with a variety of school-‐ related stressors, separate from the direct demands of the academic work alone. Such stressors can include falling behind academically (despite a subjective sense of working harder), lower than usual grades, attitudes of teachers and other students who think concussed students are not injured or struggling because they look normal, needing help but not wanting to stand out or be perceived as getting special treatment, feeling ‘stupid’ because of cognitive or speech problems, and social isolation due to decreased participation in after-‐school activities. These difficulties emerge in the context of increased susceptibility to depression or other psychiatric disorders (37, 38) due to the brain injury itself. High-‐functioning students may have little pre-‐injury experience with “failure,” and may be particularly hard on themselves as they watch the homework pile up and their
grades drop. Students with lower pre-‐injury cognitive functioning may have less cognitive reserve and thus may be more vulnerable to poor outcome after injury (39). References 1. Giza CC, Hovda DA. The Neurometabolic Cascade of Concussion. J Athl Train. 2001;36(3):228-‐35. 2. McCrory P, Johnston K, Meeuwisse W, Aubry M, Cantu R, Dvorak J, et al. Summary and agreement statement of the 2nd International Conference on Concussion in Sport, Prague 2004. Clin J Sport Med. 2005;15(2):48-‐55. 3. Lovell MR, Collins MW, Iverson GL, Field M, Maroon JC, Cantu R, et al. Recovery from mild concussion in high school athletes. J Neurosurg. 2003;98(2):296-‐301. 4. Maugans TA, Farley C, Altaye M, Leach J, Cecil KM. Pediatric sports-‐related concussion produces cerebral blood flow alterations. Pediatrics. 2012;129(1):28-‐37. 5. Brown NJ, Mannix RC, O’Brien MJ, Gostine D, Collins MW, Meehan WP. Effect of cognitive activity level on duration of post-‐concussion symptoms. Pediatrics. 2014;133(2):e299-‐e304. 6. Silverberg ND, Iverson GL. Is Rest After Concussion" The Best Medicine?": Recommendations for Activity Resumption Following Concussion in Athletes, Civilians, and Military Service Members. The Journal of Head Trauma Rehabilitation. 2012. 7. Sturzenegger M, Radanov B, Winter P, Simko M, Farra A, Di Stefano G. MRI‐based brain volumetry in chronic whiplash patients: no evidence for traumatic brain injury. Acta Neurologica Scandinavica. 2008;117(1):49-‐54. 8. Endo K, Ichimaru K, Komagata M, Yamamoto K. Cervical vertigo and dizziness after whiplash injury. European Spine Journal. 2006;15(6):886-‐90. 9. Leddy JJ. Cervicogenic Post Concussion Disorder: A Pain in the Neck. Brain Injury Professional [Internet]. 2012; 9(1):[18-‐9 pp.]. Available from: http://issuu.com/bipmagazine/docs/bip30?mode=window&viewMode=doublePage. 10. Alsalaheen BA, Mucha A, Morris LO, Whitney SL, Furman JM, Camiolo-‐Reddy CE, et al. Vestibular rehabilitation for dizziness and balance disorders after concussion. Journal of Neurologic Physical Therapy. 2010;34(2):87. 11. Thiagarajan P, Ciuffreda KJ, Ludlam DP. Vergence dysfunction in mild traumatic brain injury (mTBI): a review. Ophthalmic and Physiological Optics. 2011;31(5):456-‐68. 12. Hillier SL, McDonnell M. Vestibular rehabilitation for unilateral peripheral vestibular dysfunction. Cochrane Database Syst Rev. 2011;2. 13. Ciuffreda KJ, Kapoor N, Rutner D, Suchoff IB, Han M, Craig S. Occurrence of oculomotor dysfunctions in acquired brain injury: a retrospective analysis. Optometry-‐ Journal of the American Optometric Association. 2007;78(4):155-‐61. 14. Scheiman M, Cotter S, Kulp MT, Mitchell GL, Cooper J, Gallaway M, et al. Treatment of Accommodative Dysfunction in Children: Results from an Random Clinical Trial. Optometry and vision science: official publication of the American Academy of Optometry. 2011;88(11):1343.
15. Mucha A, Collins, M., French , J. Augmenting Neurocognitive Assessment in the Evaluation of Sports Concussion : How Vestibular and Occular Issues Impact Recovery. Brain Injury Professional [Internet]. 2012; 9(1):[12-‐5 pp.]. Available from: http://issuu.com/bipmagazine/docs/bip30?mode=window&viewMode=doublePage. 16. Kaufman Y, Tzischinsky O, Epstein R, Etzioni A, Lavie P, Pillar G. Long-‐term sleep disturbances in adolescents after minor head injury. Pediatric neurology. 2001;24(2):129-‐ 34. 17. Ouellet M-‐C, Beaulieu-‐Bonneau S, Morin CM. Insomnia in patients with traumatic brain injury: frequency, characteristics, and risk factors. The Journal of Head Trauma Rehabilitation. 2006;21(3):199. 18. Gosselin N, Thériault M, Leclerc S, Montplaisir J, Lassonde M. Neurophysiological anomalies in symptomatic and asymptomatic concussed athletes. Neurosurgery. 2006;58(6):1151-‐61. 19. Tang-‐Schomer MD, Patel AR, Baas PW, Smith DH. Mechanical breaking of microtubules in axons during dynamic stretch injury underlies delayed elasticity, microtubule disassembly, and axon degeneration. The FASEB Journal. 2010;24(5):1401-‐10. 20. Henry LC, Tremblay J, Tremblay S, Lee A, Brun C, Lepore N, et al. Acute and chronic changes in diffusivity measures after sports concussion. Journal of neurotrauma. 2011;28(10):2049-‐59. 21. Bazarian JJ, Zhu T, Blyth B, Borrino A, Zhong J. Subject-‐specific changes in brain white matter on diffusion tensor imaging after sports-‐related concussion. Magnetic Resonance Imaging. 2012;30(2):171-‐80. 22. Koerte IK, Kaufmann D, Hartl E, Bouix S, Pasternak O, Kubicki M, et al. A prospective study of physician-‐observed concussion during a varsity university hockey season: white matter integrity in ice hockey players. Part 3 of 4. Neurosurgical Focus. 2012;33(6):E3. 23. Aoki Y, Inokuchi R, Gunshin M, Yahagi N, Suwa H. Diffusion tensor imaging studies of mild traumatic brain injury: a meta-‐analysis. Journal of Neurology, Neurosurgery & Psychiatry. 2012;83(9):870-‐6. 24. Niogi SN, Mukherjee P, Ghajar J, Johnson CE, Kolster R, Lee H, et al. Structural dissociation of attentional control and memory in adults with and without mild traumatic brain injury. Brain. 2008a;131(12):3209-‐21. 25. Niogi S, Mukherjee P, Ghajar J, Johnson C, Kolster R, Sarkar R, et al. Extent of microstructural white matter injury in postconcussive syndrome correlates with impaired cognitive reaction time: a 3T diffusion tensor imaging study of mild traumatic brain injury. American Journal of Neuroradiology. 2008b;29(5):967-‐73. 26. Niogi S, Mukherjee P, Ghajar J, Johnson C, Kolster R, Sarkar R, et al. Extent of microstructural white matter injury in postconcussive syndrome correlates with impaired cognitive reaction time: a 3T diffusion tensor imaging study of mild traumatic brain injury. American Journal of Neuroradiology. 2008;29(5):967-‐73. 27. Silver JM. Diffusion tensor imaging and mild traumatic brain injury in soldiers: abnormal findings, uncertain implications. American Journal of Psychiatry. 2012;169(12):1230-‐2. 28. Chen JK, Johnston KM, Collie A, McCrory P, Ptito A. A validation of the post concussion symptom scale in the assessment of complex concussion using cognitive testing and functional MRI. J Neurol Neurosurg Psychiatry. 2007;78(11):1231-‐8. Epub 2007/03/21.
29. Chen JK, Johnston KM, Frey S, Petrides M, Worsley K, Ptito A. Functional abnormalities in symptomatic concussed athletes: an fMRI study. Neuroimage. 2004;22(1):68-‐82. Epub 2004/04/28. 30. Chen JK, Johnston KM, Petrides M, Ptito A. Recovery from mild head injury in sports: evidence from serial functional magnetic resonance imaging studies in male athletes. Clin J Sport Med. 2008;18(3):241-‐7. Epub 2008/05/13. 31. Lovell MR, Pardini JE, Welling J, Collins MW, Bakal J, Lazar N, et al. Functional brain abnormalities are related to clinical recovery and time to return-‐to-‐play in athletes. Neurosurgery. 2007;61(2):352-‐9; discussion 9-‐60. Epub 2007/09/01. 32. Leddy JJ, Cox JL, Baker JG, Wack DS, Pendergast DR, Zivadinov R, et al. Exercise Treatment for Postconcussion Syndrome: A Pilot Study of Changes in Functional Magnetic Resonance Imaging Activation, Physiology, and Symptoms. The Journal of Head Trauma Rehabilitation. 2012. 33. Gagnon I, Galli C, Friedman D, Grilli L, Iverson GL. Active rehabilitation for children who are slow to recover following sport-‐related concussion. Brain Injury. 2009;23(12):956-‐64. 34. Leddy JJ, Kozlowski K, Donnelly JP, Pendergast DR, Epstein LH, Willer B. A preliminary study of subsymptom threshold exercise training for refractory post-‐ concussion syndrome. Clinical Journal of Sport Medicine. 2010;20(1):21. 35. Leddy JJ, Darling, S., Baker, J. G., Williams, A. J., Surace, A., Willer, B. S. . The Predictive Value of Treadmill Exercise Testing versus Computerized Neuropsychological Testing for Return to Sport in Adolescents with Concussion. . Annual Meeting of the North American Brain Injury Association; . Miami, FL2012, September 36. Arbogast KB, McGinley AD, Master CL, Grady MF, Robinson RL, Zonfrillo MR. Cognitive Rest and School-‐Based Recommendations Following Pediatric Concussion The Need for Primary Care Support Tools. Clinical pediatrics. 2013. 37. Max JE, Wilde EA, Bigler ED, MacLeod M, Vasquez AC, Schmidt AT, et al. Psychiatric Disorders After Pediatric Traumatic Brain Injury: A Prospective, Longitudinal, Controlled Study. The Journal of neuropsychiatry and clinical neurosciences. 2012;24(4):427-‐36. 38. McCrory P, Meeuwisse WH, Aubry M, Cantu B, Dvořák J, Echemendia RJ, et al. Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012. British Journal of Sports Medicine. 2013;47(5):250-‐8. 39. Fay TB, Yeates KO, Taylor HG, Bangert B, Dietrich A, Nuss KE, et al. Cognitive reserve as a moderator of postconcussive symptoms in children with complicated and uncomplicated mild traumatic brain injury. Journal of the International Neuropsychological Society. 2010;16(1):94.
Table 1 Proposed Return to Learn Protocol 1. Phase A: Out of school and complete rest with very limited physical and cognitive activity for 1-‐3 days (1). a. May do light walking, light reading, and watch TV. No computer work, video games, or texting. b. Contact school personnel to arrange for gradual return to school with accommodations (2, 3) c. Some students may require more than 3 days, although more than7 days is unlikely. If symptoms are more severe and/or persist for more than10 days, consider referral to a concussion management clinic. 2. Phase B: Gradual increase in activity at home with “pacing” to stay below the student’s “symptom threshold.” a. Parents can assess a student’s readiness to concentrate in school. For example, use of pacing with various cognitive activities for 10 minute intervals followed by a rest break. Then, use of pacing with reading and homework to build up to 30-‐ 45 minutes to approximate the time required of a typical school period (3) b. Other non-‐physical activities using pacing to stay below the symptom threshold. The effects of environmental stimulation should be noted, especially noise and light. Limit stimulation to stay below symptom
threshold, and consider student’s readiness to return to crowded hallways or cafeteria in school. 3. Phase C1: Return to school with monitoring of symptom exacerbation by the school nurse or another appropriate school staff member a. If feeling better during phase B, attempt one half day of school. Monitoring of activity tolerance after two periods by the school nurse or other appropriate school staff member (mandatory check-‐in of student with staff member). Consider use of SCAT3 or Child SCAT3 symptom checklist. b. Implement core academic accommodations with additional supports based on an individual student’s needs, (e.g., as proposed in the REAP guidelines(2) c. Mandatory breaks in the school nurse's office to stay below symptom threshold. 4. Phase C2: Return to school full time with accommodations
a. If tolerating one half day of school, gradually increase to full day using pacing (e.g., rest breaks) to stay below symptom threshold. b. Continue to refine academic accommodations based on the student’s needs (see, for example, REAP guidelines and Response to Management on the Universal Tier (2, 4) c. Continued monitoring of activity tolerance by the school nurse. Gradual removal of accommodations as recovery progresses. If unable to tolerate return to school, consider referral to a concussion clinic.
5. Regarding Return to Play, no structured exercise or gym until fully participating in school without accommodations. Once resting symptoms return to baseline, as measured by symptom checklists at home and symptom checklists and teacher feedback at school, and once the student has completed the return to learn process (full school participation without accommodation), only then can the graduated return to play process be initiated. a. Consider computerized cognitive testing to assess cognitive recovery (5, 6). b. Consider exercise treadmill testing to assess physiologic recovery (7).
Discussion In Table 1, we have not included timelines beyond an initial period of rest to ensure that an individual student who is slow to recover, or who needs more specialized attention (e.g., cervical physical therapy, exercise rehabilitation, vestibular or oculomotor rehabilitation), would not be moved too quickly to the next phase. We have provided some guidance as to when a student may be ready to move to the next phase. While most students experience a reduction in symptoms from a concussion within 7 to 10 days, the studies noted above suggest that in addition to the transient effects from a concussion, there may be other changes that take longer to resolve that affect students who are slow to recover. Progression may be accelerated for those who recover faster (e.g., older adolescents) or delayed for those who are recovering more slowly (e.g., children, younger adolescents, multiple concussions, recent previous concussion, etc.). As noted in the Zurich Guidelines, persistent symptoms (specified as greater than 10 days) are generally reported in 10–15% of concussions. McCrea et al. 2012(8) found that 10% of student athletes took more than 7 days to recover, which was associated with unconsciousness, posttraumatic amnesia, and more severe acute symptoms. Thus, this return to learn process would generally be completed within a couple of weeks for most students. Some students may require less time, and students can be encouraged to return to school with necessary accommodations as soon as possible. The important role of the school nurse or another appropriate school staff member is reflected in Phase C. As noted in Table 1, students should complete the entire return to learn process and be fully participating in school without accommodations before the graduated return to play protocol is initiated. From a
practical perspective, this will necessitate communication between the medical team, parents, and school staff, which can be accomplished with formal symptom checklists or feedback forms, or more informal communications such as phone calls or e-‐mails. If symptoms persist for more than 10 days(9) from the date of injury, referral to a specialized concussion clinic is indicated.
Table 2 Core Academic Accommodations for Students Recovering From Concussion Academic Accommodation
Rationale
Reduce work load to essential material.
Academic work takes longer and requires
For example, assign fewer homework
more effort after concussion. Students
problems, shorten reading assignments,
usually feel obligated to do all the work that
and postpone some work.
is expected or assigned. Completing the usual amount of work takes extra effort after concussion, which in turn can aggravate symptoms, prevent the student from getting much-‐needed rest, and in some cases may complicate recovery.
Provide rest breaks in a quiet and dimly
Fatigue and limited mental stamina is a
lit place. Breaks should be at least 15-‐20
common problem after concussion, probably
minutes long. The student does not have to due to inefficient processing and abnormal sleep (although that’s okay), but should
energy utilization in the brain. The brain
avoid any mental exertion or stimulation.
seems to tire more quickly with an
Breaks should be mandatory and
associated increase in symptoms. Making
scheduled in advance, and their frequency the breaks mandatory avoids problems with can be adjusted as needed.
student non-‐compliance, and also with inappropriate attributions about why the student is taking a break (e.g., doesn’t like math class anyway, or probably forgot to do her homework).
Shorten the school day as needed, with a
As noted above, students recovering from
plan in place to help the student with work
concussion usually tire much more quickly
from classes that are missed
than normal. As they tire, symptoms increase, and they will no longer be able to profit from being in class or school. At the same time, sending a student home from school early without a plan in place to help make up for missed classes or material can actually cause increased academic stress.
Limit exposure to environmental
Any kind of stimulation can put a demand on
stimulation including noise, light, and
the brain as it processes and filters input.
commotion.
Bright, noisy cafeterias, loud band and chorus rooms, crowded hallways and stairwells, and the commotion on the school bus can all aggravate symptoms and increase fatigue.
To the extent possible, postpone testing
Performance on lengthy and/or demanding
(especially high-‐stakes testing) until the
tests or assignments will be sub-‐optimal due
student is recovered.
to cognitive problems and symptom burden, and the increased stress due to this will be counterproductive in terms of fostering recovery.
Frequent re-‐assessment of student’s
Concussion recovery is dynamic, variable,
symptoms and recovery so that
and usually complete in a week or two.
accommodations can be adjusted (in either
Keeping a student out of activity any longer
direction) as student’s condition evolves
than necessary can be as problematic sometimes as a premature return to full activity.
Table 3 Examples of symptoms, and physical, mental, and academic adjustments
Symptoms
Physical
Mental
Phase A Very significant Sleep and rest as Rest as much as
Academic Out of school
symptoms such much as needed needed
as sleeping
Don’t do homework
much more than
Avoid bright light,
usual, bad
loud noise,
Notify school about
headache, or
commotion, crowds, concussion
very sensitive to
emotional stress, and
noise and light
cognitive exertion
such as reading No screen time
Phase B Symptoms are Sleep and rest as May do some light Early
noticeably
Out of school
much as needed cognitive activity as
improving Student is still sleeping a lot, is
tolerated
Avoid strenuous or vigorous
having trouble
Can begin to do some schoolwork but only
Limited screen time for limited periods of
activities falling or staying
(enough to fight
asleep, and
boredom and feeling
May do light
isolated)
Notify school that
walking as
student is able to do
Take at least 15-‐30
some work, but is still
min rest breaks
very limited, and
between activities
request that only
always feels tired
Student can feel tolerated moderately good
time, as tolerated
when rested but symptoms are easily aggravated by activity or stimulation Student tolerates less than 20 minutes of schoolwork before having to stop due to symptoms
that involve mental essential assignments exertion (reading,
be sent home
conversation,
computer) or
stimulation (noise, light, or commotion) Avoid bright and noisy places such as malls, grocery stores, and sporting events.
Phase B Symptoms are Continue to rest May do moderate Later
improving but as much as
cognitive activity as Continue to focus on
are still present needed, including tolerated
only essential
taking short rest
academic material
Student is still
breaks
Screen time can be
sleeping poorly throughout the
increased, as
Provide academic
and/or sleeping day
tolerated
accommodations
more than usual,
including (but not
and feels tired Light walking is Parents can assess
limited to) extended
all the time
recommended at tolerance of
time, quiet location for
least once per day environmental
testing, and reduced
Student can
for 15-‐30
stimulation.
work load
tolerate at least minutes, as 30 minutes of
tolerated
If necessary, provide
homework
supplementary
before having to
individualized tutoring
stop due to symptoms Symptoms are improved after a 15-‐30 minute rest break
Phase C No symptoms or
Consider effect on
Can attend school but
Early
some residual
non-‐school activities only on a part-‐time
symptoms at
on ability to complete basis and no more
rest
assigned academic
than a half-‐day
work, but also
Sleeping fairly
consider emotional
Schedule one or two
well but still
benefits of non-‐
15-‐20 minute
feels more tired
academic activities
mandatory rest breaks
than usual
during the school day
Can tolerate at
Check in with school
least moderate
nurse after first two
physical activity
periods, then less
such as walking
often, until 1-‐2 times
for 15 minutes
per week
Can tolerate
Provide academic
mental activity
accommodations
for at least 2-‐3
including (but not
hours before
limited to) extended
needing rest
time, quiet location for
break
testing, and reduced
work load
15-‐30 minute
rest break
improves
Phase C No symptoms or
Can participate in all Can attend school full-‐
Later
only mild
activities as tolerated time, but with rest-‐
symptoms
breaks and/or
Consider effect on
accommodations
Sleeping
non-‐school activities
normally, but
on ability to complete 15-‐20 minute rest
may still fatigue
assigned academic
breaks when needed
more easily by
work, but also
end of school or
consider emotional
Optional use of
other activities
benefits of non-‐
academic
academic activities
accommodations, as
Symptoms may be aggravated but only by sustained or intense exertion or stimulation
needed
Full
No symptoms at A Healthcare
Recovery rest and with
Concussion-‐related
professional may home activities
academic
both physical
consider start of without restriction
accommodations can
and mental
the Graduated
be discontinued
activity
Return to play
steps.
Not taking any medication for concussion symptoms
All cognitive and
References 1. Silverberg ND, Iverson GL. Is Rest After Concussion "The Best Medicine?": Recommendations for Activity Resumption Following Concussion in Athletes, Civilians, and Military Service Members. J Head Trauma Rehabil. 2012. Epub 2012/06/13. 2. McAvoy K. Return to Learning: Going Back to School Following a Concussion. Communique. 2012b;40(6). 3. Master CL, Gioia GA, Leddy JJ, Grady MF. Importance of ‘Return-‐to-‐Learn’in Pediatric and Adolescent Concussion. Pediatric annals. 2012;41(9). 4. McAvoy K. Providing a Continuum of Care for Concussoin using Existing Educational Frameworks. Brain Injury Professional [Internet]. 2012a; 9(1):[26-‐7 pp.]. Available from: http://issuu.com/bipmagazine/docs/bip30?mode=window&viewMode=doublePage. 5. Schmidt JD, Register-‐Mihalik JK, Mihalik JP, Kerr ZY, Guskiewicz KM. Identifying Impairments after Concussion: Normative Data versus Individualized Baselines. Med Sci Sports Exerc. 2012;44(9):1621-‐8. Epub 2012/04/25. 6. Echemendia RJ, Iverson GL, McCrea M, Macciocchi SN, Gioia GA, Putukian M, et al. Advances in neuropsychological assessment of sport-‐related concussion. British Journal of Sports Medicine. 2013;47(5):294-‐8. 7. Leddy JJ, Baker JG, Kozlowski K, Bisson L, Willer B. Reliability of a graded exercise test for assessing recovery from concussion. Clin J Sport Med. 2011;21(2):89-‐94. Epub 2011/03/02. 8. McCrea M, Guskiewicz K, Randolph C, Barr WB, Hammeke TA, Marshall SW, et al. Incidence, clinical course, and predictors of prolonged recovery time following sport-‐ related concussion in high school and college athletes. Journal of the International Neuropsychological Society. 2012;19(1):22. 9. McCrory P, Meeuwisse WH, Aubry M, Cantu B, Dvořák J, Echemendia RJ, et al. Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012. British Journal of Sports Medicine. 2013;47(5):250-‐8.
Supplemental Online Content 3 Case Example
Michael is a 13 year-‐old young man who suffered a concussion when he fell and hit the back
of his head on a granite curb while skateboarding with friends. He had a helmet on, did not lose consciousness, and actually continued skateboarding with friends for a while afterwards. When he got home, however, he complained of a headache to his mother. After she started asking him questions, she grew concerned that he seemed unable to remember what he had been doing with his friends, looked very tired, and was repeating himself a lot. She took him to a nearby urgent care facility, where he was diagnosed with concussion. Michael’s mother was advised to keep an eye on him, to keep him out of gym and sports (including skateboarding), and to follow-‐up with Michael’s pediatrician if needed. The next day, Michael woke up and felt pretty good with only a mild headache. His mother had been advised that he could go to school if he felt okay, so she got him on the bus and off to school. Michael felt a little nauseous during the bus ride to school, and also noticed that the sunlight seemed to be bothering him more than usual. When he got to school, he had math class first period. He had some trouble understanding the lesson, but he thought this was probably due to the fact that his headache was starting to bother him more. By third period, Michael’s headache was getting pretty bad, and he was also starting to feel very tired. His teacher noticed that he was putting his head down on his desk during class, which was unusual for him, so after class she suggested he go to the nurse’s office. After arriving at the nurse’s office, Michael asked the nurse if he could lie down and rest as, at that point, he was feeling extremely tired. The nurse also noticed that he seemed a little wobbly
and that his speech seemed rather slow. She helped him get comfortable in the office, and then called Michael’s mother to discuss his condition with her. After hearing that Michael had been diagnosed with a concussion the day before, the nurse recommended that Michael’s mother come in to school to pick him up. She also advised Michael’s mother to take him in to see his pediatrician as soon as possible and recommended that he stay out of school until that appointment. By the time Michael’s mother got to school, he was feeling a bit better but was concerned about leaving school early because of some upcoming tests. After they got home, Michael ended up going to bed quite early and slept much longer than usual that night. The next morning, Michael woke up again with a mild headache and was feeling even more tired than the day before. His mother had scheduled a doctor’s appointment in the afternoon for him, and she wanted to keep him home from school. However, Michael was worried about a quiz he had in science class that morning, and he pleaded with his mother to let him go to school before his appointment. She agreed to take him in, and arranged to pick him up after lunch to go the doctor. Michael only felt a little worse after his first period math class, but by the time he was finished taking the quiz in science class, he felt awful. Thinking that seeing his friends and eating something would help him feel better, Michael decided to go to the lunchroom rather than to see the nurse. Unfortunately, it wasn’t long before he realized that the noise and commotion in the cafeteria was actually making things worse. When Michael’s mother arrived, he told her that he had a severe headache and felt nauseous and exhausted. At his appointment, Michael’s pediatrician confirmed the diagnosis of concussion and reviewed everything that had happened since the injury. She recognized that while Michael was being kept out of sports due to his concussion, he was obviously overdoing it mentally. She provided some education to Michael and his mother about concussion and about the importance
of physical and mental rest. She recommended that Michael stay home from school the next day, which was a Friday, regardless of how he felt when he woke up. Further, she recommended that, if he felt better by Monday, that he only go to school for a half day, and also that he have a mandatory rest-‐break and check-‐in time with the school nurse every two periods. She recommended that Michael’s mother call the office on Monday afternoon to briefly discuss his progress, and provided a letter that was to be given to the school nurse with some additional recommendations for modifying his school day and work. Michael was upset about having to miss school the next day, but also relieved because of how much his symptoms had worsened when he did try to go to school. Michael’s mother explained to the pediatrician that she had no idea that concussion symptoms could get worse from just thinking and going to school, and asked how she would know if Michael was really ready to try again on Monday—even for a half day. They agreed that Michael would be restricted from much activity for the next couple of days, but that on Sunday he could try doing some homework and perhaps try going out somewhere such as the grocery store to see how he handled that. If his mother had concerns that he was not ready to go to school on Monday, she was to keep him home and they would discuss his status by phone on Monday. Michael’s doctor also explained her recommendations for other academic accommodations, including reduced work load, being allowed to eat lunch in a quiet room, and postponing any tests until Michael was feeling better. Michael and his parents were amazed at how much he slept over the weekend, and by Sunday he did seem to be more like himself. On Sunday afternoon, his parents suggested that he try doing some reading, followed by some math problems. Michael reported to them that it seemed to be harder to focus on the work, but an hour of so of activity did not seem to make his headache or any other symptoms worse. That evening, the family went out for a previously
scheduled dinner with friends. When they got to the restaurant, Michael and his mother both noticed that it was rather crowded and noisy, but thought they would give it a try anyway. Michael did well for about 45 minutes, but then his headache started to worsen and he quickly lost his appetite. He didn’t want everyone to have to leave because of him, though, so he didn’t say much and ended up staying for almost another hour. By that time, his mother noticed that he seemed to be getting pale and was looking very tired, at which point he reported that his headache had actually gotten pretty bad, so they left and went home.
Michael woke up feeling pretty good on Monday, so he and his mother decided that he
could try to go to school. Once there, he noticed that his concentration was a little better than it had been right after the injury, but still not normal. When he got to the nurse’s office after his second class, he reported that his headache was starting to increase and towards the end of period he was bothered by the smart-‐board and the fluorescent lights. Michael and the nurse agreed that he should take a short rest-‐break in a quiet and darkened room, which he did. He actually ended up falling asleep, and when the nurse woke him after about a 20 minute rest, Michael noticed that his headache was improved and he felt a little more energetic. He attended two more classes, then came back to the nurse, who noticed that he looked pretty tired and seemed to be having a little more trouble communicating than earlier in the day. So, even though his headache wasn’t too bad, she recommended that he leave and go home for the day. She called Michael’s mother, and also sent an e-‐mail to his teachers explaining what was going on with Michael and why he wouldn’t be in afternoon classes. One of the teachers noted in an e-‐mail back to the nurse that Michael looked normal and wasn’t complaining in class, and was questioning whether there might something else going on besides a concussion. The teacher also reported to the nurse that another staff member had seen Michael at a restaurant over the past weekend, looking like he was having quite a good
time. The school nurse responded that she was not aware of any issues other than the concussion with Michael. She also made a point to speak in person with Michael’s teacher later that day to provide some education about concussion, and about the importance of recognizing the academic challenges faced by students recovering from concussion, even though they may look and act normal. Michael’s mother called his doctor to report on his progress, and it was agreed that he could remain in school but only as tolerated.
For the rest of the week, Michael continued to check in with the school nurse at least twice
a day, and on Friday was able to tolerate a full day of school . The following week, he and the nurse agreed that he could reduce his rest breaks to once per day. He was no longer getting headaches and was able to be in school all day, but was still more tired than usual and having trouble staying focused in class.
Prior to starting school the next week, Michael’s mother took him to the doctor for a follow-‐
up visit. Michael told the doctor that he was in school full-‐time, that he was no longer having headaches, and that he was able to run around in the back yard after school without a problem. His doctor was pleased with his progress, and felt that he was ready to begin the step-‐wise return-‐ to-‐play protocol outlined in the Zurich guidelines. Michael was thrilled, as he was feeling much better and was getting anxious to get back to skateboarding. The doctor gave Michael a note with her recommendations, and advised Michael’s mother to contact her if his headache or other symptoms came back during the return-‐to-‐play process.
Michael went to school after his doctor’s appointment, and a couple of periods later was
called down to see the school nurse. The nurse showed Michael the letter she had just received by fax from his doctor, stating that he was cleared to start the return-‐to-‐play process. The nurse had been noticing that Michael was feeling better and was not getting headaches, but she was also
aware from talking with him that he was still describing abnormal fatigue during the school day and trouble focusing in class. Upon questioning, it was evident that Michael had told his doctor that he was not having headaches, was in school full time, and was able to exercise a little, but had not mentioned—or been asked about—the lingering problems with paying attention in class or being more tired at the end of the school day. The nurse first contacted Michael’s mother to discuss this with her, and then called Michael’s doctor to share her observations. After talking about it, Michael’s doctor decided to postpone the start of the return-‐to-‐play process until hearing from Michael’s mother and the school nurse that his fatigue and cognitive difficulties had completely resolved. The doctor did encourage his mother and the school nurse to make sure that Michael was getting some physical activity during the day, but still staying away from activities with increased risk of head injury. After another week or so, Michael appeared to be getting through the school day without any problems, and was not more tired than usual after school. He then completed the return to play protocol and resumed all physical education activities. All concussion-‐related academic accommodations were discontinued.
