Concussion among children and adolescents is a common injury encountered by pediatricians. Although some patients will need guidance for returning to sports, all patients will need guidance for returning to school and learning after a concussion. Because pediatricians are responsible for initial management in most concussion visits, it is important that they have the skills to both diagnose concussion and aid in the school reentry process.1 This article highlights some of the common barriers to school reentry and suggests some strategies to facilitate a full return to school.
The question of how soon to return to school after a concussion does not have a simple answer. Immediately after a concussion, there is a well-described pathophysiological process that occurs at the cellular level.2 Stretch injury causes depolarization of neuronal cell membranes.2 A subsequent influx of calcium interferes with mitochondrial function and causes temporary cell dysfunction. Repair mechanisms, using adenosine triphosphate (ATP)-fueled sodium/potassium pumps, attempt to restore intracellular balance.2 During the early stages of the injury, use of glucose to generate ATP is high, ultimately increasing neuronal energy demand.3 Pediatric and adult studies have shown that cerebral blood flow, which delivers glucose, decreases in response to injury.4,5 This high use of glucose and low delivery of glucose creates a metabolic mismatch almost immediately after injury and forms the basis for cognitive and physical rest recommendations early in the injury process.
The data regarding early exertion after concussion suggest that initial rest is beneficial. Animal studies have shown that forced early reentry to physical activity delays cognitive recovery.6 In two pediatric studies looking at early school reentry, one study found an increase in symptoms and a second found prolonged recovery with an early return to higher cognitive demands.7,8 Another recent study has found that cognitive rest immediately after concussion was associated with faster recovery times.9 Finally, a recent retrospective Canadian study showed that 43% of pediatric, high school, and college students who attempted to return to school too early had worsening symptoms with school reentry.10 In light of these studies, rushing the return to school, especially to a full academic load, seems ill-advised.
Many of the recommendations for rest until the patient is symptom-free have come from the sports literature.11 These recommendations are based in part on data that a second head injury prior to recovery from the initial concussion is associated with permanent axonal injury in laboratory studies.12 Animal studies have also demonstrated significant consequences such as axonal injury and memory impairment after a second head trauma prior to recovery from the first injury.13 So, the conservative recommendations to be completely symptom-free prior to engaging in collision sports are well-founded. However, the delayed return to sports activities should not be equated with strict rest requirements regarding return to physical or mental activity.
There is a growing body of work that suggests too much rest may be detrimental to an efficient recovery.14–17 A recent study of concussion patients age 11 to 22 years randomized to either 2 or 5 days of rest showed that the 5-day rest group had increased number and slower resolution of symptoms 10 days after injury.14 Wells et al.15 have demonstrated that the re-introduction of exercise after a rest period, adjusted for the severity of injury, actually enhances recovery. Furthermore, the psychological consequences of prolonged rest by removing a child from school for extended periods of time may contribute to anxiety regarding school reentry.16 Finally, another new study shows that light, early aerobic activity, even while patients are symptomatic, may not only reduce symptoms, but also reduce abnormalities seen in functional magnetic resonance imaging.17
The decision regarding school reentry remains a clinical one. These studies6–17 indicate that clinicians must balance the benefits of early rest with the potential downside of too much rest later in the concussion recovery process. Anecdotal reports suggest adequate sleep, even up 16 hours a day, in the first 48 hours after injury aids in recovery. The current research7–10 suggests that allowing a low level of activity with both physical activity (such as walking) and mental (such as listening to schoolwork) early in the concussion process does not impair recovery. Only intensive physical activity (such as intense sports training) or intensive school work are implicated with worsening symptoms and prolonged recovery.14–17 The standard recommendation for concussion treatment remains a short period of rest from demanding physical and cognitive activities, adjusted to the severity of the injury, followed by a gradual progression back to regular activity.18 However, whereas some students have a quick uneventful recovery, others struggle with school reentry. The patient's history and physical examination can provide additional information that is helpful when deciding school reentry issues.
Common concussion symptoms can be grouped into four main categories: (1) autonomic, (2) vestibular-ocular, (3) cognitive, and (4) mood. Each of these has the potential to interfere with normal school participation. Preexisting deficits in these areas make school reentry particularly difficult and can increase the risk for prolonged recovery (Table 1). Specific questions can be asked about visual function using the Convergence Insufficiency Symptom Survey (CISS),19 which can help guide specific school accommodations.
Preexisting Conditions that May Increase Risk for Prolonged Recovery from Concussion and Influence School Reentry
In the context of concussion, the importance of the physical examination is to identify subtle deficits that will impair school reentry and ultimately full recovery. Balance deficits have long been recognized after concussion, and current practice is to treat with vestibular therapy.20,21 Neck muscle strain from whiplash injuries may either mimic concussion symptoms or exacerbate concussion headaches, and may be treated with physical therapy.22 However, eye tracking deficits, which have greater implications for school reentry, have only recently been recognized as a common problem in pediatric and adolescent concussion. A large tertiary center study of patients age 11 to 18 years showed that a large percentage (69%) of symptomatic patients with concussion had either vestibular or ocular deficits on careful physical examination.23 Early identification of these deficits will allow the clinician to make appropriate and individualized school adjustments.
A series of specialized physical examination maneuvers to evaluate for vestibular-ocular deficits have been previously described.24 The tests that provide the best information to guide school reentry include evaluation of horizontal and vertical saccades and near the point of convergence. These tests, as done by our group, are described in detail in the following text. Further details of the complete series of tests with video demonstration are available online courtesy of the Children's Hospital of Philadelphia.25
Horizontal Saccades Test
A saccade is a quick, simultaneous movement of both eyes to fixate on a target. The eyes move quickly in the same direction, stopping directly on the target. Eyes moving at different speeds, eyes slowing down with multiple repetitions, or an eye missing the target (stopping either short or past the target) are all examples of saccadic dysfunction. Horizontal saccade eye movements in reading are critical in visual processing of written text.
- Examiner faces patient. Hold index fingers shoulder-width apart and approximately half an arm's length away from the patient's nose.
- Patient is asked to move their eyes as quickly as possible between the two fingers without moving their head.
- One repetition equals eyes returning to starting point.
- Up to 30 repetitions are performed if the patient does not stop sooner because of symptoms.
- Abnormal: symptom provocation (headaches, dizziness, eye fatigue), visible eye slowing, unable to coordinate going back and forth to target, eye watering.
Vertical Saccades Test
Vertical saccade eye movements are simultaneous movement of both eyes to fixate on a target in the vertical plane. Vertical saccade eye movements are critical in visual processing when copying notes from a chalkboard/smartboard or computer screen.
- Examiner faces patient. Hold index fingers sideways forehead-chin distance apart and approximately half an arm's length away from the patient's nose.
- Repeat as described in test for horizontal saccades.
Near Point Convergence Test
The near point of convergence (NPC) is the measurement of how close (in centimeters) an individual can bring a fixed target to his/her nose while maintaining one target (fusion). When the target becomes too close, the eyes are not able to keep the target as one, and the target splints. This is referred to as the break point. In adults, the NPC is 10 cm but in adolescents and children a normal NPC is less than 6 cm.
- A standardized card with a single column of vertical letters is positioned approximately 20 cm from the patient's forehead (Figure 1). This can be done either by hand or more accurately with a Near Point Rule. If letters are blurry for the patient, move card backward until clear (standardized card discussed in detail by Rouse et al.19).
- Break: Slowly (1–2 cm/sec) move target toward the patient until he or she indicates the line of letters splits in two like a zipper (ie, becomes two separate lines). Stop when this break is reported and record distance to nearest half centimeter. (If the patient continues to converge until the target is against the nose, record as “no break.”)
- Abnormal: letters become double (break) at >6 cm, symptom provocation.
These series of eye examinations have functional implications, as they mimic the eye tracking demands of students in the school classroom. Deficits with horizontal saccades are associated with difficulties in reading and tracking words across the page. Vertical saccade deficits interfere with looking up and down while taking notes from the board. Convergence deficits cause problems both with transitioning from far to near while taking notes from the board, and with sustaining focus at near, such as reading, especially small print. Because these deficits will often cause headaches with schoolwork, appropriate identification is needed to guide treatment. Table 2 shows how the effects of each of these deficits can be minimized with specific school accommodations.
School Accommodations for Students Recovering from a Concussion
Autonomic Nervous System Dysfunction
Autonomic nervous system dysfunction is another well-recognized component of a concussion. Common symptoms include headache, light and noise sensitivity, exercise intolerance, and fatigue. Physical examination clues to autonomic dysfunction include abnormal orthostatic vital signs, elevated resting heart rate, and large but reactive pupils. In patients with prolonged symptoms, exercise testing using the Buffalo Concussion Treadmill Test has been helpful in the evaluation process. Early identification of autonomic dysfunction aids with making appropriate school accommodations, and some of the symptoms can be treated successfully with graduated exercise protocols.26,27
School reentry can be evaluated through two prisms, and school accommodations need to take both into account. Return to learning addresses the cognitive barriers to returning to full academic performance. This can include memory and attention span problems that are caused by the concussion. As part of this process, restarting school work with the goal of rehabilitation rather than academic achievement (grades), should be the initial concern. Tests that do not count toward the grade may be part of the rehabilitation process. Delaying formal test scores until rehabilitation is complete may be preferable if grades are going to affect school placement or high school transcripts needed for college admission.
Return to school will include the challenges of negotiating the physical school environment. School attendance will be affected by symptoms such as noise or light sensitivity, fatigue, or vestibular deficits. Students may have difficulty with a loud, chaotic cafeteria, the bright lights of a smart board, or moving between classrooms in crowded, noisy hallways. Ultimately, school accommodations need to be developed to address both the cognitive and physical challenges with school reentry.
Grouping a patient's symptoms into four main categories of dysfunction (ie, autonomic, vestibular-ocular, cognitive, and mood) can help a clinician develop a rational strategy for school reentry. In students with preexisting deficits as identified in their history, some accommodations may already be in place, but additional accommodations are frequently necessary. This grouping recognizes that patients may have deficits in one or more of the categories. Accommodations can be customized a la carte depending on the symptoms, and should be modified and updated as the patient moves through the recovery process as symptoms abate (Table 2). Most children and adolescents with concussion recover within 4 weeks, but in those with prolonged symptoms, concurrent treatment, as described in Table 2, should start while accommodations are in place.
Primary care providers are responsible for providing initial management of school reentry after a concussion injury. Although early rest is associated with faster recovery, too much rest is detrimental and some degree of light aerobic activity should be allowed, even while symptomatic. After a period of initial rest, a graduated return to full school is recommended. Based on a careful history and physical examination, the primary care provider can customize a wide variety of academic accommodations to successfully facilitate the school reentry process.
- Arbogast KB, Curry AE, Pfeiffer MR, et al. Point of health care entry for youth with concussion within a large pediatric care network. JAMA Pediatr. 2016;170(7):e160294. doi:10.1001/jamapediatrics.2016.0294 [CrossRef]
- Giza CC, Hovda DA. The new neurometabolic cascade of concussion. Neurosurgery. 2014;75(Suppl 4):S24–S33. doi:10.1227/NEU.0000000000000505 [CrossRef]
- 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. doi:10.1016/j.pmr.2016.01.003 [CrossRef]
- Maugans TA, Farley C, Altaye M, Leach J, Cecil KM. Pediatric sports-related concussion produces cerebral blood flow alterations. Pediatrics. 2012;129:28–37. doi:10.1542/peds.2011-2083 [CrossRef]
- Meier TB, Bellgowan PS, Singh R, Kuplicki R, Polanski DW, Mayer AR. Recovery of cerebral blood flow following sports-related concussion. JAMA Neurol. 2015;72:530–538. doi:10.1001/jamaneurol.2014.4778 [CrossRef]
- Griesbach GS, Gomez-Pinilla F, Hovda DA. The upregulation of plasticity-related proteins following TBI is disrupted with acute voluntary exercise. Brain Res. 2004;1016(2):154–162. doi:10.1016/j.brainres.2004.04.079 [CrossRef]
- Makki AY, Leddy J, Hinds A, et al. School attendance and symptoms in adolescents after sport-related concussion. Glob Pediatr Health. 2016;3:2333794X16630493.
- Brown NJ, Mannix RC, O'Brien MJ, Gostine D, Collins MW, Meehan WP. 3rd Effect of cognitive activity level on duration of post-concussion symptoms. Pediatrics. 2014;133:e299–e304. doi:10.1542/peds.2013-2125 [CrossRef]
- Taubman B, Rosen F, McHugh J, Grady MF, Elci OU. The timing of cognitive and physical rest and recovery in concussion. J Child Neurol. 2016;31(14):1555–1560. doi:10.1177/0883073816664835 [CrossRef]
- Carson JD, Lawrence DW, Kraft SA, et al. Premature return to play and return to learn after a sport-related concussion: physician's chart review. Can Fam Physician. 2014;60:e310–e315.
- McCrory P, Meeuwisse WH, Aubry M, et al. Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport, Zurich, November 2012. J Athl Train. 2013;48(4):554–575. doi:10.4085/1062-6050-48.4.05 [CrossRef]
- Yuen TJ, Browne KD, Iwata A, Smith SH. Sodium channelopathy induced by mild axonal trauma worsens outcome after a repeat injury. J Neurosci Res. 2009;87(16):3620–3625. doi:10.1002/jnr.22161 [CrossRef]
- Prins ML, Alexander D, Giza CC, Hovda DA. Repeated mild traumatic brain injury: mechanisms of cerebral vulnerability. J Neurotrauma. 2013;30(1):30–38. doi:10.1089/neu.2012.2399 [CrossRef]
- Thomas DG, Apps JN, Hoffmann RG, McCrea M, Hammeke T. Benefits of strict rest after acute concussion: a randomized controlled trial. Pediatrics. 2015;135:213–223. doi:10.1542/peds.2014-0966 [CrossRef]
- Wells EM, Goodkin HP, Griesbach GS. Challenges in determining the role of rest and exercise in the management of mild traumatic brain injury. J Child Neurol. 2016;31(1):86–92. doi:10.1177/0883073815570152 [CrossRef]
- Ponsford J, Cameron P, Fitzgerald M, et al. Predictors of postconcussive symptoms 3 months after mild traumatic brain injury. Neuropsychology. 2012;26(3):304–313. doi:10.1037/a0027888 [CrossRef]
- Leddy JJ, Willer B, Cox JL, et al. Exercise treatment for postconcussion syndrome: a pilot study of changes in functional magnetic resonance imaging activation, physiology, and symptoms. J Head Trauma Rehabil. 2013;28:241–249. doi:10.1097/HTR.0b013e31826da964 [CrossRef]
- Halstead ME, McAvoy K, Devore CD, Carl R, Lee M, Logan KCouncil on Sports Medicine and FitnessCouncil on School Health. Returning to learning following a concussion. Pediatrics. 2013;132(5):948–957. doi:10.1542/peds.2013-2867 [CrossRef]
- Rouse M, Borsting E, Mitchell GL, et al. Validity of the convergence insufficiency symptom survey: a confirmatory study. Optom Vis Sci. 2009;86(4):357–363. doi:10.1097/OPX.0b013e3181989252 [CrossRef]
- Guskiewicz KM, Ross SE, Marshall SW. Postural stability and neuropsychological deficits after concussion in collegiate athletes. J Athl Train. 2001;36(3):263–273.
- Murry DA, Meldrum D, Lennon O. Can vestibular rehabilitation exercises help patients with concussion? A systematic review of efficacy, prescription and progression patterns. Br J Sports Med. 2017;51(5):442–451. doi:10.1136/bjsports-2016-096081 [CrossRef]
- Marshall CM, Vernon H, Leddy JJ, Baldwin BA. The role of the cervical spine in post-concussion syndrome. Phys Sportsmed. 2015;43(3):274–284. doi:10.1080/00913847.2015.1064301 [CrossRef]
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- Mucha A, Collins MW, Elbin RJ, et al. A Brief Vestibular/Ocular Motor Screening (VOMS) assessment to evaluate concussions: preliminary findings. Am J Sports Med. 2014;42(10):2479–2486. doi:10.1177/0363546514543775 [CrossRef]
- Children's Hospital of Philadelphia. Pediatric exams: concussion evaluation. http://www.chop.edu/video/pediatric-exams-concussion-evaluation#. Accessed February 20, 2017.
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Preexisting Conditions that May Increase Risk for Prolonged Recovery from Concussion and Influence School Reentry
Postural orthostatic tachycardiac syndrome
||History of motion sickness
Glasses for reading
History of vision therapy for reading problems
Amblyopia (lazy eye)
History of eye surgery
||Learning disorders including dyslexia and processing delays
Oppositional defiant disorder
School Accommodations for Students Recovering from a Concussion
||Frequent school breaks in a quiet area to rest, recover, and then return to class
In younger patients, breaks may initially need to be made mandatory. In older patients, allow the patients to take breaks as needed, using some scale such as a 2-point worse rule (symptoms on a 10-point scale can get up to 2 points worse before a break is needed)
May need to limit the number of classes or increase the number of breaks if fatigue is significant
Initially, no testing. Subsequently, limit the number of make-up tests per day when returning to school, preferably no more than 1 per day
Avoid tests in consecutive class periods, putting recovery time in between tests. Can also divide tests into two or more sections, allowing the student a short break in between. This is especially important during final examinations
Allow the temporary use of sunglasses, decrease brightness on computer monitors, or receive paper printouts instead of having to take notes from a smart board
Allow temporary wearing of earplugs/headphones, eat in quiet area with a few friends, avoid busy hallways, skip music classes as needed
Avoid gym class where any contact or collision is possible, but allow light aerobic activity that does not worsen symptoms (walking is fine)
||Melatonin (1 mg for children, 3–5 mg for adolescents) early in the concussion can help with sleep issues
Start light aerobic activity that does not worsen symptoms (walking is fine) and progress to harder aerobic activity as symptoms allow
In patients with symptoms lasting >4 weeks, formal physical therapy for aerobic rehabilitation, use a formal exercise protocol, such as the Modified Balke Protocol or the Buffalo Concussion Treadmill Test
||Initial school reentry may involve just attending class and paying attention without doing any reading or note taking
Vertical saccades deficits: no note taking. Use preprinted teachers' notes (eliminates looking up and down)
Horizontal saccade deficits: adjust reading requirements by using larger font size, double-spaced lines, audio books, watch the movie in lieu of reading the book
Convergence deficits: larger font (size 18), preprinted teachers' notes so eyes can stay fixed on a far target, record audio of lectures as needed
To change font size, scan written material and convert to PDF. Then change font size and reprint (special books are not needed)
||Can start home vestibular exercises as tolerated, including saccades, gaze stabilization, and convergence exercises in the subacute phase (about 1–3 weeks after the concussion); avoid starting in the acute phase as that will make symptoms worse
If persistent symptoms, start formal vestibular therapy
Convergence retraining may be necessary for a very small percentage
Shorter attention span
Slower processing speed
||Decrease overall cognitive load, preferably with fewer classes to start. Students should attend the same class every day rather than alternating classes. Instead of half-day attendance, try having the student attend a full day of school, but miss some of the classes so they have a full period between the classes as a break
Word banks for math formulas, vocabulary words
Extra time for tests and assignments, using weekends as catch-up time
Delay test taking until the student is caught up on missed work (should not delay testing if ready or anxiety about making up tests will likely increase)
Eliminate nonessential missed assignments
If a full course load is not possible, then focus on classes that build on concepts (math, science, and foreign language) and plan to do other work later
With prolonged symptoms, convert a class to a study hall, preferably in the middle of the day to allow a break to recover. Sometimes multiple breaks are needed
Pass/fail grades as needed
Classroom modification for ADHD can be used in younger concussion patients
||Schoolwork in small increments (10–15 minutes to start), including test taking, is therapeutic
Taking difficult academic classes (but maybe not as many to decrease overall load) helps students recover to preinjury function
Selective use of neurostimulants
OT/speech therapists can provide strategies for improving memory function
||Clearly define student work expectations, particularly regarding missed work, to decrease anxiety
Have clearly defined school official (guidance counselor, principal, school nurse) to centrally coordinate academic requirements rather than having each teacher assign work without taking into consideration other classes
||Involve psychologist as needed, with lower threshold to refer based on past personal and family history of mood disorders
Medications as needed, as second-line therapy