rehabilitation strategies for prolonged recovery in...

PEDIATRIC ANNALS 41:9 | SEPTEMBER 2012 Healio.com/Pediatrics | 1

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Rehabilitation Strategies for Prolonged Recovery in Pediatric and Adolescent ConcussionPaul G. Vidal, PT, MHSc, DPT, OCS, FAAOMPT; Arlene M. Goodman, MD; Amy Colin, MA, CCC-SLP; John J. Leddy, MD; and Matthew F. Grady, MD

Most pediatric and adolescent concussion patients will heal within 1 month. However,

10% to 20% of adolescent concussions will take longer than 1 month to heal. In this subgroup, prolonged symptoms might include vestibular system deficits, residual neck muscle whiplash injury, exercise intolerance/dysautonomia, and memory issues. At this stage in recovery, these problems respond better to “active rehabilitation” via specific targeted strat-egies rather than to strict rest. During fol-low-up office visits, a careful history and physical exam can elicit specific deficits

1. Identify the time frame that distinguishes concussion with typical recovery trajectory vs. atypical prolonged recovery trajectory.

2. Use directed physical examination to identify deficits that may be addressed by targeted rehabilitation strategies.

3. Implement exercise strategies in the rehabilitation of concus-sion with atypical prolonged recovery outside of the typical return-to-play protocol.

Paul G. Vidal, PT, MHSc, DPT, OCS, FAAOMPT, is a physical therapist and

owner of Specialized Physical Therapy, LLC, Cherry Hill, NJ. Arlene M. Good-

man, MD, is a pediatric sports medicine specialist, Division of Orthopaedic

Surgery and Department of Pediatrics, The Children’s Hospital of Philadel-

phia. Amy Colin, MA, CCC-SLP, is a Senior Speech-Language Pathologist,

Department of Speech-Language Pathology, The Children’s Hospital of

Philadelphia. John J. Leddy, MD, is an Associate Professor of Clinical Ortho-

pedics, the Associate Director of University Sports Medicine, and Concus-

sion Clinic Director, State University of New York at Buffalo, UB Orthopae-

dics & Sports Medicine. Matthew F. Grady, MD, is the Director, Primary Care

Sports Medicine Fellowship, The Children’s Hospital of Philadelphia; and

Assistant Professor of Clinical Pediatrics, Departments of Surgery and Pe-

diatrics, Division of Pediatric Orthopedics and Sports Medicine, Perelman

School of Medicine at the University of Pennsylvania.Address correspondence to: Paul G. Vidal, PT, MHSc, DPT, OCS,

FAAOMPT, Specialized Physical Therapy, LLC, 1919 Greentree Road, Suite B, Cherry Hill, NJ 08003; fax: 856-424-0994; email: [email protected].

Disclosure: The authors have no relevant financial relationships to disclose.doi: 10.3928/00904481-20120827-10

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and help customize a rehabilitation pro-gram to maximize recovery.

Some novel therapies available for use by general pediatricians are target-ed rehabilitative therapies for concus-sion with atypical prolonged recovery; vestibular therapy with balance and oculomotor exercises; aerobic rehabili-tation for subsymptom threshold exer-cise; and speech therapy for working memory and executive functioning (see Sidebar).

VESTIBULAR SYSTEM INTEGRATION DYSFUNCTION

An examination assessing the inte-gration of postural control is essential in post-concussion patients and has been described in the companion article in this issue by Master and Grady (see “Office-Based Management of Pediatric and Adolescent Concussion). Vestibular and other therapies may be done by spe-cifically trained occupational, physical, or speech therapists working individu-ally or together as part of a multidisci-plinary rehabilitative team. The goal of this article is to introduce these general concepts to the practicing pediatrician.

The vestibular system combines with the visual and somatosensory systems to provide postural control to maintain a sense of vertical orientation and equi-librium relative to gravity. This interac-tion can be complex and may present with one or multiple deficits on physi-

cal exam. When these systems are not coordinated, patients often complain of headaches, dizziness, visual blurring/double vision, and balance problems. Practical complaints include symp-toms with reading (horizontal deficits), symptoms when looking up at the board and down at the desk during note taking (vertical deficits), or symptoms while running and trying to focus on a target such as a ball or goal (gaze stabiliza-tion).

Vestibular SystemThe vestibular system is both a sen-

sory and motor system.1 The semicircu-lar canals provide sensory information regarding head acceleration and angular head movement. The utricle and saccule, collectively known as the otoliths, pro-vide afferent information on linear mo-tion and acceleration, as well as static tilt of the head. The vestibulo-ocular reflex and vestibulo-spinal reflex are the mo-tor components of the vestibular system, providing gaze stabilization and body stabilization during head movement, re-spectively. Gaze stabilization functions akin to “the steady-cam” feature of the brain, and allows the athlete to maintain a stable visual picture while engaging in activity that involves vertical or horizon-tal “bouncing” such as running, jump-ing, or cutting.

Vestibular rehabilitation is a specific treatment approach designed to reduce or eliminate a patient’s dizziness, im-prove and restore balance, and increase physical activity levels. Vestibular reha-bilitation is essential for restoring defi-cits in the vestibulo-ocular reflex (VOR) and vestibulo-spinal reflex (VSR). Im-proving gaze stability and postural sta-bility will help the patient’s complaint of blurry vision, dizziness, headache, and imbalance. Vestibular rehabilitation has been shown to be effective for patients with peripheral vestibular disorders, mi-graine headache, and cervicogenic diz-ziness.2-4

Visual SystemThe visual system provides an ex-

ternal reference point for the body and gives the body a sense of alignment with regard to the downward force of gravity. The visual system also provides infor-mation about the position and movement of the head. Impairment of the oculomo-tor component of the visual system may cause difficulty in focusing eyes, blurry vision, headaches, eye strain, and avoid-ance of reading.3

Vision therapy that is part of ves-tibular rehabilitation includes a series of oculomotor exercises that guide pa-tients through a progressive routine of sets and repetitions of convergence-di-vergence, smooth pursuit, and saccadic movement. The oculomotor exercises progress based on the patient’s tolerance and provocation of symptoms. Variables of speed, support surface, and conflict-ing visual background are introduced to challenge the patient.

Somatosensory System The somatosensory system, which

includes joint mechanoreceptors and muscle spindles, provides sensory in-formation to the brain. Information in-cludes the position and motion of joints, length and tension of muscles, and the condition of the support surface (level/angulated, smooth/rocky, steady, etc.) upon which they are standing.

Musculoskeletal System in Vestibular Dysfunction

Manual physical therapy for the cer-vical spine is used to address physical impairments in range of motion (ROM) and muscle tightness that are thought to contribute to symptoms of headache, dizziness, and neck pain. Manual physi-cal therapy has been shown to be effec-tive in patients with cervicogenic head-ache and cervicogenic dizziness.5,6

Vestibular Therapy Evaluation Symptom/Functional Scales

SIDEBAR.

Targeted Rehabilitative Therapies for Concussion with Atypical Prolonged

Recovery• Vestibular therapy with balance and

oculomotor exercises

• Aerobic rehabilitation for subsymptom

threshold exercise

• Speech therapy for working memory and

executive functioning

Source: Vidal PG


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The patient’s symptoms are graded using a verbal analog scale (VAS): a score of 0 indicates no symptoms and a score of 10 is the worst symptoms. A VAS can be used for the symptoms of dizziness, headache, and cervical pain, among others. The Sport Concussion Assessment Tool (SCAT2) symptom scale can also be used to quantify the number and severity of symptoms.2

Oculomotor SystemThe oculomotor system consists of

smooth pursuit and saccadic eye move-ments as well as vergence of the eyes. Remarkable findings in oculomotor testing include non-smooth eye move-ment, over- or under-shooting a target, convergence insufficiency (greater than 6 cm from tip of nose to object), and convergence spasm. While testing, the examiner should ask the patient if symp-toms are aggravated or reproduced with specific testing.

• Smooth pursuit testing is performed by having the patient follow a slowly moving target (see Figure 1). The tar-get is held about 20 to 24 inches away from the patient and is moved 30° in all directions (ie, horizontal, vertical, and diagonal).

• Saccades are tested by having the patient look back and forth between two stationary targets (see Figure 2). The tar-gets are held about 20 to 24 inches away from the patient. Patients perform sac-cadic eye movements in the horizontal, vertical, and diagonal planes.

• Vestibular therapists may employ the King-Devick test as an alternate means of documenting saccades.7 In this test, a series of numbers is listed on a card. The patient is timed while reading the numbers on each card. Post-injury, these times are prolonged (from baseline if available) and improve with symptom-resolution, and if needed, vestibulo-ocu-lar rehabilitation.

• Vergence is tested by assessing con-vergence first (see Figure 3) followed

Figure 2. Saccade testing.

Figure 4. Divergence testing.

Figure 3. Convergence testing.

Figure 1. Smooth pursuit testing.

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by divergence (see Figure 4). The ex-aminer’s finger/pen is held in the mid-sagittal plane and slowly moved toward the patient’s nose. The patient attempts to maintain focus on the inward moving target. The point at which the patient re-ports double vision is measured from the tip of the nose. Normal convergence is less than 6 cm from the tip of the nose (a measuring tape can be placed at the tip of the patient’s nose). Divergence is then tested by slowly moving the target away from the tip of the patient’s nose. The pa-tient should be able to maintain focus on the diverging target.

• Ocular alignment can be assessed using the cover-uncover test. The pres-ence of exophoria, esophoria, hyperpho-ria, and hypophoria may be determined with the cover-uncover test. Clinically, it appears that a pre-existing compensated ocular misalignment may be unmasked by concussive injury and is associated with protracted recovery.

• Pupil reaction should be assessed with a light pen. Dilated pupils that re-act to light are common in patients with autonomic dysfunction. This may be ob-served on physical exam or reported by parents only when the child/adolescent is more symptomatic following physical or mental activity.

Vestibular SystemGaze stability involving the vestibulo-

ocular system can be assessed with the patient visually fixing on an object while nodding or shaking their head to see if symptoms are provoked.

Central Nervous System• Gait is assessed to detect deficits in

dynamic balance. Frequently, the gait appears normal and deficits are detected only when testing is made more chal-lenging. Gait and balance can be eas-ily assessed in the office using heel-toe walking. Check gait by starting with heel to toe walking forward with the eyes open. Progress to heel to toe walking

backwards first with eyes open then with eyes closed. More deficits will be detect-ed as the degree of difficulty increases. Usually decreased cadence and postural sway are noted as common deficits. In severe cases, marked deviation from a midline path, stumbling, or wide based gait may be seen.8

• The Romberg test can be used to evaluate static balance. The Balance Er-ror Scoring System (BESS test) can also

be used. The modified version of the BESS is part of the SCAT2.9 Postural control has been shown to be impaired in patients with concussion.10-12

• Coordination is assessed with fin-gertip to nose testing. Speed deficits are common early in the concussion but frank dysmetria is an unusual finding.

Cardiovascular SystemResting heart rate should be recorded.

Elevated resting heart rates can be pres-ent post-concussion, which may indicate autonomic nervous system dysfunc-tion.13 If symptoms worsen with heart rate elevations above a specific number, then therapy should be adjusted to keep the heart rate below this threshold.

Musculoskeletal System • Assessment of the musculoskeletal

system focuses on posture and cervical range of motion (ROM). The patient’s posture should be assessed for forward head position, rounded shoulders, exces-sive thoracic kyphosis, and static head tilt positions. The examiner can gain an appreciation for any muscular imbalance

that may negatively impact cervical mus-cle strength and stabilization. Static head tilt positions may provide subtle cues to vestibular system involvement or com-pensation for ocular malalignment.

• The patient is asked to perform cer-vical ROM in the directions of flexion, extension, rotation, and sidebending. Re-production of the patient’s symptoms is noted. The cervical muscles (upper tra-pezius, levator scapula, sternocleidomas-toid, cervical paraspinals, and sub-oc-cipital muscles) are palpated for tension, length, and reproduction of symptoms. If there is a component of unrehabilitated cervical spine whiplash injury, then cer-vical spine physical therapy can be added to the rehab prescription.

EXERCISE INTOLERANCE/DYSAUTONOMIA

Patients with prolonged concussion symptoms frequently complain of early fatigue with physical or mental activity, sensitivity to light and noise, sleep dis-turbance and light headedness/dizziness when going from a seated to standing position. Literature showing that some of these symptoms may have a physiologi-cal basis has begun to emerge. In a recent study by Maugans amd colleagues,13

36% of patients between 11 to 15 years of age still had reduced cerebral blood flow up to 4 weeks post-injury. Leddy and colleagues14 have proposed that these prolonged symptoms are a result of impaired autonomic function and that a gradual return-to-exercise protocol can be used to treat these symptoms.

Leddy and colleagues15 have further demonstrated that in adult patients with prolonged symptoms, a subsymptom threshold aerobic exercise rehabilitation program improved clinical outcomes.15

They designed a treadmill stress test utilizing a modified Balke Protocol, de-scribed in the Buffalo Concussion Tread-mill Test (BCTT).16 The BCTT is used to systematically determine a patient’s tolerance to aerobic activity and forms

Patients with prolonged concussion symptoms

frequently complain of early fatigue with physical or

mental activity.


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the basis for a progressive exercise regi-men based upon the heart rate achieved on the test. The BCTT has been shown to be safe and reliable in patients with pro-longed symptoms17 and helps to restore physical conditioning and return patients safely to sport within 4 to 12 weeks. A similar rehabilitation program has been established for younger children with prolonged symptoms after sustaining a sports-related concussion; it combines gradual, closely monitored physical con-ditioning, general coordination exercis-es, visualization, education, and motiva-tion activities.17

As discussed in the article in this is-sue regarding the pathophysiology of conussion (“Concussion Pathophysiol-ogy: Rational for Physical and Cogni-tive Rest” by Matthew F. Grady, MD; Christina L. Master, MD; and Gerard A. Gioia, PhD), initiation of physical exer-tion too early after a concussion is as-sociated with increased symptoms and slower recovery.18 However, emerging research supports the use of aerobic ex-ercise as a treatment therapy after the acute post-concussion period has passed (ie, 3 to 4 weeks) to facilitate neurogen-esis and physical reconditioning.14,15,18

The difficulty in the pediatric popula-tion is determining when to start aero-bic (exertional) activity. Clinically, it is reasonable to consider beginning regular aerobic training in pediatric patients 4 to 6 weeks post-concussion regardless of symptoms.

The concussed patient is instructed to exercise up to the threshold of provok-ing worsening symptoms but not beyond. The long-term goal is at least 30 minutes of sustained aerobic activity. If symp-toms prevent sustained aerobic activity, intensity must be decreased. This process can be started by physical therapists fa-miliar with the BCTT process. Early in this process, 30 minutes of activity may only be moderate walking, but over a few months this should improve to sustained hard aerobic activity.

MEMORY DIFFICULTIESIn most patients a slow, graduated

return to school is sufficient to permit recovery of school-related skills, in-cluding memory and central processing. For these individuals, return-to-school comprises their cognitive therapy. A small subset, however, may continue to struggle with more profound functional memory deficits. In this group, recovery can be aided by speech therapy that tar-gets language-based deficits in working memory and executive function.

Patients with severe post-concussion symptoms may report difficulty re-membering, concentrating, following directions, word retrieval issues, or par-ticipating in conversation with peers. Cognitive skills commonly impacted by a concussion include attention, memory, and processing speed, all of which can have a direct impact on communication and academic performance.19 At this stage in recovery, a comprehensive as-sessment of the patient’s cognitive and communication skills may be warranted. Such an evaluation is extremely helpful in academic planning for children with prolonged post-concussion symptoms and deficits.

This assessment may be conducted by a neuropsychologist and a speech-language pathologist when symptoms persist beyond 8 to 12 weeks. A neuro-psychological evaluation includes an as-sessment of the child’s overall cognitive abilities, including cognitive processes affected by concussion, and their impact on behavior. A speech-language evalua-tion will focus on the child’s ability to understand and use language, as well as the impact of cognitive skills on commu-nication. Communication may be ver-bal or nonverbal and includes listening, speaking, gesturing, reading, and writing in all domains of language (phonologic, morphologic, syntactic, semantic, and pragmatic). Cognition includes cogni-tive processes and systems (eg, attention, perception, memory, organization, ex-

ecutive function). Areas of function af-fected by cognitive impairments include behavioral self-regulation, social interac-tion, activities of daily living, learning and academic performance, and voca-tional performance.20 These assessments allow a comprehensive understanding of a child’s cognitive profile. If deficits are revealed during the evaluation process, speech therapy may be recommended to restore these skills to the child’s pre-injury baseline.

Speech-language therapy will in-clude rehabilitation and compensatory strategy training to optimize recovery of cognitive-communication functioning. Goals include introduction and training of compensatory strategies for memory, language, executive functioning and other cognitive-communication skills. The speech-language pathologist or neu-ropsychologist can also collaborate with school personnel to establish appropriate supports and accommodations during the school re-entry process.

CONCLUSIONRecovery from a concussion oc-

curs spontaneously for most patients. Clinically, patients who suffer a concus-sion and rest immediately as the initial treatment tend to recover more quickly. Those patients who physically and/or cognitively over-exert too early in the post-concussion period tend to have a prolonged recovery. These findings are consistent with research comparing im-mediate rest to immediate exertion.21

Patients who have persistent signs and symptoms 4 weeks after injury ben-efit from “active rehabilitation.” Com-mon problems include impaired bal-ance, vestibulo-ocular dysfunction, and aerobic intolerance and memory deficits. Rehabilitation prescriptions should be customized to therapies specific to the patient’s deficits.

Patients who receive vestibular thera-py are prescribed a comprehensive daily home exercise program that may include


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oculomotor, balance, and cervical spine exercises. Each patient should be en-couraged to perform progressive aerobic activity based on their level of recovery. Improvements can be seen in patients as soon as 4 weeks into therapy and some patients may report improvements within a few sessions.

For the medically difficult, post-concussion patient with an atypical pro-longed recovery trajectory, a multidis-ciplinary team approach to the overall management of protracted concussion symptoms is recommended. For patients with prolonged post-concussion symp-toms, a comprehensive evaluation for possible vestibular dysfunction, oculo-motor difficulties, musculoskeletal, aero-bic, and speech or language impairments facilitates appropriate referral to physi-cal, occupational, or speech therapists trained in the evaluation and manage-ment of concussion-related deficits.

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8. Galetta KM, Brandes LE, Karl Maki, et al. The King-Devick test and sports-relatd concus-sion. Study of a rapid visual screening tool in a collegiate cohort. J Neurol Sci. 2011;309(1-2):34-39.

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11. Cavanaugh JT, Guskiewicz KM, Giuliani C, Marshall S, Mercer VS, Stergiou N. Recovery of postural control after cerebral concussion: new insights using approximate entropy. J Ath-let Train. 2006;41(3):305-313.

12. Register-Mihalik JK, Mihalik JP, Guskiewicz KM. Balance deficits after sports-related con-cussion in individuals reporting posttraumatic headache. Neurosurgery. 2008;63(1):76-80; discussion 80-72.

13. Maugans TA, Farley C, Altaye M, Leach J, Cecil KM. Pediatric sports-related concussion

produces cerebral blood flow alterations. Pedi-atrics. 2012;129(1):28-37.

14. Leddy JJ, Kozlowski K, Fung M, Pendergast DR, Willer B. Regulatory and autoregulatory physiological dysfunction as a primary char-acteristic of post concussion syndrome: im-plications for treatment. NeuroRehabilitation. 2007;22(3):199-205.

15. Leddy JJ, Kozlowski K, Donnelly JP, Pender-gast DR, Epstein LH, Willer B. A preliminary study of subsymptom threshold exercise train-ing for refractory post-concussion syndrome. Clin J Sport Med. 2010;20(1):21-27.

16. 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.

17. Gagnon I, Galli C, Friedman D, Grilli L, Iver-son GL. Active rehabilitation for children who are slow to recover following sport-related concussion. Brain Inj. 2009;23(12):956-964.

18. Griesbach GS, Hovda DA, Molteni R, Wu A, Gomez-Pinilla F. Voluntary exercise fol-lowing traumatic brain injury: brain-derived neurotrophic factor upregulation and recovery of function. Neuroscience. 2004;125(1):129-139.

19. Yeates KO. Short Review: Mild Traumatic Brain Injury and postconcussive symptoms in children and adolescents. J Int Neuropsychol Soc. 2010;16:953-960.

20. Working Group on Cognitive-Communication Disorders of ASHA’s Special Interest Divi-sion I, Language Learning and Education; and Division 2, Neurophysiology and Neurogenic Speech and Language Disorders. Roles of Speech-Language Pathologists in the Identifi-cation, Diagnosis, and Treatment of Individu-als With Cognitive-Communication Disorders: Position Statement. Available at: www.asha.org/docs/html/PS2005-00110.html. Accessed Aug. 3, 2012.


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