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Concussion
C H A P T E R
24 mTBI/Concussion: Assessment and Rehabilitation Strategy and Program Optimization James K. Buskirk, MS Ed., PT, SCS, AIB-CON Department of Otolaryngology, Batchelor’s Children’s Research Institute, University of Miami, Miller School of Medicine, Miami, FL, United States
BACKGROUND To provide appropriate assessment and rehabilitative therapies for a specific disorder related to mTBI/Concussion, or its most common component (94% prevalence rate)1 of vestibular dysfunction (whether peripheral, central, or mixed origins), one must first ascertain and understand the heterogeneity of the commonly multifactorial dysfunction. Establishing a history, including timeline of onset, progression of functional limitations, and associated symptoms is critical for the rehabilitative clinician to establish an effective assessment and subsequent treatment program. A review of prior studies2 showed effectiveness of various rehabilitation approaches for peripheral vestibular loss with varied outcomes, leading to an individualized approach dependent on objective testing, functional presentation, and symptoms tolerance as most effective, due to progressive, targeted rather than general exercise approach. A lack of understanding of the importance of the multiple components of mTBI, or a lack of understanding of the initial self-limiting compensatory mechanisms and associated timelines may lead the clinician to not fully assess all the components of the disorder and findings relative to the persistent symptoms and functional limitations, and erroneously prescribe an inappropriate rehabilitation program, with less than optimal results obtained. Optimized, or targeted rehabilitation prescription for mTBI with associated vestibular dysfunction component has gained popularity with the advancement of technologies for objectification and quantification of both peripheral and central neurologic sensory and motor dysfunctions, and use of validated scales to quantify the presence and magnitude of common symptoms of mTBI, including (but not
Neurosensory Disorders in Mild Traumatic Brain Injury DOI: https://doi.org/10.1016/B978-0-12-812344-7.00024-8
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limited to): dizziness, vertigo, disequilibrium, sleep disorder, impaired cognition, anxiety and depression, and headache.3 These are often accompanied by musculoskeletal symptoms and resultant functional activities of daily living (ADL) limitations. Measurement of transmembrane ionic flow and resultant electrical current flow produced at the cellular level, as evidenced by what is elicited by the types I and II hair cells located within the audio-vestibular system, along with mapping of microcircuits linking the vestibular afferents with the cerebellum, hippocampus, and inferior olive has shown a baseline discharge rate inherent to each component anatomic part of the peripheral and central neurologic systems.4 These rates function in harmony and in real-time, allowing communication among all the component anatomic parts, via the complex network of excitatory and inhibitory synapses inherent to each. The synaptic junctions contain excitatory or inhibitory neurotransmitters which cause action potential modulation with resultant messages sent in the cerebellum via the mossy and climbing fibers, and throughout the central and peripheral systems.4 7 This baseline engrained pattern of cellular and, therefore, neuron discharges is unique to individuals, and may be altered with injury, surgery, or disease, and positively altered by rehabilitative, specific-task training. Specific motor/movement plans and patterns become engrained over time as a learned pattern, and stored within various parts of the brain and brainstem for basic and advanced cranial nerve functions, and gross motor tasks are initially “learned” within the cerebellum, and then integrated within the basal ganglia. Since some functionality tasks are shared among all individuals, there appears to exist a “common thread” of movement plans and patterns by species, which are further altered by repetitive daily activities. Additional, or refined patterns exist among subsets of individuals pertinent to individual task requirements for ADL, job, or sport related activities. Thus, one could hold to the assumption that this inherent rate of discharge can be altered as an adaptation to environmental changes, or alterations to the discharge rate elicited by external factors (disease, trauma, aging, etc.) or with specific task training, repetitiously. One also can assume also that the impulse patterns can be further modified or altered by training or learning new patterns of behavior and movements, with resultant functional adaptation. This ability for modulation forms the basis for an apparent hierarchy of phases of rehabilitation and recovery from mTBI, vestibular, and balance deficits.8 Prior studies have also reported a higher incidence of musculoskeletal injury in athletes after sustaining mTBI as compared to control subjects not subjected to head injury.9,10 This lends itself to the assumption of the second phase of vestibular recovery not being fully completed, with incomplete adaptation to new or relearning prior engrained movement patterns. This may include eye and head motions, as well as postural stability alterations, with learned aberrant auditory and cognitive functions which may also impact physical task performance. The peripheral vestibular system discharges at approximately 90 spikes/second at rest, and increase rapidly with head and body motions.11 These impulses are carried by both the superior and inferior branches of the vestibular portion of cranial nerve VIII to the vestibular nuclei in the midbrain. The vestibular labyrinths elicit increased unilateral discharges from the side moved toward, and resultant contralateral decreased discharges (inhibition) from the side moved away from. The otolithic system (saccule and utricle) elicit discharges continuously, and increase with translational motions horizontally and/or vertically, in response to changes in alignment with force of gravity. At the vestibular nuclei, various connections or synapses are formed with neurons
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that connect to the nuclei of cranial nerves III, IV, and VI, the cerebellum, inferior olive, and premotor and motor cortices. The oculomotor cranial nerves activate concentric or eccentric motions of the eyes to maintain focus of the environment onto the ocular fovea. Vergence of the eyes is critical for visual motion detection and spatial perception. Alterations of the necessary pathways for normal eye coordinated motions give rise to aberrant perception and elicits symptoms of disorientation. Movement of the head elicits activation of the semicircular canal mechanisms bilaterally, and concomitant change in orientation with line of gravity of the otolithic system, causing changes in electrical discharge and conduction rates of both. The importance of the oculomotor system, along with the vestibular-ocular reflex (VOR) and coordination of eyes and head motions for rehabilitation processes has been recognized for many years.12 Absence or dysfunction of such coordination elicits nystagmus and other abnormal eye movements, with resultant retinal slip, or inability to keep a visual target on the retinal fovea. Corrective saccadic eye motions are needed to replace the target back onto the retinal fovea. This extraneous eye movement elicits visual distortion and abnormal spatial perception, or dizziness symptoms. Often a subject with abnormal VOR function will rely solely on oculomotor function for spatial awareness and orientation, opting to avoid head motions entirely. Pathology of the oculomotor system affects both static visual acuity, as well as visual tracking with head and body motions. Further internal feedback loop pathways via the cerebellum, basal ganglia, and motor cortex enable alterations and refining, or “smoothing,” functions of excitation and/or inhibition of neuronal pool firing, influencing postural control, and when altered, elicits loss of balance and disequilibrium symptoms. The basal ganglia, additionally, performs centrally similarly to a “switching” mechanism, whereby neural pathways are integrated from, and sent out to, the components of the limbic system, thus modulating emotions and cognitive behaviors associated with the dysfunction. An understanding of this anatomic and physiologic relationship among the component parts allows the rehabilitation clinician to objectify and categorize symptoms reported and, therefore, form the optimized rehabilitative approach for mTBI. Benign paroxysmal positional vertigo (BPPV) has been described in the literature for many years as the result of otoconia within the otolithic system (saccule and utricle) becoming free floating within the endolymphatic fluid and relocating into one or more of the semicircular canals, causing severe vertigo whenever the subject positions the head in such a manner as to cause the otoconia to move, creating an eddy current. There appears to be a natural turn-over of the otoconia whereby “old,” or mature, otoconia are replaced by “new” ones. This process may be regulated by the ionic flow and resultant electrical current produced by the basement membrane and the outer most portion of the cellular membrane of the otoconia. Whether this is an electrical bond or chemical bond, or both, is not fully understood. Therefore, one potential cause of BPPV is alteration of the removal of the “old” otoconia or alteration of the generation of the “new” otoconia. Various external causes of BPPV have also been described, including viral infections, migraine with (or without) accompanying headache, and exposure to trauma such as that sustained which causes central pathologies, like mTBI/concussions. It is thought the otolithic otoconia are held in place on the surfaces/basement membranes of the utricle (more positioned in the horizontal plane) and saccule (more positioned in the vertical plane) by an electrical and/ or chemical bond. A disruption of the bond by trauma or by changes in ionic flow and,
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thus, electrical current flow at the cellular membrane level may cause loosening of them from the basement membrane and subsequent head motions then position them pathologically into the labyrinths. If the otoconia remain free-floating within the endolymphatic fluid, it is termed canalithiasis. However, if the outermost membranes of the otoconia become “sticky,” or adherent to the cupula, and are no longer free-floating within the endolymphatic fluid, it is termed cupulolithiasis.13 Again, the mechanisms involved in making the otoconia “sticky” are not fully understood, but may be explained by alterations in membrane potentials generated by alterations in ionic flow across the membrane, with resultant chemical and/or electrical effects, causing the affinity or adherence to the innermost lining of the endolymphatic sac within the labyrinth, or directly to the cupula. Several liberatory maneuvers with risks and benefits have been described and compared for efficacy to reposition the otoconia back out of the labyrinths and again into the otolithic organs, thus, relieving the vertigo symptoms.14 Following performance of the maneuvers, several different exercise programs have been suggested, to continue to resolve the oftenpresent concomitant symptoms of dizziness and disequilibrium, which may last hours or days after the BPPV is resolved,15 but others have compared follow up exercise program efficacy to no follow up exercise programs to rates of recurrence of symptoms of BPPV and found no significant differences.16,17 The length of time and number of repetitions per day of the exercise performance varies among opinions, with several variables being involved, including length of time from the onset to the time of clinical intervention. There appears to be a systematic process of recovery from vestibular insult8 with the initial phase of postural compensation and withdrawal from large body motion to relieve initial symptoms of vertigo and disequilibrium, whereby autogenic compensation or adaptation processes begin shortly after the onset of injury. The clinician sometimes needs to reverse or alter the subject’s newly learned restrictive movement patterns, while initializing prescribed exercise programs to reteach and integrate prior engrained movement patterns, or initiate new, novel movements. These include head and eye stabilization, and beginnings of small, simple, body motions for postural control. If not tolerated initially, these may initially be performed laying or sitting, and progressed to upright when tolerated. The performance of these maneuvers, and follow up rehabilitative exercise programs directly onto the affected vestibular apparatus could be deemed the only true peripheral vestibular system rehabilitation process, since all other forms of rehabilitation, including the follow-up or postmaneuver exercise programs themselves focus on adaptation of the central neurologic processes of motor pattern learning. This phenomenon was described prior with repeated peripheral vestibular insults after undergoing compensatory rehabilitation, whereby similar objective and subjective complaints were elicited.18
METHODS Upon initial assessment, the therapy program begins with the rehabilitation clinician obtaining a thorough history of the etiology of dysfunction. Various questionnaires have been developed to determine the magnitude of functional limitations and causes of and severity of symptoms. It is of utmost importance that the clinician gains an understanding of what has transpired from the time of injury and dysfunction to the time of initial
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assessment and treatment program. It is presumed there is an alteration almost immediately within the communication processes among all the central neurologic components and, thus, an alteration in the harmonious electrical patterns normally utilized. This alteration is perceived by the brain as an alteration to functionality and a compensatory pattern is begun. This causes a new pattern of afferent and efferent communication pattern, with resultant new feedback loops within the cerebellum, brainstem, premotor cortex, motor cortex, and basal ganglia, and new movement patterns generated. These new patterns are initially learned and stored within the cerebellum, but with repetition and use of the new patterns, they are engrained and stored within the basal ganglia for trunk and limb movements, to be used instead of the old patterns. This process forms the basis for repetitious vestibular rehabilitation exercises, for learning oculomotor, vestibular ocular, integrated vestibular visual, vestibular cancelation, and postural and balance functions. An assessment of known, common movement patterns by the clinician may show that newly learned and in-use patterns for functionality may be considered dysfunctional or pathologic in nature, and may place the subject in postural imbalance or at risk of balance loss or fall. For job or sport tasks, these altered movement patterns may cause diminished skills or tasks performance, which could place the subject at risk of further dysfunction or injury. Further studies have shown that following mTBI, the subject becomes more likely to suffer another subsequent head trauma, as well as other multiple orthopedic maladies compared to control subjects who had not previously experienced head injury. These findings may be related to the subject’s utilizing maladaptive patterns of head and eye coordinated movements, and/or abnormal postural corrective movement patterns.10 Spatial orientation and awareness may be altered, contributing also to abnormal adaptation processes. Further, connections between the vestibular components and the frontal lobe components for executive function components of cognition may be affected. Individualized, optimized, targeted rehabilitation program prescription is the goal of the rehabilitation clinician. To that end, a thorough objective assessment must be performed, which encompasses several domains being assessed. A hands-on, clinical approach is necessary, augmented with tests and measurements, using latest technologies for objectification and quantification of deficits. Sensitivity and specificity of measurement tools must be considered.
CLINICAL EXAM The clinician should begin with a simple history-taking and questioning involving age, height, weight, orientation, and any prior incidences of similar injury, with mechanism, initial symptoms and perceptions, loss of memory of events leading up to the time of injury (retrograde amnesia), problems forming new memory of events that occurred following the injury (anterograde amnesia), loss of consciousness, and functionality deficits. Details as to how the injury was initially cared for is of interest (transport to a medical facility, tests performed, diagnosis given, recommendations for management, and medications prescribed, etc.). Of particular concern to the examiner is the timeline of when the injury occurred to time of the current exam, and what the subject has been able to tolerate while performing ADL activities since the injury, with symptoms tolerance/limitations of
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functionality at present. Attention should be paid toward initial phase compensation patterns of restricted head, eyes, and body motions in attempt to limit symptoms production. This information is useful to the clinician when planning/establishing intensity of initial rehabilitative steps toward the goals of the rehabilitative processes to: (1) reduce symptoms; (2) improve static and dynamic balance function; and (3) improve general conditioning and ADL functionality.12,19 Additional information of contributory past medical history, family history of maladies/illnesses, headache (migraine or other classifications) history, and (if present) method of management, attention and/or learning disabilities, socialization issues, and prior cognitive deficits should be obtained. Changes in cognition or psychologic functionality should be followed by a clinical psychologist. Computerized screenings may be performed to document deficits in mentation. Determination of sleep status, either difficulty falling asleep (sleep onset), or difficulty staying asleep (sleep maintenance), should be performed. Sleep deficits may contribute to symptoms magnification or limit tolerance to cognition or physical activities, and should be managed by a clinical specialist in sleep disorders. Medications for normalizing the sleep cycle without inducing adverse effects of drowsiness or lethargy may be of benefit. An initial assessment of position changes and gait gives the examiner information as to any mobility limitations. Several validated tests may be employed for objective measures of mobility, such as: Timed Up and Go (TUG), Berg Balance Scale (Berg), Clinical Test of Sensory Interaction and Balance (CTSIB), the Functional Reach Test, Tinetti Balance Test of the Performance-Oriented Assessment of Mobility Problems (Tinetti), the Physical Performance Test (PPT), and the Functional Movement Screen.20,21 Reflex testing may elicit important hyporeflexia or hyperreflexia as signs of lower- or upper-motor neuron lesion (e.g., clonus, Babinski, etc.). Cerebellar/Coordination signs may be assessed: finger to nose, diadochokinesia, finger/foot tapping, heel-to-shin slide, and VOR cancellation. Hearing assessment with air and bone conduction auditory capacities may be determined by performing Weber and Rinne tests with a 512 and 1024 Hz tuning fork. The use of both will allow assessment for low- and high-frequency hearing loss to air and bone conduction. Asymmetry or positive findings should be followed with formal audiology testing. An orthopedic assessment of the cervical spine may follow. The range of motion/mobility deficits or hypermobility should be noted. Strength and mobility assessments should involve the upper and lower segments with active, passive, and segmental accessory motion testing with quadrant testing being performed. Assessment for occipital neuralgia and trigeminal neuralgia should be included. Rotation testing should involve head movements on the cervical spine, head and cervical spine movements on the torso, and torso movements under the stationary cervical spine. Postural deficits may be corrected at this point also. Assessment of cervical-ocular reflex and gaze stability exercises may be assessed at this juncture. A vision assessment may be performed next, including visual fields assessment, and oculomotor tests: smooth pursuit in horizontal, vertical, and diagonal directions, at varying velocities. Saccadic motions, predictive saccades, and antisaccades in all planes should be assessed. Abnormal spatial perceptions and/or depth perceptual deficits may be assessed with convergence and divergence tests, along with peripheral vision assessment. Sensitivity to motion may be detected with adding OKN stimulation.22 Assessments of
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strabismus may be performed with a cover test, and referral for Ophthalmology evaluation if any test appears to be abnormal. Oculography with augmented infra-red eye tracking technology or Frenzel lenses with Vestibular Electromyogenic Potential (VEMPs), and Video Head Impulse Testing (vHIT) may be helpful in detection of central versus peripheral vestibular dysfunction, evaluating spontaneous nystagmus in light and dark environments, gaze evoked nystagmus, and head shake testing. However, there is conflicting evidence within the literature as to the benefits and sensitivity of these tests.23 26 Suppression of nystagmus with ocular fixation with Frenzel lenses, Fresnel lens device27 added may lead the examiner more toward peripheral etiology rather than central origin, but should not be used alone, but in conjunction with other testing methods to be definitive.28 The results of the testing (detection of nystagmus and direction and performance of the nystagmus) may assist the examiner with decision-making for further testing (e.g., imaging studies, ENG with caloric irrigation, rotational chair, etc., if the patient is seen as being in the acute phase of symptoms onset). Further testing of Dynamic Visual Acuity (DVAT) in comparison to static acuity and/or a Gaze Stability Test (GST) may assist in detection of velocity limits for gaze stability and target recognition, and Subjective Visual Vertical assessment compared with cVEMP and oVEMP tests may clarify the contribution of the otolithic system (saccule and utricle).29 Computerized Dynamic Posturography (CDP) may be used to better determine the various components (vestibular, visual, somatosensory/proprioception) of balance maintenance, and adaptive strategy for compensation for falls prevention, symptoms reduction, and improved functionality.12 Ideally there exists an optimal relationship among the components for balance maintenance.30,31 The rehabilitation clinician may use the results of the CDP for planning specific rehabilitative measures to enhance the deficient component(s) and/or implement substitutive strategies. Further integration of the strategies may be achieved with augmented general activity exercise (walking, jogging, cycling, etc.) with the specific task challenges implemented. It should be noted that implementation of a balance rehabilitative program alone, without first initiating visual-based rehabilitative measures, will elicit a less than optimal balance strategy recovery. However, implementation of visual-based strategies has shown improvement of postural stability even without use of postural stability and balance exercises.32 The relationship of the executive function component of cognition and functionality must be considered as part of the rehabilitation assessment and treatment program. Several validated psychology scales and assessment tools exist for measurement and quan® tification of cognition, anxiety, concentration, and memory.33 37 In sports, the ImPACT test remains the standard; however, use of it or other similar computerized test measures (e.g., Axon Sports, ANAM) as a standalone measure of magnitude of injury, or readiness for return to participation has been questioned due to invalid baseline test scores due to subjects’ intentional manipulation of results, less than optimal testing conditions employed, or variable test retest results among examiners.38 However, further research is needed to determine the longitudinal relationship of cognition deficits to task performance and adaptation with vestibular rehabilitation processes. Development of new technologies for quantifying functionality and executive function components of cognition and task performance have been described.39,40 Use of eye-tracking technologies, and blood/ saliva-borne biomarkers, as well as the use of advanced imaging techniques are emerging
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as potential next-generation measures, due to their not requiring baseline comparative testing, and the limited ability of the subject to intentionally render invalid test results. Use of virtual and augmented reality devices for rehabilitation are also gaining popularity,41 44 yet further investigation is merited.
PROTOCOL A comprehensive, team-based approach to assessment and rehabilitation, including targeted, specific vestibular rehabilitation exercise combined with general exercise programs has been shown to elicit positive effects of symptoms limitation and an enhanced speed of functionality recovery after mTBI. Initiation and prescription of rehabilitation protocols is the second of three classically described phases of recovery following vestibular insult8 and is dependent on the tolerance of the subject, and somewhat determined by the timeline of injury, initiation of symptoms, and up-to-date compensation patterns employed. Recovery from injury is variable among subjects, requiring the astute clinician to formulate a program of recovery specific to the needs of the subject.30,31,45 The clinician is often first required to reverse first stage patterns of vestibular compensation that self-limit the subject’s head, eyes, and body mobilities. Notification of probability of increased symptoms production and use of prophylactic antiemetic medications may limit the subject’s anxiety toward initial exercise performance, and enhance compliance. Post-injury increased reflex response times to auditory cues suggests the possibility of enhancing auditory inputs (amplification with aides, etc.) as being helpful for recovery. Initially, exercise may be given with the subject supine or seated, to eliminate confounding somatosensory inputs. Regaining normative mobility of the cervical spine is imperative to allow for the full range of motion of the head and eyes for the vision-based exercises. Vision-based exercises for VOR recovery usually requires 4 weeks duration46 and requires daily compliance and exercise adherence. Current research efforts toward improved compliance utilizing smartphone technologies and playing video games has shown positive effects. Posture for performing exercises may be progressed from lying to sitting, to standing, to walking, or moving—as tolerated. Frequency and velocity of target acquisition is important, as the VOR is velocity specific. Likened to orthopedic active muscle rehabilitation techniques, velocity of exercises should be varied, and later in the rehabilitation process should be task-specific oriented. Use of timing devices (e.g., metronome) or more advanced computerized DVA and/or GST may be beneficial for measurement of thresholds tolerance.47,48 Advancement toward balance and proprioceptive exercises requires varied multisensory stimulation, including varied visual inputs limitations and challenging the base of support positions, along with varied surface textures. Progression from static positioning to movement-based exercise should be directed from small movements toward large-arc, segmented, body motions with functional application. Proprioceptive Neuromuscular Facilitation (PNF) exercises may be useful. Postural and balance exercise generally requires longer duration for full recovery, and may take up to 3 months, depending upon the availability of VOR stability and spatial orientation recovery.49 During the initial phase of recovery (24 48 hours post-injury), cognitive stress should be avoided, and normalization of the sleep cycle appears to be critical, as protracted recovery appears to result from failure to remove stressors and persistence of abnormal sleep IV. DIAGNOSIS AND TREATMENT
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cycles, though this may be age and gender specific. Further research is merited regarding removal of cognitive stressors with sleep pattern modulation, and progression to back to normal daily functions throughout the second and third phases of recovery. Initiation of an appropriate timeline and subsequent immersion into a vestibular and balance rehabilitation programs has shown positive benefits to cognition, even without being involved directly in a cognitive rehabilitative program.
SUMMARY/CONCLUSION Concussion/mTBI injury continues to gain public and medical professional awareness, as media coverage is heightened and increased medical research efforts give rise to empirical data to support novel objective measures and methods in combination with traditional symptom-based management. While imaging studies and blood/saliva biomarkers tests are emerging for detection, a hierarchal comprehensive assessment and rehabilitative team approach50 appears to have merit in symptom resolution and progression toward functionality.8 While efforts are made toward public education of recognition of signs and symptoms of mTBI, education of medical professionals appears merited for appropriate recognition and medical management. The astute medical and rehabilitative clinicians should be aware of the timeline of recovery at the time of assessment, the appropriate steps toward resolution for each of the three recovery stages, and the appropriate initiation and progression of objective testing and rehabilitative methods for each. Since dizziness is the most common symptom following mTBI, vestibular assessment and rehabilitative approaches have shown benefits for head and eye movement stabilization and recovery, and subsequent progressive balance and movement exercises restores static and dynamic balance, gait, and ADL functionality.51 Compliance and adherence to a prescribed recovery protocol remains a challenge, but new technologies are emerging to address it. This may allow the rehabilitation clinician to assess and monitor subjects remotely, and progress the rehabilitation program when direct access to a professional is limited. The sequelae of mistimed or inappropriate management appear to be a protracted recovery time, limited functionality, and symptoms persistence. Attention to sleep pattern normalization and cognitive recovery processes appear critical at the initial phase of recovery, as these appear to impact headache and accompanying symptoms’ persistence. Further research is merited in all aspects of medical/rehabilitative management, particularly the areas of sleep cycle and headache management, dosage and duration of rehabilitative exercise programs, objective measurement protocols to determine when thresholds of recovery steps are met, and thresholds of recovery for the safe return to participation in ADL activities (e.g., driving, sports, etc.). Longitudinal studies of cognition, repetitive trauma effects, and rehabilitative management protocols give the researcher/clinician ample opportunity to advance the science of this malady.
References 1. Gottshall K. Vestibular rehabilitation after mild traumatic brain injury with vestibular pathology. NeuroRehabilitation 2011;29(2):167 71. 2. Hillier SL, McDonnell M. Vestibular rehabilitation for unilateral peripheral vestibular dysfunction. Cochrane Database Syst Rev 2011;16:248 9
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3. Lei-Rivera L, et al. Special tools for the assessment of balance and dizziness in individuals with mild traumatic brain injury. NeuroRehabilitation 2013;32(3):463 72. 4. Ito M. Cerebellar long-term depression: characterization, signal transduction, and functional roles. Physiol Rev 2001;81:1144 95. 5. De Zeeuw CI, Hansel C, Bian F, Koekkoek SKE, van Alphen AM, Linden DJ, et al. Expression of a protein kinase C inhibitor in Purkinje cells blocks cerebellar LTD and adaptation of the vestibulo-ocular reflex. Neuron 1998;20:495 508. 6. Leitges M, Kovac J, Plomann M, Linden DJ. A unique PDZ ligand in PKCa confers induction of cerebellar long-term synaptic depression. Neuron 2004;44:585 94. 7. Linden DJ, Connor JA. Long-term synaptic depression. Annu Rev Neurosci 1995;18:319 57. 8. Balaban CD, et al. Top-down approach to vestibular compensation: translational lessons from vestibular rehabilitation. Brain Res 2012;1482:101 11. 9. Brooks MA, Peterson K, Biese K, Sanfilippo J, Heiderscheit BC, Bell DR. Concussion increases odds of sustaining a lower extremity musculoskeletal injury after return to play among collegiate athletes. Am J Sports Med 2016;44(3):742 7. 10. Herman DC, Jones D, Harrison A, Moser M, Tillman S, Farmer K, et al. Concussion may increase the risk of subsequent lower extremity musculoskeletal injury in collegiate athletes. Sports Med 2017;47(5):1003 10. 11. Fetter M. Acute unilateral loss of vestibular function. Handb Clin Neurol 2016;137:219 29. 12. Herdman SJ, Whitney SL. Interventions for the patient with vestibular hypofunction. In: Herdman SJ, editor. Vestibular rehabilitation. Philadelphia, PA: F.A. Davis; 2007. p. 309 37. 13. Imai T, et al. Classification, diagnostic criteria and management of benign paroxysmal positional vertigo. Auris Nasus Larynx 2017;44(1):1 6. 14. Zhang, Y.X., et al. Comparison of three types of self-treatments for posterior canal benign paroxysmal positional vertigo: modified Epley maneuver, Zhonghua Er Bi Yan Hou Tou Jing Wai Ke Za Zhi 2012;47(10):799 803. 15. Beynon GJ. A review of management of benign paroxysmal positional vertigo by exercise therapy and by repositioning manoeuvres. Br J Audiol 1997;31(1):11 26. 16. Semont maneuver and Brandt-Daroff maneuver. Zhonghua Er Bi Yan Hou Tou Jing Wai Ke Za Zhi 2012;47 (10):799 803. 17. Helminski JO, et al. Strategies to prevent recurrence of benign paroxysmal positional vertigo. Arch Otolaryngol Head Neck Surg 2005;131(4):344 8. 18. Helminski JO, et al. Daily exercise does not prevent recurrence of benign paroxysmal positional vertigo. Otol Neurotol 2008;29(7):976 81. 19. Magnus, R. Body posture 5 Korperstellung: experimental-physiological investigations of the reflexes involved in body posture, their cooperation and disturbances; based on a translation by William R. Rosanoff, and on a translation by Franklin Book Programs, Inc., Cairo, for the National Library of Medicine, Amerind, Springfield, VA, USA; 1924 (reprint 1980). 20. Whitney SL, Sparto PJ. Principles of vestibular physical therapy rehabilitation. Neuro Rehabil 2011;29:157 66. 21. Stanek JM, et al. Active duty firefighters can improve Functional Movement Screen (FMS) scores following an 8-week individualized client workout program. Work 2017;56(2):213 20. 22. Pavlou M. The use of optokinetic stimulation in vestibular rehabilitation. J Neurol Phys Ther 2010;34(2):105 10. 23. Cohen HS, et al. Utility of quick oculomotor tests for screening the vestibular system in the subacute and chronic populations. Acta Otolaryngol 2017;138(4):1 5. 24. Tamas TL, et al. Emergency diagnosis of the acute vestibular syndrome. Orv Hetil 2017;158(51):2029 40. 25. Lance S, Mossman SS. Misleading signs in acute vertigo. Pract Neurol. 2017;18(2):162 5 26. van de Berg R, et al. Laboratory examinations for the vestibular system. Curr Opin Neurol 2018;31(1):111 16. 27. Strupp M, et al. The takeaway Frenzel goggles: a Fresnel-based device. Neurology 2014;83(14):1241 5. 28. An SY, et al. Clinical roles of fixation suppression failure in dizzy patients in the ENT clinic. Acta Otolaryngol 2014;134(11):1134 9. 29. Slattery EL, et al. Vestibular tests for rehabilitation: applications and interpretation. NeuroRehabilitation 2011;29 (2):143 51. 30. Collins JJ, De Luca CJ. The effects of visual input on open-loop and closed-loop postural control mechanisms. Exp Brain Res 1995;103:151 63.
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31. Lacour M, Barthelemy J, Borel L, Magnan J, Xerri C, Chays A, et al. Sensory strategies in human postural control before and after unilateral vestibular neurotomy. Exp Brain Res 1997;115:300 10. 32. Morimoto H, Asai Y, Johnson EG, Lohman EB, Khoo K, Mizutani Y, et al. Effect of oculo-motor and gaze stability exercises on postural stability and dynamic visual acuity in healthy young adults. Gait Post 2011;33:600 3. 33. Hazlett RL, Tusa RJ, Waranch HR. Development of an inventory for dizziness and related factors. J Behav Med 1996;19:73 85. 34. Jacobson GP, Newman WW. The development of the dizziness handicap inventory. Arch Otolaryngol Head Neck Surg 1990;116:424 7. 35. Morris AE, Lutman ME, Yardley L. Measuring outcome from vestibular rehabilitation, part I: quantitative development of a new self-report measure. Int J Audiol 2008;47:169 77. 36. Morris AE, Lutman ME, Yardley L. Measuring outcome from vestibular rehabilitation, part II: refinement and validation of a new self-report measure. Int J Audiol 2009;48:24 37. 37. Yardley L, Masson E, Verschuur C, Haacke N, Luxon L. Symptoms, anxiety and handicap in dizziness patients: development of the Vertigo Symptom Scale. J Psychosom Res 1992;36:731 41. 38. Nelson LD, et al. Rates and predictors of invalid baseline test performance in high school and collegiate athletes for 3 computerized neurocognitive tests: ANAM, Axon Sports, and ImPACT. Am J Sports Med 2015;43 (8):2018 26. 39. Leyva A, Balachandran A, Britton JC, Eltoukhy M, Kuenze C, Myers ND, et al. The development and examination of a new walking executive function test for people over 50 years of age. Physiol Behav 2017;171:100 9. 40. Perrochon A, Kemoun G, Watelain E, Dugue B, Berthoz A. The “Stroop Walking Task”: an innovative dual-task for the early detection of executive function impairment. Neurophysiol Clin 2015;45(3):181 90. 41. Bergeron M, Lortie CL, Guitton MJ. Use of virtual reality tools for vestibular disorders rehabilitation: a comprehensive analysis. Adv Med 2015;2015:916735. 42. Chang YJ, Kang YS, Huang PC. An augmented reality (AR)-based vocational task prompting system for people with cognitive impairments. Res Dev Disabil 2013;34(10):3049 56. 43. Biffi E, Beretta E, Diella E, Panzeri D, Maghini C, Turconi AC, et al. Gait rehabilitation with a high tech platform based on virtual reality conveys improvements in walking ability of children suffering from acquired brain injury. Conf Proc IEEE Eng Med Biol Soc 2015;2015:7406 9. 44. Khademi M, Hondori HM, Dodakian L, Cramer S, Lopes CV. Comparing “pick and place” task in spatial Augmented Reality versus non-immersive Virtual Reality for rehabilitation setting. Conf Proc IEEE Eng Med Biol Soc 2013;2013:4613 16. 45. Peterka RJ, Statler KD, Wrisley DM, Horak FB. Postural compensation for unilateral vestibular loss. Front Neurol 2011;57:1 13; 2011;2:Article. 46. Herdman SJ, Schubert MC, Das VE, Tusa RJ. Recovery of dynamic visual acuity in unilateral vestibular hypofunction. Arch Otolaryngol Head Neck Surg 2003;129:819 24. 47. Gottshall KR, Hoffer ME. Tracking recovery of vestibular function in Individuals With blast-induced head trauma using vestibular—visual-cognitive interaction tests. J Neurol Phys Ther 2010;34:94 7. 48. Gottshall K, et al. Objective vestibular tests as outcome measures in head injury patients. Laryngoscope 2003;113(10):1746 50. 49. Borel L, Harlay F, Magnan J, Chays A, Lacour M. Deficits and recovery of head and trunk orientation and stabilization after unilateral vestibular loss. Brain 2002;125:880 94. 50. Gottshall KR, Sessoms PH. Improvements in dizziness and imbalance results from using a multi-disciplinary and multi-sensory approach to Vestibular Physical Therapy—a case study. Front Syst Neurosci 2015;9:106. 51. Alsalaheen BA, et al. Exercise prescription patterns in patients treated with vestibular rehabilitation after concussion. Physiother Res Int 2013;18(2):100 8.
IV. DIAGNOSIS AND TREATMENT
24 mTBI/Concussion: Assessment and Rehabilitation Strategy and Program Optimization James K. Buskirk, MS Ed., PT, SCS, AIB-CON Department of Otolaryngology, Batchelor’s Children’s Research Institute, University of Miami, Miller School of Medicine, Miami, FL, United States
BACKGROUND To provide appropriate assessment and rehabilitative therapies for a specific disorder related to mTBI/Concussion, or its most common component (94% prevalence rate)1 of vestibular dysfunction (whether peripheral, central, or mixed origins), one must first ascertain and understand the heterogeneity of the commonly multifactorial dysfunction. Establishing a history, including timeline of onset, progression of functional limitations, and associated symptoms is critical for the rehabilitative clinician to establish an effective assessment and subsequent treatment program. A review of prior studies2 showed effectiveness of various rehabilitation approaches for peripheral vestibular loss with varied outcomes, leading to an individualized approach dependent on objective testing, functional presentation, and symptoms tolerance as most effective, due to progressive, targeted rather than general exercise approach. A lack of understanding of the importance of the multiple components of mTBI, or a lack of understanding of the initial self-limiting compensatory mechanisms and associated timelines may lead the clinician to not fully assess all the components of the disorder and findings relative to the persistent symptoms and functional limitations, and erroneously prescribe an inappropriate rehabilitation program, with less than optimal results obtained. Optimized, or targeted rehabilitation prescription for mTBI with associated vestibular dysfunction component has gained popularity with the advancement of technologies for objectification and quantification of both peripheral and central neurologic sensory and motor dysfunctions, and use of validated scales to quantify the presence and magnitude of common symptoms of mTBI, including (but not
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limited to): dizziness, vertigo, disequilibrium, sleep disorder, impaired cognition, anxiety and depression, and headache.3 These are often accompanied by musculoskeletal symptoms and resultant functional activities of daily living (ADL) limitations. Measurement of transmembrane ionic flow and resultant electrical current flow produced at the cellular level, as evidenced by what is elicited by the types I and II hair cells located within the audio-vestibular system, along with mapping of microcircuits linking the vestibular afferents with the cerebellum, hippocampus, and inferior olive has shown a baseline discharge rate inherent to each component anatomic part of the peripheral and central neurologic systems.4 These rates function in harmony and in real-time, allowing communication among all the component anatomic parts, via the complex network of excitatory and inhibitory synapses inherent to each. The synaptic junctions contain excitatory or inhibitory neurotransmitters which cause action potential modulation with resultant messages sent in the cerebellum via the mossy and climbing fibers, and throughout the central and peripheral systems.4 7 This baseline engrained pattern of cellular and, therefore, neuron discharges is unique to individuals, and may be altered with injury, surgery, or disease, and positively altered by rehabilitative, specific-task training. Specific motor/movement plans and patterns become engrained over time as a learned pattern, and stored within various parts of the brain and brainstem for basic and advanced cranial nerve functions, and gross motor tasks are initially “learned” within the cerebellum, and then integrated within the basal ganglia. Since some functionality tasks are shared among all individuals, there appears to exist a “common thread” of movement plans and patterns by species, which are further altered by repetitive daily activities. Additional, or refined patterns exist among subsets of individuals pertinent to individual task requirements for ADL, job, or sport related activities. Thus, one could hold to the assumption that this inherent rate of discharge can be altered as an adaptation to environmental changes, or alterations to the discharge rate elicited by external factors (disease, trauma, aging, etc.) or with specific task training, repetitiously. One also can assume also that the impulse patterns can be further modified or altered by training or learning new patterns of behavior and movements, with resultant functional adaptation. This ability for modulation forms the basis for an apparent hierarchy of phases of rehabilitation and recovery from mTBI, vestibular, and balance deficits.8 Prior studies have also reported a higher incidence of musculoskeletal injury in athletes after sustaining mTBI as compared to control subjects not subjected to head injury.9,10 This lends itself to the assumption of the second phase of vestibular recovery not being fully completed, with incomplete adaptation to new or relearning prior engrained movement patterns. This may include eye and head motions, as well as postural stability alterations, with learned aberrant auditory and cognitive functions which may also impact physical task performance. The peripheral vestibular system discharges at approximately 90 spikes/second at rest, and increase rapidly with head and body motions.11 These impulses are carried by both the superior and inferior branches of the vestibular portion of cranial nerve VIII to the vestibular nuclei in the midbrain. The vestibular labyrinths elicit increased unilateral discharges from the side moved toward, and resultant contralateral decreased discharges (inhibition) from the side moved away from. The otolithic system (saccule and utricle) elicit discharges continuously, and increase with translational motions horizontally and/or vertically, in response to changes in alignment with force of gravity. At the vestibular nuclei, various connections or synapses are formed with neurons
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that connect to the nuclei of cranial nerves III, IV, and VI, the cerebellum, inferior olive, and premotor and motor cortices. The oculomotor cranial nerves activate concentric or eccentric motions of the eyes to maintain focus of the environment onto the ocular fovea. Vergence of the eyes is critical for visual motion detection and spatial perception. Alterations of the necessary pathways for normal eye coordinated motions give rise to aberrant perception and elicits symptoms of disorientation. Movement of the head elicits activation of the semicircular canal mechanisms bilaterally, and concomitant change in orientation with line of gravity of the otolithic system, causing changes in electrical discharge and conduction rates of both. The importance of the oculomotor system, along with the vestibular-ocular reflex (VOR) and coordination of eyes and head motions for rehabilitation processes has been recognized for many years.12 Absence or dysfunction of such coordination elicits nystagmus and other abnormal eye movements, with resultant retinal slip, or inability to keep a visual target on the retinal fovea. Corrective saccadic eye motions are needed to replace the target back onto the retinal fovea. This extraneous eye movement elicits visual distortion and abnormal spatial perception, or dizziness symptoms. Often a subject with abnormal VOR function will rely solely on oculomotor function for spatial awareness and orientation, opting to avoid head motions entirely. Pathology of the oculomotor system affects both static visual acuity, as well as visual tracking with head and body motions. Further internal feedback loop pathways via the cerebellum, basal ganglia, and motor cortex enable alterations and refining, or “smoothing,” functions of excitation and/or inhibition of neuronal pool firing, influencing postural control, and when altered, elicits loss of balance and disequilibrium symptoms. The basal ganglia, additionally, performs centrally similarly to a “switching” mechanism, whereby neural pathways are integrated from, and sent out to, the components of the limbic system, thus modulating emotions and cognitive behaviors associated with the dysfunction. An understanding of this anatomic and physiologic relationship among the component parts allows the rehabilitation clinician to objectify and categorize symptoms reported and, therefore, form the optimized rehabilitative approach for mTBI. Benign paroxysmal positional vertigo (BPPV) has been described in the literature for many years as the result of otoconia within the otolithic system (saccule and utricle) becoming free floating within the endolymphatic fluid and relocating into one or more of the semicircular canals, causing severe vertigo whenever the subject positions the head in such a manner as to cause the otoconia to move, creating an eddy current. There appears to be a natural turn-over of the otoconia whereby “old,” or mature, otoconia are replaced by “new” ones. This process may be regulated by the ionic flow and resultant electrical current produced by the basement membrane and the outer most portion of the cellular membrane of the otoconia. Whether this is an electrical bond or chemical bond, or both, is not fully understood. Therefore, one potential cause of BPPV is alteration of the removal of the “old” otoconia or alteration of the generation of the “new” otoconia. Various external causes of BPPV have also been described, including viral infections, migraine with (or without) accompanying headache, and exposure to trauma such as that sustained which causes central pathologies, like mTBI/concussions. It is thought the otolithic otoconia are held in place on the surfaces/basement membranes of the utricle (more positioned in the horizontal plane) and saccule (more positioned in the vertical plane) by an electrical and/ or chemical bond. A disruption of the bond by trauma or by changes in ionic flow and,
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thus, electrical current flow at the cellular membrane level may cause loosening of them from the basement membrane and subsequent head motions then position them pathologically into the labyrinths. If the otoconia remain free-floating within the endolymphatic fluid, it is termed canalithiasis. However, if the outermost membranes of the otoconia become “sticky,” or adherent to the cupula, and are no longer free-floating within the endolymphatic fluid, it is termed cupulolithiasis.13 Again, the mechanisms involved in making the otoconia “sticky” are not fully understood, but may be explained by alterations in membrane potentials generated by alterations in ionic flow across the membrane, with resultant chemical and/or electrical effects, causing the affinity or adherence to the innermost lining of the endolymphatic sac within the labyrinth, or directly to the cupula. Several liberatory maneuvers with risks and benefits have been described and compared for efficacy to reposition the otoconia back out of the labyrinths and again into the otolithic organs, thus, relieving the vertigo symptoms.14 Following performance of the maneuvers, several different exercise programs have been suggested, to continue to resolve the oftenpresent concomitant symptoms of dizziness and disequilibrium, which may last hours or days after the BPPV is resolved,15 but others have compared follow up exercise program efficacy to no follow up exercise programs to rates of recurrence of symptoms of BPPV and found no significant differences.16,17 The length of time and number of repetitions per day of the exercise performance varies among opinions, with several variables being involved, including length of time from the onset to the time of clinical intervention. There appears to be a systematic process of recovery from vestibular insult8 with the initial phase of postural compensation and withdrawal from large body motion to relieve initial symptoms of vertigo and disequilibrium, whereby autogenic compensation or adaptation processes begin shortly after the onset of injury. The clinician sometimes needs to reverse or alter the subject’s newly learned restrictive movement patterns, while initializing prescribed exercise programs to reteach and integrate prior engrained movement patterns, or initiate new, novel movements. These include head and eye stabilization, and beginnings of small, simple, body motions for postural control. If not tolerated initially, these may initially be performed laying or sitting, and progressed to upright when tolerated. The performance of these maneuvers, and follow up rehabilitative exercise programs directly onto the affected vestibular apparatus could be deemed the only true peripheral vestibular system rehabilitation process, since all other forms of rehabilitation, including the follow-up or postmaneuver exercise programs themselves focus on adaptation of the central neurologic processes of motor pattern learning. This phenomenon was described prior with repeated peripheral vestibular insults after undergoing compensatory rehabilitation, whereby similar objective and subjective complaints were elicited.18
METHODS Upon initial assessment, the therapy program begins with the rehabilitation clinician obtaining a thorough history of the etiology of dysfunction. Various questionnaires have been developed to determine the magnitude of functional limitations and causes of and severity of symptoms. It is of utmost importance that the clinician gains an understanding of what has transpired from the time of injury and dysfunction to the time of initial
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assessment and treatment program. It is presumed there is an alteration almost immediately within the communication processes among all the central neurologic components and, thus, an alteration in the harmonious electrical patterns normally utilized. This alteration is perceived by the brain as an alteration to functionality and a compensatory pattern is begun. This causes a new pattern of afferent and efferent communication pattern, with resultant new feedback loops within the cerebellum, brainstem, premotor cortex, motor cortex, and basal ganglia, and new movement patterns generated. These new patterns are initially learned and stored within the cerebellum, but with repetition and use of the new patterns, they are engrained and stored within the basal ganglia for trunk and limb movements, to be used instead of the old patterns. This process forms the basis for repetitious vestibular rehabilitation exercises, for learning oculomotor, vestibular ocular, integrated vestibular visual, vestibular cancelation, and postural and balance functions. An assessment of known, common movement patterns by the clinician may show that newly learned and in-use patterns for functionality may be considered dysfunctional or pathologic in nature, and may place the subject in postural imbalance or at risk of balance loss or fall. For job or sport tasks, these altered movement patterns may cause diminished skills or tasks performance, which could place the subject at risk of further dysfunction or injury. Further studies have shown that following mTBI, the subject becomes more likely to suffer another subsequent head trauma, as well as other multiple orthopedic maladies compared to control subjects who had not previously experienced head injury. These findings may be related to the subject’s utilizing maladaptive patterns of head and eye coordinated movements, and/or abnormal postural corrective movement patterns.10 Spatial orientation and awareness may be altered, contributing also to abnormal adaptation processes. Further, connections between the vestibular components and the frontal lobe components for executive function components of cognition may be affected. Individualized, optimized, targeted rehabilitation program prescription is the goal of the rehabilitation clinician. To that end, a thorough objective assessment must be performed, which encompasses several domains being assessed. A hands-on, clinical approach is necessary, augmented with tests and measurements, using latest technologies for objectification and quantification of deficits. Sensitivity and specificity of measurement tools must be considered.
CLINICAL EXAM The clinician should begin with a simple history-taking and questioning involving age, height, weight, orientation, and any prior incidences of similar injury, with mechanism, initial symptoms and perceptions, loss of memory of events leading up to the time of injury (retrograde amnesia), problems forming new memory of events that occurred following the injury (anterograde amnesia), loss of consciousness, and functionality deficits. Details as to how the injury was initially cared for is of interest (transport to a medical facility, tests performed, diagnosis given, recommendations for management, and medications prescribed, etc.). Of particular concern to the examiner is the timeline of when the injury occurred to time of the current exam, and what the subject has been able to tolerate while performing ADL activities since the injury, with symptoms tolerance/limitations of
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functionality at present. Attention should be paid toward initial phase compensation patterns of restricted head, eyes, and body motions in attempt to limit symptoms production. This information is useful to the clinician when planning/establishing intensity of initial rehabilitative steps toward the goals of the rehabilitative processes to: (1) reduce symptoms; (2) improve static and dynamic balance function; and (3) improve general conditioning and ADL functionality.12,19 Additional information of contributory past medical history, family history of maladies/illnesses, headache (migraine or other classifications) history, and (if present) method of management, attention and/or learning disabilities, socialization issues, and prior cognitive deficits should be obtained. Changes in cognition or psychologic functionality should be followed by a clinical psychologist. Computerized screenings may be performed to document deficits in mentation. Determination of sleep status, either difficulty falling asleep (sleep onset), or difficulty staying asleep (sleep maintenance), should be performed. Sleep deficits may contribute to symptoms magnification or limit tolerance to cognition or physical activities, and should be managed by a clinical specialist in sleep disorders. Medications for normalizing the sleep cycle without inducing adverse effects of drowsiness or lethargy may be of benefit. An initial assessment of position changes and gait gives the examiner information as to any mobility limitations. Several validated tests may be employed for objective measures of mobility, such as: Timed Up and Go (TUG), Berg Balance Scale (Berg), Clinical Test of Sensory Interaction and Balance (CTSIB), the Functional Reach Test, Tinetti Balance Test of the Performance-Oriented Assessment of Mobility Problems (Tinetti), the Physical Performance Test (PPT), and the Functional Movement Screen.20,21 Reflex testing may elicit important hyporeflexia or hyperreflexia as signs of lower- or upper-motor neuron lesion (e.g., clonus, Babinski, etc.). Cerebellar/Coordination signs may be assessed: finger to nose, diadochokinesia, finger/foot tapping, heel-to-shin slide, and VOR cancellation. Hearing assessment with air and bone conduction auditory capacities may be determined by performing Weber and Rinne tests with a 512 and 1024 Hz tuning fork. The use of both will allow assessment for low- and high-frequency hearing loss to air and bone conduction. Asymmetry or positive findings should be followed with formal audiology testing. An orthopedic assessment of the cervical spine may follow. The range of motion/mobility deficits or hypermobility should be noted. Strength and mobility assessments should involve the upper and lower segments with active, passive, and segmental accessory motion testing with quadrant testing being performed. Assessment for occipital neuralgia and trigeminal neuralgia should be included. Rotation testing should involve head movements on the cervical spine, head and cervical spine movements on the torso, and torso movements under the stationary cervical spine. Postural deficits may be corrected at this point also. Assessment of cervical-ocular reflex and gaze stability exercises may be assessed at this juncture. A vision assessment may be performed next, including visual fields assessment, and oculomotor tests: smooth pursuit in horizontal, vertical, and diagonal directions, at varying velocities. Saccadic motions, predictive saccades, and antisaccades in all planes should be assessed. Abnormal spatial perceptions and/or depth perceptual deficits may be assessed with convergence and divergence tests, along with peripheral vision assessment. Sensitivity to motion may be detected with adding OKN stimulation.22 Assessments of
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strabismus may be performed with a cover test, and referral for Ophthalmology evaluation if any test appears to be abnormal. Oculography with augmented infra-red eye tracking technology or Frenzel lenses with Vestibular Electromyogenic Potential (VEMPs), and Video Head Impulse Testing (vHIT) may be helpful in detection of central versus peripheral vestibular dysfunction, evaluating spontaneous nystagmus in light and dark environments, gaze evoked nystagmus, and head shake testing. However, there is conflicting evidence within the literature as to the benefits and sensitivity of these tests.23 26 Suppression of nystagmus with ocular fixation with Frenzel lenses, Fresnel lens device27 added may lead the examiner more toward peripheral etiology rather than central origin, but should not be used alone, but in conjunction with other testing methods to be definitive.28 The results of the testing (detection of nystagmus and direction and performance of the nystagmus) may assist the examiner with decision-making for further testing (e.g., imaging studies, ENG with caloric irrigation, rotational chair, etc., if the patient is seen as being in the acute phase of symptoms onset). Further testing of Dynamic Visual Acuity (DVAT) in comparison to static acuity and/or a Gaze Stability Test (GST) may assist in detection of velocity limits for gaze stability and target recognition, and Subjective Visual Vertical assessment compared with cVEMP and oVEMP tests may clarify the contribution of the otolithic system (saccule and utricle).29 Computerized Dynamic Posturography (CDP) may be used to better determine the various components (vestibular, visual, somatosensory/proprioception) of balance maintenance, and adaptive strategy for compensation for falls prevention, symptoms reduction, and improved functionality.12 Ideally there exists an optimal relationship among the components for balance maintenance.30,31 The rehabilitation clinician may use the results of the CDP for planning specific rehabilitative measures to enhance the deficient component(s) and/or implement substitutive strategies. Further integration of the strategies may be achieved with augmented general activity exercise (walking, jogging, cycling, etc.) with the specific task challenges implemented. It should be noted that implementation of a balance rehabilitative program alone, without first initiating visual-based rehabilitative measures, will elicit a less than optimal balance strategy recovery. However, implementation of visual-based strategies has shown improvement of postural stability even without use of postural stability and balance exercises.32 The relationship of the executive function component of cognition and functionality must be considered as part of the rehabilitation assessment and treatment program. Several validated psychology scales and assessment tools exist for measurement and quan® tification of cognition, anxiety, concentration, and memory.33 37 In sports, the ImPACT test remains the standard; however, use of it or other similar computerized test measures (e.g., Axon Sports, ANAM) as a standalone measure of magnitude of injury, or readiness for return to participation has been questioned due to invalid baseline test scores due to subjects’ intentional manipulation of results, less than optimal testing conditions employed, or variable test retest results among examiners.38 However, further research is needed to determine the longitudinal relationship of cognition deficits to task performance and adaptation with vestibular rehabilitation processes. Development of new technologies for quantifying functionality and executive function components of cognition and task performance have been described.39,40 Use of eye-tracking technologies, and blood/ saliva-borne biomarkers, as well as the use of advanced imaging techniques are emerging
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as potential next-generation measures, due to their not requiring baseline comparative testing, and the limited ability of the subject to intentionally render invalid test results. Use of virtual and augmented reality devices for rehabilitation are also gaining popularity,41 44 yet further investigation is merited.
PROTOCOL A comprehensive, team-based approach to assessment and rehabilitation, including targeted, specific vestibular rehabilitation exercise combined with general exercise programs has been shown to elicit positive effects of symptoms limitation and an enhanced speed of functionality recovery after mTBI. Initiation and prescription of rehabilitation protocols is the second of three classically described phases of recovery following vestibular insult8 and is dependent on the tolerance of the subject, and somewhat determined by the timeline of injury, initiation of symptoms, and up-to-date compensation patterns employed. Recovery from injury is variable among subjects, requiring the astute clinician to formulate a program of recovery specific to the needs of the subject.30,31,45 The clinician is often first required to reverse first stage patterns of vestibular compensation that self-limit the subject’s head, eyes, and body mobilities. Notification of probability of increased symptoms production and use of prophylactic antiemetic medications may limit the subject’s anxiety toward initial exercise performance, and enhance compliance. Post-injury increased reflex response times to auditory cues suggests the possibility of enhancing auditory inputs (amplification with aides, etc.) as being helpful for recovery. Initially, exercise may be given with the subject supine or seated, to eliminate confounding somatosensory inputs. Regaining normative mobility of the cervical spine is imperative to allow for the full range of motion of the head and eyes for the vision-based exercises. Vision-based exercises for VOR recovery usually requires 4 weeks duration46 and requires daily compliance and exercise adherence. Current research efforts toward improved compliance utilizing smartphone technologies and playing video games has shown positive effects. Posture for performing exercises may be progressed from lying to sitting, to standing, to walking, or moving—as tolerated. Frequency and velocity of target acquisition is important, as the VOR is velocity specific. Likened to orthopedic active muscle rehabilitation techniques, velocity of exercises should be varied, and later in the rehabilitation process should be task-specific oriented. Use of timing devices (e.g., metronome) or more advanced computerized DVA and/or GST may be beneficial for measurement of thresholds tolerance.47,48 Advancement toward balance and proprioceptive exercises requires varied multisensory stimulation, including varied visual inputs limitations and challenging the base of support positions, along with varied surface textures. Progression from static positioning to movement-based exercise should be directed from small movements toward large-arc, segmented, body motions with functional application. Proprioceptive Neuromuscular Facilitation (PNF) exercises may be useful. Postural and balance exercise generally requires longer duration for full recovery, and may take up to 3 months, depending upon the availability of VOR stability and spatial orientation recovery.49 During the initial phase of recovery (24 48 hours post-injury), cognitive stress should be avoided, and normalization of the sleep cycle appears to be critical, as protracted recovery appears to result from failure to remove stressors and persistence of abnormal sleep IV. DIAGNOSIS AND TREATMENT
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cycles, though this may be age and gender specific. Further research is merited regarding removal of cognitive stressors with sleep pattern modulation, and progression to back to normal daily functions throughout the second and third phases of recovery. Initiation of an appropriate timeline and subsequent immersion into a vestibular and balance rehabilitation programs has shown positive benefits to cognition, even without being involved directly in a cognitive rehabilitative program.
SUMMARY/CONCLUSION Concussion/mTBI injury continues to gain public and medical professional awareness, as media coverage is heightened and increased medical research efforts give rise to empirical data to support novel objective measures and methods in combination with traditional symptom-based management. While imaging studies and blood/saliva biomarkers tests are emerging for detection, a hierarchal comprehensive assessment and rehabilitative team approach50 appears to have merit in symptom resolution and progression toward functionality.8 While efforts are made toward public education of recognition of signs and symptoms of mTBI, education of medical professionals appears merited for appropriate recognition and medical management. The astute medical and rehabilitative clinicians should be aware of the timeline of recovery at the time of assessment, the appropriate steps toward resolution for each of the three recovery stages, and the appropriate initiation and progression of objective testing and rehabilitative methods for each. Since dizziness is the most common symptom following mTBI, vestibular assessment and rehabilitative approaches have shown benefits for head and eye movement stabilization and recovery, and subsequent progressive balance and movement exercises restores static and dynamic balance, gait, and ADL functionality.51 Compliance and adherence to a prescribed recovery protocol remains a challenge, but new technologies are emerging to address it. This may allow the rehabilitation clinician to assess and monitor subjects remotely, and progress the rehabilitation program when direct access to a professional is limited. The sequelae of mistimed or inappropriate management appear to be a protracted recovery time, limited functionality, and symptoms persistence. Attention to sleep pattern normalization and cognitive recovery processes appear critical at the initial phase of recovery, as these appear to impact headache and accompanying symptoms’ persistence. Further research is merited in all aspects of medical/rehabilitative management, particularly the areas of sleep cycle and headache management, dosage and duration of rehabilitative exercise programs, objective measurement protocols to determine when thresholds of recovery steps are met, and thresholds of recovery for the safe return to participation in ADL activities (e.g., driving, sports, etc.). Longitudinal studies of cognition, repetitive trauma effects, and rehabilitative management protocols give the researcher/clinician ample opportunity to advance the science of this malady.
References 1. Gottshall K. Vestibular rehabilitation after mild traumatic brain injury with vestibular pathology. NeuroRehabilitation 2011;29(2):167 71. 2. Hillier SL, McDonnell M. Vestibular rehabilitation for unilateral peripheral vestibular dysfunction. Cochrane Database Syst Rev 2011;16:248 9
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3. Lei-Rivera L, et al. Special tools for the assessment of balance and dizziness in individuals with mild traumatic brain injury. NeuroRehabilitation 2013;32(3):463 72. 4. Ito M. Cerebellar long-term depression: characterization, signal transduction, and functional roles. Physiol Rev 2001;81:1144 95. 5. De Zeeuw CI, Hansel C, Bian F, Koekkoek SKE, van Alphen AM, Linden DJ, et al. Expression of a protein kinase C inhibitor in Purkinje cells blocks cerebellar LTD and adaptation of the vestibulo-ocular reflex. Neuron 1998;20:495 508. 6. Leitges M, Kovac J, Plomann M, Linden DJ. A unique PDZ ligand in PKCa confers induction of cerebellar long-term synaptic depression. Neuron 2004;44:585 94. 7. Linden DJ, Connor JA. Long-term synaptic depression. Annu Rev Neurosci 1995;18:319 57. 8. Balaban CD, et al. Top-down approach to vestibular compensation: translational lessons from vestibular rehabilitation. Brain Res 2012;1482:101 11. 9. Brooks MA, Peterson K, Biese K, Sanfilippo J, Heiderscheit BC, Bell DR. Concussion increases odds of sustaining a lower extremity musculoskeletal injury after return to play among collegiate athletes. Am J Sports Med 2016;44(3):742 7. 10. Herman DC, Jones D, Harrison A, Moser M, Tillman S, Farmer K, et al. Concussion may increase the risk of subsequent lower extremity musculoskeletal injury in collegiate athletes. Sports Med 2017;47(5):1003 10. 11. Fetter M. Acute unilateral loss of vestibular function. Handb Clin Neurol 2016;137:219 29. 12. Herdman SJ, Whitney SL. Interventions for the patient with vestibular hypofunction. In: Herdman SJ, editor. Vestibular rehabilitation. Philadelphia, PA: F.A. Davis; 2007. p. 309 37. 13. Imai T, et al. Classification, diagnostic criteria and management of benign paroxysmal positional vertigo. Auris Nasus Larynx 2017;44(1):1 6. 14. Zhang, Y.X., et al. Comparison of three types of self-treatments for posterior canal benign paroxysmal positional vertigo: modified Epley maneuver, Zhonghua Er Bi Yan Hou Tou Jing Wai Ke Za Zhi 2012;47(10):799 803. 15. Beynon GJ. A review of management of benign paroxysmal positional vertigo by exercise therapy and by repositioning manoeuvres. Br J Audiol 1997;31(1):11 26. 16. Semont maneuver and Brandt-Daroff maneuver. Zhonghua Er Bi Yan Hou Tou Jing Wai Ke Za Zhi 2012;47 (10):799 803. 17. Helminski JO, et al. Strategies to prevent recurrence of benign paroxysmal positional vertigo. Arch Otolaryngol Head Neck Surg 2005;131(4):344 8. 18. Helminski JO, et al. Daily exercise does not prevent recurrence of benign paroxysmal positional vertigo. Otol Neurotol 2008;29(7):976 81. 19. Magnus, R. Body posture 5 Korperstellung: experimental-physiological investigations of the reflexes involved in body posture, their cooperation and disturbances; based on a translation by William R. Rosanoff, and on a translation by Franklin Book Programs, Inc., Cairo, for the National Library of Medicine, Amerind, Springfield, VA, USA; 1924 (reprint 1980). 20. Whitney SL, Sparto PJ. Principles of vestibular physical therapy rehabilitation. Neuro Rehabil 2011;29:157 66. 21. Stanek JM, et al. Active duty firefighters can improve Functional Movement Screen (FMS) scores following an 8-week individualized client workout program. Work 2017;56(2):213 20. 22. Pavlou M. The use of optokinetic stimulation in vestibular rehabilitation. J Neurol Phys Ther 2010;34(2):105 10. 23. Cohen HS, et al. Utility of quick oculomotor tests for screening the vestibular system in the subacute and chronic populations. Acta Otolaryngol 2017;138(4):1 5. 24. Tamas TL, et al. Emergency diagnosis of the acute vestibular syndrome. Orv Hetil 2017;158(51):2029 40. 25. Lance S, Mossman SS. Misleading signs in acute vertigo. Pract Neurol. 2017;18(2):162 5 26. van de Berg R, et al. Laboratory examinations for the vestibular system. Curr Opin Neurol 2018;31(1):111 16. 27. Strupp M, et al. The takeaway Frenzel goggles: a Fresnel-based device. Neurology 2014;83(14):1241 5. 28. An SY, et al. Clinical roles of fixation suppression failure in dizzy patients in the ENT clinic. Acta Otolaryngol 2014;134(11):1134 9. 29. Slattery EL, et al. Vestibular tests for rehabilitation: applications and interpretation. NeuroRehabilitation 2011;29 (2):143 51. 30. Collins JJ, De Luca CJ. The effects of visual input on open-loop and closed-loop postural control mechanisms. Exp Brain Res 1995;103:151 63.
IV. DIAGNOSIS AND TREATMENT
REFERENCES
415
31. Lacour M, Barthelemy J, Borel L, Magnan J, Xerri C, Chays A, et al. Sensory strategies in human postural control before and after unilateral vestibular neurotomy. Exp Brain Res 1997;115:300 10. 32. Morimoto H, Asai Y, Johnson EG, Lohman EB, Khoo K, Mizutani Y, et al. Effect of oculo-motor and gaze stability exercises on postural stability and dynamic visual acuity in healthy young adults. Gait Post 2011;33:600 3. 33. Hazlett RL, Tusa RJ, Waranch HR. Development of an inventory for dizziness and related factors. J Behav Med 1996;19:73 85. 34. Jacobson GP, Newman WW. The development of the dizziness handicap inventory. Arch Otolaryngol Head Neck Surg 1990;116:424 7. 35. Morris AE, Lutman ME, Yardley L. Measuring outcome from vestibular rehabilitation, part I: quantitative development of a new self-report measure. Int J Audiol 2008;47:169 77. 36. Morris AE, Lutman ME, Yardley L. Measuring outcome from vestibular rehabilitation, part II: refinement and validation of a new self-report measure. Int J Audiol 2009;48:24 37. 37. Yardley L, Masson E, Verschuur C, Haacke N, Luxon L. Symptoms, anxiety and handicap in dizziness patients: development of the Vertigo Symptom Scale. J Psychosom Res 1992;36:731 41. 38. Nelson LD, et al. Rates and predictors of invalid baseline test performance in high school and collegiate athletes for 3 computerized neurocognitive tests: ANAM, Axon Sports, and ImPACT. Am J Sports Med 2015;43 (8):2018 26. 39. Leyva A, Balachandran A, Britton JC, Eltoukhy M, Kuenze C, Myers ND, et al. The development and examination of a new walking executive function test for people over 50 years of age. Physiol Behav 2017;171:100 9. 40. Perrochon A, Kemoun G, Watelain E, Dugue B, Berthoz A. The “Stroop Walking Task”: an innovative dual-task for the early detection of executive function impairment. Neurophysiol Clin 2015;45(3):181 90. 41. Bergeron M, Lortie CL, Guitton MJ. Use of virtual reality tools for vestibular disorders rehabilitation: a comprehensive analysis. Adv Med 2015;2015:916735. 42. Chang YJ, Kang YS, Huang PC. An augmented reality (AR)-based vocational task prompting system for people with cognitive impairments. Res Dev Disabil 2013;34(10):3049 56. 43. Biffi E, Beretta E, Diella E, Panzeri D, Maghini C, Turconi AC, et al. Gait rehabilitation with a high tech platform based on virtual reality conveys improvements in walking ability of children suffering from acquired brain injury. Conf Proc IEEE Eng Med Biol Soc 2015;2015:7406 9. 44. Khademi M, Hondori HM, Dodakian L, Cramer S, Lopes CV. Comparing “pick and place” task in spatial Augmented Reality versus non-immersive Virtual Reality for rehabilitation setting. Conf Proc IEEE Eng Med Biol Soc 2013;2013:4613 16. 45. Peterka RJ, Statler KD, Wrisley DM, Horak FB. Postural compensation for unilateral vestibular loss. Front Neurol 2011;57:1 13; 2011;2:Article. 46. Herdman SJ, Schubert MC, Das VE, Tusa RJ. Recovery of dynamic visual acuity in unilateral vestibular hypofunction. Arch Otolaryngol Head Neck Surg 2003;129:819 24. 47. Gottshall KR, Hoffer ME. Tracking recovery of vestibular function in Individuals With blast-induced head trauma using vestibular—visual-cognitive interaction tests. J Neurol Phys Ther 2010;34:94 7. 48. Gottshall K, et al. Objective vestibular tests as outcome measures in head injury patients. Laryngoscope 2003;113(10):1746 50. 49. Borel L, Harlay F, Magnan J, Chays A, Lacour M. Deficits and recovery of head and trunk orientation and stabilization after unilateral vestibular loss. Brain 2002;125:880 94. 50. Gottshall KR, Sessoms PH. Improvements in dizziness and imbalance results from using a multi-disciplinary and multi-sensory approach to Vestibular Physical Therapy—a case study. Front Syst Neurosci 2015;9:106. 51. Alsalaheen BA, et al. Exercise prescription patterns in patients treated with vestibular rehabilitation after concussion. Physiother Res Int 2013;18(2):100 8.
IV. DIAGNOSIS AND TREATMENT