Vestibular Rehabilitation in Mild Traumatic Brain Injury/Concussion Management
Eagle-Vail skier Mikaela Shiffrin hurtled down the Aspen slalom course reaching speeds of 40-75mph, head vertical, timing perfect, edging out her competitors by fractions of a second. Colorado Rockies first baseman Mark Reynolds hit a two-run homer off Milwaukee Brewers pitcher Guerra’s split finger sinker early in the 2017 season. Carol B., an arborist, ducked out of the way as a large limb she had just trimmed from a 30ft ash tree fell to the ground. What did these three have in common? Each used their vestibular system to integrate visual motion, proprioception, and touch with vestibular cues to predict self and object trajectories to point of collision. Sensory inputs about gravity vertical, acceleration, angular velocity, and stored memory of gravitational effects allowed them to accurately and successfully compute and execute actions to achieve their desired goals: World Cup, home run, and safety.
The worldwide occurrence of mild traumatic brain injury (mTBI) is estimated as high as 600 per 100,000 people annually, across all populations [children, adolescents, adults, athletes, military, civilian] (Faul M 2010, Taylor CA 2015). Sports concussion incidences in the United States alone are estimated at 3.8 million per year (Harmon KG 2013), and mTBI is considered the signature injury of combat in Iraq and Afghanistan (VA/Dod 2016). 10-15{f8270180bd013a86e8a7bdc2029d331e433a151f411edd98c48642ec5f8162bf} do not recover spontaneously, developing post concussive disorders (Terrio H 2009, Pan T 2015).
Vestibular injury or disruption from mTBI may lead to progressively developing errors in perception, navigation, balance, vision and coordination, and contributes to all symptom domains described by the CDC [physical, emotional, cognitive, energy/sleep] (Kisilevski V 2001, Gurley JM 2013). Impairments are measurable immediately after concussion, and may persist for months or years. Aggregate losses cannot be accurately calculated but are estimated in the billions of dollars (CDC 2003, Langlois JA 2006). Individual stories describe significant dysfunction and disability due to persistent symptoms, ranging from heightened internal anxiety (Saman Y 2012) to job loss and social/emotional disruption.
Dizziness and imbalance are common immediate symptoms after concussion. Dizziness after brain injury is the most predictive symptom of a protracted recovery (Chamelian L 2004, Lau BC 2011). As an umbrella word describing sensory conflict, dizziness encompasses a long list of symptoms including vertigo (spinning or rocking sensation), light-headedness, floating, disorientation, disequilibrium, wooziness, fogginess, and unstable vision (Hoffer ME 2004, Miranda N 2015). While active duty military members and athletes from high school to professional levels might have the support of a formal concussion screening protocol (Kelly JC 2012, McCrory P 2013), much of the remaining brain injured population may not be asked directly about symptoms of dizziness. Symptom screening tools do not elaborate on subcategories of ‘dizziness’. Concussed individuals may minimize symptom reports for a variety of reasons, may not describe abnormal sensations as dizziness, and brain injury impairs accurate self-assessment (McCrea M 2004). Careful questioning is required to draw out symptom details of this invisible injury. The symptoms of dizziness do not identify a structure, but rather an impaired sensory process.
Sensory conflict is the miss-match of two or more sensory inputs to each other and to predictions based on memory of prior experience. That includes memory of the environment, the action, consequence, and effects of Earth’s gravity (Laquaniti F 2013, Asslander L 2016). Motion sickness is a common example of sensory conflict. Resolving conflict among sensory systems in healthy individuals requires the ability to shift or weight the use of one system over another, matching environmental demands while maintaining or recovering a normal sense of equilibrium (Peterka 2002). Amusement park rides capitalize on altering the environment visually as well as by defying gravity, producing temporary disorientation. Walking in the dark denies adequate visual information, requiring a shift to vestibular and somatosensory cues. Walking over uneven ground reduces reliable somatosensory information. Traveling in the dark over uneven ground in an unfamiliar environment can be quite disorienting if vestibular references are inaccurate or inefficient. Responses to unresolved sensory conflict vary from mild discomfort to autonomic “fight flight or freeze” reactions, nausea, misbehavior, and exhaustion (Lee H 2014).
Maladapted responses to chronically damaged, inefficient or missing vestibular inputs may present in numerous ways. Examples include avoiding crowds, restricted driving, muscle guarding or clenching to stabilize the head and body, or eyestrain from visual dependence for balance in absence of integrated multimodal sensory inputs. Timing and spatial perceptual errors will become more obvious as activities increase in speed and complexity, because visual and somatosensory neural transmissions are slower than vestibular conduction speeds, making compensation less efficient (Morris L 2014).
Whether acute or chronic, the effort to resolve the sensory conflict of dizziness causes brain fatigue and general exhaustion. The resulting delayed recovery contributes to further perceptual and cognitive errors (Franke LM 2012, Howell DR 2015).
The vestibular system is particularly vulnerable to concussive head forces because of its vast representative network at every level of the brain, and its sensory organs of the inner ears housed within the bony labyrinths of the temporal bones. The vestibular sensory system processes head station, acceleration and angular velocity data from the inner ears, integrates body motion, visual motion, eye response to head motion, and perception of Earth’s gravity. Thus it contributes the perception of weight and three-dimensional context to visual and somatosensory cues about self and the environment (Laquaniti F 2013). Navigation, gaze stability, balance, coordination, postural stability, control of heart rate and blood pressure, memory and emotional control all depend to some degree on vestibular function (Brandt T 2005, Kristjansson E 2009, Franke LM 2012, Morris L 2014).
The central vestibular system is the primary integrator of multisensory data from sensorimotor and behavioral areas (Bronstein 2016). Concussion’s neural injury and metabolic pathology disturb sensory integration at cortical and subcortical levels (Gattu R 2016). Disruption may involve the vestibular-ocular system, the vestibular-somatosensory systems (notably confounded by abnormal input and response from the cervical spine), vestibular-autonomic connections, vestibular cortex, or any combination (Furman JM 2000, Morris L 2014, Arshad Q 2017).
Diffusion Tensor magnetic resonance tractography (DTI) identifies the vestibular network as a rope ladder shape crossing the midline at every level from brainstem to cortex, including through the corpus callosum (Kirsch V 2016). Vestibular pathways are also two-way information tracts direct to the cerebellum, medulla and spinal cord, instigating and modulating neck, trunk and limb responses to head position and motion through the vestibulo-spinal system (Pan T 2015). This area is vulnerable to traction, torsion and compression during whiplash injuries to the cervical spine (Kristjansson E 2009).
Symptoms of vestibular disruption often begin with dizziness. The inability to sort sensory input caused by neural disruption at sub cortical levels pushes processing to a cortical level, creating a significantly increased metabolic demand and contributing to pervasive brain fatigue. Increased metabolic demand co-occurring with reduced blood perfusion initially creates vulnerability to a second injury from impact or exertion (Franke LM 2012). When further insult is experienced the neural crisis is extended (Vagnozzi R 2010)
The peripheral vestibular organs can be damaged by concussive forces to the ear injuring membranes and hair cells, creating inflammation resulting in endolymphatic hydrops, labyrinthitis, perforation (fistula) or by dislodging calcite crystals from the utricle of the otolith (Morris L 2014). Loose calcite crystals may float into a semicircular canal, causing abnormal fluid turbulence during head motion. The distorted perception of motion is Benign Paroxysmal Positional Vertigo (BPPV), and can be quite frightening. Nearly 30{f8270180bd013a86e8a7bdc2029d331e433a151f411edd98c48642ec5f8162bf} of post concussive dizziness is attributed to BPPV (Hoffer ME 2004). Initial brief episodes of dizziness and imbalance may devolve into lasting vague discomfort and other impairments if not treated. New symptoms will develop from the brain’s attempt to adapt and compensate for abnormal sensory spatial and motion information.
Visual disruption after mTBI is more often a problem with the oculomotor system and/or visual processing than visual acuity (Heitger MH 2009). Direct vestibular connections to the oculomotor nuclei create the fastest central reflex in humans, the vestibulo-ocular reflex (VOR). By calibrating eye motion precisely to head motion and direction, an image is maintained on the retina for clear vision despite head motion. Together with the cervico-ocular reflex and the optokinetic reflex, the VOR is an important component of gaze stabilization. Interference in accurate and precise perception of head position may disrupt the VOR resulting in blurred vision and uncoordinated voluntary eye motions of smooth pursuits, vergence and saccades (Bronstein 2016). Clients’/patients’ whose VOR is impaired find it difficult to read using print, or see objects in the environment as stable when turning, walking or running.
Ocular reflexes generated from the vestibular system also support stable vision when the environment is moving. When disrupted, symptoms include headache, eyestrain and fatigue, inability to tolerate scrolling print on a computer monitor, and nausea from the sensory conflict between visual perception and perceived head position and motion. Impairments in eye control worsen as speed increases, and with fatigue during sustained activity such as is required to attend school or work (Gottshall KR 2010, Murray NG 2014).
Accurate visual processing depends on intact vestibular information. Astronauts on the International Space Station maintain semicircular canal function, but lose otolith function in a 0g environment. In experiments they made timing errors when reaching for a vertically propelled ball (constant speed in absence of gravity acceleration). Errors persisted longer than 14 days, suggesting difficulty in learning to override ingrained prior memory of Earth’s gravitational effects (Laquaniti F 2013). When sensory integration is damaged, visual processing deficits have been identified long after a concussive event (Brosseau-Lachaine O 2008, Heitger MH 2009).
Visual processing alone is also not sufficient to determine self verses environmental motion. In the absence of accurate or adequate vestibular function, and in concert with oculomotor deficiencies, over-reliance on vision may develop into visual motion hypersensitivity (VMH), or visual vertigo (Winkler PA 2009, Pavlou 2010) Individuals with VMH may not be able to differentiate self motion from environmental motion, may see stationary objects as moving, have difficulty reading, and report dizziness. They are likely to self-limit exposure to aggravating stimuli (busy environments, travel, crowds), affecting their lives, fitness, psychological health, and relationships.
Balance is a complex expression of motor control, timing, reflexes, predictions, learned patterns, intent and constant updating and grading of information in response to sensory inputs, to arrange the body relative to gravity to achieve a desired task. The central vestibular system dictates eye, neck, trunk and extremity responses based on head position with movement input from the peripheral vestibular organs of the inner ears and proprioception from the high cervical spine (Kristjansson E 2009, Horak 2010, Bronstein 2016). Balance and equilibrium impairments are measurable immediately after concussion. Unaddressed balance impairments may persist and even worsen over time (Franke LM 2012, Murray NG 2014, Pan T 2015). When vestibular function is inadequate, inaccurate or absent, reliance on remaining sensory systems will increase. Returning to activity after mTBI, no matter how graded, without addressing vestibular impairment invites development of less efficient movement.
Individuals with post concussion syndrome or post concussion disorders represent a significant number of people in light of the total number of mTBI’s per year. There is not yet a reliable treatment intervention to stop or change the acute cascade of disruptive neural processes after mTBI. Current management guidelines recommend initial rest from all activity, then graded return to activity while monitoring symptoms during the natural course of healing (McCrory P 2013). However, symptoms are not reliable indicators of resolution stage of the neurophysiologic, hemodynamic, metabolic and micro-structural disruptions from mild traumatic brain injury. Multiple studies have demonstrated neural substrate abnormalities resolving from 30 days to four months in asymptomatic athletes (Signoretti S 2011, Yeo RA 2011).
When resolution of a concussion lasts longer than a week, disruptions at school and work can become onerous, or even insurmountable. Over time, the cost of post concussion disorders may be measured in lost opportunities, lost income, medical expense, behavioral changes, social-relational and emotional disturbances, and physiologic energy depletion. These effects are not limited to the concussed individual, but may extend to family members, caregivers, workplaces, teachers and school administrators, and social networks.
Evaluation for Functional Deficits
As part of a multidisciplinary team, Physical Therapists with highly specialized training and a neurological rehabilitation background provide vestibular rehabilitation (VR). A complex evaluation is required to identify a patient’s functional deficits (Alsalaheen BA 2013). Tools such as the Balance Error Scoring System (BESS), commonly used as part of concussion screening for athletes and military personnel, are not specific enough to inform treatment direction. A series of validated testing tools are combined to best identify specific deficits in gravity perception, postural stability, gait, oculomotor function, tolerance to exercise exertion, and sensory weighting from one system to another (Scherer MR 2009, Alsalaheen BA 2013, Morris L 2014). Underlying dysfunctions, timing, balance, and cognitive errors, may be revealed under increasingly stressful or demanding test conditions. Performance during dual-task activities, requiring a higher level of cognitive and sensorimotor processing, is significantly impaired in concussed athletes and worsens after return to activity (Roberts JC 2011).
Treatment begins with extensive education for patients and their relevant intimates. The first functional task in mTBI recovery treatment is to match sensory inputs, ideally beginning as soon as dizziness is reported. Specialized activities are designed and prescribed specifically to address an individual’s identified needs. Feedback from appropriate sensory systems, error signals, task specificity and proper dosing of challenges are required to encourage healthy neurobehavioral adaptation and reorganization. Co-existing impairments must be identified as they complicate and lengthen the rehabilitation process (Hoffer ME 2004, Shumway-Cook 2007, Scherer MR 2009, Alsalaheen BA 2010, Morris L 2014).
Benefits of VR include recalibration of sensory systems, improved postural stability and gait, improved oculomotor function and gaze stability, and reduced symptoms of dizziness. More than 85{f8270180bd013a86e8a7bdc2029d331e433a151f411edd98c48642ec5f8162bf} of dizzy patients improve with such specialized care. Studies demonstrating improvements have looked at patients with vestibular disease, BPPV both traumatic and idiopathic, mTBI, migraine, imbalance, and visual motion hypersensitivity. Success has been documented no matter how long after injury the person enters care (Hoffer ME 2004, Gottshall KR 2010, Alsalaheen BA 2013, Broglio SP 2015, Gottshall KR 2015, Whitney SL 2016).
Reducing brain energy demands by reducing dizziness early paves the way for quicker and more robust recovery from mTBI. BPPV is a mechanical problem and should be treated and resolved immediately. Stroke research has demonstrated positive structural changes in neural axons when task specific training is introduced between day 1 and 3 after onset (Lee KH 2013). In the Statements of Agreement from the Targeted Evaluation and Active Management Approaches to Treating Concussion Meeting (Collins MW 2016), 38 specialists in the care of mTBI concluded that intervention on the first day was indicated and would produce more desirable and expedient outcomes.
In their essays for The Players Tribune, Bryce Sandoval (‘Til It’s Gone, September 5, 2015) and Gabriel Landeskog (We Need to Talk About Concussions, Right Now, August 2, 2016) vividly recounted their experiences of concussions after being hit in the face with flying pucks. As a defenseman for the New Jersey Devils, Sandoval developed gradually worsening physical, perceptual and emotional dysfunction over two seasons. Night driving made him feeling as though he was floating. He misjudged puck location and trajectory and felt nauseous when turning repeatedly. Although he sought help from numerous specialists, he did not fully recover until experts in neurology and physical therapy experienced with the multisensory complications of concussion designed a novel rehabilitation program to recalibrate his vestibular, visual and somatosensory subsystems. Landeskog, as a forward and newly anointed captain for the Colorado Avalanche, pushed himself to return to play immediately, under-reporting his symptoms out of loyalty and commitment to his teammates. He developed severe light sensitivity and migraines. Fortunately he had immediate access to highly skilled care, and was force-marched through the rest and rehabilitation required to recover 100{f8270180bd013a86e8a7bdc2029d331e433a151f411edd98c48642ec5f8162bf}. But he made note of the lack of such care for non-professionals and children, highlighting the need to improve all aspects of concussion recognition and management for everyone, immediately.
Vestibular disruption following mild traumatic brain injury underlies many symptoms and impairments. The Department of Defense (VA/Dod 2016), Colorado Department of Labor and Employment (Worker’s Compensation 2012), and the Colorado Department of Education (McAvoy K 2014) have published treatment guidelines for TBI that include vestibular rehabilitation. Colorado Senate Bill 11-040, The Jake Snakenberg Youth Concussion Act (2012), establishes Required Head Trauma Guidelines as well. All 50 states have such laws. Still, too many clients/patients are not being referred for vestibular rehabilitation until months or years post injury, if at all.
One reason for delayed care could be that often our clients/patients with mild traumatic brain injuries do not specifically report dizziness unless or until asked. It is important to ask the right questions when taking the patient’s/client’s history. As described above, when the brain can’t use vestibular references efficiently the result is over-use of the eyes to orient the individual to the world and overuse of the body to orient the individual to the ground, with slowed reactions and perceptual errors. Inefficient integration of sensory inputs results in a cascade of problems when the visual system is taxed with visually busy activities such as driving, scanning to read, computer work, or being in a crowded or visually stimulating environment. Such activities become overwhelming and exhausting for the brain injured individual. The goal of vestibular therapy is to help our patients/clients use the three balance systems – vestibular, ocular and somatosensory -efficiently and make these systems relay matched information in the brain to avoid maladaptation and promote recovery.
A practitioner’s records in the medical-legal brain injury case are legal documents that will be used as evidence at the time of trial. Injury causation in these cases is typically a hotly contested issue. When injured patients/clients are not timely diagnosed with vestibular injury, this makes proving legal causation more difficult. However, medical records that clearly document a patient’s/client’s symptoms of vestibular injury go a long way toward demonstrating to the jury that the injury, in fact, existed all along. Yet many providers do not do much to detail patients’ symptoms in their records. For example, the traditional format of the SOAP notes means that the information in them is extremely limited. Yet every practitioner and their staff can observe and therefore document vestibular symptoms such as a patient’s difficulty reading and completing the patient intake form, a patient needing to wear sunglasses in their office, a patient describing nausea in the grocery store or a visually busy environment, a patient’s extreme fatigue when driving, a patient feeling sick with manipulation or overly sensitive to touch, or a patient needing to lay down after physical therapy in order to be able to drive home. All these symptoms, even without a diagnosis, tell the story of vestibular injury.
Juries understand and relate to personal stories such as Bryce Sandoval’s very real struggles with basic activities like driving and judging where things are. When presenting on the topic of vestibular injury to a group of brain injury survivors at the Brain Injury Alliance of Colorado’s conference, we asked the audience, “How many of you experience the following symptoms: feeling like your body is not attached to you, feeling like your brain is not processing where you are in space, dizziness, imbalance, motion hypersensitivity, vertigo, nausea in busy environments, feeling visually dependent?” Every hand went up. We then asked, “Do you feel like these symptoms are overlooked?” Not only did all the survivors’ hands remain up (accompanied by visible nodding), one person in the audience started crying. We had no idea that this question was going to elicit such a visceral reaction. When you ask patients/clients the right questions, the story of vestibular injury after traumatic brain injury comes forth like a waterfall. But we must ask our patients and clients the questions.
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