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Vestibular dysfunction and concussion
Handbook of Clinical Neurology, Vol. 158 (3rd series) Sports Neurology B. Hainline and R.A. Stern, Editors https://doi.org/10.1016/B978-0-444-63954-7.00014-8 Copyright © 2018 Elsevier B.V. All rights reserved
Chapter 14
Vestibular dysfunction and concussion 1
ANNE MUCHA1*, SHERI FEDOR2, AND DANIELLE DEMARCO3 UPMC Center for Rehabilitation Services, Pittsburgh, PA, United States 2
Inova Physical Therapy Center, Fairfax, VA, United States
3
Baylor Institute for Rehabilitation, Frisco, TX, United States
Abstract The assessment and treatment of sport-related concussion (SRC) often requires a multifaceted approach. Vestibular dysfunction represents an important profile of symptoms and pathology following SRC, with high prevalence and association with prolonged recovery. Signs and symptoms of vestibular dysfunction may include dizziness, vertigo, disequilibrium, nausea, and visual impairment. Identifying the central and peripheral vestibular mechanisms responsible for pathology can aid in management of SRC. The most common vestibular disturbances after SRC include benign paroxysmal positional vertigo, vestibulo-ocular reflex impairment, visual motion sensitivity, and balance impairment. A variety of evidence-based screening and assessment tools can help to identify the various types of vestibular pathology in SRC. When vestibular dysfunction is identified, there is emerging support for applying targeted vestibular rehabilitation to manage this condition.
INTRODUCTION Vestibular dysfunction is prevalent following sport-related concussion (SRC); 50–84% of athletes report dizziness following an SRC (Lau et al., 2011; Kontos et al., 2012; Merritt et al., 2015). Importantly, when signs and symptoms associated with vestibular dysfunction are present after SRC, they appear to be associated with worse outcomes and prolonged recovery. A retrospective study examining a pediatric cohort (n ¼ 247) found that 81% exhibited vestibular abnormality (Corwin et al., 2015). On average, these patients required significantly more time to return to school (56 vs. 6 days) and to be fully cleared to return to sport (106 vs. 29 days) when compared with age-matched subjects without vestibular findings. Another retrospective study involving 101 pediatric patients following SRC found that acute postconcussion vestibulo-ocular dysfunction was associated with higher risk of developing postconcussion syndrome (adjusted
odds ratio of 4.10) (Ellis et al., 2015). The National Collegiate Athletic Association Injury Surveillance System examined 1647 cases of SRC and noted that symptom duration and return to competition were significantly increased when audiovestibular symptoms of dizziness, imbalance, and noise sensitivity were present (Chorney et al., 2017). Despite the negative relationship of vestibular dysfunction to recovery, there is evidence that these effects can be modified with vestibular rehabilitation (Alsalaheen et al., 2010; Schneider et al., 2014; Broglio et al., 2015). Therefore, clinicians should be mindful of possible vestibular dysfunction when managing athletes with SRC. This chapter will provide a discussion of common vestibular dysfunction presentation and etiology following SRC. Assessment tools and intervention strategies to mitigate vestibular dysfunction will be explored.
*Correspondence to: Anne Mucha, DPT, UPMC Centers for Rehab Services, 3200 South Water St. Pittsburgh PA 15203, United States. Tel: +1-412-432-3700, Email: [email protected]
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REVIEW OF VESTIBULAR SYSTEM STRUCTURE AND FUNCTION The vestibular system is a complex sensorimotor system responsible for detection of motion and position of the head and body, motor responses, multisensory integration, and higher-level cognitive-perceptual functions (Hain, 2011; Brandt and Dieterich, 2017). The structure and function of the vestibular system are organized into peripheral and central elements. Disorders of the peripheral vestibular system involve: the vestibular nerve; the semicircular canals (SCCs), which sense angular acceleration; and the otolith organs (utricle and saccule), which detect linear acceleration and head tilt. In contrast, central vestibular disorders involve the vestibular nuclei, flocculus, and vermis of the cerebellum, midbrain, thalamus, parietoinsular vestibular cortex, visual cortex or projections between these regions (Brandt and Dieterich, 2017). Signs and symptoms such as dizziness, vertigo, nausea, postural instability, visual distortion, and altered spatial orientation are most commonly associated with vestibular pathology (Herdman and Clendaniel, 2014). Due to the highly integrative nature of the vestibular system with other sensory systems, these signs and symptoms can be significantly affected by the presence or absence of visual, somatosensory, or auditory stimuli (Keshner et al., 2004).
ETIOLOGY OF VESTIBULAR IMPAIRMENT AFTER SPORTS-RELATED CONCUSSION There are a multitude of vestibular disorders that occur due to pathology in the peripheral, central, or combined peripheral/central vestibular structures. Because etiology of impairment may inform intervention, establishing causality is important for clinical management. Currently, the literature is limited regarding the etiology of vestibular dysfunction specific to SRC. Therefore, we will use the best current evidence to discuss vestibular impairment in the context of SRC when research is lacking.
Peripheral mechanisms A direct or indirect force to the head has potential to damage the intralabyrinthine structures or the vestibular nerve. Such trauma-induced peripheral vestibular pathology, when accompanied by high-frequency hearing loss, is termed labyrinthine concussion (Choi et al., 2013). Although a peripheral vestibular etiology of dizziness accounts for approximately 45% of vestibular dysfunction in the general population (Brandt and Dieterich, 2017), prevalence of peripheral vestibular dysfunction following SRC is much lower (Zhou and Brodsky, 2015).
BENIGN PAROXYSMAL POSITIONAL VERTIGO (BPPV) BPPV is a disorder of the peripheral vestibular system that may result from head trauma (Pisani et al., 2015). BPPV results from small calcium carbonate crystals (otoconia) being dislodged in the utricle; these crystals then relocate to one or more of the adjacent SCCs. The weight of the otoconia then interferes with normal fluid dynamics within the canals, resulting in episodic vertigo. BPPV is characterized by spells of vertigo with changes in head position such as looking up, rolling in bed, lying down on a flat surface, or bending over (Fife et al., 2008). The diagnosis of BPPV is confirmed if characteristic nystagmus and vertigo manifest with either the Dix–Hallpike or supine roll test on clinical exam (Bhattacharyya et al., 2017). BPPV is the most common peripheral vestibular disorder in adults, with a lifetime prevalence of 2.4% (von Brevern et al., 2007). However, in younger patients, incidence is much lower (Bhattacharyya et al., 2017). In a large multicenter study, Lee et al. (2017) reported that BPPV was diagnosed in only 5.1% (21/411) of children and adolescents evaluated for dizziness (21/411). In studies describing BPPV rates related to traumatic brain injury (TBI), incidence was 15% in a cohort including patients with severe, moderate, and mild TBI (mTBI) and mean age of 39.9 years (Davies and Luxon, 1995). In contrast, BPPV was diagnosed in just 4.3% of cases referred for vestibular physical therapy following concussion from any cause (Alsalaheen et al., 2010), and was not identified in any cases of pediatric SRC (n ¼ 42) referred for assessment of posttraumatic dizziness (Zhou and Brodsky, 2015). Given that youth patients comprise 90.18% of all SRC diagnoses (Amoo-Achampong et al., 2017), it is likely that a combination of age and injury severity contributes to the low rate of BPPV occurrence following SRC.
SEMICIRCULAR CANAL PATHOLOGY The three orthogonally oriented SCCs in each labyrinth are the peripheral vestibular structures responsible for sensing angular acceleration. The gold-standard method for assessing function of the SCCs is the bithermal caloric test. With caloric testing, a temperature gradient is introduced which induces endolymphatic flow, stimulating the horizontal SCC primary afferents and activating the vestibulo-ocular reflex (VOR) pathway (Shepard and Jacobson, 2016). The Head Impulse Test (HIT) is an alternate, more portable method to assess SCC function through the VOR response (MacDougall et al., 2009). While the caloric test assesses low-frequency components of the VOR, the HIT assesses high-frequency components (greater than 1 Hz). Most studies examining peripheral vestibular function via caloric testing are
VESTIBULAR DYSFUNCTION AND CONCUSSION limited by mixed severity of TBI and inconsistent test interpretation criteria (Davies and Luxon, 1995). However, when examining mTBI only, abnormal caloric testing has been reported in varying degrees ranging from 3 to 21% (Tuohimaa, 1978; Zhou and Brodsky, 2015). Alshehri et al. (2016) identified no cases of abnormal horizontal SCC function by video HIT study of 56 subjects with posttraumatic dizziness.
OTOLITH DYSFUNCTION The otolith organs (utricle and saccule) sense linear head acceleration and head tilt, with the utricle detecting horizontal movements and the saccule sensing vertical motion. The otoliths provide primary input for vestibulospinal reflex output and supplementary information along with SCCs for the VOR (Carpenter et al., 1999). BPPV is a type of otolith dysfunction, as its mechanism is displacement of otoconia from the utricle. However, other forms of vestibular otolith impairment may also present posttraumatically. The vestibular-evoked myogenic potential test (VEMP) assesses otolith function. Cervical VEMPs (cVEMPs) assess the saccular-collic pathway, which is a part of the vestibulospinal reflex network (Colebatch et al., 2016). cVEMP responses are recorded from the activated sternocleidomastoid muscle in response to sound or vibration. In contrast, ocular VEMPs (oVEMPs) record responses from the inferior oblique eye muscles in response to sound or vibration, assessing the utricular-otolith pathway contribution to the VOR response (Colebatch et al., 2016). The subjective visual vertical (SVV) test also assesses otolith (primarily utricle) function. SVV requires the subject to adjust the position of a presented line to vertical orientation (parallel to gravity) in the absence of other sensory cues. The difference between perceived versus actual vertical is normally within 2° but has been shown to be significantly impaired in central and peripheral lesions involving utriculo-ocular pathways (Kingma, 2006). Studies examining otolith function via VEMPs or SVV are limited in mTBI and SRC. Otolith dysfunction rates following blast-related TBI range from 29% (Scherer et al., 2011) to 52% (Akin et al., 2017). In blunt-force TBI and associated vertigo, Ernst and colleagues (2005) reported abnormal VEMPs in 25% of 63 cases. Lee et al. (2011) reported abnormal cVEMPs in 32% of 28 patients followed prospectively after head trauma. Finally, Zhou and Brodsky (2015) studied children and adolescents who had undergone vestibular testing for evaluation of dizziness and/or balance impairment following an SRC; abnormal otolith function was identified in 18% (7/38) based on cVEMP findings and 13% (5/38) based on SVV findings.
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PERILYMPHATIC FISTULA (PLF) Some authors have proposed PLF as a cause of dizziness following concussion (Ernst et al., 2005; Fife and Giza, 2013). Traumatic forces may cause membrane rupture at the oval or round window, resulting in a PLF and fluid leakage into the middle ear. Direct trauma from temporal bone fracture and barotrauma are the most common mechanisms for PLF (Maitland, 2001). PLF typically causes fluid or blood discharge from the involved ear, unilateral auditory disturbance, tinnitus, vertigo, or imbalance. Temporal bone fracture is typically associated with moderate or severe head TBI (Naguib et al., 2012). While forces associated with moderate or severe TBI may cause PLF, there is limited evidence of PLF following mTBI (Davies and Luxon, 1995).
POSTTRAUMATIC ENDOLYMPHATIC HYDROPS Endolymphatic hydrops is a disorder of the peripheral vestibular system in which endolymphatic fluid balance in the labyrinth becomes dysregulated, leading to distension of the endolymphatic space (hydrops). Symptoms are episodic but are often quite severe and include vertigo, nausea/vomiting, auditory changes, auditory pressure/fullness, and imbalance. Idiopathic endolymphatic hydrops is synonymous with Menière’s disease. One study (Ernst et al., 2005) identified delayed endolymphatic hydrops in 19% (12 of 63) of patients following head trauma of undetermined severity. However, these findings should be considered with caution, as electrocochleography was used to confirm the presence of hydrops. The clinical utility of electrocochleography for the diagnostic evaluation of Menière’s disease is controversial (Lopez-Escamez et al., 2015; Ciorba et al., 2017) and is not validated by the Bárány Society criteria for diagnosis of Menière’s disease (Orchik et al., 1993; Ziylan et al., 2016).
Central mechanisms A direct or indirect force to the head has potential to disrupt the structure and function of central vestibular structures. The frequent coexistence of central oculomotor dysfunction with posttraumatic vestibular dysfunction suggests centrally mediated vestibular impairment (Pearce et al., 2015; Zhou and Brodsky, 2015; DuPrey et al, 2017; Howell et al, 2018). Further, vestibulospinal reflex impairment is unrelated to VOR impairment (Mucha et al., 2014; McDevitt et al., 2016; Wright et al., 2017); while these vestibular functions utilize the same peripheral structures, distinct central nervous system pathways are employed, further illustrating the likelihood of central vestibular mechanisms in SRC.
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WHITE-MATTER ABNORMALITIES The neurometabolic changes associated with concussion are triggered by acceleration and deceleration forces and associated traumatic stretching of neuronal axons (Barkhoudarian et al., 2016). Although standard imaging (magnetic resonance and computed tomography) rarely identifies findings associated with SRC (Useche and Bermudez, 2018), diffusion tensor imaging may reveal central microstructural axonal injury via fractional anisotropy. White-matter abnormalities are identified following blast-related concussion with loss of consciousness (Hayes et al., 2015) and following SRC (Cubon et al., 2011; Borich et al., 2013; Virji-Babul et al., 2013). Alhilali et al. (2014) examined diffusion tensor imaging findings specific to vestibular impairment. When comparing 30 patients with vestibular symptoms to 39 patients without vestibular symptoms, concussed patients with vestibular symptoms were more likely to manifest with decreased fractional anisotropy in the cerebellum and fusiform gyri (p < 0.05) (Alhilali et al., 2014).
MIGRAINE Migraine is the most common cause of posttraumatic headache. In a prospective study of 212 emergency department patients with headache following concussion, 49% were classified with migraine or probable migraine (Headache Classification Committee of the International Headache Society (IHS), 2013; Lucas et al., 2014). Following SRC, migraine was positively identified in more than 40% of athletes (Kontos et al., 2013; Sufrinko et al., 2018). Vestibular migraine (VM) is a common variant of migraine (Lempert et al., 2012). VM is a frequent cause of episodic dizziness, accounting for 7–11% of adult patients evaluated in specialized vestibular disorders clinics (Neuhauser et al., 2001; Brandt and Dieterich, 2017). VM is more prevalent in younger patients. In a large multicenter study of children and adolescents evaluated for dizziness, approximately 29% (120/411) were diagnosed with VM (Lee et al., 2017). In studies of military service members with dizziness following mTBI, three categories were identified: posttraumatic migraine-associated dizziness; spatial disorientation; and BPPV (Hoffer et al., 2004). In patients with mixed blast and blunt-force mTBI, 41–59% of diagnosed patients had posttraumatic migraine-associated dizziness (Hoffer et al., 2004; Gottshall, 2011). The pathophysiology of posttraumatic migraine is uncertain. In primary migraine, abnormal activation of trigeminovascular pain pathway occurs in genetically predisposed individuals (Akerman et al., 2017). Triggering
mechanisms linked to migraine headache include stress, loss of sleep, skipping meals, specific foods, alcohol, hormonal fluctuations, and certain types of light or noise (Pellegrino et al., 2017). Based on significantly higher rates of migraine following a concussion compared with the general population, posttraumatic migraine is not simply a manifestation of a pre-existing migraine diagnosis. Hypersensitivity to headache triggers is a speculated mechanism by which concussion allows for increased activation of the trigeminovascular pain pathways, leading to posttraumatic migraine (Bree and Levy, 2018). Following concussion, it is hypothesized that the unregulated release of excitatory amino acids, particularly glutamate, may create an environment of cerebral hyperexcitability (Kawamata et al., 1992; Barkhoudarian et al., 2016). In rats, mTBI is associated with increases in calcitonin gene-related peptide levels, astrocytosis, and microglia proliferation in the central trigeminal pathway, which may contribute to migraine headache after concussion (Tyburski et al., 2017). The pathophysiology of VM is also unclear, but likely related to structures common to both migraine and vestibular pathways (Furman et al., 2013). Interestingly, these overlaps involve both peripheral and central vestibular elements. The vestibular and trigeminal nuclei have reciprocal interaction (Brandt and Dieterich, 2017). In addition, the caudal parabrachial nucleus receives both afferent peripheral trigeminal nociceptive and vestibular input (Balaban, 2011), and the vasculature of the labyrinth receives trigeminal innervation (Vass et al., 1998). Not surprisingly, peripheral and central vestibular findings are observed in patients with VM (Polensek and Tusa, 2010). Caloric testing is abnormal in 10–22% of patients with VM (Blodow et al., 2014; Kang et al., 2016) and 27% have abnormal VEMP findings (Kang et al., 2016). Therefore, it may be possible that VM is causative for some SCC or otolith dysfunction observed after mTBI. The diagnostic criteria for definite and probable VM have been outlined by Lempert et al., (2012) and by the Headache Classification Committee of the International Headache Society, (2013). However, posttraumatic migraine and posttraumatic VM criteria have not been developed. Despite this, the high prevalence rates of posttraumatic migraine following SRC and the association with youth make VM a likely etiology of posttraumatic dizziness in SRC.
Other causes of posttraumatic dizziness Posttraumatic dizziness may be unrelated to vestibular dysfunction. Psychogenic etiology accounts for 8–10% of patients seen in tertiary clinics for dizziness and balance disorders (Staab and Ruckenstein, 2003;
VESTIBULAR DYSFUNCTION AND CONCUSSION Dieterich and Staab, 2017). The neurophysiologic basis underlying functional and psychiatric causes of vestibular symptoms is likely related to overlapping circuits involved in psychiatric conditions, particularly anxiety and vestibular processing (Balaban and Thayer, 2001). Alterations in autonomic regulation due to mTBI also have potential to cause posttraumatic dizziness (Esterov and Greenwald, 2017). Impaired vagal cardiac autonomic modulation (La Fountaine et al., 2011) and abnormal blood pressure responses at rest and with autonomic and graded exercise testing may manifest following concussion (Leddy et al., 2011; Kozlowski et al., 2013; Dobson et al., 2017). Cervical spine injury may occur in conjunction with SRC. Cervicogenic dizziness is the proposed result of faulty proprioceptive input to the vestibular nuclei from abnormal upper cervical spine efferents, resulting in sensory mismatch (Brandt, 1996). While more detailed discussion of each of these conditions is beyond the scope of this chapter, psychologic, autonomic, and cervical dysfunction should be given careful consideration when evaluating patients with posttraumatic dizziness.
SCREENING AND ASSESSMENT FOR VESTIBULAR IMPAIRMENT Most symptom inventories designed for use after SRC include items that may help to identify vestibular system problems (Crawford et al., 1996; McCrea et al., 2003; Lovell et al., 2006). As such, positive symptom report with respect to dizziness, balance problems, vision changes, and nausea may be an important beginning point to screen for potential vestibular dysfunction. The Dizziness Handicap Inventory may also be a useful self-report measure (Jacobson and Newman, 1990). It is a 25-item questionnaire which identifies the physical, functional, and emotional components of vestibular impairment.
Assessment of VOR impairment and visual motion sensitivity (VMS) Vestibular laboratory testing is not always necessary or practical following SRC. Laboratory findings may not always identify dysfunction, particularly if it is central in etiology. While clinical tools for screening and assessing BPPV and balance dysfunction have been established, postconcussion VOR or VMS clinical assessments have only recently been identified. Although subjective report tools are an important component in the assessment of potential vestibular symptoms in SRC, these measures are insufficient alone to determine if vestibular impairments are present. Some of the symptoms associated with vestibular dysfunction (e.g., dizziness) may have multiple etiologies, including
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autonomic, cardiovascular, or ocular impairment, and are not exclusive to the vestibular system (Furman et al., 2010). Subjective measures are also influenced by forthright accounting and rely on full activity participation, which may be altered in the athlete following SRC (Meehan et al., 2013; Asken et al., 2016). The Vestibular-Ocular Motor Screening (VOMS) was described to augment self-reports and to assist in objective screening for the presence of VOR and VMS deficits, plus other ocular motor problems, in the SRC population (Mucha et al., 2014). The VOMS measures symptom provocation after standardized assessment of smooth-pursuit, horizontal and vertical saccades, convergence, horizontal and vertical VOR, and VMS. Convergence testing is also accompanied by measure of near-point convergence distance. In a study of young athletes, the VOMS differentiated concussed participants from healthy controls (Mucha et al., 2014). The VOMS is further supported by a study which noted that positive findings on the VOMS were associated with delayed recovery following SRC (Anzalone et al., 2017). In clinical practice, the VOMS may also identify those who may benefit from more detailed vestibular assessment and rehabilitation to aid in recovery. Comprehensive vestibular evaluation also includes oculomotor examination; bedside, computerized, and laboratory VOR assessments; gaze-holding and positional testing; optokinetic testing; and static plus dynamic balance paradigms.
MANAGEMENT OF VESTIBULAR-SPECIFIC IMPAIRMENT AFTER SPORT-RELATED CONCUSSION Vestibular rehabilitation is the putative treatment for most types of vestibular impairment. Vestibular physical therapy is a specialty area within physical therapy in which customized treatments include canalith repositioning maneuvers, gaze stabilization, adaptation, habituation, substitution, and gait and postural control exercises. The efficacy of vestibular rehabilitation for vestibular dysfunction, including BPPV (Bhattacharyya et al., 2008), peripheral vestibular hypofunction (Hillier and McDonnell, 2011), central vestibular dysfunction (Brown et al., 2006), and migraine-related dizziness (Whitney et al., 2000; Gottshall et al., 2005), has been well established. There is emerging evidence regarding the efficacy of vestibular rehabilitation specific to concussion (Collins et al., 2014, 2016). Hoffer and colleagues (2004) examined dizziness in active-duty military personnel following concussion. Patients demonstrated improvement with respect to symptoms of dizziness, perception of balance function, and measures of vestibulo-ocular function after implementation of a vestibular rehabilitation program. Gottshall and Hoffer (2010) detailed the
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benefits of a vestibular physical therapy program on improving measures of gaze stability, ocular motor function, and dynamic visual acuity following blast-related mTBI. Alsalaheen et al. (2010) studied the effect of vestibular physical therapy in 114 concussed patients. Significant treatment effect was noted for 15 different measures of dizziness severity, balance confidence, gait, and static/dynamic balance. Schneider et al. (2014) demonstrated that cervicovestibular rehabilitation was effective in reducing time to medical clearance following an SRC. Addressing vestibular dysfunction as a clinical subtype with a targeted management strategy is beneficial. Following SRC, the most common subtypes of vestibular dysfunction include: BPPV; VOR impairment; VMS; and disturbances of postural control (Broglio et al., 2015). Each of these vestibular system manifestations requires unique vestibular rehabilitation elements. While these represent four distinct areas of impairment, it is important to recognize that none of these conditions is mutually exclusively and deficits often occur in combination.
Benign paroxysmal positional vertigo The most effective treatment for BPPV is canalith repositioning maneuvers, which relocate the displaced otoconia from the involved SCC (Bhattacharyya et al., 2017). Because BPPV can result in balance dysfunction (Adelsberger et al., 2015), it should be identified and treated prior to managing other vestibular issues. Management of posttraumatic BPPV is also complicated by higher rates of multicanal and bilateral involvement and may have higher recurrence rates (Gordon et al., 2004; Liu, 2012; Balatsouras et al., 2017).
Vestibulo-ocular reflex impairment The VOR network includes the vestibular periphery, the vestibular nuclei, related cerebellar connections, and direct projections from the vestibular nuclei to the abducens, trochlear and oculomotor nuclei (Balaban et al., 2016). Impairment in the VOR system results in gaze stabilization difficulties. Symptoms and impairment in VOR function have been reported in 40–58% of athletes in the first several days following SRC (Mucha et al., 2014; Anzalone et al., 2017). Gottshall et al. (2003) studied gaze stability function via computerized dynamic visual acuity testing (DVAT) in a cohort of military service members within 6 days of mTBI. Significant differences were identified between the concussed and control groups on all measures of the DVAT. Zhou and Brodsky (2015) report that more than half of adolescents have VOR impairment (demonstrated by DVAT) following
SRC. VOR impairment can be improved by gaze stability training, in which the VOR is adapted and its sensitivity habituated. Vestibular therapy exercises for VOR impairment require patients to maintain visual focus while movement of the head is superimposed. This motion creates movement of the visual image on the retina, which drives adaptation of the VOR. VOR adaptation exercises are carefully structured to maximize transference. This includes varying the size and complexity of the visual target, employing various postures and environmental challenges, or modifying duration, direction, amplitude, and velocity of movement (Herdman and Clendaniel, 2014).
Visual motion sensitivity VMS refers to a heightened awareness of normal visual stimuli, provoking dizziness, vertigo, nausea, or disequilibrium. VMS results from improper central nervous system synthesis of sensory information (vestibular, somatosensory, visual). As a result, athletes with VMS rely excessively on visual reference, and environments such as crowded hallways, sporting events, grocery stores, or even busy patterns produce visual and vestibular conflict. VMS is a component of chronic conditions such as visual vertigo (Bronstein, 2004), space and motion discomfort (Jacob et al., 2009), phobic postural vertigo (Brandt, 1996), chronic subjective dizziness (Staab and Ruckenstein, 2003), and persistent posturalperceptual dizziness (Staab et al., 2017). As with VOR impairment, VMS appears to be prevalent following concussion. In military service members with concussion, patients with ongoing VMS were categorized into a posttraumatic spatial disorientation group, comprising 19–35% of the sample (Hoffer et al., 2004; Gottshall, 2011). In a study of young athletes, 49% exhibited VMS when tested within the first week following SRC (Mucha et al., 2014). VMS is associated with uncomfortable symptoms and avoidance of environments which elicit symptoms. Vestibular rehabilitation for VMS involves gradual and systematic exposure to provocative stimuli in order to habituate the abnormal responses (Pavlou et al., 2004). VMS commonly coexists with posttraumatic migraine and/or anxiety disorders (Furman et al., 2005; Jacob et al., 2009). Early identification of and intervention for VMS issues following SRC may help to deter the development of more complex chronic conditions with high morbidity (Bittar and Lins, 2015; Dieterich and Staab, 2017).
Postural control Impaired balance is a familiar vestibular impairment identified in SRC (Guskiewicz et al., 1996, 1997; Guskiewicz, 2003). Early research revolved around
VESTIBULAR DYSFUNCTION AND CONCUSSION sensory organization, which requires multimodal integration and encoding of vestibular, visual, and somatosensory afferent information in the vestibular pathways of the brain (Cullen, 2012). Computerized platforms measuring sway under various sensory conditions were the first tools developed to measure sensory organization (Nashner et al., 1982). Additional clinical measures based on these testing concepts include the Clinical Test of Sensory Interaction in Balance (CTSIB), the modified CTSIB (Shumway-Cook and Horak, 1986), and the Balance Error Scoring System (BESS) test, which was developed specifically for athletes following concussion (Geurts et al., 1996). Although sensory organization impairment is reported acutely and subacutely following SRC, these deficits usually normalize within 5 days of injury (McCrea et al., 2003). Due to likely ceiling effects of static postural control assessments, dual-task paradigms have been used more recently to identify higher-level balance deficits postconcussion. Functional magnetic resonance imaging in youth SRC has shown altered activation patterns in the dorsolateral prefrontal and parietal cortices with slower performance time during dual task (Sinopoli et al., 2014). In a systematic review of dual-task assessment in concussion, 11 of 19 studies noted significant decreases in gait speed with dual task following concussion (Kleiner et al., 2018). Howell et al. (2018) examined dual-task gait performance in 42 individuals with SRC who were tracked for subsequent injury in the year after return to sport. Fifteen athletes (36%) reported sustaining a time loss orthopedic or concussive injury during the year after SRC. When compared with the group who did not sustain time loss injury, the injury group demonstrated worsening dual-task gait costs across the course of their clinical recovery from SRC. However, there are limitations in the clinical utility of dual-task assessment in concussion management. Although dual-task assessment may be more sensitive to concussion effects than other measures, there are currently no standardized paradigms, age-related normative values, or clinically significant cutoff scores.
CONCLUSION Vestibular dysfunction is a common manifestation of SRC and may prolong recovery. Identifying clinical subtypes and underlying etiology should guide management. While both peripheral and central structures may be involved, central mechanisms represent a significant portion of vestibular dysfunction following SRC. Vestibular assessment following SRC can be accomplished through a variety of clinical evaluation and screening tools. Treatment of vestibular dysfunction involves
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vestibular rehabilitation, which should address functional impairments, including BPPV, VOR dysfunction, VMS, and balance disturbance.
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Chapter 14
Vestibular dysfunction and concussion 1
ANNE MUCHA1*, SHERI FEDOR2, AND DANIELLE DEMARCO3 UPMC Center for Rehabilitation Services, Pittsburgh, PA, United States 2
Inova Physical Therapy Center, Fairfax, VA, United States
3
Baylor Institute for Rehabilitation, Frisco, TX, United States
Abstract The assessment and treatment of sport-related concussion (SRC) often requires a multifaceted approach. Vestibular dysfunction represents an important profile of symptoms and pathology following SRC, with high prevalence and association with prolonged recovery. Signs and symptoms of vestibular dysfunction may include dizziness, vertigo, disequilibrium, nausea, and visual impairment. Identifying the central and peripheral vestibular mechanisms responsible for pathology can aid in management of SRC. The most common vestibular disturbances after SRC include benign paroxysmal positional vertigo, vestibulo-ocular reflex impairment, visual motion sensitivity, and balance impairment. A variety of evidence-based screening and assessment tools can help to identify the various types of vestibular pathology in SRC. When vestibular dysfunction is identified, there is emerging support for applying targeted vestibular rehabilitation to manage this condition.
INTRODUCTION Vestibular dysfunction is prevalent following sport-related concussion (SRC); 50–84% of athletes report dizziness following an SRC (Lau et al., 2011; Kontos et al., 2012; Merritt et al., 2015). Importantly, when signs and symptoms associated with vestibular dysfunction are present after SRC, they appear to be associated with worse outcomes and prolonged recovery. A retrospective study examining a pediatric cohort (n ¼ 247) found that 81% exhibited vestibular abnormality (Corwin et al., 2015). On average, these patients required significantly more time to return to school (56 vs. 6 days) and to be fully cleared to return to sport (106 vs. 29 days) when compared with age-matched subjects without vestibular findings. Another retrospective study involving 101 pediatric patients following SRC found that acute postconcussion vestibulo-ocular dysfunction was associated with higher risk of developing postconcussion syndrome (adjusted
odds ratio of 4.10) (Ellis et al., 2015). The National Collegiate Athletic Association Injury Surveillance System examined 1647 cases of SRC and noted that symptom duration and return to competition were significantly increased when audiovestibular symptoms of dizziness, imbalance, and noise sensitivity were present (Chorney et al., 2017). Despite the negative relationship of vestibular dysfunction to recovery, there is evidence that these effects can be modified with vestibular rehabilitation (Alsalaheen et al., 2010; Schneider et al., 2014; Broglio et al., 2015). Therefore, clinicians should be mindful of possible vestibular dysfunction when managing athletes with SRC. This chapter will provide a discussion of common vestibular dysfunction presentation and etiology following SRC. Assessment tools and intervention strategies to mitigate vestibular dysfunction will be explored.
*Correspondence to: Anne Mucha, DPT, UPMC Centers for Rehab Services, 3200 South Water St. Pittsburgh PA 15203, United States. Tel: +1-412-432-3700, Email: [email protected]
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REVIEW OF VESTIBULAR SYSTEM STRUCTURE AND FUNCTION The vestibular system is a complex sensorimotor system responsible for detection of motion and position of the head and body, motor responses, multisensory integration, and higher-level cognitive-perceptual functions (Hain, 2011; Brandt and Dieterich, 2017). The structure and function of the vestibular system are organized into peripheral and central elements. Disorders of the peripheral vestibular system involve: the vestibular nerve; the semicircular canals (SCCs), which sense angular acceleration; and the otolith organs (utricle and saccule), which detect linear acceleration and head tilt. In contrast, central vestibular disorders involve the vestibular nuclei, flocculus, and vermis of the cerebellum, midbrain, thalamus, parietoinsular vestibular cortex, visual cortex or projections between these regions (Brandt and Dieterich, 2017). Signs and symptoms such as dizziness, vertigo, nausea, postural instability, visual distortion, and altered spatial orientation are most commonly associated with vestibular pathology (Herdman and Clendaniel, 2014). Due to the highly integrative nature of the vestibular system with other sensory systems, these signs and symptoms can be significantly affected by the presence or absence of visual, somatosensory, or auditory stimuli (Keshner et al., 2004).
ETIOLOGY OF VESTIBULAR IMPAIRMENT AFTER SPORTS-RELATED CONCUSSION There are a multitude of vestibular disorders that occur due to pathology in the peripheral, central, or combined peripheral/central vestibular structures. Because etiology of impairment may inform intervention, establishing causality is important for clinical management. Currently, the literature is limited regarding the etiology of vestibular dysfunction specific to SRC. Therefore, we will use the best current evidence to discuss vestibular impairment in the context of SRC when research is lacking.
Peripheral mechanisms A direct or indirect force to the head has potential to damage the intralabyrinthine structures or the vestibular nerve. Such trauma-induced peripheral vestibular pathology, when accompanied by high-frequency hearing loss, is termed labyrinthine concussion (Choi et al., 2013). Although a peripheral vestibular etiology of dizziness accounts for approximately 45% of vestibular dysfunction in the general population (Brandt and Dieterich, 2017), prevalence of peripheral vestibular dysfunction following SRC is much lower (Zhou and Brodsky, 2015).
BENIGN PAROXYSMAL POSITIONAL VERTIGO (BPPV) BPPV is a disorder of the peripheral vestibular system that may result from head trauma (Pisani et al., 2015). BPPV results from small calcium carbonate crystals (otoconia) being dislodged in the utricle; these crystals then relocate to one or more of the adjacent SCCs. The weight of the otoconia then interferes with normal fluid dynamics within the canals, resulting in episodic vertigo. BPPV is characterized by spells of vertigo with changes in head position such as looking up, rolling in bed, lying down on a flat surface, or bending over (Fife et al., 2008). The diagnosis of BPPV is confirmed if characteristic nystagmus and vertigo manifest with either the Dix–Hallpike or supine roll test on clinical exam (Bhattacharyya et al., 2017). BPPV is the most common peripheral vestibular disorder in adults, with a lifetime prevalence of 2.4% (von Brevern et al., 2007). However, in younger patients, incidence is much lower (Bhattacharyya et al., 2017). In a large multicenter study, Lee et al. (2017) reported that BPPV was diagnosed in only 5.1% (21/411) of children and adolescents evaluated for dizziness (21/411). In studies describing BPPV rates related to traumatic brain injury (TBI), incidence was 15% in a cohort including patients with severe, moderate, and mild TBI (mTBI) and mean age of 39.9 years (Davies and Luxon, 1995). In contrast, BPPV was diagnosed in just 4.3% of cases referred for vestibular physical therapy following concussion from any cause (Alsalaheen et al., 2010), and was not identified in any cases of pediatric SRC (n ¼ 42) referred for assessment of posttraumatic dizziness (Zhou and Brodsky, 2015). Given that youth patients comprise 90.18% of all SRC diagnoses (Amoo-Achampong et al., 2017), it is likely that a combination of age and injury severity contributes to the low rate of BPPV occurrence following SRC.
SEMICIRCULAR CANAL PATHOLOGY The three orthogonally oriented SCCs in each labyrinth are the peripheral vestibular structures responsible for sensing angular acceleration. The gold-standard method for assessing function of the SCCs is the bithermal caloric test. With caloric testing, a temperature gradient is introduced which induces endolymphatic flow, stimulating the horizontal SCC primary afferents and activating the vestibulo-ocular reflex (VOR) pathway (Shepard and Jacobson, 2016). The Head Impulse Test (HIT) is an alternate, more portable method to assess SCC function through the VOR response (MacDougall et al., 2009). While the caloric test assesses low-frequency components of the VOR, the HIT assesses high-frequency components (greater than 1 Hz). Most studies examining peripheral vestibular function via caloric testing are
VESTIBULAR DYSFUNCTION AND CONCUSSION limited by mixed severity of TBI and inconsistent test interpretation criteria (Davies and Luxon, 1995). However, when examining mTBI only, abnormal caloric testing has been reported in varying degrees ranging from 3 to 21% (Tuohimaa, 1978; Zhou and Brodsky, 2015). Alshehri et al. (2016) identified no cases of abnormal horizontal SCC function by video HIT study of 56 subjects with posttraumatic dizziness.
OTOLITH DYSFUNCTION The otolith organs (utricle and saccule) sense linear head acceleration and head tilt, with the utricle detecting horizontal movements and the saccule sensing vertical motion. The otoliths provide primary input for vestibulospinal reflex output and supplementary information along with SCCs for the VOR (Carpenter et al., 1999). BPPV is a type of otolith dysfunction, as its mechanism is displacement of otoconia from the utricle. However, other forms of vestibular otolith impairment may also present posttraumatically. The vestibular-evoked myogenic potential test (VEMP) assesses otolith function. Cervical VEMPs (cVEMPs) assess the saccular-collic pathway, which is a part of the vestibulospinal reflex network (Colebatch et al., 2016). cVEMP responses are recorded from the activated sternocleidomastoid muscle in response to sound or vibration. In contrast, ocular VEMPs (oVEMPs) record responses from the inferior oblique eye muscles in response to sound or vibration, assessing the utricular-otolith pathway contribution to the VOR response (Colebatch et al., 2016). The subjective visual vertical (SVV) test also assesses otolith (primarily utricle) function. SVV requires the subject to adjust the position of a presented line to vertical orientation (parallel to gravity) in the absence of other sensory cues. The difference between perceived versus actual vertical is normally within 2° but has been shown to be significantly impaired in central and peripheral lesions involving utriculo-ocular pathways (Kingma, 2006). Studies examining otolith function via VEMPs or SVV are limited in mTBI and SRC. Otolith dysfunction rates following blast-related TBI range from 29% (Scherer et al., 2011) to 52% (Akin et al., 2017). In blunt-force TBI and associated vertigo, Ernst and colleagues (2005) reported abnormal VEMPs in 25% of 63 cases. Lee et al. (2011) reported abnormal cVEMPs in 32% of 28 patients followed prospectively after head trauma. Finally, Zhou and Brodsky (2015) studied children and adolescents who had undergone vestibular testing for evaluation of dizziness and/or balance impairment following an SRC; abnormal otolith function was identified in 18% (7/38) based on cVEMP findings and 13% (5/38) based on SVV findings.
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PERILYMPHATIC FISTULA (PLF) Some authors have proposed PLF as a cause of dizziness following concussion (Ernst et al., 2005; Fife and Giza, 2013). Traumatic forces may cause membrane rupture at the oval or round window, resulting in a PLF and fluid leakage into the middle ear. Direct trauma from temporal bone fracture and barotrauma are the most common mechanisms for PLF (Maitland, 2001). PLF typically causes fluid or blood discharge from the involved ear, unilateral auditory disturbance, tinnitus, vertigo, or imbalance. Temporal bone fracture is typically associated with moderate or severe head TBI (Naguib et al., 2012). While forces associated with moderate or severe TBI may cause PLF, there is limited evidence of PLF following mTBI (Davies and Luxon, 1995).
POSTTRAUMATIC ENDOLYMPHATIC HYDROPS Endolymphatic hydrops is a disorder of the peripheral vestibular system in which endolymphatic fluid balance in the labyrinth becomes dysregulated, leading to distension of the endolymphatic space (hydrops). Symptoms are episodic but are often quite severe and include vertigo, nausea/vomiting, auditory changes, auditory pressure/fullness, and imbalance. Idiopathic endolymphatic hydrops is synonymous with Menière’s disease. One study (Ernst et al., 2005) identified delayed endolymphatic hydrops in 19% (12 of 63) of patients following head trauma of undetermined severity. However, these findings should be considered with caution, as electrocochleography was used to confirm the presence of hydrops. The clinical utility of electrocochleography for the diagnostic evaluation of Menière’s disease is controversial (Lopez-Escamez et al., 2015; Ciorba et al., 2017) and is not validated by the Bárány Society criteria for diagnosis of Menière’s disease (Orchik et al., 1993; Ziylan et al., 2016).
Central mechanisms A direct or indirect force to the head has potential to disrupt the structure and function of central vestibular structures. The frequent coexistence of central oculomotor dysfunction with posttraumatic vestibular dysfunction suggests centrally mediated vestibular impairment (Pearce et al., 2015; Zhou and Brodsky, 2015; DuPrey et al, 2017; Howell et al, 2018). Further, vestibulospinal reflex impairment is unrelated to VOR impairment (Mucha et al., 2014; McDevitt et al., 2016; Wright et al., 2017); while these vestibular functions utilize the same peripheral structures, distinct central nervous system pathways are employed, further illustrating the likelihood of central vestibular mechanisms in SRC.
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WHITE-MATTER ABNORMALITIES The neurometabolic changes associated with concussion are triggered by acceleration and deceleration forces and associated traumatic stretching of neuronal axons (Barkhoudarian et al., 2016). Although standard imaging (magnetic resonance and computed tomography) rarely identifies findings associated with SRC (Useche and Bermudez, 2018), diffusion tensor imaging may reveal central microstructural axonal injury via fractional anisotropy. White-matter abnormalities are identified following blast-related concussion with loss of consciousness (Hayes et al., 2015) and following SRC (Cubon et al., 2011; Borich et al., 2013; Virji-Babul et al., 2013). Alhilali et al. (2014) examined diffusion tensor imaging findings specific to vestibular impairment. When comparing 30 patients with vestibular symptoms to 39 patients without vestibular symptoms, concussed patients with vestibular symptoms were more likely to manifest with decreased fractional anisotropy in the cerebellum and fusiform gyri (p < 0.05) (Alhilali et al., 2014).
MIGRAINE Migraine is the most common cause of posttraumatic headache. In a prospective study of 212 emergency department patients with headache following concussion, 49% were classified with migraine or probable migraine (Headache Classification Committee of the International Headache Society (IHS), 2013; Lucas et al., 2014). Following SRC, migraine was positively identified in more than 40% of athletes (Kontos et al., 2013; Sufrinko et al., 2018). Vestibular migraine (VM) is a common variant of migraine (Lempert et al., 2012). VM is a frequent cause of episodic dizziness, accounting for 7–11% of adult patients evaluated in specialized vestibular disorders clinics (Neuhauser et al., 2001; Brandt and Dieterich, 2017). VM is more prevalent in younger patients. In a large multicenter study of children and adolescents evaluated for dizziness, approximately 29% (120/411) were diagnosed with VM (Lee et al., 2017). In studies of military service members with dizziness following mTBI, three categories were identified: posttraumatic migraine-associated dizziness; spatial disorientation; and BPPV (Hoffer et al., 2004). In patients with mixed blast and blunt-force mTBI, 41–59% of diagnosed patients had posttraumatic migraine-associated dizziness (Hoffer et al., 2004; Gottshall, 2011). The pathophysiology of posttraumatic migraine is uncertain. In primary migraine, abnormal activation of trigeminovascular pain pathway occurs in genetically predisposed individuals (Akerman et al., 2017). Triggering
mechanisms linked to migraine headache include stress, loss of sleep, skipping meals, specific foods, alcohol, hormonal fluctuations, and certain types of light or noise (Pellegrino et al., 2017). Based on significantly higher rates of migraine following a concussion compared with the general population, posttraumatic migraine is not simply a manifestation of a pre-existing migraine diagnosis. Hypersensitivity to headache triggers is a speculated mechanism by which concussion allows for increased activation of the trigeminovascular pain pathways, leading to posttraumatic migraine (Bree and Levy, 2018). Following concussion, it is hypothesized that the unregulated release of excitatory amino acids, particularly glutamate, may create an environment of cerebral hyperexcitability (Kawamata et al., 1992; Barkhoudarian et al., 2016). In rats, mTBI is associated with increases in calcitonin gene-related peptide levels, astrocytosis, and microglia proliferation in the central trigeminal pathway, which may contribute to migraine headache after concussion (Tyburski et al., 2017). The pathophysiology of VM is also unclear, but likely related to structures common to both migraine and vestibular pathways (Furman et al., 2013). Interestingly, these overlaps involve both peripheral and central vestibular elements. The vestibular and trigeminal nuclei have reciprocal interaction (Brandt and Dieterich, 2017). In addition, the caudal parabrachial nucleus receives both afferent peripheral trigeminal nociceptive and vestibular input (Balaban, 2011), and the vasculature of the labyrinth receives trigeminal innervation (Vass et al., 1998). Not surprisingly, peripheral and central vestibular findings are observed in patients with VM (Polensek and Tusa, 2010). Caloric testing is abnormal in 10–22% of patients with VM (Blodow et al., 2014; Kang et al., 2016) and 27% have abnormal VEMP findings (Kang et al., 2016). Therefore, it may be possible that VM is causative for some SCC or otolith dysfunction observed after mTBI. The diagnostic criteria for definite and probable VM have been outlined by Lempert et al., (2012) and by the Headache Classification Committee of the International Headache Society, (2013). However, posttraumatic migraine and posttraumatic VM criteria have not been developed. Despite this, the high prevalence rates of posttraumatic migraine following SRC and the association with youth make VM a likely etiology of posttraumatic dizziness in SRC.
Other causes of posttraumatic dizziness Posttraumatic dizziness may be unrelated to vestibular dysfunction. Psychogenic etiology accounts for 8–10% of patients seen in tertiary clinics for dizziness and balance disorders (Staab and Ruckenstein, 2003;
VESTIBULAR DYSFUNCTION AND CONCUSSION Dieterich and Staab, 2017). The neurophysiologic basis underlying functional and psychiatric causes of vestibular symptoms is likely related to overlapping circuits involved in psychiatric conditions, particularly anxiety and vestibular processing (Balaban and Thayer, 2001). Alterations in autonomic regulation due to mTBI also have potential to cause posttraumatic dizziness (Esterov and Greenwald, 2017). Impaired vagal cardiac autonomic modulation (La Fountaine et al., 2011) and abnormal blood pressure responses at rest and with autonomic and graded exercise testing may manifest following concussion (Leddy et al., 2011; Kozlowski et al., 2013; Dobson et al., 2017). Cervical spine injury may occur in conjunction with SRC. Cervicogenic dizziness is the proposed result of faulty proprioceptive input to the vestibular nuclei from abnormal upper cervical spine efferents, resulting in sensory mismatch (Brandt, 1996). While more detailed discussion of each of these conditions is beyond the scope of this chapter, psychologic, autonomic, and cervical dysfunction should be given careful consideration when evaluating patients with posttraumatic dizziness.
SCREENING AND ASSESSMENT FOR VESTIBULAR IMPAIRMENT Most symptom inventories designed for use after SRC include items that may help to identify vestibular system problems (Crawford et al., 1996; McCrea et al., 2003; Lovell et al., 2006). As such, positive symptom report with respect to dizziness, balance problems, vision changes, and nausea may be an important beginning point to screen for potential vestibular dysfunction. The Dizziness Handicap Inventory may also be a useful self-report measure (Jacobson and Newman, 1990). It is a 25-item questionnaire which identifies the physical, functional, and emotional components of vestibular impairment.
Assessment of VOR impairment and visual motion sensitivity (VMS) Vestibular laboratory testing is not always necessary or practical following SRC. Laboratory findings may not always identify dysfunction, particularly if it is central in etiology. While clinical tools for screening and assessing BPPV and balance dysfunction have been established, postconcussion VOR or VMS clinical assessments have only recently been identified. Although subjective report tools are an important component in the assessment of potential vestibular symptoms in SRC, these measures are insufficient alone to determine if vestibular impairments are present. Some of the symptoms associated with vestibular dysfunction (e.g., dizziness) may have multiple etiologies, including
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autonomic, cardiovascular, or ocular impairment, and are not exclusive to the vestibular system (Furman et al., 2010). Subjective measures are also influenced by forthright accounting and rely on full activity participation, which may be altered in the athlete following SRC (Meehan et al., 2013; Asken et al., 2016). The Vestibular-Ocular Motor Screening (VOMS) was described to augment self-reports and to assist in objective screening for the presence of VOR and VMS deficits, plus other ocular motor problems, in the SRC population (Mucha et al., 2014). The VOMS measures symptom provocation after standardized assessment of smooth-pursuit, horizontal and vertical saccades, convergence, horizontal and vertical VOR, and VMS. Convergence testing is also accompanied by measure of near-point convergence distance. In a study of young athletes, the VOMS differentiated concussed participants from healthy controls (Mucha et al., 2014). The VOMS is further supported by a study which noted that positive findings on the VOMS were associated with delayed recovery following SRC (Anzalone et al., 2017). In clinical practice, the VOMS may also identify those who may benefit from more detailed vestibular assessment and rehabilitation to aid in recovery. Comprehensive vestibular evaluation also includes oculomotor examination; bedside, computerized, and laboratory VOR assessments; gaze-holding and positional testing; optokinetic testing; and static plus dynamic balance paradigms.
MANAGEMENT OF VESTIBULAR-SPECIFIC IMPAIRMENT AFTER SPORT-RELATED CONCUSSION Vestibular rehabilitation is the putative treatment for most types of vestibular impairment. Vestibular physical therapy is a specialty area within physical therapy in which customized treatments include canalith repositioning maneuvers, gaze stabilization, adaptation, habituation, substitution, and gait and postural control exercises. The efficacy of vestibular rehabilitation for vestibular dysfunction, including BPPV (Bhattacharyya et al., 2008), peripheral vestibular hypofunction (Hillier and McDonnell, 2011), central vestibular dysfunction (Brown et al., 2006), and migraine-related dizziness (Whitney et al., 2000; Gottshall et al., 2005), has been well established. There is emerging evidence regarding the efficacy of vestibular rehabilitation specific to concussion (Collins et al., 2014, 2016). Hoffer and colleagues (2004) examined dizziness in active-duty military personnel following concussion. Patients demonstrated improvement with respect to symptoms of dizziness, perception of balance function, and measures of vestibulo-ocular function after implementation of a vestibular rehabilitation program. Gottshall and Hoffer (2010) detailed the
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benefits of a vestibular physical therapy program on improving measures of gaze stability, ocular motor function, and dynamic visual acuity following blast-related mTBI. Alsalaheen et al. (2010) studied the effect of vestibular physical therapy in 114 concussed patients. Significant treatment effect was noted for 15 different measures of dizziness severity, balance confidence, gait, and static/dynamic balance. Schneider et al. (2014) demonstrated that cervicovestibular rehabilitation was effective in reducing time to medical clearance following an SRC. Addressing vestibular dysfunction as a clinical subtype with a targeted management strategy is beneficial. Following SRC, the most common subtypes of vestibular dysfunction include: BPPV; VOR impairment; VMS; and disturbances of postural control (Broglio et al., 2015). Each of these vestibular system manifestations requires unique vestibular rehabilitation elements. While these represent four distinct areas of impairment, it is important to recognize that none of these conditions is mutually exclusively and deficits often occur in combination.
Benign paroxysmal positional vertigo The most effective treatment for BPPV is canalith repositioning maneuvers, which relocate the displaced otoconia from the involved SCC (Bhattacharyya et al., 2017). Because BPPV can result in balance dysfunction (Adelsberger et al., 2015), it should be identified and treated prior to managing other vestibular issues. Management of posttraumatic BPPV is also complicated by higher rates of multicanal and bilateral involvement and may have higher recurrence rates (Gordon et al., 2004; Liu, 2012; Balatsouras et al., 2017).
Vestibulo-ocular reflex impairment The VOR network includes the vestibular periphery, the vestibular nuclei, related cerebellar connections, and direct projections from the vestibular nuclei to the abducens, trochlear and oculomotor nuclei (Balaban et al., 2016). Impairment in the VOR system results in gaze stabilization difficulties. Symptoms and impairment in VOR function have been reported in 40–58% of athletes in the first several days following SRC (Mucha et al., 2014; Anzalone et al., 2017). Gottshall et al. (2003) studied gaze stability function via computerized dynamic visual acuity testing (DVAT) in a cohort of military service members within 6 days of mTBI. Significant differences were identified between the concussed and control groups on all measures of the DVAT. Zhou and Brodsky (2015) report that more than half of adolescents have VOR impairment (demonstrated by DVAT) following
SRC. VOR impairment can be improved by gaze stability training, in which the VOR is adapted and its sensitivity habituated. Vestibular therapy exercises for VOR impairment require patients to maintain visual focus while movement of the head is superimposed. This motion creates movement of the visual image on the retina, which drives adaptation of the VOR. VOR adaptation exercises are carefully structured to maximize transference. This includes varying the size and complexity of the visual target, employing various postures and environmental challenges, or modifying duration, direction, amplitude, and velocity of movement (Herdman and Clendaniel, 2014).
Visual motion sensitivity VMS refers to a heightened awareness of normal visual stimuli, provoking dizziness, vertigo, nausea, or disequilibrium. VMS results from improper central nervous system synthesis of sensory information (vestibular, somatosensory, visual). As a result, athletes with VMS rely excessively on visual reference, and environments such as crowded hallways, sporting events, grocery stores, or even busy patterns produce visual and vestibular conflict. VMS is a component of chronic conditions such as visual vertigo (Bronstein, 2004), space and motion discomfort (Jacob et al., 2009), phobic postural vertigo (Brandt, 1996), chronic subjective dizziness (Staab and Ruckenstein, 2003), and persistent posturalperceptual dizziness (Staab et al., 2017). As with VOR impairment, VMS appears to be prevalent following concussion. In military service members with concussion, patients with ongoing VMS were categorized into a posttraumatic spatial disorientation group, comprising 19–35% of the sample (Hoffer et al., 2004; Gottshall, 2011). In a study of young athletes, 49% exhibited VMS when tested within the first week following SRC (Mucha et al., 2014). VMS is associated with uncomfortable symptoms and avoidance of environments which elicit symptoms. Vestibular rehabilitation for VMS involves gradual and systematic exposure to provocative stimuli in order to habituate the abnormal responses (Pavlou et al., 2004). VMS commonly coexists with posttraumatic migraine and/or anxiety disorders (Furman et al., 2005; Jacob et al., 2009). Early identification of and intervention for VMS issues following SRC may help to deter the development of more complex chronic conditions with high morbidity (Bittar and Lins, 2015; Dieterich and Staab, 2017).
Postural control Impaired balance is a familiar vestibular impairment identified in SRC (Guskiewicz et al., 1996, 1997; Guskiewicz, 2003). Early research revolved around
VESTIBULAR DYSFUNCTION AND CONCUSSION sensory organization, which requires multimodal integration and encoding of vestibular, visual, and somatosensory afferent information in the vestibular pathways of the brain (Cullen, 2012). Computerized platforms measuring sway under various sensory conditions were the first tools developed to measure sensory organization (Nashner et al., 1982). Additional clinical measures based on these testing concepts include the Clinical Test of Sensory Interaction in Balance (CTSIB), the modified CTSIB (Shumway-Cook and Horak, 1986), and the Balance Error Scoring System (BESS) test, which was developed specifically for athletes following concussion (Geurts et al., 1996). Although sensory organization impairment is reported acutely and subacutely following SRC, these deficits usually normalize within 5 days of injury (McCrea et al., 2003). Due to likely ceiling effects of static postural control assessments, dual-task paradigms have been used more recently to identify higher-level balance deficits postconcussion. Functional magnetic resonance imaging in youth SRC has shown altered activation patterns in the dorsolateral prefrontal and parietal cortices with slower performance time during dual task (Sinopoli et al., 2014). In a systematic review of dual-task assessment in concussion, 11 of 19 studies noted significant decreases in gait speed with dual task following concussion (Kleiner et al., 2018). Howell et al. (2018) examined dual-task gait performance in 42 individuals with SRC who were tracked for subsequent injury in the year after return to sport. Fifteen athletes (36%) reported sustaining a time loss orthopedic or concussive injury during the year after SRC. When compared with the group who did not sustain time loss injury, the injury group demonstrated worsening dual-task gait costs across the course of their clinical recovery from SRC. However, there are limitations in the clinical utility of dual-task assessment in concussion management. Although dual-task assessment may be more sensitive to concussion effects than other measures, there are currently no standardized paradigms, age-related normative values, or clinically significant cutoff scores.
CONCLUSION Vestibular dysfunction is a common manifestation of SRC and may prolong recovery. Identifying clinical subtypes and underlying etiology should guide management. While both peripheral and central structures may be involved, central mechanisms represent a significant portion of vestibular dysfunction following SRC. Vestibular assessment following SRC can be accomplished through a variety of clinical evaluation and screening tools. Treatment of vestibular dysfunction involves
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vestibular rehabilitation, which should address functional impairments, including BPPV, VOR dysfunction, VMS, and balance disturbance.
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