Abstract
Background and Purpose There has been an increasing focus on vestibular rehabilitation (VR) after traumatic brain injury (TBI) in recent years. However, detailed descriptions of the content of and patient responses to VR after TBI are limited. The purposes of this case series are (1) to describe a modified, group-based VR intervention and (2) to examine changes in self-reported and performance-based outcome measures.
Case Description Two women and 2 men (aged 24–45 years) with mild TBI, dizziness, and balance problems participated in an 8-week intervention consisting of group sessions with guidance, individually modified VR exercises, a home exercise program, and an exercise diary. Self-reported and performance-based outcome measures were applied to assess the impact of dizziness and balance problems on functions related to activity and participation.
Outcomes The intervention caused no adverse effects. Three of the 4 patients reported reduced self-perceived disability because of dizziness, diminished frequency and severity of dizziness, improved health-related quality of life, reduced psychological distress, and improved performance-based balance. The change scores exceeded the minimal detectable change, indicating a clinically significant change or improvement in the direction of age-related norms. The fourth patient did not change or improve in most outcome measures.
Discussion A modified, group-based VR intervention was safe and appeared to be viable and beneficial when addressing dizziness and balance problems after TBI. However, concurrent physical and psychological symptoms, other neurological deficits, and musculoskeletal problems might influence the course of central nervous system compensation and recovery. The present case series may be useful for tailoring VR interventions to patients with TBI. Future randomized controlled trials are warranted to evaluate the short- and long-term effects of VR after TBI.
Patients with traumatic brain injury (TBI) commonly report dizziness and balance problems, with a prevalence of 23% to 81%.1–4 Dizziness and balance problems are considered to be adverse prognostic factors after TBI that might cause functional limitations and psychological distress and might have a negative impact on quality of life and the ability to return to work.5
The underlying mechanisms of dizziness and balance problems after TBI are complex. Trauma might affect the labyrinth and other vestibular structures and cause benign paroxysmal positional vertigo (BPPV), labyrinthine concussion, perilymphatic fistula, and unilateral vestibular loss.1,6 Dizziness without labyrinthine dysfunctions might indicate central posttraumatic vertigo, postconcussion syndrome, posttraumatic migraines, diffuse axonal injury, or anxiety-associated dizziness.1,6 The traumatic mechanism that caused a possible vestibular injury, postconcussion symptoms, and other neurological or musculoskeletal symptoms concurrently characterizes the patient with TBI.1,4,7
Reports from studies applying principles of vestibular rehabilitation (VR) in patients with TBI indicate a reduction in dizziness and balance problems.3,8–10 Modifications appear necessary to accommodate postconcussion symptoms and physical and cognitive problems after the trauma.2,7,11 However, descriptions of VR programs for patients with TBI are limited, and a preliminary search for randomized controlled trials (RCTs) to establish the effect of VR on patients with TBI did not render any results. Explorations such as in case studies that illuminate how VR can be modified in clinical practice might stimulate clinicians and researchers to quantify the effects of VR in patients with dizziness and balance problems after TBI.
We modified a group-based VR intervention originally developed for patients with chronic dizziness at Oslo and Akershus University College.12 The modifications included a follow-up twice weekly for 8 weeks, with an emphasis on individual modifications and progression of the intervention with considerations of other postconcussion symptoms and typical challenges after TBI. The program was mainly based on the motor control theory13 and the theory of positive psychology for coping with the symptom pressure and disease burden.14 The VR intervention used motor learning principles, with gradual increase in challenges of balance ability that required integration of multiple sensory inputs. Elements from established VR programs were included and followed the principles of habituation, adaptation, and substitution exercises and balance relearning.1,2,7,11,13
The primary aim of this case series is to describe a group-based VR intervention for patients with TBI. The secondary aim is to examine how the intervention may assist in addressing the targeted problems of dizziness and balance problems, by describing changes in self-perceived dizziness, balance, and health-related quality of life (HRQL). The intervention was applied in an ongoing RCT (ClinicalTrials.gov identifier: NCT01695577).
Case Descriptions: Patient History and Systems Review
Four patients were recruited at an outpatient clinic at the Department of Physical Medicine and Rehabilitation at Oslo University Hospital. They were the first 2 male and female patients recruited for this case series prior to the ongoing RCT. Inclusion criteria were TBI, age between 16 and 60 years, dizziness reported on the Rivermead Postconcussion Symptoms Questionnaire (RPQ),15 or a positive Romberg test. Patients were excluded if they had severe psychological disease, language problems, cognitive dysfunction, fractures, or other comorbidities affecting mobility and independent gait. Written informed consent was obtained from the patients.
The patients underwent a medical evaluation by a physiatrist. A physical therapist (I.K.) assessed the patients with the modified Clinical Test for Sensory Interaction in Balance (mCTSIB), single-leg stance, tests of the oculomotor system (smooth pursuit, saccadic eye movements), head-thrust test, clinical Dynamic Visual Acuity Test (DVAT), and positional testing (Dix-Hallpike test and Roll test), all of which are commonly applied clinical tests in patients with dizziness.1 Patient data are presented in Table 1.
Demographic and Injury-Related Characteristics: Baseline Status, Symptoms, and Clinical Assessmentsa
Clinical Impression 1
The patients had mild TBI according to the Glasgow Coma Scale (GCS) score and persistent dizziness and were diagnosed with postconcussion syndrome by the physiatrist using the International Statistical Classification of Diseases and Related Health Problems, 10th revision (ICD-10) criteria.1
The patients were on sick leave or had delayed their studies at college or university due to the TBI. They had persistent symptoms in the physical, cognitive, and psychological/emotional domains of the RPQ. The results from the tests performed by the physical therapist are presented in Table 1. The tests showed mild balance problems, especially with eyes closed, which may indicate visual dependency for balance, and difficulties with sensory integration. The oculomotor tests were normal but symptomatic (dizziness, eye strain) in all patients. The DVAT provoked dizziness during or right after the test and was positive (≥4 lines difference) in patient 2, indicating reduced vestibulo-ocular reflex (VOR). Patient 3 tested positive for both posterior semicircular canal (PSC) and horizontal semicircular canal (HSC) BPPV. All patients reported dizziness provoked by movements of the head or body or by watching moving visual objects (traffic, crowds of people, movies, television), indicating motion sensitivity. Head-thrust tests were negative in all patients. Patients 1 and 4 reported neck pain and decreased active range of motion (AROM), indicating a possible cervicogenic disorder. Patient 4 had a positive computed tomography scan (intraventricular hemorrhage) that indicated possible central posttraumatic vertigo.
The patients were considered relevant candidates for the modified VR intervention program. They had each received a multidisciplinary evaluation and rehabilitation at Oslo University Hospital but had not participated in a VR program prior to inclusion in this study.
Examination
Standardized self-reported and performance-based instruments measuring self-perceived handicap, dizziness, balance, mobility, and HRQL were used to evaluate patient outcomes. The overview of the outcome measures, including their psychometric properties, is presented in Table 2. The same physical therapist (I.K.) carried out the assessments on each patient before and after the intervention.
Standardized Outcome Measuresa
Self-reported Outcome Measures
Self-perceived disability because of dizziness was measured with the Dizziness Handicap Inventory (DHI).16 The frequency and severity of dizziness symptoms in the preceding month were measured using the Vertigo Symptom Scale–Short Form (VSS-SF). The VSS-SF comprises 2 subscales: vertigo-balance (VSS-V) and autonomic anxiety symptoms (VSS-A).17,18 Postconcussion symptoms were measured with the RPQ. The RPQ comprises 2 subscales: physical (RPQ-3) and psychological (RPQ-13).15 Health-related quality of life was measured with the Quality of Life After Brain Injury (QOLIBRI), a self-report instrument with 6 subscales that provides a profile of functioning and a total score for HRQL.19,20 Psychological distress was assessed with the Hospital Anxiety and Depression Scale (HADS).21,22
Performance Based Outcome Measures
Balance was assessed with the Balance Error Scoring System (BESS), a standardized balance testing system consisting of three 20-second stances with eyes closed (double-leg stance, single-leg stance, and tandem stance) on firm and foam surfaces.23,24
Mobility was measured with the High-Level Mobility Assessment Tool for traumatic brain injury (HiMAT). The HiMAT consists of walking, running, skipping, hopping, and stair items measured with a stopwatch or tape measure.25
Clinical Impression 2
The patients reported moderate-to-severe disabilities because of dizziness (DHI) and severe dizziness (VSS-SF) (Tab. 3). Postconcussion symptoms were reported in both subscales of the RPQ. The QOLIBRI sum score indicated a lower HRQL than for a reference group.19 The patients also reported some degree of psychological distress (HADS). Balance measured with the BESS test showed scores below-normal data and confirmed the visual dependency pattern and reduced sensory integration observed in the initial assessments of balance. Scores of mobility (HiMAT) showed 1 patient within the normal range and 2 patients with slightly reduced pace and increased symptoms of dizziness during testing. One patient did not perform the test due to painful feet.
Preintervention (Pre) and Postintervention (Post) Scores and Change Scores in Outcome Measures: Tentative Underlying Cause of Dizziness and Balance Problems and Number of Sessions Attendeda
The standardized self-reported and performance-based outcome measures confirmed that the patients had disabilities comprising impairments and reduced activity and participation commonly observed in the TBI population. Based on the clinical assessments and the standardized outcome measures, a tentative underlying cause of dizziness and balance problems was identified (Tab. 3). To indicate improvements, we expected that changes in the outcome measures would exceed measurement error, improve in age-related norms, and indicate a clinically significant change.
Intervention
The modified, group-based VR intervention aimed to decrease dizziness and motion sensitivity and improve gaze stability, functional balance, general activity levels, and the patient's HRQL. The intervention consisted of group sessions with guidance and individually modified VR exercises, a home exercise program (HEP), and an exercise diary (eAppendix 1). Two physical therapists experienced in vestibular and TBI rehabilitation were responsible for the intervention twice weekly for 8 weeks. The groups included 2 to 5 patients. The 2 weekly group sessions differed (Tab. 4). For both sessions, the VR exercises were individually modified. The circle training design in session 1 had stations that allowed patients to work individually, allowing them to skip stations they could not tolerate or did not need. In session 2, we focused more on general exercises for muscle conditioning and strengthening, and interactions between group members were stimulated by working in pairs and using balls and balloons for habituation and balancing tasks and exercises. The rationale for the exercises and examples of how the exercises were performed are shown in eAppendix 2.
Overview of Modified Vestibular Rehabilitation Intervention Program for Patients With Traumatic Brain Injury
The individual tailoring of exercises performed during the group sessions and in the HEP was based on symptoms, signs, and functional challenges at each patient's baseline and on the tentative underlying cause of their dizziness. The exercises typically comprised Brandt-Daroff exercises and maneuver treatment (Epley and Bar-B-Que Roll maneuvers1) for BPPV (patient 3), habituation exercises for motion sensitivity and central posttraumatic vertigo (patients 1 and 4), adaptation exercises for symptoms exhibited during eye-head coordination and reduced VOR (patient 2), and exercises for reduced balance focusing on improving sensory integration (all patients). The HEP was given at the beginning of the intervention and included 2 to 5 exercises. Additionally, the patients were encouraged to engage in physical activities that they tolerated, such as walking, swimming, or biking. The exercise diary was used to enhance awareness and motivation and to register the performed exercises and activities and the patients' responses to them. It was reviewed every week by the therapists.
Guidance sessions led by the physical therapists were held at the beginning of session 1. The guidance sessions were based on the patients' experiences, reflections, and active participation. The psychological aspect of recovery was promoted by information, confidence building, education, and reorientation. Furthermore, peer support was encouraged, and the group members shared experiences and provided emotional and practical support to each other. Increased self-efficacy was facilitated through a focus on positive experiences, gaining control by interpretation of physical and emotional symptoms, and strengthening the patients' beliefs in their own ability to reach their goals.14 The guidance sessions also were used to review the exercise diaries and discuss questions regarding goal setting, progression, and the HEP.
The parameters (intensity, frequency, duration) of the VR exercises were determined by the patients' subjective symptom level (headache, dizziness, fatigue). Feedback from each patient during the group sessions and the exercise diary was used to determine the parameters of the exercises throughout the intervention period. We practiced a conservative approach with a careful, gradual introduction to the exercises to avoid a prolonged increase of symptoms and a delayed response to treatment. If tolerated, the exercises were increased if symptoms increased the exercises, and activities were modified according to the symptom level.1,7 Resolution of increased symptoms within 15 to 30 minutes after the exercise session was used as a general guideline for modification and progression of the exercises.1 The symptoms were monitored by the patients' exercise diary descriptions of physical and psychological reactions to the exercises. Examples of progression and modifications are shown in Tables 5 and 6.
Elements in Systematic Progression of Exercises and General Parameters for the Intervention: Intensity, Frequency, and Duration for the Respective Exercise Categories
Elements of Systematic Modifications of the Intervention in Patients With Mild Traumatic Brain Injury
Outcome
The patients attended 8 to 15 sessions. Although none of the patients attended the maximum number of 16 (twice weekly for 8 weeks) sessions, they appeared motivated and positive. The patients worked with their HEP and reported gradually increased activity levels. There were no adverse effects, although some increase in symptoms was noted by all 4 patients during the first weeks of the intervention. Patients 1 and 2 tolerated a faster progression of the exercises than did patients 3 and 4.
Results from the standardized outcome measures are presented in Table 3. Perceived disability because of dizziness (DHI) changed from moderate disability to mild disability in patients 1 and 2 and from severe disability to moderate disability in patient 3 (>minimal important change).16 Patient 4's scores remained unchanged. Self-reported dizziness (VVS-SF) improved (>clinically significant change) for all but one patient (patient 4).18 Improvements were mainly observed on the vertigo balance subscale (VSS-V). Patients 3 and 4 still reported scores above the cutoff of ≥12 points on the VVS-SF, indicating severe dizziness.17 Postconcussion symptoms (RPQ) improved mainly on the physical subscale (RPQ-3) in patients 1 and 2, whereas patients 3 and 4 improved mainly on the psychological subscale (RPQ-13).
Health-related quality of life (QOLIBRI) improved in patients 2 and 3 from a score of approximately 40 to a score above 60. This finding was supported by measures on the HADS, which improved in all but one patient (patient 4), who showed a change to below the recommended cutoff point for possible psychological distress.21 The BESS test for standing balance indicated improvement (>minimal detectable change [MDC])24 in all but one patient (patient 4). Mobility and balance measured with the HiMAT showed that patient 2 improved by 8 points (>MDC),25 whereas patients 1 and 3 showed the same pretest and posttest mobility scores.
Discussion
The primary aim of this case series is to describe a group-based VR intervention for patients with TBI, as such descriptions are limited. The secondary aim is to indicate how the intervention may assist in addressing dizziness and balance problems by describing changes in self-perceived dizziness, balance, and HRQL.
The described intervention drew on the possible advantages of both group-based and individual approaches. The group-based approach benefited from interactive and social processes.14 It provided the patients with opportunities for indirect learning and peer support in addition to support, feedback, and information from the physical therapists.14 The patients identified common challenges (TBI, dizziness) and explored ways of coping with their situation, which yielded positive social relationships and increased motivation for physical activities.14 Moreover, the group-based approach was a favorable, less time-consuming approach that allowed therapists to treat several patients simultaneously. All patients in the present case series had mild TBI with different tentative underlying causes of their dizziness that were individually addressed during the intervention period. Improvements were shown in self-perceived dizziness, balance, and HRQL in 3 out of 4 patients, and there were no reports of adverse effects.
“Dizziness” is a nonspecific term that includes diffuse symptoms of disorientation and light-headedness, as well as more clear symptoms of vertigo and balance problems.4 Dizziness is subjective and difficult both for patients to describe and for clinicians to interpret. Hence, there have been several attempts to classify or categorize dizziness after TBI to simplify diagnostic information and guide therapeutic decision making.10,26 However, it may still be difficult to determine the underlying cause of dizziness. There may be overlap among categories of dizziness, and multiple causes of dizziness or vestibular dysfunction are found in 46% of patients after TBI.26,27 We did not have data on any vestibular function testing performed by ear-nose-throat specialists; therefore, specific vestibular diagnoses were not confirmed in our patients. However, based on the clinical assessment, they all appeared to have multiple causes for their dizziness or balance problems. In addition, the selection criteria for this case series were more symptom based, targeting deficits in function rather than specific diagnoses.
In a case series such as this, it is difficult to determine whether the observed improvements in outcomes are results of the intervention or due to other factors, such as natural recovery, participation in other treatments, or impact of greater attention from the therapists. However, different aspects of the intervention were designed to increase function and decrease symptoms, which were reported in 3 out of 4 patients in self-perceived disability because of dizziness (DHI) and frequency and severity of dizziness (VSS-SF). Motion sensitivity that was reported by all patients could be due to sensory conflicts or a mismatch among the visual, vestibular, and somatosensory systems, which is commonly observed after TBI.3 The intervention addressed symptoms of motion sensitivity by habituation that aimed to desensitize head and body motion sensitivity and reduce the pathologic response to motion.1,10,11 The intervention also provided the patients with coping strategies in daily life situations, such as walking in shopping centers, keeping their balance in the dark, and taking the bus, by the use of substitution exercises. In addition, by increasing awareness to challenges, the patients were gradually able to expose themselves to and take control of situations that provoked dizziness by the use of vision, proprioception, and attention.
Vestibular rehabilitation appears more effective in patients who have their headaches under control.10 All patients in the current case series used painkillers when needed and were able to control their headaches. Because several of the exercises involved movement of the head and neck, the patients had to tolerate such movements.7,11 Patients 1 and 4 had neck pain and reduced AROM. They were instructed to perform the VR exercises in a modified manner, within a pain-free AROM. Patients with severe neck pain may not do well with VR exercises until their neck problems are treated. Patient 1 saw a chiropractor for neck pain during the intervention, which might have increased the benefit of the VR intervention.
In patient 2, we found a positive DVAT, indicating impaired VOR. After TBI, impaired VOR may be due to both peripheral and central vestibular injury or dysfunction.7 Restoration of dynamic gaze stability was facilitated by the gaze stabilization exercises,1 and the DVAT was normalized during the intervention period.
The patient with BPPV (patient 3) is a reminder of its relatively common prevalence after TBI.28 Patients with TBI account for 5% to 28% of all cases of BPPV1,28 and, therefore, should be assessed for BPPV when complaining of vertigo or dizziness. Multiple canal involvement, such as combinations of PSC-BPPV and HSC-BPPV as in patient 3, does not appear to be more common after trauma.28 However, there are some indicators that traumatic BPPV can be more difficult to treat than idiopathic BPPV.28 Despite negative tests for BPPV after reposition maneuvers, our patient reported ongoing symptoms of dizziness, indicating other causes of dizziness in addition to BPPV, which is not uncommon after TBI.27
The poorer outcome for patient 4 might be explained by a higher symptom pressure at baseline and comorbidities. It also may be explained by the positive computed tomography scan, which indicated a more severe injury, and a possible combination of central posttraumatic vertigo and peripheral vestibular dysfunction. The central nervous system compensation associated with VR might take longer for patients with TBI due to central affection.11 Furthermore, postconcussion symptoms and concurrent physical, cognitive, and emotional disorders might disturb the natural recovery and central nervous system compensation of dizziness and balance problems after TBI.7 Based on this reasoning, patient 4 might have benefited from a prolonged VR intervention period. Gottshall10 described that many patients with TBI respond to VR over a period of 8 weeks. However, some patients, like patient 4, need a slower progression and might continue to improve over an additional 4 to 8 weeks.10 In our case series, however, the goal is to describe and examine the outcomes for an 8-week program.
The balance training addressed difficulties with reduced sensory integration and the visual dependency pattern seen in all 4 patients at baseline. This was done by focusing on balance exercises with eyes closed, promoting reliance on somatosensory and vestibular cues for balance, which might be attributed to the improved scores on the BESS test. Furthermore, the patients did not appear to have substantial difficulties with mobility measured with the HiMAT at baseline. This finding might be explained by the fact that the HiMAT does not specifically challenge the visual and vestibular systems, which might have been better assessed with the Dynamic Gait Index.1 Moreover, mobility tests such as the HiMAT and Dynamic Gait Index tend to have ceiling effects in the mild TBI population, which also can explain the minimal change on the HiMAT that was observed in this case series.25,29
It is documented that aerobic exercise training after TBI may reduce deconditioning, fatigue, and psychological distress.30 Thus, the increased activity level reported by all 4 patients might have contributed to the observed changes in several of the self-reported outcome measures. Additionally, psychological distress might be positively influenced by increased self-efficacy, confidence, and knowledge.8
To summarize, the modified group-based VR intervention appeared safe, viable, and beneficial when addressing dizziness and balance problems after TBI. We think the present case series might be useful for practitioners in tailoring VR interventions for patients with TBI and dizziness and balance problems. Future RCTs are warranted to evaluate short- and long-term effects of VR interventions in patients with TBI.
Footnotes
All authors provided concept/idea/project design and writing. Ms Kleffelgaard and Mrs Bruusgaard provided data collection. Ms Kleffelgaard and Dr Soberg provided data analysis and project management. Ms Kleffelgaard provided participants. Dr Soberg, Mrs Bruusgaard, Dr Tamber, and Dr Langhammer provided consultation (including review of manuscript before submission).
The study was approved by the Regional Committee for Medical Research Ethics in Norway (#2012/195b 20120306).
- Received February 23, 2015.
- Accepted November 5, 2015.
- © 2016 American Physical Therapy Association
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