Evidence for Vestibular Sensory Reweighting and Improvement in Dynamic Posturography after Computerized Vestibular Retraining for Stable Unilateral Vestibular Deficit

Abstract

Balance deficits increase the risk of falls and compromise quality of life. This single group, interventional study assesses a computerized vestibular retraining protocol in patients with objectively determined unilateral peripheral vestibular deficits. Participants received twelve twice-weekly sessions of vestibular retraining guided by an interactive display. Objective posturography tests and questionnaires were administered before and after retraining. We enrolled 13 participants (5 females and 8 males) with a median age of 51 years (range 18 to 67). After retraining, the median change in sensory organization test (SOT) composite scores was 8.8 (95% CI, 0.6 to 19.1). The SOT visual (median change of 0.12 [-0.09 to 0.30]) and vestibular (0.10 [-0.06 to 0.25]) ratios improved but there was no change in the somatosensory or visual preference ratios. Participants with moderate-to-severe disability at baseline (n=7), as measured by Dizziness Handicap Inventory, had a larger magnitude of improvement (SOT composite 14.6 [7.0 to 36.9]; visual ratio 0.16 [0.09 to 0.39]; vestibular ratio 0.12 [0.08 to 0.28]). We found that computerized vestibular retraining is associated with improvement in dynamic balance performance for individuals with stable unilateral vestibular deficits, consistent with sensory substitution to vestibular organs. Posturography improvements correlated with reduced perceived fall risk. Clinicaltrials.gov registration NCT04875013; 06/05/2021

Introduction

Individuals with vestibular deficits have an elevated risk of falling[1] and the cost to society of falls is very high[2], leading to 3 million emergency visits and 30,000 deaths per year in the United States, for those over 65 years of age.[3] Peripheral vestibular disorders have a prevalence of approximately 1% in young adults climbing to over 6% for those over 70 years old[4,5] and most commonly arise due to factors such as trauma or infection.

The maintenance of dynamic equilibrium requires the sensation of orientation and acceleration (through vision, somatosensory, and vestibular senses), the processing of that information by the central vestibular system, and the coordinated response of ocular and musculoskeletal muscles in order to maintain a stable gaze and balanced posture, respectively. Proper weighting of these sensory inputs is required for maintenance of dynamic balance and conflict between inputs can lead to dizziness and motion sickness.[6,7] After vestibular injury, acute symptoms of spontaneous nystagmus and static imbalance usually resolve quickly without treatment; however, recovery of dynamic balance by vestibular compensation is slower and often incomplete.[8–10]

Various forms of rehabilitation have been demonstrated to promote compensation[11]; however, many patients still experience debilitating symptoms many months or years after onset, even with treatment. A minority of published studies report the fraction of subjects that fail to benefit from treatment; however, among those that do, between 1/3 and 2/3 of participants to fail to respond to rehabilitation interventions.[12–16]

Computerized dynamic posturography (CDP)-mediated tests, such as the sensory organization test (SOT) can quantify deficits in an individual’s ability to sense, integrate, and respond to challenges to equilibrium.[17,18] The SOT assesses capacity to maintain stable equilibrium across six testing conditions in which visual and somatosensory sensory inputs are systematically challenged, either by closing the eyes, or by conflicting sensory information provided by the instrument visual surround and support platform.[19] Ratios of scores between conditions can be used to infer how sensory information is being used to maintain postural stability, and how susceptible individuals are to inaccurate information.[7]

The SOT has been used to document decline in postural stability with age[20,21] and to measure response to rehabilitation interventions among patients experiencing dizziness.[22–26] SOT test scores also correlate with risk of falling.[27,28]

We have previously reported amelioration of participant-reported measures of vestibular disability after CDP-assisted retraining for this cohort. We found that CDP-assisted vestibular retraining was associated with clinically meaningful improvement, as measured by three questionnaires. The responses were consistent with reduced disability, improved balance confidence, and reduced fall risk, for those with moderate-to-severe disability.[29] In this study, we sought to assess objective changes in postural stability associated with computerized vestibular retraining.

Our hypothesis is that computerized vestibular retraining will be associated with increases in SOT composite scores and scores for SOT conditions 5 and 6 for patients with stable unilateral vestibular deficits.

Methods

Results

We enrolled 13 participants (8 men [62%]; median age 51 years [range 18 to 67 years]) with stable unilateral vestibular deficits. Five participants had a deficit on the left side and 9 on the right (one had an abnormal ocular VEMP on one side and an abnormal videonystagmogram on the other). Seven showed a vestibular deficit by bithermal caloric testing with normal VEMPs, 1 had abnormal cervical VEMP and ocular VEMP but normal videonystagmogram, and 5 had abnormal VEMP and videonystagmogram results (Table 1). All 13 completed the full course of retraining sessions and all follow up.

Before retraining, the participants in this study had a median SOM ratio of 1.00 (range 0.85 to 1.30), indicating intact ability to use somatosensory information to maintain equilibrium. SOM showed a negligible change of 0.01 (-0.06 to 0.04) after retraining. The median VIS ratio before retraining was 0.78 (0.46 to 1.05) changing by 0.12 (-0.09 to 0.30) after retraining. The initial VEST ratio was 0.68 (0.32 to 0.98) changing by 0.10 (-0.060 to 0.25). The PREF ratio was 0.96 (0.64 to 1.09) prior to retraining and changed negligibly by 0.02 (-0.04 to 0.12) after retraining (Table 2, Fig. 1B). 

Is baseline severity associated with outcome?

We have previously reported for this cohort that participants with moderate-to-severe vestibular disability at baseline (defined as DHI > 30), demonstrated improvement in self-reported measures of disability and balance confidence, while those with mild disability showed no change.[29] Thus, we sought to assess whether initial severity of participant-reported disability was associated with change in the objective posturographic measures.

There were six participants (3 men) with initial DHI ≤ 30 (median age 60 years [range 22 to 67]) and seven participants (5 men) with DHI > 30 (median age 41 years [range 18 to 65]). There was no difference in median change in scores for SOT conditions 1, 2, and 3 for either group (Fig. 2A). For SOT conditions 4, 5, and 6, and the SOT composite score, those with mild disability at baseline had modest, if any, improvement. However, among participants with initial DHI > 30, SOT conditions 4, 5, 6, and the composite score all increased significantly (Table 3, Fig. 2A). Among participants with initial DHI ≤ 30, 2 (33%) had improvement in SOT composite scores exceeding the MCID. Among those with initial DHI > 30, 6 participants (86%) showed improvements exceeding the MCID. The latter group demonstrated significant improvements in the VIS ratio (0.16 [0.09 to 0.39]) and VEST ratio (0.12 [0.08 to 0.28]) after retraining while the SOM and PREF ratios did not change (Table 3, Fig. 2B).

The correlation between changes in SOT composite scores and participant-reported measures was assessed by Spearman correlation. Changes in SOT after retraining correlated well with changes in FES-I (r_s -0.6472 [95% CI -0.8872 to -0.1316]). The correlation with change in the ABC score was less robust (r_s 0.5585 [-0.0075 to 0.8534]) and there was poor correlation with change in DHI (r_s -0.2545 [-0.7155 to 0.3609]).

Discussion

Patients with stable unilateral vestibular deficits are a difficult group in which to achieve satisfactory outcomes with common treatment modalities. Many individuals with acute vestibular pathology experience spontaneous amelioration of their symptoms without treatment[39–42]; however, despite some degree of spontaneous compensation in the weeks and up to three months after the onset of the deficit, many still exhibit symptoms of imbalance, adopt self-imposed limits on head movement, and are likely to struggle with difficult or dynamic balance tasks.[43]

There is strong evidence that some form of vestibular rehabilitation is better than none.[11,44] However, many patients do not achieve satisfactory outcomes from home-based or supervised exercises.[16,39,40] There is growing evidence that supporting rehabilitation with technologies that provide feedback on postural sway can improve balance and reduce postural sway[45]; however, in many cases, improvements in stability revert when the feedback support is removed.[10] Another technological adjunct for promoting vestibular compensation is CDP. There has been limited study of CDP-based interventions.[46–48] To our knowledge, changes in objective posturography associated with computerized vestibular retraining have not been reported for individuals with unilateral vestibular deficits.

For this study, we enrolled participants whose symptoms were persistent for greater than six months. This was to avoid confounding by spontaneous resolution in the acute phase. We also excluded patients with pathologies associated with a high rate of spontaneous resolution or that are associated with variable symptoms. Because our eligibility criteria required participants to be symptomatic at the time of enrolment, any naturally variable condition would have a high likelihood of experiencing transient amelioration of symptoms during follow up. By enrolling only those with stable symptoms lasting longer than six months, we hope to measure improvement associated with retraining rather than spontaneous resolution or cyclical variability. The majority (9 of 13) of these individuals had received previous vestibular physiotherapy without satisfactory outcomes.

The ability to maintain equilibrium when provided with conflicting sensory cues requires weighting of reliable cues over unreliable ones. Among those with a vestibular deficit, vision plays an important role in adaptation[10]; however, a study of patients recovering from unilateral vestibular neurectomy found some individuals rely more heavily on vision and others on somatosensory inputs.[9]

The individual conditions of the SOT challenge the participant to maintain equilibrium with a full complement of somatosensory, visual, and vestibular information and then systematically removes or creates sensory conflict with the somatosensory and visual information. Ratios of these scores indicate preference for one sensory input over another.

When the platform remained fixed (SOT conditions 1 to 3), allowing for reliable somatosensory information, median values were not significantly different from published normative data for individuals with no documented vestibular deficit.[21] These scores did not improve with CDP-assisted retraining. This is consistent with reports that show static balance frequently resolves spontaneously in days or weeks, whereas dynamic balance, which involves integrating sensory cues that may be in conflict, resolves slowly or incompletely.[9,42]

In contrast to the results with a fixed platform, activation of the sway-referenced platform (SOT conditions 4 to 6), significantly impacted the participants’ ability to maintain their balance prior to retraining. VIS and VEST ratios were significantly lower and highly variable between participants. When instructed to close their eyes on the sway referenced platform (condition 5), some participants performed the same or better than with their eyes open, while others performed markedly worse, suggesting that participants may have had different compensation strategies upon entering the study.

Scores for conditions 4 to 6 improved significantly after CDP-assisted retraining (Fig. 1A). Participants displayed a significantly smaller decrement in postural control on the sway referenced support surface compared to the fixed surface than they did prior to retraining (Table 2). This is consistent with improved capacity for dynamic balance.

The visual nature of the retraining exercises might suggest that computerized vestibular retraining leads to compensation by sensory substitution towards vision; however, we observed that participants were better able to tolerate absent visual information (eyes closed) or conflicting visual information (sway referenced visual surround) after retraining, demonstrating that their improved postural control was not reliant on visual information. Indeed, after treatment the PREF ratio was equivalent to 1 (1.01 [0.88 to 1.05]) indicating that participants were able to maintain their equilibrium as well with no visual information (eyes closed) as with sway referenced visuals. After retraining, SOT scores compared well with published age-matched values for individuals with no vestibular deficit.[21] The ranges and confidence intervals between participants, which had been very wide prior to retraining, decreased significantly.

Taken together, these findings suggest that after computerized vestibular retraining, participants were weighting information from their vestibular organs – either on the unaffected side or from intact organs on the affected side – over vision. Substitution to intact organs on the contralateral side is known to be an important mechanism of compensation for patients with unilateral deficits.[10] In addition, restoration of function of injured semicircular canals has been reported after vestibular neuritis.[49] Lacour posited that restoration of function after vestibular neuritis could come about by regeneration of peripheral sensory hair cells, from new afferents in the vestibular nerve, or by increased synaptic weight of remaining vestibular inputs.[9] Another potential mechanism for restoration comes from experiments in mice that showed the regeneration of hair cells after ablation with diphtheria toxin.[50,51] These data suggest that substitution to contralateral vestibular organs or restoration of ipsilateral function could contribute to compensation in our subjects; however, it is less well understood how common restoration is for patients with unilateral deficits and how important it is for compensation.

Horak found that well-compensated patients had lower vestibulo-ocular reflex gains than poorly compensated patients and suggested that residual, possibly distorted vestibular information was worse than none at all; however, those who learned to use remaining vestibular information from the intact ear performed better than those who relied heavily on visual and somatosensory cues.[10] Our data suggests that such learning was taking place for the participants in this study.

We have published participant-reported outcomes for this cohort in a separate paper.[29] We observed that participants with mild cases, as determined by a pre-treatment dizziness handicap inventory (DHI) score ≤ 30, experienced no measurable benefit from CDP-assisted retraining, as measured by three questionnaires. In the current report, participants with DHI scores ≤ 30, likewise, demonstrated only modest changes in objective posturography performance, whereas patients with pre-treatment DHI > 30 demonstrated significant improvements in the SOT composite score, as well as for the VIS and VEST ratios.

There is conflicting data in the literature about how well subjective patient-reported measures correlate with posturography results.[12,52,53] We found that prior to retraining, SOT composite scores correlated well with all three participant-reported measures, the DHI, the ABC scale, and the FES-I. Changes in the SOT composite scores after CDP-assisted retraining correlated well with changes in FES-I and less closely with the ABC scale. SOT scores did not correlate with the DHI. This may be because, while the FES-I and ABC measure perceptions around performing specific tasks such as walking on a slippery surface or reaching for objects, the DHI includes an emotional domain, as well as functional and physical parameters. It might be expected that emotional status would correlate less well with posturography measures than the task-based questions in the FES-I and ABC.

Participants in this study demonstrated improved postural stability in a dynamic test with conflicting visual and somatosensory cues and this improvement correlated with reduced FES-I scores, which measures perceived fall risk. We have also reported that computerized vestibular retraining is associated with a larger functional stability region – the area over which the center of mass can be displaced by leaning without causing loss of balance (manuscript under review). These three findings – the improved performance in the SOT, the reduced perceived fall risk, and the larger functional stability region – are all consistent with improved postural control and reduced risk of falls for patients with unilateral vestibular deficits.

Conclusions

Computerized vestibular retraining for individuals with stable unilateral vestibular deficits is associated with improvements in dynamic balance performance, specific to those with moderate-to-severe self-reported disability prior to retraining. Dynamic posturography changes were consistent with sensory substitution towards intact contralateral vestibular organs or recovery of function in ipsilateral organs. Posturography improvements correlated with decreased subjective assessments of fall risk.

Limitations

This study design did not include a waitlist, sham treatment, or alternative treatment control so we cannot estimate how much change in posturographic test results was due to factors other than the CDP intervention or how it compares to other treatment modalities. Further, we cannot conclude the increased postural stability in this controlled environment and decreased perceived fall risk will translate to real-world reduction in falls and improved function. We enrolled 13 participants and only seven of these displayed mild-to-moderate symptoms. Individuals with mild impairment showed no benefit but we cannot determine whether this was because of a ceiling effect of the SOT or whether those with mild impairment do not respond to this intervention. Age is known to be associated with vestibular function but the design of this study did not allow for estimation of the effect of age on vestibular outcomes. Improvement in SOT scores due to learned familiarity with the test has been reported.[38] This has been taken into account in determining the MCID we used in this study, but it is possible that some of the increase in participants’ scores after retraining may be due to a practice effect on the instrument. Subsequent studies would benefit from enrolling more participants and from limiting eligibility to those with moderate-to-severe impairment and randomizing participants to computerized vestibular retraining or a control intervention.

Declarations

Acknowledgement

The authors acknowledge Chris Cochrane, PhD, for contributions to study design, data analysis, and manuscript preparation; and Alex Gouvea, M.Aud, for technical help with participant assessments.

Author contributions

E.A.D. conceived and executed the study, screened and enrolled participants, and contributed to study design and manuscript preparation. N.S. contributed to study design and manuscript review. All authors reviewed the manuscript.

Competing interests

The author(s) declare no competing interests.

Data availability

De-identified data on vestibular diagnosis and sensory organization test scores are available from the corresponding author on reasonable request, for a period of 5 years after publication. In order to protect the privacy of participants, data on age and sex will not be shared.

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