Citation: Basta, D.; Rossi-Izquierdo, M.; Wonneberger, K.; Brugnera, C.; Bittar, R.S.M.; Greters, M.E.; Ernst, A.; Soto-Varela, A. Individualized Vibrotactile Neurofeedback Training in Patients with Chronic Bilateral
Abstract: Patients with bilateral vestibulopathy (BVP) suffer from postural imbalance during daily life conditions, which in turn leads to a high frequency of falls. Unfortunately, vestibular rehabilita- tion has only modest and somewhat inconsistent effects in this patient group. Approximately 50% of BVP patients show an improved postural control after conventional vestibular rehabilitation training. New and more promising approaches are required. The individualized vibrotactile neu- rofeedback training (IVNT) in stance and gait conditions has already been described as highly ef- fective in patients with various vestibular disorders. The purpose of the present multicenter study was to determine the efficacy of the IVNT in improving balance, reducing self-perceived disability, and improving gait in patients with confirmed BVP. In total, 22 patients performed the IVNT with the Vertiguard® system for 10 daily sessions. The dizziness handicap inventory (DHI), the stance stability score of the sensory organization test (SOT) and the score for everyday life mobility in stance and gait tasks (SBDT) were obtained immediately before and after the rehabilitation training period, as well as 3 and 12 months later. All measures improved significantly after the IVNT. Be- tween 77.3% and 94.4% of patients showed an individual benefit (depending on outcome measure). The effect was not significantly reduced within the follow-up period of 12 months. The results demonstrate a high efficacy of the IVNT for vestibular rehabilitation in BVP patients.
Bilateral vestibulopathy (BVP) is an epidemiologically rare disease. It occurs in ap- proximately 28 of 100.000 people [1]. However, the prevalence increases with increasing age (9% in ≥65 years, 12% in ≥80 years) [2]. When those patients have subjective, clinically relevant complaints, they usually suffer from postural imbalance and unsteadiness of gait during daily life conditions that worsens in darkness and on uneven ground. This in turn leads to a high frequency of falls. A recent study reported that 43% of BVP patients expe- rienced at least one fall within a 6-month period and 70% of them were recurrent fallers [3]. The percentage of falls in patients with BVP is significantly higher than in individuals with unilateral vestibular dysfunction [4]. Whilst 83% of patients with an uncompensated unilateral vestibulopathy (UVP) feel off-balance or unsteady, 58% of UVP patients have difficulty walking in the dark, 25% have difficulties walking on uneven surfaces, 8% have blurred vision when moving their head and 8% drift to the side when trying to walk straight, all these complaints occur in 100% of BVP patients [1]. There are typically no symptoms while sitting or lying under static conditions. Some patients also complain of oscillopsia while walking. The etiology of BVP remains largely unclear in about 50% of patients (“idiopathic”). Frequent known causes are ototoxicity (e.g., due to gentamicin) [5], bilateral Menière’s disease, autoimmune disorders, meningitis and bilateral vestibular schwannoma, as well as a combination with cerebellar degeneration (cerebellar ataxia, neuropathy, vestibular areflexia syndrome (CANVAS)) [6]. Unfortunately, in the long term, there is no improvement in vestibular function and there is currently no established causal medical treatment. The recent mainstay of treatment for patients with BVP is ves- tibular rehabilitation, which relies on central compensation and the reweighting of other sensory inputs [7]. Vestibular rehabilitation has been shown to be effective for numerous vestibular disorders but is less efficacious in BVP patients [8]. Vestibular rehabilitation has only modest and somewhat inconsistent effects on postural control in this patient group [9]. Approximately 50% of BVP patients show an improved postural control after conven- tional vestibular rehabilitation training [10,11]. There is only moderate evidence that adults with BVP improve their gait and postural stability following exercise-based vestib- ular rehabilitation [12]. In particular, no significant effect was found on gait speed [10,13]. This is especially important since gait speed strongly correlates with the risk of falls. It was suggested that the benefits of physical therapy are less substantial in BVP patients than in patients with other vestibular disorders because of multiple comorbidities and a slow progression in the severity of the vestibular loss [1]. Thus, the efficacy of vestibular rehabilitation in BVP patients requires improvement. There is some evidence for an in- creased efficiency of conventional rehabilitation, if combined with the continuous appli- cation of a noisy electrical (galvanic) stimulation (nGVS), in patients with a bilateral ves- tibular loss [14]. Improvements in postural control after vestibular rehabilitation tasks with nGVS may be due to an increased information throughput within the vestibular sys- tem, due to stochastic resonance.
Vestibular rehabilitation has the primary aim of promoting central compensation and, thus, improving balance function. The central compensation of vestibular deficits is essentially a physiological process, re-evaluating remaining, nonimpaired, or nonvestib- ular stimuli (e.g., the postural muscles, vision and proprioception) to maintain balance. Most rehabilitation programs should be started as early as possible and should include feedback mechanisms to speed up the adaptation and sensory substitution of the impaired vestibular function. The approach of vibrotactile neurofeedback training is to ensure nor- mal posture or balance even with reduced vestibular, visual or proprioceptive input, by conveying the missing information through tactile stimulation. The vibro-tactile sense is particularly well suited to this, as it is processed intuitively and leads to an involuntary correction of posture. Furthermore, the vibrotactile stimulus, in contrast to the visual or acoustic stimulus, does not impede the acquisition of information from the environment. There are two different approaches in general: one with a permanent vibration signal de- pending on the body sway and a second with a signal-like stimulation only when specific swaying ranges are exceeded. The first variant is implemented, for example, by a system (BalanceBelt®) that is recommended for permanent wear instead of vestibular rehabilita- tion training. Another system (VibroTactile®) uses signal stimulation only if specific fluc- tuation values are exceeded. These thresholds are specific to each direction of body sway and should be set by a therapist. The vibratory stimulation is applied on the waist. This system is only applicable during stance tasks on a force platform. The sway is calculated based on pressure measurements on the sole of the foot. In general, the vestibular rehabil- itation protocols should be individualized to provide the best possible outcome for the patients. The latest update of the Cochran Database of Systematic Reviews indicates that moderate to strong evidence exists to support vestibular rehabilitation training being ap- plied effectively for patients with unilateral peripheral vestibular dysfunction, with the highest evidence for individualized vibrotactile neurofeedback training (IVNT) in stance and gait tasks [15].
IVNT is an approach to improve and speed up vestibular rehabilitation in stance and gait conditions, which has already been described as highly effective in patients with var- ious vestibular disorders in randomized placebo-controlled double-blind studies. In pa- tients with multifactorial dizziness in old age, uncompensated unilateral vestibulopathies and in Parkinson’s patients, a significant reduction in body swaying and the risk of falls has been demonstrated [16–19]. The single device with vibratory feedback, which could be used for IVNT in stance and gait tasks, is currently the Vertiguard®-system. The feed- back thresholds are set by the system itself based on the patient’s age and sex, and the specific sensorimotor training condition.
Before the actual training, the patient completes a body sway analysis in everyday situations, with the body swaying being continuously measured close to the body’s center of gravity. This makes it possible to objectively identify and quantify the individual defi- cits in terms of the patient’s postural control. In the subsequent training, the patient should reduce the body sway in the conditions that are problematic with the help of the additional vibrotactile signal and thus improve the body balance in everyday life.
The purpose of the present multicenter study was to determine the efficacy of the individualized vibrotactile neurofeedback training (IVNT) in improving balance, reduc- ing self-perceived disability, and improving gait in patients with confirmed BVP.
All patients included in this study reported dizziness and instability under daily life conditions. The total study sample included 22 participants who had chronic, uncompen- sated bilateral vestibulopathy. Ten female and twelve male patients with a mean age of 67.4 ± 11.3 years participated in the study.
Vestibular testing included caloric testing (horizontal semicircular canal function), recording of cervical vestibular evoked myogenic potentials (cVEMP, saccular function), and analysis of subjective visual vertical (SVV, utricular function). Diagnosis of BVP was based on the slow-phase velocity of eye nystagmus (less than 6°/s during bithermal (44 °C and 30 °C) caloric irrigation) [20]. Absent cVEMP responses were found in 40.9% and path- ologic SVV-results in 27.3% of the patients. None of the participants showed severe non- vestibular sensory deficits (e.g., polyneuropathy), an acute vestibular disorder, or medi- cation that would actively influence the vestibular system (e.g., antivertiginosa). No other treatment was provided for balance disorders during the study period.
Interventions
Individualization of the rehabilitation program was based on a body sway analysis (mobile posturography) using the diagnostic function of the VertiGuard®-system (Zeisberg GmbH, Medingen, Germany). The device was mounted with a belt at the upper pelvis (iliac crest), close to the center of mass (Figure 1). Patients younger than 60 years performed the standard balance deficit test (SBDT). All other patients performed the ger- iatric standard balance deficit test (gSBDT). Both tests contain a set of 14 different every- day life stance and gait conditions [16,21]. The following tasks are included in the SBDT:
Standing on two legs with eyes open/closed;
Standing on one leg with eyes open/closed;
Eight tandem steps (one foot in front of the other) with eyes open;
Standing with two legs on a foam support surface (height 10 cm; density 25 kg/m3) with eyes open/closed;
Standing on one leg on a foam support surface;
Eight tandem steps on a foam support surface;
Walking 3 m while rotating the head;
Walking 3 m while vertically pitching the head in rhythm;
Walking 3 m forward with eyes open/closed;
Walking over four barriers (height 26 cm with an inter-barrier distance of 1 m).
The tasks “standing on one leg with eyes closed” and “standing on one leg on a foam support surface” were substituted by “stand up” and “sit down” in the gSBDT.
For all stance tasks, the measurement time was 20 s and as long as required for gait tasks. The results of the body sway analysis were compared with age- and sex-related normative values. The normative values are inbuilt in the VertiGuard®-system and were published previously [21]. The individualized training program for vestibular rehabilita- tion consisted of up to six SBDT/gSBDT tasks which showed the largest positive difference from the normative values [16].
Individualized training was performed daily under supervision over 2 weeks, result- ing in 10 sessions as the weekend was excluded. The feedback (rehab) mode of the Verti- Guard®-system was used for the training. A training session consisted of five repetitions of each selected training task. Each repetition took a maximum of 20 s. During training, participants received a vibrotactile feedback signal for those directions that showed a higher body sway than preset individual thresholds. The preset threshold for each train- ing task was related to the age and sex of the patient and could be modified in a limited range to adjust the feedback on the participant’s daily training performance. No vibrotac- tile feedback was applied if the participant’s sway was below a preset threshold.
Figure 1. Positioning of the VertiGuard®–system close to the center of body mass for posturography and vibrotactile vestibular rehabilitation. Four vibratory actuators (front, back, left and right) are placed on the belt together with the main device.
Outcome Measures
The primary outcome measure was the Dizziness Handicap Inventory (DHI) ques- tionnaire [22]. This questionnaire characterizes disabilities resulting from balance impair- ment, with scores ranging between 0 and 100. The maximum score represents the greatest disability. The DHI and all other outcome measures were obtained immediately before and after the rehabilitation training period, as well as 3 and 12 months later.
One secondary outcome measure was the SBDT/gSBDT composite score recorded without any feedback signal. The SBDT/gSBDT composite score, a risk-of-falling indica- tor, was calculated as the sum of ratios of all SBDT/gSBDT task scores to their age- and sex-related normative values in anterior/posterior and lateral directions. It was calculated by using the following formula:
This score is scaled between 0 and 100, where 100 represents the highest risk of falling and thus represents the lowest stability [21].
Furthermore, participants underwent the sensory organization test (SOT) on the an- kle-sway referenced platform BalanceMaster® (Nicolet Biomedical®, Clackamas, OR, USA), as an additional secondary outcome measure for stance stability under different sensorimotor conditions. Measurements were taken during three repeated 20 s runs under six sensorimotor standing conditions [23]. The following stance tasks were performed in the SOT: standing with eyes open/closed, standing with a moving surrounding, standing on a tilting platform with eyes open/closed, standing on a tilting platform with a moving surrounding. The SOT composite score is scored between 0 and 100, with the highest score indicating maximal stability.
Statistical Analysis
Pre- and post-training values of all outcome measures were compared using the t– test for dependent samples if they were normally distributed, whereas for non-normally distributed data, the Wilcoxon’s test was used. The Kolmogorov–Smirnov test was chosen for testing the data distribution. The level for significance of all tests was a p value less than 0.05. A similar procedure was applied for the data analysis of follow-up results. Since not all patients showed up for follow-up measures, the comparisons (pre, post, 3 months, 12 months) were only performed with results from patients who participated on all visits. A Bonferroni alpha-correction was applied for multiple comparisons.
A clinically relevant change could be surely assumed if the SBDT- or SOT-score in- creased or decreased by 10 points [21,23] or the DHI-score increased or decreased by 18 points [24], since these values are the largest differences between qualitative interpreta- tions.
3. Results
Comparison of the Pre-Post Rehabilitation Measures
Objective parameters such as SBDT and SOT scores, as well as subjective parameters such as DHI scores, were calculated before and after the training period (Figure 2).
Figure 2. Scores of the Dizziness Handicap Inventory (DHI), the Standard Balance Deficit Test (SBDT) and the Sensory Organization Test (SOT) before and after the individualized vibrotactile neurofeedback training (IVNT). Asterisks indicate a significant difference between pre- and post- rehab values.
The SBDT composite score before the training was 60.3 (±3.5), which decreased to 50.4 (±3.6) after the training. This improvement of 16.4% was statistically significant and17 out of 22 patients showed a reduction in the score. A significant improvement in the SOT composite score was found when comparing pre- and post-training results: 47.5 (±2.8) and 58.8 (±3.5), respectively. The percentage increase in stance stability was 23.7%. Only one tested patient showed no improvement. DHI scores following the training were de- creased: 55.1 (±4.6) pre-training to 34.7 (±4.0) post-training, with this change representing a statistically significant improvement of 37% (Figure 2). In total, 19 out of 22 patients showed a reduction in this primary outcome measure due to the IVNT. Only three patients showed nearly no change in the DHI-score after the training (Table 1).
Table 1. Individual scores of the Dizziness Handicap Inventory before and after the individualized vibrotactile neurofeedback training (IVNT) and the related difference (post- minus pre-scores).
Patient
DHI Pre-IVNT
DHI Post-IVNT
Delta DHI Post-Pre
1
70
44
−26
2
96
76
−20
3
72
62
−10
4
28
36
8
5
22
24
2
6
52
28
−24
7
76
26
−50
8
74
24
−50
9
24
12
−12
10
64
28
−36
11
42
22
−20
12
26
14
−12
13
54
41
−13
14
42
16
−26
15
28
24
−4
16
58
40
−18
17
62
16
−46
18
52
18
−34
19
72
60
−12
20
64
68
4
21
42
28
−14
22
92
56
−36
Follow-Up
Only ten patients participated in the 3- and 12-month visits. The data of all visits were analyzed for these patients separately (Figure 3). The SBDT composite score significantly decreased from 73.5 (±6.5) to 61.3 (±9.2) after the training (16.6% change) and remained stable during the next 12 months (62.5 ± 8.8 after 3 months and 63.0 ± 9.7 after 12 months). The SOT-score also showed a significant change from 38.2 ± 3.3 to 49.5 ± 4.9 after the training (22.9% change). There was a clear but not significant reduction in the score 3 and 12 months after the training (39.7 ± 4.0 after 3 months and 43.3 ± 4.2 after 12 months).
The DHI-score was not significantly changed, if compared before and after the train- ing (49.7 ± 8.9 before and 43.7 ± 7.3 after the training), after the training and 3 months later (40.7 ± 9.1) and between the next 9 months of the follow-up (38.7 ± 7.4). There was a sta- tistically significant decrease in the DHI-score by 22.1% between the pre-training values and the 12-month follow-up (Figure 3).
Figure 3. Scores of the Dizziness Handicap Inventory (DHI), the Standard Balance Deficit Test (SBDT) and the Sensory Organization Test (SOT) in patients which showed-up for the follow-up measures before and after the individualized vibrotactile neurofeedback training (IVNT) as well as 3 and 12 months later. Asterisks indicate a significant difference between the time points.
4. Discussion
A vestibular rehabilitation by IVNT over 10 days was able to significantly enhance the objectively determined postural control during stance and gait tasks. These improve- ments were found in both objective methods: the ankle sway referenced platform system and the sway measurement close to the center of gravity. Interestingly, not only significant group improvements were found. A total of 77.3% of all patients enhanced their postural
control on an individual basis during everyday life stance and gait tasks and 94.4% during different sensorimotor stance tasks. These values are much more pronounced than earlier reported for any other vestibular rehabilitation in BVP patients. Gillespie and Minor (1999) [10] reported 51% of patients showed improvement after a conventional vestibular rehabilitation and Herdmann et al. (2015) [9] reported between 38 and 86% (depending on the outcome measure). Interestingly, the latter study showed the highest success rate in functional tests (e.g., gait speed, dynamic visual acuity) and the lowest success rate in subjective scores. However, the increased stability of the patients in the present study was also reflected by a significant decrease in the subjectively reported dizziness handicap. This holds true as a group measure as well as on an individual basis. An individual de- crease in the DHI-score was observed in 86.4% of all treated patients. This is a higher rate of improvement compared to other studies. A recent study, which combined conventional vestibular training with noisy galvanic vestibular stimulation for treatment of bilateral vestibulopathy, failed to show a decrease in the DHI group value, even if the postural stability during stance tasks could be significantly improved [25]. Brown et al. (2001) [11] differentiated between the percentage of patients with a DHI improvement and the per- centage of patients with a clinically significant change in the DHI score. The minimal clin- ically significant change was defined as a change of 18 points. Unfortunately, the back- ground of this cut-off value was not further explained but is possibly related to the largest difference between qualitative interpretations [24]. Based on this criterion, 33% of all pa- tients in the study of Brown et al. (2001) [11] showed a clinically significant change of the DHI scores. In the present study, the rate of improvement as calculated due to Brown et al. (2001) [11] was 54%. This evidently demonstrates the superior efficacy of the IVNT as vestibular rehabilitation measure in BVP patients.
The follow-ups could only be performed in nearly half of the patients. These patients showed no significant group improvement in the subjective measure (DHI) directly after the training and 3 months later. Possibly, this is why they participated in the follow-up visits. The phenomenon, that mainly patients with subjective poor improvement show up for follow-up visits is well documented [16]. Surprisingly, these patients enhanced their objectively measured postural control in the present study directly after the IVNT. A sig- nificant increase of the subjective improvement was only found 12 months after the train- ing, even if the objective measures for postural control were nearly unchanged or not sig- nificantly worse meanwhile. These opposite results are possibly related to the patients’ expectations. The postural control was lower in these patients before the training, if com- pared to the entire group, and the improvement directly after the training was “only” similar. Since the DHI-scoring is not linearly related to the patient´s handicap (DHI; 16– 34 points = mild handicap, 36–52 points = moderate handicap, >54 points = severe handi- cap) [24], the next step of improved handicap perception was possibly not fulfilled directly after the training.
Anyway, all follow-up measures improved after the IVNT for at least 12 months, which would suggest that such a long-term effect is not directly related to the IVNT train- ing alone. The patients were probably mobilized and left their sedentary lifestyle since they were better able to maintain postural control during any physical activity. Thus, en- hanced physical activity should have contributed to the reported long-term benefit as well.
One limitation of the study is the lack of a control group. Adding a control group is always difficult in a study that investigates a rare disease. This was also shown in previous studies by the very limited numbers of patients in the experimental group and the controls (mainly below 10) [12]. This is a disadvantage for the statistical power of the study. How- ever, the absolute lack of any effect of a placebo application in the IVNT method (only performing the exercises without the vibrotactile stimuli) was already shown for a couple of other vestibular disorders [16]. Even if similar results are expected for BVP patients, future larger studies should include a control group (e.g., placebo).
5. Conclusions
The results of the current study show that BVP patients can be effectively rehabili- tated with the easy to perform IVNT method in stance and gait conditions. This holds true not only for the whole investigated sample, but also for almost all individual patients. One limitation of the method is that the patient should be able to perform at least some of the tasks included in the SBDT/gSBDT. This is analyzed by the body sway analysis, which always precedes the rehabilitation training.
Furthermore, there is some evidence that the single 10-day training could have a long-term effect that lasts at least 12 months. However, this should be further investigated in a larger sample of BVP patients with a clear record of individual physical activity.
Author Contributions: Conceptualization, D.B., A.E. and A.S.-V.; methodology, D.B. and A.S.-V.; validation, A.S.-V., M.R.-I. and R.S.M.B.; formal analysis, M.E.G. and D.B.; investigation, C.B., M.R.- I., D.B., A.S.-V. and K.W.; writing—original draft preparation, D.B.; writing—review and editing, A.E., M.R.-I., A.S.-V., C.B., K.W. and R.S.M.B.; visualization, D.B.; supervision, A.E.; project admin- istration, D.B. All authors have read and agreed to the published version of the manuscript.
Funding: This research received no external funding.
Institutional Review Board Statement: The Institutional Review Board approved the study proto- col (EA1/134/09) and the study was conducted in accordance with the Declaration of Helsinki on Ethical Principles for Medical Research Involving Human Subjects.
Informed Consent Statement: Informed consent was obtained from all subjects involved in the study.
Data Availability Statement: All data are available upon request from the corresponding author.
Conflicts of Interest: The authors declare no conflicts of interest.
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Validation of a comprehensive diagnostic algorithm for patients with acute vertigo and dizziness
Background and purpose: Vertigo and dizziness are common complaints in emergency departments and primary care, and pose major diagnostic challenges due to their various underlying etiologies. Most supportive diagnostic algorithms concentrate on either identifying cerebrovascular events (CVEs) or diagnosing specific vestibular disorders or are restricted to specific patient subgroups. The aim of the present study was to develop and validate a comprehenisve algorithm for identifying patients with CVE and classifying the most common vestibular disorders.
Methods: The study was conducted within the scope of the “PoiSe” project (Prevention, Online feedback, and Interdisciplinary Therapy of Acute Vestibular Syndromes by e-health). A three-level algorithm was developed according to international guidelines and scientific evidence, addressing both the detection of CVEs and the classification of non-vascular vestibular disorders (unilateral vestibulopathy, benign paroxysmal positional vertigo, vestibular paroxysmia, Menière’s disease, vestibular migraine, functional dizziness). The algorithm was validated in a prospectively collected dataset of 407 patients with acute vertigo and dizziness presenting to the Emergency Department at the Ludwig-Maximilian University of Munich.
Results: The algorithm assigned 287 of 407 patients to the correct diagnosis, corresponding to an overall accuracy of 71%. CVEs were identified with high sensitivity of 94%. The six most common vestibular disorders were classified with high specificity, above 95%. Random forest identified presence of a paresis, sensory loss, central ocular motor and vestibular signs (HINTS [head impulse test, nystagmus assessment, and test of skew deviation]), and older age as the most important variables indicating a cerebrovascular event.
Conclusions: The proposed diagnostic algorithm can correctly classify the most common vestibular disorders based on a comprehensive set of key questions and clinical examinations. It is easily applied, not limited to subgroups, and might therefore be transferred to broad clinical settings such as primary healthcare.
Apogeotropic Horizontal Canal Benign Paroxysmal Positional Vertigo: Zuma e Maia Maneuver versus Appiani Variant of Gufoni
AUTORES:
Marta Alvarez de Linera-Alperi
Octavio Garaycochea
Diego Calavia
David Terrasa
Nicolas Pérez-Fernández
Raquel Manrique-Huarte
ABSTRACT
Benign paroxysmal positional vertigo (BPPV) is one of the most common disorders that causes dizziness. The incidence of horizontal semicircular canal (HSC) BPPV ranges from 5% to 40.5% of the total number of BPPV cases diagnosed. Several studies have focused on establishing methods to treat BPPV caused by the apogeotropic variant of the HSC, namely, the Appiani maneuver (App). In 2016, a new maneuver was proposed: the Zuma e Maia maneuver (ZeM), based on inertia and gravity. The aim of this study is to analyze the efficacy of App versus ZeM in the resolution of episodes of BPPV produced by an affectation of the horizontal semicircular canal with apogeotropic nystagmus (Apo-HSC). A retrospective, quasi-experimental study was conducted. Patients attended in office (November 2014–February 2019) at a third-level hospital and underwent a vestibular otoneurology assessment. Those who were diagnosed with Apo-HSC, treated with App or ZeM, were included. To consider the efficacy of the maneuvers, the presence of symptoms and/or nystagmus at the first follow up was studied. Patients classified as “A” were those with no symptoms, no nystagmus; “A/N+”: no symptoms, nystagmus present during supine roll test; “S”: symptoms present. Previous history of BPPV and/or otic pathology and calcium levels were also compiled. From the 54 patients included, 74% were women. The average age was 69. Mean follow-up: 52.51 days. In those patients without previous history of BPPV (n = 35), the probability of being group “A” was 63% and 56% (p = 0.687) when treated with App and ZeM, respectively, while being “A/N+” was 79% and 87% for App and ZeM (p = 0.508). Of the 19 patients who had previous history of BPPV, 13% and 64% were group “A” when treated with App and ZeM (p = 0.043), and 25% and 82% were “A/N+” after App and ZeM, respectively (p = 0.021). In conclusion, for HSC cupulolithiasis, ZeM is more effective than App in those cases in which there is a history of previous episodes of BPPV (“A”: 64% (p = 0.043); “A/N+”: 82% (p = 0.021)).
Clinical Evaluation of Neck in Patients with Proprioceptive Cervicogenic Dizziness
Roseli Saraiva Moreira Bittar
Nédison Gomes Paim Alves
César Bertoldo Garcia
ABSTRACT
OBJECTIVE
To establish a functional connection between neck physical evaluations, dizziness discomfort and image findings among subjects diagnosed with proprioceptive cervical dizziness.
METHODS
After exclusion of peripheral vestibular disorders, 20 subjects with proprioceptive cervical dizziness hypothesis were selected. A Visual Analogue Scale (VAS) was used to quantify pain and vertigo. The active neck Range of Motion (ROM) and the Muscle Strength (MS) of the neck region were examined. The manipulation of vertebral bodies by the Maitland method and imaging scan were performed.
RESULTS
A positive correlation between pain and vertigo VAS scores was found. The ROM of the cervical spine was limited and vertebral joint movement was restricted, especially at C3 and C5. No loss of MS was noticed.
CONCLUSIONS
Proprioceptive cervical dizziness is usually an exclusion diagnosis among episodic chronic vertigos. Characteristically, it is reported by patients as instability or vertigo in crises. It is directly related to the neck ache severity and worsens with neck movements. The common pattern on clinical examination includes restriction and pain during neck flexion without loss of MS. Reduction of joint mobility and pain are also observed, especially at C3 and C54 kHz.
Veja o texto completo em: https://www.tinnitusjournal.com/articles/clinical-evaluation-of-neck-in-patients-with-proprioceptive-cervicogenic-dizziness-18980.html
Vestibular recruitment: new application for an old concept
Roseli Saraiva Moreira Bittar
RaquelMezzalira
Alice Carolina Mataruco Ramos
Gabriel Henrique Risso
Danilo Martin Real
Signe Schuster Grasel
Highlights
Post caloric recruitment index is the ratio of the angular velocity of the slow phase obtained by cold and warm caloric stimulation of the same ear.
The normal value was established in 17.06%.
Post caloric recruitment index is useful to identify the affected ear separately.
Recruitment suggests that central compensation is not complete yet in individuals with vestibular symptoms and peripheral lesion.
Abstract
Introduction
Vestibular recruitment is a sign of hyperexcitability of central vestibular neurons and may be characteristic of peripheral vestibular damage.
Objective
To define the post-caloric recruitment index and its ability to predict the stage of vestibular compensation and peripheral lesion.
Methods
First of all, we demonstrated that larger values in the cold post-caloric stimulation compared to warm stimulation were equivalent to vestibular recruitment observed during the sinusoidal harmonic acceleration test. In the next step, patients with vestibular complaints and asymptomatic controls were submitted to the caloric test. We calculated post-caloric recruitment index for the control group. Among the study group, we analyzed the relation between post-caloric recruitment and unilateral weakness as well as the types of vestibular diagnoses.
Results
Mean post-caloric recruitment was 17.06% and 33.37% among the control and study group, respectively. The ratio between post-caloric recruitment and unilateral weakness was 1.3 in the study group. Among recruiting subjects, no significant difference of unilateral weakness from the lesioned or healthy side was observed. We found no differences in vestibular diagnoses between recruiting and non-recruiting subjects.
Conclusion
Post-caloric recruitment index identified asymmetric vestibular tonus and central compensation. The normal value was established at 17.06%.
Few of us are strangers to dizziness. As with pain, to equivocate about being dizzy is to cast doubt on one’s mastery of the language, not to express uncertainty about the experience. The practiced ease of first-person use, however, conceals great difficulty in defining the criteria for correct ascription from which a clear picture of the symptom can be derived, and on which close scientific investigation is inevitably premised.
By “dizzy” a patient may mean any one—or combination—of vertigo, oscillopsia, light-headedness, spatial disorientation, or unsteadiness (1). Though primarily perceptual, the experience is commonly coupled with an incapacity to act or move appropriately, creating a complex sensorimotor blend. Superimposed is an emotional reaction to the profound dysfunction the patient takes the symptoms to imply. How do we decompose so polymorphous a phenomenon; what dependencies can we establish between its components; and how do we relate them to the underlying neural substrate, in health and disease? These are the questions we wish to answer: we shall see we must be wary of the answers they immediately prompt in us, for intuition is here misleading.
The Nature of Dizziness
Prima facie, dizziness has perceptual, motor, and emotional components. Let us take each in turn.
Perceptual
It is natural to think of dizziness as an abnormal sensation of body movement in space. If so, it ought to be dependent on the integrity of a perceptual power. The blind cannot be dazzled by headlights; the deaf startled by a bang; the anosmic overwhelmed by perfume. And if the deficit is congenital, then these experiences are logically proscribed, for there is no framework within which their expression could have been learnt (2). But what sensory modality must a patient lack to be incapable of dizziness?
It cannot be the vestibular sense, for the kind of illusory head motion commonly associated with vertigo falls within the repertoire of normal motion as registered by the vestibular system alone. Moreover, inactivation—partial or complete—of the vestibular system does not attenuate or prevent dizziness (although patients may not experience rotational vertigo) but amplifies or causes it (3, 4). It cannot be vision either, for the same reasons: the visual correlates of dizziness are typically replicable without it, and though an image, especially a moving image, may trigger vertigo, closing one’s eyes does not universally abolish it (5). The experiential volume of proprioception is arguably too weak to carry so vivid an experience, but the same arguments apply in any event.
So the perceptual aspect of dizziness is not explicable by any single perceptual modality. Rather it requires the interaction of at least two, as classically illustrated by the caloric reflex test. Here artificial stimulation of the vestibular apparatus using water at varying temperatures creates a discrepancy between artificially stimulated vestibular and intact visual signals, generating nystagmus accompanied by vertigo (6). Removing visual input by closing one’s eyes attenuates the experience but does not abolish it, for proprioceptive signals remain at odds.
Examples of other multi-modal combinations are easy to give. But what is the nature of the critical cross-modal interaction? A cross-modal comparison can never be direct, for the signals of each modality are definitionally different. But we can compare the circumstances under which a given perceptual signal is obtained: here typically a coherent pattern of motion of the eyes and head. Dizziness generally arises where the associated circumstances—real or merely predicted—are discordant. Crucially, it is the mere presence of discordance—not its direction, quality, or magnitude—that evokes the experience (7). To the extent to which dizziness is perceptual it is meta-perceptual, superordinate on the sensory modalities whose discordance it registers. This places it in a unique experiential category: an indicator of the cross-modal coherence referenced to the body. We cannot easily construe it on the model of simple sensations, for its perceptual aspect is sui generis.
Motor
Any experience involving the perception of movement is bound to exhibit a motor aspect (8). Though affordance is widely assumed to be specific to the spatial properties of objects of action (9), there are no grounds for believing it must be so limited. Indeed, if action is to be responsive to the spatiotemporal continuity of the environment, affordance must extend both to the subject, and across time (10). If I erroneously perceive myself to be falling backwards, then when I make no corresponding motor response it is only because I have deliberately suppressed it in the realization the perception is illusory. Here the motor system is naturally activated downstream of an afferent signal—the movement, or suppressed movement is reactive—but its contribution to the experience need not be secondary.
Nowhere are action and perception more entangled than in the visual system. The primary objective of eye movements is to maintain a tight coherence of gaze and environmental salience over time (5). The global, background shift implied by a perception of self-motion—illusory or real—cannot but activate the oculomotor system, which must act automatically to stabilize an image that would otherwise become uninterpretable (11). Indeed, it is on the oculomotor system that the cross-modal comparison between the visual and the vestibular depends. The vestibular system needs to integrate multimodal signals to determine where the head is in space, and to where our gaze should be directed.
In short, collateral motor phenomena—present or merely expected—accompanying the perception of motion create a motor aspect that is impossible to ignore, and whose contribution to the experience cannot be discounted merely for being subordinate to the perceptual.
Emotional
Dizziness is characteristically accompanied by a visceral response far removed from its causal locus: nausea and vomiting. If a maladaptive instinctual reaction can be so prominent here, why could it not extend into the emotional realm, where rationality plausibly has a firmer purchase? The spatial disorientation often accompanying dizziness creates a sensory discordance that rightly generates instinctually-mediated distress (12). Again, that the emotional response is here reactive does not allow us to disentangle it from the rest of the experience, for its qualities may be peculiar to these circumstances. For example, a patient with benign paroxysmal positional vertigo [BPPV] usually not only has vertigo, but a consequent sense of loss of control. This creates secondary emotional symptoms—derealization and depersonalization—reflecting a radical redescription of the environment and the patient’s interaction with it (13). Indeed, the secondary emotional disturbance may dominate the clinical landscape, resulting in a patient with dizziness receiving a primary diagnosis of anxiety (14, 15).
The diagnosis and management of vertigo remains a challenge for clinicians, including general neurology. In recent years there have been advances in the understanding of established vestibular syndromes, and the development of treatments for existing vestibular diagnoses. In this ‘update’ I will review how our understanding of previously “unexplained” dizziness in the elderly is changing, explore novel insights into the pathophysiology of vestibular migraine, and its relationship to the newly coined term ‘persistent postural perceptual dizziness’, and finally discuss how a simple bedside oculomotor assessment may help identify vestibular presentations of stroke.
Introduction
The world of dizziness has experienced a dramatic change over the last 3 decades, as new treatable syndromes have been identified, and novel treatments developed for existing vestibular diagnoses. Despite such progress, many clinicians, including neurologists, admit to a lack of confidence in the diagnosis and management of the dizzy patient, leading to circuitous patient journeys, from one specialty to another. Most emergency and primary care ‘dizzy’ referrals in the UK are fielded to ENT surgeons, a departure from neuro towards otology, although it could be argued that vertigo is a neurological symptom, a cortically driven percept, irrespective of the causative insult.
One common challenge in the field is elderly patients reporting a vague sense of dizziness and imbalance, who as a result of normal audiovestibular testing, remain “unexplained”. I will review recent evidence suggesting possible mechanisms relating to small vessel disease that may contribute to this syndrome. Whilst new variants of benign paroxysmal positional vertigo (BPPV) have been recently described [1], the Epley and Semont treatment manoeuvres for the commonest type of BPPV are still not universally employed by neurologists [2], and BPPV remains under-diagnosed, and under-treated. The commonest differential diagnosis for BPPV is vestibular migraine, a condition that is increasingly recognised outside specialist centres, but remains under-diagnosed. Here, I review the most recent advances in vestibular migraine (VM) diagnosis and treatment. VM in turn is a common precursor to a more chronic form of dizziness recently renamed persistent postural perceptual dizziness (PPPD), and there has been a growth in the unravelling of the neurobiology of this disorder. Finally, vestibular neurology is rich in clinical bedside skills; indeed, an evaluation of eye movements may more precisely identify and localise a stroke than state-of-the-art imaging [3]. I describe and review the use and utility of the HINTS examination in stroke.
Cerebral Responses to Stationary Emotional Stimuli Measured by fMRI in Women with Persistent Postural-Perceptual Dizziness
Eliane Maria Dias von Söhsten Lins
Roseli Saraiva Moreira Bittar
Paulo Rodrigo Bazán
Edson Amaro Júnior
Jeffrey Paul Staab
Abstract
Introduction Persistent postural-perceptual dizziness (PPPD) is a functional vestibular disorder characterized by chronic dizziness, unsteadiness, and hypersensitivity to
motion. Preexisting anxiety disorders and neurotic personality traits confer vulnerability to PPPD. High anxiety during acute vertigo or dizziness incites it. A functional
magnetic resonance imaging (fMRI) study of chronic subjective dizziness found unexpectedly hypoactive responses to vestibular stimulation in cortical regions that
integrate threat assessment and spatial perception. Objective This fMRI study used non-moving, but emotionally charged visual stimuli to investigate the brain’s activity of PPPD patients and control subjects. Methods The participants included 16 women with PPPD and 16 age-matched women who recovered completely from acute episodes of vertigo or dizziness capable of triggering
PPPD. Brain responses to positive, neutral, and negative figures from the International Affective Picture System were measured with fMRI and compared between the groups.
Dizziness handicap, anxiety, and depression were assessed with validated questionnaires. Results Between group analyses: Participants with PPPD showed reduced activity in anterior cingulate cortex and increased activity in left angular gyrus in response to
negative versus positive stimuli, which was not observed in recovered individuals. Within group analyses: Participants with PPPD had increased activity in visuospatial areas (parahippocampal gyrus, intraparietal sulcus) in negative versus positive and
negative versus neutral contrasts, whereas recovered individuals had increased activity in anxiety regions (amygdala, orbitofrontal cortex). Conclusion Patients with PPPD may be more attuned to spatial elements than to the content of emotionally charged visual stimuli.
The CT was described in the early twentieth century by Robert Bárány, who received the Nobel Prize for his achievement, considering its clinical importance for the diagnosis of vestibular diseases.1 It remains the only functional test capable of isolating the stimulated side. The head impulse test (HIT), described at the end of the century, is a remarkable demonstration of how to easily and reliably observe the vestibulo-ocular reflex (VOR) performance.2 The documentation by computer programs came after the clinical description in both cases. The fact that one test was described before and the other after does not interfere with its clinical indication and applicability.
Regarding the discomfort caused by the test, the argument does not resist a more detailed assessment. As an example, one can report cases of migraine patients in whom both CT and vHIT cause great discomfort, sometimes triggering the crisis on subsequent days. Some do not even tolerate the vHIT mask, let alone the cephalic impulses. However, most patients tolerate both tests well. What drives the test indication is its benefit in attaining the final diagnosis3 and not whether it is uncomfortable or not. Or does anyone doubt that a mammogram is a fundamental diagnostic exam, although highly painful and uncomfortable?
There have been discussions regarding the stimulation mechanism caused by CT in the labyrinth cells. Since its description, there have been hypotheses about how the temperature acts on the ampullary crest and inferences about the stimulated cell type. There are still doubts as to whether the result is caused by functional, structural damage or even hair cell integrity. That is a fact, and much remains to be studied, but the question that really matters is what CT adds to the final diagnosis.
With the increase in practical knowledge, we now know that in some cases, such as in Meniere’s Disease, the alteration in the CT together with a normal vHIT is highly suggestive of the diagnosis.4 This is what matters: how much these data can help you establish the best way to manage your patient.
Although these are two forms of VOR documentation, the stimuli used are different. In CT, the stimulus is the variation in temperature and in the vHIT, the stimulus is mechanical (cephalic impulse). Both methods have limitations. In CT, the stimulus is unilateral and of low frequency and in the vHIT, the stimulation is bilateral and occurs in response to higher velocities. The high-velocity impulses in vHIT are necessary to isolate the vestibular reflex, while at low frequencies it is influenced by visual information. The examination allows documenting vertical movements, although these records are more subject to artifacts.
We see the tests as distinct evaluations to obtain response from ampullary crests – functional units of angular movements.5 The tests complement each other and may be ordered together or separately, depending on their usefulness for attaining the diagnosis.
If the question is “Does the vHIT replace the CT”, the answer is no. It is up to the physician to choose which test should be requested for their patient, introduced in their diagnostic routine and whether they will be submitted to one or both, which will be carried out before or after. There is no right or wrong: the way the physician is more comfortable when performing his diagnostic evaluation should guide the choice of diagnostic testing.
We have received recurring questions from colleagues and students about the substitution of the caloric test (CT) by the video impulse test (vHIT). Two reasons are often used to justify the change: 1) the CT dates from the early twentieth century and 2) the test is uncomfortable; the vHIT, in turn, is a recent test and causes minimal discomfort. As scientists, we must state our opinions always based on physiological foundations.
The CT was described in the early twentieth century by Robert Bárány, who received the Nobel Prize for his achievement, considering its clinical importance for the diagnosis of vestibular diseases.1 It remains the only functional test capable of isolating the stimulated side. The head impulse test (HIT), described at the end of the century, is a remarkable demonstration of how to easily and reliably observe the vestibulo-ocular reflex (VOR) performance.2 The documentation by computer programs came after the clinical description in both cases. The fact that one test was described before and the other after does not interfere with its clinical indication and applicability.
Regarding the discomfort caused by the test, the argument does not resist a more detailed assessment. As an example, one can report cases of migraine patients in whom both CT and vHIT cause great discomfort, sometimes triggering the crisis on subsequent days. Some do not even tolerate the vHIT mask, let alone the cephalic impulses. However, most patients tolerate both tests well. What drives the test indication is its benefit in attaining the final diagnosis3 and not whether it is uncomfortable or not. Or does anyone doubt that a mammogram is a fundamental diagnostic exam, although highly painful and uncomfortable?
There have been discussions regarding the stimulation mechanism caused by CT in the labyrinth cells. Since its description, there have been hypotheses about how the temperature acts on the ampullary crest and inferences about the stimulated cell type. There are still doubts as to whether the result is caused by functional, structural damage or even hair cell integrity. That is a fact, and much remains to be studied, but the question that really matters is what CT adds to the final diagnosis.
With the increase in practical knowledge, we now know that in some cases, such as in Meniere’s Disease, the alteration in the CT together with a normal vHIT is highly suggestive of the diagnosis.4 This is what matters: how much these data can help you establish the best way to manage your patient.
Although these are two forms of VOR documentation, the stimuli used are different. In CT, the stimulus is the variation in temperature and in the vHIT, the stimulus is mechanical (cephalic impulse). Both methods have limitations. In CT, the stimulus is unilateral and of low frequency and in the vHIT, the stimulation is bilateral and occurs in response to higher velocities. The high-velocity impulses in vHIT are necessary to isolate the vestibular reflex, while at low frequencies it is influenced by visual information. The examination allows documenting vertical movements, although these records are more subject to artifacts.
We see the tests as distinct evaluations to obtain response from ampullary crests – functional units of angular movements.5 The tests complement each other and may be ordered together or separately, depending on their usefulness for attaining the diagnosis.
If the question is “Does the vHIT replace the CT”, the answer is no. It is up to the physician to choose which test should be requested for their patient, introduced in their diagnostic routine and whether they will be submitted to one or both, which will be carried out before or after. There is no right or wrong: the way the physician is more comfortable when performing his diagnostic evaluation should guide the choice of diagnostic testing.
References
Lopez C, Blanke O. Nobel prize Nobel Prize centenary: Robert Bárány and the vestibular system. Curr Biol. 2014;24:R1026—8.
Halmagyi GM, Curthoys IS. A clinical sign of canal paresis. Arch Neurol. 1988;45:737—9.
Salman FA, Issam S. Video head impulse test: a review of the literature. Eur Arch Otorhinolaryngol. 2017;274:1215—22.
Hannigan IP, Welgampola MS, Watson SRD. Dissociation of caloric and head impulse tests: a marker of Meniere’s disease. J Neurol. 2019, http://dx.doi.org/10.1007/s00415-019-09431-9 [Epub ahead of print].
Mezzalira R, Bittar RSM, do Carmo Bilécki-Stipsky MM, Brugnera C, Grasel SS. Sensitivity of caloric test and video head impulse as screening test for chronic vestibular complaints. Clinics (Sao Paulo). 2017;72:469—73.
