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Effects of stabilizing reversal technique and vestibular rehabilitation exercise on dizziness and balance ability in patients with vestibular neuritis

Abstract Vestibular neuritis is a common disease of peripheral dizziness. Studies have shown that vestibular rehabilitation exercise (VRE) and proprioceptive neuromuscular facilitation (PNF) are effective to treat the symptoms of vestibular neuritis. However, the effect of VRE and PNF on the balance ability and dizziness in this patient cohort remains unclear. The aim of our observational study was to determine the changes in dizziness and balance ability of patients with vestibular neuritis who participated in the VRE program with stabilizing reversal technique (SRT). The reporting of this study conforms to the STROBE statement. Ten men and women aged ≥ 20 years who were diagnosed with vestibular neuritis were included. Patients performed VRE with SRT for 4 weeks with assistance from a therapist. VRE without SRT can also be performed at home. Dizziness was evaluated using the dizziness handicap inventory (DHI) and visual analog scale (VAS). Balance ability was assessed using the Berg's balance scale (BBS) and timed up and go test (TUG). At pre- and post-exercise, paired t test was performed to compare the within-group differences. After the program, DHI (45.40 ± 6.74 to 21.00 ± 7.07), VAS (5.90 ± 1.20 to 2.80 ± 0.92), BBS (45.10 ± 2.77 to 52.70 ± 1.83), and TUG (15.29 ± 1.13 to 12.06 ± 1.61) scores improved significantly in the VRE program group (P = .05). The VRE program combined with SRT was effective in reducing dizziness and increasing balance ability in patients with vestibular neuritis.


Introduction
Vestibular neuritis is the second most common disease of peripheral dizziness and occurs in approximately 7% of patients with dizziness. [1] Its incidence rate for 1 year is 11.7 to 15.5 per 100,000 people, with the highest frequency of occurrence in 40 to 50-year-old patients; unlike other types of peripheral dizziness, vestibular neuritis has the same occurrence in men and women. [2] Generally, vestibular neuritis invades the superior vestibular nerve. As a cause of occurrence, various hypotheses have been proposed. Of these, viral infection of the vestibular nervous system or ischemia of the internal ear is reported to be the cause of vestibular neuritis. [3] The viral infection hypothesis of the vestibular nervous system indicated that the antibody titer of herpes simplex virus, herpes zoster virus, cytomegalovirus, Epstein-Barr virus, rubella virus, adenovirus, and influenza virus is increased in the serological test of the patient. [4] However, evidence to support the development of peripheral vestibular neuritis due to viruses is lacking, and no virus has been proven to be a direct cause. The labyrinthine artery, which branches from the anterior inferior cerebellar artery, is divided into the common cochlear and anterior vestibular arteries. The anterior vestibular artery provides a similar blood flow to the semicircular canals (anterior, posterior, and horizontal) and macula of utricle, similar to the superior bronchus of the vestibular nerve. Vestibular neuritis and its clinical aspects are similar to cases of selective ischemia of the anterior vestibular artery. However, the possibility of selective ischemia of the anterior vestibular artery is not high, and hypacusis and brainstem symptoms are usually accompanied by extensive ischemia of the anterior inferior cerebellar artery region. [5] Therefore, the cause of vestibular neuritis remains unknown.
There is usually a quick decline in the clinical characteristics of vestibular neuritis within a few days owing to static vestibular imbalances, such as vertigo, nystagmus, ocular tilt reaction, and posture deviation. On the contrary, the disability caused by a dynamic vestibular imbalance, such as a nystagmus, induced by vibration stimulus, head thrust test, caloric test, and rotary chair test, persists for a long time. [6] Severe vertigo causing dysfunction has disappeared in 70% of patients with vestibular neuritis within 1 week (mean: 2-3 days), and severe vertigo in 2 weeks or more has been reported in 4% of the cases. [7] Vestibular neuritis is a disease diagnosed based on exclusion. Specific tests cannot diagnose vestibular neuritis. Therefore, it is diagnosed by synthesizing characteristic clinical aspects and several vestibular function test results. The caloric test can detect unilateral vestibular function loss. [8] The vestibular-evoked myogenic potential (VEMP) test is useful for distinguishing between the hypo-function of the vestibular organ and the superior and inferior vestibular nerves of vestibular neuritis. [9,10] A rotary chair test is useful for the early diagnosis of bilateral vestibular organ problems [11,12] ; in addition, a diagnosis of vestibular neuritis is made using the Romberg test, dynamic visual acuity, subjective visual vertical, bucket test, frenzel goggles, magnetic resonance imaging (MRI), and computed tomography (CT). [13] The mechanisms of spontaneous recovery, vestibular adaptation, and substitution are involved in the recovery from vestibular function disorders. It is associated with recovery during rehabilitation exercise. Spontaneous recovery occurs during nystagmus, skew deviation, and postural asymmetry. The vestibulo-ocular reflex and vestibulo-spinal reflex dysfunction recover naturally when there are peripheral vestibular function disorders. [14] The vestibular adaptation is due to the adaptability of the vestibular organ, in part, to recover its vestibulo-ocular reflex in peripheral vestibular disorder. This is the long-term adaptation of the vestibular system in response of the nervous system to information coming from the head movement. [15] Substitution is a vestibular function disorder that replaces the vestibular function with a body action that substitutes other functions, such as visual and somatosensory functions.
Moreover, problems in maintaining balance and dizziness due to dynamic vestibular imbalance persist in patients with vestibular neuritis. For recovery of these vestibular functions, adaptability through various external stimuli should be developed. It is necessary to further improve visual and somatosensory functions to replace vestibular function. Therefore, a method designed by Cawthorne and Cooksey for performing vestibular rehabilitation exercise (VRE) has been applied. [16,17] Proprioceptive neuromuscular facilitation (PNF) is a functional movement pattern in different directions, including flexion, extension, abduction, adduction, and rotation. PNF is an interventional concept that facilitates the motor response of the subject and enhances neuromuscular function and control using functional movement patterns and techniques. [18] The purpose of PNF is to enhance the functional movement through facilitation, inhibition, reinforcement, and relaxation of muscle groups. [19] Among the techniques of PNF, the stabilizing reversal technique (SRT) has been used for the purpose of enhancing posture stability and balance by inducing alternation or cocontraction of agonist and antagonist muscles without causing motion or movement against subject's resistance to a therapist. [19] Jung and Chung [20] showed that the hip joint strengthening exercise program, including SRT, improved the balance ability of traumatic brain injury patients. Cayco et al [21] reported that PNF, including SRT, was effective in improving the balance ability of the elderly with chronic stroke and in alleviating the fall risk.
Thus, studies have shown that PNF, including SRT, is effective in improving balance ability in patients with a brain injury. However, there have been only a few studies on the effect of VRE and SRT of PNF on the balance ability and dizziness on patients with vestibular neuritis. Therefore, this study aimed to determine the changes in dizziness and balance ability of patients with vestibular neuritis who participated in the VRE program combined with SRT of PNF.

Participants
Ten men and women aged 20 years who were diagnosed with vestibular neuritis by a doctor at the D hospital otolaryngology in J city from March 2019 to August 2019 and who received a VRE prescription were included in this study. A study flow diagram is presented in Figure 1. The diagnosis of vestibular neuritis was made when the following four diagnostic criteria for vestibular neuritis were met: rotational aquatic vertigo, nausea, and postural instability occurring within a matter of hours; when a horizontal spontaneous nystagmus with a rotational component on the physical examination appearing on the unaffected side, with the patient not reporting any central dizziness; the head impulse test on the lesion side showing eye saccade and smooth pursuit eye movement; and the caloric test showing more than 25% canal paresis on the lesion side.
The selection criteria for the patients in this study were as follows: those who were diagnosed with vestibular neuritis, who were first trained in VRE, and who were able to understand and respond to the questionnaire survey. Patients with previously diagnosed vestibular dysfunction with cochlear symptoms, such as tinnitus or acute sudden sensory neural hearing loss, are accompanied by cerebropathy, those diagnosed with dizziness (central, psychogenic, cervicogenic) other than vestibular neuritis, and those with limitation of movement due to a musculoskeletal disorder were excluded from the study. The general characteristics of the patients are presented in Table 1.

Intervention and procedure
The VRE program of this study was based on the devised VRE method of Cawthorne and Cooksey, [16,17] which combined the PNF concept. The details of VRE are as follows: In a 90-degree hook lying position, the participants performed superior/inferior and left/right eye movement slowly and then accelerating (A exercise). Then, the patients shifted their focus on their fingers and moved their head to the superior/inferior and left/ right sides slowly, then accelerating. Later, the exercise was performed with eyes closed (B exercise). At this time, the therapist placed a hand on the knee and applied the SRT to increase the trunk stability by instructing the patient to push against the therapist hands. Next, in the sitting and standing positions, the therapist stood behind the patient and placed his hand on the shoulder and performed A and B exercises with SRT. The balance walking exercise was performed with the patient's eyes opened and focusing on one target on the floor in front while walking; then, the next step was to focus on the target and walk with the eyes closed. Then, the patient was instructed is to imagine the focus on the target and move the head to the left/right and superior/inferior to perform a walking exercise. At this time, the therapist accompanied the patient to help them avoid falling down. All exercises with therapist assistance were performed for 30 minutes including break time, 3 times a week for 4 weeks. The patients were instructed to perform the VRE, without SRT, for 30 minutes a day for 4 weeks at home.

Outcome measurements
The dizziness handicap inventory (DHI) is a method for identifying the effects of dizziness and unsteady state on the quality of life of a person and to outcome subjective results that aid in quantification. DHI consists of 25 items in total (7 physical items, 9 emotional items, 9 functional items). The degree of disability is scored as follows: 4 for "Yes," 2 for "Sometimes," and 0 for "No." The total score ranges from 0 (no recognized disorders) to 100 (maximum recognized disorders). The questionnaire originated from the records of patients who reported dizziness. [22] Jacobson and Newman [22] confirmed high confidence between test and retest.
To measure the degree of dizziness, the subject was personally examined using a visual analog scale (VAS). A personal check was made on a piece of paper marked with 10 intervals with 0 for no dizziness and 10 for maximum dizziness. This test tool has a test-retest reliability [intraclass correlation coefficient (ICC) = 0.96]. [23] Berg's balance scale (BBS) is a tool for objectively evaluating static and dynamic balance ability, and it quantitatively evaluates balance ability and fall risk by directly observing performance of the elderly. [24] Fourteen items are assessed to determine the patients' ability to maintain balance through sitting, standing, and postural changes, and about 20 minutes are taken. If the items cannot be performed at minimum, 0 points are given, and for completely independent, the maximum of 4 points is noted, and the total points are 56. A score of 0 to 20 indicates a severe balance disorder, a score of 21 to 40 indicates a slight balance disorder, and a score of 41 to 56 indicates good balance ability. This tool has high validity, intra-rater reliability (ICC = 0.97), inter-rater reliability (ICC = 0.95-98), and test-retest reliability (ICC = 0.98). [25] Timed up and go test (TUG) is a tool for measuring mobility and balance quickly. The subject is seated on a chair with 46 cm high armrests. The subject is then signaled to get up from the chair, walk 3 m away from the chair, turn around, and then sit back down on the chair with a quick pace. The time taken by the subject to perform this task is then recorded. The average time was recorded by repeating the measurement three times. This test tool has intra-rater and inter-rater reliability (ICC = 0.98-0.99). [26]

Statistical analysis
Statistical analysis was performed using SPSS/PC Statistics 18.0 software for Windows (SPSS Inc., Chicago, IL). The paired t test was performed to compare the differences in dizziness and balance abilities in the experimental group before and after VRE. All statistical significance levels were set at a P value of less than .05.

Discussion
The purpose of VRE is to restore the activity of everyday life by improving the balance ability of patients with decreased vestibular function, promoting safety during walking and related movements, and reducing the symptoms of the patient, that is, dizziness. In this study, we investigated the effect of the VRE program with SRT of PNF on the dizziness and balance ability of patients with vestibular neuritis. The results of this study showed that there was a significant decrease in dizziness after VRE with SRT in the experimental group.
In the study by Sparrer et al [27] who divided their patients into the experimental group who performed customized exercise using the Nintendo Wii Balance Board with medication treatment, and a control group who performed exercise with medical treatment for patients with vestibular neuritis, a significant decrease in dizziness was observed in the experimental group, and the patients' return to everyday life was faster in the experimental group than in the control group. Crane and Schubert [28] showed an average decrease of 71% in dizziness after one month of implementing a computer-based adaptation of the vestibular rehabilitation program as compared to the traditional VRE. Preceding studies suggest that habituation exercises can reduce symptoms even if the same situation occurs by repeatedly performing various postures or situations in everyday life in which the patient's symptoms occur. This exercise usually involves the head or eyeball to reinforce adaptation of the vestibular organ. [14] In the VRE program of this study, adaptation was reinforced through head and eyeball exercises for various postures of the knee: the 90-degree hook lying position, sitting position, and standing position, suggesting that Table 2 Changes in 10MWT and functional strength before and after the treatment (N = 57).

Interaction (Group X Time) Group
Pre Mean ± SD (10MWT: 10 meter walk test, 5STST = 5-repetition sit-to-stand test). The significance levels were evaluated using the repeated ANOVA. Between-group differences at measurement independent t test. CG = control group, tDCSG = tDCS group. * P < .05.

Table 3
Changes in balance before and after the treatment (N = 57). dizziness was reduced. During the course of the exercise, subjects initially complained of dizziness multiple times, even although the repetition number of exercises was low during exercises performed for 30 minutes. However, in subsequent rehabilitation sessions, the symptoms of dizziness decreased, which led to the increased in performance frequency. This rehabilitation process is seen as a result of the reinforcement of adaptation. Halmagyi et al [29] reported that permanent loss of balance experienced by some patients after acute vestibular neuritis was due to compensation of inappropriate central nerves, incomplete peripheral recovery, and vestibular rehabilitation. However, Rossi-Izquierdo et al [30] found that vestibular rehabilitation was effective and safe for unstable patients, but there was no enough evidence to distinguish the effects of the different treatment regimens. Therefore, computerized dynamic posturography exercise was applied to the patients with chronic unilateral peripheral vestibular disorders. They were divided into one group with an intervention frequency of 10 and another group with an intervention frequency of 5. As a result, the limits of stability were improved in the group with the intervention frequency of 10. In addition, the group with the intervention frequency of 5 showed improved results, suggesting the need for 5 times more of intervention of vestibular rehabilitation in patients with peripheral vestibular disorder. In this study, the experimental groups performed the VRE with SRT 12 times and showed a significant improvement in balance ability after the exercise. The disequilibrium has no symptoms when the patient was lying or sitting down. However, when standing or walking, it is not centered, it collapses or staggers, and appears when there is an abnormality in motor control, such as vestibular spinal reflex, proprioception, and cerebellum. [31] The exercise method of this study recommends starting the VRE at the supine position, as this position has less symptoms of balance disorders. The disequilibrium was adapted through a postural change to the sitting position and then to the standing position, which gradually showed a balance disorder. In addition, the SRT, which is used to improve posture stability, is believed to improve the subject's balance ability by inducing alternation or co-contraction of the agonist and antagonist muscles during the postural change process. [19] In addition, the recovery of vestibular dysfunction has a function of substituting the body with other functions such as visual and somatosensory functions, thereby replacing the degraded vestibular function. In this study, it was considered that the balance ability was improved by improvement of visual and somatosensory functions through the application of head and eyeball exercises and alternate stimulation of the agonist and antagonist muscles by SRT. The application of SRT and VRE to patients with vestibular neuritis improved balance ability. On the basis of these results, SRT with the VRE program will more effectively improve the balance ability of elderly or nervous system patients with a balance disorder.
The limitation of this study was that it was difficult to gather subjects with vestibular neuritis, because of its low incidence rate compared with other diseases, which made it difficult for us to compare experimental and control groups. Therefore, the actual effect was not confirmed between the experimental and control groups. Exercise was performed only over a 4-week period with no follow-up. We believe that more detailed analysis of the age groups, the onset of symptoms, gender, weather, and other factors related to patients with vestibular neuritis will provide more meaningful information. Future studies should complement this limitation.

Conclusion
The VRE program with SRT was effective in reducing dizziness and improving the balance ability of patients with vestibular neuritis.