Abstract
BACKGROUND AND OBJECTIVES:
Acute vestibular syndrome is highly disabling in physical and psychological stress of patients. The aim of this study was to evaluate the effects of perioperative vestibular dysfunction in patients who received unilateral vestibular schwannoma (VS) surgery as unilateral acute vestibular dysfunction model cases and to study the vestibular compensation process in these patients.
METHODS:
The 101 participants with unilateral VS had received a series vestibular function tests including subjective visual vertical/horizontal (SVV/SVH), caloric test, cervical vestibular-evoked myogenic potentials, ocular VEMP, and video head impulse test within 3 months before surgery. SVV, SVH, and Visual Analog Scale for vertigo were evaluated on the first day (postoperative day 1, POD 1), on the third day (POD 3), on the 7 day (POD 7), in the first month (POD 30), and in the third month (POD 90) of postoperative follow-up visit.
RESULTS:
The tilts of SVV and SVH significantly increased after surgery compared with baseline on POD 1, POD 3, and POD 7. The SVV of the participants had recovered to the preoperative level on POD 30, and the SVH of the participants had recovered to the preoperative level on POD 90. The changes of SVV/SVH were significantly correlated with changes of Visual Analog Scale for vertigo within 90 days. After surgery, the tilts of SVV and SVH within 7 days were significantly higher in patients with normal caloric tests and video head impulse test than those with abnormal results in these 2 tests.
CONCLUSION:
Static vestibular function may recover effectively within 1 month after surgery in VS, which was positively correlated to the recovery of subjective dizziness. Patients with preoperative vestibular dysfunction may recover sooner and better in the process of vestibular compensation in the early postoperative stage compared with those with normal preoperative vestibular function.
KEY WORDS: Acute vestibular dysfunction, Vestibular schwannoma, Subjective visual vertical, Subjective visual horizontal, Vestibular compensation
ABBREVIATIONS:
- AVD
acute vestibular dysfunction
- cVEMP
cervical vestibular-evoked myogenic potentials
- DHI
Dizziness Handicap Inventory
- FGA
Functional Gait Assessment
- MD
mean difference
- oVEMP
ocular VEMP
- PTA
pure-tone audiometry
- SVH
0° SVH value at upright head position
- SVH
subjective visual horizontal
- SVH-Contra
SVH value for the head tilted to the contralateral side of the affected ear
- SVH-Ipsi
SVH value for the head tilted 30° to the ipsilateral side of the affected ear
- SVV 0°
SVV value at upright head position
- SVV
subjective visual vertical
- SVV-Contra
SVV value for the head tilted to the contralateral side of the affected ear
- SVV-Ipsi
SVV value for the head tilted 30° to the ipsilateral side of the affected ear
- VAS-T
VAS for tinnitus
- VAS-V
VAS for vertigo
- VC
vestibular compensation
- VFTs
vestibular function tests
- vHIT
video head impulse test
- VS
vestibular schwannoma.
Acute vestibular dysfunction (AVD) dramatically affects gaze stability and balance body control, significantly negatively affecting the patient's quality of life. Patients who received vestibular schwannoma (VS) resection surgery may suffer from such AVD syndrome.1,2 VS is a benign, slow-growing tumor originating from the Schwann cells of the vestibular nerve, resulting in chronic vestibular dysfunction.3 Surgical resection stands as one of the leading management options for individuals with large or symptomatic VS.4 After tumor removal with apparent damage to the vestibular nerve, many patients may experience sudden vestibular deafferentation, leading to a series of AVD syndromes such as vertigo, disequilibrium, and nausea.1,2 The sudden damage of unilateral vestibular nerve function caused by surgical resection makes postsurgical VS an ideal model for studying the impact of acute unilateral vestibular dysfunction and subsequent vestibular compensation (VC).
Fortunately, AVD syndrome and persistent dizziness can be ameliorated within 3 months in most patients by VC.2 The complex processes of VC were considered to include the plastic neural protection and structural reorganization, rebalance of vestibular nuclei activity, and sensory and behavioral substitutions of vestibular, visual, and somatosensory cues.5,6 Over the past century, advancements in the management of VS have emphasized the quality of life and low expected disability in patients.7,8 Therefore, postoperative balance recovery strategies warrant further investigation in VS patients.
The process and prognosis of vestibular dysfunction after surgery in VS patients remain unclear. Tilts of subjective visual vertical/horizontal (SVV/SVH) are sensitive tools for detecting vestibular function imbalance in patients receiving VS surgery.9 SVV and SVH are vestibular function tests (VFTs) measuring the ability to perceive earth-vertical or horizontal without external visual cues.10 In most VS patients, the SVV tilts may return to normal after a follow-up period, and the VC is believed to play an essential role in the recovery of SVV tilts.11,12 Thus, SVV/SVH is performed in this study to evaluate vestibular function and compensation at various postoperative stages in VS patients. It has been reported that patients with more severe preoperative caloric weakness tend to regain balance more rapidly within 6 months postsurgery.9 However, previous studies have often been limited by numbers of participants, insufficient vestibular function evaluations, or short-term follow-up. The aim of this study was to characterize vestibular dysfunction and compensation pre-VS surgery and post-VS surgery and identify potential factors influencing recovery.
METHODS
This prospective study was approved by the ethical committee of the hospital, and the protocol was registered previously. The patients were recruited between February 2022 and April 2024 from the inpatient departments of the research center. The inclusion criteria were as follows: (1) adults aged 18-70 years and (2) diagnosed with unilateral VS and scheduled for surgical ablation. The exclusion criteria were as follows: (1) affected by other balance disorders with definite etiologies, such as Meniere disease, vestibular neuritis, or multiple sclerosis and (2) patients who have already received radiotherapy or surgery for intracranial lesions. The participants would be excluded from the follow-up once there was a change in the diagnosis according to the postoperative pathological outcomes or once the surgery was canceled. All participants provided consent statements. Additional data are provided in the supplementary materials and available by emailing the corresponding authors as well. Clinical raw information, such as photographs and videos, cannot be shared to protect patient privacy.
The participants underwent MRI of internal auditory canal, pure-tone audiometry (PTA), word recognition score, auditory brainstem response, auditory steady-state response, distortion product–evoked otoacoustic emissions, facial nerve electroneurogam, SVV, SVH, caloric test, rotatory test, cervical vestibular-evoked myogenic potentials (cVEMP) test, ocular VEMP (oVEMP) test, and video head impulse test (vHIT) at baseline within 3 months before surgery. Spontaneous nystagmus, SVV, SVH, Visual Analog Scale for vertigo (VAS-V), and VAS for tinnitus (VAS-T) were evaluated at baseline and each follow-up: 1 day, 3 days, 7 days, 1 month, and 3 months after surgery, respectively. Participants also completed the Dizziness Handicap Inventory (DHI) and functional gait assessment (FGA) at baseline and the 1-month and 3-month follow-up. All participants underwent tumor resection by the retrosigmoid approach, and the study did not interfere with patients' surgery therapy. All examinations were performed by trained physicians skilled in neuro-otological tests. Find details of the examination procedures are provided in Supplemental Digital Content 1 (http://links.lww.com/NEU/E902).
The SVV and SVH tests were conducted using a commercial computerized system designed for SVV/SVH measurements (VertiSVV, Zehnit). A luminous line with randomly tilted angle generated by computer was displayed against a dark background on the virtual reality display. Participants were instructed to use the wireless controller to adjust the line's angle to what they perceived as vertical for the SVV or horizontal for the SVH. The SVV/SVH test was performed at 3 head positions: an upright position (0°), head tilted 30° to the right (+30°), or left side (−30°). The criteria for an abnormal result are ±2.0 in the 0° position and ±11.0° in the ±30° position. Each position requires the test to be conducted at least 3 times.12
In the assessment of vertigo symptoms, participants are asked to rate their level of dizziness by selecting a point on a continuous 10-cm line without numerical markings. The resulting score, as VAS-V score which varies from 0 to 10, is determined by measuring the distance from 1 end of the line to the chosen point.13
Outcome Measurements
The principal outcome measure focused on the process of VC, which was evaluated by monitoring the variations of SVV/SVH after surgery: on the first day postoperative (POD 1), the third day (POD 3), the seventh day (POD 7), the 30th day (POD 30), and the 90th day (POD 90) postoperative, compared with SVV/SVH at baseline after enrollment. The SVV/SVH values performed at different head positions were recorded as SVV 0°/SVH 0° for the upright position (0°), SVV-Ipsi/SVH-Ipsi for the head tilted 30° to the ipsilateral side of the affected ear, and SVV-Contra/SVH-Contra for the head tilted 30° to the contralateral side of the affected ear. Secondary outcomes were the following: (1) abnormal rates of each VFT, including caloric test, cVEMP, oVEMP, and vHIT, and the relationships between each of them and postoperative SVV/SVH; (2) correlations between recovery of SVV/SVH and VAS-V after surgery.
Statistical Analysis
Categorical variables were presented using frequencies and percentages, and continuous variables were presented using mean and SDs or median [25 IQR, 75 IQR]. Differences in characteristics among the groups were tested with χ2 and Fisher test for categorical variables; 1-way analysis of variance was used for normally distributed continuous variables, and the Mann-Whitney U test was used for non-normal continuous variables.
A 2-way repeated-measures analysis of variance was used to test for differences in the changes induced by the 2 groups in the patients' SVV/SVH. The independent variables included a between factor with 2 levels (normal and abnormal) and a within (time) factor with 2 levels (normal and abnormal). A generalized estimating equation model with an exchangeable correlation structure was used to analyze the longitudinal changes in SVV/SVH over the course of therapy. Age, tumor size, sex, dizziness, ipsilateral PTA, tumor origin, and abnormal VFTs were included as covariates to assess their effects on the mean changes in clinical indexes. A Gaussian distribution with an identity link function was specified, and parameter estimates were obtained using robust standard errors to account for within-subject correlations. Two-side P-values below .05 were considered significant. Statistical analyses were performed using R software (version 4.1.2).
RESULTS
Clinicodemographic Information
Between February 2022 and January 2024, 135 patients with unilateral VS (according to the imaging of internal auditory canal-MRI) were screened, of whom 9 declined to participate, and 25 did not fulfill inclusion criteria. The intention-to-treat population comprised 101 patients, 39 male and 49 left-side affected. The median age of the participants was 48.0 years (IQR, 38.0-55.0). All patients were treated by suboccipital retrosigmoid approach for tumor resection within 1 week after inclusion. Baseline characteristics are presented in Table 1 and flowchart in Supplemental Digital Content 2 (http://links.lww.com/NEU/E903).
TABLE 1.
Baseline Characteristics
| Characteristics | Values (n = 101) |
|---|---|
| Age, median (IQR), y | 48.0 (38.0, 55.0) |
| Sex, no. (%) | |
| Male | 39 (38.6) |
| Female | 62 (61.4) |
| Side, no. (%) | |
| Left | 49 (48.5) |
| Right | 52 (51.5) |
| Symptoms, no. (%) | |
| Tinnitus | 85 (84.2) |
| Hearing loss | 93 (92.1) |
| Dizziness without vertigo | 39 (38.6) |
| Vertigo | 12 (11.9) |
| Postural symptoms | 22 (21.8) |
| PTA, median (IQR), dB | 55.6 (37.5, 77.5) |
| WRS, mean (SD), % | 93.8 (16.7) |
| Hearing threshold at best WRS, mean (SD), dB | 65.3 (26.5) |
| Vestibular dysfunction | |
| Caloric UW, median (IQR), % | 76.0 (55.0, 93.0) toward affected side |
| Caloric DP, median (IQR), % | 57.0 (39.2, 80.2) toward unaffected side |
| vHIT-ASC gain, mean (SD) | 0.96 (0.21) |
| vHIT-ASC abnormal saccades, No. (%) | 19 (18.8) |
| vHIT-HSC gain, mean (SD) | 0.86 (0.61, 1.02) |
| vHIT-HSC abnormal saccades, No. (%) | 51 (50.5) |
| vHIT-PSC gain, mean (SD) | 0.86 (0.22) |
| vHIT-PSC abnormal saccades, No. (%) | 40 (39.6) |
| cVEMP threshold, median (IQR), dB | 95.0 (90.0, 95.0) |
| cVEMP P1, median (IQR), s | 15.54 (14.59, 16.42) |
| cVEMP N1, mean (SD), s | 23.90 (2.55) |
| oVEMP threshold, median (IQR), dB | 85.0 (85.0, 90.0) |
| oVEMP P1, mean (SD), s | 16.89 (1.78) |
| oVEMP N1, mean (SD), s | 12.24 (1.18) |
| SVV 0°, median (IQR), ° | 2.40 (1.00, 4.40) |
| SVV-Ipsi, median (IQR), ° | 4.80 (2.20, 8.70) |
| SVV-Contra, median (IQR),° | 5.00 (2.30, 8.00) |
| SVH 0°, median (IQR), ° | 2.40 (1.20, 4.60) |
| SVH-Ipsi, median (IQR), ° | 4.20 (1.60, 8.50) |
| SVH-Contra, median (IQR), ° | 5.80 (2.90, 9.40) |
| DHI, mean (SD) | 9.8 (13.1) |
| VAS-V, mean (SD) | 1.4 (2.0) |
| FGA, mean (SD) | 30.0 (29.0, 30.0) |
| Koos grade, No. (%) | |
| I | 12 (11.8) |
| II | 46 (45.5) |
| III | 24 (23.8) |
| IV | 19 (18.8) |
| Origin nerves, No. (%) | |
| Superior vestibular nerve | 16 (15.8) |
| Inferior vestibular nerve | 17 (16.8) |
| Vestibular nerve | 43 (42.6) |
| Unclear | 25 (24.8) |
ASC, anterior semicircular canal; cVEMP, cervical vestibular-evoked myogenic potentials; DHI, Dizziness Handicap Inventory; DP, directional preponderance; FGA, functional gait assessment; HSC, horizontal semicircular canals; oVEMP, ocular vestibular-evoked myogenic potentials; PSC, posterior semicircular canals; PTA, pure-tone audiometry; SVH 0°, SVH value at upright head position; SVH, subjective visual horizontal; SVH-Contra, SVH value for the head tilted to the contralateral side of the affected ear; SVH-Ipsi, SVH value for the head tilted 30° to the ipsilateral side of the affected ear; SVV 0°, SVV value at upright head position; SVV, subjective visual vertical; SVV-Contra, SVV value for the head tilted to the contralateral side of the affected ear; SVV-Ipsi, SVV value for the head tilted 30° to the ipsilateral side of the affected ear; UW, unilateral weakness; VAS-V, Visual Analog Scale for vertigo; VFT, vestibular function tests; vHIT, video head impulse test; WRS, word recognition score.
Data are mean (SD), median (IQR) or number (%).
A total of 81 patients (80.2%) had a significant unilateral weakness (median 76.5%, IQR 55.0%-93.0%) in the caloric test before the surgery. A total of 19 patients (18.8%) showed abnormal gains and saccades of anterior semicircular canal, 51 of horizontal semicircular canal (50.5%), and 40 of posterior semicircular canal (39.6%) in vHIT toward the affected side. As for tests of otolith organs, the abnormal rate of cVEMP was 78.2% (79 patients), and the abnormal rate of oVEMP was 79.2% (80 patients). The results of VFTs were concluded as in Table 1.
Recovery of SVV/SVH
During the follow-up visits, many participants had difficulties finishing all the SVV/SVH tests on POD 1 because of vertigo, pain, weakness, or other discomfort feelings. To improve adherence, all the patients were asked to complete only the SVV 0°/SVH 0° test on POD 1, and 75% of patients completed the POD 1 follow-up visits. Over 85% of POD 3, POD 7, POD 30, and POD 90 follow-up visits were completed according to the protocol.
The tilts of SVV 0°/SVH 0°, SVV-Ipsi/SVH-Ipsi, and SVV-Contra/SVH-Contra all significantly increased after surgery on POD 1 (SVV 0° median 7.20, IQR 3.50-13.35, P < .0001; SVH 0° median 5.20, IQR 3.20-13.60, P < .0001), POD 3 (SVV 0° median 6.70, IQR 2.40-9.90, P < .0001; SVH 0° median 5.55, IQR 2.98-9.10, P < .0001; SVV-Ipsi median 6.80, IQR 3.60-14.10, P < .01; SVH-Ipsi median 10.05, IQR 4.00-13.52, P < .001; SVV-Contra, P < .001; SVH-Contra, P < .001), and POD 7 (SVV 0° median 7.35, IQR 3.62-11.22, P < .0001; SVH 0° median 5.95, IQR 2.72-9.45, P < .0001; SVV-Ipsi median 9.05, IQR 3.70-15.22, P < .01; SVH-Ipsi median 7.60, IQR 3.72-13.82, P < .001; SVV-Contra, P < .0001; SVH-Contra, P < .0001) compared with baseline before the surgery. There was no significant difference between baseline and POD 30 values in SVV 0°, SVV-Ipsi, and SVV-Contra, which indicated that the participants might have recovered to preoperative level on POD 30 (SVV 0° median 3.10, IQR 1.45-5.30, P > .5; SVV-Ipsi median 5.80, IQR 3.20-9.05, P > .05; SVV-Contra median 4.50, IQR 2.75-8.20, P > .05). Similarly, SVH 0°, SVH-Ipsi, and SVH-Contra of the participants have also recovered to preoperative level on POD 90 (SVH 0° median 3.90, IQR 2.10-5.95, P > .05; SVH-Ipsi median 4.50, IQR 2.30-8.70, P > .05; SVH-Contra median 5.80, IQR 3.12-9.35, P > .05), Figure 1.
FIGURE 1.
Change of SVV/SVH in postoperative VS within 90 days. Means (95% CIs) or median [25 IQR, 75 IQR] were calculated for SVV 0°/SVH 0°, SVV-Ipsi/SVH-Ipsi, SVV-Contra/SVH-Contra, and VAS-V at baseline, POD 1, POD 3, POD 7, POD 30, and POD 90. A, Changes of SVV 0° in 90 days after surgery; B, changes of SVH 0° in 90 days after surgery; C, changes of SVV-ipsi in 90 days after surgery; D, changes of SVV-Contra in 90 days after surgery; E, changes of SVH-Ipsi in 90 days after surgery; F, changes of SVH-Contra in 90 days after surgery. SVV 0°/SVH 0° for the upright position (0°), SVV-Ipsi/SVH-Ipsi for the head tilted 30° to the ipsilateral side of the affected ear, and SVV-Contra/SVH-Contra for the head tilted to the contralateral side of the affected ear. POD, postoperative day; SVH, 0° SVH value at upright head position; SVH, subjective visual horizontal; SVH-Contra, SVH value for the head tilted to the contralateral side of the affected ear; SVH-Ipsi, SVH value for the head tilted 30° to the ipsilateral side of the affected ear; SVV 0°, SVV value at upright head position; SVV, subjective visual vertical; SVV-Contra, SVV value for the head tilted to the contralateral side of the affected ear; SVV-Ipsi, SVV value for the head tilted 30° to the ipsilateral side of the affected ear; VAS-V, Visual Analog Scale for vertigo; VS, vestibular schwannoma. *P < .05; **P < .01; ***P < .001; ****P < .0001.
The generalized estimating equation models revealed the impact of time, age, sex, tumor size, dizziness, PTA before surgery, and number of involved VFTs (the battery of VFTs includes caloric test, cVEMP, oVEMP, and vHIT) on recovery of SVV/SVH 0°, VAS-V, VAS-T, DHI, and FGA (Table 2). The main effects of time analysis showed a significant recovery in SVV/SVH 0° tilts and DHI on POD 30 and POD 90 compared with those on POD 1 (P < .05). Except for time effects, the recovery of SVV/SVH 0° was also significantly affected by preoperative vestibular function (number of involved VFTs, SVV: −0.67, 95% CI −1.22 to −0.11, P = .019; SVH: −0.55, 95% CI −1.08 to −0.02, P = .04). What is more, female and better preoperative PTA indicated poor recovery in subjective symptoms evaluated by VAS-V, VAS-T, DHI, and FGA (P < .05).
TABLE 2.
Recovery of SVV/SVH, VAS-V, VAS-T, DHI, and FGA After Surgery
| Predictors | SVV 0° | SVH 0° | VAS-V | VAS-T | DHI | FGA | ||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Estimates | CI | P | Estimates | CI | P | Estimates | CI | P | Estimates | CI | P | Estimates | CI | P | Estimates | CI | P | |
| (Intercept) | 11.32 | 7.08 to 15.56 | <.001 | 12.15 | 8.38 to 15.92 | <.001 | 6.41 | 5.05 to 7.78 | <.001 | 5.27 | 3.83 to 6.71 | <.001 | 29.88 | 14.38 to 45.39 | <.001 | 25.24 | 21.25 to 29.22 | <.001 |
| Age | −0.01 | −0.07 to 0.04 | .693 | −0.03 | −0.08 to 0.02 | .239 | −0.02 | −0.04 to 0.00 | .032 | −0.02 | −0.04 to −0.00 | .04 | 0.08 | −0.16 to 0.33 | .5 | −0.1 | −0.16 to −0.04 | .001 |
| Tumor size | 0.01 | −0.07 to 0.08 | .871 | −0.04 | −0.11 to 0.03 | .238 | 0 | −0.03 to 0.02 | .847 | −0.03 | −0.07 to −0.00 | .037 | −0.28 | −0.58 to 0.03 | .075 | −0.06 | −0.16 to 0.03 | .2 |
| Sex | ||||||||||||||||||
| Male | Ref | Ref | Ref | Ref | Ref | Ref | Ref | Ref | Ref | Ref | Ref | Ref | Ref | Ref | Ref | Ref | Ref | Ref |
| Female | 0.99 | −0.20 to 2.19 | .104 | 0.63 | −0.57 to 1.82 | .306 | 0.79 | 0.32 to 1.25 | .001 | 0.68 | 0.20 to 1.17 | .006 | 6.79 | 0.96 to 12.63 | .023 | −2.84 | −4.38 to −1.31 | <.001 |
| Dizziness | ||||||||||||||||||
| Yes | Ref | Ref | Ref | Ref | Ref | Ref | Ref | Ref | Ref | Ref | Ref | Ref | Ref | Ref | Ref | Ref | Ref | Ref |
| No | −0.18 | −1.37 to 1.01 | .766 | −0.08 | −1.13 to 0.96 | .875 | −0.09 | −0.55 to 0.38 | .71 | 0.23 | −0.26 to 0.73 | .348 | 0.4 | −5.43 to 6.22 | .894 | 0.67 | −0.73 to 2.07 | .348 |
| PTA | 0.01 | −0.02 to 0.04 | .568 | −0.01 | −0.03 to 0.01 | .341 | −0.01 | −0.02 to −0.00 | .037 | −0.02 | −0.03 to −0.01 | <.001 | −0.15 | −0.27 to −0.04 | .008 | 0.03 | 0.00 to 0.07 | .036 |
| Number of involved VFTs | −0.67 | −1.22 to −0.11 | .019 | −0.55 | −1.08 to −0.02 | .04 | −0.34 | −0.56 to −0.11 | .004 | 0.09 | −0.13 to 0.30 | .444 | −0.56 | −3.27 to 2.15 | .685 | 1.12 | 0.34 to 1.90 | .005 |
| Time | ||||||||||||||||||
| POD 1 | ref | ref | ref | ref | ref | ref | ref | ref | ref | ref | ref | ref | ref | ref | ref | ref | ref | ref |
| POD 3 | −1.88 | −4.10 to 0.34 | .096 | −0.75 | −2.66 to 1.17 | .444 | −0.12 | −0.82 to 0.58 | .74 | 0 | −0.68 to 0.69 | .989 | ||||||
| POD 7 | −1.31 | −3.35 to 0.73 | .207 | −0.6 | −2.36 to 1.17 | .508 | −1.19 | −1.91 to −0.47 | .001 | −0.24 | −0.90 to 0.41 | .471 | ||||||
| POD 30 | −5.18 | −7.01 to −3.36 | <.001 | −2.61 | −4.25 to −0.97 | .002 | −1.69 | −2.38 to −1.01 | <.001 | −0.06 | −0.79 to 0.67 | .874 | ref | ref | ref | ref | ref | ref |
| POD 90 | −4.5 | −6.37 to −2.62 | <.001 | −2.67 | −4.32 to −1.01 | .002 | −2.64 | −3.33 to −1.96 | <.001 | −0.05 | −0.79 to 0.68 | .885 | −4.74 | −9.98 to 0.51 | .077 | 3.4 | 2.04 to 4.76 | <.001 |
DHI, Dizziness Handicap Inventory; FGA, functional gait qssessment; POD, postoperative day; PTA, pure-tone audiometry; SVH 0°, SVH value at upright head position; SVH, subjective visual horizontal; SVV, subjective visual vertical; SVV 0°, SVV value at upright head position; VAS-T, VAS for tinnitus; VAS-V, Visual Analog Scale for vertigo; VFTs, vestibular function tests.
A generalized estimating equation model with an exchangeable correlation structure was used to analyze the longitudinal changes in SVV 0°/SVH 0°, VAS-V, VAS-T, DHI, and FGA over the course of therapy.
Bold indicates significance.
The details of changes of facial nerve function evaluated by House-Brackmann grades and hearing loss assessed by PTA after surgery are provided in Supplemental Digital Content 3 (http://links.lww.com/NEU/E904).
Correlations Between SVV/SVH and Subjective Symptoms
The mean scores of VAS-V were 1.4 (SD. 2.0) at baseline, 4.1 (SD 2.7) on POD 1, 4.0 (SD 2.2) at POD 3, 2.9 (SD 2.3) on POD 7, 2.4 (SD 2.1) on POD 30, and 1.5 (SD 1.7) on POD 90. We could notice a similar tendency in change of SVV 0°/SVH 0° and of VAS-V (Pearson, P < .05) as in Figure 2. All lines performed a peak matched to the surgery and then tend to recover slowly within 90 days. The mean scores of DHI at baseline, POD 30, and POD 90 were 9.8 (SD 13.1), 21.4 (SD 17.9), and 16.5 (SD 16.2), respectively. The median scores of FGA at baseline, POD 30, and POD 90 were 30.0 (IQR 29.0-30.0), 24.0 (IQR 21.0-28.0), and 27.0 (IQR 25.0-29.0).
FIGURE 2.
Correlations between SVV/SVH and VAS-V in postoperative VS within 90 days. A, Changes of SVV 0° and VAS-V during postoperative 90 days; B, changes of SVH 0° and VAS-V during postoperative 90 days. Only data of SVV/SVH 0° were included because that all the patients were asked to only complete SVV 0°/SVH 0° test on POD 1 to improve adherence. POD, postoperative day; SVH 0°, SVH value at upright head position; SVV, subjective visual vertical; SVH, subjective visual horizontal; VAS, Visual Analog Scale; VAS-V, VAS for vertigo; VS, vestibular schwannoma.
Correlations Between Preoperative Vestibular Function and Postoperative Vestibular Compensation
This study further investigated the relationship between the preoperative vestibular dysfunction and the postoperative VC, assessed by VFTs and SVV/SVH. Because of overmuch missed values in POD 1, we excluded the results of SVV/SVH at POD 1 in this analysis. Patients with abnormal oVEMP also performed worse in the SVV test and gained higher SVV 0° values at baseline (mean difference [MD], 3.21, SD 2.83, P = .028). After surgery, the results of SVV 0° and SVH 0° showed significant differences between subgroups divided by caloric test within 7 days (MD 7.86, SD 5.45, P = .0009 for POD 7 SVV 0°, MD 6.76, SD 5.88, P = .037 for POD 3 SVH 0°) and by vHIT within 7 days (MD 7.87, SD 5.46, P < .0001 for POD 7 SVV 0°, MD 6.98, SD 5.34, P = .007 for POD 7 SVH 0°). As a potential tendency, those patients with abnormal results of VFTs before the surgery were inclined to gain lower tilt scores of SVV 0° and SVH 0° (P > .05, Figure 3). On POD 30, the potential difference of SVV 0°/SVH 0° between each subgroup of VFTs disappeared.
FIGURE 3.
Comparisons of SVV/SVH in different VFT groups at different times. A, Comparisons of SVV 0° in groups with abnormal and normal caloric test results; B, comparisons of SVV 0° in groups with abnormal and normal cVEMP results; C, comparisons of SVV 0° in groups with abnormal and normal oVEMP results; D, comparisons of SVV 0° in groups with abnormal and normal vHIT results; E, comparisons of SVH 0° in groups with abnormal and normal caloric test results; F, comparisons of SVH 0° in groups with abnormal and normal cVEMP results; G, comparisons of SVH 0° in groups with abnormal and normal oVEMP results; H, comparisons of SVH 0° in groups with abnormal and normal vHIT results. A 2-way repeated-measures ANOVA was used to test for differences in the changes induced by the 2 groups in the patients' SVV 0°/SVH 0°. ANOVA, analysis of variance; cVEMP, cervical vestibular-evoked myogenic potentials; oVEMP, ocular VEMP; SVH, subjective visual horizontal; SVH 0°, SVH value at upright head position; SVV, subjective visual vertical; SVV 0°, SVV value at upright head position; VFT, vestibular function tests; vHIT, video head impulse test; ns P ≥ .05; *P < .05; **P < .01; ***P < .001; ****P < .0001.
DISCUSSION
In this prospective, observational study, we found that SVV and SVH recovered within 30 days in most VS patients after surgery. VC starts immediately after unilateral vestibular deafferentation.14 Previous study by Uehara reported a recovery of DHI to the preoperative baseline at 3 months after surgery in 26 VS patients.2 A significant correlation between DHI and improvements in SVV with time was reported.9 In our study, SVV recovered to the preoperative baseline within 1 month after surgery, which indicates that the patients may gain significant VC during this period of time. Thus, vestibular rehabilitation could be performed within 1 month after surgery to promote the balance of the VS patients. Participants reported significant dizziness and vestibular dysfunction evaluated by VAS-V and SVV/SVH at POD 1, POD 3, and POD 7. The positive correlation between subjective symptoms and improvements in SVV/SVH was reinforced by our results on VAS-V and SVV/SVH,9 which indicates that VC can play an important role in improving subjective symptoms.
In this study, patients with abnormal results in a caloric test or vHIT may recover sooner and better in SVV/SVH in the first postoperative week compared with those with normal results. Chronic preoperative vestibular dysfunction in some of the VS patients would initiate the process of VC before the damage to the vestibular nerve from the surgery occurred. These patients with apparent vestibular deficiency before surgery will suffer a milder disability and subjective symptom of vertigo or dizziness in the immediate postoperative period, profit from preoperative VC.9,15 Similarly, patients with worse preoperative hearing and vestibular outcome usually indicates more severe preoperative injury and earlier start of compensation, which would result in a better recovery of VC and subjective vestibular symptoms after surgery in this cohort. This finding and hypothesis were in accordance with previous studies and confirmed the importance of preoperative vestibular evaluation in VS patients.9 Similarly, patients who received intratympanic gentamicin before surgical resection of the tumor as prehabilitation treatment could performed better in the posturography test and SVV/SVH afterward.16-18 The differences did not remain significant at the 30 days postoperative follow-up. This is probably related to the well establishment of VC by daily vestibular rehabilitation. As for cVEMP and oVEMP, the patients with abnormal results got higher values in SVV/SVH in the first postoperative week compared with those with normal results. As utricular function tests, the relationships between SVV and oVEMP were confirmed previously.19,20 Patients with abnormal oVEMP results may perform higher SVV tilt just before and shortly after the surgery. The 79.2% abnormal rates of oVEMP in VS of our study corresponded with the dysfunction rates reported before.21
Limitations
This study has several limitations. First, the compliance of the patient at the POD 1 follow-up visit was influenced a lot by their postoperative symptoms and complications. The loss of follow-up was significantly higher at POD 1 than at other visits. Second, this study lacks a control group, which may bring confounding factors to the results. Despite these limitations, this study disclosed that vestibular function might quickly recover to the preoperative baseline within 1 month after surgery in VS. Moreover, the study performed a battery of VFTs to investigate the impacts of preoperative vestibular function on vestibular recovery and compensation. The enrollment of this cohort will continue for further analyses on the factors involved in recovery and VC of VS after surgery in the future.
CONCLUSION
In summary, static vestibular function recovered to the preoperative baseline within 1 month after surgery in VS. There was a positive correlation between subjective dizziness and improvements in vestibular function. Patients who already had vestibular dysfunction may recover sooner and better in VC in the first postoperative week compared with those with normal preoperative vestibular function.
Acknowledgments
We acknowledge the significant contributions of the patients, researchers, and hospital staff (Yang Jiafei et al). Author contributions: Weiming Hao and Dantong Gu contributed equally to the manuscript composition, and data analysis. Wenyan Li and Weidong Zhao designed the research and reviewed manuscript. Weiming Hao, Na Zhang, Ruiqi Zhang, Yanli Zhao, and Dongmei Zhang conducted patient follow-up and data collection. Jieli Zhao and Peixia Wu performed the data curation and validation. All authors discussed and approved the final version.
Footnotes
Supplemental digital content is available for this article at neurosurgery-online.com.
Weiming Hao and Dantong Gu contributed equally to this work.
Contributor Information
Weiming Hao, Email: haoweiming1993@163.com.
Dantong Gu, Email: gdttdg0215@163.com.
Na Zhang, Email: 1002159115@qq.com.
Ruiqi Zhang, Email: zhangrqfdu@163.com.
Yanli Zhao, Email: 23211170046@m.fudan.edu.cn.
Dongmei Zhang, Email: zdmwzx@163.com.
Jieli Zhao, Email: Zhaojieli_003@163.com.
Peixia Wu, Email: 13524844652@163.com.
Funding
This study was supported by the Shanghai Hospital Development Center (SHDC)'s 3-year program to Promote Clinical Skills and Innovation in Municipal Hospitals (no. SHDC2022CRD006), the National Key R&D Program of the Science and Technology Commission of China (no. 2023YFC2508000) and Fosun Nursing Research Program of Fudan University (FNF202445). The funding source had no role in the study design, data collection, data analysis, data interpretation, or report writing.
Disclosures
The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article.
SUPPLEMENTAL DIGITAL CONTENT
Supplemental Digital Content 1. Details of methodology.
Supplemental Digital Content 2. eTable 1. Flowchart.
Supplemental Digital Content 3. eTable 2. House-Brackmann Grades of the participants. eTable 3. Hearing loss in participants after surgery.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Supplemental Digital Content 1. Details of methodology.
Supplemental Digital Content 2. eTable 1. Flowchart.
Supplemental Digital Content 3. eTable 2. House-Brackmann Grades of the participants. eTable 3. Hearing loss in participants after surgery.