Comprehensive vestibular evaluation in patients with Otosclerosis: a case control study

Abstract

Aim

Otosclerosis is one of the common otologic diseases. The mechanism and the probable site of vestibular involvement are not yet fully understood. The present study aimed to perform a comprehensive vestibular evaluation in patients with otosclerosis, compared to the cases without otosclerosis.

Materials and methods

patients underwent a comprehensive cochleovestibular evaluation, including audiometry, ocular and cervical vestibular evoked myogenic potential (o-VEMP and c-VEMP), video head impulse (vHIT) and caloric tests. The results were compared with those obtained from the non-otosclerosis control group.

Results

A total of 61 individuals were included in the study who were divided into two groups of the case (50.82%) and control (49.18%). The results showed that there was a significant difference in the mean vHIT gain between the case and control groups (P < 0.05). However, the mean gain was still within the normal range. Besides, the patients with otosclerosis had significant bilateral or unilateral weaknesses according to caloric test results. Moreover, their o-VEMP and c-VEMP results were significantly abnormal as well (P < 0.05).

Conclusion

Based on the results of the present study, the vestibular system even in asymptomatic cases, is affected by otosclerosis. Furthermore, it seems that the otolithic system has a higher chance of involvement, compared to the semicircular canals.

Supplementary Information

The online version contains supplementary material available at 10.1007/s12070-022-03147-5.

Introduction

Otosclerosis is one of the most common causes of hearing loss among Caucasians. Despite being mostly conductive, it is still an important cause of sensorineural hearing loss [1]. According to previous studies, histological evidence of otosclerosis was detected in 7.3–10.3% of autopsy specimens taken from the temporal bone of Caucasians [2–6]. Histopathologically, the bone is absorbed by osteoclastic activity and a new bone is deposited by osteocytes which leads to stapes footplate fixation and conductive hearing loss [7]. The genetic factors have an important role in Otosclerosis [8] and many patients have a familiar history of Otosclerosis. These patients would have a higher chance for an earlier onset or bilateral involvement [9]. Review of the related literature reveals that the auditory aspects in otosclerosis are well studied, while researches on vestibular parts are scant. Based on the statistics, 24% of patients with otosclerosis are reported to experience true vertigo episodes [10]. The exact pathophysiological basis of vestibular symptoms is unknown; however, the proposed mechanism is the neuronal degeneration in the vicinities of active otosclerotic sites and compromised endolymphatic flow due to sclerotic foci, which results in endolymphatic hydrops [11–14]. Marked diminution in the vestibular dark and transitional cells population was observed in the cadaveric evaluation of otosclerotic temporal bones. This could result in suboptimal fluid and electrolyte distribution in the vestibular system and its subsequent dysfunction [15].

Given the incompletely characterized prevalence, pathophysiology, and site of vestibular damage in otosclerosis, this study was designed to comprehensively assess the peripheral vestibular system in these patients.

Materials and methods

The present case-control study was performed on patients with a history of bilateral progressive conductive hearing loss and intact tympanic membrane who were diagnosed as otosclerosis and were admitted preoperatively to XXXX teaching Hospital. The subjects with normal hearing and without any history of otologic diseases who had similar age and gender were selected and allocated to the control group. The exclusion criteria were (1) vertigo, (2) unilateral otosclerosis, (3) history of any otologic surgery on either side, (4) otorrhea, (5) history of trauma, (6) major general comorbidities (e.g., diabetes or ischemic heart disease), and (7) lack of stapedius footplate fixation intra-operatively (otosclerosis ruled out) or concomitant Malleus/Incus fixation.

The vestibular function was assessed using vestibular evoked myogenic potential (VEMP), caloric test, and video-head impulse testing (vHIT). The VEMP test is a sonomotor reflex, caused by an acoustic stimulus with a resultant motor muscular response. The vestibular apparatus and particularly the saccule are sensitive to loud sounds. Both cervical VEMP (c-VEMP) and ocular VEMP (o-VEMP) were obtained in the present study. These tests could be performed with both air and bone acoustic stimuli; considering the fact that conductive hearing loss could practically interfere with the results, the researchers decided to use only bone conduction (BC) testing. The c-VEMP and o-VEMP were tested with 500 Hz tone burst stimuli at the maximum level of BC stimulation via the B-71 bone vibrator. The rise, plateau, and fall were 4.0ms. The power of preamplifier was at default setting (60-80dB). Both tests were performed monaurally in sitting position and the muscle contraction was controlled by EMG recording. In o-VEMP, patients kept an upward gaze during the test. At least 200–300 sweeps (rate: 5.1 Hz) were used in each recording and at least two independent recordings were taken for each test to confirm the reproducibility. In both tests, the vibrator was placed on the mastoids but in o-VEMP, the recording was contra-lateral. In the c-VEMP, the electrodes were placed at clavicular joint (non-inverting), sternocleidomastoid muscle (inverting), and forehead (ground). In the o-VEMP, non-inverting, inverting, and ground electrodes were placed at upper area of forehead, infraorbital rim, and lower area of the forehead, respectively. The presence of each wave, amplitude asymmetry, and latency of waves was analyzed.

In general, vHIT is the only test that independently measures the function of every single of the six semicircular canals in a physiologic status. Moreover, it could help to further lateralize the pathology. In the caloric test, a non-physiologic stimulus (warm and cold air irrigation) is used to identify the damaged lateral semicircular canal using Jongkees’ formula. The bilateral weakness defined as response lower than 12 for each ear or lower than 20 for four stimulations. This combination can evaluate all five vestibular end organs.

The participants in both arms (before doing the surgery in case group) were referred to the Audio-vestibular Assessment and Rehabilitation Center and underwent pure tone audiometry, speech audiometry, tympanometry and acoustic reflex, vHIT, (ICS impulse 250 Hz, Otometrics, Denmark), c-VEMP, o-VEMP (EP25, Intracoustic, Denmark), and caloric test (Hortmann, otometrics, Denmark).

The responses of the VEMP test were elicited by BC burst tone and the results were reported qualitatively based on the absence of the N and P waves. The vHIT gains were reported quantitatively for each semicircular canal. Gains below 0.8 and 0.7 for horizontal and vertical canals were considered abnormal, respectively. The caloric test results were presented qualitatively as bilateral weakness (BW), unilateral (UW) or normal.

Written informed consent was obtained from all participants prior to the study. The study protocol was approved by the Ethics Committee of Mashhad university of medical sciences.

(Registration code: IR.MUMS.MEDICAL.REC.1397.719).

The collected data were analyzed in SPSS software (version 16.0) (SPSS Inc. Chicago, IL). For continuous data, we checked the normality assumptions and then the data were presented as mean and standard deviation and we used independent t-test to compare vHIT means between groups. All categorical variables were reported as the number and percentage of the sample and compared using the chi-squared test. P-value of < 0.05 was considered statistically significant and a 95% confidence interval was reported if required.

Results

Out of the total 61 participants of the study, 31 cases (50.82%) had otosclerosis, while the rest, 30 (49.18%), were in the control group. The mean age of the case and control groups were 37.77 ± 10.11 and 34.76 ± 11.65, respectively, which were not significantly different (P = 0.104). The gender distribution in the two groups was not significantly different (P = 0.06), either. Dizziness (and not a true spinning vertigo!) was reported in 2 (6.45%) cases of the otosclerosis group and none of the controls. The pre-op audiological data of the case group are as follow: speech reception threshold (SRT): 50.87 ± 14.38 dB, bone conduction threshold (BC): 23.52 ± 10.47 dB, Air bone gap (ABG): 29.03 ± 6.09 dB. In all the cases surgery was done, which confirmed stapedius fixation and Stapedotomy was done.

Only one (3.22%) of the patients with otosclerosis had normal caloric test results, while 25 (80.65%) and 5 (16.13%) of the patients had bilateral and unilateral weaknesses, respectively. These results were significantly different (P < 0.01) between the two groups (Table 1).

Table 1.

Vestibular test results in otosclerosis and non-otosclerosis groups

Test	Result	With Otosclerosis N(%)	Without otosclerosis N(%)	P-value X2
Caloric test	Normal	1 (3.22%)	25 (83.34%)	0.001**
	Bilateral Weakness	25 (80.65%)	4 (13.34%)
	Unilateral Weakness	5 (16.13%)	1 (3.32%)
o-VEMP	Normal in both sides	3 (9.675%)	26 (86.67%)	0.001**
	Abnormal in both sides	25 (80.65%)	1 (3.32%)
	Abnormal in one side	3 (9.675%)	3 (10.01%)
c-VEMP	Normal in both sides	2 (6.45%)	26 (86.67%)	0.001**
	Abnormal in both sides	25 (80.65%)	1 (3.32%)
	Abnormal in one side	4 (12.9%)	3 (10.01%)

o-VEMP: Ocular vestibular-evoked myogenic potential, c-VEMP: cervical vestibular-evoked myogenic potential. LH: Left horizontal semicircular canal, RH: Right horizontal semicircular canal, LA: Left anterior semicircular canal, RP: Right posterior semicircular canal, LP: Left posterior semicircular canal, RA: Right anterior semicircular canal

* Statistically significant at < 0.05

** Statistically significant at < 0.01

Results of the o-VEMP and c-VEMP tests were normal in less than 10% of the case group, in contrast to more than 85% normal result in the control group (Table 1). Furthermore, 80.65% of the otosclerosis cases were abnormal in both VEMP tests.

The mean vHIT gain for each semicircular canal was within the normal range in the case group (except for the left anterior semicircular canal). However, the results revealed a significant difference in mean vHIT gain in four out of the six canals between the two groups and the patients with otosclerosis had lower vHIT gain than the control group (Table 2).

Table 2.

VHIT test results in otosclerosis and non-otosclerosis groups

Test	Result	With Otosclerosis Mean ± SD	Without otosclerosis Mean ± SD	P-value T-test
vHIT	LH	0.83 ± 0.10	0.90 ± 0.08	0.004**
	RH	0.87 ± 0.15	0.97 ± 0.10	0.005**
	LA	0.68 ± 0.16	0.78 ± 0.11	0.006**
	RP	0.71 ± 0.10	0.70 ± 0.11	0.834
	LP	0.71 ± 0.25	0.85 ± 0.17	0.047*
	RA	0.77 ± 0.15	0.88 ± 0.25	0.055

vHIT: Video Head Impulse Test

* Statistically significant at < 0.05

** Statistically significant at < 0.01

The proportion of abnormality in vHIT results fot study groups were compared and summarized in Table 3. The proportion of abnormality in all the six tested canals was higher in otosclerosis group than the control group and this difference was significant in three canals (left horizontal semicircular canal, left anterior semicircular canal, and left posterior semicircular canal).

Table 3.

vHIT results in otosclerosis and non-otosclerosis groups

vHIT		With otosclerosis N(P)	Without otosclerosis N(P)	95% CI (Confidence Interval) for proportion differences	P-value
LH	Abnormal	10 (0.32)	1 (0.03)	0.10 : 0.48	0.001*
	Normal	21 (0.68)	29 (0.97)	-0.48 : -0.10	0.001*
RH	Abnormal	4 (0.13)	1 (0.03)	-0.04 : 0.23	0.17
	Normal	27 (0.87)	29 (0.97)	-0.23 : 0.04	0.17
LA	Abnormal	18 (0.58)	3 (0.10)	0.24 : 0.72	0.001*
	Normal	13 (0.42)	27 (0.90)	-0.72 : -0.24	0.001*
RP	Abnormal	17 (0.55)	13 (0.43)	-0.14 : 0.37	0.37
	Normal	14 (0.45)	17 (0.57)	-0.37 : 0.14	0.37
LP	Abnormal	11 (0.35)	4 (0.13)	0.01 : 0.44	0.04*
	Normal	20 (0.65)	26 (0.87)	-0.44 : -0.01	0.04*
RA	Abnormal	8 (0.26)	3 (0.10)	-0.03 : 0.35	0.11
	Normal	23 (0.74)	27 (0.90)	-0.35 : 0.03	0.11

LH: Left horizontal semicircular canal, RH: Right horizontal semicircular canal, LA: Left anterior semicircular canal, RP: Right posterior semicircular canal, LP: Left posterior semicircular canal, RA: Right anterior semicircular canal

N: Number of patients, P: proportion

* Statistically significant at < 0.05

Discussion

Otosclerosis is one of the most common causes of progressive hearing loss in adults [16]. However, the vestibular function has not been comprehensively studied. Therefore, it has not been yet fully understood that which vestibular organ is affected in otosclerosis and how? So, the current study aimed to answer this question through a complete vestibular assessment in bilateral otosclerosis patients using c-VEMP, o-VEMP, vHIT, and caloric examination. The obtained results were finally compared with those of the control group.

This combination had not been applied previously in the relevant literature. Nevertheless, several studies have evaluated the vestibular system in otosclerosis patients. Some of them are mainly anatomical and some others, including ours, are function-based.

Studies on temporal bone histology in otosclerosis cases have shown significantly lower hair cell density in all vestibular structures in the group with endosteal involvement [17]. Kaya and Paparella have reported a significant decrease in the density of dark cells in human temporal bone specimens of patients with otosclerosis and endosteal involvement [15]. On the other hand, imaging evaluations have revealed that endolymphatic hydrops was prevalent among otosclerosis patients, especially those diagnosed with severe hearing loss or advanced diseases according to their computed tomography scan results [18].

It is known that the utricle has membranous interconnection with the footplate in 26% of cases [19]. Pauw et al. found the saccular membrane to be more fragile and distended, compared to the utricular membrane [20]. Moreover, Lin and Yung reported that the utricle is more susceptible to damage than saccule in otosclerotic patients [21]. However, in the current study, the abnormal results are almost the same in utricle and saccule. BC-VEMP abnormality in otosclerosis has already been reported [22–26]. In the present study, absent c-VEMP waves were found in 47 (94%) cases. This was almost the same for o-VEMP with 92% absent waves, which suggest both saccule and utricle involvement in otosclerosis. This could be due to microstructural alterations in the saccule which were previously demonstrated histologically in 31.3% of temporal bones [27]. Considering the anatomic proximity of the footplate to the utricle and saccule, it can be also postulated that propagation of the otosclerotic foci is the cause of this malfunction. The ototoxic effect of the byproducts of otosclerotic foci on otolithic receptors is another proposed hypothesis [28]. In the present study, the vertiginous cases had been excluded. However, no other study has reported a correlation between VEMP results and the presence of vertigo/dizziness in otosclerotic patients which can be justified with the subtle and gradually progressive nature of the disease and the central compensation [22, 29, 30].

The analysis of the vHIT results revealed that patients with otosclerosis had a lower mean value than the control group (Table 1); however, the mean gain were mostly within the normal range. It seems that semicircular functions are less severely affected. One reason may be the more distant anatomical location from otosclerotic initiation foci. The only previous study which performed vHIT on otosclerosis patients evaluated vHIT only in the horizontal canals, and revealed no difference in pre- and post-operative gains [30].

The caloric test results of 30 patients (96.7%) in the otosclerosis group were abnormal (25 BW and 5 UW). On the other hand, the rate of canal paresis and/or areflexia in otosclerosis patients was reported to be lower in the studies conducted by Tramontani et al. [22] (57%), Lin et al. [21] (28%), and Sakaet al. [29] (16%). This difference may be attributed to the more severe disease in the bilateral cases in the present research. It is worth noting that the caloric test is not necessarily in accordance with vHIT (as clearly demonstrated in our study) since the caloric test assesses each labyrinth independently in lower movement frequency ranges, while the vHIT examines these canals in higher vestibular frequencies.

Further studies are needed to assess the course of impairment of the vestibule end organs as the disease progresses.

Conclusion

Based on the results of the present study, the vestibular system is involved in patients with otosclerosis. The Otosclerosis probably affects the otolithic system more severely. However, the semicircular canals also seem not to be spared. The difference may be due to the chorological course of disease or vestibular end organs may be impacted differently by otosclerosis pathology. Vestibular assessment should be performed in all patients with otosclerosis.

Electronic Supplementary Material

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Declarations

Conflict of interest

none declared.