Clinical characteristics and analysis of vestibular-evoked myogenic potentials in patients with sudden sensorineural hearing loss in different ages

Abstract

BACKGROUND

Numerous studies have found that patients experiencing sudden sensorineural hearing loss (SSHL), with or without accompanying vertigo, often show impaired vestibular function. However, there is a dearth of studies analyzing vestibular-evoked myogenic potentials (VEMPs) in SSHL patients across various age groups.

AIM

To investigate vestibular condition in SSHL patients across various age demographics.

METHODS

Clinical data of 84 SSHL patients were investigated retrospectively. Audiometry, cervical vestibular evoked myogenic potentials (c-VEMPs), and ocular vestibular evoked myogenic potentials (o-VEMPs) were conducted on these patients. Parameters assessed included the latencies of P1 and N1 waves, as well as the amplitudes of P1–N1 waves. Moreover, the study evaluated the influence of factors such as sex, affected side, configuration of hearing loss, and presence of accompanying vertigo.

RESULTS

Among the 84 SSHL patients, no significant differences were observed among the three groups in terms of gender, affected side, and the presence or absence of vertigo. Group II (aged 41–60 years) had the highest number of SSHL cases. The rates of absent o-VEMPs in the affected ears were 20.83%, 31.58%, and 22.72% for the three age groups, respectively, with no statistically significant difference among them. The rates of absent c-VEMPs in the affected ears were 8.3%, 34.21%, and 18.18% for the three age groups, respectively, with significant differences. In the unaffected ears, there were differences observed in the extraction rates of o-VEMPs in the unaffected ears among the age groups. In the three age groups, no significant differences were noted in the three age groups in the latencies of P1 and N1 waves or in the amplitude of N1–P1 waves for c-VEMPs and o-VEMPs, either on the affected side or on the unaffected side, across the three age groups.

CONCLUSION

The extraction rate of VEMPs is more valuable than parameters. Regardless of the presence of vertigo, vestibular organs are involved in SSHL. Notably, SSHL patients aged 41–60 appear more susceptible to damage to the inferior vestibular nerve and saccule.

Key Words: Sudden sensorineural hearing loss, Cervical vestibular evoked myogenic potential, Ocular vestibular evoked myogenic potential, Vertigo, Pure tone audiometry

Core Tip: Patients with sudden sensorineural hearing loss (SSHL), whether accompanied by vertigo or not, often show impaired vestibular function. By observing the extraction rate and various parameter indicators of vestibular-evoked myogenic potentials (VEMPs) in different age groups of SSHL patients, we found that the extraction rate of VEMPs is more valuable, and the Group II (aged 41–60 years) with the highest number of SSHL cases, and patients aged 41-60 years had the highest number of profound hearing loss and the lowest cervical-VEMPs extraction rate in affected ear. The results indicates that SSHL aged 41-60 years old patients are more susceptible to damage to the inferior vestibular nerve and saccule.

INTRODUCTION

Sudden sensorineural hearing loss (SSHL) is defined as sensorineural hearing loss ≥ 30 dB or more, affecting at least three adjacent frequencies, and developing within 72 h or less[1]. Typically unilateral, its causes are diverse, including theories such as viral infections, chronic inflammation, vascular damage, and autoimmune diseases[1,2]. The main accompanying symptoms of SSHL are tinnitus and vertigo.

Vestibular evoked myogenic potentials (VEMPs) are short-latency evoked potentials that can be categorized into ocular vestibular evoked myogenic potentials (o-VEMPs) and cervical vestibular evoked myogenic potentials (c-VEMPs). O-VEMPs evaluates the superior vestibular nerve and utricle, while c-VEMPs assesses the inferior vestibular nerve and saccule. Research has revealed abnormal VEMPs results in a considerable number of SSHL patients[3]. Based on our statistics, 66.7% had abnormal results in the VEMPs test[4]. However, the relationship between vestibular involvement and SSHL remains controversial. In addition, data regarding the clinical features and analysis of VEMPs in SSHL patients across different age groups are lacking.

In the present study, we aimed to observe the extraction rate and various parameter indicators of VEMPs in patients with SSHL in different age groups. The objective was to gain insights into the vestibular condition in SSHL across various age demographics.

MATERIALS AND METHODS

We conducted this retrospective cross-sectional study between July 2022 and August 2023 in the Department of Otorhinolaryngology of Hebei Provincial Eye Hospital. The Medical Ethical Committee of Hebei Provincial Eye Hospital approved the study (2023ZZ107). This study was conducted in accordance with the ethical standards of the Helsinki Declaration and its amendments.

Research object

A total of 84 patients diagnosed with SSHL participated in this study. All of the patients had unilateral SSHL, which occurred within 72 h, and had a 30-dB loss over three contiguous frequencies. Initial evaluation of each patient comprised clinical symptom assessment, physical examination, and a battery of tests, including pure tone audiometry (PTA), o-VEMPs, and c-VEMPs. Imaging studies such as computed tomography and magnetic resonance imaging of the brain and inner ear were conducted and found to be normal, ruling out identifiable causes such as stroke, trauma, and autoimmune disorders.

The hearing thresholds of the patients were measured at frequencies of 250, 500, 1000, 2000, 4000, and 8000 Hz. We obtained the hearing level of each patient on the first visit. The average thresholds of high, medium, and low frequencies were means of hearing thresholds at 4000 and 8000, 1000 and 2000, and 250 and 500 Hz, respectively. The four patterns of audiographic configurations were defined as follows: (1) low-frequency hearing loss, characterized by a hearing loss below 1000 Hz, with a threshold of at least 250 and 500 Hz, and a loss ≥ 20 dBHL; (2) high-frequency hearing loss, characterized by a loss at frequencies above 2000 Hz, with a threshold of at least 4000 and 8000 Hz, and a loss ≥ 20 dBHL; (3) flat-type hearing loss, where all frequencies exhibit decreased hearing, with an average threshold ≤ 80 dBHL; and (4) profound hearing loss, where all frequencies exhibit decreased hearing, with an average threshold ≥ 81 dBHL. The PTA values for the evaluated frequencies were computed accordingly.

Exclusion criteria

We excluded patients meeting the following criteria: a hearing loss onset longer than 10 d ago, conductive hearing loss, hearing loss caused by posterior cochlear lesions or cochlear malformation, Ménière’s disease, and chronic middle ear infection. Patients with hearing loss due to noise, barotrauma, ototoxicity, head injury, myasthenia gravis, and stroke were also excluded.

Pure tone threshold

Using the Danish listening instrument (Otometrics, Model 1081), the air and bone conduction hearing thresholds were tested and recorded at frequencies of 0.125, 0.25, 0.5, 1, 2, 4, and 8 kHz in a standard soundproof room.

VEMPs

The Neuro-Audio auditory evoked potential analyzer (Neurosoft Ltd., Ivanov, Russia) was used for detection. During the test, the patient was seated, and sound was delivered through a headset gave sound. The interpolar resistance was < 5KΩ, the stimulation rate was 5.1 times/second, the time window was 50 ms, the stimulus polarity was alternate wave, the stimulus sound signal was 500 Hz tone-burst, the bandpass filtering o-VEMPs was 1–1000 Hz, the c-VEMPs was 30–2000 Hz, the o-VEMPs superposition times were 100 ≤ n ≤ 200, the c-VEMPs superposition times n was 60 times, and the repetition was three times.

The initial stimulus intensity was set at 100 dBnHL to observe whether the corresponding waveform could be elicited and whether the curve and waveform were repeatable. If there was repeatability, the side was recorded. Conversely, without repeatability, the magnitude was increased by 5 dB for re-detection. This process was repeated three times to observe whether the curve and waveform were repeatable. If there was repeatability, the side was recorded; otherwise, the waveform was missing. The asymmetry ratio was calculated from the magnitude values of P1 and N1, with an asymmetry ratio > 40% considered abnormal.

o-VEMPs recording

During the o-VEMPs test, the bilateral recording electrode was positioned approximately 1 cm below the middle of the left and right eyelids. The bilateral reference electrode was located 1 cm below the recording electrode, while the grounding electrode was placed at the brow. Throughout the test, the patient maintained a still head position, gazing upward at an angle of 30–45°, while the signal was recorded on the opposite side. The first positive wave in the waveform was identified as N1, and the first negative wave as P1, from which the N1 and P1 Latencies were derived.

c-VEMPs recording

During the c-VEMPs test, bilateral recording electrodes were placed symmetrically at the first 1/3 of the sternocleidomastoid muscle located at the supracosternal fossae, while the ground electrode was placed at the center of the eyebrow. Throughout the test, the head was tilted to the opposite side of the ear being stimulated, ensuring that the tested otosternocleidomastoid muscle was in a rigid state, and signals were recorded on the same side. The first negative wave in the waveform was identified as P1 and the first positive wave as N1, from which the P1 latency and N1 latency were obtained.

Statistical analysis

The statistical analysis was conducted using SPSS Statistics Version 22.0 (IBM Corporation). Analysis of variance (ANOVA) was employed to assess statistical significance, and chi-square one-way ANOVA was utilized for comparisons between groups. In all analyses, P < 0.05 was considered statistically significant.

RESULTS

A total of 84 patients with SSHL were enrolled in this study, with ages ranging from 12 to 79 years, comprising 38 males and 46 females. The patients were divided into three groups: Group I (aged ≤ 40 years, n = 24, 28.57%), Group II (aged 41–60 years, n = 38, 45.24%), and Group III (aged 61–80 years, n = 22, 26.19%). Gender and affected side showed no significant differences among the three groups (P > 0.05; Table 1). The rates of vertigo in each group were 25%, 28.95%, and 40.91%, respectively; therefore, vertigo/no vertigo showed no significant differences among the three groups (P > 0.05, Table 1). Significant differences were observed in the distribution of audiographic patterns of hearing loss among the three groups (P < 0.05; Table 1). Among patients without vertigo, a total of 11 c-VEMPs and 11 o-VEMPs were absent in the affected ears. Specifically, one c-VEMPs and two o-VEMPs belonged to Group I, eight c-VEMPs and seven o-VEMPs belonged to Group II, and two c-VEMPs and two o-VEMPs belonged to Group III.

Table 1 Comparison of 84 sudden sensorineural hearing loss patients among different age groups, n (%).

Group	n	Gender		Side		Type of hearing loss				Vertigo
		M	F	L	R	1	2	3	4	With	Without
I (≤ 40)	24	10	14	9	15	5	3	8	8	6 (25)	18 (75)
II (41-60)	38	17	21	16	21	3	3	15	16	11 (28.95)	27 (71.05)
III (61-80)	22	11	11	10	12	0	3	15	4	9 (40.91)	13 (59.09)
Total	84	38	46	37	47	8	9	39	28	26 (30.95)	58 (69.05)
P value		P > 0.05		P > 0.05		P < 0.05				P > 0.05

Among the 84 SSHL patients, the rates of absent o-VEMPs in the affected ears in each group were 20.83%, 31.58%, and 22.72%, respectively. However, there was no statistically significant difference among the groups (P = 0.188; Table 2). Conversely, the rates of absent c-VEMPs in affected ears in each group were 8.3%, 34.21%, 18.18%, respectively (P = 0.000021; Table 2), indicating a statistically significant difference among the groups. Differences in the extraction rate of o-VEMPs in unaffected ears among the age groups were observed, with statistical significance (P = 0.036; Table 3). Additionally, the o-VEMPs amplitude P1–N1 in the affected ears of Group II was significantly larger than that in Group III (P = 0.001; Table 4). Similarly, the o-VEMP amplitude N1–P1 in affected ears of Group III was significantly different from that in Group I (P = 0.000363; Table 4). Regarding the unaffected ears, N1 Latencies in Group II were significantly prolonged compared to those in Group I (P = 0.012; Table 4), while P1 Latencies in Group III were significantly prolonged compared with Group I (P = 0.049; Table 4). Moreover, the amplitude N1–P1 in Group III was reduced compared to that in Group I (P = 0.000095; Table 4). However, c-VEMPs latencies of P1 and N1 and the amplitudes of P1–N1 were similar in the three age groups for both affected and unaffected ears (Table 5). In sum, there were no significant differences in the latencies P1 and N1 and N1–P1 amplitude of c-VEMPs and o-VEMPs on both the affected and unaffected sides among the three age groups (Tables 4 and 5).

Table 2 The comparison of absent and elicit rates of vestibular-evoked myogenic potentials between the sudden sensorineural hearing loss groups in the affected ears, n (%).

Group	n	o-VEMP		c-VEMP
		Absent	Elicit	Absent	Elicit
I (≤ 40)	24	5 (20.83)	19 (79.17)	2 (8.3)	22 (91.7)
II (41-60)	38	12 (31.58)	26 (68.42)	13 (34.21)	25 (65.79)
III (61-80)	22	5 (22.72)	17 (72.27)	4 (18.18)	18 (81.81)
P value		P > 0.05		P < 0.05

c-VEMPs: Cervical vestibular-evoked myogenic potentials; o-VEMPs: Ocular vestibular-evoked myogenic potentials.

Table 3 The comparison of absent and elicit rates of vestibular-evoked myogenic potentials between the sudden sensorineural hearing loss groups in the unaffected ears, n (%).

Group	n	o-VEMP		c-VEMP
		Absent	Elicit	Absent	Elicit
I (≤ 40)	24	2 (8.33)	22 (91.67)	2 (8.33)	22 (91.67)
II (41-60)	38	3 (7.90)	35 (92.10)	5 (13.16)	33 (86.84)
III (61-80)	22	4 (18.18)	18 (81.82)	2 (9.09)	20 (90.91)
P value		P < 0.05		P > 0.05

c-VEMPs: Cervical vestibular-evoked myogenic potentials; o-VEMPs: Ocular vestibular-evoked myogenic potentials.

Table 4 The comparison of waveform parameters of ocular vestibular-evoked myogenic potentials between the sudden sensorineural hearing loss groups in the affected and unaffected ears.

Group	Affected ear			Unaffected ear
	N1 latency (ms)	P1 latency (ms)	N1-P1 (µV)	N1 latency (ms)	P1 latency (ms)	N1-P1 (µV)
I (≤ 40)	10.62 ± 2.05	15.23 ± 1.93	15.96 ± 5.91	9.81 ± 1.17	14.44 ± 1.56	19.23 ± 9.25
II (41-60)	11.33 ± 1.69	15.52 ± 1.62	13.22 ± 5.36a	11.10 ± 2.13c	15.40 ± 2.13	16.25 ± 10.65
III (61-80)	11.62 ± 2.63	15.64 ± 1.61	8.30 ± 2.60b	11.49 ± 2.96	16.01 ± 3.71d	8.52 ± 3.95e

^aP < 0.05 vs group III (aged 61-80).

^bP < 0.05 vs group I (aged ≤ 40 years).

^cP < 0.05 vs group I (aged ≤ 40 years).

^dP < 0.05 vs group I (aged ≤ 40 years).

^eP < 0.05 vs group I (aged ≤ 40 years).

Table 5 The comparison of waveform parameters of cervical vestibular-evoked myogenic potentials between the sudden sensorineural hearing loss groups in the affected and unaffected ears.

Group	Affected ear			Unaffected ear
	P1 latency (ms)	N1 latency (ms)	N1-P1 (µV)	P1 latency (ms)	N1 latency (ms)	N1-N1 (µV)
I (≤ 40)	15.58 ± 3.21	22.13 ± 3.19	1.23 ± 0.52	15.46 ± 3.78	21.57 ± 3.7	1.19 ± 0.61
II (41-60)	14.99 ± 3.07	21.76 ± 3.40	0.93 ± 0.33	14.93 ± 2.25	21.27 ± 2.99	1.08 ± 0.45
III (61-80)	15.11 ± 2.21	21.46 ± 2.40	1.06 ± 0.41	15.30 ± 2.19	22.02 ± 1.85	0.94 ± 0.32

DISCUSSION

Research has shown that patients with SSHL, regardless of vertigo presence, exhibit reduced c-VEMPs and o-VEMPs extraction rates. In this study, there were 19 absent c-VEMPs and 22 absent o-VEMPs in the affected ears, with 11 c-VEMPs and 11 o-VEMPs absent in patients without vertigo. There were significant differences among the groups regarding the rates of absent c-VEMPs in the affected ears. However, waveform parameters, such as threshold, latency of each wave, inter-wave period, and amplitude, did not show consistent differences. This suggests that the existence of waveforms is of diagnostic value and that most affected ears that can generate waveforms have normal or near-normal waveforms[3]. In the analysis of o-VEMPs and c-VEMPs parameter results in this study, no statistically significant differences were found in N1 Latency, P1 Latency, or P1–N1 Amplitude between the affected and contralateral ears, consistent with the literature[3]. Compared with the other VEMPs parameters, the extraction rate of VEMPs showed more diagnostic value in our study than in previous studies.

In this study, we found that among the three groups of patients, Group II had the highest number of SSHL cases, consistent with previous studies[3,5]. This group, comprising individuals aged 41–60 years, appeared to be most susceptible to vestibular system involvement, potentially attributed to age-related factors and environmental influences. Group III had the highest proportion of cases of flat-type hearing loss, and the number of patients with vertigo was fewer. Group I had the lowest number of patients with vertigo. Compared to the other two groups, Group II had the highest number of sudden deafness patients with vertigo and the highest number of profound hearing loss. It was already described that vertigo occurred more frequently in patients with profound hearing loss[3,6]. Due to the anatomical condition of the hearing and vestibular system, patients with SSHL may have vestibular dysfunction along with cochlear injury[7]. Subclinical involvement of the saccule in SSHL patients without vertigo has been documented[8]. In the present study, we examined vestibular function in SSHL patients using o-VEMPs and c-VEMPs. In patients without vertigo, a total of 11 c-VEMPs and 11 o-VEMPs were absent in the affected ears, among which eight c-VEMPs and seven o-VEMPs belonged to Group II. Similarly, Yigider et al[9] reported that even in the absence of vertigo in SSHL patients, the inferior vestibular pathway may be affected, and damage in the superior vestibular pathway correlates with the degree of SSHL. Collectively, these studies underscore that regardless of the presence of vertigo, vestibular organs are involved in SSHL[10].

Additionally, the most important result of this study, which is distinct from that of previous studies, is that Group II had the lowest c-VEMPs and o-VEMPs extraction rates in the affected ears, followed by Group III. This suggests a potentially stronger involvement of closely situated inner ear structures like the saccule. While there were significant differences among the groups regarding the absence of c-VEMPs in the affected ears, no such differences were observed for the absence of o-VEMPs in the affected ears. This discrepancy may be attributed to the differing functional roles of o-VEMPs, primarily reflecting the superior vestibular nerve and utricle, and c-VEMPs, reflecting the inferior vestibular nerve and saccule[11].

Our results indicate that the SSHL patients in Group II were more susceptible to damage to the saccule and inferior vestibular nerve, followed by those in Group III. Liu et al[12] described that the utricle may be more susceptible to damage than the saccule. It is worth noting that SSHL patients with abnormal o-VEMPs may have broader infarctions, potentially involving the anterior vestibular artery[10,13]. Our findings suggest a different pattern, with the saccule being more resistant to ischemic damage because of the vestibulocochlear artery and posterior vestibular artery, which are more abundant than the anterior vestibular artery[14]. However, Fujimoto et al[11] found that the saccule is more likely to be damaged than the utricle. In our study, the rates of absent c-VEMPs in the affected ears among the groups were statistically significant, with Group II showing the highest rate (34.12%), followed by Group III (18.18%). The rates of absent o-VEMPs in the affected ears among the groups were not statistically significant, indicating that the patients with SSHL in Group II are more susceptible to damage to the inferior vestibular nerve and the saccule, followed by those in Group III. Group I is less prone to damage to the inferior vestibular and the saccule. Hong et al[8] found that the more severe the hearing loss, the higher the probability that the saccule is involved, and compared with other types, SSHL patients with profound hearing loss showed relatively high abnormal and absent c-VEMPs rates. In our study, 16 patients (42%) in Group II with profound hearing loss (Table 1) showed significant differences compared with the other groups. In addition to being anatomically close to the cochlea, vestibular hair cells have very similar ultrastructure and share a common arterial blood supply; this supports the possibility of vestibular involvement, particularly saccular deterioration[15,16]. In this study, we also found significant differences among the groups in terms of the rates of absent o-VEMPs in the unaffected ears, but there were no significant differences among the groups for the rates of absent c-VEMPs in the unaffected ears. In the unaffected ears, Group III had the lowest o-VEMPs extraction rate (18.18%). It is considered that the function of the inner ear gradually deteriorates with age[17].

Although a growing number of studies have focused on vestibular involvement in SSHL, the specific site of inner ear damage in SSHL remains uncertain. We believe that with continuous research and observation, new discoveries will be made.

CONCLUSION

In conclusion, the extraction rate is more valuable than other VEMPs parameters. Vestibular organs are involved in SSHL regardless of the presence of vertigo. This study revealed that among the three groups, Group II had the highest number of profound hearing loss, and the c-VEMPs extraction rate in the affected ears of SSHL patients aged 41–60 was significantly lower than in the other groups. These findings indicate that patients with SSHL aged 41–60 years are more susceptible to damage to the inferior vestibular nerve innervating the saccule.

ACKNOWLEDGEMENTS

Thanks for the patients and related doctors who took part in this study.