European Archives of Oto-Rhino-Laryngology

, Volume 270, Issue 8, pp 2207–2214

Involvement of peripheral vestibular nerve in individuals with auditory neuropathy

Authors

    • Department of AudiologyAll India Institute of Speech and Hearing
  • Animesh Barman
    • Department of AudiologyAll India Institute of Speech and Hearing
  • Niraj Kumar Singh
    • Department of AudiologyAll India Institute of Speech and Hearing
  • G. Rajeshwari
    • Department of OtorhinolaryngologyAll India Institute of Speech and Hearing
  • R. Sharanya
    • Department of AudiologyAll India Institute of Speech and Hearing
Otology

DOI: 10.1007/s00405-012-2272-4

Cite this article as:
Sinha, S.K., Barman, A., Singh, N.K. et al. Eur Arch Otorhinolaryngol (2013) 270: 2207. doi:10.1007/s00405-012-2272-4

Abstract

The vestibulocochlear nerve is a sensory nerve that serves the organs of hearing and equilibrium. Neuropathies of the nerve, particularly auditory neuropathy may be caused by primary demyelination or by axonal diseases. In disorders affecting the cochlear nerve, it is probable that the vestibular nerve is involved as well. There are isolated reports of the involvement of the inferior vestibular nerve (using vestibular-evoked myogenic potentials) in individuals with AN. However, there is a dearth of information on the involvement of the superior vestibular nerve and other functions such as optokinetic, saccade and vestibulo-occular reflex. A total of three subjects diagnosed as having auditory neuropathy, underwent an extensive vestibular assessment consisting of clinical tests of stability (Romberg, Fukuda stepping test), administration of dizziness questionnaire developed by Maryland hearing and balance centre, cervical vestibular-evoked myogenic potentials and a standard electronystagmography test battery. In the present study, the entire subject population assessed showed hypofunctional caloric responses and absent VEMPs. Two out of the three subjects were asymptomatic of vestibular dysfunction. On the clinical tests of stability, two subjects showed deviations to the right, while one subject performed normally. Thus, the present study indicates a possible involvement of peripheral vestibular nerve involvement in individuals with auditory neuropathy.

Keywords

Auditory neuropathyVestibular-evoked myogenic potentialsElectronystagmographyVestibular neuropathy

Introduction

Auditory neuropathy (AN) is characterized by a unique pattern of hearing loss and absent or severely distorted auditory brainstem responses (ABRs) with preservation of outer hair cell function, as revealed by otoacoustic emissions (OAEs) and/or measurable cochlear microphonics [1]. The abnormality of the VIII nerve could be at the level of the inner hair cells, the synapse between inner hair cells and VIII nerve fibres, the ganglion neurons, the nerve fibres, or may be a combination of the above [2]. The prevalence of auditory neuropathy varies significantly in the studies. Davis and Hirsh [3] reported that one in every 200 hearing-impaired children have audiologic findings consistent with a contemporary diagnosis of AN. Berlin et al. [4] estimated that AN/AD is present in at least 4 % of children having permanent hearing loss, on the other hand Tang et al. [5] reported a prevalence of 1.8 % in school going children with sensorineural hearing loss. In the Indian scenario, Kumar and Jayram [6] reported a prevalence of 0.54 % or 1 in 183 persons with sensorineural hearing loss.

In the existing literature, auditory neuropathy has predominantly been investigated as a solitary concern. The symptomatology, clinical findings and aetiology of the neuropathic condition are discussed usually in relation to one component of the VIII cranial nerve which is the cochlear branch. Apart from the cochlear branch, the VIII cranial nerve also contains the superior and inferior branch of the vestibular nerve. It is likely that a neuropathic condition involving the cochlear nerve may also affect the vestibular nerve. However, the incidence of vestibular neuropathies in patients with AN is not known because they are usually not considered the prime candidates to undergo vestibular evaluations. The subtlety of their symptoms may be the cause for such a belief.

There are few reports available in the literature regarding the involvement of the vestibular nerve in individuals with AN [1, 2, 79]. Starr et al. [2], initially described 10 subjects with AN, two of whom had absent responses to caloric testing, indicating a possible involvement of superior vestibular nerve and also three other subjects showed horizontal nystagmus on lateral gaze. All five patients had peripheral neuropathy which led the authors to suggest that the abnormal auditory and vestibular test results were part of a generalized neuropathic disorder affecting both the components of cranial nerve VIII.

Kumar et al. [9] reported that 80 % of the ears with auditory neuropathy assessed had abnormal vestibular-evoked myogenic responses (VEMP) results. This study has reported of a possible involvement of inferior vestibular nerve in individuals with AN. Also, Kaga [10] reported the involvement of superior as well as the inferior vestibular nerve of 8 individuals with AN in the absence of peripheral neuropathy. Kaga [10] reported that ice water caloric stimulation failed to elicit any response on electronystagmography (ENG), and VEMPs were also abolished in five of the AN subjects. These subjects were therefore categorized to have ‘auditory-vestibular neuropathy’. Three other subjects performed normally on the vestibular evaluations and were thereby diagnosed to have ‘auditory neuropathy only’.

Determination of the involvement of the vestibular branch of the nerve, to be diagnosed as having auditory-vestibular neuropathy or auditory neuropathy only is made possible using an assortment of vestibular tests such as ENG and VEMP. Each of these tests examines only a part of the vestibular system, and it is not appropriate to presume normality of the organ or abnormal functioning of the system based on results of just one test.

There is sporadic information regarding vestibular abnormality either based on ENG test results or VEMP test results. Interestingly, all of them have indicated certain degree of vestibular abnormality in most of the clients with AN, they have studied. In addition, in subjects with AN, there have been no reports on the functioning of the other vital components for balance such as optokinetic and saccade systems which together comprise of the central oculomotor system. Also, the vestibular signs and symptoms exhibited by these individuals have not been reported in conjunction with the objective and subjective tests of the vestibular system.

The primary aim of the study was to ascertain the involvement of different vestibular pathways in individuals with AN. The study also aimed at assessing the function of other components of the balance system such as the saccade and optokinetic system in individuals with AN. Further, the study aimed at finding a relationship between subjective signs and symptoms in conjunction with the test findings.

Materials and method

Participants

A total of three subjects, diagnosed as having auditory neuropathy, in the age range of 19–21 years were evaluated. All the subjects had sensorineural hearing loss in both ears and were diagnosed to have bilateral auditory neuropathy based on the criteria of normal outer hair cell function as evidenced by the preservation of OAEs, abnormal ABR, poor speech identification and absent acoustic reflexes to the ipsilateral and contralateral tones. The subjects had UCL greater than 105 dB HL for speech. Neurological examination revealed the absence of space occupying lesion, and the subjects did not complain of any other illness prior to the testing. The audiological test profile of the three subjects is described in Table 1.
Table 1

Audiological profile of individuals with auditory neuropathy

Sl. No

Age/Gender

Ear

Air conduction threshold

SIS (%)

ABR

OAE

Tympanometry with reflexes

250 Hz

500 Hz

1 kHz

2 kHz

4 kHz

8 kHz

1.

19 years/M

R

30

30

15

20

5

10

56

AB

PT

‘A’-NR

L

25

25

25

15

15

20

48

AB

PT

‘A’-NR

2.

21 years/M

R

35

35

45

45

45

25

0

AB

PT

‘A’-NR

L

35

40

40

40

35

25

0

AB

PT

‘A’-NR

3.

22 years/F

R

70

70

65

45

30

20

0

AB

PT

‘A’-NR

L

55

55

55

30

15

10

0

AB

PT

‘A’-NR

AB absent, PT present, NR no reflexes, SIS speech identification score, ABR auditory brainstem responses, OAE otoacoustic emissions

Case history and administration of dizziness questionnaire

A detailed clinical history was obtained regarding the nature, frequency and triggering mechanism of the vertiginous attacks. Information was also obtained regarding the existence of associated visual, neurological conditions along with pertinent medical history. In addition, a part of the dizziness questionnaire was administered. The questionnaire consists of section which pertains to the symptoms of dizziness was administered.

Clinical tests of stability

Romberg test

The subjects were instructed to stand with their feet together and arms stretched out. They were then asked to remain in the position for a few minutes in both eyes open and eyes closed position and the direction and amount of sway for each was compared.

Fukuda stepping test

The subjects were asked to march on a fixed spot, with eyes closed and hands outstretched. The angle, direction and distance of deviation from the initial source were noted.

Vestibular-evoked myogenic potentials

The subjects were seated in an upright position and were instructed to turn their heads to the side opposite to the test ear to activate the sternocleidomastoid muscle (SCM) unilaterally. Visual feedback was provided for the subjects to monitor tonic electromyographical activity of the SCM which was to be maintained between 100 and 200 % (50–100 μv) on the visual feedback system. VEMP was recorded for all the subjects with 500 Hz tone burst stimulus using Intelligent Hearing Systems. A 500-Hz tone burst stimulus was utilized; based on the reports, with the 500-Hz tone burst stimulus, amplitude of the VEMP is larger [11]. AgCl electrodes were used to record the VEMP responses. Noninverting electrode was placed on ipsilateral SCM, inverting on sternoclavicular joint and the ground electrode on the forehead. The responses were filtered from 30 to 1500 Hz. Analysis time was kept at 50 ms and a total of 100 stimuli with a repetition rate of 5.1/s were presented at 95 dBnHL intensity in alternating polarity. Waveforms produced in response to tone burst stimuli were recorded twice to ensure reliability.

Electronystagmography

The participants underwent an ENG test battery consisting of recordings of positional, positioning, gaze (30° lateral gaze) and caloric-induced nystagmus. Oculomotor system integrity was also evaluated by means of saccadic and optokinetic test. RMS ENG instrument was used to record the responses. The electrode sites were cleaned with a skin preparation agent to remove grime to ensure good skin–electrode contact. Ten-20 conduction paste was used and the electrodes were firmly applied to the respective sites. A single channel recording of horizontal eye movements was obtained by placing the non-inverting electrode to the skin of the temples 1.5 cm lateral to the outer canthi of the right eye and the inverting electrode 1.5 cm lateral to the outer canthi of the left eye. The ground electrode was placed on the forehead. The responses were filtered from 0.01 to 30 Hz. Calibration of the ENG instrument was carried out prior to the eye movement recordings for each of the participants.

Caloric test was interpreted with the help of Claussen Butterfly chart [12]. As per the butterfly chart, responses which fell within the normal limits of culmination frequency were designated as normal, those below it as hypoactive and those above it as hyperactive. Further a code system was utilised to describe the responses of the caloric test [13]. The caloric responses were designated by digits: normal = 0; hypoactive = 1; hyperactive = 2. Thus, a code [0 0 0 0] indicates a normal caloric response, whereas code [1 1 1 1] indicates a hypoactive responses in both the ears.

Results

The audiological test results and the results obtained on the extensive vestibular tests have been discussed for each of the three subjects. This would achieve a better understanding of the extent of the vestibular dysfunction and also help in establishing a relationship between their audiological and vestibular test findings.

Participant 1

Participant 1 was a 19-year-old male with a complaint of reduced hearing sensitivity and difficulty in understanding speech, particularly in noisy environments since 6 years. The condition was reported to be of sudden onset and progressive in nature. He had no other otological or neurological complaints. The results of the audiological evaluations which were carried out a year ago indicated minimal hearing loss in the right ear and hearing sensitivity within normal limits in the left ear. Auditory function tests results have been described in Table 1. Based on the audiological test results, he was suspected to have AN in both ears.

The dizziness questionnaire revealed that the participant had occasional episodes of light-headedness that occurred when he was fatigued. It lasted for 1 to 2 min and such attacks were triggered by sudden turning of the head or standing up from a supine position. There was no report of any other associated vegetative symptoms. During the Romberg test, the participant reported of perception of falling to the right. On Fukuda stepping test, rightward sway was present.

Assessment of sacculo-collic function through recording VEMP revealed absence of any responses. ENG test battery revealed normal functioning on the saccades and gaze test. The traces for positioning and positional test showed a lack of deflections indicating an absence of nystagmus. The performance on the optokinetic test could not be assessed due to complaint of perception of double vision on the task. Bithermal caloric stimulation failed to elicit any significant nystagmus activity and the participant was deemed to have hypofunctional (code: 1111) vestibular system. Figure 1 shows the butterfly chart obtained from the subject. In summary, the participant had absent VEMP and caloric responses. He complained of occasional episodes of light-headedness. Deviations to the right were evident on the Romberg and the Fukuda stepping tests.
https://static-content.springer.com/image/art%3A10.1007%2Fs00405-012-2272-4/MediaObjects/405_2012_2272_Fig1_HTML.gif
Fig. 1

The nystagmus recorded during the caloric test and the butterfly chart obtained from client-1 (RW right warm, LW left warm, RC right cold, LC left cold; warm responses elicited with 44 °C water temperature, cold response elicited with 30 °C water temperature)

Participant 2

The 21-year-old male presented with complaints of reduced hearing sensitivity in both ears since 9½ years of age. There were no reports of any other otological or neurological complaints. Auditory function tests results have been described in Table 1 which indicated him having AN in both ears. On administration of the dizziness questionnaire, the participant did not report of any vertigo or related balance problems. In addition, he performed within normal limits on Romberg and Fukuda stepping test. VEMP responses were absent in both the ears. On the ENG test battery, the participant performed within normal range on the eye tracking tests that involved saccades, gaze and optokinetic test. The positioning and positional test traces were also devoid of any nystagmic beats. Similar to participant 1, caloric stimulation also yielded hypofunctional responses in participant 2. Figure 2 shows the recordings of bithermal caloric recordings and the consequent butterfly chart. To summarise the results, the participant did not have any significant subjective complaints and performed normally on all the tests of stability as well as the central oculomotor tests. He had absent VEMP responses and a hypofunctional caloric response with a code of 1111 on the butterfly chart.
https://static-content.springer.com/image/art%3A10.1007%2Fs00405-012-2272-4/MediaObjects/405_2012_2272_Fig2_HTML.gif
Fig. 2

The nystagmus recorded during the caloric test and the butterfly chart obtained from client-2 (RW right warm, LW left warm, RC right cold, LC left cold; warm responses elicited with 44 °C water temperature, cold response elicited with 30 °C water temperature)

Participant 3

A 22-year-old female came to the clinic with the complaint of inability to perceive speech in noise as well as reduced hearing sensitivity and intermittent tinnitus in both ears. In addition, she also complained of episodes of headache of varying severity. The symptoms persisted through 6 months and were progressive in nature. Auditory function tests results have been described in Table 1, indicating AN in both ears. On the dizziness questionnaire, the participant complained of vertiginous attacks, lasting 3–4 min since 6 months with an incidence of 1–2 attacks a month. The attacks were accompanied by blurring of vision and headaches occasionally. The triggering factors were noted to be abrupt turning of the head as well as subjective changes in position. On the Romberg test, the participant swayed in a front back motion in the eyes closed position and a deviation of 50° towards the right was evident during the Fukuda stepping test in the eyes closed position. VEMP responses were abolished in this participant as well. Central ENG test battery findings were normal and so were the findings for the positional and the positioning tests. Caloric irrigation elicited minimal nystagmus activity in the participant thereby resulting in a code of 1111. The findings were indicative of hypofunctionality of the vestibular system. To sum up, the participant had active vestibular symptoms since 6 months. Deviation to the right was obtained on the fukuda stepping test. The VEMP responses in the participant were absent and hypofunctional caloric responses were obtained. Performances on the central oculomotor as well as the positioning and positional tests were normal (Fig. 3).
https://static-content.springer.com/image/art%3A10.1007%2Fs00405-012-2272-4/MediaObjects/405_2012_2272_Fig3_HTML.gif
Fig. 3

The nystagmus recorded during the caloric test and the consequent butterfly chart from client-3 (RW right warm, LW left warm, RC right cold, LC left cold; warm responses elicited with 44 °C water temperature, cold response elicited with 30 °C water temperature)

Discussion

In the present study, assessment of the vestibular functioning in individuals with AN was carried out. In all the three participant, characteristic finding of normal central oculomotor system functioning, absent VEMP responses in both ears and bilateral hypofunctional caloric responses were obtained. Participants 1 and 2 did not report of any significant complaints regarding the vestibular symptoms whereas the third participant did complain of vestibular symptoms ranging over 6 months. Two of the three participants also exhibited rightward deviations on tests of stability. All the participants showed normal test results on the ENG test battery that assesses for central involvement (saccadic, gaze and optokinetic induced eye movement’s examinations). Such a finding in individuals with AN is indicative of an intact central oculomotor system tract and its normal functioning. This is in agreement with the findings of Starr et al. [14], who reported that the distal portion of the vestibular nerve was found to have a beaded appearance compared to the proximal portion, suggesting the extent of the pathology to be restricted to the distal portion of the nerve. It has been widely reported that that distal portion of the nerve is myelinated by the Schwann cells while the central portion by the oligodendroglial cells [15]. Thus, it can be hypothesised that the neuropathy may be restricted to the Schwann cells and not the oligodendroglial cells. Thus, these central occulomotor pathways, myelinated by the oligodendroglial cells, may not undergo such changes, therefore resulting in a normal finding on these tests.

No abnormal eye movements were recorded during the positioning and positional test in all the subjects. A finding of the absence of nystagmus during positioning test occurs due to the absence of otoconial debris in the semicircular canal or adhering to the cupula. This is indicative of the absence of benign positional paroxysmal vertigo in the participant. Starr et al. [14] reported that the sensory epithelium of the vestibular end organs in subjects with AN was similar to that of normal individuals. This explains the normal results obtained on the positional test which is designed to stimulate the otolith organs.

In addition, caloric irrigation of the six ears failed to elicit any caloric-induced nystagmus thereby indicating a dysfunction of the horizontal semicircular canal and/or its innervations, the superior vestibular nerve. Taken together, the clinical findings suggest towards the extension of the neuropathic condition to the vestibular nerve in the presence of intact central vestibular connections. These findings correlate with the anatomical changes found on the vestibular nerve in individuals with AN [14]. It has been reported that the nerve itself had structural changes that were not found in the normal control group. The overall vestibular nerve population between the receptor organ and the ganglion within the internal auditory meatus has been reported to be reduced [14]. In the AN individuals who were found to have vestibular involvement, both the auditory as well as the vestibular nerve had an irregular beaded appearance [14]. Further, fragmentation of the myelin layer with gaps nearly equal to the diameter of the nerve fibres has been reported along with the distortion of the nerve structure [14]. Such changes in the structure of the vestibular nerve probably existed in the three subjects and could explain the findings of absent caloric responses obtained in the current study.

Another significant finding was that of abolished VEMPs in all six ears. This could possibly be indicative of a dysfunction along the inferior vestibular nerve and/or its end organ the sacculus. Such a deterioration of the sacculo-collic pathways functioning in individuals with auditory neuropathy has been hypothesized to occur due the commonalities shared by the auditory and the vestibular systems. There are similarities in cochlear and vestibular hair cell ultra structures in addition to the common arterial blood supply to the cochlea and vestibular end organs [14]. The obtained findings could point towards the presence of the demyelination/axonal degeneration or a combination of both pathological conditions in the inferior vestibular nerve as well [1, 4].

On the dizziness questionnaire, two of the participants were found asymptomatic for vertigo. The absence of concomitant vestibular symptoms has been hypothesized to be related to the bilateral distribution of the disorder and the slow progression of vestibular neuropathy [9, 16]. The asymptomatic nature could also be related to larger diameter of vestibular nerve fibres compared to their auditory counterparts [14]. It is well reported that the conduction of action potentials is slower in neurons with smaller diameter than their larger counterparts [17]. The presence of a pathological condition, such as demyelination, is likely to affect the physiological functioning and conduction properties of the smaller diameter fibres (i.e. the auditory fibres) to a greater extent over the larger diameter fibres (the vestibular nerve fibres). It can thus be hypothesized that the over manifestation as well as progression of the auditory deficits would be earlier and greater than that of the vestibular symptoms; this is expected to therefore provide more opportunities for compensation to occur for the vestibular symptoms.

In the current study, only participant 3 reported of vertigo. This may be attributed to a lack of effective central compensation owing to relatively smaller duration since onset and/or intake of vestibular suppressant drugs which have been reported to retard the process of compensation [18]. This lack of effective central compensation could be further emphasized by a rightward sway on Romberg and Fukuda stepping test. A similar sway was exhibited by participant 1 whereas participant 2 did not show signs of abnormal deviation or sway. These findings may be the result of asymmetrical pathologies in participants 1 and 3 as opposed to symmetrical pathology in participant 2. Similar asymmetrical results were portrayed on pure-tone thresholds by participants 1 and 3 but not by 2. This could possibly indicate towards a higher severity of the neuropathic condition in the right ear compared to the left for the participants 1 and 3. These findings, however, need to be interpreted with caution and on a case to case basis in other subjects.

One of the limitations of the present study is that we have administered only a limited number of objective tests (i.e. the electronystagmography and vestibular-evoked myogenic potentials). Certain other tests such as rotatory chair test (at low and high frequency), visual subjective vertical test, ENG with a sweep test could not be administered due to technical limitations. Hence the readers are advised to interpret the results of the above study with respect to the tests administered in the present study.

Conclusions

In the present study, the collective findings of the absence of positioning and positional nystagmus along with normal results on oculomotor test in the presence of abnormal caloric and VEMP responses in the three subjects reflects the possible involvement of both the superior and inferior vestibular nerve in AN.

Conflict of interest

None.

Copyright information

© Springer-Verlag Berlin Heidelberg 2012