Vestibular function assessment of Susac syndrome patients by the video head impulse test and cervical vestibular-evoked myogenic potentials

1 Introduction

Susac syndrome (retino-cochleo-cerebral vasculopathy, SuS) is an autoimmune endotheliopathy characterized by the clinical triad of encephalopathy, branch retinal artery occlusions (BRAOs), and sensorineural hearing loss (SNHL). Women are affected 3-4 times more than men, and the mean age at first presentation is between 30 and 35 years [4, 5]. It was first described in 1979 [10], and only 304 cases have been published up to 2013 [8]. The pathophysiology is not completely understood, and it has been speculated that anti-endothelial cell antibodies probably serve as a key component in disease development [18]. The diagnosis is challenging because only 13% of patients manifest the clinical triad at disease onset [8], and the triad is present in less than 30% of the cases [14]. Therefore, additional tests, such as magnetic resonance imaging (MRI) [11], fluorescein angiography [17], pure tone audiometry [15], and vestibular tests [7] play a pivotal role in early diagnosis and early intervention.

Vasculopathy in the auditory division of the audiovestibular end organs is well described. It is secondary to cochlear infarcts and usually presents as a fluctuating or stable SNHL that is usually bilateral, asymmetric, and affecting low-to-medium frequencies [3, 15]. Associated symptoms may include tinnitus and vertigo [1]. The diagnosis of vertigo among SuS patients is important for both the diagnostic and rehabilitation purposes.

The video head impulse test (vHIT) is a high-speed video-oculography system that measures eye velocity during head rotation [12]. It provides an objective measure of the vestibulo-ocular reflex (VOR), and detects both overt and covert catch-up saccades in patients with loss of vestibular function.

The vHIT was recently administered to one newly diagnosed SuS patient who presented with encepha-lopathy and small vessel infarctions of the brain [14]. Those authors postulated that vHIT should be considered as a confirmatory test of vestibulocochlear dysfunction in patients in whom SuS is suspected, with the expectation that it may detect subclinical involvement and support intense early treatment [14].

The aim of this report is to describe the vHIT and cervical vestibular-evoked myogenic potentials (cVEMPs) results of patients who were diagnosed as having SuS and treated in our tertiary referral center.

2 Materials and methods

The study was approved by the research ethics committee of the Tel-Aviv Sourasky Medical Center, which is an academic tertiary referral center (0439-17-TLV). Seven patients who were diagnosed as having SuS according to the accepted criteria for SuS [7] were recruited and tested at the otolaryngology outpatient clinic on a single day. All patients had undergone extensive medical investigation to establish the diagnosis including blood tests for auto-immune, metabolic and infectious diseases; cerebrospinal fluid analysis, brain MRI and fluorescein angiography (FA) of the eyes. Each subject underwent pure tone audiometry and word recognition testing (Interacoustics, AC40), cVEMPs (Interacoustics, Eclipse), and the v-HIT (Interacoustics, Eclipse) test. The cVEMP was conducted using air-induced stimulus, and the results included the p13, n23 wave latencies, amplitudes, and thresholds. In case no response was recorded, a bone-induced stimulus was used. The vHIT results included gain calculation and the presence or absence of saccades (overt and covert). Data on demographics and medical findings (with emphasis on the presence of audio-vestibular symptoms) were retrieved from the patients’ records and analyzed. The patients underwent microscopic otoscopy and a neuro-otologic examination.

3 Results

The study included seven patients (four females and three males, mean age 36.9±9.1 years) diagnosed with SuS. The diagnosis was definite in five of them and probable in two, according to the diagnostic criteria suggested by Kleffner et al. [7]. Age at diagnosis, time from presentation to the performance of the tests, audio-vestibular symptoms and treatment at the time of the tests are presented in Table 1. Audiometric findings, cVEMPs and vHIT results are presented in Table 2. Two patients did not complain of hearing loss or tinnitus, and there was no evidence of a SNHL on their audiograms. Four patients complained of tinnitus, and three patients described true vertigo.

The cVEMPs results were abnormal in only three patients (#1, #6, #7), and only one of them (patient #1) complained of vertigo. A higher amplitude was found on the right side, with a difference of 31% compared to the left side in the latter patient. The air-induced cVEMPs results of patient #6 were: normal response on the right, no response on the left (Fig. 1). The bone-induced cVEMPs results of this patient were: a normal response on the right, no response on the left side. There was also no response to both air- and bone-induced VEMPs on the left side of patient #7. The response to a bone conducted stimuli of this patient, on the right side, was normal. Both patients did not experience vertigo.

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Fig. 1

The result of cVEMP using air conduction stimulus, patient#6:normal response on the right, no response on the left.

The vHIT results were normal in six out of the seven patients (Fig. 2). The exception was patient #2, who was one of the patients who complained of vertigo. The calculated gain of the left anterior semicircular canal for that patient was 0.5, without saccades.

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Fig. 2

The results of vHIT, patient #3: normal.

Figure 3 demonstrates angiographic signs of Sus-ac’s Syndrome on FA, and Fig. 4 demonstrates brain MRI results of patient #2.

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Fig. 3

Angiographic signs of Susac Syndrome. Fluorescein ang-iography of the right eye (patient#4): Peripapillary arterial wall hyperfloresence and nasal distal branch retinal artery occlusion.

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Fig. 4

MRI scans of patient#2 showing: 1. Sagittal and axial T2 FLAIR sequence: hyperintense lesions in the corpus callosum (“snow balls”); 2,3. hyperintense lesions in the periventricular and subcortical areas; 4. Sagittal T1 sequence of the corpus callosum (“black holes”); 5. Axial DWI sequence which show restricted diffusion; 6. Leptomeningeal enhancement with gadolinium.

The diagnosis of SuS relies on laboratory, radiological and other complementary tests which may be time consuming and bothersome to the patient. Most of the blood supply to the inner ear arrives from the labyrinthine artery, which is generally a branch of the anterior inferior cerebellar artery (AICA). Not much of a collateral supply exists. Hence it is reasonable to assume that the inner ear could potentially be affected in SuS. Marrodan et al. [14] recommended the use of vHIT in SuS since it is comfortable to the patient, and also fast and easy to perform. The objective of the current report was to determine whether the vHIT can serve as a confirmatory assessment of vestibulocochlear dysfunction in cases of suspected SuS. We postulated that this exam may also serve as an adjunctive tool in the diagnosis or follow-up of patients with SuS.

Marrodan et al. reported of a patient with SuS and evidence of a right-sided posterior canal dysfunction on the vHIT [14]. In our study, the vHIT failed to demonstrate any abnormalities in six of our seven patients. It is possible that the vHIT may not be able to detect a specific insult to the inner ear that may be measurable by other exams, as in the case of Meniere’s disease [13]. Since the vHIT detects pathologies at the high frequencies of rotation, it is reasonable to assume that SuS does not affect those frequencies. As type I receptors in the inner ear are more responsive to high frequencies [9], these are probably not affected by the disease, possibly due to different effect of ischemia on the different cell types. In addition to that, the pathogenesis of SuS is vasculopathy, which affects the inner ear, but it is also possible that some other mechanism is causing the vertigo, such as microinfarctions of the cerebellum or the brainstem [19], and that the culpable pathology may not be detectable by the vHIT.

Magliulo et al. suggested the use of cVEMPs as a diagnostic exam in SuS patients [6]. Kleffner described two SuS patients out of 30 with abnormal VEMP results [7]. The cVEMPs results were abnormal in three out of the seven patients in the current study, in accordance with those studies.

A limitation to this study is that the patients did not undergo Electronystagmography (ENG) examination and so we could not compare the results of ENG with those of the vHIT. Such a comparison may shed more light on the role of the vHIT in the diagnosis of SuS. However, as ENG includes mandatory noxious vestibular stimulation, it is hard to justify for research purposes. In addition to that, all the patients were treated at the time they were examined, a fact which may have affected the tests’ results.

The diagnosis of SuS may be elusive since it requires a high index of suspicion and collaboration between various medical disciplines. However, the growing awareness of this syndrome and the advances in diagnostic tools may speed up and facilitate diagnosis and initiation of treatment of these patients.

This is the first study to describe the results of vHIT and cVEMPs among a cohort of patients diagnosed with SuS. Our results suggest that the vHIT should not be the stand-alone exam for measuring the function of the vestibular system of SuS patients, whether or not they are symptomatic for vertigo or dizziness. VEMPs and vHIT may serve as ancillary tests in cases where audiometry and FA results are inconclusive or negative. The use of vHIT in the diagnosis of SuS is potentially beneficial. Further studies on more patients and investigations that also include comparisons of the results of vHIT with those of ENG exams are warranted, in order to establish the value of vHIT in the diagnosis and follow-up of SuS.

Conflict of interest

None

Financial disclosure

There are no financial interests, arrangements or payments to disclose