|Year : 2016 | Volume
| Issue : 4 | Page : 268-274
Auditory function in vestibular migraine
John Mathew, Ramanathan Chandrasekharan, Ann Mary Augustine, Anjali Lepcha, Achamma Balraj
Department of ENT, Christian Medical College, Vellore, Tamil Nadu, India
|Date of Web Publication||13-Oct-2016|
Department of ENT, Christian Medical College, Vellore - 632 004, Tamil Nadu
Source of Support: None, Conflict of Interest: None
Introduction: Vestibular migraine (VM) is a vestibular syndrome seen in patients with migraine and is characterized by short spells of spontaneous or positional vertigo which lasts between a few seconds to weeks. Migraine and VM are considered to be a result of chemical abnormalities in the serotonin pathway. Neuhauser's diagnostic criteria for vestibular migraine is widely accepted. Research on VM is still limited and there are few studies which have been published on this topic. Materials and Methods: This study has two parts. In the first part, we did a retrospective chart review of eighty consecutive patients who were diagnosed with vestibular migraine and determined the frequency of auditory dysfunction in these patients. The second part was a prospective case control study in which we compared the audiological parameters of thirty patients diagnosed with VM with thirty normal controls to look for any significant differences. Results: The frequency of vestibular migraine in our population is 22%. The frequency of hearing loss in VM is 33%. Conclusion: There is a significant difference between cases and controls with regards to the presence of distortion product otoacoustic emissions in both ears. This finding suggests that the hearing loss in VM is cochlear in origin.
Keywords: Auditory function, Otoacoustic emission, Vestibular Migraine
|How to cite this article:|
Mathew J, Chandrasekharan R, Augustine AM, Lepcha A, Balraj A. Auditory function in vestibular migraine. Indian J Otol 2016;22:268-74
| Introduction|| |
Vestibular migraine (VM) is defined as vertigo or dizziness caused by migraine. Approximately, 10% of the population has migraine headaches  and one third of these patients experience dizziness,  so the prevalence of VM can be estimated as approximately 3% of the population. Vestibular symptoms can be surrounding rotatory type, head rotatory type, light-headedness, and imbalance.  They can also present with auditory complaints such as tinnitus, aural fullness, decreased hearing, and phonophobia. , There are reports of sudden, permanent, and fluctuating hearing loss associated with migraine However, the incidence of hearing loss in migraine is low. ,,
Glial and neuronal depolarisation occurring at cortical and brainstem levels is regarded as the mechanism of migraine aura. , The longer lasting vestibular symptoms can be attributed to the activity of the trigeminovascular system causing release of various inflammatory neuropeptides into the dural circulation during headache. 
VM is essentially a diagnosis of exclusion. Physical examination is likely to be normal. Various investigations that could be done include imaging of the brain, otoacoustic emissions, auditory brain stem evoked response, and audiometry in order to exclude other pathological conditions. Studies have shown that the interpeak and absolute latencies during brainstem evoked response testing could be prolonged in vestibular migraine.  This may be the earliest indicator of impending auditory involvement in migraine. 
There are few studies done on the auditory dysfunction present in VM. Hence, this research was undertaken to evaluate the auditory functions in VM.
There are two parts to this study. The first part was a retrospective chart review of eighty consecutive patients who were diagnosed with VM to determine the frequency of auditory dysfunction in these patients. The second part was a prospective case control study in which we compared the audiological parameters of thirty patients diagnosed with vestibular migraine with thirty controls to look for any significant differences.
| Materials and Methods|| |
This study was carried out in the Audio Vestibular Laboratory and ENT Department of a Tertiary Care Teaching Hospital after obtaining the Institutional Review Board approval.
Selection of cases
In the first part of the study, a retrospective chart review was conducted in eighty consecutive patients diagnosed with VM as per Neuhauser's criteria  in the period between 2011 and 2013. The second part was a prospective case control study in which we compared the audiological parameters of thirty patients diagnosed with vestibular migraine with thirty controls to look for any significant differences. A detailed history and examination was done for patients in the prospective arm as per the proforma attached [Appendix 1 [Additional file 1]]. About 30 age-matched healthy controls were recruited from the general population.
The inclusion and exclusion criteria for both parts of the study were as follows:
- Age between 18 and 60 years
- All patients diagnosed with VM.
Patients with typical history of benign paroxysmal positional vertigo (and a positive Dix Hallpike's manoeuvre), patients with Meniere's disease past history of chronic discharging ears/history of surgery to ear/history of permanent hearing loss, other neurological disorders such as stroke and intracranial tumors, anyone with prolonged noise exposure, history of ototoxic medications, otosclerosis or with a history of head or ear trauma, diabetes mellitus, hypertension, or ischemic heart disease were excluded from the study.
All prospective patients underwent relevant blood tests to exclude patients with dyslipidemia, diabetes mellitus, hypothyroidism, and anemia. All patients and controls underwent pure tone audiometry (PTA), impedance audiometry, brainstem evoked response audiometry (BERA), and distortion product otoacoustic emissions (DPOAE).
PTA was done using GSI audiostar pro, clinical two channel audiometer from Grason-Stadler, USA, 2010. The GSI standard tympstar (Grason-Stadler, USA, 2011) was used to obtain immittance measurements. DPOAE was tested using ER 10D manufactured by intelligent hearing systems, USA, 2011. BERA measurements were carried out using Intelligent hearing system launch pad version 2.32 X, USA, 2010.
Categorical data was presented as frequency with percentages. The continuous data with normal distribution was presented as mean with standard deviation, while nonnormally distributed data was presented as median with range. Comparison between categorical variables was done using Fishers exact test. A P ≤ 0.05 was considered statistically significant. Statistical analysis was done using SPSS for Windows v13 (SPSS Inc.Released 2007, SPSS for Windows, Version 13.0. Chicago, SPSS Inc).
| Results|| |
Hearing loss was graded using the American Speech and Hearing Association guidelines.  Conductive hearing loss was taken as air bone gap was more than 25 dB with bone conduction being <10 dB. Poor wave form morphology on auditory brainstem response testing was diagnosed when waveforms showing prolongation of inter peak latencies (IPL) i.e., Wave I to V delay more than 3.84 ms with standard deviation of 0.16 or abnormal amplitude ratios. The presence of otoacoustic emissions was taken as normal cochlear function present at the frequency of stimulus and the absence of DPOAE was taken as absence of otoacoustic emissions over a more restricted frequency range, at least third of an octave indicating abnormal outer hair cell function. 
Among the eighty patients included in the retrospective chart review, majority were in the 30-50 age group [Figure 1] and there were 44 (55%) females and 36 (45%) males. Most of the patients had normal hearing (53 of 80); 26 of 80 had bilateral mild sensorineural hearing loss (SNHL) and one patient had unilateral mild SNHL [Figure 2]. Of the 27 patients who had mild SNHL, 16 were in the age group of 31-40 years; 9 were in the 41-50 years age group; and one each was in the 21-30 and 51-60 years age groups [Figure 3].
In the prospective comparative part of the study, there were 11 males and 19 females in the study group and 16 males and 14 females in the control group. Most of the patients and the controls were in the age groups 20-40 years [Table 1]. All the thirty patients in the study group had headache sometime during their lifetime which were similar in nature each time in 27 patients. [Table 2] shows the localization of the headache. Since the choices are not mutually exclusive, each patient could have had more than one response. The most frequent site of headache was at the occipital region. Twenty-one patients had headache for more than 11 years; and nine had headache for 10 years or less. The duration of an average attack of headache was 1 h or less in 17 patients, 1-2 h in 12 and one patient had for more than 2 h [Figure 4]. A majority (83%) had two or more attacks of headache a month. All thirty experienced a throb during attacks of migraine, while nine had dizzy spells when they did not have a headache. Positional vertigo was noted in nine and motion sickness in ten patients. Twenty-five patients had a positive family history of migraine. Among the thirty patients, all experienced aura during the attack of headache or within an hour before or after the attack of headache. At least one of the brain stem symptoms such as unsteadiness, zigzag lights in vision, darkness in vision and double vision, tinnitus, and hearing loss was experienced by all the patients [Figure 5]. The dizzy spells of 16 out of 30 patients of VM were accompanied by auditory symptoms such as tinnitus and decreased hearing. Out of the thirty patients, twenty had normal PTA, nine had bilateral mild SNHL, and one patient had unilateral mild SNHL. All controls had normal audiometry. Tympanometry in all patients showed an A type curve and stapedial reflux was present in all thirty patients except one. Audiological test results, when compared in patients with and without auditory symptoms did not show any significant differences [Table 3].
|Table 3: Pure tone audiometry, brainstem evoked response audiometry and distortion product otoacoustic emission results in migrainous patients with and without auditory symptoms|
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On comparing the patients and controls with normal and abnormal DPOAE in the right ear and left ear, difference was statistically significant in both ears (P = 0.011) [Table 4]. When the normal and abnormal BERA absolute latencies of Waves I, III, and V in the right ear and left ear in patients and controls were compared, we found that the difference in absolute latency of Wave V in the right ear was statistically significant but values in the cases were overall lower than the controls. Difference in all other absolute latencies did not reach significance [Table 5]. The difference in IPL of Waves I-III, III-V, and I-V in the right ear and left ear, when compared in patients and controls, was not found to be statistically significant [Table 6].
|Table 5: Number of patients and controls with normal and abnormal absolute latency of Wave I, III, IV in the both ears and the test of significance|
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|Table 6: Number of patients and controls with normal and abnormal inter peak latencies of Waves I-III, III-V, and I-V in the both ears and the test of significance|
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| Discussion|| |
Neuhauser et al. in 2001 proposed diagnostic criteria for definite and probable VM.  The pathophysiology of VM, despite intense study, is still poorly understood but migraine has been conceptualized as a disorder of impaired sensory modulation.  Migraine sufferers are more sensitive to numerous unpleasant sensory inputs and these inputs trigger a threshold which causes a cortical event followed by a brainstem event causing more input to be perceived as noxious resulting in headache. Thus, the brain of migraine sufferers is hyper excitable. Similar mechanisms are proposed for VM. The cortical spreading depression may play a role in patients who are having short attacks.  This mechanism can produce vestibular symptoms when the sensory cortical areas at the posterior insula and temporoparietal junction are involved.  Calcitonin gene related peptide, serotonin, adrenaline, and dopamine involved in the pathogenesis of migraine also modulate the activity of a number of central and peripheral vestibular neurons thus contributing to the pathogenesis of vestibular migraine. ,,, The unilateral release of these substances causes one-sided headache and a static vestibular imbalance resulting in rotatory vertigo. Bilateral release of these substances could result in motion sickness type of dizziness. Episodic vertigo has been associated with certain genetic syndromes. Otologic symptoms such as phonophobia and hyperacusis seen in migraine patients might be related to stress induced headache. 
In the retrospective aspect of our study, the age group at which vestibular migraine was most common, was found to be between 31 and 40 years (46/80) followed by 41-50 years (26/80). Literature says that vestibular migraine can occur at any age group. ,,, The female to male ratio in our study was 1.22 is to 1 which is similar to that reported in literature. ,,, A frequency of 27/80 (21%) patients was found to have documented evidence of hearing loss in our chart review. However, there are studies which have reported lesser numbers. , The degree of hearing loss noted by us was mild and the age group at which hearing loss occurred maximum was between 31 and 40 years (16/27). This could be attributed to the maximum number of patients of VM belonging to this age group. Another study noted hearing loss ranging from mild to profound and hearing loss having equal distribution in younger adults vs older adults. 
In the second part of the study, which was prospective with controls, of the 30 diagnosed with VM, 19 were females and 11 were males, the ratio being 1.73, which is similar to what is reported. ,, The duration of each attack of headache was most commonly less than 1 h (17/30), followed by 1-2 h (12/30) and this finding is similar to other studies.  Thirty percent of patients in this study, experienced dizzy spells outside the period of headache; studies quote up to half (48%) experiencing dizzy spells outside the period of headache.  In this study, 30% of patients experienced positional vertigo.  Motion sickness was reported in 33% of patients and again less than the 48% which has been reported.  Unsteadiness was experienced by 30% of patients and double vision by 17% of patients in this study. Dash et al. have reported transient unsteadiness can occur in 16% of the patients with VM  while Hamed  has reported it to be 12.8%. The most common vestibular symptom besides vertigo was motion sickness (33%) followed by positional vertigo (30%) which is similar to that reported by Neuhauser et al.  Auditory symptoms occurring in VM are less common than vestibular symptoms. , In this study, tinnitus was experienced by 47% of patients as an aura during headache, while during the attack of VM, 53% of patients experienced auditory symptoms such as hearing loss and tinnitus. Phonophobia was experienced by 43% of patients in our study. Thirteen percent of patients experienced hearing loss alone as an aura during the attack of headache. The most common auditory symptom in this study was hearing loss with tinnitus, (53%), followed by tinnitus alone (47%), phonophobia (43%), and hearing loss alone (12%). In the study by Dash et al.,  the most common auditory symptom was phonophobia (70%), followed by tinnitus (50%). This was in discordance with our study. In this study, 43% of patients experienced photophobia, whereas in Neuhauser et al.'s study,  70% of patients experienced photophobia. Visual auras were experienced by all patients in our study, whereas in Neuhauser et al.'s study, 36% experienced visual auras and auras other than vertigo.
In our study, 83% of patients had a positive family history of migrainous headache. Migraine and vertigo were found in familial hemiplegic migraine and episodic ataxia type 2.  In all 30 patients, aura was experienced within 1 h of headache. At least one of the brain stem symptoms other than vertigo such as unsteadiness, zigzag lights in vision, darkness in vision and double vision, hearing loss and fullness of the ear, tinnitus was experienced by all the patients. This suggests that the most common involvement in vestibular migraine may be in the region of brainstem and posterior circulation territory of the brain. The physical examination was normal in all 30 patients similar to what is known.  Of the thirty patients, 10 (33%) had documented mild SNHL on PTA. Earlier studies quote 14% and 16% of SNHL. ,
Middle ear function as expected was normal in patients with VM.
Eighteen ears (18/60) had absent otoacoustic emissions in either right or left ear compared to 2 ears (2/60) in the control group which was statistically significant. This suggests that auditory dysfunction in VM is cochlear in origin.
We found a larger proportion of patients (26 patients out of 30) had abnormal values in either absolute latency or IPL in one or both ears but overall, cases had shorter latencies than controls. One study  done on migraine patients reported 28% patients having one or more BERA abnormalities in the form of prolonged absolute latency of Wave III and I-V IPL.
Kochar et al.  reported significant prolongation in absolute and IPLs at the time of acute attack of migraine. These disappeared after 7 days from the attack indicating reversible pathological changes in different areas of the brain and brainstem. Some authors reported prolonged absolute latency of Wave V and I-V IPL during the headache attack indicating transient impairment of the auditory brainstem function.  None of our patients had acute attack of migraine or vertigo at the time of BERA testing. This audiological finding is similar to those found on vestibular tests in VM, though central vestibular signs have been reported during acute episodes. The frequency of migraine attacks and the duration of illness were identified as important confounders associated with BERA abnormalities. 
Limitations of the study
This study was not powered to bring out differences between cases and controls for the various tests performed. A larger sample size may have provided results that were different.
| Conclusions|| |
The frequency of vestibular migraine in a tertiary care specialized audio vestibular clinic is 22%. Hearing loss in VM is 33% and there is statistically significant cochlear dysfunction present in these patients. The auditory brainstem pathway seems to be unaffected during the interictal phase in VM.
Financial support and sponsorship
The study was partly funded by Fluid Research Grant, Christian Medical College, Vellore .
Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]