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July2007 Vol.44 Issue:      2 Table of Contents
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The Interrelation of Migraine, Vestibular Dysfunction and Hearing Impairment

Mohamed Abdel Rahman Ahmed1, Amal Mohamed El-Attar2, Enass Sayed Mohamed2, Usama M. Rashaad3, Mohamed Abd Al-Ghaffar4

Departments of Neuropsychiatry1, Audiology Unit2, ENT3, Assiut University;

Audiology Unit and ENT, Sohag University Hospital4



ABSTRACT

Migraine is a relatively common neurological disorder. Neuro-otological symptoms were common in patients with migraines. The aim of this work is to identify the frequency of neuro-otological affection in migraine. The study includes forty–one patients with migraine, and 20 healthy volunteers. Each subject was submitted to full neurological, medical and audiological history and examination. Puretone audiometry, electronystagmography (ENG) tests, auditory brain stem response (ABR) and event related potentials (ERPs). Results: Dizziness was recorded in 56.1 %, rotational vertigo in 31.7 % and positional vertigo was occurred in 19.5 %. Sense of imbalance, tinnitus and phonophobia were reported in 12.2 %, 19.5 %, and 29.3 %, respectively. Abnormalities in at least one of ENG tests were found in 75.6% of patients that include abnormal results of positioning & positional in 34.1 %, post head shaking test in 26.8 %, saccade test in 19.5 %, optokinetic test in 19.5%, pursuit test in 14.6%, unilateral caloric weakness test in 9.8% and spontaneous nystagmus test in 2.4%. Sensorineural hearing impairment was reported in 21.9 %. Significant prolongation of mean interpeak latency of I-III of right ear at 90 dBHL with low repetition rate, III-V at 90 dBHL with high repetition rate and absolute latency of right wave V at 90 dBHL repetition rate compared with controls. No significant differences between patients and control in ERPs. Conclusion: Vestibular dysfunctions were frequently associated with common migraine also hearing impairment was reported in appreciable numbers of cases. Both central and peripheral vestibular affection were recorded in between attacks.

(Egypt J. Neurol. Psychiat. Neurosurg., 2007, 44(2): 607-614)

 




INTRODUCTION

 

Migraine is a relatively common neurological disorder that affects 6 % of men and 18% of women in the United States1. Neuro-otological symptoms have been reported in 33 % to 72% of patients with migraine2,3. Lee et al.4 reported that auditory as well as vestibular symptoms and signs are common in patients with migraine. Phonophobia is the most common auditory symptom but fluctuating hearing loss and acute permanent hearing loss occur in small percentage. Patients with migraine commonly show that vestibular symptoms occur in two-thirds of them, and a quarter have vertigo spells5.

Vestibular symptoms can occur prior to the onset of headache, during headache or during a headache free interval6. Although migraine related vertigo is not included currently in the classification of International Headache Society7, yet its specific criteria have been proposed and utilized in clinical trials8,9. A uniform categorization to describe patients with migraine related vertigo has not been adopted yet: different names have been used, such as migrainous vertigo, benign recurrent vertigo, migraine associated dizziness, migraine induced dizziness, migraine related vestibulopathy and vestibular migraine10. Neuhauser and Lempert11 reported that there is a causal relationship between migraine and vertigo and that a specific clinical entity "migrainous vertigo" can be distinguished. There is emerging clinical evidence that recurrent vertigo is often causally related to migraine and that migrainous vertigo can be diagnosed by operational diagnostic criteria. Oleson12 proposed that migraine and vertigo may be an association as migraine has many non specific symptoms beside vertigo, vertigo occurred before as well as during attack also photo and phonophobia are non specific symptoms that occurred with a variety of disorders. The aim of this work is to identify the frequency of otological affection and trying to determine the potential pathogenesis of its occurrence in common migraine.

 

SUBJECTS AND METHODS

 

Subjects:

Patients were consecutively recruited from the Headache Outpatients Service of the Neurology Department at Assiut University Hospital. Diagnosis of migraine with or without aura was made on the basis of a clinical interview using the diagnostic criteria of the Headache Classification Committee of the International Headache Society(7). The study includes forty–one patients with migraine, 11 were migraineurs with visual aura (MA) and 30 were migraineurs without aura (MO) compared to 20 healthy volunteers. The mean age of migraineurs was 30.2±9.6 years and 32.5±8.8 years for control group with no significant difference between them. In migraineurs, 7 patients were males and 34 were females. The mean duration of illness was 49.07±44.8 months, the mean duration of each attack was 25.0±16.9 hours and frequency of attacks were 1.6±0.62 / week.

Patients and controls have not received any drug at least for one month; non of the control subjects had a family history of migraine. Migraineurs were examined interictally at least 3 days after an attack (checked by history). Female subjects (patients and controls) were not tested directly pre- or during menstrual phase. Patients with criteria of basilar and familial hemiplegic migraine, history of ear diseases, systemic illness, ototoxic drugs, head or ear trauma, external or middle ear diseases were excluded.

The local ethical committee of Assiut University Hospital approved the study. Written informed consent was obtained from all subjects after explanation of all procedures and tests which will be done for them.

 

Methods:

Each subject was submitted to:

Full neurological, medical and audiological history and examination.

Basic audiological evaluation, included puretone audiometry, speech discrimination, tympanometry, and acoustic reflex were done as described by Soliman13, Silman and Gelfand14, Elwany et al.15, and American Speech and Hearing Association Committee on audiometric evaluation16. Puretone air and bone conduction audiometries were conducted using audiometer Madsen OB822. Air conduction hearing threshold levels were measured for octave frequencies between 250-8000 Hz. Low frequency tympanometry and acoustic reflex thresholds were elicited contralaterally using interacoustic AZ 7 immitancemeter.

Vestibular evaluation was done by Electronystagmography (ENG) (Micromedical tech, Meta 4, soft ware version 4.5). Full ENG test battery including a search for nystagmus both with and without fixation, with horizontal and vertical gaze deviation and with post head shaking test. Nystagmus was studied in positioning tests including Dix-Hallpike test right and left and studied in positional tests including supine, head right, head left, right lateral and left lateral positions. An assessment of saccades, smooth pursuit and optokinetic nystagmus was done. Caloric function was studied with use of alternate bithermal caloric irrigation with water at 30°C and 44°C.

Auditory Brainstem Response (ABR) recording was done by (Nicolet spirit) OS/ 2 version 3.  ABR was performed using alternating clicks at 0.1 sec, time window was 10 mesc and filter sitting were 150 Hz – 3 KHz. The stimuli was delivered at 90 dBHL with repetition rate of  11.1 and 51.1 pulse/second. Each response reflected an average of 1500 stimuli presentations. The absolute latencies of waves I, III & V and interpeak latencies of I-III, III-V & I-V of each tracing was obtained.

Event related potentials (ERPs) were elicited with an auditory discrimination task (oddball) paradigm by presenting a series of binaural 1000 Hz (standard) versus 2000 Hz (target) tones at 70 dBHL with a 10 ms rise/fall and 40 ms plateau time. Tones were presented at a rate of 0.9/sec with target tones occurring randomly with a 0.2 probability. Subjects were sitting with their eyes closed and were instructed to mentally count the number of the target, but not the frequent tones, and then asked to report the number of target tones counted at the end of each run. Evoked potentials were recorded from the scalp electrodes placed at CZ and PZ and were referred to linked ear. Filter sitting were 0.5 and 70 Hz, analysis time 1sec, sensitivity 20 μν and duration of stimulation 0.1 msec. To assess performance accuracy at the end of each session, the patient's count was compared with the actual number of target tones presented. Two or three trials were performed in order to demonstrate the consistency of the wave forms. Latencies and amplitudes of P200 and P300 were measured from stimulus artifact to the first and second major positive peaks with a range of 150- 250 and 250-500 msec, respectively. Also, the first and second negative peaks (N100 and N200) preceding the previous positive peaks were measured. ERPs were done using a Nihon Kohden equipment model (7102).

 

RESULTS

 

Eleven patients (26.8 %) of studied sample had visual aura and 30 (73.2 %) had no aura. Dizziness was reported in 23 (56.1 %), 8 of them were dizzy precede headache and 15 patients were dizzy during the attack of headache. True vertigo (rotational vertigo) occurred in 13 (31.7 %) patients, 4 of them had vertigo precede the attack and 9 reported persistence of vertigo during the attack. Positional vertigo occurred in 8 (19.5%) patients, all cases reported before the attack. Sense of imbalance, tinnitus and Phonophobia reported in 12.2 %, 19.5 %, and 29.3 % respectively, all were associated with the attack of pain (Table 1).

Thirty-one (75.6%) patients had abnormalities in at least one of ENG tests. Abnormal results were recorded of positioning & positional test in 34.1 %, post head shaking test in 26.8 %, saccade test in 19.5 %, optokinetic test in 19.5%, pursuit test in 14.6%, unilateral caloric weakness test in 9.8% and spontaneous nystagmus test in 2.4%. From ENG results, peripheral vestibular system affection (up to the root entry zone) were recorded in 10 patients, central vestibular system affection  recorded in 16 patients and inconclusive results in 5 patients (Table 2). Sensorineural hearing impairment was reported in 21.9 %, 4 patients of them (9.8%) had bilateral mild high frequency, 3 patients (7.3%) had unilateral mild high frequency and unilateral mild low frequency in 2 patients (4.9%).

In auditory brainstem response, migraineurs reported significant prolonged interpeak latency I-III of right ear at 90 dBHL with low repetition rate, III-V at 90 dBHL with high repetition rate and absolute latency of right wave V at 90 dBHL with high repetition rate compared to controls (Table 3).

Slow vertical response and P300 showed that migraineurs had longer latency in N100, P200, N200 & P300 and lower amplitude in P200 & P300 than controls but the difference was not significant (Table 4).


 

Table 1. Clinical presentation of studied sample.

 

Symptoms

Number

Percent

Migraine with aura

Migraine without aura

Dizziness

True vertigo

Positional vertigo

Sense of imbalance

Tinnitus

Phonophobia

11

30

23

13

8

5

8

12

26.8

73.2

56.1

31.7

19.5

12.2

19.5

29.3

Table 2. Electronystagmographic findings in migraineurs.

 

ENG tests

Abnormal n (%)

Normal n (%)

Spontaneous nystagmus test

Gaze nystagmus test

Post head shaking test

Positioning & Positional test

Unilateral caloric weakness

Saccade test

Pursuit test

Optokinetic test

1 (2.4%)

0

11 (26.8%)

14 (34.1%)

4 (9.8%)

8 (19.5%)

6 (14.6%)

8 (19.5%)

40 (97.6%)

41 (100%)

30 (73.2%)

27 (65.9%)

37(90.2%)

33 (80.5%)

35 (85.4%)

33 (80.5%)

From ENG tests: Peripheral vestibular system affection occurred in 10 patients. Central vestibular system affection  occurred in 16 patients. Inconclusive results occurred in 5 patients.

 

 

Table 3. Auditory Brainstem Response (ABR) in the studied sample.

 

ABR measurements

Migraineurs (M±SD)

(41)

Control (M± SD)

(20)

ABR at 90 dBHL low repetitions (ms))

Right ear                   Wave I

                                   Wave III 

                                   Wave V

Interpeak latency     I-III

                                   III-V

                                   I-V

Left ear                     Wave I

                                   Wave III

                                   Wave V

Interpeak latency     I-III

                                   III-V

                                 I-V

 

1.7±0.16

3.6±0.34

5.5±0.21

2.8±0.81*

2.1±0.81

3.9±0.26

1.6±0.15

3.5±0.31

5.5±0.26

2.0±0.23

1.9±0.18

4.2±0.76

 

1.6±0.17

3.6±0.14

5.5±0.27

2.0±0.21

1.8±0.31

3.8±0.31

1.6±0.14

3.5±0.20

5.6±0.22

1.9±0.23

1.8±0.20

3.8± 0.26

ABR at 90 dBHL high repetitions (ms))

Right ear                   Wave I

                                   Wave III 

                                   Wave V

Interpeak latency     I-III

                                   III-V

                                   I-V

Left ear                     Wave I

                                   Wave III

                                   Wave V

Interpeak latency     I-III

                                   III-V

                                 I-V

 

1.8±0.18

3.9±0.29

6.1±0.30*

1.9±0.19

2.0±0.31**

3.8±0.33

1.7±0.19

3.9±0.85

5.6±0.31

1.9±0.17

1.8±0.18

3.7±0.54

 

1.7±0.11

3.8±0.35

5.7±0.22

2.0±0.23

1.7±0.31

4.1±0.23

1.7±0.07

3.6±0.11

5.8±0.31

1.9±0.17

1.8±0.18

3.7±0.54

 

Table 4. Slow vertical response and P300 in the studied sample.

 

Event related potentials

Migraineurs (M± SD)

(41)

Control (M±SD)

(20)

N100 latency (ms)

P200 latency

P200 amplitude  (µv)

N200 latency

P300 latency

P300 amplitude

107.1±30.7

172.5±17.1

8.2±1.9

244.4±91.1

342.5±32.6

9.9±4.0

100.1±15.1

162.8±30.6

9.4±3.7

224.0±19.0

322.2±25.1

11.8±2.3

 

 


DISCUSSION

 

Vestibular as well as auditory symptoms and signs are common in patients with migraine, yet the diagnosis of migraine related vestibulopathy is often overlooked and little is known about the pathogenesis of these symptoms and signs. In the present study, dizziness occurred in more than half of the patients with common migraine followed by true vertigo, phonophobia, positional vertigo and sense of imbalance. These results were frequently reported by many authors, Cass et al.6 studied patients with migraine related vestibulopathy, and recorded that 79% had symptoms of movement associated dysequilibrium, light headedness and imbalance and only 21% of their patients described symptoms that could be classified as vertigo. Kayan and Hood3 reported that approximately half of patients had vertigo while the other half reported only giddy sensation. Cutrer and Baloh17 detected that 35% of their patients had vertigo and similar percentage with non vertiginous dizziness such as severe imbalance, nausea and sensitivity to motion. Susan et al.18 found that 64% of patients with migraine related vestibulopathy and 56% of the patients with migraine headache complained of symptoms consistent with space and motion disorders. Dizziness (30%) was the most common symptom followed by vertigo (25%) and tinnitus (20%) were recorded by Bayazit et al.19. The differences in the percentage of vistibulopathy may be attributed to criteria used for selection of the patients with migraine or may be related to methodological differences between laboratories.

In the present work, all vestibular symptoms either precede or occurred during attack of headache, as 4 out of 13 patients had true vertigo precede the attack and 8 out of 23 patients had dizziness. A slightly higher percentage was found by Neuhauser et al.20 in their study of proposed migrainous vertigo category, they found 15 of 33 patients had vertigo regularly associated with migrainous headache. In 16 patients, vertigo occurred both with and without headache, and in two patients headache and vertigo never occurred together. So migrainous vertigo can not be described as a specific subtype of migraine similar to hemiplegic and basilar migraine. This view was supported by Olesen12.

In the present study, thirty- one (75.6%) of the patients presented with dysfunction at least in one of the vestibular tests. Positioning and positional test results were abnormal in 34.1 %, post head shaking in 26.8 %, saccade in 19.5 %, optokinetic in 19.5%, pursuit in 14.6%, unilateral caloric weakness in 9.8% and  spontaneous nystagmus test in 2.4%. Our results were consistent with Togli et al.21, they reported abnormal vestibular finding in 80% of the patients with a history of common migraine, whereas Cass et al.6 reported 73% of their patients with migraine related vertigo; had abnormal results in at least one of the vestibular function test. Abnormal caloric response was demonstrated in 55%, rotational vestibular test dysfunction in 42%, oculomotor test dysfunction in 29% and positional test results were abnormal in 19%. Susan et al.18 demonstrated abnormal response in 81% in their patients, abnormal responses in ocular motor, rotational caloric and positional testing in 92% of migraine related vestibulopathy group and in 75% of migrainous headache group without vestibulopathy. Kayan and Hood(3) identified neurotologic abnormalities using ENG in 77.5% of patients. Dieterich and Brandt22 detected that, In the symptom-free interval 66% of the patients showed mild central ocular motor signs such as vertical (48%) and/or horizontal (22%) saccadic pursuit, gaze-evoked nystagmus (27%), moderate positional nystagmus (11%), and spontaneous nystagmus (11%).

Lower percentage of abnormalities in ENG were reported by, Bayazit et al.19 found that, Positional test (Hallpike maneuver) was positive in 2 (10%) and bithermal caloric testing revealed canal paresis in 3 (15%) patients. Bir et al.23 reported that 58% of the patients with migraine and 55% of the patients with migraine and vertigo had abnormal ENG findings. So, the presence of the same ENG abnormalities in patients with pure headache may be explained as that the vestibular pathways are also affected in those patients, even when there are no vestibular symptoms. Harno et al.24 detected ENG abnormalities in 29% of migraine without aura and in 33% in migraine with aura, on the other hand, 17% of the studied migraineurs without aura had peripheral abnormalities but central abnormalities were more common in migraine with and without aura.

Savundra et al.25 concluded that migraine with aura patients presenting with vertigo commonly had both central and peripheral vestibular findings. Similar results recorded in the present study, as, peripheral vestibular system affection (up to the root entry zone) reported in 10 patients, central vestibular system in 16 patients and inconclusive results reported in 5 patients. As regard response of vestibular symptoms to propylactic treatment of migraine, Maione26 reported that migraine prophylactic treatment shows encouraging results in patients with migraine-related vertigo, 69.3% had satisfactory control of symptoms (sum of complete resolutions and substantial controls) and 81.8% had at least a 50% reduction of the vertiginous episodes frequency.

Audiometric results of the present study not supported a prominent sensorineural hearing impairment with migraine as only 21.9% had abnormalities, all had mild hearing impairment. Similarly several investigators reported nearly the same results. Kayan and Hood3 reported that 18% of their patients with migraine had sensorineural hearing loss. Another 2 studies on migraine related vestibulopathy were reported that hearing loss was a rare finding and it is difficult to related to migraine alone.17,6 Baloh5 reported that photophobia was the most common auditory symptoms but fluctuating and acute permenant hearing loss occurs in a small percentage. Also, Harno et al.24 found that hearing loss was an uncommon, only 2 out of 36 patients with various types of migraine had sensorineural hearing loss, which might have been related to migraine. Viire and Baloh27 suggested that sudden unexplained hearing loss in cases who meet the diagnostic criteria for migraine may be due to vasospasm of the cochlear vasculature. Battista28 reported that audiometric findings of patients with migraine-associated dizziness were most often normal.

In the present study ABR and ERPs in migraineurs interictaly were shown that mild abnormalities in the centeral pathways as documented by significant prolongation of interpeak latencies of I-III, III-V and absolute latency of wave V. In contrast to our results Bayazit et al.19 reported that 7 out 20  patients (35%) had abnormal ABR results; four of them (20%) had peripheral pathway affection in the form of elongation in the absolute wave latencies of wave I, III and V and normal interpeek latencies (IPLs) of wave I-III, III-V and I-V. Three (15%) patients had central pathway affection in the form of elongation in the absolute wave latencies as well as in the IPLs of wave I-III, III-V and I-V. While Kochar et al.29 detected that there were significant prolonged peak and interpeak latencies in ABR at the time of acute attack of migraine. They found that, after 7 days when the attack was over, the observation obtained at this time was not significant comparable to normal values. So that in acute attacks of migraine there may be some pathological changes in different areas of brain and brainstem, producing changes in evoked potential and these changes are reversible.

In the present study, event related potentials were normal in its all components. Similarly, Mazzotta et al.30 and Evers et al.31 detected no variations of potential either of P300 latency or N2-P3 amplitude in migraineurs and tension type headache patients during the interictal period. Also Miles et al.32 recorded the same results except significant reduction in P300 amplitude.

So the present results suggest that common migraine have a central mechanism mainly sub-cortical changes in between the attacks of headache in the form of central vestibular affection in 16 patients in ENG, abnormal prolongation in interpeak latencies of I-III, III-V and absolute latency of wave V with no significant cortical changes as regarded normal P300. Sand and Vingen33, Schoenen34 and Schoenen et al.35 had the same observation.

In conclusion, vestibular dysfunctions were frequently associated with common migraine also hearing impairment was reported in appreciable numbers of cases. Both central and peripheral vestibular affection were recorded in between attacks.

 

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الملخص العربى

 

العلاقة بين الشقيقة  واختلال الجهاز الدهليزى  والسمعي

 

تعتبر الشقيقة من أحد الأمراض العصبية الشائعة والتي تمثل فيه أعراض الجهاز العصبى السمعى نسبة عالية وقد هدفت هذه الدارسة إلى إظهار معدل إصابة الجهاز العصبي السمعي في حالات الشقيقة.

وقد اشتملت الدراسة على 41 مريضا يعانون من مرض الشقيقة 11 منهم يعانون من صداع يسبقه هاله, 30 منهم بدون هاله وعشرون شخصا من الأصحاء في نفس السن والجنس كمجموعه ضابطه. وقد خضع الجميع إلي فحص تام للجهاز العصبي واستيفاء التاريخ المرضى وعمل اختبارات السمع بالنغمات النقية واختبار قياس رأرأة العين وكذلك تم عمل قياس جهد استثارى سمعي لجذع المخ و قياس جهد استثارى سمعي للموجه P300.

النتائج: كشفت الدراسة على أن 56.1 فى المائة يعانون من الدوخة، 31.7 فى المائة يعانون من الدوار، 19.5% فى المائة يعانون من الدوار الوضع، 12.2, 19.5, 29.3 في المائة يعانون من عدم الاتزان والطنين والتخوف من سماع الأصوات على التوالي. وقد أظهرت نتائج اختبارات قياس رأرأة العين أن 75.6 في المائة يعانون من تغيرات غير طبيعية في احد القياسات على الأقل وأن هذه التغيرات موجودة بنسب مختلفة و أظهرت الدراسة أيضاً فروق ذات دلالة إحصائية بين المرضى والأشخاص الأصحاء فى قياس الجهد المستثار السمعى لجذع المخ ولم تظهر فروق ذات دلالة إحصائية واضحة فى قياس الجهد المستثار السمعى للموجه P300. وتؤكد الدراسة أن اختلال الجهاز الدهليزى سواء كان طرفي أو مركزي متكررة بين نوبات الشقيقة.



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