This study was conducted on a total number of 60 subjects, classified into study group [n = 40] and control group [n = 20]. The study group was divided into migraine group [study group 1, n = 20] and vestibular migraine group [study group II, n = 20]. The mean age of study group 1 was 34.8 years and that of study group II was 33.8 years (Table 1). This agreed with the data reported by Burstein et al. [15] who reported that the mean age of migraine patients in their study was 32 years. All the study group patients had normal peripheral hearing (Fig. 1).
Both study group 1 and study group II showed more affection in females than in males, which was also reported by Furman et al. [16] and Sohn [17]. The female gender predominance may be attributed to cyclical hormonal changes in women due to fluctuations in estrogen level that seems to trigger headaches in many women. Most women report headaches immediately before or during their menstrual periods, while others develop migraine during pregnancy or menopause [18,19,20].
As regards the educational level of participants in this study, migraine was common among middle followed by high educational level than low level (Table 2). Hamed et al. [21] found that migraine prevalence was significant among those with middle educational level and labor workers. Furthermore, Lipton et al. [22] and Jeff [23] reported higher migraine prevalence with low social class and educational levels as individuals with low and middle educational levels often have more physical exhausting occupations with more exposure to sunlight, glair, and extremes of temperature and more stressful life. Moreover, the three study groups were matched as regards age, gender, and educational level (Table 1).
There was no statistically significant difference between the two study groups regarding the duration of disease and the number of attacks (Table 2). Regarding the family history of migraine, 50% of patient had a positive family history of migraine in the migraine group (Table 4). This agreed with Olsen and Russell [24] who reported that heritability of migraine was estimated to be between 40 and 60%. On the contrary, the VM group reported positive family history in 20% only. This agreed with Hazza et al. [25]; their study reported positive family history in only 16% of vestibular migraine patients.
Studying the headache nature in both study groups revealed that the pain was unilateral and throbbing in most patients (Table 3). This agreed also with Loder et al. [26], who reported that about two-thirds of their migraine patients have unilateral and throbbing headache. Most of the patients in our study reported that attacks were usually triggered by many factors such as lack of sleep, stress, riding transportation, fasting, and certain odor. Accordingly, the quality of their life either routine daily life or their work performance was severely affected in many patients in both groups (Table 4). This agreed with Hamed et al. [21] who studied the epidemiology of migraine in Upper Egypt. They reported that 65% of patients had severe attack that stopped their daily activities. Additionally, the most common auditory symptoms in the present study was phonophobia as 95% of the migraine group and 85% of the VM group were complaining of phonophobia (Table 4). This agreed with Alborzi et al. [27] who found that the most common migraine auditory symptoms is phonophobia. Usually, phonophobia comes in association with photophobia. In the present study, the same percentage of patients who had phonophobia in both groups also reported photophobia (Table 4). This agreed with Vingen et al. [28], who reported that the same number of patients who complained of phonophobia had associated photophobia. Accordingly, these similarities between phonophobia and photophobia in migraine provide evidence that both phenomena share a common pathophysiological mechanism.
The vestibular symptoms of vestibular migraine were quite variable. They included episodic true vertigo, positional vertigo, constant imbalance, movement-associated disequilibrium, and/or lightheadedness (Fig. 2). Symptoms occurred before the onset of headache, during headache, or during headache-free interval (Figs. 3 and 4). Similarly, Neuhauser et al. [29] also reported that all forms of dizziness can occur with migraine. They were examined by VNG; we found that 25% of patients did not show any VNG abnormalities. Positional nystagmus was the commonest finding and was recorded in almost 70% of subjects. Caloric hypofunction was very infrequent [5%]. None of the subjects demonstrated oculomotor abnormalities (Table 5). Similarly, Hazzaa et al. [25] studied VNG in 98 patients with VM. VNG test results demonstrated positional nystagmus in almost 60% of subjects. Accordingly, our result support the hypothesis that the lesion in VM is peripheral lesion. This agreed with Hazza et al. [30] who hypothesized the predominance of peripheral vestibular pathway affection among VM patients, with the absence of central vestibular findings in the vestibular test battery.
This was also explained by Furman [16] who supported the theory that migraine induced vasospasm and subsequent decrease in regional blood flow to the inner ear via the internal auditory artery from the anterior inferior cerebellar artery [AICA]. This could cause transient ischemia, with subsequent transient or permanent peripheral vestibular dysfunction. Numerous studies have documented that migraine can lead to permanent auditory and vestibular deficits resulting from the repeated circulation problems and plasma extravasation during the attacks. Subsequently, in patients with long-standing repeated attacks of migraine, vestibular dysfunction of peripheral type is more vulnerable to occur.
Table 6 and Fig. 4 represented the results of the Central Auditory Processing Questionnaire. The most common complaint for both groups was problems in memory and attention followed by difficulty in understanding speech in background noise. Central auditory processing test result in the control as well as in the study groups were shown in Tables 7 and 8. They showed reduced scores of both study groups in comparison with the control group. The mean scores were below the ninety-five confidence limit of the control group denoting abnormal central auditory test results. Further analysis by comparing the three groups showed statistically significant difference in all central auditory test results between the two study groups and the control group. However, there was no significant difference between the migraine group and the vestibular migraine group. This agreed with Dash et al. [31] who stated that clinical symptoms and cochleovestibular findings in cases of migraine with and without vertigo revealed no statistically significant difference.
The SPIN test result showed the highest percent of abnormality in both study groups, 100% in study group II and 95% in study group I (Table 9). This abnormality was consistent with the results of the APD questionnaire as difficulty in understanding speech in background noise was a common complaint. It was found in 65% of study group I and 75% of study group II (Table 9 and Fig. 4). This finding proved that migraine patient had severely impaired speech discrimination in noise, with no difference between the two study groups (Table 9). This agreed with Hosein et al. [32] who reported that migraine patients without aura have difficulty in speech perception in background noise, and their signal noise ratio [SNR] loss in quick speech in noise [Q-SIN] test showed an abnormal increase compared to the control group. This was attributed to the structural and functional changes including the presence of white matter lesions under the cortex and thickening of the cortical regions that have been confirmed by imaging studies in people with migraine.
Krishnamurti [33] proved that the SPIN test is a useful procedure with moderate sensitivity to a variety of central auditory nervous system [CANS] disorder at different levels in the brain. Accordingly, SPIN test results should be interpreted cautiously in association with other central auditory tests as it is non-localizing to the site of lesion.
Regarding the dichotic integration ability, the DDT was used. Our results showed abnormal scores in both ears with marked reduction in Lt ear scores in both groups (Table 7). This denoted affection of higher auditory pathways mostly at the cortical level. This agreed with Morlet et al. [34], who found that problems in dichotic integration during the nonverbal dichotic test [NVDT] and abnormal N1 peak related to attention in the long latency response test were observed in people with migraine.
The Gap in Noise [GIN] Test in this study was used to evaluate the auditory temporal resolution ability at the cortical level of the brain. The results showed the highest percent of abnormality, 100% in both groups (Table 7). These results were consistent with the study conducted by Agessi et al. [8] who observed that adults with migraine presented with impairment in the physiologic mechanism of temporal processing, especially in temporal resolution and temporal ordering when compared with controls. The difference in performance on the GIN Test between patients with migraine and the control group may denote a central auditory system dysfunction in migraine patients either with or without dizziness.
The DPT test results showed reduced scores in the two migraine groups when compared with control (Table 7 and Fig. 5). Furthermore, the mode of response to the duration pattern test was analyzed. It showed that the humming response was better than the verbal response in both groups (Table 10). This means that the response was hummed more correctly, denoting normal function of the right hemisphere. On the other hand, patients had difficulty reporting the response verbally denoting dysfunction either in the left hemisphere or interhemispheric pathways. There was no difference in performance between the two groups of migraine.
As regards memory test results, migraine patients showed impaired memory function in all tests including recognition memory, memory for content, and memory for sequence tests. This was consistent with Zeitlin and Oddy [35] who found that in a group of patients with severe migraine, they had significantly poorer performances in memory and information processing tests. These results were consistent with the APD questionnaire as memory and attention were frequently encountered complaints in the APD questionnaire in both groups (Table 6 and Fig. 4).
Similarly, a systematic review by Barbosa et al. [36] studied 23 articles to evaluate cognitive impairment in migraine. They found that patients with migraine especially those followed at neurology clinics, often report cognitive complaints, especially regarding attention and memory. The most important cognitive functions include attention, short-term memory, and working memory. These cognitive activities act as compensatory mechanisms of the auditory system in cases of affected bottom-up processing such as lack of temporal encoding.
From all the previous results, we can hypothesize that migraine is triggered by a bottom-up mechanism from the brain stem up to the higher cortex. This agreed with Borsook and Burstein [37]. They suggested that migraine was more than a headache. It was viewed as a complex neurological disorder that affects multiple cortical, subcortical, and brainstem areas which regulate autonomic, affective, cognitive, and sensory functions. As such, it was evident that the migraine brain differs from the non-migraine brain.
As shown in Table 11, temporal processing was the most frequently affected central auditory ability. All migraine patients in both groups had poor temporal resolution. While temporal patterning was affected in 85% group I and 95% group II. The next affected ability was speech in noise discrimination and the least is dichotic listening. On the other hand, auditory memory abnormality was denoted in 55% in group I and 61% in group II denoting less affection of top-down cognitive processing than bottom-up processing. The correlation studies that compared the duration of migraine, the frequency of attack, and the central auditory test results in study group I showed that there was no correlation (Tables 12 and 13). Similarly, Hosein et al. [32] found that migraine patients without aura have difficulty in speech perception in background noise, but there was no correlation between the duration of the disease or the frequency of attacks and [SNR] loss. Also, Bockowski et al. [38] on their study on cortical event-related potentials [CERP] in children with migraine headache found that no significant correlation between [CERP] parameters and duration of disease. This supported the recent theory that migraine occurs due to the release of neurogenic inflammation [NI] that is produced by the release of vasoactive pro-inflammatory neuropeptides from peripheral nerve endings such as calcitonin gene-related peptide [CGRP] and substance P in several brain areas and not due to repeated ischemia caused by repeated attacks.
Regarding the vestibular migraine, there was no correlation between the number of attacks and the results of central auditory tests (Tables 12 and 13), but there was a negative correlation between the duration of disease and some of the central auditory test results. This may be related to the long presence of vestibular symptoms not to migraine duration itself. This agreed with Neuhauser et al. [29].
In addition, there was no difference in performance between vestibular and non-vestibular migraine. This may indicate that subclinical vestibular dysfunction is an integral part of migraine pathology in general and not only in vestibular migraine. Accordingly, it can be assumed that the a large overlap between migraine pathways and vestibular pathways and this is consistent with the view that vestibular migraine is a migraine variant with vestibular manifestations.
Finally, the present study showed that most patients with migraine-type headaches may experience changes in their auditory processing abilities through the different stages of a migraine attack, which may hinder their ability to complete tasks at work or home. This decrease in central auditory processing can impact the quality of life if not addressed and treated early. We recommend performing another longitudinal study to investigate the effect of different types of medical treatment on the central auditory processing of these patients. We expect an improvement of central auditory test scores, notably, the cognitive abilities.
Limitations of this study
Patients were receiving different types of migraine treatment and patients were suffering from different degrees of migraine. However, this heterogeneity did not affect the study results because most of the patients showed abnormal test scores, and the results were correlated to the duration and number of attacks.
