Introduction
Migraine and tension type headaches are the most common primary headache disorders and affect young people with an estimated global prevalence of around 40.5% [1]. The visual system participates in the clinical presentation of migraine headaches in the form of visual aura, scotoma etc. and it is known that visual stimulation can precipitate migraine attacks. The visual system is also important for the maintenance of spatial balance. The visual system is an integral component of the balance mechanism along with the vestibular and the proprioceptive inputs. The saccadic and the smooth pursuit movements are two important controls for the oculomotor system. There is decline in speed of smooth pursuit and saccadic eye movements among patients with migraine and in tension type headache [2, 3]. It is suggested that functional abnormalities of the frontal– parietal– brainstem– cerebellar circuit may cause different clinical or subclinical deficits in the oculomotor system in migraineurs [3]. Visual vertical is a gravitational reference that allows the brain to control body orientation and stability in space. The brain creates this reference by integrating vestibular, visual and somatosensory cues. Static visual vertical refers to the vertical that is perceived without the visual background rotating. Dynamic visual vertical (DVV) is the change in perceived vertical upon rotation of a visual background. DVV is a multisensory integration task that allows us to better understand visual adaptation in vestibular deficits [4]. Subjective Visual Vertical (SVV) test assesses the patient’s ability to align a vertical line to its gravitational vertical. SVV is a non-invasive, quick and easy test when done correctly and can detect otolith dysfunction with 100% specificity and sensitivity [5]. Migraine patients demonstrate a greater deviation from the gravitational vertical compared to their normal counterparts [6]. It has been seen that the vestibular organ is affected in migraine headache which causes abnormality in the vestibular evoked myogenic potential (VEMP) [7]. Although the exact mechanism is not clear, vestibular dysfunction and nonspecific balance disorders have been widely associated to headaches [1, 8]. Subclinical otolith dysfunction may be partly responsible for the subclinical impairment in the vestibular spinal reflex system observed in migraine patients [9]. However, it is not known if the same is seen in other types of primary headache disorders. The oculomotor movement particularly the saccadic and the smooth pursuit movement need to be studied in primary headache disorders. As such, the primary objectives of the present study were:
To compare the degree of static and dynamic tilt in patients with primary headache disorders with that of the controls.
To compare the velocity, latency and precision of saccadic eye movements in patients with primary headache disorders with that of the controls.
To compare the gain in smooth pursuit movements in patients with primary headache disorders with that of the controls.
The secondary objectives of the study were to correlate the degree of static and dynamic tilt in SVV with headache severity as well as to correlate the Smooth pursuit movement and saccades with headache severity.
Methodology
The study was an analytical cross-sectional design of 2 months duration and comprised of two groups with a total sample size of 60 (30 in each group):
Group A(cases)- Individuals diagnosed with primary headache disorders.
Group B (control)- Individuals without any history of persistent or recurrent headaches.
Group A consisted of patients aged 20–60 years, patients with a documented diagnosis of any of the primary headache disorders. Patients presenting with history of headache of at least 4 weeks duration (either intermittent or continuous) and patients with history of frequent headaches requiring analgesic medications at least once a week and or frequency more than or equal to 2 episodes per month were included.
Group B (controls) consisted of patients of age 20–60 years, patients without any history of headache, patients with history of occasional headache not requiring any analgesics and / or frequency less than 2 episode per month.
Pregnant women or lactating mothers, headache with any focal neurological symptoms and or seizure disorders, patients with any known psychiatric disorders, diabetes, hypertension, thyroid dysfunction, any history of intracranial surgery or radiation in the past and those with restricted neck movements were excluded from the study.
Case Definition for Primary Headache
The diagnosis of primary headaches was established as per the International classification of headache disorders (ICHD)-3. Following primary headaches were included in the study as per the diagnostic criteria laid down by ICHD 3.
Migraine.
Tension type headache.
Trigeminal Autonomic cephalgia.
Other primary headaches.
Test Protocol
Subjective Visual Vertical Test
Subjective visual vertical test was performed in the audio- vestibulometry laboratory of ENT department. Static SVV was tested at 00 head tilt, head tilt at 30 0 right and head tilt at 30 0 left. Dynamic SVV was tested in clockwise and anticlockwise visual background rotation. SVV protocol was explained and demonstrated to the patient before starting the test. The test was performed in a dark room with the patient seated upright approximately 3 feet from the screen wearing standardized SVV goggles (Neuroequilibrium Ltd). The SVV goggles were auto calibrated by the device software after placing the goggles on a straight flat surface. A bright yellow luminous line was projected on the screen by the device software at random angulation, and the patient was asked to make it gravitationally vertical. Multiple recordings were taken for each SVV test conditions. The degree of deviation from the true gravitational vertical was recorded by the device software and average value was estimated.
Assessment of Ocular Movement
The following ocular movements were recorded:
Saccades (Random and fixed).
Smooth pursuit movement.
The recording was carried out with the videonystagmography (VNG) equipment (Neuroequilibrium Ltd ) installed in the audio- vestibulometry unit. For recording purpose, the patient was seated in a semi dark room about 3 feet away from the projection screen. Calibrated (videonystagmography) VNG goggles were worn by the patient and sequential recordings were carried out for the latency, velocity, precision of random and fixed saccades, and the gain in smooth pursuit movements.
Assessment of Headache Severity
The severity of headache was assessed with the help of standard Migraine Disability Assessment Test (MIDAS) questionnaire.
Results and Observations
The study included 60 patients in total, 30 in the primary headache study group and 30 in the control group. The primary headache group comprised of 17 females and 13 males, while the control group had 16 females and 14 males. Demographic profile of the participants is depicted in Table 1. In the study group there were 9 patients with migraine while 21 patients had Tension type headache. Clinical profile of primary headache is summarized in Table 2. Figure 1 shows distribution of MIDAS grading among the primary headache cases.
Table 1.
Demographic profile of study participants
| Item | Sub group | Case- Group A n = 30 |
Control-Group B n = 30 |
|---|---|---|---|
| Age Group | 20–29 years | 9(30.0%) | 11(36.7%) |
| 30–39 years | 8 (26.7%) | 8(26.7%) | |
| 40–49 year | 7(23.3%) | 7(23.3%) | |
| > 50 years | 6(20.0%) | 4(13.3%) | |
| Gender | Male | 13(43.3%) | 14(46.7%) |
| Female | 17(56.7%) | 16(53.3%) | |
| Occupation | Employed | 14(46.7%) | 13(43.3%) |
| Unemployed | 16(53.3%) | 17(56.7%) |
Table 2.
Features of primary headache
| Item | n = 30 | Frequency | Percentage% |
|---|---|---|---|
| Duration of Headache | < 1 month | 8 | 26.7% |
| 1 month– 1 year | 7 | 23.3% | |
| > 1 year | 15 | 50% | |
| Location of Headache | Bilateral | 21 | 70% |
| Unilateral | 9 | 30% | |
| localised in any particular area | Yes | 22 | 73.3% |
| No | 8 | 26.7% | |
| Type of Primary headache | Tension type headache | 21 | 70% |
| Migraine | 9 | 30% | |
| Site of localization of headache | Frontal | 9 | 30% |
| Temporal | 20 | 66.7% | |
| Occipital | 7 | 23.3% | |
| Vertex | 5 | 16.6% | |
| Holocranial | 2 | 6.6% | |
| Frequency | Daily | 10 | 33.3% |
| Once in a week | 3 | 10.0% | |
| More than once in a week | 7 | 23.3% | |
| Once in a month | 7 | 23.3% | |
| More than once in a month | 1 | 3.3% |
Fig. 1.
Distribution of MIDAS grading of primary headache patients
Results of SVV in Control and Primary Headache Groups
SVV assessment was conducted on all the participants and comparison made between the control group and primary headache group. Significant statistical difference was found in the average static SVV between the control group and Primary headache group (P = 0.007). SVV with head tilt 30 degrees right, head tilt 30 degrees left also reveal a significant difference between control and the primary headache group. (P = 0.011; and P = 0.001), respectively. Other SVV parameters like the dynamic SVV with clockwise background visual rotation and dynamic SVV with anti-clockwise background visual rotation did not show any statistical significance between the primary headache and the control group (Table 3).
Table 3.
Table showing analysis of SVV, saccades and smooth pursuit between the study group and controls
| Parameters | Control | Case | P-value | ||
|---|---|---|---|---|---|
| Mean | Std. Deviatio n |
Mean | Std. Deviatio n | ||
| SVV-static tilt | 0.79 | 0.46 | 1.25 | 0.77 | 0.007 |
| SVV-Static tilt left | 1.26 | 0.50 | 2.17 | 1.27 | 0.001 |
| SVV - Static Tilt Right | 1.15 | 0.50 | 1.73 | 1.11 | 0.011 |
| SVV-Dynamic Clockwise | 2.96 | 9.14 | 2.69 | 2.84 | 0.877 |
| SVV-Dynamic Anticlockwise | -0.78 | 0.95 | -1.94 | 3.39 | 0.074 |
Fig. 2.
Showing correlation between MIDAS total score and SVV - static 0 degree tilt
Results of Ocular Movements in Controls and Primary Headache Patients
Ocular movements were assessed and recorded for smooth pursuit movements, fixed and random saccades in all participants by using VNG equipment (Neuroequilibrium Ltd, India) and analysis was done between control group and primary headache group. Velocity, latency and precision of saccadic eye movements (fixed and random saccades) show no significant difference between participants with primary headache and controls.
There was no significant difference in the gain in smooth pursuit movements between participants with primary headache and controls.
Correlation between MIDAS Total Score and SVV Parameters
A correlation analysis was carried out between the MIDAS total score and SVV. There is significant correlation between MIDAS total score and Static SVV, Static SVV with head tilt 30 degrees (right and left) Table 4.
Table 4.
Correlation between MIDAS total score and SVV
| Parameters | SVV-static tilt | SVV-Static tilt left | SVV - Static Tilt Right | |
|---|---|---|---|---|
| MIDAS total Score | Pearson Correlation | 0.305* | 0.460** | 0.480** |
| Sig. (2-tailed) | 0.020 | 0.000 | 0.000 | |
** Correlation is significant at the level 0.01 level( 2- tailed)
* Correlation is significant at the 0.05 level (2 - tailed)
Post Hoc Analysis between MIDAS Grades and SVV Parameters
Bonferroni post hoc analysis was done between the MIDAS grades and SVV parameters in which there is significant difference between grade 1 and 4 and no significant difference between grade 2 and 3 was present. (Table 5)
Table 5.
Bonferroni post hoc analysis between MIDAS grades and SVV parameters
| Dependent Variable | (I) VAR00005 | (J) VAR00005 | Mean Difference (I-J) | Std. Error | Sig. | 95% Confidence Interval | |
|---|---|---|---|---|---|---|---|
| Lower Bound | Upper Bound | ||||||
| SVV-static tilt | 1.00 | 2.00 | − 0.34531 | 0.26255 | 1.000 | -1.0635 | 0.3728 |
| 3.00 | − 0.23531 | 0.22796 | 1.000 | − 0.8588 | 0.3882 | ||
| 4.00 | − 0.71895* | 0.21992 | 0.011 | -1.3205 | − 0.1174 | ||
| 2.00 | 1.00 | 0.34531 | 0.26255 | 1.000 | − 0.3728 | 1.0635 | |
| 3.00 | 0.11000 | 0.31009 | 1.000 | − 0.7382 | 0.9582 | ||
| 4.00 | − 0.37364 | 0.30423 | 1.000 | -1.2058 | 0.4585 | ||
| 3.00 | 1.00 | 0.23531 | 0.22796 | 1.000 | − 0.3882 | 0.8588 | |
| 2.00 | − 0.11000 | 0.31009 | 1.000 | − 0.9582 | 0.7382 | ||
| 4.00 | − 0.48364 | 0.27493 | 0.504 | -1.2356 | 0.2684 | ||
| 4.00 | 1.00 | 0.71895* | 0.21992 | 0.011 | 0.1174 | 1.3205 | |
| 2.00 | 0.37364 | 0.30423 | 1.000 | − 0.4585 | 1.2058 | ||
| 3.00 | 0.48364 | 0.27493 | 0.504 | − 0.2684 | 1.2356 | ||
| SVV-Static tilt left | 1.00 | 2.00 | − 0.20170 | 0.36591 | 1.000 | -1.2025 | 0.7991 |
| 3.00 | − 0.23712 | 0.31770 | 1.000 | -1.1061 | 0.6318 | ||
| 4.00 | -1.66676* | 0.30650 | 0.000 | -2.5051 | − 0.8284 | ||
| 2.00 | 1.00 | 0.20170 | 0.36591 | 1.000 | − 0.7991 | ||
| 3.00 | − 0.03543 | 0.43215 | 1.000 | -1.2175 | |||
| 4.00 | -1.46506* | 0.42399 | 0.006 | -2.6248 | |||
| 3.00 | 1.00 | 0.23712 | 0.31770 | 1.000 | − 0.6318 | 1.1061 | |
| 2.00 | 0.03543 | 0.43215 | 1.000 | -1.1466 | 1.2175 | ||
| 4.00 | -1.42964* | 0.38316 | 0.003 | -2.4777 | − 0.3816 | ||
| 4.00 | 1.00 | 1.66676* | 0.30650 | 0.000 | 0.8284 | 2.5051 | |
| 2.00 | 1.46506* | 0.42399 | 0.006 | 0.3054 | 2.6248 | ||
| 3.00 | 1.42964* | 0.38316 | 0.003 | 0.3816 | 2.4777 | ||
| SVV - Static Tilt Right | 1.00 | 2.00 | − 0.31424 | 0.29944 | 1.000 | -1.1333 | 0.5048 |
| 3.00 | − 0.22981 | 0.25998 | 1.000 | − 0.9409 | 0.4813 | ||
| 4.00 | -1.51099* | 0.25082 | 0.000 | -2.1970 | − 0.8250 | ||
| 2.00 | 1.00 | 0.31424 | 0.29944 | 1.000 | − 0.5048 | 1.1333 | |
| 3.00 | 0.08443 | 0.35365 | 1.000 | − 0.8829 | 1.0517 | ||
| 4.00 | -1.19675* | 0.34697 | 0.006 | -2.1458 | − 0.2477 | ||
| 3.00 | 1.00 | 0.22981 | 0.25998 | 1.000 | − 0.4813 | 0.9409 | |
| 2.00 | − 0.08443 | 0.35365 | 1.000 | -1.0517 | 0.8829 | ||
| 4.00 | -1.28118* | 0.31355 | 0.001 | -2.1388 | − 0.4235 | ||
| 4.00 | 1.00 | 1.51099* | 0.25082 | 0.000 | 0.8250 | 2.1970 | |
| 2.00 | 1.19675* | 0.34697 | 0.006 | 0.2477 | 2.1458 | ||
| 3.00 | 1.28118* | 0.31355 | 0.001 | 0.4235 | 2.1388 | ||
*. The mean difference is significant at the 0.05 level
Fig. 3.
Showing correlation between MIDAS total score and SVV static tilt 30 degree left
Fig. 4.
Showing correlation between MIDAS total score and SVV static tilt right 30 degree
Discussion
Headache disorders significantly impact social, occupational, recreational, and family activities. They can result in higher ictal and interictal burden, as well as economic losses from lost production and medical costs [10].
In the present study 17 females (56.7%) and 13 males (43.3%) were included in the primary headache group (Table 2) and were age and gender matched with the control group. Most common age group of patients with primary headaches 20-29 years of age (30%) (Table 2).
9 (30%) of the thirty people in the primary headache group had migraine, while 21 (70%) had tension-type headaches (ICHD-3 criteria). These finding are similar to the findings of the study Saritha et al. [11]. Of these, 50% experienced sound sensitivity, 40% light sensitivity, 7% were associated with nausea, 4% with tinnitus, and 4% with limb weakness (Table 2).
Even though the primary headache group did not exhibit any clinical symptoms and signs of vestibular dysfunction, the current study found a statistically significant difference in the average static SVV (P = 0.007), SVV with head tilt 30 degrees left (P = 0.001), and SVV with head tilt 30 degrees right (P = 0.011) among them. However, there is no statistically significant difference between the control group and the primary headache group according to the clockwise dynamic SVV and anti-clockwise SVV. This is interesting as migrainuers are known to be sensitive to moving visual field. However, dynamic SVV can be affected by ageing and relies on visual input in presence of vestibular impairment [12]. We assume that the results of dynamic SVV in the present study might be affected due to small sample size and a smaller age stratified subgroups. Study shows that headache populations with dizziness have varying degrees of peripheral and central vestibular dysfunction [13]. Patients with vestibular migraine often complain of dizziness with changes in the head or body position. These symptoms may be due to the impairment of spatial orientation. Impairment of spatial orientation is widely thought to be caused by abnormalities in the otolith pathways, which include brain stem, thalamus and vestibular cortex [14].
According to Bisdorrf et al., dizziness is a common symptom of headache, particularly migraine, and the presence of dizziness has been shown to exacerbate disability and depression associated with migraine [15]. Vertigo in migraine patients is considered a manifestation of migraine [16]. According to previous studies [9] patients with migraine show subclinical vestibular spinal reflex dysfunction, which may be caused in part by asymptomatic otolith dysfunction. The visual vestibular misperception in patients with primary headache disorder may be facilitated by alterations in any of the three systems involved in forming the pattern of central verticality (vestibular, visual, and somatosensory systems). Vestibular symptoms such as unsteadiness are known to be associated with headaches and these interactions may be due to a link between the trigeminal and vestibular nuclei [17].
In the present study, all patients with primary headache were devoid of any clinically manifested vestibular dysfunction. As such the study assumes significance because there is evidence of statistical difference in the perception of verticality between the study group and the control group. This may be due to an underlying otolith impairment even in the absence of any clinical manifestation of vestibular dysfunction. It remains to be seen whether this statistical difference progresses later in the course of the disease into clinically manifested otolith dysfunction. It will also be interesting to study the effect of complete resolution of headache disorder on the SVV parameters. At present, SVV is not utilized in the diagnosis and clinical management of primary headaches. However, it is necessary to study and establish its role as early indicator and predictor of vestibular impairment in primary headache disorders and also for objective assessment of response to treatment.
The severity of disability due to headache is assessed with the help of MIDAS questionnaire. The present study shows a significant positive correlation between MIDAS score and the degree of SVV tilt. This correlation is more pronounced when MIDAS grade 1 was compared with MIDAS grade 4. It is therefore probable that greater the severity of primary headache, more likely is the possibility of involvement of the otolith organ.
Primary headaches with undiagnosed vestibular dysfunction can severely affect the daily activities and can negatively impact the functional status of the individual. According to Chan et al. possible mechanisms for vestibular dysfunction in headache population may include vestibulo-cerebellar loss of inhibition, central vestibular network misfiring, and peripheral pathology aggravating central hypersensitization [13].
Vestibular migraines can severely impair daily functioning and make it difficult to accomplish obligations and tasks related to work, school, and home life, if they are not treated [18]. Dizziness brought on by headaches is linked to depression and impairs social and professional functioning. Even when headache frequency, type, and gender are taken into account, impact of dizziness is still significant, indicating that it is a separate factor contributing to the negative effects [14]. Studies have reported that vestibular dysfunction can lead to cognitive problems such as visuospatial disability, inattention, loss of executive function, and memory [19]. In order to start a suitable rehabilitation and risk-reduction plan, it is crucial to detect vestibular dysfunction early.
The present study did not find any statistically significant difference in the gain of smooth pursuit movement. Saccadic latency, velocity and precision also did not show any difference between the groups. Carlsson and Rosenhall in their study demonstrated a reduction in the gain of smooth pursuit and saccadic velocity in patients with tension type headache [20]. This was probably because of impaired proprioception from the cervical muscles secondary to increased tension in neck muscles in TTH [20]. Similarly, Filippopulos et al. found an increase in saccadic latency in patients with migraine with or without aura when compared with the control group [3]. Oculomotor abnormalities were detected in patients with vestibular migraine which were more pronounced during the acute episode rather than in the interictal period [21]. It is interesting to note that study by Vivek et al. found abnormality in the smooth pursuit movement only in the vertical plane while all other oculomotor tests did not show any statistically significant difference [22]. It has not been studied if the changes in saccades and smooth pursuit in TTH patients are temporary or permanent in nature. Improvement in headache symptoms relieve the tension in cervical muscle and can lead to normalcy of the pursuit and saccadic eye movements. It is also not known if the duration, frequency and severity of headache has any effect on the saccadic and the pursuit movements.
Limitation of the Study
The study was conducted for a period of only 2 months with a small sample size and follow up was not done. Further, we assessed the participants only during the period when there was no headache. As such, the outcome of SVV and oculomotor changes during the episodes of headache are not known. This limitation can be overcome by longitudinal study in future to look in the progression and the variability of the present findings with disease severity and response to prophylactic interventions in primary headache disorders.
Conclusion
Subclinical otolith impairment may be associated with primary headache disorders. It is not known at present whether this progresses to manifest otolith dysfunction in the future. Further evaluation is needed to establish the role of SVV in predicting vestibular function in patients with primary headache disorders in the future. It may be worthwhile to study the oculomotor changes and the SVV during the episode of headache. It is also necessary to study the effect of complete resolution of primary headache disorders on the SVV. Early prediction of the otolith dysfunction with SVV in headache patients can help us initiate proper treatment or rehabilitation measures so that the long term impact of otolith dysfunction is avoided.
Acknowledgements
The study was carried out under the Short Term Studentship (STS) program of Indian Council of Medical Research (ICMR) for the year 2023 with Reference ID 2023–04502. We would like to thank ICMR STS program for the same.
Author Contributions
All the authors have contributed to the manuscript and have read and approved the final version of the manuscript.
Funding
Nil.
Declarations
Conflict of Interest
The authors do not have any conflict of interest to declare.
Ethics Approval
The ethical clearance was obtained from the Institute Ethics Committee before starting the study ( Ethical clearance certificate number: AIIMS /MG/IEC/2023-24/56, dated 01/12/2023).
The manuscript was not presented in any conference and it was not published in any other scientific or non-scientific journals either in part or as whole.
Footnotes
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
References
- 1.GE, Manrique-Navarro M, Lerida-Ortega MA, Rodríguez-Almagro D, Osuna-Perez MC, Lomas-Vega R (2020) Misperception of visual verticality in patients with primary headache disorders: a systematic review with meta-analysis. Brain Sci 10(10):664 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Cachinero-Torre A, Díaz-Pulido B, Asúnsolo-del-Barco Á. Relationship of the lateral rect6) Filippopulos FM, Goeschy C, Schoeberl F, Eren OE, Straube A, Eggert T (2021) Reflexive and Intentional Saccadic Eye Movements in Migraineurs.Front Neuro.;12:66992 [DOI] [PMC free article] [PubMed]
- 3.Filippopulos FM, Goeschy C, Schoeberl F, Eren OE, Straube A, Eggert T (2021) Reflexive and intentional Saccadic Eye Movements in migraineurs. Front Neuro 12:669922 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Miller MA, Crane BT (2016) Static and dynamic visual vertical perception in subjects with migraine and vestibular migraine. World J Otorhinolaryngol Head Neck Surg 2(3):175–180 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Kumar L, Thakar A, Thakur B, Sikka K (2017) Sensitivity and specificity of clinical and laboratory otolith function tests. Otol Neurotol 38(9):e378–e383 [DOI] [PubMed] [Google Scholar]
- 6.Winnick A, Sadeghpour S, Otero-Millan J, Chang TP, Kheradmand A (2018) Errors of upright perception in patients with vestibular migraine. Front Neuro 9:892 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Tutar B, Berkiten G, Akan O, Saltürk Z, Gürpinar B, Karaketir S, Kumral TL, Uyar Y, Tuna ÖB (2020) Analysis of vestibular-evoked myogenic potentials in the vestibular migraine. Neurol Sci Neurophysiol 37(2):63 [Google Scholar]
- 8.Burns KN, Langford TD, Tierney R, McDevitt J (2021) Premorbid primary headache and vestibular and oculomotor baseline assessments in collegiate atletes. Clin J Sport Med.;32(5) [DOI] [PubMed]
- 9.Asai M, Aoki M, Hayashi H, Yamada N, Mizuta K, Ito Y (2009) Subclinical deviation of the subjective visual vertical in patients affected by a primary headache. Acta Otolaryngol 129(1):30–35 [DOI] [PubMed] [Google Scholar]
- 10.Waliszewska-Prosół M, Montisano DA, Antolak M, Bighiani F, Cammarota F, Cetta I, Corrado M, Ihara K, Kartamysheva R, Petrušić I, Pocora MM (2024) The impact of primary headaches on disability outcomes: a literature review and meta-analysis to inform future iterations of the Global Burden of Disease study. J Headache Pain 25(1):27 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Sharma SK, Ukey UU (2023) Epidemiology of primary headache and its Associated Psychosocial factors amongst Undergraduate Medical students: a cross-sectional study from the Vidarbha Region. Cureus.;15(5) [DOI] [PMC free article] [PubMed]
- 12.Kobayashi H, Hayashi Y, Higashino K, Saito A, Kunihiro T, Kanzaki J, Goto F (2002) Dynamic and static subjective visual vertical with aging. Auris Nasus Larynx 29(4):325–328. 10.1016/s0385-8146(02)00058-5 [DOI] [PubMed] [Google Scholar]
- 13.Chan TL, Hale TD, Steenerson KK (2020) Vestibular lab testing: interpreting the results in the headache patient with dizziness. Curr Neurol Neurosci Rep 20:1–0 [DOI] [PubMed] [Google Scholar]
- 14.Li F, Xu J, Li GR, Gao R, Shang CY, Tian E, Kong WJ, Zhuang JH, Zhang SL (2021) The value of subjective visual vertical in diagnosis of vestibular migraine. Curr Med Sci 41:654–656 [DOI] [PubMed] [Google Scholar]
- 15.Bisdorff A, Andree C, Vaillant M, Sándor PS (2010) Headache-associated dizziness in a headache population: prevalence and impact. Cephalalgia 30(7):815–820 [DOI] [PubMed] [Google Scholar]
- 16.Lampl C, Rapoport A, Levin M, Bräutigam E (2019) Migraine and episodic Vertigo: a cohort survey study of their relationship. J Headache Pain 20:1–5 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Rodríguez-Almagro D, Achalandabaso-Ochoa A, Molina-Ortega FJ, Obrero-Gaitán E, Ibáñez-Vera AJ, Lomas-Vega R (2020) Neck pain-and unsteadiness-inducing activities and their relationship to the presence, intensity, frequency, and disability of headaches. Brain Sci 10(7):425 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Lempert T, Neuhauser H (2009) Epidemiology of vertigo, migraine and vestibular migraine. J Neurol 256:333–338 [DOI] [PubMed] [Google Scholar]
- 19.Sugaya N, Arai M, Goto F (2018) Changes in cognitive function in patients with intractable dizziness following vestibular rehabilitation. Sci Rep 8(1):9984 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Carlsson J, Rosenhall U (1988) Oculomotor disturbances in patients with tension headache. Acta Otol (Stockh) 106:354–360 [DOI] [PubMed] [Google Scholar]
- 21.Moaty AS, Afifi KH, Allam MA, Abd El Mageed HK (2022) Assessment of oculomotor and vestibulo-ocular function in vestibular-migraine patients. Menoufia Med J 35(3):1593 [Google Scholar]
- 22.Vivek S, Prem G, Dorasala S, Faizal B, Joy M, Nair AS Videonystagmography (VNG) findings in patients with vestibular migraine: a hospital-based study. Indian J Otolaryngol Head Neck Surg 2022;2:1–8 [DOI] [PMC free article] [PubMed]