Abstract
BACKGROUND:
To evaluate retinal structural and vascular changes using optical coherence 15 tomography (OCT) and OCT angiography (OCT-A) in migraine patients and to explore 16 their associations with clinical and epidemiological characteristics.
SUBJECTS AND METHODS:
This cross-sectional, comparative study included 136 eyes from 68 subjects, divided into 68 eyes from migraine patients and 68 eyes from controls. Participants underwent full ophthalmological examinations, OCT, and OCT-A.
RESULTS:
Patients had a mean age of 35.8 years and a female-to-male ratio of 1.83. Migraine with aura was present in 47.1% of cases. A reduction in upper retinal nerve fiber layer thickness was found in migraine patients, with no other significant OCT or OCT-A differences compared to controls. Correlations were observed between OCT metrics and disease duration, severity, and attack frequency, though no correlations were noted with laterality.
CONCLUSION:
Optical coherence tomography and optical coherence tomography–angiography may serve as valuable biomarkers for diagnosing, monitoring, and predicting outcomes in both aura and nonaura migraines.
Keywords: Aura, migraine, optical coherence tomography angiography, vascular density
Introduction
Migraine, a prevalent, chronic, and multifactorial neurovascular disorder, is characterized by typical headaches triggered by internal and external factors in genetically predisposed individuals. Among neurological disorders, the prevalence in adults is reported at 33% in women and 13% in men. Migraine can be categorized into two main entities: migraine with aura and migraine without aura.[1]
Although the pathophysiology of migraine remains incompletely understood, two theories, vascular and neurogenic, have been proposed to explain its pathogenesis. In the vascular theory, migraine is considered a form of vascular disorder, and aura is thought to be triggered by a decrease in cerebral blood flow. Conversely, in the neurogenic theory, migraine is viewed as a neurological disorder, and vascular changes are presumed to result from neuronal dysfunction.[2]
With the advent of optical coherence tomography (OCT), whether or not coupled with angiographic evaluation, structural and microvascular assessment in both macula and optic nerve head has become feasible. This noninvasive technique enables the separate study of superficial and deep capillary networks using amplitude or phase decorrelation technology.
At the intersection of vascular and neurogenic theories that seek to explain migraine, the use of OCT and OCT-A sheds new light on both vascular and neurological aspects of the condition. However, studies demonstrating the utility of OCT-A in migraine patients remain limited.[3]
This study aimed to evaluate structural alterations of macular and optic nerve head parameters among migraine patients, using SD-OCT/OCT-A, and to identify the relationships between structural changes and patients’ clinical and epidemiological features.
Subjects and Methods
A cross-sectional comparative, descriptive, and analytical study was conducted in a third-level university hospital, from June 1, 2024, to March 30, 2025. Approval was acquired from the hospital’s ethics committee. Written informed consent was obtained from all participating patients.
The study included 136 eyes from 68 subjects, divided into two groups: 68 eyes from 34 migraine patients and 68 eyes from 34 control subjects. Inclusion criteria for the migrainous group specified individuals aged between 18 and 60 years, intraocular pressure below 18 mmHg, cup–disc ratio below 0.4, and absence of ophthalmological pathology. The diagnosis of migraine with or without aura was established according to the criteria of the International Classification of Headache Disorders, 3rd Edition.
Control group participants were randomly selected from a cohort of nonmigrainous individuals and were subsequently randomized according to age and sex.
Exclusion criteria for both the groups were as follows: high ametropia, glaucoma, media disorders like cataracts, systemic and neurological diseases, previous ocular surgery, and specific medications for migraine prophylaxis. Poor-quality OCT and OCT-A scans were also excluded.
Participants underwent a complete ophthalmologic examination. Spectral-domain optic coherence tomography Spectral-domain optical coherence tomography (SD-OCT) and OCT-A scans were performed for all subjects by an OCT RTVue 100 imaging system (AngioVue; Optovue, Inc., Fremont, CA, USA) with eye-tracking gaze control.
Peripapillary retinal nerve fiber layer (RNFL) thickness was analyzed in “Optic Nerve Head” mode along a 4.5-mm diameter circle centered around the optic disc.
The following parameters were investigated: average RNFL thickness, superior RNFL thickness (in the upper quadrant), inferior RNFL thickness (in the lower quadrant), and temporal and nasal RNFL thickness (in both temporal and nasal quadrants).
Subsequently, ganglion cell complex analysis was conducted, encompassing RNFL, ganglion cell layer, and inner plexiform layer, on a 7 mm × 7 mm grid, 1 mm temporally to the fovea.
We evaluated vascular density (VD) in the macular region using a 6 mm × 6 mm scan centered on the fovea. VD indicates surface area percentage occupied by microvasculature in the segmented region. In macular acquisitions, VD was assessed for both the full image of the superficial capillary plexus (SCP) and the deep capillary plexus (DCP).
The radial peripapillary capillary (RPC) plexus was defined as a 4.5 mm × 4.5 mm-wide ring centered on the optic disc. VD in this region was measured from the inner limiting membrane to the posterior boundary of the RNFL. In the case of RPC scans, VD was evaluated for the entire image. Foveal avascular zone (FAZ) has been defined as the circular area devoid of capillaries in the macula, as observed in OCT-A images of the superficial vascular network.
Statistical analysis was performed using the SPSS software system, version 18.0 (SPSS Inc., Chicago, Illinois, USA). Values were expressed as mean ± standard deviation. The value of normality was assessed using the Kolmogorov–Smirnov test. Each eye was assessed individually, and a generalized estimating equation was employed to address the correlation between eyes within the same subject for group comparisons. Categorical variables were compared using the Chi-square test. Mann–Whitney U test was employed to compare independent groups for continuous variables exhibiting nonnormal distributions. Correlations between quantitative variables were investigated based on the Spearman correlation coefficient. P <0.05 was considered statistically significant.
Results
The mean age of the migraine group was 36.3 ± 7.7 years, with a female-to-male ratio of 1.83. In the control group, the mean age was 35.9 ± 7.5 years, with a female-to-male ratio of 1.75. The two groups demonstrated no statistically significant difference regarding age (P = 0.89) and gender distribution (P = 0.742). The mean migraine duration was 10.1 ± 5.2 years. Among the migraine group, 16 (47.1%) patients experienced migraine with aura, while 18 (52.9%) patients had migraine without aura. The mean number of attacks per quarter was 4.23 ± 2.7, with 16 (47.1%) patients presenting Grade III in Migraine Disability Assessment and 12 (35.2%) patients with Grade II.
In terms of RNFL thickness, the mean thickness did not significantly differ between migraine eyes and controls, except in the superior quadrant. Here, migraine eyes showed a mean thickness of 119.11 ± 9.94 μm, which was significantly lower than the 128.61 ± 10.09 μm observed in controls (P < 0.01). In the inferior quadrant, there was also a reduction (114.85 ± 16.07 μm in migraine eyes vs. 131.94 ± 13.58 μm in controls), though this was not statistically significant (P = 0.066) [Table 1].
Table 1.
Comparison of thickness of the retinal nerve fiber layer between migraine patients and the control group
| RNFL thickness (µm) | Migraine group | Control | P |
|---|---|---|---|
| Average thickness | 99.11±7.55 | 103.85±7.18 | 0.07 |
| Superior quadrant | 119.11±9.94 | 128.61±10.09 | <0.01 |
| Inferior quadrant | 114.85±16.07 | 131.94±13.58 | 0.066 |
| Temporal quadrant | 74.5±5.64 | 77.26±7.77 | 0.24 |
| Nasal quadrant | 77.6±9.2 | 79.94±8.88 | 0.459 |
| GCC thickness | 96.44±4.69 | 98.17±3.14 | 0.214 |
RNFL: Retinal nerve fiber layer, GCC: Ganglion cell complex
Comparing migraine eyes with aura (MwA), migraine eyes without aura (MwoA), and controls, and controls, a significant reduction was observed in the average RNFL thickness for MwA (94.94 ± 5.32 μm) compared to controls (103.85 ± 7.18 μm, P = 0.003) and for MwA compared to MwoA (102.83 ± 7.48 μm, P = 0.024). Differences in the superior and inferior quadrants were also significant, with lower measurements in MwA than MwoA (P = 0.001 and P < 0.001, respectively). For GCC thickness, it was slightly lower in MwA compared to MwoA and controls, though these differences were not statistically significant [Table 2].
Table 2.
Comparison of retinal nerve fiber layer, ganglion cell thickness, and optical coherence tomography–angiography parameters between migraine spatients with and without aura and the control group
| MwA | MwoA | Control | P* | P † | P ‡ | |
|---|---|---|---|---|---|---|
| Average thickness of RNFL (µm) | 94.94±5.32 | 102.83±7.48 | 103.85±7.18 | 0.003 | 0.737 | 0.024 |
| Superior quadrant (µm) | 114.25±6.93 | 123.44±10.52 | 128.61±10.09 | 0.001 | 0.232 | 0.053 |
| Inferior quadrant (µm) | 117.75±9.68 | 129.5±8.62 | 131.94±13.58 | <0.001 | 0.631 | 0.02 |
| Temporal quadrant (µm) | 72.36±4.19 | 76.39±6.3 | 77.26±7.77 | 0.053 | 0.774 | 0.149 |
| Nasal quadrant (µm) | 73.31±4.97 | 81.44±10.61 | 79.94±8.88 | 0.063 | 0.063 | 0.67 |
| GCC thickness (µm) | 94.19±4.43 | 98.44±4.15 | 98.17±3.14 | 0.059 | 0.868 | 0.059 |
| Vascular density in DCP (%) | 47.66±2.86 | 51.15±4.03 | 50.61±5.64 | 0.179 | 0.803 | 0.06 |
| Vascular density in SCP (%) | 49.28±1.73 | 50.70±1.46 | 49.86±2.93 | 0.611 | 0.430 | 0.085 |
| Vascular density in RCP (%) | 49.97±1.52 | 51.49±1.66 | 51.0 1±2.24 | 0.247 | 0.591 | 0.069 |
| FAZ (mm2) | 0.347±0.55 | 0.27±0.09 | 0.284±0.098 | 0.106 | 0.820 | 0.073 |
*Comparison between MwA and control, †Comparison between MwoA and control, ‡Comparison between MwA and MwoA. MwA: Migraine with aura, MwoA: Migraine without aura, RNFL: Retinal nerve fiber layer, GCC: Ganglion cell complex, DCP: Deep capillary plexus, SCP: Superficial capillary plexus, RCP: Radial peripapillary capillary plexus, FAZ: Foveal avascular zone
OCT-A parameters also varied. VD in the DCP was slightly lower in MwA (47.66 ± 2.86) compared to MwoA (51.15 ± 4.03) and controls (50.61 ± 5.64), though not reaching statistical significance (P = 0.06). VD in both SCP and RCP showed no significant variation between the groups. The FAZ area was larger in the MwA group compared with the MwoA and control groups, yet the difference was not statistically significant [Table 2].
A breakdown by gender and laterality of headache revealed no significant RNFL and GCC thickness differences between male and female migraine patients, though some variation was noted in quadrant-specific measurements. For instance, the superior quadrant thickness was slightly higher in female eyes (123.75 ± 11.7 μm) compared to male eyes (116.59 ± 8.34 μm). In addition, RNFL and GCC thickness appeared slightly reduced in eyes on the headache side [Table 3].
Table 3.
Comparison of retinal nerve fiber layer thickness by gender and migraine laterality
| Male | Female | P | Headache side eye | Contralateral side eye | P | |
|---|---|---|---|---|---|---|
| Average RNFL thickness (µm) | 97.77±5.75 | 101.58±10.24 | 0.336 | 98.11±8.37 | 100.11±7.39 | 0.466 |
| Superior quadrant (µm) | 116.59±8.34 | 123.75±11.7 | 0.162 | 120.35±10.82 | 117.88±10.47 | 0.504 |
| Inferior quadrant (µm) | 122.77±9.45 | 126.17±13.29 | 0.55 | 122.53±11.98 | 125.42±11.22 | 0.474 |
| Temporal quadrant (µm) | 74.9±5.33 | 73.75±8.63 | 0.699 | 74.58±5.82 | 74.41±5.99 | 0.931 |
| Nasal quadrant (µm) | 75.72±6.6 | 81.08±12.6 | 0.364 | 76.68±10.67 | 78.58±8.45 | 0.561 |
| GCC (µm) | 96.27±1.94 | 96.75±1.94 | 0.849 | 96.05±5.05 | 96.82±4.95 | 0.659 |
RNFL: Retinal nerve fiber layer, GCC: Ganglion cell complex
Further correlation analyses demonstrated a significant inverse relationship between RNFL thickness and migraine characteristics such as age, disease duration, number of attacks per month, and severity in four quadrants [Table 4]. OCT-A parameters, including VD in DCP, SCP, and RCP, were not associated with gender distribution and laterality of headache [Table 5]. However, they were inversely correlated with these clinical features, reinforcing the link between prolonged disease and reduced VD [Table 6].
Table 4.
Correlation between retinal nerve fiber layer thickness parameters and migraine characteristics
| Age | Disease duration | Number of attacks per month | Severity | |
|---|---|---|---|---|
| Average thickness of RNFL (µm) | r=0.566 | r=−0.67 | r=−0.670 | r=−0.632 |
| P=0.18 | P=0.003 | P=0.003 | P=0.006 | |
| Superior quadrant (µm) | r=−0.394 | r=−0.569 | r=0.615 | r=0.575 |
| P=0.117 | P=0.017 | P=0.009 | P=0.016 | |
| Inferior quadrant (µm) | r=−0.634 | r=−0.712 | r=−0.641 | r=−0.607 |
| P=0.006 | P=0.001 | P=0.006 | P=0.01 | |
| Temporal quadrant (µm) | r=−0.521 | r=−0.519 | r=−0.407 | r=−0.375 |
| P=0.032 | P=0.033 | P=0.105 | P=0.138 | |
| Nasal quadrant (µm) | r=−0.419 | r=−0.514 | r=−0.593 | r=−0.581 |
| P=0.094 | P=0.035 | P=0.012 | P=0.014 | |
| GCC thickness (µm) | r=−0.564 | r=−0.683 | r=−0.590 | r=−0.612 |
| P=0.018 | P=0.003 | P=0.013 | P=0.009 |
RNFL: Retinal nerve fiber layer, GCC: Ganglion cell complex
Table 5.
Comparison of optical coherence tomography–angiography parameters and both gender and laterality in migraine patients
| Male | Female | P | Headache side eye | Contralateral side eye | P | |
|---|---|---|---|---|---|---|
| Vascular density in DCP (%) | 48.97±3.52 | 50.45±4.62 | 0.477 | 49.39±4.11 | 49.62±4.11 | 0.881 |
| Vascular density in SCP (%) | 49.95±1.59 | 50.18±2.03 | 0.802 | 49.92±1.88 | 50.13±1.9 | 0.749 |
| Vascular density in RCP (%) | 50.64±1.32 | 51.03±2.43 | 0.669 | 50.71±2.06 | 50.84±2 | 0.862 |
| FAZ (mm2) | 0.295±0.89 | 0.334±0.74 | 0.373 | 0.308±0.1 | 0.31±0.077 | 0.953 |
DCP: Deep capillary plexus, SCP: Superficial capillary plexus, RCP: Radial peripapillary capillary plexus, FAZ: Foveal avascular zone
Table 6.
Correlation between optical coherence tomography–angiography parameters and migraine characteristics
| Age | Disease duration | Number of attacks per month | Severity | |
|---|---|---|---|---|
| Vascular density in DCP (%) | r=−0.307 | r=−0.601 | r=−0.750 | r=−0.730 |
| P=0.230 | P=0.011 | P=0.001 | P=0.001 | |
| Vascular density in SCP (%) | r=−0.569 | r=−0.724 | r=−0.499 | r=−0.523 |
| P=0.017 | P=0.001 | P=0.041 | P=0.031 | |
| Vascular density in RCP (%) | r=−0.502 | r=−0.719 | r=−0.748 | r=−0.723 |
| P=0.40 | P=0.855 | P=0.001 | P=0.001 | |
| FAZ (mm2) | r=−0.31 | r=0.178 | r=0.3 | r=0.345 |
| P=0.906 | P=0.494 | P=0.243 | P=0.175 |
DCP: Deep capillary plexus, SCP: Superficial capillary plexus, RCP: Radial peripapillary capillary plexus, FAZ: Foveal avascular zone
Discussion
The application of innovative technology, exemplified by OCT, has significantly advanced the assessment of retinal involvement in patients suffering from migraines. However, this progress has given rise to a complex landscape of research outcomes, marked by conflicting findings.[4,5] In migraine pathophysiology, cerebral vasodilation has long been emphasized as a key factor in attacks, supported by the effectiveness of vasoconstrictors such as triptans and ergotamine.[6] However, there has been a shift in focus to dysfunctional neurogenic mechanisms during the ictal period, such as brainstem and hypothalamus activation. Despite this shift, vascular dysregulation remains crucial to understanding migraine pathogenesis. The trigeminal vascular system activation during a migraine attack releases pro-inflammatory vasoactive markers such as substance P, calcitonin gene-related peptide, neuropeptide Y, norepinephrine, and nitric oxide. These markers activate and sensitize nociceptive neuronal pathways, contributing to the intricate web of migraine-related phenomena.
Neurovascular coupling has been highlighted in studies involving human brain imaging during migraine aura and animal models simulating cortical spreading depression. The latter represents a key pathophysiological mechanism related to migraine aura, trigeminal activation, and headache, involving neuronal depolarization, energy metabolism alterations, and blood flow changes.[7]
Among these complexities, RNFL thickness examination using OCT emerges as a valuable diagnostic avenue. However, the literature reports inconsistencies in findings. Some studies reveal a significant difference in average RNFL thickness between migraine patients and control subjects, while others report no significant decrease.[4,5]
In our study, we undertook a comprehensive exploration, revealing no significant difference in average RNFL thickness between control subjects and migraine patients. This divergence in results, we propose, could be attributed to variations in methodology, sample size, ethnic disparities, and the absence of standardized migraine characteristics across studies.
Expanding the investigation to specific quadrants, our study uncovered a significant difference in the superior quadrant, aligning with findings by Gipponi et al.[5] However, discordance exists in other quadrants among different studies, underscoring the complexity of the relationship between RNFL thickness and migraine.
GCC thickness in migraine patients has been a less explored domain. Similar to the study by Tunç et al., our study revealed no significant thinning of GCC thickness in migraine patients compared to the control group.[8] However, other studies have presented varying outcomes, reflecting the intricacies involved in unraveling the relationship between migraines and retinal structures.
Despite the wealth of knowledge generated by various studies, controversies continue to shroud several aspects of the intricate relationship between migraines and retinal structures. Few studies have ventured into the correlation between RNFL thickness and age and gender. Our study is congruent with the recent meta-analysis by Lin et al., showing no significant correlations between age, gender, and RNFL thickness.[9]
Controversies surround the impact of aura on RNFL thickness. Some authors found no significant difference between migraine patients with and without aura.[10] This could be attributed to vascular spasm occurring not only in migraines with aura but also in those without, supported by increased resistance in retinal arteries during crises demonstrated by Doppler ultrasound.[11]
Migraine with aura poses a recognized risk for subclinical brain ischemic lesions and strokes, particularly in young women. The heightened vascular assault in migraines with aura, driven by trigeminal vascular system activation, releases vasoactive neurotransmitters, leading to exacerbated vascular changes.[12] Rare cases of retinal vasospasm during migraines suggest that recurrent spasms induce vascular occlusive events, potentially causing permanent ocular damage.[13]
Our study, consistent with Martinez et al.’s findings, reveals a more substantial decrease in RNFL thickness in migrainous eyes, potentially linked to chronic vasospasms and focal ischemia during attacks.[14] Peripapillary RNFL thickness may correlate with migraine duration, as seen in Feng et al.’s study, suggesting that chronic migraine contributes to severe neuronal degeneration.[4]
Further exploring the potential correlation between peripapillary RNFL thickness and migraine duration, our study delved into existing disparities in the literature. While some authors have reported no significant correlation between RNFL changes and migraine duration.[5,15] Our findings are consistent with those of Feng et al., suggesting that chronic migraine may contribute to more pronounced RNFL thickness alterations and neuronal degeneration.[4]
Intriguingly, this observation, while controversial, draws parallels with glaucoma. The nature of chronic migraine, characterized by recurrent vasospasms and focal ischemia during attacks, could explain chronic optic nerve lesions with subsequent peripapillary RNFL thinning.
Migraine severity, assessed using the Migraine Disability Assessment score, shows a significant correlation with various OCT parameters. However, discrepancies exist with studies using visual analog scales, likely due to the subjectivity of the latter.[16,17]
Regarding RNFL thickness and migraine laterality, our findings are in agreement with the literature, suggesting no significant results despite observed differences between ipsilateral and contralateral eyes.[18,19] Bilateral RNFL thinning may reflect diffuse hypoperfusion affecting beyond the involved hemisphere.
Diving deeper into the realm of OCT-A parameters, studies examining the vascular dynamics in migrainous eyes have been relatively scarce. The study by Chang et al. reported reduced VD in the SCP in migraine eyes with aura compared to those without aura.[20] Ulusoy et al. demonstrated significantly reduced VD in both SCP and DCP in migraine eyes with and without aura.[21] Conversely, our study in line with Bingöl et al. demonstrated no VD difference in SCP and DCP among different groups, suggesting that the absence of retinal microvasculature changes in migraine eyes may be attributed to a regulatory system maintaining constant retinal blood flow despite variations in ocular perfusion pressure.[22]
RPC and FAZ analysis showed no significant difference between migraine eyes and control subjects in agreement with the results presented in the literature.[21,22,23,24]
Few studies have analyzed correlations of OCT-A parameters with age and gender. Taşlı and Ersoy were among the few to analyze this association, demonstrating a negative correlation between age and VD in SCP, DCP, and RPC. While a positive correlation was shown between FAZ area and age.[24] We showed a weakly significant relationship between age and VD in SCP.
Most studies found no significant difference in FAZ among migraine eyes with and without aura. Combining results from nine studies, Ke et al. demonstrated a tendency for wider FAZ in eyes with aura.[25] Our results are consistent with Ke et al. revealing a VD reduction in both vascular plexus and an enlargement of the FAZ in eyes with migraine with aura, although not statistically significant.[25]
We demonstrated a weakly significant negative correlation between VD in DCP and migraine duration, as well as a negative correlation between duration and VD in SCP. These findings are congruent with Taşlı and Ersoy, proving that even though migraine is a periodic disease, it is also chronic, explaining the effect of duration on VD.[24]
It is important to note that our study has certain limitations. The sample size is relatively small, which may impact the generalizability of the findings. Additionally, the inability to assist patients during migraine attacks constitutes a serious limitation, as real-time observations during crises could have provided valuable insights. These limitations underscore the need for caution in interpreting results, and future studies with larger and more diverse samples, rigorous statistical corrections, and consideration of potential confounding factors are warranted to enhance the robustness and generalizability of the findings.
Conclusion
Understanding ocular perfusion abnormalities in migraine may offer insights into the pathophysiology of this prevalent neurological disorder. Hence, OCT-A revealed a trend toward vessel density decrease in SCP and DCP of migraine eyes with aura, potentially indicating ocular perfusion abnormalities. Notably, significant correlations were found between certain migraine clinical characteristics and vascular alterations. Further research is warranted to validate these findings and the potential of OCT-A as a biomarker for migraine with aura. Our novel exploration of OCT-A parameters and migraine laterality showed no significant correlation, supporting the concept of widespread hypoperfusion beyond the affected hemisphere.
Conflicts of interest
There are no conflicts of interest.
Funding Statement
Nil.
References
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