Assessment of the Optic Disc and Retinal Microvasculature by Optical Coherence Tomography Angiography in Patients With Pediatric Migraine

Migraine, as a chronic neurovascular disease, is known to be a risk factor for retinal and optic nerve head damage. Herein, we aimed to evaluate the optic disc and retinal microvasculature in pediatric migraine (PM) patients using optical coherence tomography angiography (OCTA).

Original Contribution Section Editors: Clare Fraser, MD Susan Mollan, MD Assessment of the Optic Disc and Retinal Microvasculature by Optical Coherence Tomography Angiography in Patients With Pediatric Migraine Bengi Ece Kurtul, MD, Cansu Sipal, MD, Yilmaz Akbas, MD Background: Migraine, as a chronic neurovascular disease, is known to be a risk factor for retinal and optic nerve head damage. Herein, we aimed to evaluate the optic disc and retinal microvasculature in pediatric migraine (PM) patients using optical coherence tomography angiography (OCTA). Methods: Forty-six eyes of 23 patients with PM without aura (PM group) and 46 eyes of 23 age- and sex-matched healthy subjects (control group) were included in this crosssectional prospective study. Demographic features and ophthalmological examination including OCTA measurements were evaluated. OCTA was performed with 6- · 6-mm sections for macula and 4.5- · 4.5-mm sections for optic nerve head in all eyes. Foveal retinal thickness (FRT), peripapillary retinal nerve fiber layer (RNFL) thickness, vessel density in different sections of the retina, and optic disc were analyzed and compared between the groups. All measurements of the PM patients were taken in the attackfree period. Results: The mean ages of the PM group and control group were 11.17 ± 3.3 and 11.83 ± 2.8 years, respectively (P = 0.479). Gender and mean intraocular pressures were similar between the groups. The mean central corneal thickness levels in the PM group were significantly lower than control group, 548.28 ± 26.3 mm and 562.04 ± 24.5 mm, respectively (P = 0.011). There was no significant difference regarding average and all quadrant RNFL thicknesses, foveal avascular zone and flow areas, deep vessel densities, and optic disc capillary densities between the groups. However, compared with the control group, the PM group showed significant higher values of FRT, and lower values of superficial whole and parafoveal vessel densities (247.28 ± 15.8 mm vs 285.93 ± 11.1, P , 0.001, 51.85 ± 2.4% vs 50.31 ± 4.0%, P = 0.02, 55.09 ± 2.3% vs 53.5 ± 3.5%, P = Tayfur Ata Sökmen Faculty of Medicine (BEK), Department of Ophthalmology, Hatay Mustafa Kemal University, Hatay, Turkey; Tayfur Ata Sökmen Faculty of Medicine (CS), Department of Ophthalmology, Mustafa Kemal University, Hatay, Turkey; and Tayfur Ata Sökmen Faculty of Medicine (YA), Department of Pediatric Neurology, Hatay Mustafa Kemal University, Hatay, Turkey. The authors report no conflicts of interest. Address correspondence to Bengi E. Kurtul, MD, Tayfur Ata Sökmen Faculty of Medicine, Department of Ophthalmology, Hatay Mustafa Kemal University, Hatay, Turkey 31060; E-mail: [e-mail] Kurtul et al: J Neuro-Ophthalmol 2023; 43: 191-196 0.01, respectively). Disease duration and attacks/year did not show any significant correlations with OCTA values. Conclusions: PM seems to be associated with lower superficial whole and parafoveal vessel densities because of hypoperfusion and ischemia. OCTA may be suggested for use in follow-up and management of PM patients. Journal of Neuro-Ophthalmology 2023;43:191–196 doi: 10.1097/WNO.0000000000001697 © 2022 by North American Neuro-Ophthalmology Society M igraine is a chronic neurovascular disorder characterized by recurrent headache attacks associated with gastrointestinal, neurologic, and autonomic dysfunction (1). Migraine prevalence was reported as 9.1% in children (1). The common symptoms of migraine are unilateral headache, photophobia, phonophobia, nausea, dizziness, and worsening of pain during physical activity (2,3). Although there are several theories, the pathophysiologic mechanisms of migraine are not clear. Migraine typically occurs with vascular tone changes of cerebral blood vessels leading to cerebral hypoperfusion (4). Ischemia related to hypoperfusion during migraine may lead to changes in the brain, and also the retina and choroid. Although constriction of cerebral and retrobulbar arteries is a transient situation, repeated migraine attacks may cause permanent cerebral and retinal damage (3). Migraine has been reported to be a risk factor for ischemic complications of the retina and optic nerve (5). Retinal vascular occlusions, ischemic optic neuropathy, and normotensive glaucoma are ophthalmic disorders associated with migraine (6–8). Optical coherence tomography angiography (OCTA) is an innovative, noninvasive, rapid, and high-resolution method that shows the microvascular structure of the retina and optic nerve. OCTA is believed to be useful in explaining the pathophysiology of ocular disorders other than retina such as glaucoma or extraocular neurological disorders (9). There are several studies about OCTA 191 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution findings in adults with migraine (10–16). However, to the best of our knowledge, there are no data regarding the effect of migraine on optic nerve head and retinal microvasculature in pediatric patients. Therefore, in this study, we aimed to assess the OCTA findings of pediatric migraine (PM) patients and compare them with age- and sex-matched healthy subjects. METHODS This cross-sectional study was approved by the ethics committee of our institution (approval number: 2021/ 109) and conducted in accordance with all the relevant tenets of the Declaration of Helsinki. PM patients without aura (PM group) who were referred to the ophthalmology outpatient clinic from the department of pediatric neurology, age- and sex-matched healthy subjects (control group) who were admitted to the ophthalmology outpatient clinic for a routine examination with no known migraine were randomly included in the study. Patients who had been newly diagnosed as having PM in our pediatric neurology clinic according to the criteria of the International Classification of Headache Society were recruited for the study (17). PM patients with aura, a neurologic disease other than migraine, and abnormal brain MRI were excluded. All subjects with refractive error of $ ±2.00 diopters, amblyopia, contact lens wear, previous ocular surgery, ocular trauma, and other ocular diseases such as uveitis, cataract, or glaucoma, any systemic disease such as diabetes, hypertension were also excluded. None of the PM patients were receiving chronic migraine prophylactic treatment and all measurements of the patients were performed during the attack-free period. Both eyes of all subjects underwent full ophthalmologic examination including best-corrected visual acuity, biomicroscopic anterior segment, and fundus examination. Intraocular pressure (IOP) and central corneal thickness (CCT) measurements were assessed by noncontact tonometer. The OCTA images were obtained by a single technician using a spectral-domain OCT system with the AngioVue OCTA software (Avanti RTVue-XR 100, Optovue Inc, Fremont, CA). This device uses an increased A scan rate of 70 kHz, which allows the generation of high axial resolution of 5 mm in tissue. The OCTA provides vascular information of retinal layers as an en face angiogram, a vessel density map and a vessel density percentage (%) calculated as the area covered by flowing blood vessels in the selected region. Volumetric angiograms were semi-automatically segmented into 3 layers allowing for separate angiograms of the inner retina, outer retina, and choroid. The OCTA image protocol involved 2 raster scans acquired by repeated B-scans at 304 raster positions, and each B-scan consisted of 304 A-scans covering a 6- · 6-mm area centered on macula and 4.5- · 4.5-mm area centered in optic nerve head. 192 Two volumetric raster scans were taken consecutively, with one in the horizontal priority (x-fast) and one in the vertical priority (y-fast). Motion artifacts including residual axial motion and transverse saccadic motion were removed by three-dimensional (3D) orthogonal registration and by merging the pair of scans using the contained software (ReVue, version 2014.2.0.15; Optovue Inc). Shadow graphic projection artefacts were removed with a slabsubtraction method, reducing inner retinal projection onto the outer retinal angiogram. En face retinal angiograms were created by projecting the flow signal internal to the retinal pigment epithelium. Foveal retinal thickness (FRT), vessel density in fovea of superficial, and deep capillary plexus, 300 mm width around the foveal avascular zone (FAZ) were measured. FAZ was defined as the area without vessels that covers the center of the fovea. Fovea was defined as an annulus centered on the foveal avascular zone with inner and outer ring diameters of 1 mm. Flow areas of outer retina and choriocapillaris were noted, too. Radial peripapillary capillary (RPC) densities including; whole image, inside disc, and peripapillary capillary plexus densities and retinal nerve fiber layer thickness (RNFL) were also obtained. The peripapillary region was automatically defined by the software as a 1.0-mm-wide round annulus extending from the optic disc. OCTA scans with a quality level less than 8, artifacts or decentered were not used in the study. All measurements were taken at the same hour of the day (10:00 AM–12:00 PM) in all groups to rule out effect of diurnal variations on OCTA values. Statistical Analysis Statistical analyses were performed with IBM SPSS for Windows Version 21.0 software. Numerical variables were expressed as mean ± SD. Categorical variables were summarized as numbers and percentages. The normality of distribution of continuous variables was evaluated with the aid of the Kolmogorov–Smirnov test. Independent samples t test was used to determine the difference between 2 groups. Pearson correlation coefficient was used for the correlations between variables, and P value #0.05 was considered to reflect statistical significance. RESULTS Forty-six eyes of 23 PM patients and 46 eyes of 23 control subjects were enrolled. The mean ages of the PM group and control group were 11.17 ± 3.3 and 11.83 ± 2.8 years, respectively (P = 0.479). Gender and mean IOP levels were similar between the groups. Best-corrected visual acuities were 20/20 in all study patients. Number of eyes with refractive errors (# ±1.75 Diopter) in the PM group were significantly higher than the control group (21 [45.7%] vs 4 [8.7%], respectively, P , 0.001). Eleven PM patients had myopia (simple or compound), 9 PM patients had hyperopia (simple or compound), and 1 PM patient had simple Kurtul et al: J Neuro-Ophthalmol 2023; 43: 191-196 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution astigmatism refractive errors. Two subjects had simple hyperopia, and 2 had simple astigmatism refractive errors in control subjects. The mean myopia degrees were significantly different (P = 0.003), but the mean hyperopia, astigmatism, and spherical equivalent degrees were not significantly different (P = 0.117, P = 0.100, and P = 0.065, respectively) between the groups. The mean CCT levels in the PM group were significantly lower than control group, 548.28 ± 26.3 mm and 562.04 ± 24.5 mm, respectively (P = 0.011). The comparisons of demographic and clinical characteristics between the groups were shown in Table 1. There was no significant difference regarding average and all quadrant RNFL thicknesses, foveal avascular zone and flow areas, deep vessel densities, and optic disc capillary densities between the groups. However, compared with the control group, PM group showed significant higher values of FRT, and lower values of superficial whole and parafoveal vessel densities (247.28 ± 15.8 mm vs 285.93 ± 11.1 mm, P , 0.001, 51.85 ± 2.4% vs 50.31 ± 4.0%, P = 0.028, 55.09 ± 2.3% vs 53.5 ± 3.5%, P = 0.017, respectively). OCTA images of a subject from control group and PM group were presented in Figures 1 and 2, respectively. The outcomes of retina and optic disc OCTA parameters of the groups were shown in Tables 2 and 3, respectively. Disease duration and attacks/year did not show any significant correlations with OCTA values. DISCUSSION This study evaluates the optic disc and retinal microvasculature in PM patients with OCTA. Our study showed that compared with the control group, the PM group showed significant higher values of FRT, and lower values of central corneal thicknesses, superficial whole, and parafoveal vessel densities. Nalcacioglu et al (18) evaluated the thickness of the peripapillary RNFL, total macula, macular ganglion cell layer, inner plexiform layer by spectral-domain optic coher- ence tomography, and choroid in PM patients. They mentioned that childhood migraine does not cause changes in posterior ocular structure parameters. In contrast to this study, Yener et al (19) reported that children with migraine showed significant variations in specific RNFL and optic disc parameters using swept-source optical coherence tomography, compared with control subjects. In our study, RNFL levels were similar between the groups. However, different from these studies, we investigated the retinal and optic disc microvasculature by OCTA in PM patients. Based on our findings, OCTA may provide us more detailed information in PM patients compared with optical coherence tomography. Observations of changes in vascular density of retinal microvascular layers could strengthen the link between ischemia and migraine pathophysiology (11). The scientific validity of OCTA for adult migraine patients was reported (11). Herein, we have demonstrated the clinical importance of OCTA also in PM patients. Güler et al (10) compared retinal and peripapillary blood flow parameters in migraine patients during an attack with healthy controls using OCTA. They reported that results suggest that an acute migraine attack does not affect retinal or peripapillary blood flow. They explained this with the retinal autoregulatory system, which may maintain constant retinal blood flow during the migraine attack. In our study, all measurements of the PM patients were taken in the attack-free period. If the OCTA measurements were taken during the attack, different results could be obtained. We were not able to evaluate the patients during a migraine attack. It would be better to compare results with during the attack measurements. However, PM patients in pain could not tolerate such a time-consuming process. OCTA was mentioned as a potentially useful biomarker for migraine with aura (11). Migraine with, but not without, aura was found to be associated with foveal and peripapillary vascular decrements, which may possibly mediate increased risk of ocular and systemic vascular complications TABLE 1. Comparison of demographic and clinical characteristics between the groups Characteristics Number of subjects, n Age, yr (mean ± SD) Gender, n (%) Female Male Body mass index (kg/m2) (mean ± SD) Central corneal thickness (mm) (mean ± SD) Intraocular pressure (mm Hg) (mean ± SD) Number of eyes with refractive errors (#± 1.75 Diopter), n (%) Spherical equivalent (Diopter) (mean ± SD) Duration of migraine (yr) (mean ± SD) Attacks/yr Foveal retinal thickness (mm) (mean ± SD) Kurtul et al: J Neuro-Ophthalmol 2023; 43: 191-196 Pediatric Migraine Group n = 46 Eyes Control Group n = 46 Eyes P 23 11.17 ± 3.3 23 12.33 ± 2.98 0.479 9 (39.1) 14 (60.9) 19.29 ± 4.5 548.28 ± 26.3 16.58 ± 3.2 21 (45.7) 0.69 ± 0.22 1.32 ± 1.2 16.04 ± 10.7 285.93 ± 11.1 11 (47.8) 12 (52.2) 19.69 ± 4.2 562.04 ± 24.5 17.23 ± 2.47 4 (8.7) 0.23 ± 0.02 — — 247.28 ± 15.8 0.552 0.860 0.011 0.284 ,0.001 0.065 ,0.001 193 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution FIG. 1. OCTA image (superficial vessel density) of a 10-year-old female subject from the control group. OCTA indicates optical coherence tomography angiography. FIG. 2. OCTA image (superficial vessel density) of a 10-year-old female patient with migraine. OCTA indicates optical coherence tomography angiography. 194 Kurtul et al: J Neuro-Ophthalmol 2023; 43: 191-196 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution TABLE 2. The outcomes of retina parameters by optical coherence tomography angiography Superficial vessel density (%) Whole image Fovea Parafovea Perifovea Deep vessel density (%) Whole image Fovea Parafovea Perifovea FAZ area (mm2) Flow area for outer retina (mm2) Flow area for choriocapillaris (mm2) Pediatric Migraine Group (n = 46 Eyes) Control Group (n = 46 Eyes) P 50.30 ± 4.0 23.88 ± 7.9 53.57 ± 3.5 51.32 ± 2.8 51.85 ± 2.4 23.64 ± 6.1 55.09 ± 2.3 52.27 ± 2.4 0.028 0.869 0.017 0.090 53.86 ± 6.7 40.43 ± 7.7 57.95 ± 4.7 55.33 ± 7.3 0.25 ± 0.0 0.79 ± 0.4 2.22 ± 0.1 55.90 ± 4.6 41.19 ± 6.6 59.36 ± 3.2 57.45 ± 4.9 0.25 ± 0.0 0.74 ± 0.3 2.23 ± 0.0 0.093 0.616 0.096 0.108 0.801 0.511 0.720 FAZ, area of 300 mm width around the foveal avascular zone. in these patients. In our study, all PM patients had no aura. It may be one reason for insignificant outcomes regarding peripapillary vascular densities in the groups. In the study of Gürakar Özçift et al (16) macular and peripapillary microvasculature were found not be significantly different in patients with migraine than in controls. The mean age was 42.74 ± 8.14 years and 43.09 ± 14.28 years in the migraine group and control group, respectively, in their study. They mentioned that as the duration of migraine prolonged, a significant decrease in choroidal thickness was observed. In our study, there was no significant difference regarding peripapillary microvascularity between groups. Optic nerve head may be affected later or more resistant to hypoxia and inflammation then the fovea, and fovea especially superficial capillaries may be more sensitive to blood circulation changes. We assumed that the elevated FRT measurements were also for compensation. The small number of patients may also be a possible reason for the optic nerve head to appear unaffected. Disease duration and attacks/year did not show any significant correlations with OCTA values. Optic nerve head and retinal layers may probably be affected by many parameters such as caffeine, smoking, current medications, systemic disease, age, gender, and body mass indices. However, none of these factors were present or effective in our pediatric study population. One of the known risk factors in normal tension glaucoma is migraine (20). It was believed that the significantly lower CCT values in PM patients may be the precursor of glaucomatous damage, which has a risk of developing in the future. The mean spherical equivalent degrees were not significantly different between the groups. In addition, the subjects with any corneal pathology and surgery, contact lens wear, and systemic disease such as diabetes that could affect CCT levels, were excluded from the study. Therefore, we believed that CCT values would not be related to refractive error or any other cause except migraine in this study. Our study has some limitations. First, the number of patients in the groups was relatively small. Second, if PM patients with aura were included, we could have obtained more comprehensive results; however, the percentage of aura observed in PM was known as very low in literature. Third, numbers of eyes with refractive errors in the PM TABLE 3. The outcomes of optic disc parameters by optical coherence tomography angiography RNFL thickness (mm) (mean ± SD) Inferior quadrant (mm) Superior quadrant (mm) Temporal quadrant (mm) Nasal quadrant (mm) RPC density (%) (mean ± SD) Whole image Inside disc Peripapillary Pediatric Migraine Group n = 46 eyes Control Group n = 46 eyes P 115.17 ± 13.7 145.76 ± 20.7 138.50 ± 19.9 75.43 ± 10.1 104.26 ± 16.6 117.80 ± 26.59 145.52 ± 35.78 146.15 ± 32.23 77.73 ± 9.73 105.95 ± 33.71 0.553 0.969 0.174 0.269 0.760 49.26 ± 2.2 52.15 ± 5.0 50.52 ± 2.9 49.03 ± 2.7 52.08 ± 3.7 50.37 ± 3.1 0.660 0.941 0.818 RNFL, retinal nerve fiber layer; RPC, radial peripapillary capillary. Kurtul et al: J Neuro-Ophthalmol 2023; 43: 191-196 195 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution group were significantly higher than the control group, and P-value regarding mean spherical equivalent level was close to the limit of significance. However, we believed that the OCTA values would not be affected because these refraction errors were # ±1.75 diopter, and the vision levels were full. For this reason, we believed that the high rate of hyperopic or myopic refractive errors in the PM group would not affect the OCTA values. In addition, it would be better to evaluate axial lengths; however, another device is required for axial length measurement, and this would be very difficult to assess in a group of children with limited tolerance beside OCTA examination device. Finally, PM patients who were receiving treatment were excluded from our study. The PM patients were newly diagnosed ones. Outcomes could also be evaluated in the follow-up of PM patients to predict responses to treatment modalities. This can be the subject of another study. In conclusion, we suggest that OCTA may play an important role in the detection of PM patients. OCTA may provide valuable information about the structural changes of the retinal microvascularity and this can be used for the follow-up of the migraine progression. Larger prospective longitudinal studies are needed to determine whether OCTA findings show a possible increased risk of ocular and systemic vascular events in patients with migraine. STATEMENT OF AUTHORSHIP Conception and design: B. E. Kurtul, Y. Akbas; Acquisition of data: B. E. Kurtul, C. Sipal, Y. Akbas; Analysis and interpretation of data: B. E. Kurtul, Y. Akbas. Drafting the manuscript: B. E. Kurtul, C. Sipal, Y. Akbas; Revising the manuscript for intellectual content: B. E. Kurtul. Final approval of the completed manuscript: B. E. Kurtul, C. Sipal, Y. Akbas. 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