Optic disc and visual test findings in patients with migraine

Optic disc and visual test findings in patients with migraine

Journal of Clinical Neuroscience 20 (2013) 72–74 Contents lists available at SciVerse ScienceDirect Journal of Clinical Neuroscience journal homepag...

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Journal of Clinical Neuroscience 20 (2013) 72–74

Contents lists available at SciVerse ScienceDirect

Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn

Clinical Study

Optic disc and visual test findings in patients with migraine Inci I. Dersu a,⇑, Jeff Thostenson b, F. Jane Durcan c, Sarah M. Hamilton d, Kathleen B. Digre e a

Department of Ophthalmology, College of Medicine, University of Arkansas for Medical Sciences, Little Rock, AR, USA Department of Biostatistics, College of Public Health, University of Arkansas for Medical Sciences, Little Rock, AR, USA c Spokane Eye Clinic, Spokane, WA, USA d Family Medicine Clinic, Salt Lake City, UT, USA e John Moran Eye Center, Salt Lake City, UT, USA b

a r t i c l e

i n f o

Article history: Received 7 March 2012 Accepted 21 May 2012

Keywords: Migraine Optic disc Visual field test

a b s t r a c t This study was conducted to determine whether the optic disc appearance and the visual field parameters of patients with migraine vary from those of age-matched controls. Twenty-two patients with migraine and 20 control participants were enrolled in the study. The automated visual field tests by Humphrey Field AnalyzerÒ and optic disc images by TopconÒ fundus camera were obtained from each participant. Horizontal and vertical cup-to-disc ratios were calculated by a manual, planimetric technique performed by two independent observers. The visual field indices including mean deviation (MD) and pattern standard deviations (PSD) were documented. No difference was found in the average cup-to-disc ratio between patients with migraine and control participants. However, MD and PSD of the groups were different. The average MD in the migraine group was 0.86 + 1.21, and in the control group was 0.10 + 1.03 (p = 0.009). The average PSD in the migraine group was 2.11 + 0.68 and in the control group was 1.68 + 0.44 (p = 0.024). In conclusion, this study demonstrated that patients with migraine had decreased sensitivity in their visual fields compared to the control participants. Published by Elsevier Ltd.

1. Introduction Migraine is a complex neurological disease with undetermined etiology.1 The prevalence of this disease has been reported as 24.4% among the women aged between 30 years and 40 years, when the prevalence reaches to its highest peak.2 The prevalence declines with advancing age to 5% among 60 years and older women. Low tension glaucoma is a type of open angle glaucoma and is observed mainly in those 60 years and older. A higher prevalence of migraine was reported by Corbett and Phelps in the 1980s in patients with low-tension glaucoma, and since then, migraine has been considered a potential vascular risk factor for patients with lowtension glaucoma in other studies.3–5 The relationship between glaucoma and migraine was explored later in two large population-based studies, the Blue Mountain Eye Study and the Beaver Dam Eye Study, and their results were conflicting as the former supported the relationship whereas the latter did not.6,7 However, regardless of any plausible association between glaucoma and migraine, visual field abnormalities have been observed in the migraine population.6–9 Our research question was whether patients with migraine show an early sign of cupping, a hallmark of

⇑ Corresponding author. Address: Jones Eye Institute, 4301 West Markham Street, # 523, Little Rock, AR 72205, USA. Tel.: +1 501 686 5822. E-mail address: [email protected] (I.I. Dersu). 0967-5868/$ - see front matter Published by Elsevier Ltd. http://dx.doi.org/10.1016/j.jocn.2012.05.016

glaucoma, at an age when the migraine attacks are most frequent. Our aim was to investigate the disc appearance and visual field findings in patients with migraine and to compare those to age-matched non-migraine subjects.

2. Methods The study was approved by our Institutional Review Board. Informed consent was obtained from each participant. Subjects diagnosed with migraines according to the criteria established by the International Headache Society were recruited from the neuroophthalmology clinic at the University of Utah.10 Non-migraine subjects were recruited from a general ophthalmology clinic. A detailed questionnaire was given to control subjects to rule out any history of migraine. Migraine subjects with other central nervous system diseases or abnormal MRI findings were excluded. Visual acuity, refraction, and intraocular pressure (IOP) were measured in all subjects followed by an anterior segment slit lamp exam and a dilated fundoscopic exam. Subjects with > 6 diopter myopia and those with a cup-to-disc (C/D) ratio P 0.7 or > 0.2 ratio asymmetry between the eyes were excluded from both groups. Stereo disc photographs and standard automated visual field tests 30.2 pattern (Humphrey Field Analyzer; Humphrey Instruments, Dublin, CA, USA) were obtained. Subjects with unreliable visual field tests (fixation loss > 20%, false negative or false positive responses

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> 33%) were excluded. The photographic slides were projected onto a screen. Disc and cup diameters were measured horizontally and vertically with a ruler by two independent observers masked to the subject’s identity and diagnosis while stereographic paired photographs were being viewed to clearly identify the disc and cup margins. An average of two measurements was used. The horizontal and vertical C/D ratios were calculated by dividing the cup by disc size. The visual field parameters were obtained from the visual field machine print-out. Patient demographics, IOP, visual field parameters, and optic disc parameters were compared by using the Student’s t-test. The Wilcoxon Rank-Sum test was used when normality assumption did not hold. The correlation between visual field and disc parameters was tested by using Spearman’s rank correlation. A p value <0.05 was deemed statistically significant. 3. Results Twenty-two patients with migraine and 20 age-matched control subjects were included. All migraine patients and 17 out of 20 control subjects were females. Age, refractive error and IOP were comparable between the groups (Table 1). The average refractive error was 0.77 ± 1.39 D (range: +0.50, 3.25) in the migraine group and 0.63 ± 1.32 D (range: +1.50, 3.50) in the control group (p = 0.78). The average mean deviation (MD) was 0.86 ± 1.21 in the migraine group, and 0.10 ± 1.03 in the control group (p = 0.009). The average pattern standard deviation (PSD) was 2.11 ± 0.68 and 1.68+ 0.44 in the migraine and control group, respectively (p = 0.024) (Table 2). Optic disc parameters, horizontal, vertical or average C/D ratios, did not show any significant difference between the two groups (Table 2). No significant correlation was found between visual field indices (MD, PSD) and C/D ratios in either the migraine or the control group (Spearman correlation test, p > 0.05). Due to unilateral presentation of the migraine, analysis was repeated for the right and left eyes separately and the results did not change. 4. Discussion We found a statistically significant difference of the MD and PSD between the migraine and the control group upon testing by standard automated perimetry (SAP). Table 1 Demographics of patients with migraine and control participants Control (mean ± SD) No. patients Age Refraction IOP

20 41.95 ± 17.6 0.63 ± 1.32 14.9 ± 2.9

Migraine (mean ± SD) 22 39.04 ± 16.6 –0.77 ± 1.39 14.7 ± 2.6

p-value NS NS NS

⁄ NS = Not significant. IOP = intraocular pressure, SD = standard deviation.

Table 2 Visual field test and optic disc measurements of patients with migraine and control participants Control Average Average Average Average

MD PSD horizontal C/D ratio vertical C/D ratio

0.10 ± 1.03 1.68 ± 0.44 0.33 ± 0.15 0.32 ± 0.15

Migraine 0.86 ± 1.21 2.11 ± 0.6 0.38 ± 0.15 0.35 ± 0.14

p-value 0.009 0.024 0.299 0.474

C/D ratio = cup-to-disc ratio, MD = Mean deviation, PSD = Pattern standard deviation.

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We detected mostly general depression of sensitivity in the visual field. Local changes were rather non-specific and were not suggestive of nasal step or arcuate defect. These findings are consistent with one of the earliest studies reporting automated visual field abnormalities in patients with migraine. Lewis et al. found that approximately one-third (35%) of migraine subjects had visual field changes, mostly in the form of general depression rather than localized defects.9 Also, prevalence of visual field loss was found to be greater with increasing age and duration of disease in the aforementioned study. Although the visual symptoms of migraine represent cortical excitability, visual field defects observed in migraine patients may be unilateral and non-homonymous.8,9 It was postulated that cerebral vasospasm associated with migraine could lead to retinal ganglion cell death by compromising the ocular perfusion to the anterior optic nerve head, although this is not proven.11 We took the opportunity of reviewing the relevant literature about the newer visual field test techniques and optic nerve imaging in migraine subjects. Bistratified ganglion cells and magnocellular retinal ganglion cells (M cells) constitute 10% to 20% of the ganglion cell population as smaller parvocellular ganglion cells comprise nearly 80% of the all ganglion cells.12 Short-wavelength automated perimetry (SWAP), also known as blue-on-yellow perimetry, tests the S-cone neuronal pathway which originates from blue–yellow (bistratified) ganglion cells. SWAP was found more sensitive than SAP for early diagnosis of glaucoma due to the scarcity of this type of ganglion cell.13 It was of interest to the investigators whether SWAP is more sensitive in detecting early visual field defects in migraine patients.14,15 McKendrick et al. studied 25 migraine subjects and 20 age-matched nonmigraine subjects and found that MD and PSD with SWAP were worse than SAP in half of the migraine subjects.14 However, the Farnsworth-Munsell 100-hue test also utilizes the S-cone system, as SWAP was reported to be abnormal in migraine patients; therefore, it was suggested that migraine alone could interfere with SWAP, and could cause visual field defects in patients with migraine without ganglion loss.16 Another test, the Frequency Doubling Perimeter test (FDT), which assesses the function of M-cells, has proved to be a sensitive tool in the detection of early ganglion cell loss in glaucoma due to lower redundancy of this subgroup of ganglion cells.17 A limited number of FDT studies performed in migraine patients showed conflicting results; one study found that MD was worse in patients with migraine, however the other one did not find any differences between migraine and controls.11,18 Nevertheless, owing to frequent abnormal visual field findings, the recommendation that emerged from these studies and our study is to exclude patients with migraine from the normative database studies that engage visual field testing. In addition, when we examined the average C/D ratios in migraine sufferers, we did not find any difference between migraine and controls groups. This is consistent with previous studies by Martinez et al., who examined the stereodisc photographs of migraine patients and age-matched healthy controls and found no difference in the C/D ratio between the two groups.11,19 Furthermore, the confocal scanning laser ophthalmoscope, which provides a computerized optic nerve head topographic analysis, did not detect a difference between the migraine and control groups.20 Retinal nerve fiber layer (RNFL) thickness information is particularly valuable as thinning in this tissue may precede the changes in optic disc topography.21 In a study by Tan et al., RNFL thickness was measured in 39 migraine patients and 25 control subjects by scanning laser polarimetry (GDx VCCÒ, Laser Diagnostic Technologies, San Diego, CA, USA) and no difference was found between the groups.22 Neither average RNFL nor sectorial RNFL in superior or inferior segments was statistically different. In another study by Martinez et al., RNFL thickness was measured in patients with

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migraine with Optical Coherence Tomography (Stratus OCT; Carl Zeiss Meditec, Dublin, CA, USA). Normal average RNFL thickness and, normal superior and inferior quadrant RNFL thicknesses was found in these patients.11 However, in patients with migraine, RNFL thickness in the temporal quadrant was determined to be thinner than in the control group. The temporal quadrant is normally the thinnest segment of the peripapillary RNFL, and thinning in the temporal quadrant has previously been identified in multiple sclerosis; however, the implication of thinning in migraine patients is unknown.23 Our study had some limitations. First, the sample size was small. Second, the visual field data from single tests were used. However, we included only subjects with good reliability test indices in the study. In addition, some researchers have raised the point of repeating the test, since the time of the test in relation to the last headache attack in migraine patients may cause poor reproducibility.18 Last, we did not study the correlation between the duration of migraine and visual field abnormality, and therefore we were unable to address the impact of duration of migraine on the visual field test findings. With these limitations in mind, our study supports the growing evidence of abnormal visual field tests in migraine patients. There is no clear explanation for visual field changes in the migraine population, but not detecting optic disc changes by gold standard disc photos suggests that visual field changes in migraine may not share a common causal pathway with glaucoma. However, prospective cohort studies in a large population using a higher resolution, three-dimensional, optic nerve head analysis technology may be warranted for confirmation. In conclusion, we suggest that migraine patients need to be excluded from serving as controls in any study that requires visual field testing.

Conflicts of interest/disclosures The authors declare that they have no financial, commercial or proprietary or other conflicts of interest in relation to this research and its publication.

Acknowledgements We thank Janet Howard, MD, and Cynthia Bond, MA, for their assistance in the study. This study has been supported by Research to Prevent Blindness Inc, New York, NY.

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