984
Views
1
CrossRef citations to date
0
Altmetric
Review

The eye in migraine: a review of retinal imaging findings in migraine

ORCID Icon & ORCID Icon
Pages 186-193 | Received 02 Apr 2021, Accepted 17 Aug 2021, Published online: 19 Sep 2021

References

  • Stovner L, Hagen K, Jensen R, et al. The global burden of headache: a documentation of headache prevalence and disability worldwide. Cephalalgia. 2007;27:193–210.
  • GBD Neurology Collaborators. Global, regional, and national burden of neurological disorders, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol. 2019;18:459–480.
  • Headache Classification Committee of the International Headache Society (IHS). The International Classification of Headache Disorders, 3rd edition. Cephalalgia. 2018;38:1–211.
  • Karsan N, Goadsby PJ. Biological insights from the premonitory symptoms of migraine. Nat Rev Neurol. 2018;14:699–710.
  • Bose P, Goadsby PJ. The migraine postdrome. Curr Opin Neurol. 2016;29:299–301.
  • Viana M, Sances G, Linde M, et al. Clinical features of migraine aura: results from a prospective diary-aided study. Cephalalgia. 2017;37:979–989.
  • Lipton RB, Stewart WF, Simon D. Medical consultation for migraine: results from the American migraine study. Headache. 1998;38:87–96.
  • PJ Goadsby, Pr Holland. An update: pathophysiology of migraine. Neurol Clin. 2019;37:651–671.
  • Gross EC, Lisicki M, Fischer D, et al. The metabolic face of migraine - from pathophysiology to treatment. Nat Rev Neurol. 2019;15:627–643.
  • May A, Burstein R. Hypothalamic regulation of headache and migraine. Cephalalgia. 2019;39:1710–1719.
  • Pietrobon D, Brennan KC. Genetic mouse models of migraine. J Headache Pain. 2019;20:79.
  • Colombo B, Messina R, Rocca MA, et al. Imaging the migrainous brain: the present and the future. Neurol Sci. 2019;40:49–54.
  • Vecchia D, Pietrobon D. Migraine: a disorder of brain excitatory-inhibitory balance? Trends Neurosci. 2012;35:507–520.
  • Jacobs B, Dussor G. Neurovascular contributions to migraine: moving beyond vasodilation. Neuroscience. 2016;338:130–144.
  • Akerman S, Pr Holland, PJ Goadsby. Diencephalic and brainstem mechanisms in migraine. Nat Rev Neurosci. 2011;12:570–584.
  • Mason BN, Russo AF. Vascular contributions to migraine: time to revisit? Front Cell Neurosci. 2018;12:233.
  • Noseda R, Burstein R. Migraine pathophysiology: anatomy of the trigeminovascular pathway and associated neurological symptoms, cortical spreading depression, sensitization, and modulation of pain. Pain. 2013;154(Suppl):S44–53.
  • Ashina M, Hansen JM, Do TP, et al. Migraine and the trigeminovascular system-40 years and counting. Lancet Neurol. 2019;18:795–804.
  • Hoffmann J, Baca SM, Akerman S. Neurovascular mechanisms of migraine and cluster headache. J Cereb Blood Flow Metab. 2019;39:573–594.
  • Harriott AM, Takizawa T, Chung DY, et al. Spreading depression as a preclinical model of migraine. J Headache Pain. 2019;20:45.
  • Pietrobon D, Moskowitz MA. Chaos and commotion in the wake of cortical spreading depression and spreading depolarizations. Nat Rev Neurosci. 2014;15:379–393.
  • Flammer J, Konieczka K, Flammer AJ. The primary vascular dysregulation syndrome: implications for eye diseases. EPMA J. 2013;4:14.
  • Flammer J, Pache M, Resink T. Vasospasm, its role in the pathogenesis of diseases with particular reference to the eye. Prog Retin Eye Res. 2001;20:319–349.
  • Hauptmann A. Capillaries in the finger nail fold in patients with neurosis, epilepsy and migraine. Arch Neurol Psychiatry. 1946;56:631–642.
  • Gasser P, Meienberg O. Finger microcirculation in classical migraine. A video-microscopic study of nailfold capillaries. Eur Neurol. 1991;31:168–171.
  • Hegyalijai T, Meienberg O, Dubler B, et al. Cold-induced acral vasospasm in migraine as assessed by nailfold video-microscopy: prevalence and response to migraine prophylaxis. Angiology. 1997;48:345–349.
  • Komatsu K, Fukutake T, Hattori T. Fingertip photoplethysmography and migraine. J Neurol Sci. 2003;216:17–21.
  • O’Keeffe ST, Tsapatsaris NP, Beetham WP Jr. Association between Raynaud’s phenomenon and migraine in a random population of hospital employees. J Rheumatol. 1993;20:1187–1188.
  • Atkinson RA, Appenzeller O. Hemicrania and Raynaud’s phenomenon; manifestations of the same disease? Headache. 1976;16:1–3.
  • Zahavi I, Chagnac A, Hering R, et al. Prevalence of Raynaud’s phenomenon in patients with migraine. Arch Intern Med. 1984;144:742–744.
  • Kamshilin AA, Volynsky MA, Khayrutdinova O, et al. Novel capsaicin-induced parameters of microcirculation in migraine patients revealed by imaging photoplethysmography. J Headache Pain. 2018;19:43.
  • Gomi S, Gotoh F, Komatsumoto S, et al. Sweating function and retinal vasomotor reactivity in migraine. Cephalalgia. 1989;9:179–185.
  • Kara SA, Erdemoglu AK, Karadeniz MY, et al. Color Doppler sonography of orbital and vertebral arteries in migraineurs without aura. J Clin Ultrasound. 2003;31:308–314.
  • Liew G, Mitchell P, Wong TY, et al. Retinal vascular caliber and migraine: the blue mountains eye study. Headache. 2006;46:997–1004.
  • Rose KM, Wong TY, Carson AP, et al. Migraine and retinal microvascular abnormalities: the atherosclerosis risk in communities study. Neurology. 2007;68:1694–1700.
  • Wen KX, Mutlu U, Ikram MK, et al. The retinal microcirculation in migraine: the rotterdam study. Cephalalgia. 2018;38:736–743.
  • Unlu M, Sevim DG, Gultekin M, et al. Changes in retinal vessel diameters in migraine patients during attack-free period. Int J Ophthalmol. 2017;10:439–444.
  • Killer HE, Forrer A, Flammer J. Retinal vasospasm during an attack of migraine. Retina. 2003;23:253–254.
  • Abdul-Rahman AM, Gilhotra JS, Selva D. Dynamic focal retinal arteriolar vasospasm in migraine. Indian J Ophthalmol. 2011;59:51–53.
  • Friedman MW. Occlusion of central retinal vein in migraine. AMA Arch Ophthalmol. 1951;45:678–682.
  • Graveson GS. Retinal arterial occlusion in migraine. Br Med J. 1949;2:838–840.
  • Gray JA, Carroll JD. Retinal artery occlusion in migraine. Postgrad Med J. 1985;61:517–518.
  • Gutteridge IF, McDonald RA, Plenderleith JG. Branch retinal artery occlusion during a migraine attack. Clin Exp Optom. 2007;90:371–375.
  • Hykin PG, Gartry D, Brazier DJ, et al. Bilateral cilio-retinal artery occlusion in classic migraine. Postgrad Med J. 1991;67:282–284.
  • Katz B. Migrainous central retinal artery occlusion. J Clin Neuroophthalmol. 1986;6:69–75.
  • Krapin D. Occlusion of the central retinal artery in migraine. N Engl J Med. 1964;270:359–360.
  • Coppeto JR, Lessell S, Sciarra R, et al. Vascular retinopathy in migraine. Neurology. 1986;36:267–270.
  • Christakis PG, Alon R, Brent MH. Recurrent visual field defect associated with migraine resulting in a hemiretinal artery occlusion. Can J Ophthalmol. 2018;53:e92–e94.
  • Al-Moujahed A, Tran EM, Azad A, et al. Risk of retinal artery occlusion in patients with migraine. Am J Ophthalmol. 2020;225:157–165.
  • Grosberg BM, Solomon S, Friedman DI, et al. Retinal migraine reappraised. Cephalalgia. 2006;26:1275–1286.
  • Alizadeh R, Vickers L, Hirunpatravong P, et al. A phenotype of primary open-angle glaucoma with systemic vasospasm. J Glaucoma. 2018;27:987–992.
  • Konieczka K, Choi HJ, Koch S, et al. Relationship between normal tension glaucoma and Flammer syndrome. EPMA J. 2017;8:111–117.
  • Orzalesi N, Rossetti L, Omboni S, et al. Conproso. Vascular risk factors in glaucoma: the results of a national survey. Graefes Arch Clin Exp Ophthalmol. 2007;245:795–802.
  • Klein BE, Klein R, Meuer SM, et al. Migraine headache and its association with open-angle glaucoma: the Beaver Dam Eye Study. Invest Ophthalmol Vis Sci. 1993;34:3024–3027.
  • Orgul S, Flammer J. Headache in normal-tension glaucoma patients. J Glaucoma. 1994;3:292–295.
  • Usui T, Iwata K, Shirakashi M, et al. Prevalence of migraine in low-tension glaucoma and primary open-angle glaucoma in Japanese. Br J Ophthalmol. 1991;75:224–226.
  • Chen HY, Lin CL, Kao CH. Does migraine increase the risk of glaucoma?: a population-based cohort study. Medicine (Baltimore). 2016;95:e3670.
  • Landers J, Goldberg I, Graham SL. Analysis of risk factors that may be associated with progression from ocular hypertension to primary open angle glaucoma. Clin Exp Ophthalmol. 2002;30:242–247.
  • Suzuki Y, Iwase A, Araie M, et al. Risk factors for open-angle glaucoma in a Japanese population: the Tajimi Study. Ophthalmology. 2006;113:1613–1617.
  • Perruccio AV, Badley EM, Trope GE. Self-reported glaucoma in Canada: findings from population-based surveys, 1994-2003. Can J Ophthalmol. 2007;42:219–226.
  • Pradalier A, Hamard P, Sellem E, et al. Migraine and glaucoma: an epidemiologic survey of French ophthalmologists. Cephalalgia. 1998;18:74–76.
  • Wang JJ, Mitchell P, Smith W. Is there an association between migraine headache and open-angle glaucoma? Findings from the blue mountains eye study. Ophthalmology. 1997;104:1714–1719.
  • Hewitt AW, Wu J, Green CM, et al. Systemic disease associations of familial and sporadic glaucoma: the glaucoma inheritance study in Tasmania. Acta Ophthalmol. 2010;88:70–74.
  • Corbett JJ, Phelps CD, Eslinger P, et al. The neurologic evaluation of patients with low-tension glaucoma. Invest Ophthalmol Vis Sci. 1985;26:1101–1104.
  • Cursiefen C, Wisse M, Cursiefen S, et al. Migraine and tension headache in high-pressure and normal-pressure glaucoma. Am J Ophthalmol. 2000;129:102–104.
  • Phelps CD, Corbett JJ. Migraine and low-tension glaucoma. A case-control study. Invest Ophthalmol Vis Sci. 1985;26:1105–1108.
  • Gramer G, Weber BH, Migraine Gramer E. Vasospasm in glaucoma: age-related evaluation of 2027 patients with glaucoma or ocular hypertension. Invest Ophthalmol Vis Sci. 2015;56:7999–8007.
  • Lin HC, Chien CW, Hu CC, et al. Comparison of comorbid conditions between open-angle glaucoma patients and a control cohort: a case-control study. Ophthalmology. 2010;117:2088–2095.
  • Morgan RW, Drance SM. Chronic open-angle glaucoma and ocular hypertension. An epidemiological study. Br J Ophthalmol. 1975;59:211–215.
  • Girkin CA, McGwin G Jr., McNeal SF, et al. Hypothyroidism and the development of open-angle glaucoma in a male population. Ophthalmology. 2004;111:1649–1652.
  • Motsko SP, Jones JK. Is there an association between hypothyroidism and open-angle glaucoma in an elderly population? An epidemiologic study. Ophthalmology. 2008;115:1581–1584.
  • Huang JY, Su CC, Wang TH, et al. Migraine and increased risk of developing open angle glaucoma: a population-based cohort study. BMC Ophthalmol. 2019;19:50.
  • Xu C, Li J, Li Z, et al. Migraine as a risk factor for primary open angle glaucoma: a systematic review and meta-analysis. Medicine (Baltimore). 2018;97:e11377.
  • Furlanetto RL, De Moraes CG, Teng CC, et al. Low-pressure glaucoma treatment study g. risk factors for optic disc hemorrhage in the low-pressure glaucoma treatment study. Am J Ophthalmol. 2014;157:945–952.
  • Anderson DR. Normal Tension Glaucoma S. Collaborative normal tension glaucoma study. Curr Opin Ophthalmol. 2003;14:86–90.
  • Lin X, Yi Z, Zhang X, et al. Retinal nerve fiber layer changes in migraine: a systematic review and meta-analysis. Neurol Sci. 2021;42 (3):871–881.
  • Cankaya C, Tecellioglu M. Foveal thickness alterations in patients with migraine. Med Arch. 2016;70:123–126.
  • Gunes A, Karadag AS, Yazgan S, et al. Evaluation of retinal nerve fibre layer, ganglion cell layer and choroidal thickness with optical coherence tomography in migraine patients: a case-control study. Clin Exp Optom. 2018;101:109–115.
  • Yener AU, Korucu O. Quantitative analysis of the retinal nerve fiber layer, ganglion cell layer and optic disc parameters by the swept source optical coherence tomography in patients with migraine and patients with tension-type headache. Acta Neurol Belg. 2019;119:541–548.
  • Ekinci M, Ceylan E, Cagatay HH, et al. Retinal nerve fibre layer, ganglion cell layer and choroid thinning in migraine with aura. BMC Ophthalmol. 2014;14:75.
  • Reggio E, Chisari CG, Ferrigno G, et al. Migraine causes retinal and choroidal structural changes: evaluation with ocular coherence tomography. J Neurol. 2017;264:494–502.
  • Nguyen CTO, Hui F, Charng J, et al. Retinal biomarkers provide “insight” into cortical pharmacology and disease. Pharmacol Ther. 2017;175:151–177.
  • Tsokolas G, Tsaousis KT, Diakonis VF, et al. Optical coherence tomography angiography in neurodegenerative diseases: a review. Eye Brain. 2020;12:73–87.
  • Pellegrini M, Vagge A, Ferro Desideri LF, et al. Optical coherence tomography angiography in neurodegenerative disorders. J Clin Med. 2020;9.
  • Chang MY, Phasukkijwatana N, Garrity S, et al. Foveal and peripapillary vascular decrement in migraine with aura demonstrated by optical coherence tomography angiography. Invest Ophthalmol Vis Sci. 2017;58:5477–5484.
  • Broadway DC, Drance SM. Glaucoma and vasospasm. Br J Ophthalmol. 1998;82:862–870.
  • Tasli NG, Ersoy A. Altered macular vasculature in migraine patients without aura: is it associated with ocular vasculature and white matter hyperintensities? J Ophthalmol. 2020;2020:3412490.
  • Ulusoy MO, Horasanli B, Kal A. Retinal vascular density evaluation of migraine patients with and without aura and association with white matter hyperintensities. Acta Neurol Belg. 2019;119:411–417.
  • Bingol Kiziltunc P, Ozcan G, Ozer F, et al. Evaluation of retinal vessel density and choriocapillaris flow in migraine patients with and without aura. Graefes Arch Clin Exp Ophthalmol. 2020;258:2517–2521.
  • Guo Y, Pang Y, Kang Y, et al. Correlations among peripapillary vasculature, macular superficial capillaries, and eye structure in healthy and myopic eyes of Chinese young adults (STROBE). Medicine (Baltimore). 2020;99:e22171.
  • Bingol Kiziltunc P, Atilla H. Vascular changes with optical coherence tomography angiography during aura of migraine: a case report. Eur J Ophthalmol. 2020;31 (2):NP54–NP57.
  • Guler O, Guler M, Tugan Yildiz CB, et al. Peripapillary blood flows affected during migraine attack? Neuroophthalmology. 2020;44:299–306.
  • McKendrick AM, Badcock DR. Decreased visual field sensitivity measured 1 day, then 1 week, after migraine. Invest Ophthalmol Vis Sci. 2004;45:1061–1070.
  • Nguyen BN, Vingrys AJ, McKendrick AM. The effect of duration post-migraine on visual electrophysiology and visual field performance in people with migraine. Cephalalgia. 2014;34:42–57.
  • Schindelin J, Arganda-Carreras I, Frise E, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9:676–682.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.