Retinal Nerve Fiber Layer Thickness and Oxidative Stress Parameters in Migraine Patients without Aura: A Pilot Study

Adriana Elena Bulboacă, Ioana C Stănescu, Sorana D Bolboacă, Angelo C Bulboacă, Gyorgy I Bodizs, Cristina A Nicula, Adriana Elena Bulboacă, Ioana C Stănescu, Sorana D Bolboacă, Angelo C Bulboacă, Gyorgy I Bodizs, Cristina A Nicula

Abstract

Background: Migraine is one of the most common disorders and its pathophysiological mechanisms are still under research, oxidative stress being emphasized as an important contributor. This study aimed to analyze the retinal nerve fiber layer (RNFL) thickness and oxidative/anti-oxidant balance in migraine patients.

Methods: Two groups of subjects were evaluated: a group of patients with migraine and a control group of healthy volunteers. RNFL thickness was assessed for all subjects by the ocular coherence tomography spectral domain (OCT-SD). The oxidative stress parameter, namely nitric oxide (NOx), malondialdehyde (MDA), and total oxidative stress (TOS) were assessed. The antioxidant capacity of plasma was evaluated by assessing the level of catalase, and total anti-oxidative (TOS) capacity. Migraine severity was graded using the Migraine Disability Assessment Score (MIDAS) questionnaire.

Results: All the oxidative stress parameters (NOx, MDA, and TOS) were significantly increased, and both parameters for anti-oxidative status were significantly decreased in the migraine group compared with the control group (p < 0.0001). Significant correlations with all the quadrants and different oxidative stress parameters were found, most involved being temporal quadrant. A significant positive correlation between catalase and macular RNFL thickness (inner ring, temporal quadrant) in migraine patients, for both eyes, was observed (p = 0.014 for the right eye and p = 0.12 for the left eye).

Conclusion: The assessment of the oxidative stress/anti-oxidative balance together with RFLN thickness can constitute a promising method to evaluate the progression of the diseases. It can also contribute to the estimation of the efficiency of various therapies targeting oxidative stress and associated inflammation.

Keywords: migraine; optical coherence tomography (OCT); oxidative stress; retinal nerve fiber layer (RNFL) thickness.

Conflict of interest statement

The authors declare no conflict of interest.

References

    1. Stovner L.J., Hagen K., Jensen R., Katsarava Z., Lipton R., Scher A., Steiner T., Zwart J.A. The global burden of headache: A documentation of headache prevalence and disability worldwide. Cephalalgia. 2007;27:193–210. doi: 10.1111/j.1468-2982.2007.01288.x.
    1. Ferroni P., Barbanti P., Della-Morte D., Palmirotta R., Jirillo E., Guadagni F. Redox mechanisms in migraine: Novel therapeutics and dietary interventions. Antioxid. Redox Signal. 2018;28:1144–1183. doi: 10.1089/ars.2017.7260.
    1. Bulboacă A., Dogaru G., Blidaru M., Bulboaca A.C., Stănescu I. Evaluation of oxidative stress in migraine patients with visual aura—the experience of an Rehabilitation Hospital. Balneo Res. J. 2018;9:303–308. doi: 10.12680/balneo.2018.201.
    1. Martin H., Sanchez del Rio M., de Silanes C.L., Alvarez-Linera J., Hernandez J.A., Pareja J.A. Photoreactivity of the occipital cortex measured by functional magnetic resonance imaging-blood oxygenation level dependent in migraine patients and healthy volunteers: Pathophysiological implications. Headache. 2011;51:1520–1528. doi: 10.1111/j.1526-4610.2011.02013.x.
    1. Denuelle M., Boulloche N., Payoux P., Fabre N., Trotter Y., Geraud G. A PET study of photophobia during spontaneous migraine attacks. Neurology. 2011;76:213–218. doi: 10.1212/WNL.0b013e3182074a57.
    1. Huang J., Zong X., Wilkins A., Jenkins B., Bozoki A., Cao Y. fMRI evidence that precision ophthalmic tints reduce cortical hyperactivation in migraine. Cephalalgia. 2011;31:925–936. doi: 10.1177/0333102411409076.
    1. Borkum J.M. Migraine triggers and oxidative stress: A narrative review and synthesis. Headache. 2016;56:12–35. doi: 10.1111/head.12725.
    1. Förster A., Wenz H., Kerl H.U., Brockmann M.A., Groden C. Perfusion patterns in migraine with aura. Cephalalgia. 2014;34:870–876. doi: 10.1177/0333102414523339.
    1. Ekinci M., Ceylan E., Cağatay H.H., Keleş S., Hüseyinoğlu N., Tanyildiz B., Cakici O., Kartal B. Retinal nerve fiber layer, ganglion cell layer and choroid thinning in migraine with aura. BMC Ophthalmol. 2014;14:75. doi: 10.1186/1471-2415-14-75.
    1. Reggio E., Chisari C.G., Ferrigno G., Keleş S., Hüseyinoğlu N., Tanyildiz B., Cakici O., Kartal B. Migraine causes retinal and choroidal structural changes: Evaluation with ocular coherence tomography. J. Neurol. 2017;264:494–502. doi: 10.1007/s00415-016-8364-0.
    1. Sacco S., Ricci S., Carolei A. Migraine and vascular diseases: A review of the evidence and potential implications for management. Cephalalgia. 2012;32:785–795. doi: 10.1177/0333102412451361.
    1. Larrosa-Campo D., Ramón-Carbajo C., Para-Prieto M., Calleja-Puerta S., Cernuda-Morollón E., Pascual J. Migraine as a vascular risk factor. Rev. Neurol. 2012;55:349–358.
    1. Bulboacă A.E., Blidaru M., Dogaru G., Bulboacă A., Stănescu I.C. The effect of nitro-oxidative stress on platelet aggregability in migraine patients in a Rehabilitation Hospital—A pilot study. Balneo Res. J. 2018;9:385–389. doi: 10.12680/balneo.2018.217.
    1. Bulboacă A.E., Bolboacă S.D., Stănescu I.C., Sfrângeu C.A., Porfire A., Tefas L., Bulboacă A.C. The effect of intravenous administration of liposomal curcumin in addition to sumatriptan treatment in an experimental migraine model in rats. Int. J. Nanomed. 2018;13:3093–3103. doi: 10.2147/IJN.S162087.
    1. Lukacs M., Tajti J., Fulop F., Toldi J., Edvinsson L., Vecsei L. Migraine, neurogenic inflammation, drug development—Pharmacochemical aspects. Curr. Med. Chem. 2017;24:3649–3665. doi: 10.2174/0929867324666170712163437.
    1. Yücel M., Kotan D., Gurol Çiftçi G., Çiftçi I.H., Cikriklar H.I. Serum levels of endocan, claudin-5 and cytokines in migraine. Eur. Rev. Med. Pharmacol. Sci. 2016;20:930–936.
    1. Aguggia M., Saracco M.G., Cavallini M., Bussone G., Cortelli P. Sensitization and pain. Neurol. Sci. 2013;34:S37–S40. doi: 10.1007/s10072-013-1382-0.
    1. Friedman D.I. The eye and headache. Continuum. 2015;21:1109–1117. doi: 10.1212/CON.0000000000000204.
    1. Russo A., Tessitore A., Tedeschi G. Migraine and trigeminal system-I can feel it coming. Curr. Pain Headache Rep. 2013;17:367. doi: 10.1007/s11916-013-0367-2.
    1. Shayestagul N.A., Christensen C.E., Amin F.M., Ashina S., Ashina M. Measurement of blood flow velocity in the middle cerebral artery during spontaneous migraine attacks: A systematic review. Headache. 2017;57:852–861. doi: 10.1111/head.13106.
    1. Feng Y.F., Guo H., Huang J.H., Yu J.G., Yuan F. Retinal nerve fiber layer thickness changes in migraine: A meta-analysis of case-control studies. Curr. Eye. Res. 2016;41:814–822. doi: 10.3109/02713683.2015.1056373.
    1. Verroiopoulos G.V., Nitoda E., Ladas I.D., Brouzas D., Antonakaki D., Moschos M.M. Ophthalmological assessment of OCT and electrophysiological changes in migraine patients. J. Clin. Neurophysiol. 2016;33:431–442. doi: 10.1097/WNP.0000000000000256.
    1. Ascaso F.J., Marco S., Mateo J., Martínez M., Esteban O., Grzybowski A. Optical coherence tomography in patients with chronic migraine: Literature review and update. Front Neurol. 2017;8:684. doi: 10.3389/fneur.2017.00684.
    1. Costello F., Burton J.M. Retinal imaging with optical coherence tomography: A biomarker in multiple sclerosis? Eye Brain. 2018;10:47–63. doi: 10.2147/EB.S139417.
    1. Cunha L.P., Lopes L.C., Costa-Cunha L.V., Costa C.F., Pires L.A., Almeida A.L., Monteiro M.L. Macular thickness measurements with frequency domain-OCT for quantification of retinal neural loss and its correlation with cognitive impairment in Alzheimer’s disease. PLoS ONE. 2016;11:e0153830. doi: 10.1371/journal.pone.0153830.
    1. Doustar J., Torbati T., Black K.L., Koronyo Y., Koronyo-Hamaoui M. Optical coherence tomography in Alzheimer’s disease and other neurodegenerative diseases. Front. Neurol. 2017;8:701. doi: 10.3389/fneur.2017.00701.
    1. Costello F. Optical coherence tomography in neuro-ophthalmology. Neurol. Clin. 2017;35:153–163. doi: 10.1016/j.ncl.2016.08.012.
    1. Rebolleda G., Diez-Alvarez L., Casado A., Sánchez-Sánchez C., de Dompablo E., González-López J.J., Muñoz-Negrete F.J. OCT: New perspectives in neuro-ophthalmology. Saudi J. Ophthalmol. 2015;29:9–25. doi: 10.1016/j.sjopt.2014.09.016.
    1. Kwon J.Y., Yang J.H., Han J.S., Kim D.G. Analysis of the retinal nerve fiber layer thickness in Alzheimer disease and mild cognitive impairment. Korean J. Ophthalmol. 2017;31:548–556. doi: 10.3341/kjo.2016.0118.
    1. Lamirel C., Newman N., Biousse V. The use of optical coherence tomography in neurology. Rev. Neurol. Dis. 2009;6:E105–E120.
    1. Cankaya C., Tecellioglu M. Foveal thickness alterations in patients with migraine. Med. Arch. 2016;70:123–126. doi: 10.5455/medarh.2016.70.123-126.
    1. Simsek I.B., Aygun D., Yildiz S. Retinal nerve fiber layer thickness in migraine patients with or without aura. Neuroophthalmology. 2014;39:17–21. doi: 10.3109/01658107.2014.968740.
    1. Karalezli A., Simsek C., Celik G., Eroglu F.C. Evaluation of choroidal thickness using spectral-domain optical coherence tomography in migraine patients during acute migraine attacks: A comparative study. Eye Lond. 2014;28:1477–1481. doi: 10.1038/eye.2014.218.
    1. Sorkhabi R., Mostafaei S., Ahoor M., Talebi M. Evaluation of retinal nerve fiber layer thickness in migraine. Iran J. Neurol. 2013;12:51–55.
    1. Headache Classification Subcommittee of the International Headache Society The international classification of headache disorders: 2nd ed. Cephalalgia: Int. J. Headache. 2004;24(Suppl. 1):9–160. doi: 10.1111/j.1468-2982.2003.00824.x.
    1. Stewart W.F., Lipton R.B., Dowson A.J., Sawyer J. Development and testing of the Migraine Disability Assessment (MIDAS) Questionnaire to assess headache-related disability. Neurology. 2001;56:S20–S28. doi: 10.1212/WNL.56.suppl_1.S20.
    1. Chan A., Duker J.S., Ko T.H., Fujimoto J.G., Schuman J.S. Normal macular thickness measurements in Healthy eyes using stratus optical coherence tomography. Arch. Ophthalmol. 2006;124:193–198. doi: 10.1001/archopht.124.2.193.
    1. Erel O. A new automated colorimetric method for measuring total oxidative status. Clin. Biochem. 2005;38:1103–1111. doi: 10.1016/j.clinbiochem.2005.08.008.
    1. Ohkawa H., Ohishi N., Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem. 1979;95:351–358. doi: 10.1016/0003-2697(79)90738-3.
    1. Giustarini D., Rossi R., Milzani A., Dalle-Donne I. Nitrite and nitrate measurement by Griess reagent in human plasma: Evaluation of interferences and standardization. Methods Enzymol. 2008;440:361–380. doi: 10.1016/S0076-6879(07)00823-3.
    1. Aebi H. Catalase in vitro. Methods Enzymol. 1984;105:121–126.
    1. Yagl K. Assay for blood plasma and serum peroxides. Methods Enzymol. 1984;105:28–31.
    1. Jäntschi L., Bolboacă S.D. Exact probabilities and confidence limits for binomial samples: Applied to the difference between two proportions. Sci. World J. 2010;10:865–878. doi: 10.1100/tsw.2010.75.
    1. May A., Schulte L.H. Chronic migraine: Risk factors, mechanisms and treatment. Nat. Rev. Neurol. 2016;12:455–464. doi: 10.1038/nrneurol.2016.93.
    1. Chai N.C., Peterlin B.L., Calhoun A.H. Migraine and estrogen. Curr. Opin. Neurol. 2014;27:315–324. doi: 10.1097/WCO.0000000000000091.
    1. Vetvik K.G., MacGregor E.A. Sex differences in the epidemiology, clinical features, and pathophysiology of migraine. Lancet Neurol. 2017;16:76–87. doi: 10.1016/S1474-4422(16)30293-9.
    1. Kander M.C., Cui Y., Liu Z. Gender difference in oxidative stress: A new look at the mechanisms for cardiovascular diseases. J. Cell. Mol. Med. 2017;21:1024–1032. doi: 10.1111/jcmm.13038.
    1. Tuncel D., Tolun F.I., Gokce M., Imrek S., Ekerbiçer H. Oxidative stress in migraine with and without aura. Biol. Trace Elem. Res. 2008;126:92–97. doi: 10.1007/s12011-008-8193-9.
    1. Borkum J.M. Harnessing migraines for neural regeneration. Neural. Regen. Res. 2018;13:609–615. doi: 10.4103/1673-5374.230275.
    1. Kozai D., Ogawa N., Mori Y. Redox regulation of transient receptor potential channels. Antioxid. Redox Signal. 2014;21:971–986. doi: 10.1089/ars.2013.5616.
    1. Shimizu S., Takahashi N., Mori Y. TRPs as chemosensors (ROS, RNS, RCS, gasotransmitters) Handb. Exp. Pharmacol. 2014;223:767–794. doi: 10.1007/978-3-319-05161-1_3.
    1. Benemei S., Fusi C., Trevisan G., Geppetti P. The TRPA1 channel in migraine mechanism and treatment. Br. J. Pharmacol. 2014;171:2552–2567. doi: 10.1111/bph.12512.
    1. Wang X., Michaelis E.K. Selective neuronal vulnerability to oxidative stress in the brain. Front. Aging Neurosci. 2010;2:12. doi: 10.3389/fnagi.2010.00012.
    1. Carrì M.T., Valle C., Bozzo F., Cozzolino M. Oxidative stress and mitochondrial damage: Importance in non-SOD1 ALS. Front. Cell. Neurosci. 2015;9:41. doi: 10.3389/fncel.2015.00041.
    1. Schulte L.H., May A. The migraine generator revisited: Continuous scanning of the migraine cycle over 30 days and three spontaneous attacks. Brain. 2016;139:1987–1993. doi: 10.1093/brain/aww097.
    1. Lai T.H., Protsenko E., Cheng Y.C., Loggia M.L., Coppola G., Chen W.T. Neural Plasticity in Common Forms of Chronic Headaches. Neural Plast. 2015;2015:205985. doi: 10.1155/2015/205985.
    1. Förstermann U., Sessa W.C. Nitric oxide synthases: Regulation and function. Eur. Heart J. 2012;33:829–837. doi: 10.1093/eurheartj/ehr304.
    1. Alderton W.K., Cooper C.E., Knowles R.G. Nitric oxide synthases: Structure, function and inhibition. Biochem J. 2001;357:593–615. doi: 10.1042/bj3570593.
    1. Radi R. Oxygen radicals, nitric oxide, and peroxynitrite: Redox pathways in molecular medicine. PNAS. 2018;115:5839–5848. doi: 10.1073/pnas.1804932115.
    1. Mueller C.F., Laude K., McNally J.S., Harrison D.G. Redox mechanisms in blood vessels. Arterioscler. Thromb. Vasc. Biol. 2005;25:274–278. doi: 10.1161/01.ATV.0000149143.04821.eb.
    1. Mosek A., Novak V., Opfer-Gehrking T.L., Swanson J.W., Low P.A. Autonomic dysfunction in migraineurs. Headache. 1999;39:108–117. doi: 10.1046/j.1526-4610.1999.3902108.x.
    1. Pourshoghi A., Danesh A., Tabby D.S., Grothusen J., Pourrezaei K. Cerebral reactivity in migraine patients measured with functional near-infrared spectroscopy. Eur. J. Med. Res. 2015;20:96. doi: 10.1186/s40001-015-0190-9.
    1. Hamel E. Serotonin and migraine: Biology and clinical implications. Cephalalgia. 2007;27:1293–1300. doi: 10.1111/j.1468-2982.2007.01476.x.
    1. Borkum J.M. The migraine attack as a homeostatic, neuroprotective response to brain oxidative stress: Preliminary evidence for a theory. Headache. 2018;58:118–135. doi: 10.1111/head.13214.
    1. Goadsby P.J. Pathophysiology of migraine. Ann. Indian Acad. Neurol. 2012;15:S15–S22. doi: 10.4103/0972-2327.99993.
    1. Shichiri M. The role of lipid peroxidation in neurological disorders. J. Clin. Biochem. Nutr. 2014;54:151–160. doi: 10.3164/jcbn.14-10.
    1. Yigit M., Sogut O., Tataroglu Ö., Yamanoglu A., Yigit E., Güler E.M., Ozer O.F., Kocyigit A. Oxidative/antioxidative status, lymphocyte DNA damage, and urotensin-2 receptor level in patients with migraine attacks. Neuropsychiatr. Dis. Treat. 2018;14:367–374. doi: 10.2147/NDT.S156710.
    1. Geyik S., Altunısık E., Neyal A.M., Taysi S. Oxidative stress and DNA damage in patients with migraine. J. Headache Pain. 2016;17:10. doi: 10.1186/s10194-016-0606-0.
    1. Guillaumet-Adkins A., Yañez Y., Peris-Diaz M.D., Calabria I., Palanca-Ballester C., Sandoval J. Epigenetics and oxidative stress in aging. Oxid. Med. Cell Longev. 2017;2017:9175806. doi: 10.1155/2017/9175806.
    1. Alp R., Selek S., Alp S.I., Taşkin A., Koçyiğit A. Oxidative and antioxidative balance in patients of migraine. Eur. Rev. Med. Pharmacol. Sci. 2010;14:877–882.
    1. Neyal M., Yimenicioglu F., Aydeniz A., Taskin A., Saglam S., Cekmen M., Neyal A., Gursoy S., Erel O., Balat A. Plasma nitrite levels, total antioxidant status, total oxidant status, and oxidative stress index in patients with tension-type headache and fibromyalgia. Clin. Neurol. Neurosurg. 2013;115:736–740. doi: 10.1016/j.clineuro.2012.08.028.
    1. Vurucu S., Karaoglu A., Paksu M.S., Yesilyurt O., Oz O., Unay B., Akin R. Relationship between oxidative stress and chronic daily headache in children. Hum. Exp. Toxicol. 2013;32:113–119. doi: 10.1177/0960327112459204.
    1. Neri M., Frustaci A., Milic M., Valdiglesias V., Fini M., Bonassi S., Barbanti P. A meta-analysis of biomarkers related to oxidative stress and nitric oxide pathway in migraine. Cephalalgia. 2015;35:931–937. doi: 10.1177/0333102414564888.
    1. Aytac B., Coskun O., Alioglu B., Durak Z.E., Büber S., Tapçi E., Ocal R., Inan L.E., Durak İ., Yoldaş T.K. Decreased antioxidant status in migraine patients with brain white matter hyperintensities. Neurol. Sci. 2014;35:1925–1929. doi: 10.1007/s10072-014-1864-8.
    1. Erol I., Alehan F., Aldemir D., Ersin Ogus Increased vulnerability to oxidative stress in pediatric migraine patients. Pediatr. Neurol. 2010;43:21–24. doi: 10.1016/j.pediatrneurol.2010.02.014.
    1. Martinez A., Proupim N., Sanchez M. Retinal nerve fiber layer thickness measurement using optical coherence tomography in migraine patients. Br. J. Ophthalmol. 2008;92:1069–1075. doi: 10.1136/bjo.2008.137471.
    1. Colak H.N., Kantarci F.A., Tatar M.G., Eryilmaz M., Uslu H., Goker H., Yildirim A., Gurler B. Retinal nerve fiber layer, ganglion cell complex, and choroidal thickness in migraine. Arq. Bras. Oftalmol. 2016;79:78–81. doi: 10.5935/0004-2749.20160024.
    1. Demircan S., Atas M., Arik Y.S., Ulusoy M.D., Yuvacı İ., Arifoğlu H.B., Başkan B., Zararsız G. The impact of migraine on posterior ocular structures. J. Ophthalmol. 2015;2015:868967. doi: 10.1155/2015/868967.
    1. Simsek I.B. Retinal nerve fiber layer thickness of migraine patients with or without white matter lesions. Neuroophthalmology. 2016;41:7–11. doi: 10.1080/01658107.2016.1243131.
    1. Abdellatif M.K., Fouad M.M. Effect of duration and severity of migraine on retinal nerve fiber layer, ganglion cell layer, and choroidal thickness. Eur. J. Ophthalmol. 2018;28:714–721. doi: 10.1177/1120672117750054.
    1. Tunç A., Güngen B.D., Evliyaoğlu F., Aras Y.G., Tekeşin A.K. Evaluation of retinal nerve fiber layer, ganglion cell layer and macular changes in patients with migraine. Acta Neurol. Belg. 2017;117:121–129. doi: 10.1007/s13760-016-0715-1.
    1. Gunes A., Karadag A.S., Yazgan S., Celik H.U., Simsek A. Evaluation of retinal nerve fiber 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. doi: 10.1111/cxo.12585.
    1. Karaca E.E., Koçer E.B., Özdek Ş., Akçam H.T., Ercan M.B. Choroidal thickness measurements in migraine patients during attack-free period. Neurol. Sci. 2016;37:81–88. doi: 10.1007/s10072-015-2364-1.

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