Skip to main content

Advertisement

Log in

Migraine causes retinal and choroidal structural changes: evaluation with ocular coherence tomography

  • Original Communication
  • Published:
Journal of Neurology Aims and scope Submit manuscript

Abstract

Few studies have evaluated whether the retina is involved in migraine through the evaluation of retinal nerve fiber layer (RNFL) examined with ocular coherence tomography (OCT) with conflicting results. Aim of this case–control study is to evaluate the retina and the choroid in migraine. Patients having migraine with aura (MwA) or without aura (MoA) and chronic migraine (CM) were evaluated. Age- and sex-matched normal subjects were selected as healthy controls (HC). Patients and HC were examined with OCT. RNFL, ganglion cell layer (GCL), foveal thickness (FT), choroidal thickness (CT) and total macular volume (TMV) were calculated for right eyes (RE) and left eyes (LE). Seventy-seven patients (62 women; 80.5%), 21 MoA, 12 MwA, 44 CM and 42 HC were enrolled in the study. Patients compared to HC had a significant reduction of RNFL (RE: 91.2 ± 9.2 vs 99.3 ± 7.5 μm; p < 0.001. LE: 93.3 ± 8.7 vs 100.2 ± 6.5 μm; p < 0.001). GCL (RE: 80.6 ± 6.4 vs 86.9 ± 2.1 μm; p < 0.0001. LE: 81.5 ± 5.7 vs 87.1 ± 2.6 μm; p < 0.0001) and CT (RE: 286.4 ± 31.4 vs 333.2 ± 3.1 μm; p < 0.0001. LE: 287.2 ± 31.6 vs 334.5 ± 4.1 μm; p < 0.0001) were thinner in patients compared to HC. Moreover, CM showed reduction of RNFL and of GCL compared to the other migraineurs. Finally, we found a significant inverse correlation between RNFL thickness and total number of headache attacks per months. Our data suggest the involvement of retina and choroid in migraineurs, especially in the CM group. Although migraine is an episodic and recurrent disease, its chronic nature might cause permanent structural abnormalities involving not only the brain, but also the retina.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Headache Classification Committee of the International Headache S (2013) The international classification of headache disorders, 3rd edition (beta version). Ceph Int J Headache 33(9):629–808. doi:10.1177/0333102413485658

    Article  Google Scholar 

  2. Schwedt TJ (2014) Chronic migraine. BMJ 348:g1416. doi:10.1136/bmj.g1416

    Article  PubMed  Google Scholar 

  3. Russo A, Tessitore A, Tedeschi G (2013) Migraine and trigeminal system-I can feel it coming. Curr Pain Headache Rep 17(10):367. doi:10.1007/s11916-013-0367-2

    Article  PubMed  Google Scholar 

  4. Aguggia M, Saracco MG, Cavallini M, Bussone G, Cortelli P (2013) Sensitization and pain. Neurol Sci Off J Ital Neurol Soc Ital Soc Clin Neurophysiol 34(Suppl 1):S37–S40. doi:10.1007/s10072-013-1382-0

    Google Scholar 

  5. Friedman DI (2015) The eye and headache. Continuum 21(4 Headache):1109–1117. doi:10.1212/CON.0000000000000204

  6. Flammer J, Pache M, Resink T (2001) Vasospasm, its role in the pathogenesis of diseases with particular reference to the eye. Prog Retinal Eye Res 20(3):319–349

    Article  CAS  Google Scholar 

  7. Killer HE, Forrer A, Flammer J (2003) Retinal vasospasm during an attack of migraine. Retina 23(2):253–254

    Article  PubMed  Google Scholar 

  8. Banik S, Bhutto HU, Bagga P (2006) Recurrent branch retinal vein occlusion with factor V leiden mutation. Eye (Lond) 20(8):948–949. doi:10.1038/sj.eye.6702060

    Article  CAS  Google Scholar 

  9. Wang JJ, Mitchell P, Smith W (1997) Is there an association between migraine headache and open-angle glaucoma? Findings from the Blue Mountains Eye Study. Ophthalmology 104(10):1714–1719

    Article  CAS  PubMed  Google Scholar 

  10. Drexler W, Sattmann H, Hermann B, Ko TH, Stur M, Unterhuber A, Scholda C, Findl O, Wirtitsch M, Fujimoto JG, Fercher AF (2003) Enhanced visualization of macular pathology with the use of ultrahigh-resolution optical coherence tomography. Arch Ophthalmol 121(5):695–706. doi:10.1001/archopht.121.5.695

    Article  PubMed  Google Scholar 

  11. Fercher AF (2010) Optical coherence tomography—development, principles, applications. Z Med Phys 20(4):251–276. doi:10.1016/j.zemedi.2009.11.002

    Article  PubMed  Google Scholar 

  12. Wang J, Gao X, Huang W, Wang W, Chen S, Du S, Li X, Zhang X (2015) Swept-source optical coherence tomography imaging of macular retinal and choroidal structures in healthy eyes. BMC Ophthalmol 15(1):122. doi:10.1186/s12886-015-0110-3

    Article  PubMed  PubMed Central  Google Scholar 

  13. Tewarie P, Balk L, Costello F, Green A, Martin R, Schippling S, Petzold A (2012) The OSCAR-IB consensus criteria for retinal OCT quality assessment. PLoS One 7(4):e34823. doi:10.1371/journal.pone.0034823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Schippling S, Balk LJ, Costello F, Albrecht P, Balcer L, Calabresi PA, Frederiksen J, Frohman E, Green AJ, Klistorner A, Outteryck O, Paul F, Plant GT, Traber G, Vermersch P, Villoslada P, Wolf S, Petzold A (2015) Quality control for retinal OCT in multiple sclerosis: validation of the OSCAR-IB criteria. Mult Scler J 21(2):163–170. doi:10.1177/1352458514538110

    Article  CAS  Google Scholar 

  15. Cruz-Herranz A, Balk LJ, Oberwahrenbrock T, Saidha S, Martinez-Lapiscina EH, Lagreze WA, Schuman JS, Villoslada P, Calabresi P, Balcer L, Petzold A, Green AJ, Paul F, Brandt AU, Albrecht P, consortium I (2016) The APOSTEL recommendations for reporting quantitative optical coherence tomography studies. Neurology 86(24):2303–2309. doi:10.1212/WNL.0000000000002774

    Article  PubMed  PubMed Central  Google Scholar 

  16. Zeger SL, Liang KY (1986) Longitudinal data analysis for discrete and continuous outcomes. Biometrics 42(1):121–130

    Article  CAS  PubMed  Google Scholar 

  17. Boston RC, Sumner AE (2003) STATA: a statistical analysis system for examining biomedical data. Adv Exp Med Biol 537:353–369

    Article  PubMed  Google Scholar 

  18. Ekinci M, Ceylan E, Cagatay HH, Keles S, Huseyinoglu N, Tanyildiz B, Cakici O, Kartal B (2014) Retinal nerve fibre layer, ganglion cell layer and choroid thinning in migraine with aura. BMC Ophthalmol 14:75. doi:10.1186/1471-2415-14-75

    Article  PubMed  PubMed Central  Google Scholar 

  19. Tan FU, Akarsu C, Gullu R (2005) Retinal nerve fiber layer thickness is unaffected in migraine patients. Acta Neurol Scand 112(1):19–23. doi:10.1111/j.1600-0404.2005.00423.x

    Article  CAS  PubMed  Google Scholar 

  20. Feng YF, Guo H, Huang JH, Yu JG, Yuan F (2015) Retinal nerve fiber layer thickness changes in migraine: a meta-analysis of case–control studies. Curr Eye Res 41(6):814–822. doi: 10.3109/02713683.2015.1056373

    Article  PubMed  Google Scholar 

  21. Martinez A, Proupim N, Sanchez M (2009) Scanning laser polarimetry with variable corneal compensation in migraine patients. Acta Ophthalmol 87(7):746–753. doi:10.1111/j.1755-3768.2008.01356.x

    Article  PubMed  Google Scholar 

  22. Martinez A, Proupim N, Sanchez M (2008) Retinal nerve fibre layer thickness measurements using optical coherence tomography in migraine patients. Br J Ophthalmol 92(8):1069–1075. doi:10.1136/bjo.2008.137471

    Article  CAS  PubMed  Google Scholar 

  23. Gipponi S, Scaroni N, Venturelli E, Forbice E, Rao R, Liberini P, Padovani A, Semeraro F (2013) Reduction in retinal nerve fiber layer thickness in migraine patients. Neurol Sci 34(6):841–845. doi:10.1007/s10072-012-1103-0

    Article  PubMed  Google Scholar 

  24. Kirbas S, Tufekci A, Turkyilmaz K, Kirbas A, Oner V, Durmus M (2013) Evaluation of the retinal changes in patients with chronic migraine. Acta Neurol Belg 113(2):167–172. doi:10.1007/s13760-012-0150-x

    Article  PubMed  Google Scholar 

  25. Yulek F, Dirik EB, Eren Y, Simavli H, Ugurlu N, Cagil N, Simsek S (2015) Macula and retinal nerve fiber layer in migraine patients: analysis by spectral domain optic coherence tomography. Semin Ophthalmol 30(2):124–128. doi:10.3109/08820538.2013.833270

    Article  PubMed  Google Scholar 

  26. Demircan S, Atas M, Arik Yuksel S, Ulusoy MD, Yuvaci I, Arifoglu HB, Baskan B, Zararsiz G (2015) The impact of migraine on posterior ocular structures. J Ophthalmol 2015:868967. doi:10.1155/2015/868967

    PubMed  PubMed Central  Google Scholar 

  27. Huseyinoglu N, Ekinci M, Ozben S, Buyukuysal C, Kale MY, Sanivar HS (2014) Optic disc and retinal nerve fiber layer parameters as indicators of neurodegenerative brain changes in patients with obstructive sleep apnea syndrome. Sleep Breath 18(1):95–102. doi:10.1007/s11325-013-0854-z

    Article  PubMed  Google Scholar 

  28. Kruit MC, van Buchem MA, Hofman PA, Bakkers JT, Terwindt GM, Ferrari MD, Launer LJ (2004) Migraine as a risk factor for subclinical brain lesions. JAMA 291(4):427–434. doi:10.1001/jama.291.4.427

    Article  CAS  PubMed  Google Scholar 

  29. Hougaard A, Amin FM, Ashina M (2014) Migraine and structural abnormalities in the brain. Curr Opin Neurol 27(3):309–314. doi:10.1097/WCO.0000000000000086

    Article  PubMed  Google Scholar 

  30. Bashir A, Lipton RB, Ashina S, Ashina M (2013) Migraine and structural changes in the brain: a systematic review and meta-analysis. Neurology 81(14):1260–1268. doi:10.1212/WNL.0b013e3182a6cb32

    Article  PubMed  PubMed Central  Google Scholar 

  31. Sacco S, Pistoia F, Degan D, Carolei A (2015) Conventional vascular risk factors: their role in the association between migraine and cardiovascular diseases. Ceph Int J Headache 35(2):146–164. doi:10.1177/0333102414559551

    Article  Google Scholar 

  32. Kruit MC, van Buchem MA, Launer LJ, Terwindt GM, Ferrari MD (2010) Migraine is associated with an increased risk of deep white matter lesions, subclinical posterior circulation infarcts and brain iron accumulation: the population-based MRI CAMERA study. Ceph Int J Headache 30(2):129–136. doi:10.1111/j.1468-2982.2009.01904.x

    CAS  Google Scholar 

  33. Speciali JG, Bigal ME (2006) Subcortical lesions in migraine: are they related to mitochondrial dysfunction? Headache 46(9):1461–1462. doi:10.1111/j.1526-4610.2006.00591_1.x

    Article  PubMed  Google Scholar 

  34. Le Pira F, Reggio E, Quattrocchi G, Sanfilippo C, Maci T, Cavallaro T, Zappia M (2014) Executive dysfunctions in migraine with and without aura: what is the role of white matter lesions? Headache 54(1):125–130. doi:10.1111/head.12158

    Article  PubMed  Google Scholar 

  35. Hessler H, Zimmermann H, Oberwahrenbrock T, Kadas EM, Mikolajczak J, Brandt AU, Kauert A, Paul F, Schreiber SJ (2015) No evidence for retinal damage evolving from reduced retinal blood flow in carotid artery disease. Biomed Res Int. Artn 604028. doi:10.1155/2015/604028

  36. Biagi C, Poluzzi E, Roberto G, Puccini A, Vaccheri A, D’Alessandro R, Motola D, Montanaro N (2011) Pattern of triptan use and cardiovascular coprescription: a pharmacoepidemiological study in Italy. Eur J Clin Pharmacol 67(12):1283–1289. doi:10.1007/s00228-011-1076-6

    Article  CAS  PubMed  Google Scholar 

  37. Ewering C, Hasal N, Alten F, Clemens CR, Eter N, Oberwahrenbrock T, Kadas EM, Zimmermann H, Brandt AU, Osada N, Paul F, Marziniak M (2015) Temporal retinal nerve fibre layer thinning in cluster headache patients detected by optical coherence tomography. Cephalalgia 35(11):946–958. doi:10.1177/0333102414560632

    Article  PubMed  Google Scholar 

  38. Abdul-Rahman AM, Gilhotra JS, Selva D (2011) Dynamic focal retinal arteriolar vasospasm in migraine. Indian J Ophthalmol 59(1):51–53

    Article  PubMed  PubMed Central  Google Scholar 

  39. Beversdorf D, Stommel E, Allen C, Stevens R, Lessell S (1997) Recurrent branch retinal infarcts in association with migraine. Headache 37(6):396–399

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mario Zappia.

Ethics declarations

Conflicts of interest

The authors declare no financial or other conflict of interests.

Ethical standard

The study was approved by the institutional review board of the University of Catania, Italy and was performed in accordance with the ethical standards of the 1964 Declaration of Helsinki and its later amendments.

Informed consent

Previous written informed consent was obtained from each patient.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Reggio, E., Chisari, C.G., Ferrigno, G. et al. Migraine causes retinal and choroidal structural changes: evaluation with ocular coherence tomography. J Neurol 264, 494–502 (2017). https://doi.org/10.1007/s00415-016-8364-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00415-016-8364-0

Keywords

Navigation