Skip to main content

Advertisement

SpringerLink
Log in

The association between retinal nerve fibre layer thickness and corpus callosum index in different clinical subtypes of multiple sclerosis

  • Original Article
  • Published:
Neurological Sciences Aims and scope Submit manuscript

Abstract

The objective of this paper is to evaluate the association between physical disability in multiple sclerosis (MS) patients, the thickness of the retinal nerve fibre layer (RNFL) and corpus callosum volumes, as expressed by the corpus callosum index (CCI). This study was based on a cohort of 212 MS patients and 52 healthy control subjects, who were age and gender matched. The MS patients included 144 women and 177 relapsing-remitting MS (RRMS) patients. Peripapillary and volumetric optical coherence tomography (OCT) scans of the macula were performed using spectral-domain OCT technology. All magnetic resonance imaging (MRI) scans were performed using 1.5-T systems. CCI and RNFL were lower in MS than healthy control subjects (0.341 versus 0.386, p < 0.01 and 92.1 versus 105.0, p < 0.01). In addition, CCI correlated with RNFL (r = 0.464, p < 0.01). This was also true for the subgroup of patients with no history of optic neuritis (ON). There is a correlation between the thickness of the RNFL and CCI values in MS patients with no history of ON, which suggests that OCT might be a suitable marker for neurodegeneration in MS clinical trials.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Friese MA, Montalban X, Willcox N, Bell JI, Martin R, Fugger L (2006) The value of animal models for drug development in multiple sclerosis. Brain 129:1940–1952

    Article  PubMed  Google Scholar 

  2. Manrique-Hoyos N, Jürgens T, Grønborg M, Kreutzfeldt M, Schedensack M, Kuhlmann T, Schrick C, Brück W, Urlaub H, Simons M, Merkler D (2012) Late motor decline after accomplished remyelination: impact for progressive multiple sclerosis. Ann Neurol 71:227–244

    Article  PubMed  Google Scholar 

  3. Huang D, Swanson EA, Lin CP, Schuman JS, Stinson WG, Chang W, Hee MR, Flotte T, Gregory K, Carmen AP, James GF (1991) Optical coherence tomography. Science 254:1178–1181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Gordon-Lipkin E, Chodkowski B, Reich DS, Smith SA, Pulicken M, Balcer LJ, Frohman EM, Cutter G, Calabresi PA (2007) Retinal nerve fiber layer is associated with brain atrophy in multiple sclerosis. Neurology 69:1603–1609

    Article  CAS  PubMed  Google Scholar 

  5. Grazioli E, Zivadinov R, Weinstock-Guttman B, Lincoff N, Baier M, Wong JR, Hussein S, Cox JL, Hojnacki D, Ramanathan M (2007) Retinal nerve fiber layer thickness is associated with brain MRI outcomes in multiple sclerosis. J Neurol Sci 268:12–17

    Article  PubMed  Google Scholar 

  6. Hines M, Chiu L, McAdams LA, Bentler PM, Lİpcamon J (1992) Cognition and the corpus callosum: verbal fluency, visuospatial ability, and language lateralization related to midsagittal surface areas of callosal subregions. Behav Neurosci 106:3–14

    Article  CAS  PubMed  Google Scholar 

  7. Pelletier J, Suchet L, Witjas T, Habib M, Guttmann CR, Salamon G, Lyon-Caen O, Chérif AA (2001) A longitudinal study of callosal atrophy and interhemispheric dysfunction in relapsing remitting multiple sclerosis. Arch Neurol 58:105–111

    Article  CAS  PubMed  Google Scholar 

  8. Barkhof FJ, Elton M, Lindeboom J, Tas MW, Schmidt WF, Hommes OR, Polman CH, Kok A, Valk J (1998) Functional correlates of callosal atrophy in relapsing-remitting multiple sclerosis patients. A preliminary MRI study. J Neurol 245:153–158

    Article  CAS  PubMed  Google Scholar 

  9. Figueira FF, Santos VS, Figueira GM, Silva AC (2007) Corpus callosum index: a practical method for long-term follow-up in multiple sclerosis. Arq Neuropsiquiatr 65:931–935

    Article  PubMed  Google Scholar 

  10. Yaldizli Ö, Atefy R, Gass A, Sturm D, Glassl S, Tettenborn B, Putzki NJ (2010) Corpus callosum index and long-term disability in multiple sclerosis patients. Neurol 257:1256–1264

    Article  Google Scholar 

  11. Frohman EM, Fujimoto JG, Frohman TC, Calabresi PA, Cutter G, Balcer LJ (2008) Optical coherence tomography: a window in to the mechanisms of multiple sclerosis. Nat Clin Pract Neurol 4:664–675

    Article  PubMed  PubMed Central  Google Scholar 

  12. Petzold A, De Boer JF, Schippling S, Vermersch P, Kardon R, Green A, Calabresi PA, Polman C (2010) Optical coherence tomography in multiple sclerosis: a systematic review and meta-analysis. Lancet Neurol 9:921–932

    Article  PubMed  Google Scholar 

  13. Polman CH, Reingold SC, Edan G, Filippi M, Hartung HP, Kappos L, Lublin FD, Metz LM, McFarland HF, O’Connor PW, Sandberg-Wollheim M, Thompson AJ, Weinshenker BG, Wolinsky JS (2005) Diagnostic criteria for multiple sclerosis: 2005 revisions to the “McDonald criteria”. Ann Neurol 58:840–846

    Article  PubMed  Google Scholar 

  14. Kurtzke JF (1983) Rating neurologic impairment in multiple sclerosis: an Expanded Disability Status Scale (EDSS). Neurology 33:1444–1452

    Article  CAS  PubMed  Google Scholar 

  15. Consortium of Multiple Sclerosis Centers (2003) Available at http://www.mscare.org/

  16. Pretegiani E, Rosini F, Dotti MT, Bianchi S, Federico A, Rufa A (2013) Visual system involvement in CADASIL. J Stroke Cerebrovasc Dis 22:1377–1384

    Article  PubMed  Google Scholar 

  17. La Morgia C, Ross-Cisneros FN, Koronyo Y, Hannibal J, Gallassi R, Cantalupo G, Sambati L, Pan BX, Tozer KR, Barboni P, Provini F, Avanzini P, Carbonelli M, Pelosi A, Chui H, Liquori R, Baruzzi A, Koronyo M, Sadun AA, Carelli V (2016) Melanopsin retinal ganglion cell loss in Alzheimer disease. Ann Neurol 79:90–109

    Article  CAS  PubMed  Google Scholar 

  18. Oktem EO, Derle E, Kibaroglu S, Oktem C, Akkoyun I, Can U (2015) The relationship between the degree of cognitive impairment and retinal nerve fiber layer thickness. Neurol Sci 36:1141–1146

    Article  PubMed  Google Scholar 

  19. Jimenez B, Ascaso FJ, Cristobal JA, Val JL (2014) Development of a prediction formula of Parkinson disease severity by optical coherence tomography. Mov Disord 29:68–74

    Article  PubMed  Google Scholar 

  20. Scheel M, Finke C, Oberwahrenbrock T, Freing A, Pech LM, Schlichting J, Sömmer C, Wuerfel J, Paul F, Brandt AU (2014) Retinal nerve fibre layer thickness correlates with brain white matter damage in multiple sclerosis: a combined optical coherence tomography and diffusion tensor imaging study. Mult Scler 20:1904–1907

    Article  PubMed  Google Scholar 

  21. Sullivan EV, Rohlfing T, Pfefferbaum A (2010) Longitudinal study of callosal microstructure in the normal adult aging brain using quantitative DTI fiber tracking. Dev Neuropsychol 35:233–256

    Article  PubMed  PubMed Central  Google Scholar 

  22. Granberg T, Martola J, Bergendal G, Shams S, Damangir S, Aspelin P, Fredrikson S, Kristoffersen-Wiberg M (2015) Corpus callosum atrophy is strongly associated with cognitive impairment in multiple sclerosis: results of a 17-year longitudinal study. Mult Scler 21:1151–1158

    Article  PubMed  Google Scholar 

  23. Caligiuri ME, Barone S, Cherubini A, Augimeri A, Chiriaco C, Trotta M, Granata A, Filippelli E, Perrotta P, Valentino P, Quattrone A (2014) The relationship between regional microstructural abnormalities of the corpus callosum and physical and cognitive disability in relapsing–remitting multiple sclerosis. Neuroimage Clin 7:28–33

    Article  PubMed  PubMed Central  Google Scholar 

  24. Young KL, Brandt AU, Petzold A, Reitz LY, Lintze F, Paul F, Martin R, Schippling S (2013) Loss of retinal nerve fibre layer axons indicates white but not grey matter damage in early multiple sclerosis. Eur J Neurol 20:803–811

    Article  CAS  PubMed  Google Scholar 

  25. Zivadinov R, Bergsland N, Cappellani R, Hagemeier J, Melia R, Carl E, Dwyer MG, Lincoff N, Weinstock-Guttman B, Ramanathan M (2014) Retinal nerve fiber layer thickness and thalamus pathology in multiple sclerosis patients. Eur J Neurol 21:1137–1144

    Article  CAS  PubMed  Google Scholar 

  26. Vogt J, Paul F, Aktas O, Müller-Wielsch K, Dörr J, Dörr S, Bharathi BS, Glumm R, Schmitz C, Steinbusch H, Raine CS, Tsokos M, Nitsch R, Zipp F (2009) Lower motor neuron loss in multiple sclerosis and experimental autoimmune encephalomyelitis. Ann Neurol 66:310–322

    Article  PubMed  Google Scholar 

  27. Oberwahrenbrock T, Ringelstein M, Jentschke S, Deuschle K, Klumbies K, Bellmann-Strobl J, Harmel J, Ruprecht K, Schippling S, Hartung HP, Aktas O, Brandt AU, Paul F (2013) Retinal ganglion cell and inner plexiform layer thinning in clinically isolated syndrome. Mult Scler 19:1887–1895

    Article  PubMed  Google Scholar 

  28. Lucchinetti CF, Popescu BF, Bunyan RF, Moll NM, Roemer SF, Lassmann H, Brück W, Parisi JE, Scheithauer BW, Giannini C, Weigand SD, Mandrekar J, Ransohoff RM (2011) Inflammatory cortical demyelination in early multiple sclerosis. N Engl J Med 365:2188–2197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Syc SB, Saidha S, Newsome SD, Ratchford JN, Levy M, Ford E, Crainiceanu CM, Durbin MK, Oakley JD, Meyer SA, Frohman EM, Calabresi PA (2012) Optical coherence tomographysegmentation reveals ganglion cell layer pathology after optic neuritis. Brain 135:521–533

    Article  PubMed  Google Scholar 

  30. Huang-Link YM, Al-Havasi A, Lindehammar H (2015) Acute optic neuritis: retinal ganglion cell loss precedes retinal nerve fiber thinning. Neurol Sci 36:617–620

    Article  PubMed  Google Scholar 

  31. Green AJ, McQuaid S, Hauser SL, Allen IV, Lyness R (2010) Ocular pathology in multiple sclerosis: retinal atrophy and inflammation irrespective of disease duration. Brain 133:1591–1601

    Article  PubMed  PubMed Central  Google Scholar 

  32. Kupersmith MJ, Gravin MK, Wang JK, Durbin M, Kardon R (2016) Retinal ganglion cell layer thinning within one month of presentation for optic neuritis. Mult Scler 22:641–648

    Article  PubMed  Google Scholar 

  33. Jehna M, Pirpamer L, Khalil M, Fuchs S, Ropele S, Langkammer C, Pichler A, Stulnig F, Deutschmann H, Fazekas F, Enzinger C (2015) Periventricular lesions correlate with cortical thinning in multiple sclerosis. Ann Neurol 78:530–539

    Article  PubMed  Google Scholar 

  34. Henderson AP, Trip SA, Schlottmann PG, Altmann DR, Garway-Heath DF, Plant GT, Miller DH (2008) An investigation of the retinal nerve fibre layer in progressive multiple sclerosis using optical coherence tomography. Brain 131:277–287

    PubMed  Google Scholar 

  35. Huang-Link YM, Fredrikson M, Link H (2015) Benign multiple sclerosis is associated with reduced thinning of the retinal nerve fibre and ganglion cell layers in non-optic-neuritis eyes. J Clin Neurol 11:241–224

    Article  PubMed  PubMed Central  Google Scholar 

  36. Klistorner A, Garrick R, Barnett MH, Graham SL, Arvind H, Sriram P, Yiannikas C (2012) Axonal loss in non-optic neuritis eyesof patients with multiple sclerosis linked to delayed visual evoked potential. Neurology 80:242–245

    Article  PubMed  Google Scholar 

  37. Sriram P, Wang C, Yiannikas C, Garrick R, Barnett M, Parratt J, Graham SL, Arvind H, Klistorner A (2014) Relationship between optical coherence tomography and electrophysiology of the visual pathway in non-optic neuritis eyes of multiple sclerosis patients. PLoS One 9(8):102546

    Article  Google Scholar 

  38. Balk L, Tewarie P, Killestein J, Polman C, Uitdehaag B, Petzold A (2014) Disease course heterogeneity and OCT in multiple sclerosis. Mult Scler 20:1198–1206

    Article  CAS  PubMed  Google Scholar 

  39. Gelfand JM, Goodin DS, Boscardin WJ, Nolan R, Cuneo A, Green AJ (2012) Retinal axonal loss begins early in the course of multiple sclerosis and is similar between progressive phenotypes. PLoS One 7:e36847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Costello F, Hodge W, Pan YI, Eggenberger E, Freedman MS (2010) Using retinal architecture to help characterize multiple sclerosis patients. Can J Ophthalmol 45:520–526

    Article  PubMed  Google Scholar 

  41. Costello F, Hodge W, Pan YI, Freedman M, DeMeulemeester C (2009) Differences in retinal nerve fiber layer atrophy between multiple sclerosis subtypes. J Neurol Sci 281:74–79

    Article  PubMed  Google Scholar 

  42. Saidha S, Calabresi AP (2014) Optical coherence tomography should be part of the routine monitoring of patients with multiple sclerosis: yes. Mult Scler 20(10):1296–1298

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank our patients and healthy volunteers.

Author information

Authors and Affiliations

  1. Faculty of Medicine Neurology Department, Yuzuncu Yil University, 65000, Kampus Van, Turkey

    Vedat Cilingir, Aysel Milanlioglu, Abdullah Yılgor & Temel Tombul

  2. Faculty of Medicine Ophthalmology Department, Yuzuncu Yil University, Van, Turkey

    Muhammed Batur & Tekin Yasar

  3. Faculty of Medicine Radiology Department, Yuzuncu Yil University, Van, Turkey

    Mehmet Deniz Bulut & Abdussamet Batur

Authors
  1. Vedat Cilingir
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Muhammed Batur
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mehmet Deniz Bulut
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Aysel Milanlioglu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Abdullah Yılgor
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Abdussamet Batur
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tekin Yasar
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Temel Tombul
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Vedat Cilingir.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Institute the study was conducted: Yuzuncu Yil University Faculty of Medicine Neurology Clinic

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cilingir, V., Batur, M., Bulut, M.D. et al. The association between retinal nerve fibre layer thickness and corpus callosum index in different clinical subtypes of multiple sclerosis. Neurol Sci 38, 1223–1232 (2017). https://doi.org/10.1007/s10072-017-2947-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10072-017-2947-0

Keywords

Search

Navigation