Semin Neurol 2019; 39(06): 711-717
DOI: 10.1055/s-0039-1700528
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Optical Coherence Tomography in Multiple Sclerosis

Jennifer S. Graves
1   Department of Neurosciences, University of California, San Diego, California
› Author Affiliations
Further Information

Publication History

Publication Date:
17 December 2019 (online)

Abstract

Optical coherence tomography (OCT) grew out of a convergence of rapid advancements in femtoseconds optics research and fiber optic commercial technology. The basic concept of OCT is to “see” into tissues using light echoes, analogous to the sound echoes of ultrasonography. Multiple A-scans are assembled into a B-scan two-dimensional image of the tissue of interest. Retina is an ideal tissue for evaluation by OCT, since the eye is designed to minimize light scattering through the anterior chamber and vitreous. OCT has had a significant impact on the field of multiple sclerosis, where it has allowed direct imaging of the myelin-free segments of axons and cell bodies of retinal ganglion cells. Together with precise functional measurements of the afferent visual system, the addition of robust structural measurements of retinal injury has allowed for an unprecedented ability to correlate clinical effects with the degree of neuronal loss. In addition, OCT has proven helpful to distinguish different forms of demyelinating disease, such as multiple sclerosis (MS) and neuromyelitis optica, and has provided ideal outcome measures in remyelination and neuroprotection trials.

 
  • References

  • 1 Fujimoto J, Swanson E. The development, commercialization, and impact of optical coherence tomography. Invest Ophthalmol Vis Sci 2016; 57 (09) OCT1-OCT13
  • 2 Duguay MA, Mattick AT. Ultrahigh speed photography of picosecond light pulses and echoes. Appl Opt 1971; 10 (09) 2162-2170
  • 3 Fujimoto JG, De Silvestri S, Ippen EP, Puliafito CA, Margolis R, Oseroff A. Femtosecond optical ranging in biological systems. Opt Lett 1986; 11 (03) 150
  • 4 Huang D, Wang J, Lin CP, Puliafito CA, Fujimoto JG. Micron-resolution ranging of cornea anterior chamber by optical reflectometry. Lasers Surg Med 1991; 11 (05) 419-425
  • 5 Huang D, Swanson EA, Lin CP. , et al. Optical coherence tomography. Science 1991; 254 (5035): 1178-1181
  • 6 Swanson EA, Izatt JA, Hee MR. , et al. In vivo retinal imaging by optical coherence tomography. Opt Lett 1993; 18 (21) 1864-1866
  • 7 Pieroth L, Schuman JS, Hertzmark E. , et al. Evaluation of focal defects of the nerve fiber layer using optical coherence tomography. Ophthalmology 1999; 106 (03) 570-579
  • 8 Mistlberger A, Liebmann JM, Greenfield DS. , et al. Heidelberg retina tomography and optical coherence tomography in normal, ocular-hypertensive, and glaucomatous eyes. Ophthalmology 1999; 106 (10) 2027-2032
  • 9 Parisi V, Manni G, Spadaro M. , et al. Correlation between morphological and functional retinal impairment in multiple sclerosis patients. Invest Ophthalmol Vis Sci 1999; 40 (11) 2520-2527
  • 10 Sormani MP, Pardini M. Assessing Repair in Multiple Sclerosis: Outcomes for Phase II Clinical Trials. Neurotherapeutics 2017; 14 (04) 924-933
  • 11 Fox RJ, Coffey CS, Cudkowicz ME. , et al. Design, rationale, and baseline characteristics of the randomized double-blind phase II clinical trial of ibudilast in progressive multiple sclerosis. Contemp Clin Trials 2016; 50: 166-177
  • 12 Lambe J, Murphy OC, Saidha S. Can optical coherence tomography be used to guide treatment decisions in adult or pediatric multiple sclerosis?. Curr Treat Options Neurol 2018; 20 (04) 9
  • 13 Oertel FC, Zimmermann HG, Brandt AU, Paul F. Novel uses of retinal imaging with optical coherence tomography in multiple sclerosis. Expert Rev Neurother 2019; 19 (01) 31-43
  • 14 Fisher JB, Jacobs DA, Markowitz CE. , et al. Relation of visual function to retinal nerve fiber layer thickness in multiple sclerosis. Ophthalmology 2006; 113 (02) 324-332
  • 15 Noval S, Contreras I, Rebolleda G, Muñoz-Negrete FJ. Optical coherence tomography versus automated perimetry for follow-up of optic neuritis. Acta Ophthalmol Scand 2006; 84 (06) 790-794
  • 16 Talman LS, Bisker ER, Sackel DJ. , et al. Longitudinal study of vision and retinal nerve fiber layer thickness in multiple sclerosis. Ann Neurol 2010; 67 (06) 749-760
  • 17 Costello F, Coupland S, Hodge W. , et al. Quantifying axonal loss after optic neuritis with optical coherence tomography. Ann Neurol 2006; 59 (06) 963-969
  • 18 Trip SA, Schlottmann PG, Jones SJ. , et al. Optic nerve atrophy and retinal nerve fibre layer thinning following optic neuritis: evidence that axonal loss is a substrate of MRI-detected atrophy. Neuroimage 2006; 31 (01) 286-293
  • 19 Bertuzzi F, Suzani M, Tagliabue E. , et al. Diagnostic validity of optic disc and retinal nerve fiber layer evaluations in detecting structural changes after optic neuritis. Ophthalmology 2010; 117 (06) 1256-1264.e1
  • 20 Pro MJ, Pons ME, Liebmann JM. , et al. Imaging of the optic disc and retinal nerve fiber layer in acute optic neuritis. J Neurol Sci 2006; 250 (1-2): 114-119
  • 21 Schneider E, Zimmermann H, Oberwahrenbrock T. , et al. Optical coherence tomography reveals distinct patterns of retinal damage in neuromyelitis optica and multiple sclerosis. PLoS One 2013; 8 (06) e66151
  • 22 Burton JM, Eliasziw M, Trufyn J, Tung C, Carter G, Costello F. A prospective cohort study of vitamin D in optic neuritis recovery. Mult Scler 2017; 23 (01) 82-93
  • 23 Kallenbach K, Frederiksen J. Optical coherence tomography in optic neuritis and multiple sclerosis: a review. Eur J Neurol 2007; 14 (08) 841-849
  • 24 Gordon-Lipkin E, Chodkowski B, Reich DS. , et al. Retinal nerve fiber layer is associated with brain atrophy in multiple sclerosis. Neurology 2007; 69 (16) 1603-1609
  • 25 Shen T, You Y, Arunachalam S. , et al. Differing structural and functional patterns of optic nerve damage in multiple sclerosis and neuromyelitis optica spectrum disorder. Ophthalmology 2019; 126 (03) 445-453
  • 26 Balk LJ, Steenwijk MD, Tewarie P. , et al. Bidirectional trans-synaptic axonal degeneration in the visual pathway in multiple sclerosis. J Neurol Neurosurg Psychiatry 2015; 86 (04) 419-424
  • 27 Gabilondo I, Martínez-Lapiscina EH, Martínez-Heras E. , et al. Trans-synaptic axonal degeneration in the visual pathway in multiple sclerosis. Ann Neurol 2014; 75 (01) 98-107
  • 28 Patel NB, Lim M, Gajjar A, Evans KB, Harwerth RS. Age-associated changes in the retinal nerve fiber layer and optic nerve head. Invest Ophthalmol Vis Sci 2014; 55 (08) 5134-5143
  • 29 Maghzi AH, Graves J, Revirajan N. , et al. Retinal axonal loss in very early stages of multiple sclerosis. Eur J Neurol 2015; 22 (07) 1138-1141
  • 30 Galetta KM, Graves J, Talman LS. , et al. Visual pathway axonal loss in benign multiple sclerosis: a longitudinal study. J Neuroophthalmol 2012; 32 (02) 116-123
  • 31 Saidha S, Syc SB, Ibrahim MA. , et al. Primary retinal pathology in multiple sclerosis as detected by optical coherence tomography. Brain 2011; 134 (Pt 2): 518-533
  • 32 Graves JS, Chohan H, Cedars B. , et al. Sex differences and subclinical retinal injury in pediatric-onset MS. Mult Scler 2017; 23 (03) 447-455
  • 33 Winges KM, Werner JS, Harvey DJ. , et al. Baseline retinal nerve fiber layer thickness and macular volume quantified by OCT in the North American phase 3 fingolimod trial for relapsing-remitting multiple sclerosis. J Neuroophthalmol 2013; 33 (04) 322-329
  • 34 Brandt AU, Oberwahrenbrock T, Ringelstein M. , et al. Primary retinal pathology in multiple sclerosis as detected by optical coherence tomography. Brain 2011; 134 (Pt 11): e193 , author reply e194
  • 35 Bock M, Brandt AU, Kuchenbecker J. , et al. Impairment of contrast visual acuity as a functional correlate of retinal nerve fibre layer thinning and total macular volume reduction in multiple sclerosis. Br J Ophthalmol 2012; 96 (01) 62-67
  • 36 Rothman A, Murphy OC, Fitzgerald KC. , et al. Retinal measurements predict 10-year disability in multiple sclerosis. Ann Clin Transl Neurol 2019; 6 (02) 222-232
  • 37 Davies EC, Galetta KM, Sackel DJ. , et al. Retinal ganglion cell layer volumetric assessment by spectral-domain optical coherence tomography in multiple sclerosis: application of a high-precision manual estimation technique. J Neuroophthalmol 2011; 31 (03) 260-264
  • 38 Petzold A, Balcer LJ, Calabresi PA. , et al; ERN-EYE IMSVISUAL. Retinal layer segmentation in multiple sclerosis: a systematic review and meta-analysis. Lancet Neurol 2017; 16 (10) 797-812
  • 39 He Y, Carass A, Solomon SD, Saidha S, Calabresi PA, Prince JL. Retinal layer parcellation of optical coherence tomography images: Data resource for multiple sclerosis and healthy controls. Data Brief 2018; 22: 601-604
  • 40 Oberwahrenbrock T, Traber GL, Lukas S. , et al. Multicenter reliability of semiautomatic retinal layer segmentation using OCT. Neurol Neuroimmunol Neuroinflamm 2018; 5 (03) e449
  • 41 Syc SB, Saidha S, Newsome SD. , et al. Optical coherence tomography segmentation reveals ganglion cell layer pathology after optic neuritis. Brain 2012; 135 (Pt 2): 521-533
  • 42 Green AJ, McQuaid S, Hauser SL, Allen IV, Lyness R. Ocular pathology in multiple sclerosis: retinal atrophy and inflammation irrespective of disease duration. Brain 2010; 133 (Pt 6): 1591-1601
  • 43 Graham EC, You Y, Yiannikas C. , et al. Progressive loss of retinal ganglion cells and axons in nonoptic neuritis eyes in multiple sclerosis: a longitudinal optical coherence tomography study. Invest Ophthalmol Vis Sci 2016; 57 (04) 2311-2317
  • 44 Huang-Link YM, Al-Hawasi A, Lindehammar H. Acute optic neuritis: retinal ganglion cell loss precedes retinal nerve fiber thinning. Neurol Sci 2015; 36 (04) 617-620
  • 45 Saidha S, Syc SB, Durbin MK. , et al. Visual dysfunction in multiple sclerosis correlates better with optical coherence tomography derived estimates of macular ganglion cell layer thickness than peripapillary retinal nerve fiber layer thickness. Mult Scler 2011; 17 (12) 1449-1463
  • 46 Nguyen J, Rothman A, Gonzalez N. , et al. Macular ganglion cell and inner plexiform layer thickness is more strongly associated with visual function in multiple sclerosis than bruch membrane opening-minimum rim width or peripapillary retinal nerve fiber layer thicknesses. J Neuroophthalmol 2019
  • 47 Saidha S, Sotirchos ES, Oh J. , et al. Relationships between retinal axonal and neuronal measures and global central nervous system pathology in multiple sclerosis. JAMA Neurol 2013; 70 (01) 34-43
  • 48 Button J, Al-Louzi O, Lang A. , et al. Disease-modifying therapies modulate retinal atrophy in multiple sclerosis: a retrospective study. Neurology 2017; 88 (06) 525-532
  • 49 Gelfand JM, Nolan R, Schwartz DM, Graves J, Green AJ. Microcystic macular oedema in multiple sclerosis is associated with disease severity. Brain 2012; 135 (Pt 6): 1786-1793
  • 50 Saidha S, Sotirchos ES, Ibrahim MA. , et al. Microcystic macular oedema, thickness of the inner nuclear layer of the retina, and disease characteristics in multiple sclerosis: a retrospective study. Lancet Neurol 2012; 11 (11) 963-972
  • 51 Kessel L, Hamann S, Wegener M, Tong J, Fraser CL. Microcystic macular oedema in optic neuropathy: case series and literature review. Clin Exp Ophthalmol 2018; 46 (09) 1075-1086
  • 52 Abegg M, Dysli M, Wolf S, Kowal J, Dufour P, Zinkernagel M. Microcystic macular edema: retrograde maculopathy caused by optic neuropathy. Ophthalmology 2014; 121 (01) 142-149
  • 53 Albrecht P, Ringelstein M, Müller AK. , et al. Degeneration of retinal layers in multiple sclerosis subtypes quantified by optical coherence tomography. Mult Scler 2012; 18 (10) 1422-1429
  • 54 Dietrich M, Helling N, Hilla A. , et al. Early alpha-lipoic acid therapy protects from degeneration of the inner retinal layers and vision loss in an experimental autoimmune encephalomyelitis-optic neuritis model. J Neuroinflammation 2018; 15 (01) 71
  • 55 Nolan R, Gelfand JM, Green AJ. Fingolimod treatment in multiple sclerosis leads to increased macular volume. Neurology 2013; 80 (02) 139-144
  • 56 Nolan RC, Liu M, Akhand O. , et al. Optimal inter-eye difference thresholds by OCT in MS: an international study. Ann Neurol 2019; 85 (05) 618-629
  • 57 Bennett JL, de Seze J, Lana-Peixoto M. , et al; GJCF-ICC&BR. Neuromyelitis optica and multiple sclerosis: Seeing differences through optical coherence tomography. Mult Scler 2015; 21 (06) 678-688
  • 58 Ratchford JN, Quigg ME, Conger A. , et al. Optical coherence tomography helps differentiate neuromyelitis optica and MS optic neuropathies. Neurology 2009; 73 (04) 302-308
  • 59 Graves JS. Can Visual Testing Be Used to Distinguish Neuromyelitis Optica and Multiple Sclerosis?. Ophthalmology 2019; 126 (03) 454-455
  • 60 Oertel FC, Kuchling J, Zimmermann H. , et al. Microstructural visual system changes in AQP4-antibody-seropositive NMOSD. Neurol Neuroimmunol Neuroinflamm 2017; 4 (03) e334
  • 61 You Y, Zhu L, Zhang T. , et al. Evidence of Müller glial dysfunction in patients with aquaporin-4 immunoglobulin G-positive neuromyelitis optica spectrum disorder. Ophthalmology 2019; 126 (06) 801-810
  • 62 Yeh EA, Marrie RA, Reginald YA. , et al; Canadian Pediatric Demyelinating Disease Network. Functional-structural correlations in the afferent visual pathway in pediatric demyelination. Neurology 2014; 83 (23) 2147-2152
  • 63 Waldman AT, Hiremath G, Avery RA. , et al. Monocular and binocular low-contrast visual acuity and optical coherence tomography in pediatric multiple sclerosis. Mult Scler Relat Disord 2013; 3 (03) 326-334
  • 64 Caldito NG, Saidha S, Sotirchos ES. , et al. Brain and retinal atrophy in African-Americans versus Caucasian-Americans with multiple sclerosis: a longitudinal study. Brain 2018; 141 (11) 3115-3129
  • 65 Rosso M, Kimbrough DJ, Gonzalez CT. , et al. Cross-sectional study of smoking exposure: no differential effect on OCT metrics in a cohort of MS patients. Mult Scler J Exp Transl Clin 2019; 5 (01) 2055217319828400
  • 66 Warner CV, Syc SB, Stankiewicz AM. , et al. The impact of utilizing different optical coherence tomography devices for clinical purposes and in multiple sclerosis trials. PLoS One 2011; 6 (08) e22947
  • 67 Sühs KW, Hein K, Sättler MB. , et al. A randomized, double-blind, phase 2 study of erythropoietin in optic neuritis. Ann Neurol 2012; 72 (02) 199-210
  • 68 Raftopoulos R, Hickman SJ, Toosy A. , et al. Phenytoin for neuroprotection in patients with acute optic neuritis: a randomised, placebo-controlled, phase 2 trial. Lancet Neurol 2016; 15 (03) 259-269