Investigation of the Retinal Nerve Fiber Layer in Multiple Sclerosis Using Spectral Domain Optical Coherence Tomography
Authors:
M. Michalec 1; P. Praksová 2; M. Hladíková 2; V. Matušková 1; E. Vlková 1; P. Štourač 2; L. Michalcová 1
Authors place of work:
LF MU a FN Brno
Oční klinika
1; LF MU a FN Brno
Neurologická klinika
2
Published in the journal:
Cesk Slov Neurol N 2016; 79/112(1): 41-50
Category:
Original Paper
Summary
Background:
Optic neuritis (ON) is an inflammatory optic nerve disease that is strongly associated with multiple sclerosis (MS). Axonal damage in the optic nerve is manifested as retinal nerve fiber layer (RNFL) deficits that can be detected by the optical coherence tomography (OCT).
Aim:
To characterize the inner retinal layer changes in patients with clinically isolated syndrome (CIS) and MS while utilizing the spectral domain OCT (SD-OCT) and a comparative sample of healthy controls.
Participants and methods:
30 eyes of 15 patients with CIS, 104 eyes of 52 MS patients with or without history of ON and 30 eyes of healthy patients that underwent SD-OCT examination. Results: CIS ON eyes had lower mean RNFL thickness (92.1 µm; p = 0.007) compared to the comparative sample (100.8 µm). The mean RNFL thickness decrease (97.5 µm; p = 0.25) was not detected in the eyes unaffected by CIS ON. Reduction of the mean RNFL thickness was not found in the post-ON eyes compared to unaffected eyes of CIS patients (p = 0.14). Eyes of MS patients with a history of ON showed significantly reduced mean RNFL thickness (73.1µm; p < 0.001) compared to the comparative sample (100.8 µm). Patients with MS with no history of ON also had lower mean RNFL thickness (91.4µm; p = 0.002). Statistically significant RNFL thinning was detected in the ON eyes compared to unaffected eyes (p = 0.04).
Conclusions:
SD-OCT is a promising tool designed to detect subclinical changes in RNFL thickness in patients with MS.
Key words:
multiple sclerosis – optic neuritis – clinically isolated syndrome – optical coherence tomography – retinal nerve fiber layer
The authors declare they have no potential conflicts of interest concerning drugs, products, or services used in the study.
The Editorial Board declares that the manuscript met the ICMJE “uniform requirements” for biomedical papers.
Zdroje
1. Shams PN, Plant GT. Optic neuritis: a review. Int MS J 2009; 16(3): 82– 89.
2. Rizzo JF, Lessell S. Risk of developing multiple sclerosis after uncomplicated optic neuritis: a long-term prospective study. Neurology 1988; 38(2): 185– 190.
3. Optic Neuritis Study Group. Multiple sclerosis risk after optic neuritis: final optic neuritis treatment trial follow--up. Arch Neurol 2008; 65(6): 727– 732. doi: 10.1001/ archneur.65.6.727.
4. Volpe N. The optic neuritis treatment trial. A definitive answer and profound impact with unexpected results. Arch Ophthalmol 2008; 126(7): 996– 999. doi: 10.1001/ archopht.126.7.996.
5. Sadun AA. Optic atrophy and papilledema. In: Albert DM, Jakobiec FA (eds). Principle and practice of ophthalmology. 2nd ed. Philadelphia: WB Saunders 2000: 4108– 4116.
6. Noval S, Contreras I, Munoz S, Oreja-Guevara C, Manzano B, Rebolleda G. Optical coherence tomography in multiples sclerosis and neuromyelitis optica: an update. Mult Scler Int 2011; 2011: 472790. doi: 10.1155/ 2011/ 472790.
7. Kusuhara S, Nakamura M, Nagai-Kusuhara A, Nakanishi Y, Kanamori A, Negi A. Macular thickness reduction in eyes with unilateral optic atrophy detected with optical coherence tomography. Eye (Lond) 2006; 20(8): 882– 887.
8. Alasil T, Wang K, Keane PA, Lee H, Baniasadi N, de Boer JF et al. Analysis of normal retinal nerve fiber layer thickness by age, sex, and race using spectral domain optical coherence tomography. J Glaucoma 2013; 22(7): 532– 541. doi: 10.1097/ IJG.0b013e318255bb4a.
9. Mohammad Salih PA. Evaluation of peripapillary retinal nerve fiber layer thickness in myopic eyes by spectral-domain optical coherence tomography. J Glaucoma 2012; 21(1): 41– 44. doi: 10.1097/ IJG.0b013e3181fc8053.
10. Rauscher FM, Sekhon N, Feuer WJ, Budenz DL. Myopia affects retinal nerve fiber layer measurements as determined by optical coherence tomography. J Glaucoma 2009; 18(7): 501– 505. doi: 10.1097/ IJG.0b013e318193c2be.
11. Leung CK, Cheung CY, Weinreb RN, Qiu K, Liu S, Li H et al. Evaluation of retinal nerve fiber layer progression in glaucoma: a study on optical coherence tomography guided progression analysis. Invest Ophthalmol Vis Sci 2010; 51(1): 217– 222. doi: 10.1167/ iovs.09-3468.
12. Kirbas S, Turkyilmaz K, Tufekci A, Durmus M. Retinal nerve fiber layer thickness in Parkinson disease. J Neuroophthalmol 2013; 33(1): 62– 65. doi: 10.1097/ WNO.0b013e3182701745.
13. Altintas O, Iseri P, Ozkan B, Caglar Y. Correlation between retinal morphological and functional findings and clinical severity in Parkinson’s disease. Doc Ophthalmol 2008; 116(2): 137– 146.
14. Frohman EM, Fujimoto JG, Frohman TC, Calabresi PA, Cutter G, Balcer LJ. Optical coherence tomography: a window into the mechanisms of multiple sclerosis. Nat Clin Pract Neurol 2008; 49(12): 664– 675. doi: 10.1038/ ncpneuro0950.
15. Kirbas S, Turkyilmaz K, Anlar O, Tufekci A, Durmus M. Retinal nerve fiber layer thickness in patients with Alzheimer’s disease. J Neuroophthalmol 2013; 33(1): 58– 61. doi: 10.1097/ WNO.0b013e318267fd5f.
16. Berisha F, Feke GT, Trempe CL, McMeel JW, Schepens CL. Retinal abnormalities in early Alzheimer‘s dis ease. Invest Ophthalmol Vis Sci 2007; 48(5): 2285– 2289. doi: 10.1167/ iovs.06-1029.
17. Parisi V, Restuccia R, Fattapposta F, Mina C, Bucci MG, Pierelli F. Morphological and functional retinal impairment in Alzheimer‘s disease patients. Clin Neurophysiol 2001; 112(10): 1860– 1867.
18. Petzold A, de Boer JF, Schippling S, Vermersch P, Kardon R, Green A et al. Optical coherence tomography in multiple sclerosis: a systematic review and meta-analysis. Lancet Neurol 2010; 9(9): 921– 932. doi: 10.1016/ S1474-4422(10)70168-X.
19. Newman N, Hoyt W. Ophthalmologic observation of retinal nerve fiber layer damage. West J Med 1975; 122(3): 238– 239.
20. Syc SB, Warner CV, Hiremath GS, Farrell SK, Ratchford JN, Conger A et al. Reproducibility of high-resolution optical coherence tomographx in multiple slerosis. Mult Scler 2010; 16(7): 829– 839. doi: 10.1177/ 1352458510371640.
21. Matušková V, Lízrová Preiningerová J, Vysloužilová D, Michalec M, Kasl Z, Vlková E. Použití optické koherenční tomografie u roztroušené sklerózy. Cesk Slov Neurol N 2016; 79/ 112(1): 33–40.
22. Henderson AP, Trip SA, Schlottmann PG, Altmann DR, Garway-Heath DF, Plant GT et al. An investigation of the retinal nerve fiber layer in progressive multiple sclerosis using optical coherence tomography. Brain 2008; 131(1): 277– 287.
23. Levkovitch-Verbin H, Quigley HA, Kerrigan-Baumrind LA, Danna S, Kerrigan D, Pease ME. Optic nerve transection in monkeys may result in secondary degeneration of retinal ganglion cells. Invest Ophthalmol Vis Sci 2001; 42(5): 975– 982.
24. Shindler KS, Ventura E, Dutt M, Rostami A. Inflammatory demyelination induces axonal injury and retinal ganglion apoptosis in experimental optic neuritis. Exp Eye Res 2008; 87(3): 208– 213. doi: 10.1016/ j.exer.2008.05.017.
25. Kaufman D, Celesia GG. Simultaneous recording of pattern electroretinogram and visual evoked responses in neuro-ophthalmic disorders. Neurology 1985; 35(5): 644– 651.
26. Green AJ, McQuaid S, Haser SL, Allen IV, Lynnes R. Ocular pathology in multiple sclerosis: retinal atrophy and inflammation irrespective of disease duration. Brain 2010; 133(6): 1591– 1601. doi: 10.1093/ brain/ awq080.
27. Costello F, Coupland S, Hodge W, Lorello GR, Koroluk J, Pan YI et al. Quantifying axonal loss after optic neuritis with optical coherence tomography. Ann Neurol 2006; 59(6): 963– 969.
28. Trip SA, Schlottmann PG, Jones SJ, Altmann DR, Garway-Heath DF, Thompson AJ et al. Retinal nerve fiber layer axonal loss and visual dysfunction in optic neuritis. Ann Neurol 2005; 58(3): 383– 391.
29. Pulicken M, Gordon-Lipkin E, Balcer LJ, Frohman E, Cutter G, Calabresi PA. Optical coherence tomography and disease subtype in multiple sclerosis. Neurology 2007; 69(22): 2085– 2092. doi: 10.1212/ 01.wnl.0000294876.49861.dc.
30. Kim JS, Ishikawa H, Sung KR, Xu J, Wollstein G, Bilonic RA et al. Retinal nerve fiber layer thickness measurement reproducibility improved with spectral domain optical coherence tomography. Br J Ophthalmol 2009; 93(8): 1057– 1063. doi: 10.1136/ bjo.2009.157875.
31. Parisi V, Mannini G, Spadaro M, Colacino G, Restuc-cia R, Marchi S et al. Correlation between morphological and functional retinal impairment in multiple sclerosis patients. Invest Ophthalmol Vis Sci 1999; 40(11): 2520– 2527.
32. Costello F. Evaluating the use of optical coherence tomography in optic neuritis. Mult Scler Int 2011; 2011: 148394. doi: 10.1155/ 2011/ 148394.
33. Charcot JM. Histologie de la sclérose en plaques. Gaz Hop (Paris) 1868; 41: 554– 555, 557– 558, 566.
34. Friesen L, Hoyt WF. Insidious atrophy of retinal nerve fibers in multiple sclerosis. Funduscopic identification in patients with and without visual complaints. Arch Ophthalmol 1974; 92(2): 91– 97.
35. Elbol P, Work K. Retinal nerve fibre layer in multiple sclerosis. Acta Ophthalmol 1990; 68(4): 481– 486.
36. Oreja-Guevara C, Noval S, Manzano B, Diez-Tejedor E. Optic neuritis, multiple sclerosis-related or not: structural and functional study. Neurologia 2010; 25(2): 78– 82.
37. Hickman SJ, Dalton CM, Miller DH, Plant GT. Management of acute optic neuritis. Lancet 2002; 360(9349): 1953– 1962.
38. Beck RW, Trobe JD, Moke PS, Gal RL, Xing D, Bhatti MT et al. High- and low-risk profiles for the development of multiple sclerosis within 10 years after optic neuritis: experience of the optic neuritis treatment trial. Arch Ophthalmol 2003; 121(7): 944– 949.
39. Beck RW, Moke PS, Trobe JD. The 5-year risk of MS after optic neuritis. Neurology 1998; 51(4): 1237– 1238.
40. Bertuzzi F, Suzani M, Tagliabue E, Cavaletti G, Angeli R, Balgera R et al. Diagnostic validity of optic disc and retinal nerves fibre layer evaluations in detecting structural changes after optic neuritis, Ophthalmology 2010; 117(6): 1256– 1264. doi: 10.1016/ j.ophtha.2010.02.024.
41. Costello F, Hodge W, Pan YI, Eggenberger E, Coupland S, Kardon RH. Tracking retinal nerve fiber layer loss after optic neuritis: a prospective study using optical coherence tomography. Mult Scler 2008; 14(7): 893– 905. doi: 10.1177/ 1352458508091367.
42. Klistorner A, Arvind H, Nguyen T, Garrick R, Paine M, Graham S et al. Axonal loss and myelin in early ON loss in postacute optic neuritis. Ann Neurol 2008; 64(3): 325– 331. doi: 10.1002/ ana.21474.
43. Yau GS, Lee JW, Lau PP, Tam VT, Wong WW, Yuen CY. Longitudinal changes in retinal nerve fibre layer thickness after an isolated unilateral retrobulbar optic neuritis: 1-year results. Neuroophthalmology 2015; 39(1): 22– 25. doi: 10.3109/ 01658107.2014.984230.
44. Halliday AM, McDonald WI, Mushin J. Visual- evoked response in diagnosis of multiple sclerosis. Br Med J 1973; 4(5893): 661– 664.
45. Kerrison JB, Flynn T, Green WR. Retinal changes in multiple sclerosis. Retina 1994; 14(5): 445– 451.
46. Fisher JB, Jacobs DA, Markowitz CE, Galetta SL, Volpe NJ, Nano-Schiavi ML et al. Relation of visual function to retinal nerve fiber layer thickness in multiple sclerosis. Ophthalmology 2006; 113(2): 324– 332.
47. Outteryck O, Zephyr H, Defoort S, Bouyon M, Debruyne P, Bouacha I et al. Optical coherence tomography in clinically isolated syndrome: no evidence of subclinical retinal axonal loss. Arch Neurol 2009; 66(11): 1373– 1377. doi: 10.1001/ archneurol.2009.265.
48. Gundogan FC, Demirkaya S, Sobaci G. Is optical coherence tomography really a new biomarker candidate in multiple sclerosis? A structural and functional evaluation. Invest Ophthalmol Vis Sci 2007; 48(12): 5773– 5781. doi: 10.1167/ iovs.07-0834.
49. Khanifar AA, Parlitsis GJ, Ehrlich JR, Aaker GD, D‘Amico DJ, Gauthier AS et al. Retinal nerve fiber layer evaluation in multiple sclerosis with spectral domain optical coherence tomography. Clin Ophthalmol 2010; 4: 1007– 1013.
50. Costello F, Hodge W, Pan YI, Eggenberger E, Freedman MS. Using retinal architecture to help characterize multiple sclerosis patients. Can J Ophthalmol 2010; 45(5): 520– 526. doi: 10.3129/ i10-063.
51. Burkholder BM, Osborne B, Loguidice MJ, Bisker E, Frohman TC, Conger A et al. Macular volume determined by optical coherence tomography as a measure of neuronal loss in multiple sclerosis. Arch Neurol 2009; 66(11): 1366– 1372. doi: 10.1001/ archneurol.2009.230.
52. Talman LS, Bisker ER, Sackel DJ, Long DA jr, Galetta KM, Ratchford JN et al. Longitudinal study of vision and retinal nerve fiber layer thickness in multiple sclerosis. Ann Neurol 2010; 67(6): 749– 760. doi: 10.1002/ ana.22005.
53. Pueyo V, Martin J, Fernandez J, Almarcegui C, Ara J, Egea C et al. Axonal loss in the retinal nerve fiber layer in patients with multiple sclerosis. Mult Scler 2008; 14(5): 609– 614. doi: 10.1177/ 1352458507087326.
54. Frohman E, Costello F, Zivadinov R, Stuve O,Conger A, Winslow H. Optical coherence tomography in multiple sclerosis. Lancet Neurol 2006; 5(10): 853– 863.
55. Knight OJ, Chang RT, Feuer WJ, Budenz DL. Comparison of retinal nerve fiber layer measurements using time domain and spectral domain optical coherent tomography. Ophthalmology 2009; 116(7): 1271– 1277. doi: 10.1016/ j.ophtha.2008.12.032.
56. Giani A, Cigada M, Choudhry N, Deiro AP, Oldani M, Pellegrini M et al. Reproducibility of retinal thickness measurements on normal and pathologic eyes by different optical coherence tomography instruments. Am J Ophthalmol 2010; 150(6): 815– 824. doi: 10.1016/ j.ajo.2010.06.025.
57. Bock M, Brandt AU, Dörr J, Pfueller CF, Ohlraun S, Zipp F et al. Time domain and spectral domain optical coherence tomography in multiple sclerosis: a comparative cross-sectional study. Mult Scler 2010; 16(7): 893– 896. doi: 10.1177/ 1352458510365156.
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