Optical Coherence Tomography Reveals Distinct Patterns of Retinal Damage in Neuromyelitis Optica and Multiple Sclerosis

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Schneider, Elisa ^a   Zimmermann, Hanna ^a   Oberwahrenbrock, Timm ^a   Kaufhold, Falko ^a   Kadas, Ella Maria ^a   Petzold, Axel ^b   Bilger, Frieder ^a   Borisow, Nadja ^a   Jarius, Sven ^c   Wildemann, Brigitte ^c   Ruprecht, Klemens ^a   Brandt, Alexander U ^a   Paul, Friedemann ^a,d  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGED; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DIFFERENTIAL DIAGNOSIS; DISEASE SEVERITY; FEMALE; HUMAN; MALE; MULTIPLE SCLEROSIS; MYELOOPTIC NEUROPATHY; RETINA BIPOLAR GANGLION CELL; RETINA GANGLION CELL; RETINA INJURY; RETINA MACULA EDEMA; RETINAL NERVE FIBER LAYER THICKNESS; SPECTRAL DOMAIN OPTICAL COHERENCE TOMOGRAPHY; VISUAL ACUITY; CASE CONTROL STUDY; COMPLICATION; DIAGNOSTIC IMAGING; MIDDLE AGED; MULTIPLE SCLEROSIS, RELAPSING-REMITTING; NEUROMYELITIS OPTICA; OPTIC NEURITIS; OPTICAL COHERENCE TOMOGRAPHY; PATHOPHYSIOLOGY; PHYSIOLOGY; RETINA; YOUNG ADULT;

ADULT; AGED; CASE-CONTROL STUDIES; FEMALE; HUMANS; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS, RELAPSING-REMITTING; NEUROMYELITIS OPTICA; OPTIC NEURITIS; RETINA; RETINAL GANGLION CELLS; TOMOGRAPHY, OPTICAL COHERENCE; VISUAL ACUITY; YOUNG ADULT;

EID: 84879256356     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066151     Document Type: Article

References (73)

1. Jarius S, Ruprecht K, Wildemann B, Kuempfel T, Ringelstein M, et al. (2012) Contrasting disease patterns in seropositive and seronegative neuromyelitis optica: A multicentre study of 175 patients. J Neuroinflammation 9: 14.
2. Wingerchuk DM, Hogancamp WF, O'Brien PC, Weinshenker BG, (1999) The clinical course of neuromyelitis optica (Devic's syndrome). Neurology 53: 1107-1114.
3. Lennon VA, Wingerchuk DM, Kryzer TJ, Pittock SJ, Lucchinetti CF, et al. (2004) A serum autoantibody marker of neuromyelitis optica: distinction from multiple sclerosis. Lancet 364: 2106-2112.
4. Lennon VA, Kryzer TJ, Pittock SJ, Verkman AS, Hinson SR, (2005) IgG marker of optic-spinal multiple sclerosis binds to the aquaporin-4 water channel. J Exp Med 202: 473-477.
5. Wingerchuk DM, Lennon VA, Lucchinetti CF, Pittock SJ, Weinshenker BG, (2007) The spectrum of neuromyelitis optica. Lancet Neurol 6: 805-815.
6. Lucchinetti CF, Mandler RN, McGavern D, Bruck W, Gleich G, et al. (2002) A role for humoral mechanisms in the pathogenesis of Devic's neuromyelitis optica. Brain 125: 1450-1461.
7. Jarius S, Paul F, Franciotta D, Waters P, Zipp F, et al. (2008) Mechanisms of disease: aquaporin-4 antibodies in neuromyelitis optica. Nat Clin Pract Neurol 4: 202-214.
8. Wingerchuk DM, Weinshenker BG, (2003) Neuromyelitis optica: clinical predictors of a relapsing course and survival. Neurology 60: 848-853.
9. Mealy MA, Wingerchuk DM, Greenberg BM, Levy M, (2012) Epidemiology of neuromyelitis optica in the United States: a multicenter analysis. Arch Neurol 69: 1176-1180.
10. Bock M, Brandt AU, Dorr J, Pfueller CF, Ohlraun S, et al. (2010) Time domain and spectral domain optical coherence tomography in multiple sclerosis: a comparative cross-sectional study. Multiple Sclerosis 16: 893-896.
11. Petzold A, de Boer JF, Schippling S, Vermersch P, Kardon R, et al. (2010) Optical coherence tomography in multiple sclerosis: a systematic review and meta-analysis. Lancet Neurol 9: 921-932.
12. Noval S, Contreras I, Muñoz S, Oreja-Guevara C, Manzano B, et al. (2011) Optical coherence tomography in multiple sclerosis and neuromyelitis optica: an update. Mult Scler Int 2011: 472790.
13. Costello F, (2011) Evaluating the use of optical coherence tomography in optic neuritis. Mult Scler Int 2011: 148394.
14. Oberwahrenbrock T, Schippling S, Ringelstein M, Kaufhold F, Zimmermann H, et al. (2012) Retinal Damage in Multiple Sclerosis Disease Subtypes Measured by High-Resolution Optical Coherence Tomography. Multiple Sclerosis International 2012: 1-10.
15. Pulicken M, Gordon-Lipkin E, Balcer LJ, Frohman EM, Cutter G, et al. (2007) Optical coherence tomography and disease subtype in multiple sclerosis. Neurology 69: 2085-2092.
16. Saidha S, Syc SB, Ibrahim MA, Eckstein C, Warner CV, et al. (2011) Primary retinal pathology in multiple sclerosis as detected by optical coherence tomography. Brain 134: 518-533.
17. Burkholder BM, Osborne B, Loguidice MJ, Bisker E, Frohman TC, et al. (2009) Macular volume determined by optical coherence tomography as a measure of neuronal loss in multiple sclerosis. Archives of Neurology 66: 1366-1372.
18. Sepulcre J, Murie-Fernandez M, Salinas-Alaman A, García-Layana A, Bejarano B, et al. (2007) Diagnostic accuracy of retinal abnormalities in predicting disease activity in MS. Neurology 68: 1488-1494.
19. Toledo J, Sepulcre J, Salinas-Alaman A, García-Layana A, Murie-Fernandez M, et al. (2008) Retinal nerve fiber layer atrophy is associated with physical and cognitive disability in multiple sclerosis. Mult Scler 14: 906-912.
20. Albrecht P, Ringelstein M, Müller AK, Keser N, Dietlein T, et al. (2012) Degeneration of retinal layers in multiple sclerosis subtypes quantified by optical coherence tomography. Mult Scler 18: 1422-1429.
21. Brandt AU, Oberwahrenbrock T, Ringelstein M, Young KL, Tiede M, et al. (2011) Primary retinal pathology in multiple sclerosis as detected by optical coherence tomography. Brain 134: e193; author reply e194.
22. Oberwahrenbrock T, Ringelstein M, Jentschke S, Deuschle K, Klumbies K, et al. (2013) Retinal ganglion cell and inner plexiform layer thinning in clinically isolated syndrome. Mult Scler: in press, doi:10.1177/1352458513489757.
23. Gordon-Lipkin E, Chodkowski B, Reich DS, Smith SA, Pulicken M, et al. (2007) Retinal nerve fiber layer is associated with brain atrophy in multiple sclerosis. Neurology 69: 1603-1609.
24. Siger M, Dziegielewski K, Jasek L, Bieniek M, Nicpan A, et al. (2008) Optical coherence tomography in multiple sclerosis: thickness of the retinal nerve fiber layer as a potential measure of axonal loss and brain atrophy. J Neurol 255: 1555-1560.
25. Dörr J, Wernecke KD, Bock M, Gaede G, Wuerfel JT, et al. (2011) Association of Retinal and Macular Damage with Brain Atrophy in Multiple Sclerosis. PLoS ONE 6: e18132.
26. Zimmermann H, Freing A, Kaufhold F, Gaede G, Bohn E, et al. (2012) Optic neuritis interferes with optical coherence tomography and magnetic resonance imaging correlations. Mult Scler 19: 443-450.
27. Saidha S, Sotirchos ES, Oh J, Syc SB, Seigo MA, et al. (2012) Relationships Between Retinal Axonal and Neuronal Measures and Global Central Nervous System Pathology in Multiple Sclerosis. Arch Neurol: 1-10.
28. Merle H, Olindo S, Donnio A, Richer R, Smadja D, et al. (2008) Retinal peripapillary nerve fiber layer thickness in neuromyelitis optica. Invest Ophthalmol Vis Sci 49: 4412-4417.
29. Naismith RT, Tutlam NT, Xu J, Klawiter EC, Shepherd J, et al. (2009) Optical coherence tomography differs in neuromyelitis optica compared with multiple sclerosis. Neurology 72: 1077-1082.
30. Ratchford JN, Quigg ME, Conger A, Frohman T, Frohman EM, et al. (2009) Optical coherence tomography helps differentiate neuromyelitis optica and MS optic neuropathies. Neurology 73: 302-308.
31. Green AJ, Cree BAC, (2009) Distinctive retinal nerve fibre layer and vascular changes in neuromyelitis optica following optic neuritis. J Neurol Neurosurg Psychiatr 80: 1002-1005.
32. Monteiro MLR, Fernandes DB, Apóstolos-Pereira SL, Callegaro D, (2012) Quantification of Retinal Neural Loss in Patients with Neuromyelitis Optica and Multiple Sclerosis with or without Optic Neuritis Using Fourier-Domain Optical Coherence Tomography. Invest Ophthalmol Vis Sci 53: 3959-3966.
33. De Seze J, Blanc F, Jeanjean L, Zéphir H, Labauge P, et al. (2008) Optical coherence tomography in neuromyelitis optica. Arch Neurol 65: 920-923.
34. Bouyon M, Collongues N, Zéphir H, Ballonzoli L, Jeanjean L, et al. (2013) Longitudinal follow-up of vision in a neuromyelitis optica cohort. Mult Scler, 2013. doi:10.1177/1352458513476562.
35. Wingerchuk DM, Pittock SJ, Lucchinetti CF, Lennon VA, Weinshenker BG, (2007) A secondary progressive clinical course is uncommon in neuromyelitis optica. Neurology 68: 603-605.
36. Syc SB, Saidha S, Newsome SD, Ratchford JN, Levy M, et al. (2012) Optical coherence tomography segmentation reveals ganglion cell layer pathology after optic neuritis. Brain 135: 521-533.
37. Fernandes DB, Raza AS, Nogueira RGF, Wang D, Callegaro D, et al. (2012) Evaluation of Inner Retinal Layers in Patients with Multiple Sclerosis or Neuromyelitis Optica Using Optical Coherence Tomography. Ophthalmology.
38. Gelfand JM CB (2013) MIcrocystic inner nuclear layer abnormalities and neuromyelitis optica. JAMA Neurol: 1-5.
39. Sotirchos ES, Saidha S, Byraiah G, Mealy MA, Ibrahim MA, et al. (2013) In vivo identification of morphologic retinal abnormalities in neuromyelitis optica. Neurology 80: 1406-1414.
40. Wingerchuk DM, Lennon VA, Pittock SJ, Lucchinetti CF, Weinshenker BG, (2006) Revised diagnostic criteria for neuromyelitis optica. Neurology 66: 1485-1489.
41. Paul F, Jarius S, Aktas O, Bluthner M, Bauer O, et al. (2007) Antibody to aquaporin 4 in the diagnosis of neuromyelitis optica. PLoS Med 4: e133.
42. Jarius S, Probst C, Borowski K, Franciotta D, Wildemann B, et al. (2010) Standardized method for the detection of antibodies to aquaporin-4 based on a highly sensitive immunofluorescence assay employing recombinant target antigen. J Neurol Sci 291: 52-56.
43. Kalluri SR, Illes Z, Srivastava R, Cree B, Menge T, et al. (2010) Quantification and functional characterization of antibodies to native aquaporin 4 in neuromyelitis optica. Arch Neurol 67: 1201-1208.
44. Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, et al. (2011) Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol 69: 292-302.
45. Tewarie P, Balk L, Costello F, Green A, Martin R, et al. (2012) The OSCAR-IB Consensus Criteria for Retinal OCT Quality Assessment. PLoS ONE 7: e34823.
46. Gelfand JM, Nolan R, Schwartz DM, Graves J, Green AJ, (2012) Microcystic macular oedema in multiple sclerosis is associated with disease severity. Brain 135: 1786-1793.
47. Bock M, Brandt AU, Kuchenbecker J, Dörr J, Pfueller CF, et al. (2012) 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 96: 62-67.
48. Frisén L, Hoyt WF, (1974) Insidious atrophy of retinal nerve fibers in multiple sclerosis. Funduscopic identification in patients with and without visual complaints. Arch Ophthalmol 92: 91-97.
49. Kerrison JB, Flynn T, Green WR, (1994) Retinal pathologic changes in multiple sclerosis. Retina 14: 445-451.
50. Bock M, Brandt AU, Dörr J, Kraft H, Weinges-Evers N, et al. (2010) Patterns of retinal nerve fiber layer loss in multiple sclerosis patients with or without optic neuritis and glaucoma patients. Clin Neurol Neurosurg 112: 647-652.
51. Costello F, Hodge W, Pan YI, Eggenberger E, Coupland S, et al. (2008) Tracking retinal nerve fiber layer loss after optic neuritis: a prospective study using optical coherence tomography. Multiple Sclerosis 14: 893-905.
52. Trip SA, Schlottmann PG, Jones SJ, Altmann DR, Garway-Heath DF, et al. (2005) Retinal nerve fiber layer axonal loss and visual dysfunction in optic neuritis. Ann Neurol 58: 383-391.
53. Mowry EM, Loguidice MJ, Daniels AB, Jacobs DA, Markowitz CE, et al. (2009) Vision related quality of life in multiple sclerosis: correlation with new measures of low and high contrast letter acuity. J Neurol Neurosurg Psychiatr 80: 767-772.
54. Walter SD, Ishikawa H, Galetta KM, Sakai RE, Feller DJ, et al. (2012) Ganglion cell loss in relation to visual disability in multiple sclerosis. Ophthalmology 119: 1250-1257.
55. Nakamura M, Nakazawa T, Doi H, Hariya T, Omodaka K, et al. (2010) Early high-dose intravenous methylprednisolone is effective in preserving retinal nerve fiber layer thickness in patients with neuromyelitis optica. Graefes Arch Clin Exp Ophthalmol 248: 1777-1785.
56. Sühs K-W, Hein K, Sättler MB, Görlitz A, Ciupka C, et al. (2012) A randomized, double-blind, phase 2 study of erythropoietin in optic neuritis. Ann Neurol 72: 199-210.
57. Sellner J, Boggild M, Clanet M, Hintzen RQ, Illes Z, et al. (2010) EFNS guidelines on diagnosis and management of neuromyelitis optica. Eur J Neurol 17: 1019-1032.
58. Stricker S, Oberwahrenbrock T, Zimmermann H, Schroeter J, Endres M, et al. (2011) Temporal Retinal Nerve Fiber Loss in Patients with Spinocerebellar Ataxia Type 1. PLoS ONE 6: e23024.
59. Van Horssen J, Witte ME, Ciccarelli O, (2012) The role of mitochondria in axonal degeneration and tissue repair in MS. Mult Scler 18: 1058-1067.
60. Evangelou N, Konz D, Esiri MM, Smith S, Palace J, et al. (2001) Size-selective neuronal changes in the anterior optic pathways suggest a differential susceptibility to injury in multiple sclerosis. Brain 124: 1813-1820.
61. Balk LJ, Killestein J, Polman CH, Uitdehaag BMJ, Petzold A, (2012) Microcystic macular oedema confirmed, but not specific for multiple sclerosis. Brain 135: e226-e226.
62. Abegg M, Zinkernagel M, Wolf S, (2012) Microcystic macular degeneration from optic neuropathy. Brain 135: e225-e225.
63. Li J, Patil RV, Verkman AS, (2002) Mildly abnormal retinal function in transgenic mice without Müller cell aquaporin-4 water channels. Invest Ophthalmol Vis Sci 43: 573-579.
64. Jarius S, Wildemann B, (2010) AQP4 antibodies in neuromyelitis optica: diagnostic and pathogenetic relevance. Nat Rev Neurol 6: 383-392.
65. Kleiter I, Hellwig K, Berthele A, Kümpfel T, Linker RA, et al. (2012) Failure of natalizumab to prevent relapses in neuromyelitis optica. Arch Neurol 69: 239-245.
66. Jacob A, Hutchinson M, Elsone L, Kelly S, Ali R, et al. (2012) Does natalizumab therapy worsen neuromyelitis optica? Neurology 79: 1065-1066.
67. Bomprezzi R, Powers JM, Shimizu J, Tsuji S, Weinshenker BG, et al. (2011) IFNβ-1b may severely exacerbate Japanese opticspinal MS in neuromyelitis optica spectrum: Japanese optic-spinal MS: is it MS or neuromyelitis optica and does the answer dictate treatment? Neurology 77: 195; discussion 195-196.
68. Barnett MH, Prineas JW, Buckland ME, Parratt JDE, Pollard JD, (2012) Massive astrocyte destruction in neuromyelitis optica despite natalizumab therapy. Mult Scler 18: 108-112.
69. Jarernsook B, Siritho S, Prayoonwiwat N (2012) Efficacy and safety of beta-interferon in Thai patients with demyelinating diseases. Mult Scler.
70. Kim S-H, Kim W, Li XF, Jung I-J, Kim HJ, (2012) Does interferon beta treatment exacerbate neuromyelitis optica spectrum disorder? Mult Scler 18: 1480-1483.
71. Papeix C, Vidal J-S, de Seze J, Pierrot-Deseilligny C, Tourbah A, et al. (2007) Immunosuppressive therapy is more effective than interferon in neuromyelitis optica. Mult Scler 13: 256-259.
72. Shimizu J, Hatanaka Y, Hasegawa M, Iwata A, Sugimoto I, et al. (2010) IFNβ-1b may severely exacerbate Japanese optic-spinal MS in neuromyelitis optica spectrum. Neurology 75: 1423-1427.
73. Min J-H, Kim BJ, Lee KH, (2012) Development of extensive brain lesions following fingolimod (FTY720) treatment in a patient with neuromyelitis optica spectrum disorder. Mult Scler 18: 113-115.