CoChat
Sign Up
Cited by 585Multiple Sclerosis Research StudiesGlaucoma and retinal disordersRetinal Imaging and Analysis

Retinal layer segmentation in multiple sclerosis: a systematic review and meta-analysis

Open access
Petzold, Axel, Balcer, Laura J, Calabresi, Peter A, Costello, Fiona, Frohman, Teresa C, Frohman, Elliot M, Martinez-Lapiscina, Elena H, Green, Ari J +88 more·2017·The Lancet Neurology
DOI 10.1016/s1474-4422(17)30278-8
Open this paper in CoChat — free accountOpen PDF

Abstract

Background Structural retinal imaging biomarkers are important for early recognition and monitoring of inflammation and neurodegeneration in multiple sclerosis. With the introduction of spectral domain optical coherence tomography (SD-OCT), supervised automated segmentation of individual retinal layers is possible. We aimed to investigate which retinal layers show atrophy associated with neurodegeneration in multiple sclerosis when measured with SD-OCT. Methods In this systematic review and meta-analysis, we searched for studies in which SD-OCT was used to look at the retina in people with multiple sclerosis with or without optic neuritis in PubMed, Web of Science, and Google Scholar between Nov 22, 1991, and April 19, 2016. Data were taken from cross-sectional cohorts and from one timepoint from longitudinal studies (at least 3 months after onset in studies of optic neuritis). We classified data on eyes into healthy controls, multiple-sclerosis-associated optic neuritis (MSON), and multiple sclerosis without optic neuritis (MSNON). We assessed thickness of the retinal layers and we rated individual layer segmentation performance by random effects meta-analysis for MSON eyes versus control eyes, MSNON eyes versus control eyes, and MSNON eyes versus MSON eyes. We excluded relevant sources of bias by funnel plots. Findings Of 25 497 records identified, 110 articles were eligible and 40 reported data (in total 5776 eyes from patients with multiple sclerosis [1667 MSON eyes and 4109 MSNON eyes] and 1697 eyes from healthy controls) that met published OCT quality control criteria and were suitable for meta-analysis. Compared with control eyes, the peripapillary retinal nerve fibre layer (RNFL) showed thinning in MSON eyes (mean difference -20·10 μm, 95% CI -22·76 to -17·44; p<0·0001) and in MSNON eyes (-7·41 μm, -8·98 to -5·83; p<0·0001). The macula showed RNFL thinning of -6·18 μm (-8·07 to -4·28; p<0·0001) in MSON eyes and -2·15 μm (-3·15 to -1·15; p<0·0001) in MSNON eyes compared with control eyes. Atrophy of the macular ganglion cell layer and inner plexiform layer (GCIPL) was -16·42 μm (-19·23 to -13·60; p<0·0001) for MSON eyes and -6·31 μm (-7·75 to -4·87; p<0·0001) for MSNON eyes compared with control eyes. A small degree of inner nuclear layer (INL) thickening occurred in MSON eyes compared with control eyes (0·77 μm, 0·25 to 1·28; p=0·003). We found no statistical difference in the thickness of the combined outer nuclear layer and outer plexiform layer when we compared MSNON or MSON eyes with control eyes, but we found a small degree of thickening of the combined layer when we compared MSON eyes with MSNON eyes (1·21 μm, 0·24 to 2·19; p=0·01). Interpretation The largest and most robust differences between the eyes of people with multiple sclerosis and control eyes were found in the peripapillary RNFL and macular GCIPL. Inflammatory disease activity might be captured by the INL. Because of the consistency, robustness, and large effect size, we recommend inclusion of the peripapillary RNFL and macular GCIPL for diagnosis, monitoring, and research. Funding None.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/s1474-4422(17)30278-8

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 83

  1. Huang, D, Swanson, E, Lin, C, et al. "Optical coherence tomography." Science 1991;254:1178-1181.
  2. Liu, YZ, South, F A, Xu, Y, Carney, P S, and Boppart, S A. "Compu- tational optical coherence tomography [Invited]". Biomedical Optics Express 2017;8:1549-1574.
  3. Petzold, A, Boer, J F de, Schippling, S, et al. "Optical coherence to- mography in multiple sclerosis: a systematic review and meta-analysis." Lancet Neurol 2010;9:921-932.
  4. Balcer, L J, Miller, D H, Reingold, S C, and Cohen, J A. "Vision and vision-related outcome measures in multiple sclerosis". Brain 2014;138:11- 27.
  5. Gabilondo, I, Martnez-Lapiscina, E H, Martnez-Heras, E, et al. "Trans- synaptic axonal degeneration in the visual pathway in multiple sclero- sis." Ann Neurol 2014;75:98-107.
  6. Oberwahrenbrock, T, Ringelstein, M, Jentschke, S, et al. "Retinal gan- glion cell and inner plexiform layer thinning in clinically isolated syn- drome." Mult Scler 2013;19:1887-1895.
  7. Costello, F. "The afferent visual pathway: designing a structural-functional paradigm of multiple sclerosis." ISRN Neurol 2013;2013:134858.
  8. Graham, S L and Klistorner, A. "Afferent visual pathways in multiple sclerosis: a review." Clin Experiment Ophthalmol 2017;45:62-72.
  9. Cruz-Herranz, A, Balk, L J, Oberwahrenbrock, T, et al. "The APOS- TEL recommendations for reporting quantitative optical coherence to- mography studies." Neurology 2016;86:2303-2309.
  10. Petzold, A, Wattjes, M P, Costello, F, et al. "The investigation of acute optic neuritis: a review and proposed protocol." Nat Rev Neurol 2014;10:447- 458.
  11. Voss, E, Raab, P, Trebst, C, and Stangel, M. "Clinical approach to optic neuritis: pitfalls, red flags and differential diagnosis." Ther Adv Neurol Disord 2011;4:123-134.
  12. Beck, R. "The clinical profile of optic neuritis-experience of the optic neuritis treatment trial". Archives of Ophthalmology 1991;109:1673- 1678.
  13. Costello, F, Pan, Y I, Yeh, E A, Hodge, W, Burton, J M, and Kardon, R. "The temporal evolution of structural and functional measures after acute optic neuritis". Journal of Neurology, Neurosurgery & Psychiatry 2015:1369-1373.
  14. Lublin, F D, Reingold, S C, Cohen, J A, et al. "Defining the clinical course of multiple sclerosis: The 2013 revisions." Neurology 2014;83:278- 286.
  15. Tewarie, P, Balk, L, Costello, F, Green, A, Martin, R, Schippling, S, and Petzold, A. "The OSCAR-IB Consensus Criteria for Retinal OCT Quality Assessment." PLoS One 2012;7:e34823.
  16. Schippling, S, Balk, L, Costello, F, et al. "Quality control for retinal OCT in multiple sclerosis: validation of the OSCAR-IB criteria." Mult Scler 2015;21:163-170.
  17. Kiernan, D F, Mieler, W F, and Hariprasad, S M. "Spectral-domain op- tical coherence tomography: a comparison of modern high-resolution retinal imaging systems." Am J Ophthalmol 2010;149:18-31.
  18. Al-Louzi, O A, Bhargava, P, Newsome, S D, et al. "Outer retinal changes following acute optic neuritis." Mult Scler 2016;22:362-372.
  19. Balk, L J, Twisk, J W R, Steenwijk, M D, et al. "A dam for retrograde axonal degeneration in multiple sclerosis?" J Neurol Neurosurg Psy- chiatry 2014;85:782-789.
  20. Behbehani, R, Al-Hassan, A A, Al-Khars, A, Sriraman, D, and Al- roughani, R. "Retinal nerve fiber layer thickness and neurologic dis- ability in relapsing-remitting multiple sclerosis." J Neurol Sci 2015;359:305- 308. 44
  21. Behbehani, R, Al-Moosa, A, Sriraman, D, and Alroughani, R. "Gan- glion cell analysis in acute optic neuritis." Mult Scler Relat Disord 2016;5:66-69.
  22. Chilinska, A, Ejma, M, Turno-Krecicka, A, Guranski, K, and Misiuk- Hojlo, M. "Analysis of retinal nerve fibre layer, visual evoked potentials and relative afferent pupillary defect in multiple sclerosis patients." Clin Neurophysiol 2016;127:821-826.
  23. Esen, E, Sizmaz, S, Balal, M, Yar, K, Demirkiran, M, Unal, I, and Demircan, N. "Evaluation of the Innermost Retinal Layers and Visual Evoked Potentials in Patients with Multiple Sclerosis." Curr Eye Res 2016;41:1353-1358.
  24. Feng, L, Shen, J, Jin, X, Li, J, and Li, Y. "The evaluation of the reti- nal nerve fiber layer in multiple sclerosis with special-domain optical coherence tomography." Ophthalmologica 2013;230:116-120.
  25. Fernandes, D B, Raza, A S, Nogueira, R G F, Wang, D, Callegaro, D, Hood, D C, and Monteiro, M L R. "Evaluation of inner retinal layers in patients with multiple sclerosis or neuromyelitis optica using optical coherence tomography." Ophthalmology 2013;120:387-394.
  26. Fjeldstad, C, Bemben, M, and Pardo, G. "Reduced retinal nerve fiber layer and macular thickness in patients with multiple sclerosis with no history of optic neuritis identified by the use of spectral domain high- definition optical coherence tomography." J Clin Neurosci 2011;18:1469- 1472.
  27. Garcia-Martin, E, Pablo, L E, Herrero, R, et al. "Neural networks to identify multiple sclerosis with optical coherence tomography." Acta ophthalmologica 8 2013;91:e628-e634.
  28. Gonz ález-L ópez, J J, Rebolleda, G, Leal, M, Oblanca, N, Mu ñoz- Negrete, F J, Costa-Frossard, L, and Álvarez-Cerme ño, J C. "Com- parative diagnostic accuracy of ganglion cell-inner plexiform and reti- nal nerve fiber layer thickness measures by Cirrus and Spectralis op- tical coherence tomography in relapsing-remitting multiple sclerosis". BioMed research international 2014;2014:128517.
  29. Hadhoum, N, Hodel, J, Defoort-Dhellemmes, S, et al. "Length of optic nerve double inversion recovery hypersignal is associated with retinal axonal loss." Mult Scler 2015;22:649-658.
  30. Hokazono, K, Raza, A S, Oyamada, M K, Hood, D C, and Monteiro, M L. "Pattern electroretinogram in neuromyelitis optica and multiple sclerosis with or without optic neuritis and its correlation with FD-OCT and perimetry". Documenta Ophthalmologica 2013;127:201-215.
  31. Huang-Link, YM, Fredrikson, M, and Link, H. "Benign Multiple Scle- rosis is Associated with Reduced Thinning of the Retinal Nerve Fiber and Ganglion Cell Layers in Non-Optic-Neuritis Eyes." J Clin Neurol 2015;11:241-247.
  32. Kaushik, M, Wang, C Y, Barnett, M H, et al. "Inner nuclear layer thick- ening is inversley proportional to retinal ganglion cell loss in optic neu- ritis." PLoS One 2013;8:e78341.
  33. Khanifar, A A, Parlitsis, G J, Ehrlich, J R, Aaker, G D, D'Amico, D J, Gauthier, S A, and Kiss, S. "Retinal nerve fiber layer evaluation in mul- tiple sclerosis with spectral domain optical coherence tomography." Clin Ophthalmol 2010;4:1007-1013.
  34. Klistorner, A, Sriram, P, Vootakuru, N, et al. "Axonal loss of retinal neurons in multiple sclerosis associated with optic radiation lesions." Neurology 24 2014;82:2165-2172.
  35. Knier, B, Berthele, A, Buck, D, et al. "Optical coherence tomography indicates disease activity prior to clinical onset of central nervous sys- tem demyelination." Mult Scler 2016;22:893-900.
  36. Lange, A P, Zhu, F, Sayao, AL, et al. "Retinal nerve fiber layer thick- ness in benign multiple sclerosis." Mult Scler 2013;19:1275-1281.
  37. Oberwahrenbrock, T, Schippling, S, Ringelstein, M, et al. "Retinal damage in multiple sclerosis disease subtypes measured by high- resolution optical coherence tomography." Mult Scler Int 2012;2012:530305.
  38. Park, KA, Kim, J, and Oh, S Y. "Analysis of spectral domain optical coherence tomography measurements in optic neuritis: differences in neuromyelitis optica, multiple sclerosis, isolated optic neuritis and normal healthy controls." Acta Ophthalmol 2014;92:e57-e65.
  39. Petracca, M, Cordano, C, Cellerino, M, et al. "Retinal degeneration in primary-progressive multiple sclerosis: A role for cortical lesions?" Mult Scler 2016;23:43-50.
  40. Rebolleda, G, Garca-Garca, A, Won Kim, H R, and Mu ñoz-Negrete, F J. "Comparison of retinal nerve fiber layer measured by time domain 48 and spectral domain optical coherence tomography in optic neuritis." Eye (Lond) 2011;25:233-238.
  41. Saidha, S, Al-Louzi, O, Ratchford, J N, et al. "Optical coherence to- mography reflects brain atrophy in multiple sclerosis: A four-year study". Annals of neurology 2015;78:801-813.
  42. Salari, M, Janghorbani, M, Etemadifar, M, Dehghani, A, Razmjoo, H, and Naderian, G. "Effects of vitamin D on retinal nerve fiber layer in vitamin D deficient patients with optic neuritis: Preliminary findings of a randomized, placebo-controlled trial." J Res Med Sci 2015;20:372- 378.
  43. 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:e66151.
  44. Schnurman, Z S, Frohman, T C, Beh, S C, et al. "Retinal architecture and mfERG Optic nerve head component response characteristics in MS". Neurology 2014;82:1888-1896.
  45. Soufi, G, AitBenhaddou, E, Hajji, Z, et al. "Evaluation of retinal nerve fiber layer thickness measured by optical coherence tomography in Moroccan patients with multiple sclerosis." J Fr Ophtalmol 2015;38:497- 503.
  46. Sriram, P, Wang, C, Yiannikas, C, et al. "Relationship between optical coherence tomography and electrophysiology of the visual pathway 49 in non-optic neuritis eyes of multiple sclerosis patients." PloS one 8 2014;9:e102546.
  47. Syc, S B, Saidha, S, Newsome, S D, et al. "Optical coherence tomog- raphy segmentation reveals ganglion cell layer pathology after optic neuritis." Brain 2012;135:521-533.
  48. Walter, S D, Ishikawa, H, Galetta, K M, et al. "Ganglion cell loss in relation to visual disability in multiple sclerosis." Ophthalmology 2012;119:1250-1257.
  49. Xu, L T, Bermel, R A, Nowacki, A S, and Kaiser, P K. "Optical Co- herence Tomography for the Detection of Remote Optic Neuritis in Multiple Sclerosis." J Neuroimaging 2016;26:283-288.
  50. Zimmermann, H, Freing, A, Kaufhold, F, et al. "Optic neuritis interferes with optical coherence tomography and magnetic resonance imaging correlations." Mult Scler 2013;19:443-450.
  51. Knier, B, Schmidt, P, Aly, L, et al. "Retinal inner nuclear layer vol- ume reflects response to immunotherapy in multiple sclerosis." Brain 2016;139:2855-2863. 50
  52. Bailar, J C. "The promise and problems of meta-analysis." The New England journal of medicine 8 1997;337:559-561.
  53. Greenland, S. "Can meta-analysis be salvaged?" American journal of epidemiology 9 1994;140:783-787.
  54. Frohman, E, Costello, F, Zivadinov, R, et al. "Optical coherence to- mography in multiple sclerosis." Lancet Neurol 2006;5:853-863.
  55. Warner, C V, Syc, S B, Stankiewicz, A M, et al. "The impact of utilizing different optical coherence tomography devices for clinical purposes and in multiple sclerosis trials." PLoS One 2011;6:e22947.
  56. Roe, A W. "Functional Architecture and Maps in the Visual Cortex". Annual Review of Vision Science 2017;3.
  57. Petzold, A, Wong, S, and Plant, G T. "Autoimmunity in visual loss." Handb Clin Neurol 2016;133:353-376.
  58. Dinkin, M. "Trans-synaptic Retrograde Degeneration in the Human Vi- sual System: Slow, Silent, and Real." Current neurology and neuro- science reports 2 2017;17:16.
  59. Balk, L J, Cruz-Herranz, A, Albrecht, P, et al. "Timing of retinal neu- ronal and axonal loss in MS: a longitudinal OCT study." J Neurol 2016;263:1323-1331.
  60. Graham, E C, You, Y, Yiannikas, C, Garrick, R, Parratt, J, Barnett, M H, and Klistorner, A. "Progressive Loss of Retinal Ganglion Cells and 51 Axons in Nonoptic Neuritis Eyes in Multiple Sclerosis: A Longitudi- nal Optical Coherence Tomography Study." Invest Ophthalmol Vis Sci 2016;57:2311-2317.
  61. Talman, L S, Bisker, E R, Sackel, D J, et al. "Longitudinal study of vision and retinal nerve fiber layer thickness in multiple sclerosis." Ann Neurol 2010;67:749-760.
  62. Saidha, S, Sotirchos, E S, Ibrahim, M A, et al. "Microcystic macu- lar oedema, thickness of the inner nuclear layer of the retina, and disease characteristics in multiple sclerosis: a retrospective study." Lancet Neurol 2012;11:963-972.
  63. Sepulcre, J, Murie-Fernandez, M, Salinas-Alaman, A, García-Layana, A, Bejarano, B, and Villoslada, P. "Diagnostic accuracy of retinal ab- normalities in predicting disease activity in MS." Neurology 2007;68:1488- 1494.
  64. Petzold, A, Nijland, P G, Balk, L J, et al. "Visual pathway neurodegen- eration winged by mitochondrial dysfunction." Ann Clin Transl Neurol 2015;2:140-150. 52
  65. Cadavid, D, Balcer, L, Galetta, S, et al. "Safety and efficacy of opicinumab in acute optic neuritis (RENEW): a randomised, placebo-controlled, phase 2 trial." The Lancet. Neurology 3 2017;16:189-199.
  66. Kupersmith, M J, Garvin, M K, Wang, JK, Durbin, M, and Kardon, R. "Retinal ganglion cell layer thinning within one month of presentation for optic neuritis". Multiple sclerosis (Houndmills, Basingstoke, Eng- land) 2016;22:641-648.
  67. Gabilondo, I, Martnez-Lapiscina, E H, Fraga-Pumar, E, et al. "Dynam- ics of retinal injury after acute optic neuritis". Annals of Neurology 2015;77:517-528.
  68. Britze, J, Pihl-Jensen, G, and Frederiksen, J L. "Retinal ganglion cell analysis in multiple sclerosis and optic neuritis: a systematic review and meta-analysis." Journal of Neurology 2017. [epub ahead of print].
  69. Burggraaff, M C, Trieu, J, Vries-Knoppert, W A E J de, Balk, L, and Petzold, A. "The Clinical Spectrum of Microcystic Macular Edema". Invest Ophthalmol Vis Sci 2014;55:952-961.
  70. Brandt, A U, Oberwahrenbrock, T, Kadas, E M, Lagr èze, W A, and Paul, F. "Dynamic formation of macular microcysts independent of vitreous traction changes." Neurology 2014;83:73-77. 53
  71. retinal layer volume changes?" Brain 2016;139:2816-2826.
  72. Gelfand, J M, Nolan, R, Schwartz, D M, Graves, J, and Green, A J. "Microcystic macular oedema in multiple sclerosis is associated with disease severity." Brain 2012;135:1786-1793.
  73. Spaide, R F. "RETINAL VASCULAR CYSTOID MACULAR EDEMA: Review and New Theory". Retina 2016;36:1823-1842.
  74. Wostyn, P, De Groot, V, Van Dam, D, Audenaert, K, Killer, H E, and De Deyn, P P. "Age-related macular degeneration, glaucoma and Alzheimer's disease: amyloidogenic diseases with the same glym- phatic background?" Cellular and Molecular Life Sciences 2016;73:4299- 4301.
  75. Havla, J, K ümpfel, T, Schinner, R, et al. "Myelin-oligodendrocyte-glycoprotein (MOG) autoantibodies as potential markers of severe optic neuritis and subclinical retinal axonal degeneration." Journal of neurology 1 2017;264:139-151.
  76. Petzold, A and Plant, G T. "Clinical Use of OCT and MSON Mim- ics". Optical Coherence Tomography in Multiple Sclerosis. Springer Nature, 2016:59-83.
  77. Schlaeger, R, Papinutto, N, Panara, V, et al. "Spinal cord gray matter atrophy correlates with multiple sclerosis disability." Annals of neurol- ogy 4 2014;76:568-580. 54
  78. Balk, L J, Vries-Knoppert, W A E J de, and Petzold, A. "A Simple Sign for Recognizing Off-Axis OCT Measurement Beam Placement in the Context of Multicentre Studies." PLoS One 2012;7:e48222.
  79. Oberwahrenbrock, T, Weinhold, M, Mikolajczak, J, Zimmermann, H, Paul, F, Beckers, I, and Brandt, A U. "Reliability of Intra-Retinal Layer Thickness Estimates." PLoS One 2015;10:e0137316.
  80. Martinez-Lapiscina, E H, Sepulveda, M, Torres-Torres, R, et al. "Use- fulness of optical coherence tomography to distinguish optic neuritis associated with AQP4 or MOG in neuromyelitis optica spectrum dis- orders". Therapeutic Advances in Neurological Disorders 2016;9:436.
  81. Green, A J, McQuaid, S, Hauser, S L, Allen, I V, and Lyness, R. "Oc- ular pathology in multiple sclerosis: retinal atrophy and inflammation irrespective of disease duration." Brain 2010;133:1591-1601.
  82. Holder, G E. "Pattern electroretinography (PERG) and an integrated approach to visual pathway diagnosis." Prog Retin Eye Res 2001;20:531- 561.
  83. Petzold, A. "Neuroprotection and visual function after optic neuritis." Current opinion in neurology 1 2017;30:67-73.

Cited by

Sorted by citations

Authors
Petzold, A., Balcer, L. J., Calabresi, P. A., Costello, F., Frohman, T. C., Frohman, E. M., Martinez-Lapiscina, E. H., Green, A. J., Kardon, R., Outteryck, O., Paul, F., Schippling, S., Vermersch, P., Villoslada, P., Balk, L. J., Aktas, O., Albrecht, P., Ashworth, J., Asgari, N., Balcer, L., Balk, L., Black, G., Boehringer, D., Behbehani, R., Benson, L., Bermel, R., Bernard, J., Brandt, A., Burton, J., Calabresi, P., Calkwood, J., Cordano, C., Costello, F., Courtney, A., Cruz-Herranz, A., Diem, R., Daly, A., Dollfus, H., Fasser, C., Finke, C., Frederiksen, J., Frohman, E., Frohman, T., Garcia-Martin, E., Suárez, I. G., Pihl-Jensen, G., Graves, J., Green, A., Havla, J., Hemmer, B., Huang, S.-C., Imitola, J., Jiang, H., Keegan, D., Kildebeck, E., Klistorner, A., Knier, B., Kolbe, S., Korn, T., LeRoy, B., Leocani, L., Leroux, D., Levin, N., Liskova, P., Lorenz, B., Preiningerova, J. L., Martínez-Lapiscina, E. H., Mikolajczak, J., Montalban, X., Morrow, M., Nolan, R., Oberwahrenbrock, T., Oertel, F. C., Oreja-Guevara, C., Osborne, B., Outteryck, O., Papadopoulou, A., Paul, F., Petzold, A., Ringelstein, M., Saidha, S., Sanchez-Dalmau, B., Sastre-Garriga, J., Schippling, S., Shin, R., Shuey, N., Soelberg, K., Toosy, A., Torres, R., Vidal-Jordana, A., Villoslada, P., Waldman, A., White, O., Yeh, A., Wong, S., & Zimmermann, H.
Affiliations
University of Iowa (US)
ORCID
Venue
The Lancet Neurology
Publisher
Elsevier BV
Published
2017-10
Volume
16
Issue
10
Pages
797-812
ISSN
1474-4422 (ISSN-L)
DOI
10.1016/s1474-4422(17)30278-8
OpenAlex
W2755106885
Cited by
585
References
1
Citations by year
2026: 62 · 2025: 68 · 2024: 74 · 2023: 65 · 2022: 69 · 2021: 65 · 2020: 78 · 2019: 52 · 2018: 43 · 2017: 8
FWCI
7.91
Type
journal article
Language
en
Open access
Licence
Locations
  • The Lancet Neurology (publishedVersion)
  • PubMed (publishedVersion)
  • Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
  • Research Explorer (The University of Manchester) (submittedVersion, cc-by-nc-nd)
  • MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (submittedVersion)
  • UCL Discovery (University College London) (submittedVersion)
  • Archivio Istituzionale della Ricerca - Università Vita-Salute San Raffaele (submittedVersion)
  • mediaTUM – the media and publications repository of the Technical University Munich (Technical University Munich) (submittedVersion, other-oa)
  • Pure Amsterdam UMC (submittedVersion)
  • Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
  • Data Archiving and Networked Services (DANS) (submittedVersion)
Topics
  • Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
  • Health Sciences › Medicine › Ophthalmology › Glaucoma and retinal disorders
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Retinal Imaging and Analysis
Keywords
multiple sclerosis, retinal layer segmentation, spectral-domain optical coherence tomography, retinal nerve fiber layer thinning, optic neuritis, inner plexiform layer, neurodegeneration biomarkers, retinal atrophy, macula, peripapillary retina, retinal thickness, disease surveillance
MeSH terms
Adult, Aged, Female, Humans, Male, Middle Aged, Multiple Sclerosis, Optic Neuritis, Retina, Tomography, Optical Coherence, Young Adult

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review