Abstract
To analyze retinal thickness changes in multiple system atrophy (MSA) and correlate changes with disease severity and subtypes of MSA. A total of 36 MSA (27 MSA-P and 9 MSA-C) patients and 71 healthy control subjects underwent general ophthalmologic examination and optical coherence tomography (OCT) scans. Peripapillary retinal nerve fiber layer (RNFL) thickness and perifoveal retinal thickness were analyzed separately. The generalized estimating equation model was used with age as a covariate to adjust for within-patient inter-eye correlations and the effect of age on retinal or RNFL thickness. Correlation analysis between RNFL, perifoveal thickness, and clinical parameters, the Unified MSA Rating Scale (UMSARS) and Global Disability Score (GDS), was also done. MSA patients showed significantly decreased peripapillary RNFL thickness in the inferior (P = 0.047) and inferotemporal (P = 0.017) sectors and significant perifoveal thinning in the superior outer sector (P = 0.042) compared to healthy controls. Both RNFL and perifoveal thinning were more marked and widespread in MSA-P than MSA-C patients. The UMSARS and GDS showed significant negative correlation with center and total macular perifoveal thickness and also the inferior and nasal outer sectors. Peripapillary RNFL and perifoveal retinal thinning were observed in MSA patients and retinal thinning correlated with the clinical severity of MSA. Structural changes in the retina may reflect the degree and pattern of neurodegeneration occurring in MSA.
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Fanciulli A, Wenning GK (2015) Multiple-system atrophy. N Engl J Med 372(3):249–263. doi:10.1056/NEJMra1311488
Bodis-Wollner I, Miri S, Glazman S (2014) Venturing into the no-man’s land of the retina in Parkinson’s disease. Mov Disord Off J Mov Disord Soc 29(1):15–22. doi:10.1002/mds.25741
Oliveira C, Cestari DM, Rizzo JF 3rd (2012) The use of fourth-generation optical coherence tomography in multiple sclerosis: a review. Semin Ophthalmol 27(5–6):187–191. doi:10.3109/08820538.2012.708808
Bodis-Wollner I, Kozlowski PB, Glazman S, Miri S (2014) alpha-synuclein in the inner retina in parkinson disease. Ann Neurol 75(6):964–966. doi:10.1002/ana.24182
Beach TG, Carew J, Serrano G, Adler CH, Shill HA, Sue LI, Sabbagh MN, Akiyama H, Cuenca N, Arizona Parkinson’s Disease C (2014) Phosphorylated alpha-synuclein-immunoreactive retinal neuronal elements in Parkinson’s disease subjects. Neurosci Lett 571:34–38. doi:10.1016/j.neulet.2014.04.027
Moreno-Ramos T, Benito-Leon J, Villarejo A, Bermejo-Pareja F (2013) Retinal nerve fiber layer thinning in dementia associated with Parkinson’s disease, dementia with Lewy bodies, and Alzheimer’s disease. J Alzheimers Dis JAD 34(3):659–664. doi:10.3233/JAD-121975
Lee JY, Kim JM, Ahn J, Kim HJ, Jeon BS, Kim TW (2014) Retinal nerve fiber layer thickness and visual hallucinations in Parkinson’s Disease. Mov Disord Off J Mov Disord Soc 29(1):61–67. doi:10.1002/mds.25543
Fischer MD, Synofzik M, Heidlauf R, Schicks J, Srulijes K, Kernstock C, Berg D, Schols L, Schiefer U (2011) Retinal nerve fiber layer loss in multiple system atrophy. Mov Disord Off J Mov Disord Soc 26(5):914–916. doi:10.1002/mds.23523
Pula JH, Towle VL, Staszak VM, Cao D, Bernard JT, Gomez CM (2011) Retinal nerve fibre layer and macular thinning in spinocerebellar ataxia and cerebellar multisystem atrophy. Neuroophthalmology 35(3):108–114. doi:10.3109/01658107.2011.580898
Fischer MD, Synofzik M, Kernstock C, Dietzsch J, Heidlauf R, Schicks J, Srulijes K, Wiethoff S, Menn O, Berg D, Schols L, Schiefer U (2013) Decreased retinal sensitivity and loss of retinal nerve fibers in multiple system atrophy. Graefes Arch Clin Exp Ophthalmol (Albrecht von Graefes Archiv fur klinische und experimentelle Ophthalmologie) 251(1):235–241. doi:10.1007/s00417-012-2118-1
Schneider M, Muller HP, Lauda F, Tumani H, Ludolph AC, Kassubek J, Pinkhardt EH (2014) Retinal single-layer analysis in Parkinsonian syndromes: an optical coherence tomography study. J Neural Transm 121(1):41–47. doi:10.1007/s00702-013-1072-3
Mendoza-Santiesteban CE, Palma JA, Martinez J, Norcliffe-Kaufmann L, Hedges TR 3rd, Kaufmann H (2015) Progressive retinal structure abnormalities in multiple system atrophy. Mov Disord Off J Mov Disord Soc 30(14):1944–1953. doi:10.1002/mds.26360
Albrecht P, Muller AK, Sudmeyer M, Ferrea S, Ringelstein M, Cohn E, Aktas O, Dietlein T, Lappas A, Foerster A, Hartung HP, Schnitzler A, Methner A (2012) Optical coherence tomography in parkinsonian syndromes. PLoS One 7(4):e34891. doi:10.1371/journal.pone.0034891
Gilman S, Wenning GK, Low PA, Brooks DJ, Mathias CJ, Trojanowski JQ, Wood NW, Colosimo C, Durr A, Fowler CJ, Kaufmann H, Klockgether T, Lees A, Poewe W, Quinn N, Revesz T, Robertson D, Sandroni P, Seppi K, Vidailhet M (2008) Second consensus statement on the diagnosis of multiple system atrophy. Neurology 71(9):670–676. doi:10.1212/01.wnl.0000324625.00404.15
Silveira LC, Saito CA, Lee BB, Kremers J, da Silva Filho M, Kilavik BE, Yamada ES, Perry VH (2004) Morphology and physiology of primate M- and P-cells. Prog Brain Res 144:21–46. doi:10.1016/S0079-6123(03)14402-0
Armstrong RA (2014) Visual signs and symptoms of multiple system atrophy. Clin Exp Optom 97(6):483–491. doi:10.1111/cxo.12206
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This study protocol was approved by the Institutional Review Board of Seoul National University BMC and informed consent was obtained from all participants.
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Ahn, J., Lee, JY. & Kim, T.W. Retinal thinning correlates with clinical severity in multiple system atrophy. J Neurol 263, 2039–2047 (2016). https://doi.org/10.1007/s00415-016-8230-0
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DOI: https://doi.org/10.1007/s00415-016-8230-0