Optical coherence tomography as retinal imaging biomarker of neuroinflammation/neurodegeneration in systemic disorders in adults and children.


Journal

Eye (London, England)
ISSN: 1476-5454
Titre abrégé: Eye (Lond)
Pays: England
ID NLM: 8703986

Informations de publication

Date de publication:
02 2023
Historique:
received: 26 11 2021
accepted: 31 03 2022
revised: 10 03 2022
pubmed: 17 4 2022
medline: 27 1 2023
entrez: 16 4 2022
Statut: ppublish

Résumé

The retina and the optic nerve are considered extensions of the central nervous system (CNS) and thus can serve as the window for evaluation of CNS disorders. Spectral domain optical coherence tomography (OCT) allows for detailed evaluation of the retina and the optic nerve. OCT can non-invasively document changes in single retina layer thickness and structure due to neuronal and retinal glial cells (RGC) modifications in systemic and local inflammatory and neurodegenerative diseases. These can include evaluation of retinal nerve fibre layer and ganglion cell complex, hyper-reflective retinal spots (HRS, sign of activated microglial cells in the retina), subfoveal neuroretinal detachment, disorganization of the inner retinal layers (DRIL), thickness and integrity of the outer retinal layers and choroidal thickness. This review paper will report the most recent data on the use of OCT as a non invasive imaging biomarker for evaluation of the most common systemic neuroinflammatory and neurodegenerative/neurocognitive disorders in the adults and in paediatric population. In the adult population the main focus will be on diabetes mellitus, multiple sclerosis, optic neuromyelitis, neuromyelitis optica spectrum disorders, longitudinal extensive transverse myelitis, Alzheimer and Parkinson diseases, Amyotrophic lateral sclerosis, Huntington's disease and schizophrenia. In the paediatric population, demyelinating diseases, lysosomal storage diseases, Nieman Pick type C disease, hypoxic ischaemic encephalopathy, human immunodeficiency virus, leukodystrophies spinocerebellar ataxia will be addressed. 摘要: 视网膜和视神经是中枢神经系统 (CNS) 的延续, 因此可以作为评估CNS疾病的窗口。频域光学相干断层扫描 (SD-OCT) 可以对视网膜和视神经进行详细的评估。OCT可以无创性地记录系统性和局部炎症/神经退行性病变中, 由于神经元和视网膜胶质细胞 (RGC) 改变引起的视网膜单层厚度和结构的变化。OCT的观察的指征包括评估视网膜神经纤维层和神经节细胞复合体、视网膜高反射点 (HRS, 视网膜中小胶质细胞激活的征象) 、中心凹下神经视网膜脱离、视网膜内层结构紊乱 (DRIL) 、视网膜外层的厚度和完整性以及脉络膜厚度。本文将总结OCT作为无创成像生物标志物评估成人和儿童中最常见的系统性神经炎症和神经退行性病变/神经认知障碍的最新数据。在成人中, 我们最关注的疾病为糖尿病、多发性硬化症、视神经脊髓炎、视神经脊髓炎谱系障碍、纵向广泛横贯性脊髓炎、阿尔茨海默病和帕金森病、肌萎缩侧索硬化症、亨廷顿病和精神分裂症。在儿童中, 我们着重讨论的疾病有脱髓鞘疾病、溶酶体贮积病、尼曼-匹克病、缺氧缺血性脑病、人类免疫缺陷病毒、脑白质营养不良脊髓小脑性共济失调。.

Autres résumés

Type: Publisher (chi)
摘要: 视网膜和视神经是中枢神经系统 (CNS) 的延续, 因此可以作为评估CNS疾病的窗口。频域光学相干断层扫描 (SD-OCT) 可以对视网膜和视神经进行详细的评估。OCT可以无创性地记录系统性和局部炎症/神经退行性病变中, 由于神经元和视网膜胶质细胞 (RGC) 改变引起的视网膜单层厚度和结构的变化。OCT的观察的指征包括评估视网膜神经纤维层和神经节细胞复合体、视网膜高反射点 (HRS, 视网膜中小胶质细胞激活的征象) 、中心凹下神经视网膜脱离、视网膜内层结构紊乱 (DRIL) 、视网膜外层的厚度和完整性以及脉络膜厚度。本文将总结OCT作为无创成像生物标志物评估成人和儿童中最常见的系统性神经炎症和神经退行性病变/神经认知障碍的最新数据。在成人中, 我们最关注的疾病为糖尿病、多发性硬化症、视神经脊髓炎、视神经脊髓炎谱系障碍、纵向广泛横贯性脊髓炎、阿尔茨海默病和帕金森病、肌萎缩侧索硬化症、亨廷顿病和精神分裂症。在儿童中, 我们着重讨论的疾病有脱髓鞘疾病、溶酶体贮积病、尼曼-匹克病、缺氧缺血性脑病、人类免疫缺陷病毒、脑白质营养不良脊髓小脑性共济失调。.

Identifiants

pubmed: 35428871
doi: 10.1038/s41433-022-02056-9
pii: 10.1038/s41433-022-02056-9
pmc: PMC9012155
doi:

Substances chimiques

Biomarkers 0

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

203-219

Subventions

Organisme : NEI NIH HHS
ID : R01 EY015130
Pays : United States
Organisme : NEI NIH HHS
ID : R01 EY017011
Pays : United States

Commentaires et corrections

Type : ErratumIn

Informations de copyright

© 2022. The Author(s), under exclusive licence to The Royal College of Ophthalmologists.

Références

Chen WW, Zhang X, Huang WJ. Role of neuroinflammation in neurodegenerative diseases (Review). Mol Med Rep. 2016;13:3391–6.
doi: 10.3892/mmr.2016.4948
Amor S, Puentes F, Baker D, van der Valk P. Inflammation in neurodegenerative diseases. Immunology 2010;129:154–69.
doi: 10.1111/j.1365-2567.2009.03225.x
Bakhtadze S, Geladze N, Khachapuridze N. Inflammation in childhood epilepsy syndromes. Georgian Med N. 2021;312:88–92.
Sudhakar SV, Muthusamy K, Shroff M. Imaging of childhood inflammatory brain diseases. Top Magn Reson Imaging. 2018;27:409–31.
doi: 10.1097/RMR.0000000000000187
Borchert M, Liu GT, Pineles S, Waldman AT. Pediatric optic neuritis: what is new. J Neuroophthalmol. 2017;37:S14–s22.
doi: 10.1097/WNO.0000000000000551
Strimbu K, Tavel JA. What are biomarkers? Curr Opin HIV AIDS. 2010;5:463–6.
doi: 10.1097/COH.0b013e32833ed177
Zhou WC, Tao JX, Li J. Optical coherence tomography measurements as potential imaging biomarkers for Parkinson’s disease: A systematic review and meta-analysis. Eur J Neurol. 2021;28:763–74.
doi: 10.1111/ene.14613
Yeh EA, Weinstock-Guttman B, Lincoff N, Reynolds J, Weinstock A, Madurai N, et al. Retinal nerve fiber thickness in inflammatory demyelinating diseases of childhood onset. Mult Scler (Houndmills, Basingstoke, Engl). 2009;15:802–10.
doi: 10.1177/1352458509104586
Waldman AT, Hiremath G, Avery RA, Conger A, Pineles SL, Loguidice MJ, et al. Monocular and binocular low-contrast visual acuity and optical coherence tomography in pediatric multiple sclerosis. Mult Scler Relat Disord. 2013;3:326–34.
doi: 10.1016/j.msard.2013.10.008
Bennett JL, de Seze J, Lana-Peixoto M, Palace J, Waldman A, Schippling S, et al. Neuromyelitis optica and multiple sclerosis: Seeing differences through optical coherence tomography. Mult Scler (Houndmills, Basingstoke, Engl). 2015;21:678–88.
doi: 10.1177/1352458514567216
van Ballegoij WJC, Huffnagel IC, van de Stadt SIW, Weinstein HC, Bennebroek CAM, Engelen M, et al. Optical coherence tomography to measure the progression of myelopathy in adrenoleukodystrophy. Ann Clin Transl Neurol. 2021;8:1064–72.
doi: 10.1002/acn3.51349
Alvarez G, Rey A, Sanchez-Dalmau FB, Muñoz E, Ríos J, Adán A. Optical coherence tomography findings in spinocerebellar ataxia-3. Eye (Lond, Engl). 2013;27:1376–81.
doi: 10.1038/eye.2013.201
Tran-Viet D, Wong BM, Mangalesh S, Maldonado R, Cotten CM, Toth CA. Hanheld spectral domain optical coherence tomography imaging through the undilated pupil in infants born preterm or with hipoxic injury or hydrocephalus. Retina. 2017;38:1588–94.
doi: 10.1097/IAE.0000000000001735
Grego L, Pignatto S, Busolini E, Rassu N, Samassa F, Prosperi R, et al. Spectral-domain OCT changes in retina and optic nerve in children with hypoxic-ischaemic encephalopathy. Graefe’s Arch Clin Exp Ophthalmol = Albrecht von Graefes Arch fur klinische und experimentelle Ophthalmologie. 2021;259:1343–55.
doi: 10.1007/s00417-020-04996-y
McGeer PL, McGeer EG. The inflammatory response system of brain: implications for therapy of Alzheimer and other neurodegenerative diseases. Brain Res Brain Res Rev. 1995;21:195–218.
doi: 10.1016/0165-0173(95)00011-9
Lynch MA. The multifaceted profile of activated microglia. Mol Neurobiol. 2009;40:139–56.
doi: 10.1007/s12035-009-8077-9
Vujosevic S, Simó R. Local and systemic inflammatory biomarkers of diabetic retinopathy: an integrative approach. Invest Ophthalmol Vis Sci. 2017;58:Bio68–bio75.
doi: 10.1167/iovs.17-21769
Antonetti DA, Barber AJ, Bronson SK, Freeman WM, Gardner TW, Jefferson LS, et al. Diabetic retinopathy: seeing beyond glucose-induced microvascular disease. Diabetes. 2006;55:2401–11.
doi: 10.2337/db05-1635
Vujosevic S, Micera A, Bini S, Berton M, Esposito G, Midena E. Aqueous humor biomarkers of müller cell activation in diabetic eyes. Investigative Ophthalmol Vis Sci. 2015;56:3913–8.
doi: 10.1167/iovs.15-16554
Vujosevic S, Torresin T, Bini S, Convento E, Pilotto E, Parrozzani R, et al. Imaging retinal inflammatory biomarkers after intravitreal steroid and anti-VEGF treatment in diabetic macular oedema. Acta Ophthalmol. 2017;95:464–71.
doi: 10.1111/aos.13294
Hanisch UK, Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci. 2007;10:1387–94.
doi: 10.1038/nn1997
Vujosevic S, Midena E. Retinal layers changes in human preclinical and early clinical diabetic retinopathy support early retinal neuronal and Müller cells alterations. J Diabetes Res. 2013;2013:905058.
doi: 10.1155/2013/905058
Yu Y, Chen H, Su SB. Neuroinflammatory responses in diabetic retinopathy. J Neuroinflammation. 2015;12:141.
doi: 10.1186/s12974-015-0368-7
Vujosevic S, Bini S, Torresin T, Berton M, Midena G, Parrozzani R, et al. Hyperreflective retinal spots in normal and diabetic eyes: b-scan and en face spectral domain optical coherence tomography evaluation. Retina 2017;37:1092–103.
doi: 10.1097/IAE.0000000000001304
Vujosevic S, Bini S, Midena G, Berton M, Pilotto E, Midena E. Hyperreflective intraretinal spots in diabetics without and with nonproliferative diabetic retinopathy: an in vivo study using spectral domain OCT. J Diabetes Res. 2013;2013:491835.
doi: 10.1155/2013/491835
Ogino K, Murakami T, Tsujikawa A, Miyamoto K, Sakamoto A, Ota M, et al. Characteristics of optical coherence tomographic hyperreflective foci in retinal vein occlusion. Retina. 2012;32:77–85.
doi: 10.1097/IAE.0b013e318217ffc7
Coscas GCF, Vismara S, Zourdanic A, Li Calzi CI. Optical coherence tomography in age-related macular degeneration: OCT in AMD. Publishing S, editor 2009 1–389 p.
Curcio CA, Zanzottera EC, Ach T, Balaratnasingam C, Freund KB. Activated retinal pigment epithelium, an optical coherence tomography biomarker for progression in age-related macular degeneration. Investig Ophthalmol Vis Sci. 2017;58:BIO211–BIO26.
Vujosevic S, Berton M, Bini S, Casciano M, Cavarzeran F, Midena E. Hyperreflective retinal spots and visual function after anti-vascular endothelial growth factor treatment in center-involving diabetic macular edema. Retina. 2016;36:1298–308.
doi: 10.1097/IAE.0000000000000912
Pilotto E, Miante S, Torresin T, Puthenparampil M, Frizziero L, Federle L, et al. Hyperreflective foci in the retina of active relapse-onset multiple sclerosis. Ophthalmology. 2020;127:1774–6.
doi: 10.1016/j.ophtha.2020.03.024
Vujosevic S, Toma C, Villani E, Muraca A, Torti E, Florimbi G, et al. Diabetic macular edema with neuroretinal detachment: OCT and OCT-angiography biomarkers of treatment response to anti-VEGF and steroids. Acta Diabetol. 2020;57:287–96.
doi: 10.1007/s00592-019-01424-4
Chen KC, Jung JJ, Curcio CA, Balaratnasingam C, Gallego-Pinazo R, Dolz-Marco R, et al. Intraretinal hyperreflective foci in acquired vitelliform lesions of the macula: clinical and histologic study. Am J Ophthalmol. 2016;164:89–98.
doi: 10.1016/j.ajo.2016.02.002
Pang CE, Messinger JD, Zanzottera EC, Freund KB, Curcio CA. The onion sign in neovascular age-related macular degeneration represents cholesterol crystals. Ophthalmology. 2015;122:2316–26.
doi: 10.1016/j.ophtha.2015.07.008
Cao D, Leong B, Messinger JD, Kar D, Ach T, Yannuzzi LA, et al. Hyperreflective foci, optical coherence tomography progression indicators in age-related macular degeneration, include transdifferentiated retinal pigment epithelium. Invest Ophthalmol Vis Sci. 2021;62:34.
doi: 10.1167/iovs.62.10.34
Lee H, Jang H, Choi YA, Kim HC, Chung H. Association between soluble CD14 in the aqueous humor and hyperreflective foci on optical coherence tomography in patients with diabetic macular edema. Investigative Ophthalmol Vis Sci. 2018;59:715–21.
doi: 10.1167/iovs.17-23042
Deák GG, Bolz M, Kriechbaum K, Prager S, Mylonas G, Scholda C, et al. Effect of retinal photocoagulation on intraretinal lipid exudates in diabetic macular edema documented by optical coherence tomography. Ophthalmology. 2010;117:773–9.
doi: 10.1016/j.ophtha.2009.09.027
Sonoda S, Sakamoto T, Yamashita T, Shirasawa M, Otsuka H, Sonoda Y. Retinal morphologic changes and concentrations of cytokines in eyes with diabetic macular edema. Retina. 2014;34:741–8.
doi: 10.1097/IAE.0b013e3182a48917
Coscas G, Gaudric A. Natural course of nonaphakic cystoid macular edema. Surv Ophthalmol. 1984;28:471–84.
doi: 10.1016/0039-6257(84)90229-7
van Dijk HW, Verbraak FD, Kok PH, Garvin MK, Sonka M, Lee K, et al. Decreased retinal ganglion cell layer thickness in patients with type 1 diabetes. Invest Ophthalmol Vis Sci. 2010;51:3660–5.
doi: 10.1167/iovs.09-5041
van Dijk HW, Verbraak FD, Kok PH, Stehouwer M, Garvin MK, Sonka M, et al. Early neurodegeneration in the retina of type 2 diabetic patients. Invest Ophthalmol Vis Sci. 2012;53:2715–9.
doi: 10.1167/iovs.11-8997
Barber AJ, Gardner TW, Abcouwer SF. The significance of vascular and neural apoptosis to the pathology of diabetic retinopathy. Invest Ophthalmol Vis Sci. 2011;52:1156–63.
doi: 10.1167/iovs.10-6293
Lynch SK, Abràmoff MD. Diabetic retinopathy is a neurodegenerative disorder. Vis Res. 2017;139:101–7.
doi: 10.1016/j.visres.2017.03.003
Knier B, Schmidt P, Aly L, Buck D, Berthele A, Mühlau M, et al. Retinal inner nuclear layer volume reflects response to immunotherapy in multiple sclerosis. Brain. 2016;139:2855–63.
doi: 10.1093/brain/aww219
Martinez-Lapiscina EH, Sepulveda M, Torres-Torres R, Alba-Arbalat S, Llufriu S, Blanco Y, et al. Usefulness of optical coherence tomography to distinguish optic neuritis associated with AQP4 or MOG in neuromyelitis optica spectrum disorders. Ther Adv Neurol Disord. 2016;9:436–40.
doi: 10.1177/1756285616655264
Zafar S, Sachdeva M, Frankfort BJ, Channa R. Retinal neurodegeneration as an early manifestation of diabetic eye disease and potential neuroprotective therapies. Curr Diabetes Rep. 2019;19:17.
doi: 10.1007/s11892-019-1134-5
Maheshwary AS, Oster SF, Yuson RM, Cheng L, Mojana F, Freeman WR. The association between percent disruption of the photoreceptor inner segment-outer segment junction and visual acuity in diabetic macular edema. Am J Ophthalmol. 2010;150:63–7.
doi: 10.1016/j.ajo.2010.01.039
Kim BJ, Irwin DJ, Song D, Daniel E, Leveque JD, Raquib AR, et al. Optical coherence tomography identifies outer retina thinning in frontotemporal degeneration. Neurology. 2017;89:1604–11.
doi: 10.1212/WNL.0000000000004500
Sun JK, Lin MM, Lammer J, Prager S, Sarangi R, Silva PS, et al. Disorganization of the retinal inner layers as a predictor of visual acuity in eyes with center-involved diabetic macular edema. JAMA Ophthalmol. 2014;132:1309–16.
doi: 10.1001/jamaophthalmol.2014.2350
Radwan SH, Soliman AZ, Tokarev J, Zhang L, van Kuijk FJ, Koozekanani DD. Association of disorganization of retinal inner layers with vision after resolution of center-involved diabetic macular edema. JAMA Ophthalmol. 2015;133:820–5.
doi: 10.1001/jamaophthalmol.2015.0972
Rübsam A, Parikh S, Fort PE. Role of inflammation in diabetic retinopathy. Int J Mol Sci. 2018;19:942.
doi: 10.3390/ijms19040942
Nian S, Lo ACY, Mi Y, Ren K, Yang D. Neurovascular unit in diabetic retinopathy: pathophysiological roles and potential therapeutical targets. Eye Vis. 2021;8:15.
doi: 10.1186/s40662-021-00239-1
Simó R, Hernández C. Neurodegeneration in the diabetic eye: new insights and therapeutic perspectives. Trends Endocrinol Metab. 2014;25:23–33.
doi: 10.1016/j.tem.2013.09.005
Santos AR, Ribeiro L, Bandello F, Lattanzio R, Egan C, Frydkjaer-Olsen U, et al. Functional and structural findings of neurodegeneration in early stages of diabetic retinopathy: cross-sectional analyses of baseline data of the EUROCONDOR Project. Diabetes 2017;66:2503–10.
doi: 10.2337/db16-1453
Montesano G, Ometto G, Higgins BE, Das R, Graham KW, Chakravarthy U, et al. Evidence for structural and functional damage of the inner retina in diabetes with no diabetic retinopathy. Investigative Ophthalmol Vis Sci. 2021;62:35.
doi: 10.1167/iovs.62.3.35
Soni D, Sagar P, Takkar B. Diabetic retinal neurodegeneration as a form of diabetic retinopathy. Int Ophthalmol. 2021;41:3223–48.
doi: 10.1007/s10792-021-01864-4
van de Kreeke JA, Darma S, Chan Pin Yin JMPL, Tan HS, Abramoff MD, Twisk JWR, et al. The spatial relation of diabetic retinal neurodegeneration with diabetic retinopathy. PLOS ONE. 2020;15:e0231552.
doi: 10.1371/journal.pone.0231552
Vujosevic S, Muraca A, Alkabes M, Villani E, Cavarzeran F, Rossetti L, et al. Early microvascular and neural changes in patients with type 1 and type 2 diabetes mellitus without clinical signs of diabetic retinopathy. Retina 2019;39:435–45.
doi: 10.1097/IAE.0000000000001990
Gallina D, Zelinka CP, Cebulla CM, Fischer AJ. Activation of glucocorticoid receptors in Müller glia is protective to retinal neurons and suppresses microglial reactivity. Exp Neurol. 2015;273:114–25.
doi: 10.1016/j.expneurol.2015.08.007
Scarinci F, Varano M, Parravano M. Retinal sensitivity loss correlates with deep capillary plexus impairment in diabetic macular ischemia. J Ophthalmol. 2019;2019:7589841.
Campos A, Campos EJ, Martins J, Rodrigues FSC, Silva R, Ambrósio AF. Inflammatory cells proliferate in the choroid and retina without choroidal thickness change in early Type 1 diabetes. Exp Eye Res. 2020;199:108195.
doi: 10.1016/j.exer.2020.108195
Gupta C, Tan R, Mishra C, Khandelwal N, Raman R, Kim R, et al. Choroidal structural analysis in eyes with diabetic retinopathy and diabetic macular edema—A novel OCT based imaging biomarker. PLOS ONE. 2018;13:e0207435.
doi: 10.1371/journal.pone.0207435
Abadia B, Suñen I, Calvo P, Bartol F, Verdes G, Ferreras A. Choroidal thickness measured using swept-source optical coherence tomography is reduced in patients with type 2 diabetes. PLOS ONE. 2018;13:e0191977.
doi: 10.1371/journal.pone.0191977
Huang-Link YM, Fredrikson M, Link H. Benign Multiple Sclerosis is Associated with Reduced Thinning of the Retinal Nerve Fiber and Ganglion Cell Layers in Non-Optic-Neuritis Eyes. J Clin Neurol. 2015;11:241–7.
doi: 10.3988/jcn.2015.11.3.241
Birkeldh U, Manouchehrinia A, Hietala MA, Hillert J, Olsson T, Piehl F, et al. The temporal retinal nerve fiber layer thickness is the most important optical coherence tomography estimate in multiple sclerosis. Front Neurol. 2017;1–8.
Petzold A, Balcer LJ, Calabresi PA, Costello F, Frohman TC, Frohman EM, et al. Retinal layer segmentation in multiple sclerosis: a systematic review and meta-analysis. Lancet Neurol. 2017;16:797–812.
doi: 10.1016/S1474-4422(17)30278-8
Pietroboni AM, Carandini T, Dell’Arti L, Bovis F, Colombi A, De Riz MA, et al. Evidence of retinal anterograde neurodegeneration in the very early stages of multiple sclerosis: a longitudinal OCT study. Neurol Sci. 2020;41:3175–83.
doi: 10.1007/s10072-020-04431-4
Reis AS, O’Leary N, Yang H, Sharpe GP, Nicolela MT, Burgoyne CF, et al. Influence of clinically invisible, but optical coherence tomography detected, optic disc margin anatomy on neuroretinal rim evaluation. Invest Ophthalmol Vis Sci. 2012;53:1852–60.
doi: 10.1167/iovs.11-9309
Nguyen J, Rothman A, Gonzalez N, Avornu A, Ogbuokiri E, Balcer LJ, 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;39:444–50.
doi: 10.1097/WNO.0000000000000768
Walter SD, Ishikawa H, Galetta KM, Sakai RE, Feller DJ, Henderson SB, et al. Ganglion cell loss in relation to visual disability in multiple sclerosis. Ophthalmology. 2012;119:1250–7.
doi: 10.1016/j.ophtha.2011.11.032
Ashtari F, Ataei A, Kafieh R, Khodabandeh Z, Barzegar M, Raei M, et al. Optical coherence tomography in neuromyelitis optica spectrum disorder and multiple sclerosis: a population-based study. Mult Scler Relat Disord. 2021;47:102625.
doi: 10.1016/j.msard.2020.102625
Gelfand JM, Nolan R, Schwartz DM, Graves J, Green AJ. Microcystic macular oedema in multiple sclerosis is associated with disease severity. Brain. 2012;135:1786–93.
doi: 10.1093/brain/aws098
Saidha S, Sotirchos ES, Ibrahim MA, Crainiceanu CM, Gelfand JM, Sepah YJ, 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;11:963–72.
doi: 10.1016/S1474-4422(12)70213-2
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;46:1075–86.
doi: 10.1111/ceo.13327
Abegg M, Dysli M, Wolf S, Kowal J, Dufour P, Zinkernagel M. Microcystic macular edema: retrograde maculopathy caused by optic neuropathy. Ophthalmology. 2014;121:142–9.
doi: 10.1016/j.ophtha.2013.08.045
Barboni P, Carelli V, Savini G, Carbonelli M, La Morgia C, Sadun AA. Microcystic macular degeneration from optic neuropathy: not inflammatory, not trans-synaptic degeneration. Brain 2013;136:e239.
doi: 10.1093/brain/awt014
Lujan BJ, Horton JC. Microcysts in the inner nuclear layer from optic atrophy are caused by retrograde trans-synaptic degeneration combined with vitreous traction on the retinal surface. Brain. 2013;136:e260.
doi: 10.1093/brain/awt154
Brandt AU, Oberwahrenbrock T, Kadas EM, Lagrèze WA, Paul F. Dynamic formation of macular microcysts independent of vitreous traction changes. Neurology. 2014;83:73.
doi: 10.1212/WNL.0000000000000545
Garcia-Martin E, Jarauta L, Pablo LE, Bambo MP, Ara JR, Martin J, et al. Changes in peripapillary choroidal thickness in patients with multiple sclerosis. Acta Ophthalmol. 2019;97:e77–e83.
doi: 10.1111/aos.13807
Barreiro-González A, Sanz MT, Carratalà-Boscà S, Pérez-Miralles F, Alcalá C, Carreres-Polo J, et al. Magnetic resonance imaging and optical coherence tomography correlations in multiple sclerosis beyond anatomical landmarks. J Neurol Sci. 2020;419:117180.
doi: 10.1016/j.jns.2020.117180
Alonso R, Gonzalez-Moron D, Garcea O. Optical coherence tomography as a biomarker of neurodegeneration in multiple sclerosis: a review. Mult Scler Relat Disord. 2018;22:77–82.
doi: 10.1016/j.msard.2018.03.007
Weinshenker BG, Wingerchuk DM. Neuromyelitis spectrum disorders. Mayo Clin Proc. 2017;92:663–79.
doi: 10.1016/j.mayocp.2016.12.014
Jarius S, Wildemann B, Paul F. Neuromyelitis optica: clinical features, immunopathogenesis and treatment. Clin Exp Immunol. 2014;176:149–64.
doi: 10.1111/cei.12271
Syc SB, Saidha S, Newsome SD, Ratchford JN, Levy M, Ford ET, et al. Optical coherence tomography segmentation reveals ganglion cell layer pathology after optic neuritis. Brain. 2011;135:521–33.
doi: 10.1093/brain/awr264
Fernandes DB, Raza AS, Nogueira RGF, Wang D, Callegaro D, Hood DC, et al. Evaluation of inner retinal layers in patients with multiple sclerosis or neuromyelitis optica using optical coherence tomography. Ophthalmology. 2013;120:387–94.
doi: 10.1016/j.ophtha.2012.07.066
Peng A, Qiu X, Zhang L, Zhu X, He S, Lai W, et al. Evaluation of the retinal nerve fiber layer in neuromyelitis optica spectrum disorders: a systematic review and meta-analysis. J Neurol Sci. 2017;383:108–13.
doi: 10.1016/j.jns.2017.10.028
Akaishi T, Kaneko K, Himori N, Takeshita T, Takahashi T, Nakazawa T, et al. Subclinical retinal atrophy in the unaffected fellow eyes of multiple sclerosis and neuromyelitis optica. J Neuroimmunol. 2017;313:10–5.
doi: 10.1016/j.jneuroim.2017.10.001
Gelfand JM, Cree BA, Nolan R, Arnow S, Green AJ. Microcystic inner nuclear layer abnormalities and neuromyelitis optica. JAMA Neurol. 2013;70:629–33.
doi: 10.1001/jamaneurol.2013.1832
Oertel FC, Kuchling J, Zimmermann H, Chien C, Schmidt F, Knier B, et al. Microstructural visual system changes in AQP4-antibody-seropositive NMOSD. Neurol Neuroimmunol Neuroinflamm. 2017;4:e334.
doi: 10.1212/NXI.0000000000000334
Kwapong WR, Peng C, He Z, Zhuang X, Shen M, Lu F. Altered macular microvasculature in neuromyelitis optica spectrum disorders. Am J Ophthalmol. 2018;192:47–55.
doi: 10.1016/j.ajo.2018.04.026
Yap TE, Balendra SI, Almonte MT, Cordeiro MF. Retinal correlates of neurological disorders. Ther Adv Chronic Dis. 2019;10:2040622319882205.
doi: 10.1177/2040622319882205
Lee GI, Park KA, Oh SY, Min JH, Kim BJ. Differential patterns of parafoveal and peripapillary vessel density in multiple sclerosis and neuromyelitis optica spectrum disorder. Mult Scler Relat Disord. 2021;49:102780.
doi: 10.1016/j.msard.2021.102780
Monteiro ML, Fernandes DB, Apóstolos-Pereira SL, Callegaro D. 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. 2012;53:3959–66.
doi: 10.1167/iovs.11-9324
Ratchford JN, Quigg ME, Conger A, Frohman T, Frohman E, Balcer LJ, et al. Optical coherence tomography helps differentiate neuromyelitis optica and MS optic neuropathies. Neurology. 2009;73:302–8.
doi: 10.1212/WNL.0b013e3181af78b8
Dulz S, Atiskova Y, Wibbeler E, Wildner J, Wagenfeld L, Schwering C, et al. An ophthalmic rating scale to assess ocular involvement in juvenile CLN3 disease. Am J Ophthalmol. 2020;220:64–71.
doi: 10.1016/j.ajo.2020.07.015
Spina Tensini F, Sato MT, Shiokawa N, Ashizawa T, Teive HAG. A comparative optical coherence tomography study of spinocerebellar ataxia types 3 and 10. Cerebellum 2017;16:797–801.
doi: 10.1007/s12311-017-0856-7
Havla J, Moser M, Sztatecsny C, Lotz-Havla AS, Maier EM, Hizli B, et al. Retinal axonal degeneration in Niemann-Pick type C disease. J Neurol. 2020;267:2070–82.
doi: 10.1007/s00415-020-09796-2
Pineda M, Perez-Poyato MS, O’Callaghan M, Vilaseca MA, Pocovi M, Domingo R, et al. Clinical experience with miglustat therapy in pediatric patients with Niemann-Pick disease type C: a case series. Mol Genet Metab. 2010;99:358–66.
doi: 10.1016/j.ymgme.2009.11.007
Schmitz-Hübsch T, du Montcel ST, Baliko L, Berciano J, Boesch S, Depondt C, et al. Scale for the assessment and rating of ataxia. Neurology. 2006;66:1717.
doi: 10.1212/01.wnl.0000219042.60538.92
Jensen K, Beylergil SB, Shaikh AG. Slow saccades in cerebellar disease. Cerebellum Ataxias. 2019;6:1.
doi: 10.1186/s40673-018-0095-9
Blokhuis C, Demirkaya N, Cohen S, Wit FWNM, Scherpbier HJ, Reiss P, et al. The eye as a window to the brain: neuroretinal thickness is associated with microstructural white matter injury in HIV-infected children. Investigative Ophthalmol Vis Sci. 2016;57:3864–71.
doi: 10.1167/iovs.16-19716
Meyer-Moock S, Feng Y-S, Maeurer M, Dippel F-W, Kohlmann T. Systematic literature review and validity evaluation of the Expanded Disability Status Scale (EDSS) and the Multiple Sclerosis Functional Composite (MSFC) in patients with multiple sclerosis. BMC Neurol. 2014;14:58.
doi: 10.1186/1471-2377-14-58
Ashizawa T, Öz G, Paulson HL. Spinocerebellar ataxias: prospects and challenges for therapy development. Nat Rev Neurol. 2018;14:590–605.
doi: 10.1038/s41582-018-0051-6
Mastrangelo M. Clinical approach to neurodegenerative disorders in childhood: an updated overview. Acta neurologica Belgica. 2019;119:511–21.
doi: 10.1007/s13760-019-01160-0
Chan VTT, Sun Z, Tang S, Chen LJ, Wong A, Tham CC, et al. Spectral-domain OCT measurements in alzheimer’s disease: a systematic review and meta-analysis. Ophthalmology. 2019;126:497–510.
doi: 10.1016/j.ophtha.2018.08.009
Koronyo-Hamaoui M, Koronyo Y, Ljubimov AV, Miller CA, Ko MK, Black KL, et al. Identification of amyloid plaques in retinas from Alzheimer’s patients and noninvasive in vivo optical imaging of retinal plaques in a mouse model. Neuroimage 2011;54:S204–17.
doi: 10.1016/j.neuroimage.2010.06.020
Koronyo Y, Biggs D, Barron E, Boyer DS, Pearlman JA, Au WJ, et al. Retinal amyloid pathology and proof-of-concept imaging trial in Alzheimer’s disease. JCI Insight. 2017;2:e93621.
Scharre DW. Preclinical, prodromal, and dementia stages of alzheimer’s disease. Pract Neurol. 2019.
Hinton DR, Sadun AA, Blanks JC, Miller CA. Optic-nerve degeneration in Alzheimer’s disease. N. Engl J Med. 1986;315:485–7.
doi: 10.1056/NEJM198608213150804
Cheung CY, Chan VTT, Mok VC, Chen C, Wong TY. Potential retinal biomarkers for dementia: what is new? Curr Opin Neurol. 2019;32:82–91.
doi: 10.1097/WCO.0000000000000645
Alber J, Goldfarb D, Thompson LI, Arthur E, Hernandez K, Cheng D, et al. Developing retinal biomarkers for the earliest stages of Alzheimer’s disease: What we know, what we don’t, and how to move forward. Alzheimers Dement. 2020;16:229–43.
doi: 10.1002/alz.12006
den Haan J, Verbraak FD, Visser PJ, Bouwman FH. Retinal thickness in Alzheimer’s disease: A systematic review and meta-analysis. Alzheimers Dement (Amst). 2017;6:162–70.
doi: 10.1016/j.dadm.2016.12.014
Cheung CY, Ong YT, Hilal S, Ikram MK, Low S, Ong YL, et al. Retinal ganglion cell analysis using high-definition optical coherence tomography in patients with mild cognitive impairment and Alzheimer’s disease. J Alzheimers Dis. 2015;45:45–56.
doi: 10.3233/JAD-141659
Trebbastoni A, Marcelli M, Mallone F, D’Antonio F, Imbriano L, Campanelli A, et al. Attenuation of Choroidal Thickness in Patients With Alzheimer Disease: Evidence From an Italian Prospective Study. Alzheimer Dis Assoc Disord. 2017;31:128–34.
doi: 10.1097/WAD.0000000000000176
Bulut M, Yaman A, Erol MK, Kurtuluş F, Toslak D, Doğan B, et al. Choroidal Thickness in Patients with Mild Cognitive Impairment and Alzheimer’s Type Dementia. J Ophthalmol. 2016;2016:7291257.
Rifai OM, McGrory S, Robbins CB, Grewal DS, Liu A, Fekrat S, et al. The application of optical coherence tomography angiography in Alzheimer’s disease: A systematic review. Alzheimers Dement (Amst). 2021;13:e12149.
Harnois C, Di Paolo T. Decreased dopamine in the retinas of patients with Parkinson’s disease. Invest Ophthalmol Vis Sci. 1990;31:2473–5.
Chhablani PP, Ambiya V, Nair AG, Bondalapati S, Chhablani J. Retinal Findings on OCT in Systemic Conditions. Semin Ophthalmol. 2018;33:525–46.
doi: 10.1080/08820538.2017.1332233
Bodis-Wollner I, Kozlowski PB, Glazman S, Miri S. α-synuclein in the inner retina in parkinson disease. Ann Neurol. 2014;75:964–6.
doi: 10.1002/ana.24182
Chrysou A, Jansonius NM, van Laar T. Retinal layers in Parkinson’s disease: A meta-analysis of spectral-domain optical coherence tomography studies. Parkinsonism Relat Disord. 2019;64:40–9.
doi: 10.1016/j.parkreldis.2019.04.023
Huang J, Wang Q, Li K, Zhang Q, Xu G, Liu J, et al. Spectral domain OCT can differentiate the retinal morphological changes of patients with Parkinson’s disease in clinical middle stages. Neurol Sci 2020;41:1909–12.
doi: 10.1007/s10072-020-04266-z
Bayer AU, Keller ON, Ferrari F, Maag KP. Association of glaucoma with neurodegenerative diseases with apoptotic cell death: Alzheimer’s disease and Parkinson’s disease. Am J Ophthalmol. 2002;133:135–7.
doi: 10.1016/S0002-9394(01)01196-5
La Morgia C, Barboni P, Rizzo G, Carbonelli M, Savini G, Scaglione C, et al. Loss of temporal retinal nerve fibers in Parkinson disease: a mitochondrial pattern? Eur J Neurol. 2013;20:198–201.
doi: 10.1111/j.1468-1331.2012.03701.x
Moschos MM, Chatziralli IP. Evaluation of Choroidal and Retinal Thickness Changes in Parkinson’s Disease Using Spectral Domain Optical Coherence Tomography. Semin Ophthalmol. 2018;33:494–7.
doi: 10.1080/08820538.2017.1307423
Kwapong WR, Ye H, Peng C, Zhuang X, Wang J, Shen M, et al. Retinal Microvascular Impairment in the Early Stages of Parkinson’s Disease. Invest Ophthalmol Vis Sci. 2018;59:4115–22.
doi: 10.1167/iovs.17-23230
Murueta-Goyena A, Del Pino R, Reyero P, Galdós M, Arana B, Lucas-Jiménez O, et al. Parafoveal thinning of inner retina is associated with visual dysfunction in Lewy body diseases. Mov Disord. 2019;34:1315–24.
doi: 10.1002/mds.27728
Cerveró A, Casado A, Riancho J. Retinal changes in amyotrophic lateral sclerosis: looking at the disease through a new window. J Neurol. 2021;268:2083–9.
doi: 10.1007/s00415-019-09654-w
Kersten HM, Danesh-Meyer HV, Kilfoyle DH, Roxburgh RH. Optical coherence tomography findings in Huntington’s disease: a potential biomarker of disease progression. J Neurol. 2015;262:2457–65.
doi: 10.1007/s00415-015-7869-2
Nouri MN, Yeh EA. Neuroinflammatory and demyelinating disorders of childhood. Clin Child Neurol. 2020:651–77.
Malani Shukla N, Lotze TE, Muscal E. Inflammatory diseases of the central nervous system. Neurol Clin. 2021;39:811–28.
doi: 10.1016/j.ncl.2021.04.004
Twilt M, Benseler SM. Childhood inflammatory brain diseases: pathogenesis, diagnosis and therapy. Rheumatol. 2014;53:1359–68.
doi: 10.1093/rheumatology/ket398
Balcer LJ, Raynowska J, Nolan R, Galetta SL, Kapoor R, Benedict R, et al. Validity of low-contrast letter acuity as a visual performance outcome measure for multiple sclerosis. Mult Scler. 2017;23:734–47.
doi: 10.1177/1352458517690822

Auteurs

Stela Vujosevic (S)

Department of Biomedical, Surgical and Dental Sciences, University of Milan, Milan, Italy. stela.vujosevic@unimi.it.
Eye Clinic, IRCCS MultiMedica, Milan, Italy. stela.vujosevic@unimi.it.

M Margarita Parra (MM)

Department of Ophthalmology and Visual Sciences, John A. Moran Eye Center, University of Utah, Salt Lake City, UT, USA.

M Elizabeth Hartnett (ME)

Department of Ophthalmology and Visual Sciences, John A. Moran Eye Center, University of Utah, Salt Lake City, UT, USA.

Louise O'Toole (L)

Department of Ophthalmology Mater Private Network, Dublin, Ireland.

Alessia Nuzzi (A)

Eye Clinic, IRCCS MultiMedica, Milan, Italy.
University of Milan, Milan, Italy.

Celeste Limoli (C)

Eye Clinic, IRCCS MultiMedica, Milan, Italy.
University of Milan, Milan, Italy.

Edoardo Villani (E)

Eye Clinic, IRCCS MultiMedica, Milan, Italy.
Department of Clinical Sciences and Community Health, University of Milan, Milan, Italy.

Paolo Nucci (P)

Department of Biomedical, Surgical and Dental Sciences, University of Milan, Milan, Italy.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH