Skip to main content
Top

Open Access 05-11-2024 | Multiple Sclerosis | REVIEW

Barriers in Healthcare to the Use of Optical Coherence Tomography Angiography in Multiple Sclerosis

Authors: Lukas G. Reeß, Hadi Salih, Murat Delikaya, Friedemann Paul, Frederike Cosima Oertel

Published in: Neurology and Therapy

Login to get access

Abstract

Optical coherence tomography angiography (OCT-A) is a state-of-the-art imaging technique for the retinal vasculature to accurately segment the capillary network and assign it to retinal layers. OCT-A is a promising technique to better understand neurological diseases with visual system manifestations, such as multiple sclerosis (MS), and to identify and characterize vascular biomarkers. Initial studies suggested vascular changes in MS and its differential diagnoses such as myelin oligodendrocyte glycoprotein antibody-associated disease (MOGAD) and neuromyelitis optica spectrum disorder (NMOSD). Here we review clinical and technical aspects of OCT-A imaging and discuss the potential for the MS field as well as barriers that need to be overcome before OCT-A can be established in clinical application.
Literature
1.
go back to reference Walton C, King R, Rechtman L, Kaye W, Leray E, Marrie RA, et al. Rising prevalence of multiple sclerosis worldwide: insights from the Atlas of MS, third edition. Mult Scler. 2020;26(14):1816–21. Walton C, King R, Rechtman L, Kaye W, Leray E, Marrie RA, et al. Rising prevalence of multiple sclerosis worldwide: insights from the Atlas of MS, third edition. Mult Scler. 2020;26(14):1816–21.
2.
go back to reference Kuhlmann T, Moccia M, Coetzee T, Cohen JA, Correale J, Graves J, et al. Time for a new mechanism-driven framework to define multiple sclerosis progression. Lancet Neurol. 2023;22(1):78–88.PubMedCrossRef Kuhlmann T, Moccia M, Coetzee T, Cohen JA, Correale J, Graves J, et al. Time for a new mechanism-driven framework to define multiple sclerosis progression. Lancet Neurol. 2023;22(1):78–88.PubMedCrossRef
3.
go back to reference Abdelhak A, Benkert P, Schaedelin S, Boscardin WJ, Cordano C, Oechtering J, et al. Neurofilament light chain elevation and disability progression in multiple sclerosis. JAMA Neurol. 2023;80(12):1317–25.PubMedCrossRef Abdelhak A, Benkert P, Schaedelin S, Boscardin WJ, Cordano C, Oechtering J, et al. Neurofilament light chain elevation and disability progression in multiple sclerosis. JAMA Neurol. 2023;80(12):1317–25.PubMedCrossRef
4.
go back to reference Kappos L, Wolinsky JS, Giovannoni G, Arnold DL, Wang Q, Bernasconi C, et al. Contribution of relapse-independent progression vs relapse-associated worsening to overall confirmed disability accumulation in typical relapsing multiple sclerosis in a pooled analysis of 2 randomized clinical trials. JAMA Neurol. 2020;77(9):1132–40.PubMedCrossRef Kappos L, Wolinsky JS, Giovannoni G, Arnold DL, Wang Q, Bernasconi C, et al. Contribution of relapse-independent progression vs relapse-associated worsening to overall confirmed disability accumulation in typical relapsing multiple sclerosis in a pooled analysis of 2 randomized clinical trials. JAMA Neurol. 2020;77(9):1132–40.PubMedCrossRef
5.
go back to reference Tur C, Rocca MA. Progression independent of relapse activity in multiple sclerosis. Neurology. 2024;102(1): e207936.PubMedCrossRef Tur C, Rocca MA. Progression independent of relapse activity in multiple sclerosis. Neurology. 2024;102(1): e207936.PubMedCrossRef
6.
go back to reference Tur C, Carbonell-Mirabent P, Cobo-Calvo Á, Otero-Romero S, Arrambide G, Midaglia L, et al. Association of early progression independent of relapse activity with long-term disability after a first demyelinating event in multiple sclerosis. JAMA Neurol. 2023;80(2):151–60.PubMedCrossRef Tur C, Carbonell-Mirabent P, Cobo-Calvo Á, Otero-Romero S, Arrambide G, Midaglia L, et al. Association of early progression independent of relapse activity with long-term disability after a first demyelinating event in multiple sclerosis. JAMA Neurol. 2023;80(2):151–60.PubMedCrossRef
7.
go back to reference 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(10):797–812.PubMedCrossRef 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(10):797–812.PubMedCrossRef
8.
go back to reference Heesen C, Haase R, Melzig S, Poettgen J, Berghoff M, Paul F, et al. Perceptions on the value of bodily functions in multiple sclerosis. Acta Neurol Scand. 2018;137(3):356–62.PubMedCrossRef Heesen C, Haase R, Melzig S, Poettgen J, Berghoff M, Paul F, et al. Perceptions on the value of bodily functions in multiple sclerosis. Acta Neurol Scand. 2018;137(3):356–62.PubMedCrossRef
9.
go back to reference Mowry EM, Loguidice MJ, Daniels AB, Jacobs DA, Markowitz CE, Galetta SL, et al. Vision related quality of life in multiple sclerosis: correlation with new measures of low and high contrast letter acuity. J Neurol Neurosurg Psychiatry. 2009;80(7):767–72.PubMedCrossRef Mowry EM, Loguidice MJ, Daniels AB, Jacobs DA, Markowitz CE, Galetta SL, et al. Vision related quality of life in multiple sclerosis: correlation with new measures of low and high contrast letter acuity. J Neurol Neurosurg Psychiatry. 2009;80(7):767–72.PubMedCrossRef
10.
go back to reference Schinzel J, Zimmermann H, Paul F, Ruprecht K, Hahn K, Brandt AU, et al. Relations of low contrast visual acuity, quality of life and multiple sclerosis functional composite: a cross-sectional analysis. BMC Neurol. 2014;14(1):31.PubMedPubMedCentralCrossRef Schinzel J, Zimmermann H, Paul F, Ruprecht K, Hahn K, Brandt AU, et al. Relations of low contrast visual acuity, quality of life and multiple sclerosis functional composite: a cross-sectional analysis. BMC Neurol. 2014;14(1):31.PubMedPubMedCentralCrossRef
11.
go back to reference Wingerchuk DM, Banwell B, Bennett JL, Cabre P, Carroll W, Chitnis T, et al. International consensus diagnostic criteria for neuromyelitis optica spectrum disorders. Neurology. 2015;85(2):177–89.PubMedPubMedCentralCrossRef Wingerchuk DM, Banwell B, Bennett JL, Cabre P, Carroll W, Chitnis T, et al. International consensus diagnostic criteria for neuromyelitis optica spectrum disorders. Neurology. 2015;85(2):177–89.PubMedPubMedCentralCrossRef
12.
go back to reference Dumrikarnlert C, Siritho S, Chulapimphan P, Ngamsombat C, Satukijchai C, Prayoonwiwat N. The characteristics of spinal imaging in different types of demyelinating diseases. J Neurol Sci. 2017;372:138–43.PubMedCrossRef Dumrikarnlert C, Siritho S, Chulapimphan P, Ngamsombat C, Satukijchai C, Prayoonwiwat N. The characteristics of spinal imaging in different types of demyelinating diseases. J Neurol Sci. 2017;372:138–43.PubMedCrossRef
13.
go back to reference Bartels F, Lu A, Oertel FC, Finke C, Paul F, Chien C. Clinical and neuroimaging findings in MOGAD–MRI and OCT. Clin Exp Immunol Dezember. 2021;206(3):266–81.CrossRef Bartels F, Lu A, Oertel FC, Finke C, Paul F, Chien C. Clinical and neuroimaging findings in MOGAD–MRI and OCT. Clin Exp Immunol Dezember. 2021;206(3):266–81.CrossRef
14.
go back to reference Banwell B, Bennett JL, Marignier R, Kim HJ, Brilot F, Flanagan EP, et al. Diagnosis of myelin oligodendrocyte glycoprotein antibody-associated disease: International MOGAD Panel proposed criteria. Lancet Neurol. 2023;22(3):268–82.PubMedCrossRef Banwell B, Bennett JL, Marignier R, Kim HJ, Brilot F, Flanagan EP, et al. Diagnosis of myelin oligodendrocyte glycoprotein antibody-associated disease: International MOGAD Panel proposed criteria. Lancet Neurol. 2023;22(3):268–82.PubMedCrossRef
15.
go back to reference Ramanathan S, Prelog K, Barnes EH, Tantsis EM, Reddel SW, Henderson AP, et al. Radiological differentiation of optic neuritis with myelin oligodendrocyte glycoprotein antibodies, aquaporin-4 antibodies, and multiple sclerosis. Mult Scler J. 2016;22(4):470–82.CrossRef Ramanathan S, Prelog K, Barnes EH, Tantsis EM, Reddel SW, Henderson AP, et al. Radiological differentiation of optic neuritis with myelin oligodendrocyte glycoprotein antibodies, aquaporin-4 antibodies, and multiple sclerosis. Mult Scler J. 2016;22(4):470–82.CrossRef
16.
go back to reference Lin TY, Chien C, Lu A, Paul F, Zimmermann HG. Retinal optical coherence tomography and magnetic resonance imaging in neuromyelitis optica spectrum disorders and MOG-antibody associated disorders: an updated review. Expert Rev Neurother. 2021;21(10):1101–23.PubMedCrossRef Lin TY, Chien C, Lu A, Paul F, Zimmermann HG. Retinal optical coherence tomography and magnetic resonance imaging in neuromyelitis optica spectrum disorders and MOG-antibody associated disorders: an updated review. Expert Rev Neurother. 2021;21(10):1101–23.PubMedCrossRef
17.
go back to reference Cortese R, Prados Carrasco F, Tur C, Bianchi A, Brownlee W, De Angelis F, et al. Differentiating multiple sclerosis from AQP4-neuromyelitis optica spectrum disorder and MOG-antibody disease with imaging. Neurology. 2023;100(3):e308–23.PubMedPubMedCentralCrossRef Cortese R, Prados Carrasco F, Tur C, Bianchi A, Brownlee W, De Angelis F, et al. Differentiating multiple sclerosis from AQP4-neuromyelitis optica spectrum disorder and MOG-antibody disease with imaging. Neurology. 2023;100(3):e308–23.PubMedPubMedCentralCrossRef
18.
go back to reference Wilf-Yarkoni A, Zmira O, Tolkovsky A, Pflantzer B, Gofrit SG, Kleffner I, et al. Clinical characterization and ancillary tests in Susac syndrome. Neurol Neuroimmunol Neuroinflammation. 2024;11(3): e200209.CrossRef Wilf-Yarkoni A, Zmira O, Tolkovsky A, Pflantzer B, Gofrit SG, Kleffner I, et al. Clinical characterization and ancillary tests in Susac syndrome. Neurol Neuroimmunol Neuroinflammation. 2024;11(3): e200209.CrossRef
19.
go back to reference Petzold A, Fraser CL, Abegg M, Alroughani R, Alshowaeir D, Alvarenga R, et al. Diagnosis and classification of optic neuritis. Lancet Neurol. 2022;21(12):1120–34.PubMedCrossRef Petzold A, Fraser CL, Abegg M, Alroughani R, Alshowaeir D, Alvarenga R, et al. Diagnosis and classification of optic neuritis. Lancet Neurol. 2022;21(12):1120–34.PubMedCrossRef
20.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
21.
go back to reference Brandt AU, Martinez-Lapiscina EH, Nolan R, Saidha S. Monitoring the course of MS with optical coherence tomography. Curr Treat Options Neurol. 2017;19(4):15.PubMedCrossRef Brandt AU, Martinez-Lapiscina EH, Nolan R, Saidha S. Monitoring the course of MS with optical coherence tomography. Curr Treat Options Neurol. 2017;19(4):15.PubMedCrossRef
22.
go back to reference Yu DY, Cringle SJ, Yu PK, Balaratnasingam C, Mehnert A, Sarunic MV, et al. Retinal capillary perfusion: spatial and temporal heterogeneity. Prog Retin Eye Res. 2019;70:23–54.PubMedCrossRef Yu DY, Cringle SJ, Yu PK, Balaratnasingam C, Mehnert A, Sarunic MV, et al. Retinal capillary perfusion: spatial and temporal heterogeneity. Prog Retin Eye Res. 2019;70:23–54.PubMedCrossRef
23.
go back to reference Kallab M, Hommer N, Schlatter A, Bsteh G, Altmann P, Popa-Cherecheanu A, et al. Retinal oxygen metabolism and haemodynamics in patients with multiple sclerosis and history of optic neuritis. Front Neurosci. 2021;15: 761654.PubMedPubMedCentralCrossRef Kallab M, Hommer N, Schlatter A, Bsteh G, Altmann P, Popa-Cherecheanu A, et al. Retinal oxygen metabolism and haemodynamics in patients with multiple sclerosis and history of optic neuritis. Front Neurosci. 2021;15: 761654.PubMedPubMedCentralCrossRef
24.
go back to reference D’haeseleer M, Cambron M, Vanopdenbosch L, De Keyser J. Vascular aspects of multiple sclerosis. Lancet Neurol. 2011;10(7):657–66.PubMedCrossRef D’haeseleer M, Cambron M, Vanopdenbosch L, De Keyser J. Vascular aspects of multiple sclerosis. Lancet Neurol. 2011;10(7):657–66.PubMedCrossRef
25.
go back to reference Green AJ, Cree BC. Distinctive retinal nerve fibre layer and vascular changes in neuromyelitis optica following optic neuritis. J Neurol Neurosurg Psychiatry. 2009;80(9):1002–5.PubMedCrossRef Green AJ, Cree BC. Distinctive retinal nerve fibre layer and vascular changes in neuromyelitis optica following optic neuritis. J Neurol Neurosurg Psychiatry. 2009;80(9):1002–5.PubMedCrossRef
26.
go back to reference Goldenberg D, Shahar J, Loewenstein A, Goldstein M. Diameters of retinal blood vessels in a healthy cohort as measured by spectral domain optical coherence tomography. Retina. 2013;33(9):1888.PubMedCrossRef Goldenberg D, Shahar J, Loewenstein A, Goldstein M. Diameters of retinal blood vessels in a healthy cohort as measured by spectral domain optical coherence tomography. Retina. 2013;33(9):1888.PubMedCrossRef
27.
go back to reference Tan PEZ, Yu PK, Balaratnasingam C, Cringle SJ, Morgan WH, McAllister IL, et al. Quantitative confocal imaging of the retinal microvasculature in the human retina. Invest Ophthalmol Vis Sci. 2012;53(9):5728–36.PubMedCrossRef Tan PEZ, Yu PK, Balaratnasingam C, Cringle SJ, Morgan WH, McAllister IL, et al. Quantitative confocal imaging of the retinal microvasculature in the human retina. Invest Ophthalmol Vis Sci. 2012;53(9):5728–36.PubMedCrossRef
28.
go back to reference Cui Y, Zhu Y, Wang JC, Lu Y, Zeng R, Katz R, et al. Comparison of widefield swept-source optical coherence tomography angiography with ultra-widefield color fundus photography and fluorescein angiography for detection of lesions in diabetic retinopathy. Br J Ophthalmol. 2021;105(4):577–81.PubMedCrossRef Cui Y, Zhu Y, Wang JC, Lu Y, Zeng R, Katz R, et al. Comparison of widefield swept-source optical coherence tomography angiography with ultra-widefield color fundus photography and fluorescein angiography for detection of lesions in diabetic retinopathy. Br J Ophthalmol. 2021;105(4):577–81.PubMedCrossRef
30.
go back to reference Kreitner L, Paetzold JC, Rauch N, Chen C, Hagag AM, Fayed AE, et al. Synthetic optical coherence tomography angiographs for detailed retinal vessel segmentation without human annotations. IEEE Trans Med Imaging. 2024;43(6):2061–73. Kreitner L, Paetzold JC, Rauch N, Chen C, Hagag AM, Fayed AE, et al. Synthetic optical coherence tomography angiographs for detailed retinal vessel segmentation without human annotations. IEEE Trans Med Imaging. 2024;43(6):2061–73.
31.
go back to reference Yu X, Ge C, Aziz MZ, Li M, Shum PP, Liu L, et al. CGNet-assisted automatic vessel segmentation for optical coherence tomography angiography. J Biophotonics. 2022;15(10): e202200067.PubMedCrossRef Yu X, Ge C, Aziz MZ, Li M, Shum PP, Liu L, et al. CGNet-assisted automatic vessel segmentation for optical coherence tomography angiography. J Biophotonics. 2022;15(10): e202200067.PubMedCrossRef
32.
go back to reference Ma Y, Hao H, Xie J, Fu H, Zhang J, Yang J, et al. ROSE: a retinal OCT-angiography vessel segmentation dataset and new model. IEEE Trans Med Imaging. 2021;40(3):928–39.PubMedCrossRef Ma Y, Hao H, Xie J, Fu H, Zhang J, Yang J, et al. ROSE: a retinal OCT-angiography vessel segmentation dataset and new model. IEEE Trans Med Imaging. 2021;40(3):928–39.PubMedCrossRef
33.
go back to reference Giarratano Y, Bianchi E, Gray C, Morris A, MacGillivray T, Dhillon B, et al. Automated segmentation of optical coherence tomography angiography images: benchmark data and clinically relevant metrics. Transl Vis Sci Technol. 2020;9(13):5.PubMedPubMedCentralCrossRef Giarratano Y, Bianchi E, Gray C, Morris A, MacGillivray T, Dhillon B, et al. Automated segmentation of optical coherence tomography angiography images: benchmark data and clinically relevant metrics. Transl Vis Sci Technol. 2020;9(13):5.PubMedPubMedCentralCrossRef
34.
go back to reference Spaide RF, Klancnik JM Jr, Cooney MJ. Retinal vascular layers imaged by fluorescein angiography and optical coherence tomography angiography. JAMA Ophthalmol. 2015;133(1):45–50.PubMedCrossRef Spaide RF, Klancnik JM Jr, Cooney MJ. Retinal vascular layers imaged by fluorescein angiography and optical coherence tomography angiography. JAMA Ophthalmol. 2015;133(1):45–50.PubMedCrossRef
35.
go back to reference Feucht N, Maier M, Lepennetier G, Pettenkofer M, Wetzlmair C, Daltrozzo T, et al. Optical coherence tomography angiography indicates associations of the retinal vascular network and disease activity in multiple sclerosis. Mult Scler J. 2019;25(2):224–34.CrossRef Feucht N, Maier M, Lepennetier G, Pettenkofer M, Wetzlmair C, Daltrozzo T, et al. Optical coherence tomography angiography indicates associations of the retinal vascular network and disease activity in multiple sclerosis. Mult Scler J. 2019;25(2):224–34.CrossRef
36.
go back to reference Farci R, Carta A, Cocco E, Frau J, Fossarello M, Diaz G. Optical coherence tomography angiography in multiple sclerosis: a cross-sectional study. PLOS ONE. 2020;15(7): e0236090. Farci R, Carta A, Cocco E, Frau J, Fossarello M, Diaz G. Optical coherence tomography angiography in multiple sclerosis: a cross-sectional study. PLOS ONE. 2020;15(7): e0236090.
37.
go back to reference Murphy OC, Kwakyi O, Iftikhar M, Zafar S, Lambe J, Pellegrini N, et al. Alterations in the retinal vasculature occur in multiple sclerosis and exhibit novel correlations with disability and visual function measures. Mult Scler. 2020;26(7):815–28. Murphy OC, Kwakyi O, Iftikhar M, Zafar S, Lambe J, Pellegrini N, et al. Alterations in the retinal vasculature occur in multiple sclerosis and exhibit novel correlations with disability and visual function measures. Mult Scler. 2020;26(7):815–28.
38.
go back to reference Bostan M, Chua J, Sim YC, Tan B, Bujor I, Wong D, et al. Microvascular changes in the macular and parafoveal areas of multiple sclerosis patients without optic neuritis. Sci Rep. 2022;12(1):1–12.CrossRef Bostan M, Chua J, Sim YC, Tan B, Bujor I, Wong D, et al. Microvascular changes in the macular and parafoveal areas of multiple sclerosis patients without optic neuritis. Sci Rep. 2022;12(1):1–12.CrossRef
39.
go back to reference Liu J, Song S, Gu X, Li H, Yu X. Microvascular impairments detected by optical coherence tomography angiography in multiple sclerosis patients: a systematic review and meta-analysis. Front Neurosci. 2023;16:1121899.PubMedPubMedCentralCrossRef Liu J, Song S, Gu X, Li H, Yu X. Microvascular impairments detected by optical coherence tomography angiography in multiple sclerosis patients: a systematic review and meta-analysis. Front Neurosci. 2023;16:1121899.PubMedPubMedCentralCrossRef
40.
go back to reference Cordon B, Vilades E, Orduna E, Satue M, Perez-Velilla J, Sebastian B, et al. Angiography with optical coherence tomography as a biomarker in multiple sclerosis. PLOS ONE. 2020;15(12): e0243236. Cordon B, Vilades E, Orduna E, Satue M, Perez-Velilla J, Sebastian B, et al. Angiography with optical coherence tomography as a biomarker in multiple sclerosis. PLOS ONE. 2020;15(12): e0243236.
41.
go back to reference Fursova AZ, Zubkova MY, Vasilyeva MA, Karlash YA, Derbeneva AS. Optical coherence tomography angiography in the diagnosis of multiple sclerosis. Vestn Oftalmol. 2024;140(2):63–70.PubMedCrossRef Fursova AZ, Zubkova MY, Vasilyeva MA, Karlash YA, Derbeneva AS. Optical coherence tomography angiography in the diagnosis of multiple sclerosis. Vestn Oftalmol. 2024;140(2):63–70.PubMedCrossRef
42.
go back to reference Aly L, Noll C, Wicklein R, Wolf E, Romahn EF, Wauschkuhn J, et al. Dynamics of retinal vessel loss after acute optic neuritis in patients with relapsing multiple sclerosis. Neurol Neuroimmunol Neuroinflammation. 2022;9(3): e1159.CrossRef Aly L, Noll C, Wicklein R, Wolf E, Romahn EF, Wauschkuhn J, et al. Dynamics of retinal vessel loss after acute optic neuritis in patients with relapsing multiple sclerosis. Neurol Neuroimmunol Neuroinflammation. 2022;9(3): e1159.CrossRef
43.
go back to reference Lanzillo R, Cennamo G, Criscuolo C, Carotenuto A, Velotti N, Sparnelli F, et al. Optical coherence tomography angiography retinal vascular network assessment in multiple sclerosis. Mult Scler. 2018;24(13):1706–14. Lanzillo R, Cennamo G, Criscuolo C, Carotenuto A, Velotti N, Sparnelli F, et al. Optical coherence tomography angiography retinal vascular network assessment in multiple sclerosis. Mult Scler. 2018;24(13):1706–14.
44.
go back to reference Wang X, Jia Y, Spain R, Potsaid B, Liu JJ, Baumann B, et al. Optical coherence tomography angiography of optic nerve head and parafovea in multiple sclerosis. Br J Ophthalmol. 2014;98(10):1368–73.PubMedCrossRef Wang X, Jia Y, Spain R, Potsaid B, Liu JJ, Baumann B, et al. Optical coherence tomography angiography of optic nerve head and parafovea in multiple sclerosis. Br J Ophthalmol. 2014;98(10):1368–73.PubMedCrossRef
45.
go back to reference Jiang H, Gameiro GR, Liu Y, Lin Y, Jeffrey H, Deng Y, et al. Visual function and disability are associated with increased retinal volumetric vessel density in patients with multiple sclerosis. Am J Ophthalmol. 2020;213:34–45.PubMedPubMedCentralCrossRef Jiang H, Gameiro GR, Liu Y, Lin Y, Jeffrey H, Deng Y, et al. Visual function and disability are associated with increased retinal volumetric vessel density in patients with multiple sclerosis. Am J Ophthalmol. 2020;213:34–45.PubMedPubMedCentralCrossRef
46.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
47.
go back to reference Tiftikcioglu BI, Emre S, Idiman F, Idiman E. Optical coherence tomography angiography (OCTA) in differential diagnosis of aquaporin-4 antibody seronegative NMOSD and multiple sclerosis. Mult Scler Relat Disord. 2022;58: 103503.PubMedCrossRef Tiftikcioglu BI, Emre S, Idiman F, Idiman E. Optical coherence tomography angiography (OCTA) in differential diagnosis of aquaporin-4 antibody seronegative NMOSD and multiple sclerosis. Mult Scler Relat Disord. 2022;58: 103503.PubMedCrossRef
48.
go back to reference Rogaczewska M, Michalak S, Stopa M. Optical coherence tomography angiography of peripapillary vessel density in multiple sclerosis and neuromyelitis optica spectrum disorder: a comparative study. J Clin Med. 2021;10(4):609.PubMedPubMedCentralCrossRef Rogaczewska M, Michalak S, Stopa M. Optical coherence tomography angiography of peripapillary vessel density in multiple sclerosis and neuromyelitis optica spectrum disorder: a comparative study. J Clin Med. 2021;10(4):609.PubMedPubMedCentralCrossRef
49.
go back to reference Jarius S, Paul F, Weinshenker BG, Levy M, Kim HJ, Wildemann B. Neuromyelitis optica. Nat Rev Dis Primer. 2020;6(1):1–32. Jarius S, Paul F, Weinshenker BG, Levy M, Kim HJ, Wildemann B. Neuromyelitis optica. Nat Rev Dis Primer. 2020;6(1):1–32.
51.
go back to reference Filosa JA, Morrison HW, Iddings JA, Du W, Kim KJ. Beyond neurovascular coupling, role of astrocytes in the regulation of vascular tone. Neuroscience. 2016;323:96–109.PubMedCrossRef Filosa JA, Morrison HW, Iddings JA, Du W, Kim KJ. Beyond neurovascular coupling, role of astrocytes in the regulation of vascular tone. Neuroscience. 2016;323:96–109.PubMedCrossRef
52.
go back to reference Yu J, Huang Y, Quan C, Zhou L, ZhangBao J, Wu K, et al. Alterations in the retinal vascular network and structure in MOG antibody-associated disease: an optical coherence tomography angiography study. J Neuroophthalmol. 2021;41(4): e424.PubMedCrossRef Yu J, Huang Y, Quan C, Zhou L, ZhangBao J, Wu K, et al. Alterations in the retinal vascular network and structure in MOG antibody-associated disease: an optical coherence tomography angiography study. J Neuroophthalmol. 2021;41(4): e424.PubMedCrossRef
53.
go back to reference Ringelstein M, Albrecht P, Kleffner I, Bühn B, Harmel J, Müller AK, et al. Retinal pathology in Susac syndrome detected by spectral-domain optical coherence tomography. Neurology. 2015;85(7):610–8.PubMedCrossRef Ringelstein M, Albrecht P, Kleffner I, Bühn B, Harmel J, Müller AK, et al. Retinal pathology in Susac syndrome detected by spectral-domain optical coherence tomography. Neurology. 2015;85(7):610–8.PubMedCrossRef
54.
go back to reference Alba-Linero C, Liscombe-Sepúlveda JP, Llorenç V, GiraltJosa J, Adán A. Use of ultra-wide field retinal imaging and optical coherence tomography angiography in the diagnosis of incomplete Susac syndrome. Eur J Ophthalmol. 2021;31(6):3238–47.PubMedCrossRef Alba-Linero C, Liscombe-Sepúlveda JP, Llorenç V, GiraltJosa J, Adán A. Use of ultra-wide field retinal imaging and optical coherence tomography angiography in the diagnosis of incomplete Susac syndrome. Eur J Ophthalmol. 2021;31(6):3238–47.PubMedCrossRef
55.
go back to reference Mastropasqua R, Toto L, Senatore A, D’Uffizi A, Neri P, Mariotti C, et al. Optical coherence tomography angiography findings in Susac’s syndrome: a case report. Int Ophthalmol. 2018;38(4):1803–8.PubMedCrossRef Mastropasqua R, Toto L, Senatore A, D’Uffizi A, Neri P, Mariotti C, et al. Optical coherence tomography angiography findings in Susac’s syndrome: a case report. Int Ophthalmol. 2018;38(4):1803–8.PubMedCrossRef
56.
go back to reference Cerquaglia A, Iaccheri B, Fiore T, Fruttini D, Belli FB, Khairallah M, et al. New insights on ocular sarcoidosis: an optical coherence tomography angiography study. Ocul Immunol Inflamm. 2019;27(7):1057–66.PubMedCrossRef Cerquaglia A, Iaccheri B, Fiore T, Fruttini D, Belli FB, Khairallah M, et al. New insights on ocular sarcoidosis: an optical coherence tomography angiography study. Ocul Immunol Inflamm. 2019;27(7):1057–66.PubMedCrossRef
57.
go back to reference Yang QC, Yao F, Li QY, Chen MJ, Zhang LJ, Shu HY, et al. Ocular microvascular alteration in Sjögren syndrome. Quant Imaging Med Surg. 2022;12(2):1324–35.PubMedPubMedCentralCrossRef Yang QC, Yao F, Li QY, Chen MJ, Zhang LJ, Shu HY, et al. Ocular microvascular alteration in Sjögren syndrome. Quant Imaging Med Surg. 2022;12(2):1324–35.PubMedPubMedCentralCrossRef
58.
go back to reference Fernandes EA, Wildner P, Oset M, Siger M, Stasiołek M, Matysiak M, et al. Optical coherence tomography angiography as a potential tool in differential diagnosis of multiple sclerosis and rheumatic disorders with central nervous system involvement. Int Ophthalmol. 2024;44(1):281.PubMedPubMedCentralCrossRef Fernandes EA, Wildner P, Oset M, Siger M, Stasiołek M, Matysiak M, et al. Optical coherence tomography angiography as a potential tool in differential diagnosis of multiple sclerosis and rheumatic disorders with central nervous system involvement. Int Ophthalmol. 2024;44(1):281.PubMedPubMedCentralCrossRef
59.
go back to reference Castillo L, Berrozpe-Villabona C, Miserachs-García S, Haulani H, Gómez-Gutiérrez C, Díaz-García RS, et al. Quantitative assessment of macular and circumpapillary retinal vessel density across all stages of Leber hereditary optic neuropathy using swept source optical coherence tomography angiography. Acta Ophthalmol (Copenh). 2022;100(8):e1646–56.CrossRef Castillo L, Berrozpe-Villabona C, Miserachs-García S, Haulani H, Gómez-Gutiérrez C, Díaz-García RS, et al. Quantitative assessment of macular and circumpapillary retinal vessel density across all stages of Leber hereditary optic neuropathy using swept source optical coherence tomography angiography. Acta Ophthalmol (Copenh). 2022;100(8):e1646–56.CrossRef
60.
go back to reference Balducci N, Cascavilla ML, Ciardella A, La Morgia C, Triolo G, Parisi V, et al. Peripapillary vessel density changes in Leber’s hereditary optic neuropathy: a new biomarker. Clin Exp Ophthalmol. 2018;46(9):1055–62.PubMedCrossRef Balducci N, Cascavilla ML, Ciardella A, La Morgia C, Triolo G, Parisi V, et al. Peripapillary vessel density changes in Leber’s hereditary optic neuropathy: a new biomarker. Clin Exp Ophthalmol. 2018;46(9):1055–62.PubMedCrossRef
61.
go back to reference Li X, Yu Y, Liu X, Shi Y, Jin X, Zhang Y, et al. Quantitative analysis of retinal vessel density and thickness changes in diabetes mellitus evaluated using optical coherence tomography angiography: a cross-sectional study. BMC Ophthalmol. 2021;21:259.PubMedPubMedCentralCrossRef Li X, Yu Y, Liu X, Shi Y, Jin X, Zhang Y, et al. Quantitative analysis of retinal vessel density and thickness changes in diabetes mellitus evaluated using optical coherence tomography angiography: a cross-sectional study. BMC Ophthalmol. 2021;21:259.PubMedPubMedCentralCrossRef
62.
go back to reference Zhang B, Chou Y, Zhao X, Yang J, Chen Y. Early detection of microvascular impairments with optical coherence tomography angiography in diabetic patients without clinical retinopathy: a meta-analysis. Am J Ophthalmol. 2021;222:226–37.PubMedCrossRef Zhang B, Chou Y, Zhao X, Yang J, Chen Y. Early detection of microvascular impairments with optical coherence tomography angiography in diabetic patients without clinical retinopathy: a meta-analysis. Am J Ophthalmol. 2021;222:226–37.PubMedCrossRef
63.
64.
go back to reference Vujosevic S, Limoli C, Piccoli G, Costanzo E, Marenzi E, Torti E, et al. A gender-based analysis of retinal microvascular alterations in patients with diabetes mellitus using OCT angiography. J Diabetes Complicat. 2024;38(10): 108852.CrossRef Vujosevic S, Limoli C, Piccoli G, Costanzo E, Marenzi E, Torti E, et al. A gender-based analysis of retinal microvascular alterations in patients with diabetes mellitus using OCT angiography. J Diabetes Complicat. 2024;38(10): 108852.CrossRef
65.
go back to reference Dan AO, Mocanu CL, Bălășoiu AT, Tănasie CA, Puiu I, Târtea AE, et al. Correlations between retinal microvascular parameters and clinical parameters in young patients with type 1 diabetes mellitus: an optical coherence tomography angiography study. Diagnostics. 2024;14(3):317.PubMedPubMedCentralCrossRef Dan AO, Mocanu CL, Bălășoiu AT, Tănasie CA, Puiu I, Târtea AE, et al. Correlations between retinal microvascular parameters and clinical parameters in young patients with type 1 diabetes mellitus: an optical coherence tomography angiography study. Diagnostics. 2024;14(3):317.PubMedPubMedCentralCrossRef
66.
go back to reference Zeng R, Garg I, Bannai D, Kasetty M, Katz R, Park JY, et al. Retinal microvasculature and vasoreactivity changes in hypertension using optical coherence tomography-angiography. Graefes Arch Clin Exp Ophthalmol. 2022;260(11):3505–15.PubMedCrossRef Zeng R, Garg I, Bannai D, Kasetty M, Katz R, Park JY, et al. Retinal microvasculature and vasoreactivity changes in hypertension using optical coherence tomography-angiography. Graefes Arch Clin Exp Ophthalmol. 2022;260(11):3505–15.PubMedCrossRef
67.
go back to reference Sun C, Ladores C, Hong J, Nguyen DQ, Chua J, Ting D, et al. Systemic hypertension associated retinal microvascular changes can be detected with optical coherence tomography angiography. Sci Rep. 2020;10(1):9580.PubMedPubMedCentralCrossRef Sun C, Ladores C, Hong J, Nguyen DQ, Chua J, Ting D, et al. Systemic hypertension associated retinal microvascular changes can be detected with optical coherence tomography angiography. Sci Rep. 2020;10(1):9580.PubMedPubMedCentralCrossRef
68.
go back to reference Shin YI, Nam KY, Lee WH, Ryu CK, Lim HB, Jo YJ, et al. Peripapillary microvascular changes in patients with systemic hypertension: an optical coherence tomography angiography study. Sci Rep. 2020;10(1):6541.PubMedPubMedCentralCrossRef Shin YI, Nam KY, Lee WH, Ryu CK, Lim HB, Jo YJ, et al. Peripapillary microvascular changes in patients with systemic hypertension: an optical coherence tomography angiography study. Sci Rep. 2020;10(1):6541.PubMedPubMedCentralCrossRef
69.
go back to reference Remolí Sargues L, Monferrer Adsuara C, Castro Navarro V, Navarro Palop C, Montero Hernández J, Cervera TE. Swept-source optical coherence tomography angiography automatic analysis of microvascular changes secondary to systemic hypertension. Eur J Ophthalmol. 2023;33(3):1452–8.PubMedCrossRef Remolí Sargues L, Monferrer Adsuara C, Castro Navarro V, Navarro Palop C, Montero Hernández J, Cervera TE. Swept-source optical coherence tomography angiography automatic analysis of microvascular changes secondary to systemic hypertension. Eur J Ophthalmol. 2023;33(3):1452–8.PubMedCrossRef
70.
go back to reference Sung JY, Lee KH, Jun JH, Lee MW. Changes in peripapillary microvasculature in patients with type 2 diabetes patients: effect of systemic hypertension. Sci Rep. 2023;13(1):19459.PubMedPubMedCentralCrossRef Sung JY, Lee KH, Jun JH, Lee MW. Changes in peripapillary microvasculature in patients with type 2 diabetes patients: effect of systemic hypertension. Sci Rep. 2023;13(1):19459.PubMedPubMedCentralCrossRef
71.
go back to reference Liu X, Lai S, Ma S, Yang H, Liu L, Yu G, et al. Development of a novel retina-based diagnostic score for early detection of major depressive disorder: an interdisciplinary view. Front Psychiatry. 2022;13: 897759. Liu X, Lai S, Ma S, Yang H, Liu L, Yu G, et al. Development of a novel retina-based diagnostic score for early detection of major depressive disorder: an interdisciplinary view. Front Psychiatry. 2022;13: 897759.
72.
go back to reference Wang Y, Li C, Liu L, Yang Y, He X, Li G, et al. Association of retinal neurovascular impairment with disease severity in patients with major depressive disorder: an optical coherence tomography angiography study. Psychol Res Behav Manag. 2024;17:1573.PubMedPubMedCentralCrossRef Wang Y, Li C, Liu L, Yang Y, He X, Li G, et al. Association of retinal neurovascular impairment with disease severity in patients with major depressive disorder: an optical coherence tomography angiography study. Psychol Res Behav Manag. 2024;17:1573.PubMedPubMedCentralCrossRef
73.
go back to reference Poli M, Cornut PL, Nguyen AM, De Bats F, Denis P. Accuracy of peripapillary versus macular vessel density in diagnosis of early to advanced primary open angle glaucoma. J Fr Ophtalmol. 2018;41(7):619–29.PubMedCrossRef Poli M, Cornut PL, Nguyen AM, De Bats F, Denis P. Accuracy of peripapillary versus macular vessel density in diagnosis of early to advanced primary open angle glaucoma. J Fr Ophtalmol. 2018;41(7):619–29.PubMedCrossRef
74.
go back to reference Sui J, Li H, Bai Y, He Q, Sun Z, Wei R. Morphological characteristics of the foveal avascular zone in pathological myopia and its relationship with macular structure and microcirculation. Graefes Arch Clin Exp Ophthalmol. 2024;262(7):2121–33.PubMedCrossRef Sui J, Li H, Bai Y, He Q, Sun Z, Wei R. Morphological characteristics of the foveal avascular zone in pathological myopia and its relationship with macular structure and microcirculation. Graefes Arch Clin Exp Ophthalmol. 2024;262(7):2121–33.PubMedCrossRef
75.
go back to reference Dastiridou A, Kassos I, Samouilidou M, Koutali D, Mataftsi A, Androudi S, et al. Age and signal strength-related changes in vessel density in the choroid and the retina: an OCT angiography study of the macula and optic disc. Acta Ophthalmol (Copenh). 2022;100(5):e1095–102.CrossRef Dastiridou A, Kassos I, Samouilidou M, Koutali D, Mataftsi A, Androudi S, et al. Age and signal strength-related changes in vessel density in the choroid and the retina: an OCT angiography study of the macula and optic disc. Acta Ophthalmol (Copenh). 2022;100(5):e1095–102.CrossRef
76.
go back to reference Jo YH, Sung KR, Shin JW. Effects of age on peripapillary and macular vessel density determined using optical coherence tomography angiography in healthy eyes. Invest Ophthalmol Vis Sci. 2019;60(10):3492–8.PubMedCrossRef Jo YH, Sung KR, Shin JW. Effects of age on peripapillary and macular vessel density determined using optical coherence tomography angiography in healthy eyes. Invest Ophthalmol Vis Sci. 2019;60(10):3492–8.PubMedCrossRef
77.
go back to reference Samadzadeh S, Adnan R, Berglova P, Barzegar M, Debrabant B, Roikjaer SG, et al. Protocol of a prospective multicenter study on comorbidity impact on multiple sclerosis and antibody-mediated diseases of the central nervous system (COMMIT). Front Immunol. 2024;15:1380025.PubMedPubMedCentralCrossRef Samadzadeh S, Adnan R, Berglova P, Barzegar M, Debrabant B, Roikjaer SG, et al. Protocol of a prospective multicenter study on comorbidity impact on multiple sclerosis and antibody-mediated diseases of the central nervous system (COMMIT). Front Immunol. 2024;15:1380025.PubMedPubMedCentralCrossRef
78.
go back to reference Lim HB, Kim YW, Kim JM, Jo YJ, Kim JY. The Importance of signal strength in quantitative assessment of retinal vessel density using optical coherence tomography angiography. Sci Rep. 2018;8:12897.PubMedPubMedCentralCrossRef Lim HB, Kim YW, Kim JM, Jo YJ, Kim JY. The Importance of signal strength in quantitative assessment of retinal vessel density using optical coherence tomography angiography. Sci Rep. 2018;8:12897.PubMedPubMedCentralCrossRef
79.
go back to reference Iftikhar M, Zafar S, Gonzalez N, Murphy O, Ohemaa Kwakyi M, Sydney Feldman B, et al. Image artifacts in optical coherence tomography angiography among patients with multiple sclerosis. Curr Eye Res. 2019;44(5):558–63.PubMedCrossRef Iftikhar M, Zafar S, Gonzalez N, Murphy O, Ohemaa Kwakyi M, Sydney Feldman B, et al. Image artifacts in optical coherence tomography angiography among patients with multiple sclerosis. Curr Eye Res. 2019;44(5):558–63.PubMedCrossRef
80.
go back to reference Tewarie P, Balk L, Costello F, Green A, Martin R, Schippling S, et al. The OSCAR-IB consensus criteria for retinal OCT quality assessment. PLOS ONE. 2012;7(4): e34823. Tewarie P, Balk L, Costello F, Green A, Martin R, Schippling S, et al. The OSCAR-IB consensus criteria for retinal OCT quality assessment. PLOS ONE. 2012;7(4): e34823.
81.
go back to reference Schippling S, Balk L, Costello F, Albrecht P, Balcer L, Calabresi P, et al. Quality control for retinal OCT in multiple sclerosis: validation of the OSCAR-IB criteria. Mult Scler J. 2015;21(2):163–70.CrossRef Schippling S, Balk L, Costello F, Albrecht P, Balcer L, Calabresi P, et al. Quality control for retinal OCT in multiple sclerosis: validation of the OSCAR-IB criteria. Mult Scler J. 2015;21(2):163–70.CrossRef
82.
go back to reference Wicklein R, Yam C, Noll C, Aly L, Banze N, Romahn EF, et al. The OSCAR-MP consensus criteria for quality assessment of retinal optical coherence tomography angiography. Neurol Neuroimmunol Neuroinflamm. 2023;10(6): e200169.PubMedPubMedCentralCrossRef Wicklein R, Yam C, Noll C, Aly L, Banze N, Romahn EF, et al. The OSCAR-MP consensus criteria for quality assessment of retinal optical coherence tomography angiography. Neurol Neuroimmunol Neuroinflamm. 2023;10(6): e200169.PubMedPubMedCentralCrossRef
Metadata
Title
Barriers in Healthcare to the Use of Optical Coherence Tomography Angiography in Multiple Sclerosis
Authors
Lukas G. Reeß
Hadi Salih
Murat Delikaya
Friedemann Paul
Frederike Cosima Oertel
Publication date
05-11-2024
Publisher
Springer Healthcare
Published in
Neurology and Therapy
Print ISSN: 2193-8253
Electronic ISSN: 2193-6536
DOI
https://doi.org/10.1007/s40120-024-00670-1

Keynote series | Spotlight on menopause

Menopause can have a significant impact on the body, with effects ranging beyond the endocrine and reproductive systems. Learn about the broader systemic effects of menopause, so you can help patients in your clinics through the transition.

Launching: Thursday 12th December 2024
 

Prof. Martha Hickey
Dr. Claudia Barth
Dr. Samar El Khoudary
Developed by: Springer Medicine
Register your interest now

Advances in Alzheimer's

Alzheimer's research and care is changing rapidly. Keep up with the latest developments from key international conferences, together with expert insights on how to integrate these advances into practice.

This content is intended for healthcare professionals outside of the UK.

Supported by:
  • Lilly
Developed by: Springer Healthcare IME
Learn more