Stellenwert der optischen Kohärenztomografie-Angiografie bei neuroophthalmologischen Erkrankungen

Zusammenfassung

Die optische Kohärenztomografie-Angiografie (OCTA) ist eine der am intensivsten untersuchten Neuentwicklungen in der bildgebenden Ophthalmologie der letzten Jahre. Dabei fand diese nicht invasive Bildgebung von retinalem, chorioidalem und peripapillärem Blutfluss initial Anklang in der Retinologie und neuerdings auch zunehmend Beachtung in der neuroophthalmologischen Diagnostik. Besonderes Interesse wurde auf Erkrankungen gelegt, bei denen eine vaskuläre Pathogenese diskutiert wird, wie die nicht arteriitische und die arteriitische anteriore ischämische Optikusneuropathie (NAION und AAION). Zahlreiche Studien demonstrierten eine Rarefizierung des peripapillären Gefäßnetzes und einen reduzierten Blutfluss in NAION- und in AAION-Patienten im Vergleich zu gesunden Patienten. Dabei korreliert das Ausmaß des Gefäßschadens mit der Schwere der Optikusatrophie. Ähnliche Ergebnisse treffen auch für Optikusatrophien anderer Ursachen zu (z. B. Drusenpapille, hereditäre Optikusatrophien usw.). Die genauen Kausalzusammenhänge zwischen Optikusneuropathie und Blutflussminderung bleiben vorerst jedoch unklar und müssen in zukünftigen Untersuchungen adressiert werden. Bei einigen Erkrankungen scheint die OCTA auch von differenzialdiagnostischem Wert zu sein. Bei Hämangioblastomen lieferte sie besonders bei großen und breitbasigen Befunden relevante Mehrinformationen im Vergleich zur Fluoreszenzangiografie und kann die hämangioblastomtypischen Gefäßnetze und die zuführenden Gefäße darstellen. Diese Übersicht fasst die neuen Informationen der OCTA-Studien zu neuroophthalmologischen Erkrankungen zusammen und hinterfragt diese bez. Relevanz und Mehrwert in der klinischen Anwendung. Zukünftig ist zu erwarten, dass die OCTA durch longitudinale Studien mit größeren Fallzahlen Normwerte liefert, relevante Durchblutungsveränderungen bei verschiedensten Krankheitsbildern tiefgreifender analysiert und möglicherweise zu differenzialdiagnostischen und therapeutischen Zwecken beitragen wird.

Abstract

Within the last few years, optical coherence tomography angiography (OCTA) has been one of the most intensively investigated developments in ophthalmic research. As a non-invasive imaging tool, it can visualise retinal, choroidal and peripapillary blood flow and was first introduced in retinology. Recently, OCTA has received increasing attention in neuro-ophthalmological diagnostic testing. Special consideration has been given to diseases in which vascular pathogenesis is discussed, such as non-arteritic and arteritic anterior ischemic optic neuropathy (NAION and AAION). Numerous studies have demonstrated rarefication of the peripapillary vascular network and reduced blood flow in NAION and AAION patients compared to healthy patients. The extent of the vascular damage correlates with the severity of optic atrophy. Similar findings also apply to optic atrophy from other causes (e.g., optic nerve head drusen, hereditary optic neuropathy, etc.). However, the exact causal relationships between optic neuropathy and blood flow reduction remain unclear and must be addressed in future investigations. In some diseases, OCTA also seems to be of differential diagnostic value. In haemangioblastomas, it has provided relevant information, especially in large and broad-based findings, and may represent the haemangioblastoma-typical vascular networks and the afferent vessels. This review summarises new information from OCTA studies on neuro-ophthalmic diseases, and questions their relevance and value in clinical use. In the future, it can be expected that OCTA will provide standard values through longitudinal studies with larger numbers of cases that more relevant changes in blood flow in a wide variety of clinical pictures will be analysed more profoundly and will possibly contribute to differential diagnostic and therapeutic studies.

Schlüsselwörter

Neuroophthalmologie - optische Kohärenztomografie-Angiografie - OCTA - Flussdichte - Mikrozirkulation - Sehnerv

Key words

neuro-ophthalmology - optical coherence tomography angiography - OCTA - flow density - optic nerve head - microcirculation

• Literatur

• 1 Spaide R, Klancnik J, Cooney M. Retinal vascular layers imaged by fluorescein angiography and optical coherence tomography angiography. JAMA Ophthalmol 2015; 133: 45-50 doi:10.1001/jamaophthalmol.2014.3616
• 2 Kim D, Fingler J, Zawadzki R. et al. Optical imaging of the chorioretinal vasculature in the living human eye. Proc Natl Acad Sci U S A 2013; 110: 14354-14359 doi:10.1073/pnas.1307315110
• 3 Ghasemi Falavarjani K, Al-Sheikh M, Akil H. et al. Image artefacts in swept-source optical coherence tomography angiography. Br J Ophthalmol 2017; 101: 564-568 doi:10.1136/bjophthalmol-2016-309104
• 4 Lauermann JL, Treder M, Heiduschka P. et al. Impact of eye-tracking technology on OCT-angiography imaging quality in age-related macular degeneration. Graefes Arch Clin Exp Ophthalmol 2017; 255: 1535-1542 doi:10.1007/s00417-017-3684-z
• 5 Cheung CY, Li J, Yuan N. et al. Quantitative retinal microvasculature in children using swept-source optical coherence tomography: the Hong Kong Children Eye Study. Br J Ophthalmol 2018; DOI: 10.1136/bjophthalmol-2018-312413.
• 6 Wang Q, Chan S, Yang JY. et al. Vascular density in retina and choriocapillaris as measured by optical coherence tomography angiography. Am J Ophthalmol 2016; 168: 95-109 doi:10.1016/j.ajo.2016.05.005
• 7 Falavarjani KG, Shenazandi H, Naseri D. et al. Foveal avascular zone and vessel density in healthy subjects: an optical coherence tomography angiography study. J Ophthalmic Vis Res 2018; 13: 260-265 doi:10.4103/jovr.jovr_173_17
• 8 Lim HB, Lee MW, Park JH. et al. Changes in ganglion cell-inner plexiform layer thickness and retinal microvasculature in hypertension: an OCT angiography study. Am J Ophthalmol 2019; 199: 167-176 doi:10.1016/j.ajo.2018.11.016
• 9 Müller V, Storp J, Kerschke L. et al. Diurnal variations in flow density measured using optical coherence tomography angiography and the impact of heart rate, mean arterial pressure and intraocular pressure on flow density in primary open-angle glaucoma patients. Acta Ophthalmol 2019; DOI: 10.1111/aos.14089.
• 10 Hayreh SS. Ischemic optic neuropathy. Prog Retin Eye Res 2009; 28: 34-62 doi:10.1016/j.preteyeres.2008.11.002
• 11 Ghasemi Falavarjani K, Tian JJ, Akil H. et al. Swept-source optical coherence tomography angiography of the optic disk in optic neuropathy. Retina 2016; 36 (Suppl. 01) S168-S177 doi:10.1097/IAE.0000000000001259
• 12 Rebolleda G, Díez-Álvarez L, García Marín Y. et al. Reduction of peripapillary vessel density by optical coherence tomography angiography from the acute to the atrophic stage in non-arteritic anterior ischaemic optic neuropathy. Ophthalmologica 2018; 240: 191-199 doi:10.1159/000489226
• 13 Rougier MB, Le Goff M, Korobelnik JF. Optical coherence tomography angiography at the acute phase of optic disc edema. Eye Vis (Lond) 2018; 5: 15 doi:10.1186/s40662-018-0109-y
• 14 Gandhi U, Chhablani J, Badakere A. et al. Optical coherence tomography angiography in acute unilateral nonarteritic anterior ischemic optic neuropathy: a comparison with the fellow eye and with eyes with papilledema. Indian J Ophthalmol 2018; 66: 1144-1148 doi:10.4103/ijo.IJO_179_18
• 15 Fard MA, Ghahvechian H, Sahrayan A. et al. Early macular vessel density loss in acute ischemic optic neuropathy compared to papilledema: implications for pathogenesis. Transl Vis Sci Technol 2018; 7: 10 doi:10.1167/tvst.7.5.10
• 16 Balducci N, Morara M, Veronese C. et al. Optical coherence tomography angiography in acute arteritic and non-arteritic anterior ischemic optic neuropathy. Graefes Arch Clin Exp Ophthalmol 2017; 255: 2255-2261 doi:10.1007/s00417-017-3774-y
• 17 Liu CH, Kao LY, Sun MH. et al. Retinal vessel density in optical coherence tomography angiography in optic atrophy after nonarteritic anterior ischemic optic neuropathy. J Ophthalmol 2017; 2017: 9632647 doi:10.1155/2017/9632647
• 18 Chen JJ, AbouChehade JE, Iezzi jr. R. et al. Optical coherence angiographic demonstration of retinal changes from chronic optic neuropathies. Neuroophthalmology 2017; 41: 76-83 doi:10.1080/01658107.2016.1275703
• 19 Jonas JB, Schmidt AM, Müller-Bergh JA. et al. Human optic nerve fiber count and optic disc size. Invest Ophthalmol Vis Sci 1992; 33: 2012-2018
• 20 Gaier ED, Gilbert AL, Cestari DM. et al. Optical coherence tomographic angiography identifies peripapillary microvascular dilation and focal non-perfusion in giant cell arteritis. Br J Ophthalmol 2018; 102: 1141-1146 doi:10.1136/bjophthalmol-2017-310718
• 21 Augstburger E, Zéboulon P, Keilani C. et al. Retinal and choroidal microvasculature in nonarteritic anterior ischemic optic neuropathy: an optical coherence tomography angiography study. Invest Ophthalmol Vis Sci 2018; 59: 870-877 doi:10.1167/iovs.17-22996
• 22 Gaier ED, Wang M, Gilbert AL. et al. Quantitative analysis of optical coherence tomographic angiography (OCT-A) in patients with non-arteritic anterior ischemic optic neuropathy (NAION) corresponds to visual function. PLoS One 2018; 13: e0199793 doi:10.1371/journal.pone.0199793
• 23 Valmaggia C, Speiser P, Bischoff P. et al. Indocyanine green versus fluorescein angiography in the differential diagnosis of arteritic and nonarteritic anterior ischemic optic neuropathy. Retina 1999; 19: 131-134
• 24 Sharma S, Ang M, Najjar RP. et al. Optical coherence tomography angiography in acute non-arteritic anterior ischaemic optic neuropathy. Br J Ophthalmol 2017; 101: 1045-1051 doi:10.1136/bjophthalmol-2016-309245
• 25 Yu-Wai-Man P, Griffiths P, Hudson G. et al. Inherited mitochondrial optic neuropathies. J Med Genet 2009; 46: 145-158 doi:10.1136/jmg.2007.054270
• 26 Meyerson C, Van Stavern G, McClelland C. Leber hereditary optic neuropathy: current perspectives. Clin Ophthalmol 2015; 9: 1165-1176 doi:10.2147/OPTH.S62021
• 27 Piotrowska A, Korwin M, Bartnik E. et al. Leber hereditary optic neuropathy – historical report in comparison with the current knowledge. Gene 2015; 555: 41-49 doi:10.1016/j.gene.2014.09.048
• 28 Nikoskelainen E, Sogg RL, Rosenthal AR. et al. The early phase in Leber hereditary optic atrophy. Arch Ophthalmol 1977; 95: 969-978
• 29 Chalmers RM, Schapira AH. Clinical, biochemical and molecular genetic features of Leberʼs hereditary optic neuropathy. Biochim Biophys Acta 1999; 1410: 147-158
• 30 Balducci N, Cascavilla ML, Ciardella A. et al. Peripapillary vessel density changes in Leberʼs hereditary optic neuropathy: a new biomarker. Clin Exp Ophthalmol 2018; 46: 1055-1062 doi:10.1111/ceo.13326
• 31 Kousal B, Kolarova H, Meliska M. et al. Peripapillary microcirculation in Leber hereditary optic neuropathy. Acta Ophthalmol 2019; 97: e71-e76 doi:10.1111/aos.13817
• 32 Feucht N, Maier M, Lepennetier G. et al. Optical coherence tomography angiography indicates associations of the retinal vascular network and disease activity in multiple sclerosis. Mult Scler 2019; 25: 224-234 doi:10.1177/1352458517750009
• 33 Martins A, Rodrigues TM, Soares M. et al. Peripapillary and macular morpho-vascular changes in patients with genetic or clinical diagnosis of autosomal dominant optic atrophy: a case-control study. Graefes Arch Clin Exp Ophthalmol 2019; 257: 1019-1027 doi:10.1007/s00417-019-04267-5
• 34 Cennamo G, Rossi C, Ruggiero P. et al. Study of the radial peripapillary capillary network in congenital optic disc anomalies with optical coherence tomography angiography. Am J Ophthalmol 2017; 176: 1-8 doi:10.1016/j.ajo.2016.12.016
• 35 Duvall J, Miller S, Cheatle E. et al. Histopathologic study of ocular changes in a syndrome of multiple congenital anomalies. Am J Ophthalmol 1987; 103: 701-705
• 36 Pollock S. The morning glory disc anomaly: contractile movement, classification and embryogenesis. Doc Ophthalmol 1987; 65: 439-460
• 37 Dempster AG, Lee WR, Forrester JV. et al. The ‘morning glory’ syndrome a mesodermal defect?. Ophthalmologica 1983; 187: 222-230
• 38 Wylęgała A. Principles of OCTA and applications in clinical neurology. Curr Neurol Neurosci Rep 2018; 18: 96 doi:10.1007/s11910-018-0911-x
• 39 Spain RI, Liu L, Zhang X. et al. Optical coherence tomography angiography enhances the detection of optic nerve damage in multiple sclerosis. Br J Ophthalmol 2018; 102: 520-524 doi:10.1136/bjophthalmol-2017-310477
• 40 Kwapong WR, Peng C, He Z. et al. Altered macular microvasculature in neuromyelitis optica spectrum disorders. Am J Ophthalmol 2018; 192: 47-55 doi:10.1016/j.ajo.2018.04.026
• 41 Huang Y, Zhou L, ZhangBao J. et al. Peripapillary and parafoveal vascular network assessment by optical coherence tomography angiography in aquaporin-4 antibody-positive neuromyelitis optica spectrum disorders. Br J Ophthalmol 2018; 103: 789-796 doi:10.1136/bjophthalmol-2018-312231
• 42 Parrozzani R, Frizziero L, Londei D. et al. Peripapillary vascular changes in radiation optic neuropathy: an optical coherence tomography angiography grading. Br J Ophthalmol 2018; 102: 1238-1243 doi:10.1136/bjophthalmol-2017-311389
• 43 Joussen A, Kirchhof B. Solitary peripapillary hemangioblastoma. A histopathological case report. Acta Ophthalmol Scand 2001; 79: 83-87
• 44 Neumann H, Eggert H, Weigel K. et al. Hemangioblastomas of the central nervous system. J Neurosurg 1989; 70: 24-30
• 45 In S, Miyagi J, Kohjo N. et al. Intra‐orbital optic nerve hemangioblastoma with Hippel‐Lindau disease. Case Report. J Neurosurg 1982; 56: 426-429
• 46 Lang S, Cakir B, Evers C. et al. Value of optical coherence tomography angiography imaging in diagnosis and treatment of hemangioblastomas in von Hippel-Lindau disease. Ophthalmic Surg Lasers Imaging Retina 2016; 47: 935-946 doi:10.3928/23258160-20161004-07
• 47 Higashiyama T, Ichiyama Y, Muraki S. et al. Optical coherence tomography angiography in a patient with optic atrophy after non-arteritic anterior ischaemic optic neuropathy. Neuroophthalmology 2016; 40: 146-149
• 48 Liu CH, Wu WC, Sun MH. et al. Comparison of the retinal microvascular density between open angle glaucoma and nonarteritic anterior ischemic optic neuropathy. Invest Ophthalmol Vis Sci 2017; 58: 3350-3356 doi:10.1167/iovs.17-22021
• 49 Wright Mayes E, Cole ED, Dang S. et al. Optical coherence tomography angiography in nonarteritic anterior ischemic optic neuropathy. J Neuroophthalmol 2017; 37: 358-364 doi:10.1097/WNO.0000000000000493
• 50 Rougier MB, Delyfer MN, Korobelnik JF. OCT angiography of acute non-arteritic anterior ischemic optic neuropathy. J Fr Ophtalmol 2017; 40: 102-109 doi:10.1016/j.jfo.2016.09.020
• 51 Hata M, Oishi A, Muraoka Y. et al. Structural and functional analyses in nonarteritic anterior ischemic optic neuropathy: optical coherence tomography angiography study. J Neuroophthalmol 2017; 37: 140-148 doi:10.1097/WNO.0000000000000470
• 52 Song Y, Min JY, Mao L. et al. Microvasculature dropout detected by the optical coherence tomography angiography in nonarteritic anterior ischemic optic neuropathy. Lasers Surg Med 2018; 50: 194-201 doi:10.1002/lsm.22712
• 53 Tao Z, Chou Y, Ma J. et al. [Vessel density and structure in the macular region of non-arteritic anterior ischemic optic neuropathy patients]. Zhonghua Yan Ke Za Zhi 2019; 55: 195-202 doi:10.3760/cma.j.issn.0412-4081.2019.03.008
• 54 Tao ZY, Ma J, Zhong Y. [The status of the application of optical coherence tomography angiography in nonarteritic ischemic optic neuropathy]. Zhonghua Yan Ke Za Zhi 2019; 55: 306-310 doi:10.3760/cma.j.issn.0412-4081.2019.04.015
• 55 Gaier ED, Gittinger JW, Cestari DM. et al. Peripapillary capillary dilation in Leber hereditary optic neuropathy revealed by optical coherence tomographic angiography. JAMA Ophthalmol 2016; 134: 1332-1334 doi:10.1001/jamaophthalmol.2016.3593
• 56 Takayama K, Ito Y, Kaneko H. et al. Optical coherence tomography angiography in leber hereditary optic neuropathy. Acta Ophthalmol 2017; 95: e344-e345 doi:10.1111/aos.13244
• 57 Matsuzaki M, Hirami Y, Uyama H. et al. Optical coherence tomography angiography changes in radial peripapillary capillaries in Leber hereditary optic neuropathy. Am J Ophthalmol Case Rep 2018; 9: 51-55 doi:10.1016/j.ajoc.2018.01.003
• 58 Asanad S, Meer E, Fantini M. et al. Leberʼs hereditary optic neuropathy: shifting our attention to the macula. Am J Ophthalmol Case Rep 2018; 13: 13-15 doi:10.1016/j.ajoc.2018.11.010
• 59 Borrelli E, Balasubramanian S, Triolo G. et al. Topographic macular microvascular changes and correlation with visual loss in chronic Leber hereditary optic neuropathy. Am J Ophthalmol 2018; 192: 217-228 doi:10.1016/j.ajo.2018.05.029
• 60 Asanad S, Meer E, Tian JJ. et al. Leberʼs hereditary optic neuropathy: severe vascular pathology in a severe primary mutation. Intractable Rare Dis Res 2019; 8: 52-55 doi:10.5582/irdr.2018.01126
• 61 Balducci N, Ciardella A, Gattegna R. et al. Optical coherence tomography angiography of the peripapillary retina and optic nerve head in dominant optic atrophy. Mitochondrion 2017; 36: 60-65 doi:10.1016/j.mito.2017.03.002
• 62 Shin JH, Jung JH. Optical coherence tomography angiography findings in superior segmental optic nerve hypoplasia. J Neuroophthalmol 2019; 39: 103-104 doi:10.1097/WNO.0000000000000727
• 63 Higashiyama T, Nishida Y, Ohji M. Optical coherence tomography angiography in eyes with good visual acuity recovery after treatment for optic neuritis. PLoS One 2017; 12: e0172168 doi:10.1371/journal.pone.0172168
• 64 Fard MA, Yadegari S, Ghahvechian H. et al. Optical coherence tomography angiography of a pale optic disc in demyelinating optic neuritis and ischemic optic neuropathy. J Neuroophthalmol 2019; DOI: 10.1097/WNO.0000000000000775.
• 65 Flores-Reyes E, Hoskens K, Mansouri K. Optic nerve head drusen: imaging using optical coherence tomography angiography. J Glaucoma 2017; 26: 845-849 doi:10.1097/IJG.0000000000000730
• 66 Gaier ED, Rizzo 3rd JF, Miller JB. et al. Focal capillary dropout associated with optic disc drusen using optical coherence tomographic angiography. J Neuroophthalmol 2017; 37: 405-410 doi:10.1097/WNO.0000000000000502
• 67 Cennamo G, Tebaldi S, Amoroso F. et al. Optical coherence tomography angiography in optic nerve drusen. Ophthalmic Res 2018; 59: 76-80 doi:10.1159/000481889
• 68 Higashiyama T, Ichiyama Y, Muraki S. et al. Optical coherence tomography angiography of retinal perfusion in chiasmal compression. Ophthalmic Surg Lasers Imaging Retina 2016; 47: 724-729 doi:10.3928/23258160-20160808-05
• 69 Tüntaş Bilen F, Atilla H. Peripapillary vessel density measured by optical coherence tomography angiography in idiopathic intracranial hypertension. J Neuroophthalmol 2018; DOI: 10.1097/WNO.0000000000000745.
• 70 Lang SJ, Evers C, Cakir B. et al. [Optical coherence tomography angiography in diagnosis and post-treatment assessment of hemangioblastomas in Hippel-Lindau disease]. Klin Monatsbl Augenheilkd 2017; 234: 1146-1153 doi:10.1055/s-0043-102574
• 71 Sagar P, Rajesh R, Shanmugam M. et al. Comparison of optical coherence tomography angiography and fundus fluorescein angiography features of retinal capillary hemangioblastoma. Indian J Ophthalmol 2018; 66: 872-876 doi:10.4103/ijo.IJO_1199_17
• 72 Holló G. Influence of myelinated retinal nerve fibers on retinal vessel density measurement with AngioVue OCT angiography. Int Ophthalmol 2016; 36: 915-919
• 73 Ang M, Sng C, Milea D. Optical coherence tomography angiography in dural carotid-cavernous sinus fistula. BMC Ophthalmol 2016; 16: 93 doi:10.1186/s12886-016-0278-1
• 74 Goto K, Miki A, Yamashita T. et al. Retinal nerve fiber layer and peripapillary capillary density reduction detected using optical coherence tomography enface images and angiography in optic tract syndrome. J Neuroophthalmol 2019; 39: 253-256 doi:10.1097/WNO.0000000000000716