OCT Angiography of the Central Macular Capillary Network in Glaucoma Patients and Healthy Controls

Olena Müller; Margarita G. Todorova; Torsten Schlote

doi:10.1055/s-0043-124651

Klinische Monatsblätter für Augenheilkunde, Table of Contents

Klin Monbl Augenheilkd 2018; 235(04): 436-444
DOI: 10.1055/s-0043-124651

Klinische Studie

Georg Thieme Verlag KG Stuttgart · New York

OCT Angiography of the Central Macular Capillary Network in Glaucoma Patients and Healthy Controls

Optische Kohärenztomografie-Angiografie der zentralen makulären Gefäßversorgung bei Glaukompatienten und gesunden Probanden

Olena Müller

¹Augenklinik, Tagesklinik, Ambimed AG, Basel, Switzerland

²Department of Ophthalmology, University of Basel, Basel, Switzerland

,

Margarita G. Todorova

²Department of Ophthalmology, University of Basel, Basel, Switzerland

,

Torsten Schlote

¹Augenklinik, Tagesklinik, Ambimed AG, Basel, Switzerland

› Author Affiliations

Abstract

Purpose We aimed to investigate central macular microvasculature by optical coherence tomography angiography (OCTA) and to analyse its relation to alterations in classical parameters of optical coherence tomography (OCT) in glaucoma patients.

Methods Using OCTA (Avanti incl. AngioVue; Optovue, Inc., Fremont, CA), the superficial flow (SF) and the superficial non-flow (SNF) area of the macula, as well as the S-ETDRS (based on Early Treatment Diabetic Retinopathy charts). and S-grid vessel density (zones 1 – 9) of the macula, were evaluated in 27 glaucoma patients (49 eyes) and compared to those of 27 age-matched healthy controls (50 eyes; p = 0.253). The interactions between OCTA parameters representing macular microvasculature and classical OCT measurements of the circumpapillary retinal nerve fibre layer (RNFL) and macular ganglion cells (mGCC) were analysed within groups (linear mixed-effects model).

Results SF, SNF, and S-ETDRS vessel density exhibited no significant difference between the glaucoma and control groups (all p ≥ 0.158). However, within the glaucoma group, decreased RNFL and mGCC thickness correlated significantly with decreased S-ETDRS density (zones 1; 2 – 9, p ≤ 0.033). The same held true for the interactions between the RNFL and mGCC thickness with S-grid density (zones 1 – 3; 6 – 9; p ≤ 0.033). For perimetric glaucoma patients, subgroup analyses demonstrated significantly reduced density maps of superficial foveal flow as well as significant interactions between OCT and OCTA parameters; this was not the case within the preperimetric group.

Conclusions Even if the central macular microvasculature, as measured by SF and SNF, is found preserved in glaucoma, the strong positive relation between the central microvascular and structural changes in OCTA and OCT indicates that there are alterations in central macular microvasculature in subclinical glaucoma.

Zusammenfassung

Hintergrund Ziel der Studie war die Untersuchung der zentralen makulären Gefäßversorgung mittels optischer Kohärenztomografie-Angiografie (OCTA) bei Glaukompatienten und die Korrelation dieser OCTA-Parameter mit klassischen OCT- und klinischen Befunden.

Patienten und Methoden Für die Studie wurden 27 Glaukompatienten und 27 alterskorrelierte, gesunde Probanden gewonnen. Mit der OCTA (Avanti incl. AngioVue; Fa. Optovue, Inc, Fremont, CA) wurden verschiedene Parameter der oberflächlichen kapillaren Blutversorgung der Makula gemessen: das oberflächliche Flussareal (Superficial Flow = SF) und das kapillar nicht durchblutete Areal (Non-Flow Area = SNF) der Makula sowie zusätzlich die Messung der kapillaren Gefäßdichte unter zonaler Aufteilung der Makularegion nach 2 Mustern (S-ETDRS- und S-Grid-Muster mit jeweils 9 Zonen). Neben den klinischen Befunden wurden klassische OCT-Parameter der Glaukomdiagnostik (zirkularpapillare retinale Nervenfaserschicht = RNFL, makulärer Ganglienzellkomplex = mGCC) erhoben und eine Analyse der OCT- und OCTA-Parameter vorgenommen (Linear Mixed-Effects Model).

Ergebnisse Verschiedene OCTA-Parameter (SF, SNF und S-ETDRS-Gefäßdichte) zeigten keinen signifikanten Unterschied zwischen Glaukomgruppe und Kontrollgruppe (alle p = 0,158). Jedoch ergab sich innerhalb der Glaukomgruppe eine starke Korrelation zwischen reduzierter RNFL-Dicke und mGCC-Dicke einerseits und reduzierten S-ETDRS-Gefäßdichtezonen (Zonen 1; 2 – 9; p = 0,033) und S-Grid-Gefäßdichtezonen (Zonen 1 – 3; 6 – 9; p = 0,033) andererseits. In einer Subgruppenanalyse zeigten Glaukomaugen mit manifesten Gesichtsfeldausfällen signifikante Veränderungen der kapillaren Gefäßversorgung, die bei einem präperimetrischen Glaukomstatus nicht sichtbar waren.

Schlussfolgerung Veränderungen der zentralen mikrovakulären Gefäßversorgung der Makula sind zumindest auf subklinischer Ebene mittels OCTA bei Glaukompatienten darstellbar und zeigen eine Korrelation zu Veränderungen klassischer OCT-Parameter und dem Gesichtsfeldstatus.

Key words

glaucoma - optical coherence tomography angiography - optical coherence tomography - microvasculature - optic nerve - macula

Schlüsselwörter

Glaukom - optische Kohärenztomografie - OCT-Angiografie - Makula - mikrovaskuläre Gefäßversorgung - Sehnerv

Full Text

References

References
1 Resnikoff S, Pascolini D, Etyaʼale D. et al. Global data on visual impairment in the year 2002. Bull World Health Organ 2004; 82: 844-851
2 Tham YC, Li X, Wong TY. et al. Global prevalence of glaucoma and projections of glaucoma burden through 2040: a systematic review and meta-analysis. Ophthalmology 2014; 121: 2081-2090
3 Kuehn MH, Fingert JH, Kwon YH. Retinal ganglion cell death in glaucoma: mechanisms and neuroprotective strategies. Ophthalmol Clin North Am 2005; 18: 383-395
4 Quigley HA, Addicks EM, Green WR. Optic nerve damage in human glaucoma. III. Quantitative correlation of nerve fiber loss and visual field defect in glaucoma, ischaemic neuropathy, papilledema, and toxic neuropathy. Arch Ophthalmol 1982; 100: 135-146
5 Quigley HA, Dunkelberger GR, Green WR. Retinal ganglion cell atrophy correlated with automated perimetry in human eyes with glaucoma. Am J Ophthalmol 1989; 107: 453-464
6 Wang M, Hood DC, Cho JS. et al. Measurement of local retinal ganglion cell layer thickness in patients with glaucoma using frequency-domain optical coherence tomography. Arch Ophthalmol 2009; 127: 875-881
7 Fujimoto JG, Schuman JS, Hitzenberger CK. Optical coherence tomography (OCT) in ophthalmology: introduction. Opt Express 2009; 17: 3978-3979
8 Lee EJ, Lee SH, Kim TW. OCT angiography of the peripapillary retina in primary open-angle glaucoma. Invest Ophthalmol Vis Sci 2016; 57: 6265-6270
9 Sung KR, Kim NR, Na JH. et al. Macular assessment using optical coherence tomography for glaucoma diagnosis. Br J Ophthalmol 2012; 96: 1452-1455
10 Parikh RS, Thomas R. Diagnostic capability of macular parameters of Stratus OCT 3 in detection of early glaucoma. Br J Ophthalmol 2010; 94: 197-201
11 Brandao LM, Schötzau A, Palmowski-Wolfe AM. Comparison of two different OCT systems: retina layer segmentation and impact on structure-function analysis in glaucoma. J Ophthalmol 2016; 2016: 8307639 doi:10.1155/2016/8307639
12 Medeiros FA, Zangwill LM, Bowd C. et al. Evaluation of retinal nerve fiber layer, optic nerve head, and macular thickness measurements for glaucoma detection using optical coherence tomography. Am J Ophthalmol 2005; 139: 44-55
13 Holló G, Zhou Q. Evaluation of retinal nerve fiber layer thickness and ganglion cell complex progression rates in healthy, ocular hypertensive, and glaucoma eyes with the Avanti RTVue-XR optical coherence tomograph based on 5-year follow-up. J Glaucoma 2016; 25: e905-e909
14 Jeong JH, Choi YJ, Park KH. et al. Macular ganglion cell imaging study: covariate effects on the spectral domain optical coherence tomography for glaucoma diagnosis. PLoS One 2016; 11: e0160448
15 Jeoung JW, Choi YJ, Park KH. et al. Macular ganglion cell imaging study: glaucoma diagnostic accuracy of spectral-domain optical coherence tomography. Invest Ophthalmol Vis Sci 2013; 54: 4422-4429
16 Sambhav K, Grover S, Chalam KV. The application of optical coherence tomography angiography in retinal diseases. Surv Ophthalmol 2017;
17 Akil H, Falavarjani KG, Sadda SR. et al. Optical coherence tomography angiography of the optic disc: an overview. J Ophthalmic Vis Res 2017; 12: 98-105
18 Kim SB, Lee EJ, Han JC. et al. Comparison of peripapillary vessel density between preperimetric and perimetric glaucoma evaluated by OCT-angiography. PLoS One 2017; 12: e0184297
19 Chen HS, Liu CH, Wu WC. et al. Optical coherence tomography angiography of the superficial microvasculature in the macular and peripapillary areas in glaucomatous and healthy eyes. Invest Ophthalmol Vis Sci 2017; 58: 3637-3645
20 Suh MH, Zangwill LM, Manalastas PI. et al. Optical coherence tomography angiography vessel density in glaucomatous eyes with focal lamina cribrosa defects. Ophthalmology 2016; 123: 2309-2317
21 Suh MH, Zangwill LM, Manalastas PI. et al. Deep retinal layer microvasculature dropout detected by the optical coherence tomography angiography in glaucoma. Ophthalmology 2016; 123: 2509-2518
22 Lévêque PM, Zèboulon P, Brasnu E. et al. Optic disc vascularization in glaucoma: value of spectral-domain optical coherence tomography angiography. J Ophthalmol 2016; 2016: 6956717 doi:10.1155/2016/6956717
23 Yarmohammadi A, Zangwill LM, Diniz-Filho A. et al. Relationship between optical coherence tomography angiography vessel density and severity of visual field loss in glaucoma. Ophthalmology 2016; 123: 2498-2508
24 Nützi C, Schötzau A, Grieshaber MC. Structure and function relationship of activated retinal glia in primary open-angle glaucoma patients. J Ophthalmol 2017; 2017: 7043752
25 Jung KI, Park CK. Detection of functional change in preperimetric and perimetric glaucoma using 10-2 matrix perimetry. Am J Ophthalmol 2017; 182: 35-44
26 Tanna AP. Growing evidence of the importance of the macula in glaucoma. JAMA Ophthalmol 2017; 135: 747-748
27 Hood DC, Raza AS, de Moraes CG. et al. Initial arcuate defects within the central 10 degrees in glaucoma. Invest Ophthalmol Vis Sci 2011; 52: 940-946