Retinal Vascular Density Evaluated by Optical Coherence Tomography Angiography in Macular Telangiectasia Type 2
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Int Ophthalmol (2019) 39:2245–2256 https://doi.org/10.1007/s10792-018-01060-x (0123456789().,-volV)( 0123456789().,-volV) ORIGINAL PAPER Retinal vascular density evaluated by optical coherence tomography angiography in macular telangiectasia type 2 Berna Dogan . Muhammet Kazim Erol . Melih Akidan . Elcin Suren . Yusuf Akar Received: 18 March 2018 / Accepted: 21 December 2018 / Published online: 3 January 2019 Ó Springer Nature B.V. 2019 Abstract retinal thickness, choroidal thickness (CT) and retinal Purpose To evaluate the retinal and choroidal vas- ganglion cell–inner plexiform layer (GCIPL) were cular changes through optical coherence tomography compared between MacTel 2 patients and normal age- angiography (OCTA) in patients with macular telang- matched controls. iectasia type 2 (MacTel 2). Results The retinal whole vascular density and Methods Our study included 20 patients (40 eyes) PFVD of the deep plexus were significantly lower in with MacTel 2, and age-matched and sex-matched 18 patients with MacTel 2 than that of the control group subjects (36 eyes) in the control group. Fundus color (56.93% vs. 58.54%, p = 0.003; and 60.38% vs. photographs, fundus autofluorescence, fundus fluores- 61.66%, p = 0.045). The foveal avascular zone cein angiography, spectral-domain optical coherence (FAZ) of the deep plexus was significantly enlarged tomography and OCTA were performed. Foveal in patients with MacTel 2 than that of the control vascular density and parafoveal vascular density group (0.44 vs. 0.36, p = 0.009). There was a positive (PFVD), and foveal retinal thickness and parafoveal and statistically significant correlation between the FAZ of the superficial and deep plexus and CT in patients with MacTel 2. There was a positive and B. Dogan (&) Á M. K. Erol Á E. Suren statistically significant correlation between retinal Department of Ophthalmology, Antalya Education and whole, parafoveal temporal quadrant vascular density Research Hospital, Varlık Mah., Kazim Karabekir Caddesi, 07100 Antalya, Turkey of the superficial and deep plexus and GCIPL thick- e-mail: [email protected] ness in patients with MacTel 2. M. K. Erol Conclusions Our study demonstrated that important e-mail: [email protected] retinal vascular density and FAZ changes in MacTel 2 E. Suren occur in the deep capillary plexus of the retina. e-mail: [email protected] Keywords Optical coherence tomography M. Akidan angiography Á Macular telangiectasia type 2 Á Vascular Department of Ophthalmology, Kepez State Hospital, Antalya, Turkey density Á Retinal ganglion cell–inner plexiform layer Á e-mail: [email protected] Choroidal thickness Y. Akar Department of Ophthalmology, Akdeniz University Medical Faculty, Antalya, Turkey e-mail: [email protected] 123 2246 Int Ophthalmol (2019) 39:2245–2256 Introduction In this study, we aimed to compare the superficial and deep retinal capillary density, choroidal vascular Idiopathic macular telangiectasia type 2 (MacTel 2) is density, FAZ, choroidal thickness (CT) and ganglion bilateral disease characterized by Mu¨ller cell dysfunc- cell–inner plexiform layer (GCIPL) in patient with tion, changes in macular capillary network and neural MacTel 2 and control groups. atrophy [1]. Early manifestations of the disease include loss of retinal transparency, superficial retinal crystalline deposits, right-angled venules and presence Materials and methods of intraretinal cystoid spaces in the fovea. In later stages, the intraretinal pigment migrates, forming Approval was obtained from the local ethics commit- pigment plaques, and subretinal neovascular mem- tee of University of Health Sciences, Antalya Training brane (SNV) develops. There is not usually lipid and Research Hospital, where the study was conducted exudation or hemorrhages associated with MacTel 2 and performed in compliance with the ethical stan- unless SNV is present [2]. dards set out in the Declaration of Helsinki. Before the Fundus fluorescein angiography (FFA) has been participants were included in this study, their written considered for many years the gold standard for informed consent was obtained. diagnosis of MacTel 2. The classic FFA finding is All patients and controls underwent a comprehen- telangiectatic vessels that leak dye in the parafoveal sive ophthalmologic examination, including measure- area with fluorescein leakage not related to the cystic ments of best-corrected visual acuity (BCVA), slit spaces [3]. Spectral-domain optical coherence tomog- lamp examination of the anterior segment, intraocular raphy (SD-OCT) provides a useful visualization of the pressure, dilated fundus examination and OCTA retinal and choroidal changes in patients with MacTel imaging (Optovue RTVue XR 100 Avanti, Freemont, 2. SD-OCT has shown neurodegenerative changes in California, USA) and SD-OCT (Cirrus HD-OCT, Carl MacTel 2, including presence of hyporeflective spaces Zeiss Meditec, Dublin, CA, USA). Each patient with in the inner or outer retina, foveal thinning, intraretinal MacTel type 2 underwent color fundus photography, pigments, breaks in the ellipsoid zone with progressive fundus autofluorescence (FAF) and FFA to confirm outer retinal atrophy in which the retinal layers interior the diagnosis. to the outer nuclear layer seemingly ‘collapse’ through Inclusion criteria for the patient group were all eyes these breaks toward the retinal pigment epithelium with either nonproliferative or proliferative MacTel (RPE). Progression of the disease is characterized by type 2. The exclusion criteria for groups were as shrinkage of the outer retinal layers and reduction in follows: Refractive error [ ± 3 spherical equivalent; the central foveal thickness [4–6]. poor image quality \ 60 due to unstable fixation; With the development of optical coherence tomog- intraocular pressure (IOP) [ 21 mm Hg; preexisting raphy angiography (OCTA), it is now possible to macular pathologies, such as age-related macular noninvasively image the retinal and choroidal degeneration, epiretinal membrane or macular hole; microvasculature without the use of exogenous intra- other retinopathies, such as retinal vascular occlusion, venous dye injection. Both structural and blood flow diabetic retinopathy or retinal dystrophy; preexisting information could be evaluated together via OCTA. ocular diseases, such as glaucoma, optic neuropathy or Superficial and deep capillary plexus, vascular density uveitis; previous vitreoretinal surgery or photody- and foveal avascular zone (FAZ) changes have been namic therapy, diabetes mellitus, systemic arterial started to be evaluated through OCTA, and an hypertension, cardiovascular diseases. effective imaging method has been obtained in the clarification of the pathophysiology of MacTel 2 Spectral-domain optical coherence tomography [7, 8]. Since the response to anti-VEGF in the proliferative phase is good, OCTA seems to be more Spectral-domain OCT scans were obtained using the advantageous than other imaging methods regarding Cirrus HD-OCT. The Macular Cube 512 9 128 scan early detection of choroidal neovascularization (CNV) protocol was used for all subjects. The average, and planning the treatment. minimum (lowest GCIPL thickness over a single meridian crossing the annulus) and sectoral 123 Int Ophthalmol (2019) 39:2245–2256 2247 (superotemporal, superior, superonasal, inferonasal, Statistical analysis inferior, inferotemporal) GCIPL thicknesses were measured in an elliptical annulus around the fovea. Statistical analyses were performed using SPSS Statistics, version 22 (SPSS, Inc. Chicago, IL).To Optical coherence tomography angiography compare the groups, independent t test and Mann– Whitney U test were applied. The normality assump- The imaging of all subjects was performed with a tion for the independent variables was checked with commercial OCTA that had a scan rate of 70,000 A- Shapiro–Wilk test. The variables that were compliant scans/s, scan beam wavelength of 840 ± 10 nm and with the normality assumption were subjected to the bandwidth of 45 nm. This device can do the volumet- independent t test, while those that do not meet the ric scans of 304 9 304 A-scans at 70,000 A-scans/s normality assumption were subjected to Mann–Whit- in around 3.0 s [9]. All measurements were taken ney U test. For the analysis of correlation, Pearson between 09:00 and 11:00 on the same day. correlation coefficient and Spearman correlation coef- To evaluate the vascular structures, 3 9 3mm ficient were used. p \ 0.05 was considered significant. OCT angiogram software was used. Split Spectrum Amplitude Decorrelation Angiography images were obtained. Images that could not be evaluated due to the Results low resolution were excluded. The OCTA images were independently graded and assessed by two Our study included 20 patients (40 eyes) with MacTel clinicians. The software automatically segmented 2, and age-matched and sex-matched 18 subjects (36 these full-thickness retinal scans into the superficial eyes) in the control group. The mean age ± standard and deep inner retinal vascular plexuses, outer retina deviation (SD) was 56.2 ± 8.8 years in patients with and choriocapillaris. The vascular density in superfi- MacTel 2 and 59.3 ± 10.2 years in the control group cial and deep retinal vascular zone was calculated (p = 0.328). automatically by this software, and FAZ was also Optical coherence tomography angiography pro- automatically identified. The area 3 lm beneath the vided detailed images of the retinal microcirculation in internal limiting membrane was defined as the starting all