Microvascular Abnormalities on Optical Coherence Tomography Angiography in Macular Edema Associated With Branch Retinal Vein Occlusion




Purpose


To determine the ability of optical coherence tomography (OCT) angiography to image the microvascular structures compared with fluorescein angiography (FA) in patients with macular edema associated with branch retinal vein occlusion (BRVO).


Design


Retrospective, observational, consecutive case series.


Methods


Twenty-eight eyes of 27 patients (14 men, 13 women; mean age, 68.4 years) with macular edema associated with BRVO were enrolled. Simultaneous OCT angiography and FA were performed in all patients to evaluate the microvascular abnormalities and nonperfused areas.


Results


OCT angiography detected nonperfused areas in 28 eyes and FA in 18 eyes. The respective findings of superficial capillary telangiectasias by OCT angiography and FA were 13 and 11 eyes, for deep capillary telangiectasias 28 eyes and 11 eyes, for collateral vessels 18 eyes and 16 eyes, and for microaneurysms 13 eyes and 14 eyes. OCT angiography facilitated differential layer analysis of microaneurysms and collaterals as well as capillary telangiectasias in the retina.


Conclusions


OCT angiography can visualize microvascular abnormalities equally well or better than FA in eyes with BRVO. Multimodal imaging using OCT angiography and FA can be a powerful tool to evaluate the pathology in BRVO.


Branch retinal vein occlusion (BRVO) usually results from a thrombus at the arteriovenous crossings where a thickened artery compresses the underlying venous wall, resulting in elevated venous pressure and consequent macular edema, retinal ischemia, and rupture of the retinal wall with intraretinal hemorrhage. In the chronic phase, after absorption of the intraretinal hemorrhage, there are several retinal vascular abnormalities, such as capillary nonperfusion, capillary dilation, microaneurysms, telangiectatic vessels, and collateral vessels.


Fluorescein angiography (FA) is useful to confirm the diagnosis of BRVO and evaluate complications. The characteristic findings on FA are delayed filling of the occluded retinal vein, capillary nonperfusion, microaneurysms, and dye extravasation from macular edema or retinal neovascularization. Ultra-wide-field FA using the Optos 200Tx (Optos PLC, Dunfermline, Scotland, UK) shows nonperfused areas in the peripheral retina. However, dense retinal hemorrhages and/or macular edema make interpretation of FA images difficult because of blocked or pooled fluorescein. In addition, FA does not visualize the deeper capillary network in the retina well, possibly because of light scattering in the retina.


Optical coherence tomography (OCT) is a rapid, noninvasive technique that provides high-resolution retinal images. Recently, 3-dimensional and noninvasive vascular mapping without dye was accomplished using OCT angiography. OCT angiography has the advantage of 3-dimensional noninvasive vascular mapping in the retina and choroid in just a few seconds, thus displaying several vascular layers (ie, the superficial and deep capillaries, outer retina, and choriocapillaris). Recently, de Carlo reported the microvascular changes in patients with BRVO. We evaluated the ability of OCT angiography to visualize several vascular abnormalities and compared the findings with conventional FA.


Methods


Study Design and Setting


This was a retrospective, observational, consecutive case series conducted in an institutional setting. The study design was approved by the Institutional Review Board of Nagoya City University Graduate School of Medical Sciences. All patients provided written informed consent for participation in the study. The described research methods and analysis adhered to the tenets of the Declaration of Helsinki.


This study was conducted at Nagoya City University Hospital from November 1, 2014 through May 31, 2015. Twenty-eight eyes of 27 patients (14 men, 13 women; mean age, 68.4 years; range, 41–86 years) with macular edema associated with BRVO were enrolled. The mean follow-up period was 28.8 months (range, 4–122 months). All patients underwent a complete ophthalmic examination including measurement of best-corrected visual acuity, indirect ophthalmoscopy, fundus photography, OCT (Cirrus HD-OCT; Carl Zeiss Meditec, Jena, Germany), OCT angiography (RTVue XR Avanti, AngioVue; Optovue Inc, Fremont, California, USA), and/or FA. FA was performed using the wide-field laser ophthalmoscope Optos 200Tx and/or confocal scanning laser ophthalmoscopy (Heidelberg Retina Angiograph 2 [HRA2]; Heidelberg Engineering, Heidelberg, Germany). OCT angiography and FA also were performed on the same day. The mean measurement time of OCT angiography and FA was 25.1 months (range, 1–120 months) after disease onset. The incidence rates of nonperfused areas, superficial and deep capillary telangiectasias, collateral vessels, and microaneurysms were determined using OCT angiography and FA. Patients whose OCT angiography images were of inadequate quality for evaluation because of eye movement or cataract or who had not undergone FA because of renal and/or liver dysfunction or allergy to fluorescein were excluded.


Optical Coherence Tomography Angiography


OCT angiography images were obtained using the RTVue XR Avanti AngioVue with a split-spectrum amplitude-decorrelation angiography algorithm, as previously described. The instrument obtains 70 000 A-scans/second, using a light source centered on 840 nm; the tissue resolution is 5 μm in depth and 15 μm in width. Two consecutive B-scans (M-B frames) were captured at a fixed position before proceeding to the next sampling position, split into 11 decorrelation sets, compared to detect motion, and merged. The merging of the sets increased the signal-to-noise ratio and provided the high-detail, motion contrast “angioflow” image.




Results


Nonperfused Areas


OCT angiography detected nonperfused areas in all 28 eyes compared with FA, which detected them in 18 eyes. In some FA images, the nonperfused areas were masked by hyperfluorescence from the leaking vessels or hypofluorescence due to retinal hemorrhage ( Figure 1 ), whereas OCT angiography detected them clearly because of the absence of fluorescein dye. OCT angiography also visualized the nonperfused areas clearer than FA ( Figure 1 ) and was superior for differentiating the foveal avascular zone from nonperfused areas because the OCT angiography system provided higher-resolution images than FA. OCT angiography did not detect nonperfused areas in the peripheral retina. However, the Optos 200Tx visualized the nonperfused areas in the peripheral retina ( Figure 1 ).




Figure 1


Nonperfused areas in macular edema associated with branch retinal vein occlusion. (Top, left and Top, second from left) Fluorescein angiography (FA) images obtained by Optos 200Tx and (Bottom, left and Bottom, second from left) optical coherence tomography (OCT) angiography images obtained by AngioVue (scan size, 3 × 3 mm). (Top, second from left) Magnified image of the yellow square in Top left scan. (Bottom, left) Superficial layer. (Bottom, second from left) Deep layer. (Top, second from left) Hyperfluorescence from leaking vessels masks the nonperfused areas. (Bottom, left and Bottom, second from left) OCT angiography clearly visualizes the nonperfused areas and microaneurysms (arrowhead). (Top, third from left and Top, fourth from left) The images were obtained by Heidelberg Retina Angiograph 2. (Top, fourth from left) Magnified image of the yellow square in Top, third from left scan. (Bottom, third from left and Bottom, fourth from left) The images were obtained by AngioVue (scan size, 3 × 3 mm). (Bottom, third from left) Superficial layer. (Bottom, fourth from left) Deep layer. The border between the nonperfused areas and foveal avascular zone is obscured on FA (Top, third from left and Top, fourth from left), whereas OCT angiography clearly visualizes the nonperfused areas and foveal avascular zone (Bottom, third from left and Bottom, fourth from left). (Right) An FA image obtained by Optos 200Tx. The nonperfused areas in the peripheral retina are imaged well.


Superficial Capillary Telangiectasia


OCT angiography detected superficial capillary telangiectasia in 13 of 28 eyes, vs FA in 11 eyes; even with high-resolution confocal scanning laser ophthalmoscopy HRA2 imaged the superficial capillary telangiectasia in 11 eyes maximally, but it was difficult to observe the normal capillary network in the superficial capillary layer ( Figure 2 ). OCT angiography detected even the very thin capillary networks in the superficial layer ( Figure 2 ).




Figure 2


Telangiectasia in macular edema associated with branch retinal vein occlusion. (Top row) Fluorescein angiography (FA) images (Top left and Top middle) obtained by Heidelberg Retina Angiograph 2 and optical coherence tomography (OCT) angiography image (Top right) obtained by AngioVue (scan size 3 mm × 3 mm, superficial layer). (Top middle) Magnified image of the yellow square in Top left scan. Collateral vessels (arrows) are seen on FA and OCT angiography, but a normal capillary network in the superficial layer is hardly visible on FA (Top middle). OCT angiography clearly visualizes the microvascular network (Top right). (Bottom row) FA (Bottom left and Bottom middle) and OCT angiography (Bottom right). (Bottom middle) Magnified image of the yellow square in Bottom left scan. Deep capillary telangiectasia and normal deep capillary network are not visible on FA (Bottom left and Bottom middle). OCT angiography clearly visualizes the deep capillary, deep telangiectasia, and microaneurysms (arrowheads) (Bottom right).


Deep Capillary Telangiectasia


OCT angiography detected deep capillary telangiectasia in all 28 eyes, vs FA in 11 eyes. On FA, the deep capillary network was barely visible because of the 2-dimensional image photography and blockage by choroidal vessels ( Figure 2 ). OCT angiography easily detected the capillary telangiectasia and the normal capillary networks in the deep layer ( Figure 2 ).


Collateral Vessels (Venovenous Shunt)


OCT angiography detected collateral vessels in 18 eyes, vs FA in 16 eyes. Pre-existing collateral vessels that connected adjacent venous beds were distended and carried more blood, which tended to decrease the retinal venous pressure in the occluded segment. The collateral vessels were present where the occlusive vein was connected to another vein ( Figure 3 ) or a normal (circulated) vein that traversed the nonperfused retina ( Figure 3 ). OCT angiography facilitated differential layer analysis of the collateral vessels ( Figure 3 ) and showed that the collateral vessels were in the superficial and deep layers in all 18 eyes. FA did not clarify the location of the collateral vessels with differential layer analysis in the retina ( Figure 3 ).




Figure 3


Collateral vessels in macular edema associated with branch retinal vein occlusion. Fluorescein angiography (FA) images (Top row) obtained by Optos 200Tx and optical coherence tomography (OCT) angiography images (Bottom row) obtained by AngioVue (scan size, 3 × 3 mm). (Top, second from left and Top, right) Magnified images of the yellow squares in Top left and Top, second from right scans, respectively. (Bottom left) Superficial layer. (Bottom, second from left) Deep layer. The collateral vessel network is obscured on FA (Top, left and Top, second from left), but OCT angiography visualizes the collateral vessel formation in the superficial layer (arrows) (Bottom, left and Bottom, second from right). (Top, right and Bottom, second from right) Bridging collateral vessels (arrows) between occlusive vein and normal circulated vein are observed. Microaneurysms (arrowheads) are detected in the collateral vessels as well.

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Jan 6, 2017 | Posted by in OPHTHALMOLOGY | Comments Off on Microvascular Abnormalities on Optical Coherence Tomography Angiography in Macular Edema Associated With Branch Retinal Vein Occlusion

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