Ophthalmic Surgery, Lasers and Imaging Retina

Clinical Science 

Choriocapillaris Hypoperfusion Artifact in OCT Angiography

Kim Vieira Kayat, MD; Luiz Roisman, PhD; Claudio Zett, MT; Eduardo A. Novais, PhD; Michel Eid Farah, PhD

Abstract

BACKGROUND AND OBJECTIVE:

To illustrate how optical coherence tomography (OCT) angiography (OCTA) can be misinterpreted if not evaluated along with structural en face OCT to analyze the signal intensity.

PATIENTS AND METHODS:

Patients with different macular diseases associated with suspicious flow impairment in the choriocapillaris were recruited to be imaged on the RTVue XR Avanti device (Optovue, Fremont, CA) with the Angio Retina mode. En face OCT angiograms, structural en face OCT, and corresponding OCT B-scans with flow signal overlaid were compared to evaluate the correspondence of signal strength to areas of flow reduction in the choriocapillaris.

RESULTS:

Six eyes from six patients were enrolled. Macular lesions evaluated in this study included acute central serous chorioretinopathy, paracentral acute middle maculopathy, age-related macular degeneration, adult-onset foveomacular vitelliform dystrophy, and branch retinal vein occlusion. In all cases, areas of suspicious flow decrement in the choriocapillaris corresponded to hyporeflective areas in the intensity en face OCT. Thus, a precise confirmation of choriocapillaris flow impairment was not possible.

CONCLUSION:

It is essential to be aware of the importance of analyzing the structural image alongside with the flow image to interpret flow impairment. This is more important in subretinal pigment epithelial structures such as choriocapillaris and choroid.

[Ophthalmic Surg Lasers Imaging Retina. 2018;49:603–610.]

Abstract

BACKGROUND AND OBJECTIVE:

To illustrate how optical coherence tomography (OCT) angiography (OCTA) can be misinterpreted if not evaluated along with structural en face OCT to analyze the signal intensity.

PATIENTS AND METHODS:

Patients with different macular diseases associated with suspicious flow impairment in the choriocapillaris were recruited to be imaged on the RTVue XR Avanti device (Optovue, Fremont, CA) with the Angio Retina mode. En face OCT angiograms, structural en face OCT, and corresponding OCT B-scans with flow signal overlaid were compared to evaluate the correspondence of signal strength to areas of flow reduction in the choriocapillaris.

RESULTS:

Six eyes from six patients were enrolled. Macular lesions evaluated in this study included acute central serous chorioretinopathy, paracentral acute middle maculopathy, age-related macular degeneration, adult-onset foveomacular vitelliform dystrophy, and branch retinal vein occlusion. In all cases, areas of suspicious flow decrement in the choriocapillaris corresponded to hyporeflective areas in the intensity en face OCT. Thus, a precise confirmation of choriocapillaris flow impairment was not possible.

CONCLUSION:

It is essential to be aware of the importance of analyzing the structural image alongside with the flow image to interpret flow impairment. This is more important in subretinal pigment epithelial structures such as choriocapillaris and choroid.

[Ophthalmic Surg Lasers Imaging Retina. 2018;49:603–610.]

Introduction

Optical coherence tomography (OCT) angiography (OCTA) is a diagnostic method that allows for the evaluation of retinal and choroidal vascularization by detecting the movement of red blood cells in the lumen of the vessels without the use of intravenous dye.1,2 Compared to dye-based examinations, OCTA is noninvasive; faster, obtaining the images within seconds; and depth-resolved, whereas fluorescein angiography and indocyanine green angiography provide only two-dimensional images. This allows the segmentation of the retina to different depths and layers, improving the precise localization of the lesion. OCTA has been shown to be useful in evaluating common retinal conditions such as age-related macular degeneration (AMD), diabetic maculopathy, retinal vascular occlusions, central serous chorioretinopathy (CSCR), polypoidal choroidal vasculopathy (PCV), paracentral acute middle maculopathy (PAMM), and others.3–7 Disadvantages of this modality are the limited field of the angiogram; the absence of leakage identification; and the great number of image artifacts, such as projection, shading, and motion artifacts. Therefore, the analysis of OCT angiograms is not simple and requires experience to avoid misinterpretation.7–10

En face structural OCT image, or just structural image, provides the intensity of the signal captured by the OCT angiograms. The loss of the signal can be secondary to increased light blockage or scattering from an overlying layer, resulting in decreased light penetration into the external retina or choroid. If the flow signal in the en face flow image appears absent or reduced, the corresponding structural image needs to be evaluated side-by-side to determine if the flow is truly compromised or whether the OCT signal is diminished. Reduced signal is identified as hyporeflective areas in the structural image. If the intensity signal is reduced, it is impossible to draw any conclusion about whether flow is present, decreased, or simply undetectable due to the diminished intensity signal.9,10 Whatever the reason, the intensity OCT image is crucial for the appropriate interpretation of the OCT angiograms. Some studies have shown decreased choriocapillaris (CC) flow in some diseases such as CSCR, AMD, adult vitelliform maculopathy, PCV, PAMM, and posterior uveitis. However, most of them did not evaluate or include the structural images, prejudicing the analysis of the images by the reader.11–15 Some papers have been published previously regarding the multiple artifacts related to OCTA.10 However, despite these publications, is still common to find publications with misinterpretation of OCTA images, especially concerning the CC.13

This study aims to highlight how signal blockage artifact can be misdiagnosed as CC hypoperfusion in different chorioretinal diseases in clinical practice.

Patients and Methods

This case series study included selected cases of patients who were attended at Ophthalmology Department of the Federal University of São Paulo and Instituto da Visão, São Paulo, Brazil, with different macular diseases, in which questionable hypoperfusion at the level of the CC was present.

The OCT angiograms were acquired using the OCT system (Avanti RTVue XR; Optovue, Fremont, CA) with the Angio-Retina mode. This instrument operates at approximately 840 nm wavelength and 70,000 A-scans per second to acquire OCTA volumes consisting of two repeated B-scans from 304 sequential uniformly spaced locations. Each B-scan consisted of 304 A-scans for a total of 2 × 304 × 304 A-scans per acquisition, with a total acquisition time of approximately 3 seconds, and an axial optical resolution of approximately 5 μm. Split-spectrum amplitude-decorrelation angiography (SSADA) was employed to improve the signal-to-noise ratio.16,17 Motion correction was performed by recording two orthogonally acquired volumes.18,19 The 3 mm × 3 mm and 6 mm × 6 mm volume cubes were used. The images have an A-scan depth of 2 mm in tissue (1,024 pixels). Automated segmentation boundaries allow for separate viewing of the superficial and deep retinal microvascular layers, outer avascular retina, CC, and choroid vasculature. In the current study, automated default of choriocapillaris segmentation was used (top boundary was 31 μm under the RPE and bottom boundary 60 um under the RPE). All en face flow images were analyzed alongside with the en face structural images and corresponding OCTA B-scans for interpretation of the flow results.

Results

Six eyes of six patients with different macular diseases were imaged. In all six cases, a decreased flow signal was seen on the angiogram of the CC secondary to decreased signal, when evaluated with corresponding structural image. The signal loss in the CC happened due to different anatomic alterations such as macular serous detachment, subretinal hyperreflective material, hyperreflective lesions in the middle retinal layers, thickened and hyperreflective RPE, and drusen.

Case 1

A 46-year-old woman followed for acute central serous chorioretinopathy in her right eye had a best-corrected visual acuity (BCVA) of 20/25 in her right eye and 20/20 in her left eye. The OCT B-scan showed a macular serous detachment (Figure 1A). The en face flow image identified an apparently decreased flow of the CC underneath the subretinal fluid (Figure 1B). When compared to the structural image (Figure 1C), this same area of flow impairment corresponded to a hyporeflective area. Therefore, it was not possible to confirm the presence of flow alteration in the CC, since the signal in that region was diminished.

(A) B-scan structural optical coherence tomography (OCT) showing macular serous detachment. The white arrows indicate the extent of the serous detachment. The parallel red lines indicate the automatic segmentation of the choriocapillaris (CC). (B) En face flow image of the CC, demonstrating a dark central area, corresponding to apparent flow impairment. The white arrows in A correspond to the arrows in B, encompassing the detached retina. (C) Structural image of the CC, showing a hyporeflective central area, corresponding to an attenuation of the signal from the CC, probably due to interference by the subretinal fluid. (D) OCT angiography B-scan exhibiting a possible decrease in the decorrelation signal from the CC under the serous detachment (yellow rectangle). The yellow rectangle corresponds to the yellow arrow in C crossing the fovea.

Figure 1.

(A) B-scan structural optical coherence tomography (OCT) showing macular serous detachment. The white arrows indicate the extent of the serous detachment. The parallel red lines indicate the automatic segmentation of the choriocapillaris (CC). (B) En face flow image of the CC, demonstrating a dark central area, corresponding to apparent flow impairment. The white arrows in A correspond to the arrows in B, encompassing the detached retina. (C) Structural image of the CC, showing a hyporeflective central area, corresponding to an attenuation of the signal from the CC, probably due to interference by the subretinal fluid. (D) OCT angiography B-scan exhibiting a possible decrease in the decorrelation signal from the CC under the serous detachment (yellow rectangle). The yellow rectangle corresponds to the yellow arrow in C crossing the fovea.

Case 2

An 83-year-old man followed for exudative AMD in his left eye had a BCVA of 20/50 in the right eye and 20/400 in the left eye. The OCT B-scan showed an irregular elevation of the macular RPE and the presence of subretinal hyperreflective material and subretinal fluid (Figure 2A). The en face flow image demonstrated an area of hypoperfusion in the macular CC (Figure 2B). When compared to the structural image (Figure 2C), the area of flow impairment corresponded to a hyporeflective area, thus demonstrating signal decrease, probably due to blockage of the subretinal material. Therefore, it was not possible to conclude whether there was perfusion alteration in the CC in that region.

(A) B-scan structural optical coherence tomography (OCT) showing submacular hyperreflective material and subretinal fluid. The parallel red lines indicate the automatic segmentation of the choriocapillaris (CC). (B) En face flow image of the CC, showing a dark central area, suggesting hypoperfusion. (C) Structural image of the CC, showing a hyporeflective central area, revealing an attenuation of the signal from the CC, probably due to interference by the subretinal hyperreflective material. (D) OCT angiography B-scan exhibiting a questionable decrease in the decorrelation signal from the CC (yellow rectangle). The yellow rectangle corresponds to the yellow arrow in C crossing the fovea.

Figure 2.

(A) B-scan structural optical coherence tomography (OCT) showing submacular hyperreflective material and subretinal fluid. The parallel red lines indicate the automatic segmentation of the choriocapillaris (CC). (B) En face flow image of the CC, showing a dark central area, suggesting hypoperfusion. (C) Structural image of the CC, showing a hyporeflective central area, revealing an attenuation of the signal from the CC, probably due to interference by the subretinal hyperreflective material. (D) OCT angiography B-scan exhibiting a questionable decrease in the decorrelation signal from the CC (yellow rectangle). The yellow rectangle corresponds to the yellow arrow in C crossing the fovea.

Case 3

A 70-year-old woman followed for PAMM in her left eye had a BCVA of 20/25 in her right eye and counting fingers in her left eye. The OCT B-scan showed hyperreflective changes located at the retinal middle layers (Figure 3A). The en face flow image showed an apparent local hypoperfusion in the CC underneath the area of retinal hyperreflectivity (Figure 3B). This area corresponded to a hyporeflective zone in the structural image (Figure 3C). Therefore, it was not possible to confirm the existence of flow alteration in the CC, since the signal in that region was reduced.

(A) B-scan structural optical coherence tomography (OCT) demonstrating hyperreflectivity of the middle layers of the retina (arrow). The parallel red lines indicate the automatic segmentation of the choriocapillaris (CC). (B) En face flow image of the CC, showing a dark area (arrow) under the retinal alteration. (C) Structural image of the CC, showing a hyporeflective area (arrow), There is an attenuation of the signal from the CC, suggesting a shadowing artifact caused by the hyperreflective retinal alteration. (D) OCT angiography B-scan exhibiting a possible decrease in the decorrelation signal from the CC under the hyperreflective retinal alteration. The yellow rectangle corresponds to the yellow arrow in C.

Figure 3.

(A) B-scan structural optical coherence tomography (OCT) demonstrating hyperreflectivity of the middle layers of the retina (arrow). The parallel red lines indicate the automatic segmentation of the choriocapillaris (CC). (B) En face flow image of the CC, showing a dark area (arrow) under the retinal alteration. (C) Structural image of the CC, showing a hyporeflective area (arrow), There is an attenuation of the signal from the CC, suggesting a shadowing artifact caused by the hyperreflective retinal alteration. (D) OCT angiography B-scan exhibiting a possible decrease in the decorrelation signal from the CC under the hyperreflective retinal alteration. The yellow rectangle corresponds to the yellow arrow in C.

Case 4

A 45-year-old man followed for adult-onset foveomacular vitelliform dystrophy in both eyes, had a BCVA of 20/150 in his right eye and 20/100 in his left eye. The OCT B-scan of the right eye showed submacular hyperreflective accumulation, suggestive of vitelliform material (Figure 4A). The en face flow image showed a diminished perfusion in the CC right under the area of vitelliform lesion (Figure 4B). When evaluating the structural image (Figure 4C), the area of flow impairment in the en face angiogram image demonstrated low signal. Therefore, it was impossible to draw any conclusions regarding choriocapillaris perfusion.

(A) Structural optical coherence tomography (OCT) B-scan shows submacular hyperreflective material between the photoreceptor and retinal pigment epithelium. The parallel red lines indicate the automatic segmentation of the choriocapillaris (CC). (B) En face OCTA flow image of the CC showing a dark central area, suggesting hypoperfusion. (C) Structural image of the CC showing a hyporeflective central area, revealing an attenuation of the signal from the CC, probably due to interference by the submacular hyperreflective material. (D) OCT angiography B-scan exhibiting a questionable decrease in the decorrelation signal from the CC.

Figure 4.

(A) Structural optical coherence tomography (OCT) B-scan shows submacular hyperreflective material between the photoreceptor and retinal pigment epithelium. The parallel red lines indicate the automatic segmentation of the choriocapillaris (CC). (B) En face OCTA flow image of the CC showing a dark central area, suggesting hypoperfusion. (C) Structural image of the CC showing a hyporeflective central area, revealing an attenuation of the signal from the CC, probably due to interference by the submacular hyperreflective material. (D) OCT angiography B-scan exhibiting a questionable decrease in the decorrelation signal from the CC.

Case 5

An 86-year-old woman followed for dry AMD in the left eye had a BCVA of 20/50 in her right eye and 20/100 in her left eye. The OCT B-scan showed some drusen (Figure 5A). The en face flow image showed an apparently decreased flow in the CC under the area of drusenoid detachments of the RPE (Figure 5B). When analyzing the structural image (Figure 5C), this same area of flow impairment corresponded to a hyporeflective area. Thus, it was possible that the hypoperfusion was not real but an artifact caused by the signal attenuation created by the drusen.

(A) Structural optical coherence tomography (OCT) B-scan shows macular drusen. The parallel red lines indicate the automatic segmentation of the choriocapillaris (CC). (B) En face OCTA flow image of the CC, demonstrating a dark central area and some dark spots surrounding (arrows), which indicates apparent flow impairment. (C) Structural image of the CC, showing a hyporeflective central area, corresponding to an attenuation of the signal from the CC, probably caused by the drusen. (D) OCT angiography B-scan demonstrating sparse areas of decreased decorrelation under the drusen. The white arrows represent the same anatomical point as in B and C, corresponding to signal impairment related to the drusen.

Figure 5.

(A) Structural optical coherence tomography (OCT) B-scan shows macular drusen. The parallel red lines indicate the automatic segmentation of the choriocapillaris (CC). (B) En face OCTA flow image of the CC, demonstrating a dark central area and some dark spots surrounding (arrows), which indicates apparent flow impairment. (C) Structural image of the CC, showing a hyporeflective central area, corresponding to an attenuation of the signal from the CC, probably caused by the drusen. (D) OCT angiography B-scan demonstrating sparse areas of decreased decorrelation under the drusen. The white arrows represent the same anatomical point as in B and C, corresponding to signal impairment related to the drusen.

Case 6

An 81-year-old man followed for branch retinal artery occlusion on his right eye had a BCVA of 20/400 in the right eye and 20/30 in the left eye. The B-scan flow signal showed hyperreflective lesion in the middle macular layers, which caused a decrease in the decorrelation signal from the CC (Figures 6A and 6D). The en face flow image showed a presumably decreased flow in the CC right under the area of inner retinal hyperreflectivity (Figure 6B). When compared the en face structural image (Figure 6C), this same area of flow impairment corresponded to a hyporeflective region. It is interesting to observe how the inner retina hyperreflectivity affects the decorrelation signal in the CC, which is less intense the greater the hyperreflective extension is (Figures 6A and 6D).

(A) Optical coherence tomography (OCT) B-scan, corresponding to the red line in B, showing two hyperreflective areas of the middle layers of the retina (white arrows), which coincides with the decrease in the decorrelation signal from the choriocapillaris (CC). (B) OCT angiography en face flow image of the CC showing a dark area in the inferior half of the angiogram, suggesting flow impairment. The white arrows correspond to the hyperreflective lesions in A. (C) Structural image of the CC, exhibiting a hyporeflective area corresponding to the dark region in B, revealing an attenuation of the signal from the CC, probably due to the hyperreflectivity of the middle retina, causing signal reduction from the CC. (D) OCT angiography B-scan, corresponding to the green line in D, a more intense reduction of the decorrelation signal is observed, since this area corresponds to the region with greater retinal hyperreflectivity.

Figure 6.

(A) Optical coherence tomography (OCT) B-scan, corresponding to the red line in B, showing two hyperreflective areas of the middle layers of the retina (white arrows), which coincides with the decrease in the decorrelation signal from the choriocapillaris (CC). (B) OCT angiography en face flow image of the CC showing a dark area in the inferior half of the angiogram, suggesting flow impairment. The white arrows correspond to the hyperreflective lesions in A. (C) Structural image of the CC, exhibiting a hyporeflective area corresponding to the dark region in B, revealing an attenuation of the signal from the CC, probably due to the hyperreflectivity of the middle retina, causing signal reduction from the CC. (D) OCT angiography B-scan, corresponding to the green line in D, a more intense reduction of the decorrelation signal is observed, since this area corresponds to the region with greater retinal hyperreflectivity.

Discussion

OCTA is safe, fast, noninvasive, and can be repeated at every follow-up visit without any known adverse effect. However, many artifacts may affect its interpretation. Thus, experience in evaluating the obtained images is required to avoid misdiagnosis. To improve OCT angiogram quality, manufacturers have rapidly optimized their instruments, implementing better segmentation, better eye-tracking, better algorithms, and software to reduce artifacts.1,8,9,20 The structural image is available in all OCTA devices. However, investigators have neglected its use.13,15,21

The structural image is useful to analyze an area with suspicion of flow impairment in the flow angiogram. If the area of decreased flow in the OCT angiogram corresponds to a hyporeflective area in en face structural OCT, it means that there is a signal blockage in that selected slab; therefore, it is impossible to say whether there is real flow impairment or simply undetectable data. If the same region is accompanied by regular intensity, it is possible to infer that the flow is truly reduced or absent. The loss of signal can occur when the light is scattered by a hyperreflective and/or blocking layer, above the slab of interest, such as a thickened RPE, pigment epithelial detachments, subretinal fluid, subretinal fibrosis, and intraretinal hyperreflective alterations.

In the current study, we chose to use the automated default CC slab to reproduce the daily practice scenario, despite acknowledging that such configuration actually reproduces not exactly the CC but the anterior choroid, because most physicians may not move the boundaries on a routine basis. We then analyzed the generated en face flow images together with the respective structural image and B-scan with flow decorrelation. This same slab was also used in other studies that demonstrated decreased choriocapillaris flow in CSCR, vitelliform and AMD, although none of them showed the structural image alongside with the en face flow angiogram in their figures.12–15,21 Consequently, the reader could not analyze them accurately and determine if there was a real flow reduction in the CC.

Several studies have recently demonstrated the importance of CC perfusion in the pathophysiology and prognosis of many retinal diseases.22–24 Additionally, the quantitative analysis of OCTA images is rapidly gaining relevance and a blocking artifact may underestimate CC perfusion while the unmasking artifact may overestimate it, for example. New software in development may be capable of minimizing the effects of artifacts in the vascular density quantification.

Despite the limitation of a small number of cases, this is a descriptive study to demonstrate how different diseases can lead to the signal blockage artifact on the CC. It is not the aim of the study to find the incidence of this event. Therefore, further studies with a more significant number of patients are needed.

In summary, it is essential to be aware of the importance of analyzing the structural image alongside the flow image to interpret flow impairment. This is more important in sub-RPE structures as CC and choroid, since the RPE is a natural barrier to OCT signal.

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Authors

From the Department of Ophthalmology and Visual Sciences — Paulista School of Medicine, Federal University of São Paulo, São Paulo, Brazil (KK, CZ, EAN, MEF); and Pontificia Universidad Católica de Valparaíso, Valparaíso, Chile (CZ).

This study was supported by the Ophthalmology Department of the Federal University of São Paulo (UNIFESP) / School of Medicine (EPM) and Instituto da Visão — IPEPO, São Paulo, Brazil.

The authors report no relevant financial disclosures.

Address correspondence to Kim Vieira Kayat, MD, Universidade Federal de São Paulo, Departamento de Oftalmologia – Secretaria Administrativa,Rua Botucatu, 821, 1o Andar, São Paulo, 04023-062, Brazil; email: kim_kayat@hotmail.com.

Received: July 09, 2017
Accepted: December 04, 2017

10.3928/23258160-20180803-08

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