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Quantitative Optical Coherence Tomography Angiography of Vascular Abnormalities in the Living Human

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Quantitative Optical Coherence Tomography Angiography of Vascular Abnormalities in the Living Human Quantitative optical coherence tomography PNAS PLUS angiography of vascular abnormalities in the living human eye Yali Jiaa, Steven T. Baileya, Thomas S. Hwanga, Scott M. McClintica, Simon S. Gaoa, Mark E. Pennesia, Christina J. Flaxela, Andreas K. Lauera, David J. Wilsona, Joachim Horneggerb, James G. Fujimotoc, and David Huanga,1 aCasey Eye Institute, Oregon Health & Science University, Portland, OR 97239; bPattern Recognition Lab and School of Advanced Optical Technologies, University Erlangen-Nuremberg, D-91058 Erlangen, Germany; and cDepartment of Electrical Engineering and Computer Science and Research Laboratory of Electronics, Massachusetts Institute of Technology, Cambridge, MA 02139 Edited by Morton Goldberg, The Johns Hopkins Wilmer Eye Institute, Baltimore, MD, and accepted by the Editorial Board March 26, 2015 (received for review January 6, 2015) Retinal vascular diseases are important causes of vision loss. A develop a no-injection, dye-free method for 3D visualization of detailed evaluation of the vascular abnormalities facilitates diagno- ocular circulation. sis and treatment in these diseases. Optical coherence tomography In recent years, several OCT angiography methods have been (OCT) angiography using the highly efficient split-spectrum ampli- developed to detect changes in the OCT signal caused by flowing tude decorrelation angiography algorithm offers an alternative to red blood cells in blood vessels. Initially, Doppler OCT angiog- conventional dye-based retinal angiography. OCT angiography has raphy methods were investigated for the visualization and mea- several advantages, including 3D visualization of retinal and cho- surement of blood flow (3–8). Because Doppler OCT is only roidal circulations (including the choriocapillaris) and avoidance of sensitive to motion parallel to the OCT probe beam, it is limited dye injection-related complications. Results from six illustrative in its ability to image retinal and choroidal circulations, which cases are reported. In diabetic retinopathy, OCT angiography can are predominantly perpendicular to the OCT beam. More recent detect neovascularization and quantify ischemia. In age-related approaches, based on detecting variation in the speckle pattern macular degeneration, choroidal neovascularization can be ob- over time, are sensitive to both transverse and axial flow. Several served without the obscuration of details caused by dye leakage types of speckle-based techniques have been described, including in conventional angiography. Choriocapillaris dysfunction can be amplitude-based (9–11), phase-based (12), or a combination of detected in the nonneovascular form of the disease, furthering our both amplitude and phase (13) variance methods. ’ understanding of pathogenesis. In choroideremia, OCT s ability to We developed an amplitude-based method called split-spectrum show choroidal and retinal vascular dysfunction separately may be amplitude-decorrelation angiography (SSADA). The SSADA al- valuable in predicting progression and assessing treatment re- gorithm detects motion in the blood vessel lumen by measuring the sponse. OCT angiography shows promise as a noninvasive alter- variation in reflected OCT signal amplitude between consecutive native to dye-based angiography for highly detailed, in vivo, 3D, cross-sectional scans. The novelty of SSADA lies in how the OCT quantitative evaluation of retinal vascular abnormalities. optical coherence tomography angiography | ophthalmic imaging | Significance ocular circulation Retinal vascular diseases are a leading cause of blindness. Optical coherence tomography (OCT) has become the standard ptical coherence tomography (OCT) has become the most imaging modality for evaluating fluid accumulation in these commonly used imaging modality in ophthalmology. It pro- O diseases and for guiding treatment. However, fluorescein an- vides cross-sectional and 3D imaging of the retina and optic giography (FA) is still required for initial evaluation of retinal nerve head with micrometer-scale depth resolution. Structural ischemia and choroidal neovascularization, which are not visi- OCT enhances the clinician’s ability to detect and monitor fluid ble in conventional structural OCT. The limitations of FA include exudation associated with retinal vascular diseases. Whereas poor penetration of fluorescence through blood and pigment, anatomical alterations that impact vision are readily visible, inability to determine the depth of the pathology due to its structural OCT has a limited ability to image the retinal or two-dimensional nature, and some uncommon but potentially choroidal vasculatures. Furthermore, it is unable to directly de- severe complications. As a noninvasive three-dimensional al- tect capillary dropout or pathologic new vessel growth (neo- ternative, OCT angiography may be used in routine screening MEDICAL SCIENCES vascularization) that are the major vascular changes associated and monitoring to provide new information for clinical diag- with two of the leading causes of blindness, age-related macular nosis and management. degeneration (AMD) and diabetic retinopathy (1). To visualize these changes, traditional i.v. contrast dye-based angiography Author contributions: Y.J., S.T.B., T.S.H., M.E.P., C.J.F., A.K.L., D.J.W., and D.H. designed re- techniques are currently used. search; J.H. and J.G.F. contributed new reagents/analytic tools; Y.J., S.T.B., T.S.H., S.M.M., S.S.G., Fluorescein dye is primarily used to visualize the retinal vas- M.E.P., C.J.F., A.K.L., D.J.W., and D.H. analyzed data; and Y.J., S.T.B., T.S.H., S.M.M., S.S.G., M.E.P., culature. A separate dye, indocyanine green (ICG), is necessary and D.H. wrote the paper. ENGINEERING to evaluate the choroidal vasculature. Both fluorescein angiog- Conflict of interest statement: Oregon Health & Science University (OHSU), Y.J., J.G.F., and D.H. have a significant financial interest in Optovue, Inc., a company that may have a raphy (FA) and ICG angiography require i.v. injection, which is commercial interest in the results of this research and technology. These potential con- time consuming, and which can cause nausea, vomiting, and, flicts of interest have been reviewed and managed by OHSU. J.G.F. and D.H. receive rarely, anaphylaxis (2). Dye leakage or staining provides infor- royalties on an optical coherence tomography patent licensed by the Massachusetts In- mation regarding vascular incompetence (e.g., from abnormal stitute of Technology (MIT) to Carl Zeiss Meditec. J.G.F. and J.H. receive royalties from intellectual property owned by MIT and licensed to Optovue, Inc. Other authors do not capillary growth), but it also obscures the image and blurs the have financial interest in the subject of this article. boundaries of neovascularization. Additionally, conventional an- This article is a PNAS Direct Submission. M.G. is a guest editor invited by the Editorial giography is 2D, which makes it difficult to distinguish vascular Board. abnormalities within different layers. Therefore, it is desirable to 1To whom correspondence should be addressed. Email: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1500185112 PNAS | Published online April 20, 2015 | E2395–E2402 Downloaded by guest on September 25, 2021 signal is processed to enhance flow detection and reject axial bulk this technique, both blood flow and retinal structural information motion noise. Compared with the full-spectrum amplitude method, are presented on a single image. SSADA using fourfold spectral splits improved the signal-to-noise En face presentation of OCT angiography is comparable to ratio (SNR) by a factor of two, which is equivalent to reducing the the traditional view of dye-based angiography and is necessary scan time by a factor of four (14). More recent SSADA imple- for clinicians to identify vascular patterns. Segmented en face mentations use even more than a fourfold split to further enhance OCT angiograms can be displayed as individual retinal and the SNR of flow detection. This highly efficient algorithm gener- choroidal circulations (Fig. 1 C and E). In healthy eyes, the vit- ates high-quality angiograms of both the retina and choroid. The reous and outer retinal layers are colored black (Fig. 1 B and D), angiograms have capillary-level detail and can be obtained with representing the absence of flow. currently available commercial OCT systems. In vivo imaging of the choroid is limited with current imaging This article uses six illustrative cases and highlights the various modalities (15). High-quality OCT angiograms of the chorioca- μ types of vascular pathologies that can be detected and measured pillaris can be obtained by segmenting a thin slice (10 m) of the ’ E using SSADA and an OCT angiography system of visualization. inner choroid below Bruch s membrane (Fig. 1 ). The larger and Additionally, we describe techniques designed to help clinicians deeper choroidal vessels are more difficult to visualize with rapidly interpret OCT angiograms and to easily identify patho- SSADA-based OCT angiography because choriocapillaris flow logical vascular features. These techniques include (i) separation causes a flow projection artifact in the deeper layers. Selective removal of this artifact is impossible, given the near confluent of the 3D angiogram into individual vascular beds via segmenta- nature of the choriocapillaris. Another reason is that high flow in tion algorithms, (ii) presentation of en face OCT angiograms, the larger choroidal vessels reduces the OCT signal due to
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