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Optical Imaging of the Chorioretinal Vasculature in the Living Human Eye Optical imaging of the chorioretinal vasculature in the living human eye Dae Yu Kima, Jeff Finglera, Robert J. Zawadzkib, Susanna S. Parkb, Lawrence S. Morseb, Daniel M. Schwartzc, Scott E. Frasera,1, and John S. Wernerb,1 aBiological Imaging Center, California Institute of Technology, Pasadena, CA 91125; bDepartment of Ophthalmology and Vision Science, University of California, Davis, Sacramento, CA 95817; and cDepartment of Ophthalmology, University of California, San Francisco, CA 94143 Edited* by Napoleone Ferrara, University of California, San Diego, La Jolla, CA, and approved July 9, 2013 (received for review April 18, 2013) Detailed visualization of microvascular changes in the human retina cells, as well as atrophy of the underlying CC and choroidal is clinically limited by the capabilities of angiography imaging, a vessels (4–6). GA regional identification is typically accomplished 2D fundus photograph that requires an intravenous injection of using autofluorescence imaging techniques, which depend on fluorescent dye. Whereas current angiography methods enable lipofuscin accumulation within RPE cells associated with this visualization of some retinal capillary detail, they do not ade- disease, but the current clinical imaging methods are limited in quately reveal the choriocapillaris or other microvascular features detecting early morphological changes in the choriocapillaris beneath the retina. We have developed a noninvasive microvas- (7, 8). An improved understanding of the progression of GA cular imaging technique called phase-variance optical coherence and its underlying mechanisms is important to develop potential tomography (pvOCT), which identifies vasculature three dimen- therapeutic targets for intervention, and diagnostic tools capable sionally through analysis of data acquired with OCT systems. The of observing the key features of atrophic AMD are critical for fulfilling this goal. pvOCT imaging method is not only capable of generating capillary Optical coherence tomography (OCT) is a noninvasive clinical perfusion maps for the retina, but it can also use the 3D capabilities diagnostic tool that performs high-resolution (few micrometers), to segment the data in depth to isolate vasculature in different 3D cross-sectional imaging of the retina (9, 10). Current OCT layers of the retina and choroid. This paper demonstrates some of imaging provides detailed retinal morphology that correlates the capabilities of pvOCT imaging of the anterior layers of well with histologic findings. Although high-resolution OCT is choroidal vasculature of a healthy normal eye as well as of eyes capable of depicting structural alterations of the outer retinal with geographic atrophy (GA) secondary to age-related macular layers including the RPE layer in patients with atrophic AMD degeneration. The pvOCT data presented permit digital segmenta- (11), conventional OCT imaging provides limited visualization of tion to produce 2D depth-resolved images of the retinal vascula- the retinal and choroidal circulation. Recently, the enhanced ture, the choriocapillaris, and the vessels in Sattler’sandHaller’s depth imaging technique demonstrated cross-sectional images of layers. Comparisons are presented between en face projections of choriocapillaris and larger choroidal vessels with improved OCT pvOCT data within the superficial choroid and clinical angiography sensitivity in the choroid to measure choroidal thickness (12, 13). images for regions of GA. Abnormalities and vascular dropout ob- To image retinal and choroidal vasculature noninvasively, we served within the choriocapillaris for pvOCT are compared with have developed phase-variance optical coherence tomography regional GA progression. The capability of pvOCT imaging of the (pvOCT), which calculates contrast based on the motion ob- microvasculature of the choriocapillaris and the anterior choroi- served over time of the 3D OCT data. This additional contrast dal vasculature has the potential to become a unique tool to method allows for in vivo visualization of volumetric morphology evaluate therapies and understand the underlying mechanisms of retinal and choroidal microvasculature with high sensitivity of age-related macular degeneration progression. as well as presentation of the vascular data in the form of depth- encoded 2D perfusion maps of the retina. A principal benefitof ocular circulation | ocular vasculature | optical angiography | pvOCT for translational research and further clinical applica- ophthalmic imaging | Fourier-domain optical coherence tomography tions is that this is a data analysis technique that can be adapted for use by clinically available OCT systems without requiring any hardware modifications. Composite imaging of conventional urrent clinical evaluation of outer retinal disease progression OCT intensity images and pvOCT images highlights localiza- Cis accomplished with multiple imaging modalities including tion of vascular changes in three dimensions, which may allow fl fundus photography, uorescein angiography (FA), indocyanine for more accurate diagnosis of changes in CC that may lead to fl green angiography (ICGA), fundus auto uorescence (FAF), and GA. In addition, disruptions in the photoreceptors and RPE fl near infrared auto uorescence (1, 2). Whereas angiography that may be associated with these vascular changes can also be techniques are ideal to observe retinal and choroidal circulation, studied simultaneously. the lack of depth selectivity limits the ability to observe micro- vasculature in the choriocapillaris (CC) and the anterior choroid. Results FA is typically limited to retinal vasculature due to light ab- We acquired OCT volumetric data of the macula (posterior ret- sorption by the retinal pigment epithelial (RPE) cells and leakage ina) of a normal human subject and one AMD patient with GA. of fluorescein from the choriocapillaris, whereas ICGA primarily Using a custom-built Fourier-domain OCT (Fd-OCT) system, we images only the larger choroidal vessels. The development of a unique noninvasive method for visualizing changes in the RPE layer and CC with high resolution could advance our un- Author contributions: D.Y.K., S.E.F., and J.S.W. designed research; D.Y.K., J.F., and R.J.Z. derstanding of disease progression and invites unique oppor- performed research; D.Y.K., S.S.P., L.S.M., and D.M.S. analyzed data; and D.Y.K., J.F., tunities for early diagnosis, timely treatment, and evaluating R.J.Z., S.S.P., L.S.M., D.M.S., S.E.F., and J.S.W. wrote the paper. potential therapeutics. The authors declare no conflict of interest. One of the major applications of noninvasive choroidal *This Direct Submission article had a prearranged editor. imaging is for late stages of age-related macular degeneration Freely available online through the PNAS open access option. (AMD), the leading cause of central visual loss and legal 1To whom correspondence may be addressed. E-mail: [email protected] or sefraser@ blindness in Americans 65 y of age and older (3). Geographic caltech.edu. atrophy (GA), one of the common features of AMD, involves This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. the progressive loss of the retinal photoreceptors and the RPE 1073/pnas.1307315110/-/DCSupplemental. 14354–14359 | PNAS | August 27, 2013 | vol. 110 | no. 35 www.pnas.org/cgi/doi/10.1073/pnas.1307315110 Downloaded by guest on September 27, 2021 performed pvOCT imaging scans over retinal areas of 1.5 × 1.5 mm2 progresses. One major difficulty in studying the changes in CC and 3 × 3mm2 with an acquisition time of 3.6 s in addition to scans has been its anatomical location below the photoreceptors and of 1.5 × 3mm2 and 3 × 1.5 mm2 acquired in 6.9 s. Healthy retinal the highly pigmented RPE, where most of the incident light is areas at the macula and the peripheral retina were imaged for absorbed or scattered. The CC consists of lobules of fenestrated comparison with atrophic areas in AMD. The pvOCT images capillary plexus in the macula. These features make CC difficult were created using postprocessing procedures including phase- to visualize by FA and ICGA. variance–based analysis to identify motion contrast as well as Our OCT angiographic technique, pvOCT, allows in vivo segmentation of the 3D data for visualizing vasculature both in visualization of the retinal and choroidal circulation with depth the retina and the choroid. Details of the phase-variance pro- information. The cross-sectional composite image (Fig. 1C) cessing and visualization for pvOCT are described in Fig. S1. scanned at the retinal location identifiedbytheyellowdashed line in Fig. 1A emphasizes vascular depth information (red) Microcirculation in the Retina and the Choroid. Fundus FA has available in the retina and the choroid. This cross-sectional served as the gold standard for imaging the retinal vasculature and (B-scan) image was a combination of the standard Fd-OCT its abnormalities, including but not limited to microaneurysms, B-scan (Fig. S3A) and the phase variance processed contrast capillary nonperfusion, and neovascularization. In addition, for the same location (Fig. S3B). An en face projection of the fundus ICGA has been mainly used to identify choroidal vascular pvOCT volumetric data (Movie S1) enables visualization of abnormalities, although it visualizes both retinal and choroidal capillary perfusion maps of different posterior layers. The retinal circulation. Unlike FA, the absorption (∼790–800 nm) and vasculature (Fig. 1D) was segmented from the retinal
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