Choriocapillaris Imaging Using Multiple En Face Optical Coherence Tomography Angiography Image Averaging

Abstract

Importance: Imaging of the choriocapillaris in vivo is challenging with existing technology. Optical coherence tomography angiography (OCTA), if optimized, could make the imaging less challenging.

Objective: To investigate multiple en face image averaging on OCTA images of the choriocapillaris.

Design, setting, and participants: Observational, cross-sectional case series at a referral institutional practice in Los Angeles, California. From the original cohort of 21 healthy individuals, 17 normal eyes of 17 participants were included in the study. The study dates were August to September 2016.

Exposures: All participants underwent OCTA imaging of the macula covering a 3 × 3-mm area using OCTA software (Cirrus 5000 with AngioPlex; Carl Zeiss Meditec). One eye per participant was repeatedly imaged to obtain 9 OCTA cube scan sets. Registration was first performed using superficial capillary plexus images, and this transformation was then applied to the choriocapillaris images. The 9 registered choriocapillaris images were then averaged. Quantitative parameters were measured on binarized OCTA images and compared with the unaveraged OCTA images.

Main outcome and measure: Vessel caliber measurement.

Results: Seventeen eyes of 17 participants (mean [SD] age, 35.1 [6.0] years; 9 [53%] female; and 9 [53%] of white race/ethnicity) with sufficient image quality were included in this analysis. The single unaveraged images demonstrated a granular appearance, and the vascular pattern was difficult to discern. After averaging, en face choriocapillaris images showed a meshwork appearance. The mean (SD) diameter of the vessels was 22.8 (5.8) µm (range, 9.6-40.2 µm). Compared with the single unaveraged images, the averaged images showed more flow voids (1423 flow voids [95% CI, 967-1909] vs 1254 flow voids [95% CI, 825-1683], P < .001), smaller average size of the flow voids (911 [95% CI, 301-1521] µm2 vs 1364 [95% CI, 645-2083] µm2, P < .001), and greater vessel density (70.7% [95% CI, 61.9%-79.5%] vs 61.9% [95% CI, 56.0%-67.8%], P < .001). The distribution of the number vs sizes of the flow voids was skewed in both unaveraged and averaged images. A linear log-log plot of the distribution showed a more homogeneous distribution in the averaged images compared with the unaveraged images.

Conclusions and relevance: Multiple en face averaging can improve visualization of the choriocapillaris on OCTA images, transforming the images from a granular appearance to a level where the intervascular spaces can be resolved in healthy volunteers.

Figure 1.. Quantitative Image Analysis of the Choriocapillaris Optical Coherence Tomography Angiography (OCTA) Images

A, Single unaveraged OCTA image of the superficial capillary plexus. B, Single unaveraged OCTA image of the choriocapillaris. C, Binarized choriocapillaris image (B) for quantitative analysis of the flow voids. White area is the flow voids. D, Binarized choriocapillaris image (B) for quantitative analysis of the vessels. White area is the vessels. In both C and D, the shadow of the major retinal vessels and the foveal avascular zone were masked and eliminated from the analyses. E, Averaged OCTA image of the superficial capillary plexus. The image shows more continuous vessels and less background noise compared with the single unaveraged image (A). F, Averaged OCTA image of the choriocapillaris. After averaging, the poorly defined granular appearance observed in B was transformed to a meshwork appearance. G, Binarized choriocapillaris image (F) for quantitative analysis of the flow voids. White area is the flow voids. The average size of the flow voids is smaller than those in the single unaveraged image (C). H, Binarized choriocapillaris image (F) for quantitative analysis of the vessels. White area is the vessels. Vessel area is greater than those in the single unaveraged image (G).

Figure 2.. Difference in Granular Pattern of the Choriocapillaris Between the Single Unaveraged Optical Coherence Tomography Angiography Images

A-C, Three images of the choriocapillaris slab from different optical coherence tomography angiography cube scan sets of the left eye of a woman in her early 40s. The single unaveraged choriocapillaris en face images each showed a granular appearance. The bright areas are thought to represent blood flow, and the dark areas are believed to indicate areas of impaired or absent flow (flow voids [the area without flow information]). D-F, Magnified views of the insets in A-C. The pattern of this granular appearance can be seen to change from image to image, although there is some overlap (white circle).

Figure 3.. Comparison Between the Unaveraged and Averaged Optical Coherence Tomography Angiography (OCTA) Images of the Choriocapillaris

A-C, Single unaveraged OCTA images of the choriocapillaris. A, The right eye of a man in his mid-30s. B, The left eye of a man in his late 30s. C, The right eye of a woman in her early 30s. D-F, The OCTA images after averaging multiple frames (A-C). The granular appearance observed in the single unaveraged images was transformed to a more apparent meshwork appearance in the averaged images. The vessels were densely packed, and the averaged images showed a smaller proportion of the dark area (flow voids [the area without flow information]). The flow voids were homogeneously distributed, and most of them appeared to be similar in size, although several larger flow voids may be seen.

Figure 4.. Averaged Optical Coherence Tomography Angiography Image of the Choriocapillaris

A, Averaged optical coherence tomography angiography image of the choriocapillaris. After averaging, en face choriocapillaris images revealed a meshwork structure reminiscent of the histology of the human choriocapillaris (B). The flow voids in the foveal avascular zone area are less detectable than those outside the foveal avascular zone area. Scale bar = 500 μm. B, Scanning electron micrograph of the corrosion vascular cast from macular choriocapillaris (original magnification ×135). Asterisks indicate postcapillary venules. The image is reproduced and adapted with permission from the study by Yoneya and Tso. Video. Registration of the Multiple Optical Coherence Tomography Angiography Images of Superficial Capillary Plexus