Spatially resolved imaging of human macular capillaries using adaptive optics-enhanced optical coherence tomography angiography

Abstract

Documenting the organization of the retinal capillaries is of importance to understand the visual consequences of vascular diseases which may differentially affect the microvascular layers. Here we detailed the spatial organization of the macular capillaries in ten healthy human subjects using a prototypic adaptive optics-enhanced optical coherence tomography angiography (AO-OCTA) system. Within the central 6° × 6°, the radial peripapillary capillaries and the superficial, intermediate and deep vascular plexuses (SVP, IVP and DVP, respectively) were consistently resolved. In 8 out of the 10 eyes, the capillary segments composing the perifoveal arcade (PFA) were perfused only by the SVP, while drainage of the PFA showed more variability, comprising a case in which the PFA was drained by the DVP. Around the center, a distinct central avascular zone could be documented for each layer in 7 of the 10 cases; in three eyes, the IVP and SVP merged tangentially around the center. In all eyes, the foveal avascular zone was larger in the DVP than in the SVP and IVP. In one eye with incomplete separation of the inner foveal layers, there was continuity of both the SVP and the IVP; a central avascular zone was only present in the DVP. The diversity of perfusion and drainage patterns supported a connectivity scheme combining parallel and serial organizations, the latter being the most commonly observed in perifoveal vessels. Our results thus help to further characterize the diversity of organization patterns of the macular capillaries and to robustly analyze the IVP, which will help to characterize early stages of microvascular diseases.

Keywords: Fovea; Macula; Microcirculation; Optical coherence tomography angiography; Retina.

Figure 1

Adaptive optics optical coherence tomography angiography (AO-OCTA) imaging of the microvascular plexuses of subject 1. A to C: Montages of the superficial (SVP) (A), intermediate (IVP) (B) and deep vascular plexus (DVP) (C). The fovea is marked with an asterisk in the SVP. D to G: Magnification of the orange rectangle from A showing the radial peripapillary capillaries (D), the SVP (E), the IVP (F), and the DVP (G). The yellow and the blue rectangles correspond to Supplementary Video 1 and Supplementary Video 2, respectively. All scale bars represent 100 microns.

Figure 2

Illustration of different connectivity patterns of an arteriole in the SVP from subject 1 (magnification of the yellow rectangle in Fig. 1, see also supplementary video 1). A to F: successive AO-OCTA slabs from the SVP (A) to the IVP (F). The white arrows follow a vessel emerging from an arteriole that perfuses the IVP without branching into the SVP. The green arrows follow a capillary in the SVP that branches into the IVP. The red arrowheads follow a capillary that drains in the SVP (A: arteriole, V: venule).

Figure 3

Illustration of venous connectivity patterns in subject 1 (blue rectangle in Fig. 1). The presumed location of the transverse (vertical) vein is indicated by the blue arrows. The white arrows show the emergence of a vein from the IVP to the SVP. The pink arrows show an example of a vein emerging from the DVP to the SVP without connecting to the IVP. The presence of separate, superimposed venous confluences in the three layers suggests that the SVP and IVP each have their own drainage pathway (See also Supplementary Video 2).

Figure 4

Tracings of the perifoveal area of subject 5 splitted by capillary layers. The perifoveal area is supplied by the SVP and drained by the DVP. Note the precapillary arteriole contributing to the PFA. The diameter of the circles fitting the FAZ were 260 µm, 290 µm and 370 µm in the SVP, IVP and DVP, respectively.

Figure 5

Comparison of the central capillary-free zones of the SVP, IVP and DVP for each patient (y axis: diameter of the largest fitting circle in µm). Each line represents one patient.

Figure 6

Correlation between neuronal and vascular structures. Tracings of subjects 1 (A), 5 (B) and 8 (C) and corresponding B-scans (D, E and F). The capillaries of the SVP are traced in green, the capillaries of the IVP are traced in magenta and the capillaries of the DVP are traced in blue. The central foveal thickness is indicated on each B-scan (D, E and F). Note that the slight difference in foveal structure between subjects 5 and 8 contrasts with the profound changes in foveal capillary coverage.

Figure 7

Tracings of perifoveal vessels in subject 8 splitted by capillary layers. The central avascular zone is only visible in the DVP (See also supplementary video 5). Note that the SVP over the center forms a venous confluence.