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1: Interpretation of Stereo Ocular Angiography : 
Retinal and Choroidal Anatomy

An understanding of the anatomy of the retina and choroid, and of the descriptive terminology applied to both, is critical when interpreting fluorescein and ICG angiography. The retina is a complex matrix of neural cells lining the innermost wall of the globe. It is a specialized structure that may be described both clinically and anatomically.

From a clinical perspective, the retina emanates at the optic disc and extends anteriorly to the ora serrata. The optic disc represents the confluence of the retinal nerve fiber layer (NFL) as it exits the globe. The retina is divided into the macular area within the central posterior pole and the peripheral fundus. The peripheral retina is further subdivided into the midperipheral (posterior to the equator) and far peripheral (anterior to the equator) retina, with their junction at the equator of the globe (Figure 1-3).

fig. 1-3

FIGURE 1-3. The posterior pole and peripheral retina.

The macula is subdivided into the umbo, foveola, fovea, parafovea, and perifovea areas. The umbo is the center of the foveola (Figure 1-4). Diagnostically and therapeutically important landmarks of the macula include the foveola, fovea, FAZ, and macular xanthophyll. When macular topography is distorted, the distribution of yellow macular xanthophyll is helpful in macular identification. These structures must be recognized as an integral part of the therapeutic decision-making process; for example, recognition of the margin of the FAZ is impor-tant when photocoagulation of diabetic microaneurysms or CNVMs is considered. Histologic support for this clinical stratification is based on the number of cellular lay-ers and associated nuclei present in each area of the macula. The fovea consists of the internal limiting mem-brane, outer plexiform layer, outer nuclear layer, and photoreceptor layer. The outer plexiform layer is oriented obliquely in the fovea, in contradistinction to its perpendicular orientation in the peripheral macula, which explains the petaloid pattern of cystoid macular edema.

fig. 1-4

FIGURE 1-4. Regions in the macular area of the retina defined on fluorescein angiography. The foveola is the central fovea and measures 0.35 mm across, centered at the umbo. Most of the yellow xanthophyll pigment is concentrated in the foveola. The fovea is the central depression of the macula, measuring 0.5 mm across, and is surrounded by a 0.5-mm zone called the parafovea. Surrounding the parafovea is a 1.5-mm zone called the penfovea, where the ganglion cells are depleted from five layers to a single layer. (FAZ = foveal avascular zone.)

The parafoveal area contains the largest number of nerve cells (i.e., seven rows of ganglion cell nuclei, 12 rows of inner nuclear layer nuclei, and four to five rows of nuclei in the outer nuclear layer) and the thickest outer plexi-form layer in the macula. The perifoveal area begins pos-teriorly with four layers of ganglion cell nuclei and gradually thins to a single layer at its periphery as it blends into the midperipheral retina at approximately 2.75 mm from the umbo. The perifovea also contains five to six rows of outer nuclear layer nuclei, a significantly thinner outer plexiform layer, and six to seven rows of nuclei in the inner nuclear layer. The remainder of the retina contains a single nuclear layer of ganglion cells. Both mid- and far peripheral retina progressively thin as they approach the ora serrata, and the ratio of cones to rods reverses from the fovea to the retinal far periphery.

Histologically, the retinal and choroidal tissue complex is composed of multiple layers (Figure 1-5) that subserve its visual function. They include, from anterior to posterior, the nerve fiber layer, ganglion cell layer, inner plexiform layer, inner nuclear layer, outer plexiform layer, outer nuclear layer, external limiting membrane, outer segment photoreceptor layer (rods and cones), RPE, Bruch's membrane, choriocapillaris, and choroid.

fig. 1-5

FIGURE 1-5. The layers of the retina. (Reprinted with permission from PJ Saine, ME Tyler. Ophthalmic Photography. Boston: Butterworth-Heinemann, 1997;46.)

The RPE is a layer of tight junction pigment cells that forms the outer blood-retina barrier. It serves a critical function in its role as the scavenger of decaying photoreceptor debris and waste disposal system for the retina. The pigment of the RPE also functions as a filter during angiography, obscuring the more posteriorly located choroid, choriocapillaris, and sclera (Figure 1-6).

fig. 1-6

FIGURE 1-6. The cellular tight junctions of the retinal pigment epithelium effectively separate the retinal and choroidal circulation during fluorescein angiography. (Reprinted with permission from P3 Saine, ME Tyler. Ophthalmic Pho-tography. Boston: Butterworth-Heinemann, 1997;281.)

Contiguous with and underlying the RPE, Bruch's membrane is a sandwich-like collagenous layer that provides connective tissue support for the RPE anteriorly and the choriocapillaris posteriorly. Bruch's membrane is composed of the basal lamina of the RPE, thick collagen, elastic fibers, thin collagen, and the basement membrane of the choriocapillaris. It interdigitates with the chorio-capillary vascular channels externally, and there is no potential tissue space between Bruch's membrane and the choriocapillaris, as there may be between its inner boundary and the RPE.

The choriocapillaris, the choroid, and the systemic circulation that supplies them represent the primary source of macular perfusion for the RPE and outer retina. The remaining oxygen supply emanates from the macular retinal arterioles.

The choroid is the posterior portion of the uveal tract and represents a high-flow vascular mesh composed of arteries, veins, melanocytes, and the choriocapillaris, as well as a supportive connective-tissue framework interspersed with a regulatory nervous system. The chorio-capillaris has a lobular form in the posterior pole.1° From a central feeder choroidal arteriole, precapillary arterioles emanate, each supplying an individual choriocapillary lobule (Figure 1-7). The arteriole enters the lobule centrally, and venules forming the perimeter of the lobular vascular ring drain into the choroidal veins. The chorio-capillaris has fenestrated vascular walls with a relatively large luminal diameter. Hence it represents a high-flow, non-tight junction capillary system that leaks fluorescein and ICG dye during angiography. An appreciation of the typical right angle by which the choroidal precapillary arteriole enters the choriocapillaris lobule and the oblique angle of exit of the postcapillary venule is helpful when the ICG angiographic interpreter begins to develop pattern recognition skills. Although the angiographic patterns defined by fluorescein angiography have been well described, those observed on ICG angiography are less obvious. There is a normal potential space between the choroid and surrounding sclera posteriorly, but only significant pathologic disorders allow creation of a space between Bruch's membrane and the RPE, and between the RPE and overlying sensory retina.

fig. 1-7

FIGURE 1-7. The lobular structure of the choroid. Note the arterioles (A) entering the center of each Lobule and the circumreferential venous drainage (V) of the lobule perimeter. (Courtesy of Lee Allen.)

The retinal circulation perfuses the inner retina (bounded by the nerve fiber layer anteriorly and the inner nuclear layer posteriorly) via the central retinal artery. The retinal blood vessels are located in the inner retina, which they perfuse primarily. They are lined by endothelial cells with tight junctions, constituting the blood—inner retina barrier. This barrier, in concert with the blood—outer retina barrier formed by the tight junction between the RPE and Bruch's membrane, is responsible for regulating the extra-cellular fluid milieu of the retinal cellular component and thereby maintaining optimal retinal function. A break in the integrity of these barriers may result in intraretinal and sub-RPE fluid accumulation, with secondary reduction in visual function.

The source of the central retinal artery (CRA) is the ophthalmic artery, which is the major conduit to both the retina and choroid. The ophthalmic artery arises as the first branch of the internal carotid artery, passes through the optic canal within the dural sheath of the optic nerve, and branches into many variable tributaries. The most important branches from the perspective of posterior seg-ment blood flow are the medial and lateral posterior cil-iary arteries, each of which divides into a long posterior ciliary artery (LPCA) and multiple short posterior ciliary arteries (SPCAs), and the CRA, which enters the globe with the optic nerve before again branching into the four major retinal vascular arcades. The LPCAs enter the globe near the optic nerve, course anteriorly along the horizontal meridian through the suprachoroidal space, and then reflect posteriorly to supply the choriocapillaris anterior to the equator." The SCPAs enter the globe and then thesuprachoroidal space, dividing and perfusing the chorio-capillaris posterior to the equator. Anterior ciliary arteries (which follow the rectus muscles) also supply the anterior choriocapillaris. Cilioretinal vessels radiate temporally from the optic nerve through the papillomacular bundle, providing an accessory blood supply to the macular inner retina from the ciliary circulation.

The retinal veins follow a similar pattern, draining the inner retina via four vascular arcades into the central retinal vein, which shares a common adventitial sheath with the CRA as they exit the globe through the lamina cribrosa of the optic nerve. The retinal veins are generally posterior to the arteries at vessel crossing points as they traverse the inner retina, and they complete the vascular circuit of blood through the retina by draining the inter-mediary capillary bed fed by the arterial system. This cap-illary bed may be further subdivided into the radial peripapillary capillary bed and the capillaries at the level of the inner nuclear layer and nerve fiber—ganglion cell layers.12 The central retinal vein drains into the cavernous sinus, although it may occasionally drain via the superior ophthalmic vein.

The vortex venous system drains the majority of the choriocapillaris via quadrantic vortex veins. These major veins are connected to a saccular venous ampulla, which collects blood from the postcapillary venules. The vortex veins drain into the superior (SOV) and inferior ophthalmic veins (IOV). The SOV drains into the cavernous sinus via the superior orbital fissure and the IOV drains into the pterygoid plexus through the inferior orbital fissure.


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