The Vasculature of Choroid

Imran A. Bhutto and Gerard A. Lutty

Wilmer Ophthalmological Institute, Johns Hopkins Hospital, Baltimore, Maryland

The choroidal microvasculature lies immediately under or posterior to the retina. Although the gross choroidal anatomy is well known, little information is available on the arrangement of arterioles and venules and their relationship to the choriocapillaris. This chapter will focus on mammalian choroids because avian choroids are uniquely different.

Gross Anatomy

The choroid is considered to be the ocular homolog of the pia arachnoid in brain. It is a long, thin, vascular, and pig-mented tissue, which forms the posterior portion of the uveal tract (the iris, ciliary body, and choroid). Because of its great vascularity, the choroid has some of the properties of erectile tissue. Its capillaries form a very unusual pattern, being arranged in a single layer restricted to the inner portion of the choroid; this arrangement enables the capillary layer to provide nutrition for the outer retina (Figure 1). The choroidal stroma contains a considerable number of pig-mented melanocytes, which are distributed through all areas of the choroid, although they are more sparse in the innermost layers. The pigment in the melanocytes gives the choroid its characteristic dusky brown color. The choroid has an extensive nerve supply, and many ganglion cells can be found in the stroma and suprachoroidea. The choroid is easily detached from the sensory retina and from the sclera (the collagenous coat of the eye), but it is firmly bound to the optic nerve, because its connective tissue is continuous with that of the optic nerve.

Internally, the choroid is so closely attached to the retina that the retinal pigment epithelium adheres more to Bruch's membrane than to the retinal photoreceptors. Bruch's membrane is the anatomical border between retina and choroid (Figure 1). The area around the choriocapillaris has little or no pigment (Figure 1). Externally the pigmented supra-

choroidal connective tissue lamellae are closely bound to those of the lamina fusca of the sclera, the border of choroid and sclera.

The thickness of the choroid is difficult to determine because it diminishes after enucleation or fixation; it has been estimated to be approximately 0.1mm anteriorly and 0.22 mm posteriorly, with greatest thickness under the macula. The choroidal vasculature in primates is composed of the choriocapillaris (an internal or anterior layer), medium-sized vessels (Sattler's layer), and large arteries measuring 40 to 90 mm, large veins measuring 20 to 100 mm (Haller's layer), nerves, and lymphatics (Figure 2).

The Choroidal Vasculature and Associated Structures

Arteries

There are three main arterial sources of blood to the choroid. The long posterior ciliary arteries (LPCA, temporal, and nasal) follow long, oblique intrascleral courses and, therefore, are easily affected by scleritis. The LPCAs travel in the potential suprachoroidal space and send branches from the ora serrata region posteriorly to supply the choroid as far posterior as the anatomical equator. A ciliary nerve accompanies each LPCA. The second arterial source is the short posterior ciliary arteries (SPCA, 15 to 20 in number) that supply the choroid from equator to optic nerve. The distribution of their entry is perifoveal, peripapillary, or in a compromise pattern, the papillomacular oval. The arteries surround the optic nerve (the circle of Zinn), penetrating and then branching peripherally in a wheel-shaped arrangement. The radial areas supplied by the arteries are separated by watersheds and are triangular, with the apices directed toward the fovea. A watershed zone in choroid is an area that normally fills slowly with blood. Hayreh [1], one of the pio

Figure 1 Section from the eye of a rhesus monkey showing retina from the internal limiting membrane (ILM) at the interface of retina and vitreous to the retinal pigment epithelial cells (RPE). Retinal blood vessels (white arrows) are in the ganglion cell layer (GCL) of inner retina, and also a secondary or deep plexus is associated with the inner nuclear layer; their inner and outer segments are below the external limiting membrane (ELM). The nuclei of the photoreceptors are in the outer nuclear layer (ONL). Below Bruch's membrane (BM) is the choroid with choriocapillaris (CC), immediately posterior to Bruch's membrane and large choroidal vessels posterior in the densely pigmented outer choroid. (see color insert)

Figure 1 Section from the eye of a rhesus monkey showing retina from the internal limiting membrane (ILM) at the interface of retina and vitreous to the retinal pigment epithelial cells (RPE). Retinal blood vessels (white arrows) are in the ganglion cell layer (GCL) of inner retina, and also a secondary or deep plexus is associated with the inner nuclear layer; their inner and outer segments are below the external limiting membrane (ELM). The nuclei of the photoreceptors are in the outer nuclear layer (ONL). Below Bruch's membrane (BM) is the choroid with choriocapillaris (CC), immediately posterior to Bruch's membrane and large choroidal vessels posterior in the densely pigmented outer choroid. (see color insert)

neers in the study of the choroidal vasculature, has done extensive in vivo experimental studies on choroidal circulation and its watershed zones in human. He has shown that the choroidal vascular bed is a strictly segmental and end-arterial system and has watershed zones situated between the various PCAs, the short PCAs, the choroidal arteries, the arterioles, and the vortex veins. The nature of the choroidal vasculature and the existence of watershed zones in the choroid are of great clinical importance and play a significant role in the production of various ischemic lesions in the choroid. The final arterial source of blood is the anterior ciliary arteries, which send recurrent branches posteriorly to supply the choroid at 3 o'clock and 9 o'clock soon after they pierce the anterior sclera. The arteries of all three vessel systems rapidly extend internally via arterioles to supply blood to the choriocapillaris. Mast cells are intimately associated with most choroidal arteries.

Choroidal Veins (Vortex Veins)

The main venous drainage of the choroid occurs through four to six vortex veins that drain into superior and inferior ophthalmic veins. Postcapillary venules are closely arranged

Eye Choroid Vasculature

Figure 2 A vascular cast of the choroidal vasculature of a dog. The oval-shaped choriocapillaris (arrow) are at the top with draining venules below connecting to a large vein (asterisk). This section of the cast is the area of the tapedum lucidum, so the venules are more elongated to traverse the tapedum than they would be in a primate.

Figure 2 A vascular cast of the choroidal vasculature of a dog. The oval-shaped choriocapillaris (arrow) are at the top with draining venules below connecting to a large vein (asterisk). This section of the cast is the area of the tapedum lucidum, so the venules are more elongated to traverse the tapedum than they would be in a primate.

in the macular region. In this area, the venous portion predominates over the arterial one. The meshwork of the venous plexus becomes less dense with increasing distance from the macula. In the extramacular region, the vessels are straighter, losing the tortuousity that is characteristic of the macular region. Vessels of larger lumen form the subcapil-laris plexus and eventually flow into the vortex veins. Venous drainage is segmentally organized into quadrants, with watersheds oriented horizontally through the disc and fovea and vertically through the papillomacular region. The macula is centered over both arterial and venous watersheds, which may either predispose it to relative ischemia or prevent ischemia through multiple submacular blood supplies.

Choriocapillaris

The choriocapillaris, located solely in the internal portion of the choroid, appears as a nonhomogenous network of large (20 to 50 mm) capillaries (Figure 2). This monolayer vascular network, flattened in the anterior-posterior aspect, changes from a dense, honeycomb-like, nonlobular structure in the peripapillary area to a lobule-like pattern in submacu-lar areas and most of the posterior pole and equatorial areas (Figure 3). In the peripheral area, choriocapillaries form more elongated, palmlike or fanlike vascular networks, and finally form arcades that terminate at the ora serrata [2]. The network of choriocapillaris is supplied by feeding arterioles derived from the short posterior ciliary arteries and drained by the collecting venules (Figure 2). These arterioles and venules form the medium-sized vessels of the choroid occupying the choroidal stroma (Sattler's layer). The majority of these vessels in the peripapillary and submacular areas form a 90-degree angle with the posterior aspect of the chorio-capillaris (Figure 2). The choriocapillaris lobules measure 0.6 to 1.0 mm (Figure 3).

There is controversy over the idea that "lobules" exist and subdivide the choroid into many functional islands. One hypotheses suggests that the choriocapillaris is a single, continuous capillary vascular layer; although lobules were anatomically separated, they were functionally interconnected. The other hypothesis proposed by Hayreh [1] has advocated the presence of noncommunicating lobules. On the basis of fluorescein angiography findings he described a

Choroicapillaris

Figure 3 (A) Alkaline phosphatase incubated normal human choroid after bleaching. In this area of choroid near the macula, the lobular organization of the choriocapillaris is apparent. There is a draining venule (asterisk) in the center of this lobule. (B) Section through the center of the lobule shown in (A) shows blue APase activity in choriocapillaris lumens (arrow) and in the draining venuole (asterisk). The internal limiting membrane (arrowhead) is PAS positive. RPE cells have been removed from Bruch's membrane in processing. (Blue APase reaction product, PAS, and hematoxylin stain.) (see color insert)

Figure 3 (A) Alkaline phosphatase incubated normal human choroid after bleaching. In this area of choroid near the macula, the lobular organization of the choriocapillaris is apparent. There is a draining venule (asterisk) in the center of this lobule. (B) Section through the center of the lobule shown in (A) shows blue APase activity in choriocapillaris lumens (arrow) and in the draining venuole (asterisk). The internal limiting membrane (arrowhead) is PAS positive. RPE cells have been removed from Bruch's membrane in processing. (Blue APase reaction product, PAS, and hematoxylin stain.) (see color insert)

mosaic of lobules, each one containing an arteriole in the middle and a venule at its periphery.

There is disagreement as well about the location of arte-rioles and venules in the lobule. Shimizu and Ujiie [3] confirmed the central location of the artery and the peripheral location of the venule. On the contrary, McLeod and Lutty [2], who performed histologic studies of the chorio-capillaris stained with alkaline phosphatase reaction product, described a lobular organization of the choroid with arterioles and venules located peripherally and centrally, respectively, in most lobules.

Bruch's Membrane (Lamina Vitrea)

Bruch's membrane is a thin noncellular lamina separating the choriocapillaris from the retinal pigment epithelium (RPE). Ultrastructurally, it is composed of the basement membrane of the retinal pigment epithelium (inner basal lamina; 0.3 mm thick); inner collagenous zone (1.5 mm thick); elastic fibers; outer collagenous zone (0.7 mm thick); and basement membrane of the choriocapillaris (0.14 mm thick). Bruch's membrane is eosinophilic and PAS-positive. Mallory and other connective tissue stains show its collagen, and elastic tissue stains show that the membrane contains a well-developed layer of elastic tissue. The inner collagenous layer is thick and may degenerate and split with age. The elastic layer distribution is much more diffuse posteriorly. The basal lamina of the choriocapillaris is incomplete in that it is limited to the actual capillaries and absent at the inter-capillary septa.

Retinal Pigment Epithelial (RPE) Cells

RPE cells form the outer blood retinal barrier (BRB). RPE cells measure 16 mm in height and 10 to 60 mm in diameter; they feature apical zonulae occludens (the outer BRB). The RPE nucleus is basal, and its pigment is apical and therefore distant from the choriocapillaris (Figure 1). Inner choroidal vessels (choriocapillaris and medium-sized vessels) are sandwiched between apical RPE pigment of neu-roepithelial origin and outer choroidal pigment of neural crest origin.

Visualization of the Choroidal Vasculature

In vivo visualization of the choroid in humans is difficult because of pigmentation of the RPE and choroidal melanocytes. Angiography can be accomplished with sodium fluorescein in lightly pigmented or albino eyes, but not in darkly pigmented fundi as observed in humans of African descent. Angiography with indocyanine green dye, which absorbs and fluoresces in the infrared, has provided the best tool to view the choroidal vasculature in any pigmented fundus. ICG angiography clearly shows blood flow in large choroidal blood vessels, but only high-speed ICG

angiography with pulsed laser light source provides enough resolution to study the choriocapillaris [4].

McLeod and Lutty developed an alkaline phosphatase technique to study histologically the human, cat, and dog choroidal vasculature postmortem [2]. By incubating the excised choroid for alkaline phosphatase histochemical activity and then bleaching the choroid, the choroidal vas-culature can be studied at high resolution. The choroid can then be flat-embedded in glycol methacrylate and viewed in dual perspective: choroidal vessel pattern in the flat perspective; vessels of interest sectioned and viewed in cross section as well (Figure 3). Only viable choroidal vessels have alkaline phosphatase activity, so sites of vascular dropout can be studied in detail.

The corrosion cast technique is also an excellent method for studying the three dimensional properties of the choroidal vasculature postmortem [3]. A polymer is injected into the vasculature and allowed to polymerize, and then the tissue is digested away from the polymer. After coating the cast with gold palladium, the vasculature can be viewed in three dimensions with scanning electron microscopy (Figure 2).

Essentials of Human Physiology

Essentials of Human Physiology

This ebook provides an introductory explanation of the workings of the human body, with an effort to draw connections between the body systems and explain their interdependencies. A framework for the book is homeostasis and how the body maintains balance within each system. This is intended as a first introduction to physiology for a college-level course.

Get My Free Ebook


Post a comment