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Electron Microscopy of the Human Choroid
Introduction
The choroid is sandwiched between the sclera and Bruch’s membrane (BM) of the eye. It is the predominant vascular bed of the eye and contains diverse cell types forming the stroma. It performs a number of anatomical, physiological, photoprotective, and immunological functions. Many of these functions are understood from studies employing electron microscopy. This chapter illustrates the structural features of the choroidal elements and how they are related to its functions. An attempt is made to describe how they alter with aging and diseases, for example, age-related macular degeneration (AMD).
Contents of the Choroid
The choroid shows five distinct regions: (1) BM, (2) the choroiocapillaris, (3) Sattler’s layer (with small and medium-sized vessels), (4) Haller’s layer (with large vessels), and (5) the suprachoroid. It is separated from the retina by a composite structure, called BM, which behaves like a filtration barrier to it. Adjoining to BM, there is a layer of capillaries, called choriocapillaris ( Fig. 2.1A and B ), which supplies oxygen and nutrients to the outer retina. The remainder of the choroid, the stroma, is populated by melanocytes, connective tissue elements (fibroblasts, mast cells, elastic, and collagen fibrils), blood vessels ( Fig. 2.1A, C, and D ), macrophages, dendritic cells, lymphocytes, nonvascular smooth muscle cells (NVSMC), intrinsic neurons, and nerve fibers associated with vessels.
Choroidal Thickness
The choroidal thickness varies over its entire extent. It is thicker in the subfoveal zone than elsewhere; the thickness, measured with enhanced depth imaging optical coherence tomography, is reportedly between 250 μm and 330 μm, which is thicker than temporal or nasal counterparts. Choroidal thinning occurs in aging macula, high axial length, and in certain diseases, for example, glaucoma, pseudoxanthoma elasticum, and in birdshot chorioretinopathy. Its thickness remains unaltered in advanced stages of AMD.
Fine Structure of BM
BM is pentalaminate ( Fig. 2.2A ) and consists of (1) the basal lamina of the retinal pigment epithelium (RPE), (2) inner collagenous layer, (3) elastic layer, (4) outer collagenous layer, and (5) the basal lamina of the choriocapillaris endothelium. It measures 2.5–3.0 µm in the submacular zone and 1.5–2.0 µm in the periphery.
Changes in BM in Aging and Diseases
BM alters with age and in AMD. It thickens in submacular region up to 4.7 μm in 10th decade of life due to accumulation of debris ( Fig. 2.2B–F ), such as long-spacing collagens, fibrous-banded materials, vesicles, lipids, and lipoprotein-like particles. The elastic lamina thickens and become irregular in aging ( Fig. 2.2D and E ). In AMD, BM may contain iron in its elastic layer and undergoes calcification and fragmentation, in eyes with exudative AMD. Also, there is formation of drusen, and basal linear deposits (BLinD) between the RPE basal lamina and inner collagenous layer of BM ( Fig. 2.2F ), and basal laminar deposits (BLamD) beneath the RPE basal lamina. Drusen in eyes with AMD may contain carbohydrates, proteins, and abundant neutral lipids in age-related maculopathy. In eyes with AMD, there is an exclusive presence of soft, large, and diffuse drusen and abundant BLamD, whereas large drusen and BLinD are specific for early age-related maculopathy. RPE atrophy leads to formation of large, soft drusen (diameter >30 µm), a risk factor for the onset of neovascular AMD when choroidal vessels grow into RPE. BM deposit results from partial removal of RPE debris, which leads to a decrease of BM permeability. This hampers the diffusion of macromolecules from choriocapillaris to outer retina via BM, resulting in gradual loss of photoreceptors. Due to the decreased BM permeability, RPE-released vascular endothelial growth factor (VEGF) cannot diffuse to the choriocapillaris, leading to its atrophy.
Choriocapillaris
The choriocapillaris is a network of wide-caliber capillaries (diameter: 10–40 μm; Fig. 2.3A ). It is about 10–12 μm thick at the macula and 6–7 μm in the periphery. The macular region contains the highest density of capillaries. Their lumen is lined by endothelial cells whose cytoplasm is attenuated and fenestrated at the retinal aspect ( Fig. 2.3B–D ) and contain Weibel–Palade bodies, pinocytotic vesicles ( Fig. 2.3E ), and intermediate filaments ( Fig. 2.3E–G ). The cells are connected by tight junctions ( Fig. 2.3E ). Outer to the endothelium, there is a layer of pericytes ( Fig. 2.3F and G ) surrounded by the same basal lamina that lines the endothelium ( Fig. 2.3B–G ). Peg and socket joints are present between endothelial cells and pericytes. The pericytes contain large nuclei and intermediate filaments and help in thermoregulation. It is unknown if they are contractile. Cytoplasmic processes from the endothelium often protrude into BM ( Fig. 2.3D ). These may play a role in the maintenance of patency of the vessels and clearance of BM debris.
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