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Vitreous and Developmental Vitreoretinopathies Kevin R CHAPTER 3 Vitreous and Developmental Vitreoretinopathies Kevin R. Tozer, Kenneth M. P. Yee, and J. Sebag Invisible (Fig. 3.1) by design, vitreous was long unseen the central vitreous and adjacent to the anterior cortical as important in the physiology and pathology of the eye. gel. HA molecules have a different distribution from col- Recent studies have determined that vitreous plays a sig- lagen, being most abundant in the posterior cortical gel nificant role in ocular health (1) and disease (1,2), includ- with a gradient of decreasing concentration centrally ing a number of important vitreoretinal disorders that and anteriorly (6,7). arise from abnormal embryogenesis and development. Both collagen and HA are synthesized during child- Vitreous embryology is presented in detail in Chapter 1. hood. Total collagen content in the vitreous gel remains Notable is that primary vitreous is filled with blood ves- at about 0.05 mg until the third decade (8). As collagen sels during the first trimester (Fig. 3.2). During the second does not appreciably increase during this time but the trimester, these vessels begin to disappear as the second- size of the vitreous does increase with growth, the den- ary vitreous is formed, ultimately resulting in an exqui- sity of collagen fibrils effectively decreases. This could sitely clear gel (Fig. 3.1). The following will review vitreous potentially weaken the collagen network and destabilize development and the congenital disorders that arise from the gel. However, since there is active synthesis of HA abnormalities in hyaloid vessel formation and regression during this time, the dramatic increase in HA concentra- during the primary vitreous stage and biochemical abnor- tion may stabilize the thinning collagen network (9). malities related to secondary vitreous dysgenesis. Bishop (10) proposed that the leucine-rich repeat protein, opticin, is the predominant structural protein in short-range spacing of collagen fibrils. Scott (11) and BIOCHEMISTRY OF THE VITREOUS BODY Mayne et al. (12) claimed that HA plays a pivotal role in stabilizing the vitreous gel via long-range spacing. At birth, vitreous is composed primarily of collagen However, studies (13) using HA lyase to digest vitreous resulting in a dense appearance on dark-field slit micros- HA found that the gel structure was not destroyed, sug- copy (Fig. 3.3), because collagen scatters light intensely. gesting that HA is not essential for the maintenance of Hyaluronan (HA) synthesis begins after birth. Due to vitreous gel stability, leading to the proposal that colla- considerable hydrophilicity, HA generates a “swelling” gen alone is responsible for the gel state of vitreous (10). pressure within the burgeoning vitreous that contrib- utes to growth of the eye and also spreads apart the collagen fibrils to minimize light scattering inducing PRIMARY VITREOUS transparency (Figs. 3.1 and 3.4). This is evident when comparing dark-field microscopy of a human embryo Vitreous vascularization begins with the hyaloid artery (Fig. 3.3) with similar imaging in a 4-year-old child entering the intraocular space through the optic cup. (Fig. 3.4) (see also Chapter 4). By 10 weeks of gestation (WG), the hyaloid system is There is heterogeneous distribution of collagen well established, branching to form the vasa hyaloi- throughout the vitreous. Chemical (3,4) and light-scat- dea propria (VHP) with anastomoses to a dense capil- tering studies (5) have shown that the highest density of lary network, the tunica vasculosa lentis (TVL), which collagen fibrils is present in the vitreous base, followed is posterior to the lens, and the pupillary membrane by the posterior vitreous cortex anterior to the retina, (PM) adherent to the anterior surface of the lens and and then the anterior vitreous cortex behind the poste- iris diaphragm (14). Maximal development of the hya- rior chamber and lens. The lowest density is found in loid vasculature is reached by 12 to 13 WG (15) although 17 Hartnett9781451151404-ch03.indd 17 6/6/2013 11:06:12 PM 18 SECTION I DEVELOPMENT OF THE EYE AND RETINA FIGURE 3.3 Dark-field slit microscopy of vitreous from a 33-week-gestational-age human. The anterior segment is below where the posterior aspect of the lens can be seen. Coursing through the central vitreous is the remnant of the hyaloid artery, destined to become Cloquet canal. There is considerable light scattering by the gel vitreous. (TGF) has also been implicated in ocular vasculature FIGURE 3.1 Vitreous from a 9-month-old child was remodeling (23). Since all four forms of TGF- were found dissected of the sclera, choroid, and retina. In spite of the β specimen being on a surgical towel exposed to room air, in vitreous hyalocytes, these cells may be involved in the gel state is maintained. (Specimen is courtesy of the the induction of hyaloid vessel regression. Other mech- New England Eye Bank.) anisms may be involved. There is evidence that family members of the Wnt signaling pathway, particularly Wnt7b expressed in macrophages, are involved in nor- evidence of regression is apparent as early as 11 WG mal hyaloid regression (24) in the mouse, although this (16). The hyaloid system shows clear signs of regres- mechanism has not been confirmed in humans. sion by 13 to 15 WG beginning in the VHP followed by the TVL and then the PM (16–18). Although the precise biochemical process involved SECONDARY VITREOUS in hyaloid vasculature formation and regression is poorly defined, studies have shown that vascular endothelial Secondary (avascular) vitreous formation arises from growth factor (VEGF) may trigger the growth of the a remodeling of the earlier primary (vascular) vitreous TVL and PM (19–22). Thus, decreased VEGF levels may (25). By the 40- to 60-mm stage in humans, the VHP has induce vascular regression. Transforming growth factor FIGURE 3.4 Dark-field slit microscopy of vitreous from a FIGURE 3.2 Human primary vitreous featuring the 4-year-old child. The posterior aspect of the lens is seen hyaloid artery (3) arising from the optic disc and below. Other than the peripheral vitreous cortex that con- branching to form the VHP (2), which anastomoses with tains densely packed collagen fibrils, there is little light the TVL and PM (1). scattering within the vitreous body. Hartnett9781451151404-ch03.indd 18 6/6/2013 11:06:14 PM CHAPTER 3 VITREOUS AND DEVELOPMENTAL VITREORETINOPATHIES 19 reached maximum maturity and regression begins (22). The posterior VHP is the first component to degenerate. The regression continues to move centrally affecting the TVL and finally the hyaloid artery itself. Although flow through the hyaloid artery is decreasing during this time, ceasing entirely around the 240-mm stage, the artery may continue to elongate as the eye lengthens (26). As the pri- mary vitreous regresses, its remnants provide a frame- work for collagen fibrils of the secondary vitreous that form via interactive remodeling. As this occurs, the pri- mary and secondary vitreous coexist in the same space during this transitional developmental period (25,26). VITREOUS STRUCTURE In the human embryo, vitreous structure (27–33) has a dense homogenous appearance (Fig. 3.3) primarily as a result of the aforementioned collagen synthesis during secondary vitreous formation. HA synthesis after birth separates collagen fibrils, inducing transparency (Fig. 3.4). In the absence of diabetes and myopia, vitreous remains largely transparent until around the fifth decade when fine, parallel fibers appear coursing in an anteroposterior direction (Fig. 3.5B and C) (2,30–32). The fibers arise from the vitreous base (Fig. 3.5H) where they insert anterior and posterior to the ora serrata. As the peripheral fibers course posteriorly, they are circumferential with the vit- reous cortex, while central fibers “undulate” in a con- figuration parallel with Cloquet canal (33). The fibers are continuous and do not branch. Posteriorly, these fibers insert into the vitreous cortex (Fig. 3.5E and F). Ultrastructural studies (34) have demonstrated that collagen fibrils are the only microscopic structures that could correspond to these fibers. These studies also FIGURE 3.5 Dark-field slit microscopy of human vitreous detected the presence of bundles of packed, parallel col- in eyes dissected of the sclera, choroid, and retina. The anterior segment is below and the posterior pole is above lagen fibrils. Eventually, the aggregates of collagen fibrils in all images. (Courtesy of the New York Eye Bank for attain sufficiently large proportions so as to be visual- Sight Restoration.) ized in vitro (Fig. 3.5) and clinically. The areas adjacent to these large fibers have a low density of collagen fibrils separated by HA molecules and therefore do not scatter (Fig. 3.5H). The anterior-most fibers form the “anterior light as intensely as the bundles of collagen fibrils. loop” of the vitreous base, a structure that is important in the pathophysiology of anterior proliferative vitreo- Vitreous Base retinopathy (2,39–41). Studies by Gloor and Daicker (42) Vitreous base is a three-dimensional zone extending showed that cords of vitreous collagen insert into gaps 1.5 to 2 mm anterior to the ora serrata, 1 to 3 mm poste- between the neuroglia of the peripheral retina. They rior to the ora serrata (35), and several millimeters into likened this structure to Velcro (a self-adhesive nylon the vitreous body itself (36). The posterior extent of the material) and proposed that this would explain the posterior border of the vitreous base varies with age strong vitreoretinal adhesion at this site. In the anterior (37,38). In a variety of vitreoretinal developmental dis- vitreous base, fibrils interdigitate with a reticular com- orders, the temporal vitreous never forms; thus, there is plex of fibrillar basement membrane material between a different peripheral terminus bounded by vitreous gel the crevices of the nonpigmented ciliary epithelium posteriorly and liquid vitreous anteriorly (see below).
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