Choriocapillaris, Photoreceptors, and Inner Retinal Layer in Spatial Relationship to Parapapillary Alpha, Beta, Gamma, and Delta Zones

Abstract

Purpose: To examine the spatial relationships between the retinal inner nuclear layer (INL), outer nuclear layer (ONL), retinal pigment epithelium (RPE) layer, Bruch's membrane (BM), and choriocapillaris in the parapapillary region.

Methods: Human eyes enucleated due to uveal melanomas or secondary angle-closure glaucoma were histomorphometrically examined. We compared the tissue dimensions between four groups of eyes categorized based on the presence/absence of high myopia and glaucoma.

Results: The investigation consisted of 100 globes (axial length: 25.6 ± 3.1 mm; range: 20.0-35.0 mm). In non-highly myopic nonglaucomatous eyes, the INL, ONL, RPE, BM, and choriocapillaris ended approximately at the end of the RPE layer, with no significant (all P ≥ 0.10) difference between the layers in their distance to the RPE-layer end. From non-highly myopic nonglaucomatous eyes to non-highly myopic glaucomatous eyes, highly myopic nonglaucomatous eyes, and eventually highly myopic glaucomatous eyes, the choriocapillaris, INL, and ONL increasingly extended into the beta zone, most marked for the choriocapillaris and least marked for the ONL. A larger extension of the choriocapillaris into the parapapillary beta zone correlated with longer axial length (standardized regression coefficient β, 0.24; B, 23.0; 95% confidence interval [CI], 1.6-44.5; P = 0.04) and wider parapapillary beta zone (β, 0.59; B, 0.32; 95% CI, 0.22-0.41; P < 0.001); a larger extension of the INL correlated with longer axial length (β, 0.34; B, 43.7; 95% CI, 11.6-75.7; P = 0.009), longer gamma zone (β, 0.52; B, 0.28; 95% CI, 0.15-0.41; P < 0.001), and diagnosis of non-highly myopic glaucoma (β, 0.28; B, 267; 95% CI, 80.8-454; P = 0.006); and a larger extension of the ONL into parapapillary beta zone correlated with longer axial length (β, 0.50; B, 32.2; 95% CI, 21.6-42.8; P < 0.001) and wider parapapillary beta zone (β, 0.28; B, 0.10; 95% CI, 0.04-0.16; P < 0.001).

Conclusions: Nonglaucomatous non-highly myopic eyes differ from highly myopic eyes and glaucomatous eyes in the spatial relationship of the parapapillary tissue layers.

Figure 1.

(a) Histophotograph of the parapapillary region showing the parapapillary regions alpha and beta. Extension of the retinal inner nuclear layer, retinal outer nuclear layer, and open choriocapillaris layer into beta zone. (b) Histophotograph of the parapapillary region showing the parapapillary regions alpha and beta. Higher magnification of (a). Extension of the retinal inner nuclear layer, retinal outer nuclear layer, and open choriocapillaris layer into the beta zone.

Figure 2.

(a) Histophotograph of the parapapillary region in a highly myopic eye and showing the parapapillary regions alpha, beta, and gamma. Extension of the retinal inner nuclear layer, retinal outer nuclear layer, and open choriocapillaris layer into the beta zone and gamma zone. (b) Histophotograph of the parapapillary region in a highly myopic eye and showing the parapapillary regions alpha, beta, and gamma. Higher magnification of (a).

Figure 3.

(a) Histophotograph of the parapapillary region in a highly myopic eye and showing the parapapillary regions of alpha zone, gamma zone, and delta zone. Extension of the retinal inner nuclear layer, retinal outer nuclear layer, and open choriocapillaris layer into the gamma zone and delta zone. Since the end of the retinal pigment epithelium layer coincides with the end of Bruch's membrane, the beta zone is not present. (b) Histophotograph of the parapapillary region in a highly myopic eye and showing the parapapillary regions of the alpha zone and gamma zone. Since the end of the retinal pigment epithelium layer coincides with the end of Bruch's membrane, the beta zone is not present. Higher magnification of (a).

Figure 4.

Graph showing the distribution of the distance of the photoreceptor layer end to the retinal pigment epithelium end in the parapapillary region (correlation coefficient r² = 0.50).

Figure 5.

Graph showing the distribution of the distance of the retinal inner nuclear layer end to the retinal pigment epithelium end in the parapapillary region (correlation coefficient r² = 0.43).

Figure 6.

Schema showing the spatial relationships of the retinal inner nuclear layer, outer nuclear layer, RPE layer, and choriocapillaris in the parapapillary region of an emmetropic nonglaucomatous eye (upper part) and of an emmetropic glaucomatous eye (lower part). In the emmetropic nonglaucomatous eye, all parapapillary tissues end mostly at the level of the end of the lamina cribrosa. In the emmetropic glaucomatous eye, in particular on the temporal side, Bruch's membrane is free of RPE cells (beta zone), followed by a region of Bruch's membrane covered by an irregularly structured RPE (alpha zone). The inner nuclear layer more than the outer nuclear layer and the choriocapillaris extend into the beta zone. In addition, the lamina cribrosa is condensed and the optic cup is deepened.

Figure 7.

Schema showing the spatial relationships of the retinal inner nuclear layer, outer nuclear layer, RPE layer, and choriocapillaris in the parapapillary region of a moderately myopic eye (upper part) and of a highly myopic eye (lower part). In the temporal parapapillary region of the moderately myopic eye, the end of Bruch's membrane has receded from the level of the end of the lamina cribrosa. The Bruch's membrane-free parapapillary region is called the gamma zone. The parapapillary part of Bruch's membrane is free of RPE cells (beta zone). The inner nuclear layer more than the outer nuclear layer and the choriocapillaris extend into the beta zone and partially into the gamma zone. On the nasal side, Bruch's membrane together, with the choriocapillaris and the outer and inner nuclear layer, are overhanging into the nasal part of the intrapapillary compartment and covering the nasal part of the lamina cribrosa. The overhanging part of Bruch's membrane corresponds to the temporal parapapillary region without Bruch's membrane (gamma zone). The peripapillary border tissue of the choroid is elongated (by the amount of the width of the gamma zone) and thinned. The size of the optic disc (defined as the ophthalmoscopically visible part of the lamina cribrosa with or without neuroretinal rim) is reduced due to the nasally overhanging Bruch's membrane. In the highly myopic eye, the end of Bruch's membrane has receded from the lamina cribrosa on all sides, so a circular gamma zone is present. The parapapillary part of Bruch's membrane is free of RPE cells on all sides, leading to a circular beta zone. Again, the inner nuclear layer more than the outer nuclear layer and the choriocapillaris extends into the beta zone and partially into gamma zone. The peripapillary border tissue of the choroid is markedly elongated (by the amount of the width of the gamma zone) and thinned. The size of the optic disc (defined as the ophthalmoscopically visible part of the lamina cribrosa with or without neuroretinal rim) is enlarged, since Bruch's membrane is (no longer) overhanging into the intrapapillary compartment and since the lamina cribrosa has become elongated (and thinned).