Quantitative Analysis of Outer Retinal Tubulation in Age-Related Macular Degeneration From Spectral-Domain Optical Coherence Tomography and Histology

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Abstract

Purpose

To assess outer retinal tubulation (ORT) morphology from spectral-domain optical coherence tomography (SD-OCT) volumes and donor eye histology, analyze ORT reflectivity, and estimate the number of cones surviving in ORT.

Methods

In SD-OCT volumes from nine patients with advanced AMD, ORT was analyzed en face and in B-scans. The hyperreflective ORT border in cross-section was delineated and surface area calculated. Reflectivity was compared between ORT types (Closed, Open, Forming, and Branching). A flatmount retina from a donor with neovascular AMD was labeled to visualize the external limiting membrane that delimits ORT and allow measurements of cross-sectional cone area, center-to-center cone spacing, and cone density. The number of cones surviving in ORT was estimated.

Results

By en face SD-OCT, ORT varies in complexity and shape. Outer retinal tubulation networks almost always contain Closed cross-sections. Spectral-domain OCT volumes containing almost exclusively Closed ORTs showed no significant direction-dependent differences in hyperreflective ORT border intensity. The surface areas of partial ORT assessed by SD-OCT volumes ranged from 0.16 to 1.76 mm ². From the flatmount retina, the average cross-sectional area of cone inner segments was 49.1 ± 7.9 μm ². The average cone spacing was 7.5 ± 0.6 μm. Outer retinal tubulation cone density was 20,351 cones/mm ². The estimated number of cones in ORT in a macula ranged from 26,399 to 186,833 cones, which is 6% to 44% of the cones present in a healthy macula.

Conclusions

These first estimates for cone density and number of cones surviving in ORT suggest that ORT formation considerably distorts the photoreceptor mosaic. Results provide additional insight into the reflectivity characteristics and number of ORT cones observable in living patients by SD-OCT, as cones persist and disease progresses.

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Most cited references 34

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Proposed lexicon for anatomic landmarks in normal posterior segment spectral-domain optical coherence tomography: the IN•OCT consensus.

Giovanni Staurenghi, Srinivas Sadda, Usha Chakravarthy … (2014)

To develop a consensus nomenclature for the classification of retinal and choroidal layers and bands visible on spectral-domain optical coherence tomography (SD-OCT) images of a normal eye.

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Anatomical correlates to the bands seen in the outer retina by optical coherence tomography: literature review and model.

Richard Spaide, Christine A. Curcio (2011)

To evaluate the validity of commonly used anatomical designations for the four hyperreflective outer retinal bands seen in current-generation optical coherence tomography, a scale model of outer retinal morphology was created using published information for direct comparison with optical coherence tomography scans. Articles and books concerning histology of the outer retina from 1900 until 2009 were evaluated, and data were used to create a scale model drawing. Boundaries between outer retinal tissue compartments described by the model were compared with intensity variations of representative spectral-domain optical coherence tomography scans using longitudinal reflectance profiles to determine the region of origin of the hyperreflective outer retinal bands. This analysis showed a high likelihood that the spectral-domain optical coherence tomography bands attributed to the external limiting membrane (the first, innermost band) and to the retinal pigment epithelium (the fourth, outermost band) are correctly attributed. Comparative analysis showed that the second band, often attributed to the boundary between inner and outer segments of the photoreceptors, actually aligns with the ellipsoid portion of the inner segments. The third band corresponded to an ensheathment of the cone outer segments by apical processes of the retinal pigment epithelium in a structure known as the contact cylinder. Anatomical attributions and subsequent pathophysiologic assessments pertaining to the second and third outer retinal hyperreflective bands may not be correct. This analysis has identified testable hypotheses for the actual correlates of the second and third bands. Nonretinal pigment epithelium contributions to the fourth band (e.g., Bruch membrane) remain to be determined.

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Photoreceptor loss in age-related macular degeneration.

N Medeiros, David C Millican, B. Curcio (1996)

The authors showed previously that parafoveal rods, but not cones, decrease during the course of adulthood in donor eyes that were screened to exclude the grossly visible macular drusen and pigmentary disturbances typical of age-related macular degeneration (AMD). Because AMD begins in the parafovea, this selective loss of rods actually may be subclinical AMD not yet visible in the fundus. If so, AMD must have a predilection for rods over cones. The authors tested this hypothesis by determining the relative numbers of cones and rods in donor eyes with mid-to late-stage AMD and in age-matched controls. Thirteen eyes (from seven donors) with grossly visible macular drusen and pigmentary disturbances were either wholemounted for photoreceptor counts or sectioned through the fovea for histopathology and carbonic anhydrase histochemistry to label red-green cones. Eyes were assigned to AMD or control groups on the basis of histopathology and clinical history. Five nonexudative AMD (NE-AMD) eyes from three donors showed sparing of foveal cones and loss of rods and cones in the parafovea. In two donors, rod loss exceeded cone loss at most parafoveal locations, and in one donor, rod density was normal and cone density was reduced. In eight exudative AMD (EX-AMD) eyes from five donors, photoreceptors surviving along the margins of and overlying disciform scars were largely cones. Photoreceptors are lost in NE-AMD as well as in the more severe exudative form, consistent with functional and clinical studies. The authors propose that rods die in older eyes without evidence of overt retinal pigment epithelial disease. In persons susceptible to AMD, the retinal pigment epithelium becomes dysfunctional. Secondarily, rod loss continues and cones begin to degenerate. Eventually, only degenerate cones remain; ultimately, all photoreceptors may disappear.

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Author and article information

Journal

Journal ID (nlm-ta): Invest Ophthalmol Vis Sci

Journal ID (iso-abbrev): Invest. Ophthalmol. Vis. Sci

Journal ID (hwp): iovs

Journal ID (pmc): iovs

Journal ID (publisher-id): iovs

Title: Investigative Ophthalmology & Visual Science

Publisher: The Association for Research in Vision and Ophthalmology

ISSN (Print): 0146-0404

ISSN (Electronic): 1552-5783

Publication date (Electronic): 13 May 2016

Publication date (Print): May 2016

Volume: 57

Issue: 6

Pages: 2647-2656

Affiliations

[1 ]Department of Ophthalmology University of Alabama School of Medicine, University of Alabama at Birmingham, Birmingham, Alabama, United States

[2 ]Vision Science Graduate Program, University of Alabama at Birmingham, Birmingham, Alabama, United States

[3 ]Department of Ophthalmology, University Hospital Würzburg, Würzburg, Germany

[4 ]Department of Computer and Information Sciences, University of Alabama at Birmingham, Birmingham, Alabama, United States

[5 ]Vitreous Retina Macula Consultants of New York, New York, New York, United States

[6 ]Department of Ophthalmology, New York University School of Medicine, New York, New York, United States

Author notes

Correspondence: Christine A. Curcio, Department of Ophthalmology, EyeSight Foundation of Alabama Vision Research Laboratories, University of Alabama School of Medicine, 1670 University Boulevard, Room 360, Birmingham, AL 35294-0099, USA; curcio@ 123456uab.edu .

Article

Serial Item and Contribution ID: iovs-57-04-73 Publisher ID: IOVS-16-19262

DOI: 10.1167/iovs.16-19262

PMC ID: 4868096

PubMed ID: 27177321

SO-VID: 6d77d27a-77ab-4ace-869e-7187450b88ab

License:

This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

Quantitative Analysis of Outer Retinal Tubulation in Age-Related Macular Degeneration From Spectral-Domain Optical Coherence Tomography and Histology

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Abstract

Purpose

Methods

Results

Conclusions

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Karger: Ophthalmology

Most cited references 34

Proposed lexicon for anatomic landmarks in normal posterior segment spectral-domain optical coherence tomography: the IN•OCT consensus.

Anatomical correlates to the bands seen in the outer retina by optical coherence tomography: literature review and model.

Photoreceptor loss in age-related macular degeneration.

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