Ophthalmic Surgery, Lasers and Imaging Retina

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Imaging 

Scattered Lamellar Microholes as a Complication of Epiretinal Membranes

Marie-Hélène Errera, MD; Salomon-Yves Cohen, MD; Sadri Chahed, MD; Alain Gaudric, MD

Abstract

The authors present two cases of an unusual pattern of the fundus corresponding to multiple “scattered lamellar microholes” located at the periphery of thick and contractile idiopathic epiretinal membranes. The retinal defects were documented with blue reflectance fundus photographs and three-dimensional spectral domain optical coherence tomography. They seem to correspond to multiple small areas of partial-thickness or lamellar disruptions of the retina. The authors suggest that the contraction of the epiretinal membrane may have caused tangential traction on the adjacent inner retina, creating disruptions in the internal limiting membrane and inner retina.

Abstract

The authors present two cases of an unusual pattern of the fundus corresponding to multiple “scattered lamellar microholes” located at the periphery of thick and contractile idiopathic epiretinal membranes. The retinal defects were documented with blue reflectance fundus photographs and three-dimensional spectral domain optical coherence tomography. They seem to correspond to multiple small areas of partial-thickness or lamellar disruptions of the retina. The authors suggest that the contraction of the epiretinal membrane may have caused tangential traction on the adjacent inner retina, creating disruptions in the internal limiting membrane and inner retina.

Scattered Lamellar Microholes as a Complication of Epiretinal Membranes

From the Department of Ophthalmology, Hôpital Lariboisière, Assistance Publique-Hôpitaux de Paris and University Paris 7, Paris, France.

The authors have no financial or proprietary interest in the materials presented herein.

The authors thank Dr. Bénédicte Dupas for her technical support.

Address correspondence to Marie-Hélène Errera, MD, Department of Ophthalmology, Hôpital Lariboisière, 2 rue Ambroise-Paré, 75010 Paris, France. E-mail: marie-helene.errera@orange.fr

Received: October 12, 2009
Accepted: August 03, 2010
Posted Online: December 01, 2010

Introduction

Optical coherence tomography (OCT) is currently used to document epiretinal membranes before surgery.1,2 The new generation of three-dimensional spectral domain optical coherence tomography (SD-OCT) technology offers high precision of 7-μm axial resolution in the retina. The system provides accurate three-dimensional images of the topographic dynamics of traction lines from the retinal surface down to the level of the photoreceptor segments.3,4

Short wavelength waves have a weaker penetration depth in the retinal layers than longer wavelength waves. As a result, short wavelength (488 nm) blue reflectance photographs enable visualization of the retinal nerve layer, the internal limiting membrane, and cysts. In addition, this noninvasive and sensitive method is useful in imaging alterations of the vitreoretinal interface as retinal folds and epiretinal membranes.5,6

Many complications of epiretinal membranes have been reported, such as edema with cystic spaces, lamellar macular holes, macular pseudoholes, and photoreceptors defects.7 However, to our knowledge, scattered extramacular lamellar microholes have not been reported in the course of the disease. Herein, we report the occurrence of this pattern diagnosed on blue reflectance fundus photographs (Topcon Retinal Camera TRC-50DX1; Topcon Corporation, Tokyo, Japan) and SD-OCT (Cirrus SD OCT; Carl Zeiss Meditec, Inc., Dublin, CA).

Case Reports

Case 1

A 70-year-old man presented with a 1-year history of visual loss in his left eye. Best-corrected visual acuity was 20/120 in the left eye and 20/40 in the right eye. Fundus examination of the left eye showed a contractile idiopathic epiretinal membrane and a pattern of alveolar oval areas of retinal thinning temporal to the macular area and adjacent to a retinal fold created by the epiretinal membrane contraction (Fig. 1C). These retinal defects were better seen on blue reflectance fundus photographs than on color photographs (Figs. 1A and 1C). SD-OCT images showed that these oval retinal defects corresponded to cystic changes in the inner retina and small interruptions of the inner retina from the internal limiting membrane to half of the thickness of the outer retina (Figs. 1B and 1D).

Preoperative Findings in Case 1. (A) Blue Reflectance Fundus Photograph Depicting Alveolar Cluster of Retinal Microholes in the Lower Temporal Margin of the Epiretinal Membrane (black Arrows). (B) The Corresponding Virtual Optical Coherence Tomography (OCT) Fundus Picture Acquired with Spectral Domain OCT and Correlated with Blue Reflectance Fundus Photograph. The Blue Line Shows the Direction of OCT Scans. (C) Colour Fundus Photography Showing Contractile Epiretinal Membrane and a Discrete Pattern of Alveolar Oval Areas of Retinal Thinning, Temporal to the Macular Area (arrows), Although Less Obvious than on Blue Reflectance Fundus Photographs. (D) Scan Images of the Lamellar Microholes with Spectral Domain OCT. Note Small Interruptions of the Outer Retina from the Internal Limiting Membrane to Half of the Thickness of the Outer Retina.

Figure 1. Preoperative Findings in Case 1. (A) Blue Reflectance Fundus Photograph Depicting Alveolar Cluster of Retinal Microholes in the Lower Temporal Margin of the Epiretinal Membrane (black Arrows). (B) The Corresponding Virtual Optical Coherence Tomography (OCT) Fundus Picture Acquired with Spectral Domain OCT and Correlated with Blue Reflectance Fundus Photograph. The Blue Line Shows the Direction of OCT Scans. (C) Colour Fundus Photography Showing Contractile Epiretinal Membrane and a Discrete Pattern of Alveolar Oval Areas of Retinal Thinning, Temporal to the Macular Area (arrows), Although Less Obvious than on Blue Reflectance Fundus Photographs. (D) Scan Images of the Lamellar Microholes with Spectral Domain OCT. Note Small Interruptions of the Outer Retina from the Internal Limiting Membrane to Half of the Thickness of the Outer Retina.

The patient underwent pars plana vitrectomy with peeling of the epiretinal membrane and internal limiting membrane. After surgery, blue reflectance fundus photographs showed areas of alveolar imprints instead of the alveolar retinal microholes (Fig. 2A). These residual imprints are easier to detect on blue reflectance fundus photographs (Fig. 2A) than on color photographs (Fig. 2C). OCT images revealed that macular thickness had significantly decreased (466 vs 346 μm) and foveal contour had improved. OCT showed that the retina became thinner and that the lamellar holes were no longer visible but some tiny cystic spaces in the inner retina persisted (Figs. 2B and 2D).

Postoperative Findings in Case 1. (A) Blue Reflectance Fundus Photograph Showing the Location of Alveolar Imprints Coincides Exactly with the Area of Alveolar Retinal Microholes (black Arrows). (B) The Corresponding Virtual Optical Coherence Tomography (OCT) Fundus Photograph Acquired with Spectral Domain OCT and Correlated with Blue Reflectance Fundus Photograph. (C) Color Fundus Photograph Showing Tiny Alveolar Imprints Have Replaced the Lamellar Holes. (D) Scan Images with Spectral Domain OCT Showing Hyporeflective Cystic Spaces.

Figure 2. Postoperative Findings in Case 1. (A) Blue Reflectance Fundus Photograph Showing the Location of Alveolar Imprints Coincides Exactly with the Area of Alveolar Retinal Microholes (black Arrows). (B) The Corresponding Virtual Optical Coherence Tomography (OCT) Fundus Photograph Acquired with Spectral Domain OCT and Correlated with Blue Reflectance Fundus Photograph. (C) Color Fundus Photograph Showing Tiny Alveolar Imprints Have Replaced the Lamellar Holes. (D) Scan Images with Spectral Domain OCT Showing Hyporeflective Cystic Spaces.

Case 2

A 76-year-old woman presented with an idiopathic epiretinal membrane in her right eye. Visual acuity was 20/60. Color and blue reflectance fundus photographs of the right eye showed a contractile epiretinal membrane involving the fovea and distorting the superotemporal retinal vessels (Figs. 3A and 3C). Multiple small, oval retinal defects were detected along the edge of the contractile epiretinal membrane. SD-OCT showed that these defects corresponded to lamellar holes (Figs. 3B and 3D). After the surgical removal of epiretinal membrane and internal limiting membrane peeling, OCT images showed a decrease of macular thickness (462 vs 318 μm). Color and blue reflectance fundus photographs showed imprints of the microholes (Figs. 4A and 4C) not detected on OCT examination of the same area (Figs. 4B and 4D) and dissociated optic nerve fiber layer appearance of the fundus.8

Preoperative Findings in Case 2. (A) Blue Reflectance Fundus Photograph Showing an Alveolar Cluster of Retinal Microholes Present on the Edge of the Epiretinal Membrane (thick Arrow). (B) The Corresponding Virtual Optical Coherence Tomography (OCT) Fundus Photograph Acquired with Spectral Domain OCT and Correlated with Blue Reflectance Fundus Photograph. (C) Color Fundus Photograph Showing a Contractile Epiretinal Membrane Involving the Fovea and Distorting the Superotemporal Retinal Vessels. The Lamellar Microholes Are Hardly Visible. (D) Scan Images with Spectral Domain OCT of the Lamellar Microholes, Which Shows the Small Interruption of the Outer Retina from Internal Limiting Membrane to One-Third of the Thickness of the Retina (arrow).

Figure 3. Preoperative Findings in Case 2. (A) Blue Reflectance Fundus Photograph Showing an Alveolar Cluster of Retinal Microholes Present on the Edge of the Epiretinal Membrane (thick Arrow). (B) The Corresponding Virtual Optical Coherence Tomography (OCT) Fundus Photograph Acquired with Spectral Domain OCT and Correlated with Blue Reflectance Fundus Photograph. (C) Color Fundus Photograph Showing a Contractile Epiretinal Membrane Involving the Fovea and Distorting the Superotemporal Retinal Vessels. The Lamellar Microholes Are Hardly Visible. (D) Scan Images with Spectral Domain OCT of the Lamellar Microholes, Which Shows the Small Interruption of the Outer Retina from Internal Limiting Membrane to One-Third of the Thickness of the Retina (arrow).

Postoperative Findings in Case 2. (A) Blue Reflectance Fundus Photograph Showing Areas of Alveolar Imprints Remaining (white Arrow). Note the Dissociated Optic Nerve Fiber Layer Appearance of the Fundus (black Arrows) that Consists of Numerous Arcuate Striae Within the Posterior Pole in the Direction of the Optic Nerve Fibers and Slightly Darker than the Surrounding Retina. (B) The Corresponding Virtual Optical Coherence Tomography (OCT) Fundus Picture Acquired with Spectral Domain OCT and Correlated with Blue Reflectance Fundus Photograph. (C) Color Fundus Photograph Showing the Lamellar Microholes Are No Longer Visible After Surgery. (D) Scan Images with Spectral Domain OCT Revealed Normal Retinal Contour.

Figure 4. Postoperative Findings in Case 2. (A) Blue Reflectance Fundus Photograph Showing Areas of Alveolar Imprints Remaining (white Arrow). Note the Dissociated Optic Nerve Fiber Layer Appearance of the Fundus (black Arrows) that Consists of Numerous Arcuate Striae Within the Posterior Pole in the Direction of the Optic Nerve Fibers and Slightly Darker than the Surrounding Retina. (B) The Corresponding Virtual Optical Coherence Tomography (OCT) Fundus Picture Acquired with Spectral Domain OCT and Correlated with Blue Reflectance Fundus Photograph. (C) Color Fundus Photograph Showing the Lamellar Microholes Are No Longer Visible After Surgery. (D) Scan Images with Spectral Domain OCT Revealed Normal Retinal Contour.

Discussion

We describe two patients with an unusual pattern of the fundus associated with epiretinal membranes, corresponding to multiple scattered lamellar microholes located outside the fovea at the epiretinal membrane’s contraction border. These lesions were more easily observed with blue light than with color photographs of the fundus. On SD-OCT, the scattered lamellar microholes appeared as a loss of substance that extended from the level of the internal limiting membrane to approximately half to two-thirds of the thickness of the inner retina. In the two eyes, these morphologic changes were associated with contractile epiretinal membranes.

To our knowledge, these anomalies have not been previously described associated with epiretinal membranes. Our findings differ from paravascular lamellar holes, retinal microfolds, or paravascular intraretinal cysts, which have been documented on OCT scans in highly myopic eyes.9–13 These previously reported retinal changes are likely due to the vitreoretinal adhesion over the retinal vessels combined with the progressive global scleral stretching.10 We suggest that the contraction of the epiretinal membrane may have caused tangential traction on the adjacent inner retina followed by tears of the inner retina, creating disruptions in the internal limiting membrane and the inner retina. The complication of lamellar retinal defects is probably rare, but should be added to the list of retinal disturbances due to epiretinal membrane contraction. SD-OCT in combination with blue reflectance photography was helpful to detect this entity and may lead to a better understanding of the pathogenesis of idiopathic epiretinal membranes.

References

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Authors

From the Department of Ophthalmology, Hôpital Lariboisière, Assistance Publique-Hôpitaux de Paris and University Paris 7, Paris, France.

The authors have no financial or proprietary interest in the materials presented herein.

Address correspondence to Marie-Hélène Errera, MD, Department of Ophthalmology, Hôpital Lariboisière, 2 rue Ambroise-Paré, 75010 Paris, France. E-mail: marie-helene.errera@orange.fr

10.3928/15428877-20101124-12

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