Ophthalmic Surgery, Lasers and Imaging Retina

Clinical Science 

Degenerative Peripheral Retinoschisis: Observations From Ultra-Widefield Fundus Imaging

Aristomenis Thanos, MD; Bozho Todorich, MD, PhD; Sirichai Pasadhika, MD; Tahsin Khundkar, MD; David Xu, MD; Atul Jain, MD; Cindy Ung, MD; Lisa J. Faia, MD; Antonio Capone, MD; George A. Williams, MD; Yoshihiro Yonekawa, MD; David Sarraf, MD; Jeremy D. Wolfe, MD, MS

Abstract

BACKGROUND AND OBJECTIVE:

To describe the ultra-widefield (UWF) imaging characteristics of patients with degenerative peripheral retinoschisis (DPR) using Optomap technology.

PATIENTS AND METHODS:

In this multicenter, retrospective, noncomparative, consecutive case series, eligible patients underwent detailed retinal examination including indirect ophthalmoscopy. UWF fundus imaging, including color fundus photography, autofluorescence, and angiography, was performed using standardized protocols and findings were recorded and reviewed and analyzed.

RESULTS:

A total of 35 patients (58 eyes) with DPR were identified who underwent 55 sessions of UWF imaging. Mean age was 65 years, and the inferotemporal quadrant was most commonly affected (74% of eyes). Of these patients, 31 underwent fluorescein angiography and 90% of these studies illustrated abnormalities in the area affected by the schisis. The most common finding was retinal vascular leakage originating from the deep capillary plexus observed in 29 eyes (93.5%).

CONCLUSIONS:

UWF imaging enables a more detailed identification of the clinical features associated with DPR and provides simple, practical, and noninvasive tools to monitor progression of disease. The breadth of retinal vascular complications identified with fluorescein angiography may suggest an important vascular component associated with the pathogenesis of this entity.

[Ophthalmic Surg Lasers Imaging Retina. 2019;50:557–564.]

Abstract

BACKGROUND AND OBJECTIVE:

To describe the ultra-widefield (UWF) imaging characteristics of patients with degenerative peripheral retinoschisis (DPR) using Optomap technology.

PATIENTS AND METHODS:

In this multicenter, retrospective, noncomparative, consecutive case series, eligible patients underwent detailed retinal examination including indirect ophthalmoscopy. UWF fundus imaging, including color fundus photography, autofluorescence, and angiography, was performed using standardized protocols and findings were recorded and reviewed and analyzed.

RESULTS:

A total of 35 patients (58 eyes) with DPR were identified who underwent 55 sessions of UWF imaging. Mean age was 65 years, and the inferotemporal quadrant was most commonly affected (74% of eyes). Of these patients, 31 underwent fluorescein angiography and 90% of these studies illustrated abnormalities in the area affected by the schisis. The most common finding was retinal vascular leakage originating from the deep capillary plexus observed in 29 eyes (93.5%).

CONCLUSIONS:

UWF imaging enables a more detailed identification of the clinical features associated with DPR and provides simple, practical, and noninvasive tools to monitor progression of disease. The breadth of retinal vascular complications identified with fluorescein angiography may suggest an important vascular component associated with the pathogenesis of this entity.

[Ophthalmic Surg Lasers Imaging Retina. 2019;50:557–564.]

Introduction

The term retinoschisis (RS) refers to the abnormal splitting of the retinal layers. The juvenile X-linked form of this disorder is caused by mutations in the RS1 gene that encodes the protein retinoschisin, a pivotal protein maintaining the integrity of the retina.1 By contrast, degenerative peripheral retinoschisis (DPR), also referred to as senile RS develops in the retinal periphery of middle-aged patients — despite the misnomer senile — and its pathogenesis is unclear without any known genetic associations. Histopathologic studies have proposed that DPR forms in the retinal periphery as cystoid retinal degeneration and gradual enlargement and coalescence of the cysts leads to development of larger schisis cavities. Two forms of DPR have been described histologically: “typical” (flat) and “reticular” (bullous). The split in the “typical” form occurs in the outer plexiform layer (OPL), whereas the split in the “reticular” form occurs in the nerve fiber layer.2

The advent of ultra-widefield (UWF) imaging has ushered a new era in the diagnosis and management of peripheral retinal disorders. Optomap technology (Optos, Dunfermline, Scottland) was first introduced in 2000 and provides the first camera capable of imaging up to 200 internal degrees (approximately 82%) of the retina in a single capture, providing a simultaneous view of the posterior pole and the periphery. The technology utilizes an ellipsoid mirror and a red (635-nm) and green (532-nm) laser to scan the retina and acquire pseudocolor and fundus autofluorescence (FAF, green laser only) images. For fluorescein angiography (FA), a blue (488-nm) laser is employed.3 Several studies have validated the utility of UWF imaging in the diagnosis and management of peripheral retinal disorders, including vascular occlusions and diabetic retinopathy.4,5

Ever since the landmark studies on DPR performed by Byer,6 which established the clinical characteristics of the disease,7,8 there has been a paucity of literature on the subject and therefore many aspects of the disease remain poorly understood. In this study, we describe the imaging characteristics, including UWF color fundus photography, autofluorescence, and angiography of patients with degenerative peripheral retinoschisis using Optomap technology.

Patients and Methods

The study was approved by the institutional review board/ethics committees of the respective co-author institutions and conformed to the requirements of the Health Insurance Portability and Accountability Act of 1996 and followed the tenets of the Declaration of Helsinki.

The design of the study was a multicenter, retrospective, noncomparative, case series of patients with degenerative peripheral RS who were examined at four institutions (Associated Retinal Consultants, Devers Eye Institute, Stein Eye Institute, and Massachusetts Eye & Ear Infirmary) between January 2009 and October 2017.

All patients underwent UWF fundus imaging using the Optos 200Tx or P200dTx imaging system. Participants were identified by their International Classification of Diseases diagnosis. Inclusion criteria were the presence of degenerative peripheral RS in either eye. Exclusion criteria included any evidence (by history or examination) of congenital X-linked RS; retinal detachment surgery; or retinal vascular disease, including diabetic retinopathy, retinal vein occlusion, familial exudative vitreoretinopathy, and sickle cell retinopathy.

After pupillary dilation, UWF fundus photography and fluorescein angiography (UWFFA) were performed according to standard protocol. Patients received an intravenous injection of 5 cc of sodium fluorescein 10%. Images were digitally archived and reviewed using the Optos Advance or V2 Vantage review platform, which provides high-resolution zoom and multimodality review of images. Two masked observers reviewed the UWF images and findings were recorded.

Spectral-domain optical coherence tomography (SD-OCT) (Spectralis; Heidelberg Engineering, Heidelberg, Germany) was performed in the periphery, when feasible, and images were reviewed to identify the microstructural features of RS. The following patient data were recorded: demographics at the first imaging session, phakic status, presence of posterior vitreous detachment in the eye with schisis, location and extent of RS, and ocular involvement (unilateral or bilateral).

Results

Patient Demographics

A total of 35 patients (58 eyes) with DPR who underwent 55 sessions of UWF imaging, including color fundus photography, FAF, and FA were identified. Table 1 lists basic demographic information and characteristics of these patients. Patients ranged in age from 37 years to 89 years (average: 65 years). Nine eyes (nine of 58; 16%) with DPR were pseudophakic, 49 of 58 eyes (84%) were phakic, and posterior vitreous detachment was present in 17 of 58 eyes (29%) with DPR. Mean best-corrected visual acuity was 20/25. Average length of follow-up was 18 months (range: 1 month to 92 months). None of the patients enrolled in the study demonstrated progression of the RS from their initial presentation until their last follow-up visit.

Patient Demographics Involved in the Study and RS Characteristics

Table 1:

Patient Demographics Involved in the Study and RS Characteristics

Color Fundus Findings

Bullous DPR was readily identified in pseudo-color images obtained with Optomap technology as a peripheral dome-shaped elevation with a smooth, taut convex surface lacking folds and undulations in all 35 patients enrolled in the study (Figure 1A). DPR was bilateral in 23 of 35 patients (66%) enrolled in the study (Table 1). The inferotemporal quadrant was most commonly affected (43 of 58; 74%). Of those, a significant proportion (seven of 58; 12%) demonstrated features of shallow schisis or cystoid degeneration extending to the temporal and superior quadrants, which were contiguous to the inferotemporal, often bullous, area of RS (Supplemental Figures A and E, available at www.healio.com/OSLIRetina). No RS was observed in the nasal quadrants. Shallow RS was identified by identification of the following features: mild haze of the underlying choroidal detail, presence of Gunn's dots (ie, visible reflections of the internal limiting membrane created by the footplate of the Müller cells) and minimal elevation of the superficial retinal layers. In 28 of 58 eyes (48%), the retinal vessels on the dome of the schisis appeared darker compared to the blood vessels of attached retina, a finding not observed in retinal detachment Optomap photos (Figures 1D, 1G, 1M, 1P; Figure A available at www.healio.com/OSLIRetina). Outer retinal holes were visible in 18 of 58 eyes (33%). Isolated retinal hemorrhages over the area of the schisis were observed in six of 58 cases (10%). Sclerotic vessels over the area of the schisis were evident in six of 58 (10%), and yellow-white surface dots — presumably Gunn's dots — were visible in 22 of 58 eyes (37%) with retinoschisis (Figures 1D, 1G, 1J, 1P; Figure A, available at www.healio.com/OSLIRetina). Lipid exudates at the edge of the schisis cavity were also observed in two of 58 cases (3%) (Figure 2A). Diffuse retinal pigment epithelium (RPE) pigmentary changes, including cobblestone degeneration over the area of the schisis were present in nine of 58 eyes (16%).

Representative pseudocolor, fundus autofluorescence (FAF), and fluorescein angiography (FA) ultra-widefield images of seven different patients with degenerative retinoschisis. In the pseudocolor fundus images, outer retinal holes (A, M, P, S), Gunn's dots (D, G, J, P), isolated retinal hemorrhages (J, S), and “dark” vessels running the dome of the schisis cavity (D, G, M, P) can be observed. In the FAF images, localized hyperautofluorescence, due to unmasking of retinal pigment epithelium autofluorescence, can be identified in the areas corresponding to the outer retinal breaks (B, M, S). In the FA images, transmission of fluorescence is noted in the areas associated with outer retinal breaks (C, O, U). Delayed vascular filling in the early frames (F), vessel wall staining (I), areas of capillary nonperfusion (I), and diffuse vascular leakage (L, O, R) are also noted.

Figure 1.

Representative pseudocolor, fundus autofluorescence (FAF), and fluorescein angiography (FA) ultra-widefield images of seven different patients with degenerative retinoschisis. In the pseudocolor fundus images, outer retinal holes (A, M, P, S), Gunn's dots (D, G, J, P), isolated retinal hemorrhages (J, S), and “dark” vessels running the dome of the schisis cavity (D, G, M, P) can be observed. In the FAF images, localized hyperautofluorescence, due to unmasking of retinal pigment epithelium autofluorescence, can be identified in the areas corresponding to the outer retinal breaks (B, M, S). In the FA images, transmission of fluorescence is noted in the areas associated with outer retinal breaks (C, O, U). Delayed vascular filling in the early frames (F), vessel wall staining (I), areas of capillary nonperfusion (I), and diffuse vascular leakage (L, O, R) are also noted.

Pseudocolor fundus photo illustrating contiguous areas of retinoschisis (RS) affecting the superotemporal, temporal, and inferotemporal retinal quadrants. Note the outer retinal holes, shallow RS and dark vessels on the schisis cavity (A, arrows). Yellow-white dots, presumably Gunn's dots on the surface of the schisis cavity (B). Pseudo-color fundus photo of a rhegmatogenous retinal detachment (C) and degenerative peripheral RS with outer retinal holes (D). Notice the presence of dark vessels on the dome of the schisis cavity (E, arrow) compared to the vessels on the bullous retinal detachment (D, arrows). Peripheral cystoid degeneration noted on Optomap pseudo-color imaging (E, arrows).

Figure A.

Pseudocolor fundus photo illustrating contiguous areas of retinoschisis (RS) affecting the superotemporal, temporal, and inferotemporal retinal quadrants. Note the outer retinal holes, shallow RS and dark vessels on the schisis cavity (A, arrows). Yellow-white dots, presumably Gunn's dots on the surface of the schisis cavity (B). Pseudo-color fundus photo of a rhegmatogenous retinal detachment (C) and degenerative peripheral RS with outer retinal holes (D). Notice the presence of dark vessels on the dome of the schisis cavity (E, arrow) compared to the vessels on the bullous retinal detachment (D, arrows). Peripheral cystoid degeneration noted on Optomap pseudo-color imaging (E, arrows).

Representative pseudocolor (A) and fluorescein angiography (B–D) ultra-widefield images of a patient with degenerative retinoschisis (RS). Early (B), mid- (C), and late-phase angiograms illustrate diffuse retinal vascular leakage at the border of the schisis cavity that emanates from the deep retinal capillary plexus. Notice the delayed vascular filling of the retinal vein over the schisis cavity (B, arrow), despite the presence of laminar flow elsewhere (B). Peripheral shallow RS (E) with diffuse vascular leakage in a ground glass pattern (F, arrows). There are microaneurysmal-like hyperfluorescent lesions at the edge of the schisis (F, arrowheads).

Figure 2.

Representative pseudocolor (A) and fluorescein angiography (B–D) ultra-widefield images of a patient with degenerative retinoschisis (RS). Early (B), mid- (C), and late-phase angiograms illustrate diffuse retinal vascular leakage at the border of the schisis cavity that emanates from the deep retinal capillary plexus. Notice the delayed vascular filling of the retinal vein over the schisis cavity (B, arrow), despite the presence of laminar flow elsewhere (B). Peripheral shallow RS (E) with diffuse vascular leakage in a ground glass pattern (F, arrows). There are microaneurysmal-like hyperfluorescent lesions at the edge of the schisis (F, arrowheads).

Fundus Autofluorescence Findings

UWF fundus autofluorescence images illustrated the extent of the schisis cavity in 35 of 58 cases (67%) with variable features. A crescent of hypoautofluorescence was often evident at the edge of the schisis cavity, aiding in its identification. Bullous retinoschisis was associated with trace hypoautofluorescence of the area under the cavity (Figures 1E and 1N), whereas outer retinal holes corresponded with focal hyperautofluorescence (Figures 1B, 1N, 1T) due to unmasking of underlying RPE autofluorescence.

Fluorescein Angiography Findings

A total of 31 UWFFA were reviewed, and 28 of 31 (90%) of these studies illustrated abnormalities in the area affected by the schisis. The most common finding was retinal vascular leakage observed in 29 of 31 eyes (93.5%). This was most commonly identified at the posterior border of the schisis cavity (Figure 2). Fluorescein leakage in a ground glass pattern also occurred in areas adjacent to the schisis cavity (Figures 2E and 2F). Microaneurysmal-like hyperfluorescent lesions were observed in 11 of 31 eyes (36%) (Figure 2F, arrowheads). Vessel staining as well as patchy areas of poorly perfused capillary beds on the dome of the schisis cavity in the late phases of the angiogram were observed in nine of 31 (29%) eyes. Delayed filling of the retinal vessels in the early frames of the angiogram was observed in 10 of 31 eyes (32%) (Figures 1F and 2B, arrow). Unmasking of underlying RPE autofluorescence and transmission of background fluorescence was observed in cases where outer retinal holes were present (eight of 31 eyes; 26%) (Figure 1O). No evidence of retinal neovascularization was observed.

SD-OCT Findings

Peripheral SD-OCT scanning through the area of RS was feasible in 18 of 58 eyes (31 %) and demonstrated inverted image artifacts in all of these eyes (Figures 3A and 3B). Retinal splitting at the level of the OPL was most commonly observed. Interestingly, SD-OCT adjacent to the schisis cavities revealed multi-laminar schisis affecting the inner plexiform layer and OPL (Figures 3A–3D). In three of 58 eyes (5%), SD-OCT identified a subclinical retinal detachment associated with an outer retinal hole (Figures 3E and 3F).

Pseudocolor fundus photos (A, C, E) and spectral-domain optical coherence tomographies (B, D, F) through the areas of retinoschisis illustrating inverted image artifacts (B, asterisk), variable splitting in the OPL and IPL layers (B and D, arrowheads) and a subclinical retinal detachment (F, arrow) associated with an outer retinal hole.

Figure 3.

Pseudocolor fundus photos (A, C, E) and spectral-domain optical coherence tomographies (B, D, F) through the areas of retinoschisis illustrating inverted image artifacts (B, asterisk), variable splitting in the OPL and IPL layers (B and D, arrowheads) and a subclinical retinal detachment (F, arrow) associated with an outer retinal hole.

Discussion

This study employed UWF fundus imaging to analyze a large cohort of patients with DPR and demonstrated that both UWF color fundus photography and FAF are reliable, noninvasive tools that can aid in the diagnosis and objective monitoring of patients with DPR. We identified unique imaging characteristics of RS on UWF images, including the presence of Gunn's dots and “dark vessels” that aid in the differentiation of DPR from rhegmatogenous retinal detachment (Supplemental Figure A–D). The latter, seen both in bullous and shallow schisis, is likely a differential optical effect of the Optos ellipsoid mirror system.

Although the diagnosis of DPR has traditionally been based on clinical examination, it is difficult to identify the precise level of retinal splitting. In accordance with prior histopathologic studies, SD-OCT analysis in our study confirmed that DPR can occur both in the inner and OPLs of the retina.2 Differences in the layer of splitting may render some patients with DPR more prone to vascular complications, such as hemorrhage inside the schisis or vitreous cavity due to the dense anastomotic vascular network between the superficial and intermediate capillary plexus. Moreover, SD-OCT can be used for the long-term monitoring of schisis progression and the diagnosis of subclinical schisis-detachment, as previously shown by others.9,10

Another important finding of this study was the breadth of retinal vascular abnormalities that were identified in areas of DPR using UWFFA. Our findings confirmed previous reports of retinal capillary nonperfusion, telangiectasis, and intracavitary hemorrhage observed in patients with DPR.11,12 Although reported by others, we did not observe any evidence of retinal13 or anterior segment neovascularization.14 UWFFA demonstrated almost universal late leakage at the border of the schisis cavity, which appeared to originate from the deep retinal capillary plexi. In fact, the more posterior the schisis was located, the more prominent the leakage — consistent with prior histopathologic observations that the deep capillary layers disappear in the midperipheral retina, leaving only the superficial capillary plexus with wider spaced capillary loops in the far peripheral retina.15 Given the ubiquitous leakage observed, we postulate that intraretinal exudation from disruption of the blood retinal barrier may be contributing to the development and expansion of the schisis cavity. Although none of the patients in this study demonstrated progression of their schisis, intraretinal leakage may explain the dynamic features of this entity, as degenerative peripheral retinoschisis can progress laterally (6%), vertically (5%), posteriorly (3%), or even spontaneously regress.7,16 In fact, in an uncontrolled study of patients with intermediate uveitis and peripheral RS, control of intraocular inflammation led to decrease in fluorescein vascular leakage and resolution of the schisis.17

Consistent with prior reports, the inferotemporal retinal quadrant was the most commonly affected area in our study.2,6,18,19 However, to date, it is unknown why there is such disease predilection localized to the temporal retinal periphery and relative sparing of the nasal retina. A similar anatomic distribution is also seen with peripheral cystoid degeneration, which is considered the precursor of DPR.20 Furthermore, it is unclear if peripheral cystoid degeneration represents intraretinal fluid accumulation or true cystic spaces devoid of fluid and, thus, several theories have been proposed for its pathogenesis.20 Iwanoff et al. and Bruno et al. were among the first ones to propose that blood-retinal barrier breakdown and intraretinal edema lead to cystoid degeneration.20,21 Therefore, the abnormalities observed with UWFFA in this study may suggest that there could be a primary vascular component involved in the pathophysiology of degenerative peripheral RS, as also initially suggested by Campo et al.22 Interestingly, it has been illustrated that the temporal retina has a higher metabolic demand and receives 65% greater blood flow than the nasal retina, leading to marked differences in the retinal vascular circulation.23 Additionally, gravitational forces may explain the coalescence of smaller intraretinal cysts leading to subsequent expansion of the schisis cavity, and redistribution of intraretinal fluid to the inferotemporal quadrant.

Tractional mechanisms have also long been suspected to be implicated in the pathogenesis of DPR, but definitive evidence is lacking. In the studies performed by Byer, no systematic attempt was made to document the presence or absence of posterior vitreous detachment (PVD),6,8 whereas more recent smaller studies did not identify any correlations between PVD and schisis-detachments.10 In our RS cohort, the prevalence of PVD was only 29%, and its status was assessed by both clinical examination and SD-OCT. However, regardless of the PVD status, vitreous traction has been shown to induce hemodynamic changes to the retinal vasculature and result in vascular leakage.24–26 Therefore, the presence of leakage at the border of the schisis cavity and the identification of nonperfusion over the dome of the schisis may be secondary to localized hydrostatic and/or tractional mechanisms. Interestingly, similar vascular phenomena, including leakage in schisis cavities, opacified retinal vessels, and vascular sheathing, have been described in patients with juvenile RS.27 Further studies are required in order to fully elucidate the underlying mechanisms involved in the pathogenesis of DPR.

Limitations of our study included the retrospective design and lack of a control group. Eyelid artifacts, distortion, and flattening of the peripheral retina with limited views of the superior and inferior retinal quadrants are limitations associated with the Optomap imaging system.

In conclusion, previous investigations studying DPR have been limited by inadequate imaging technology to properly study this peripheral disorder. With the aid of UWF imaging, this study has identified more detailed clinical features associated with this common peripheral retinal condition and alternative mechanisms of disease have also been proposed for its pathogenesis. Although UWFFA was instrumental in elucidating these novel imaging findings, it did not alter patient management and, thus, it is not recommended by the authors for the routine follow-up of these patients. However, the development of novel imaging technologies, including OCT and OCT angiography, reaching the far retinal periphery will undoubtedly shed more light on the pathophysiology of this complex disease process.

References

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Patient Demographics Involved in the Study and RS Characteristics

Total Number of Patients35

Total Number of Eyes With RS58

Gender (n)
  Male14/35 (40%)
  Female21/35 (60%)
  Average Age (Years) [Range]65 [37 – 89]
  Hyperopia21/35 (60%)

Lens Status
  Phakic49/58 (84%)
  Pseudophakic9/58 (16%)

Posterior Vitreous Detachment
  Present17/58 (29%)
  Absent41/58 (71%)

Laterality
  Unilateral12/35 (34%)
  Bilateral (n)23/35 (66%)

Location of Schisis (Eyes, %)
  Superotemporal8/58 (14%)
  Inferotemporal36/58 (62%)
  Inferotemporal & Superotemporal7/58 (12%)
  Temporal6/58 (10%)
  Inferior1/58 (2%)

Schisis Characteristics
  Bullous38/58 (65%)
  Shallow20/58 (35%)
Authors

From Legacy Devers Eye Institute, Legacy Health, Portland, Oregon (AT, SP); Pennsylvania Retina Specialists, Camp Hill, Pennsylvania (BT); Massachusetts Eye and Ear Infirmary, Harvard Medical School, Boston (CU, YY); San Diego Retina Associates, San Diego (AJ); Stein Eye Institute, Department of Ophthalmology, University of California Los Angeles, David Geffen School of Medicine, Los Angeles (DX, DS); VA Greater Los Angeles Healthcare System, Los Angeles (DS); and Associated Retinal Consultants, Oakland University William Beaumont School of Medicine, Royal Oak, Michigan (AT, BT, LJF, AC, GAW, JDW).

Dr. Sarraf has received personal fees from Amgen, Bayer, Novartis, and Optovue; non-financial support from Heidelberg, Optovue, and Topcon; and grants and personal fees from Genentech, Regeneron, and Optovue outside the submitted work. The remaining authors report no relevant financial disclosures.

Address correspondence to Jeremy D. Wolfe, MD, MS, Associated Retinal Consultants, P.C., William Beaumont Hospital, 3555 West Thirteen Mile Road, Suite LL-20, Royal Oak, MI 48073; email: jwolfe@arcpc.net.

Received: October 01, 2018
Accepted: February 01, 2019

10.3928/23258160-20190905-04

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