Ophthalmic Surgery, Lasers and Imaging Retina

Clinical Science 

Ultra-Widefield Autofluorescence Imaging of Retinal Detachment Compared to Retinoschisis

Jennifer B. Nadelmann, MD; Mrinali P. Gupta, MD; Szilard Kiss, MD; Gulce Askin, MPH; R.V. Paul Chan, MD; Thanos Papakostas, MD; Donald J. D'Amico, MD; Anton Orlin, MD

Abstract

BACKGROUND AND OBJECTIVE:

Localized retinal detachment can appear similar to peripheral retinoschisis (RS) based on clinical exam alone. This study utilized ultra-widefield autofluorescence (UAF) to characterize retinal changes in patients with rhegmatogenous retinal detachment (RRD) compared to RS and to help differentiate these two entities in the era of multimodal imaging.

PATIENTS AND METHODS:

A retrospective review of 282 eyes undergoing diagnostic UAF. Eyes were excluded if the quality of the color photograph or UAF prevented reliable evaluation, or if they contained significant peripheral retinal pathology such as diabetic retinopathy or retinal vein occlusions. Eyes were determined to have RRD or RS based on dilated fundus examination, ultrasound, and optical coherence tomography imaging consistent with the diagnosis.

RESULTS:

Fifty-three eyes were included; 38 had retinal detachment, and 25 had RS. Eyes were determined to be bullous or not from the color photographs. Based on all UAFs reviewed, images were determined to have granular, normal, hypo-, hyper-, or mixed autofluorescence patterns. The posterior border of the RRD and RS was evaluated separately and determined to have hyper-, hypo-, granular, mixed, or normal autofluorescence. Thirty-three eyes with RRD (86.8%) appeared bullous compared to 12 eyes with RS (48%; P = .002). UAF was considered granular in zero (0%) of RRD eyes and one (4%) RS eye, normal in one RRD eye (2.63%) and 17 (68%) RS eyes, hypoautofluorescent in 27 (71.1%) RRD eyes and four (16%) RS eyes, hyperautofluorescent in one (2.63%) RRD eye and one (4%) RS eye, and mixed in nine (4%) RRD eyes and two (8%) RS eyes (P < .001). When evaluating the posterior leading edge on UAF, 84.2% (n = 32) of patients with RRD had a hyperautofluorescent leading edge compared to 25% (n = 6) of patients with RS (P < .001). UAF was homogenous in 65.8% (n = 25) of cases of RRD versus in 92% (n = 23) of cases of RS (P = .037).

CONCLUSIONS:

To the authors' knowledge, this is the first study to utilize UAF imaging to differentiate RRD and RS. Findings suggest there are differences between RRD and RS with regards to UAF, UAF of the posterior border, and homogeneity of the area affected. UAF should be considered in the era of multimodal imaging, particularly when clinical exam alone is inadequate to differentiate these two entities.

[Ophthalmic Surg Lasers Imaging Retina. 2019;50:550–556.]

Abstract

BACKGROUND AND OBJECTIVE:

Localized retinal detachment can appear similar to peripheral retinoschisis (RS) based on clinical exam alone. This study utilized ultra-widefield autofluorescence (UAF) to characterize retinal changes in patients with rhegmatogenous retinal detachment (RRD) compared to RS and to help differentiate these two entities in the era of multimodal imaging.

PATIENTS AND METHODS:

A retrospective review of 282 eyes undergoing diagnostic UAF. Eyes were excluded if the quality of the color photograph or UAF prevented reliable evaluation, or if they contained significant peripheral retinal pathology such as diabetic retinopathy or retinal vein occlusions. Eyes were determined to have RRD or RS based on dilated fundus examination, ultrasound, and optical coherence tomography imaging consistent with the diagnosis.

RESULTS:

Fifty-three eyes were included; 38 had retinal detachment, and 25 had RS. Eyes were determined to be bullous or not from the color photographs. Based on all UAFs reviewed, images were determined to have granular, normal, hypo-, hyper-, or mixed autofluorescence patterns. The posterior border of the RRD and RS was evaluated separately and determined to have hyper-, hypo-, granular, mixed, or normal autofluorescence. Thirty-three eyes with RRD (86.8%) appeared bullous compared to 12 eyes with RS (48%; P = .002). UAF was considered granular in zero (0%) of RRD eyes and one (4%) RS eye, normal in one RRD eye (2.63%) and 17 (68%) RS eyes, hypoautofluorescent in 27 (71.1%) RRD eyes and four (16%) RS eyes, hyperautofluorescent in one (2.63%) RRD eye and one (4%) RS eye, and mixed in nine (4%) RRD eyes and two (8%) RS eyes (P < .001). When evaluating the posterior leading edge on UAF, 84.2% (n = 32) of patients with RRD had a hyperautofluorescent leading edge compared to 25% (n = 6) of patients with RS (P < .001). UAF was homogenous in 65.8% (n = 25) of cases of RRD versus in 92% (n = 23) of cases of RS (P = .037).

CONCLUSIONS:

To the authors' knowledge, this is the first study to utilize UAF imaging to differentiate RRD and RS. Findings suggest there are differences between RRD and RS with regards to UAF, UAF of the posterior border, and homogeneity of the area affected. UAF should be considered in the era of multimodal imaging, particularly when clinical exam alone is inadequate to differentiate these two entities.

[Ophthalmic Surg Lasers Imaging Retina. 2019;50:550–556.]

Introduction

Rhegmatogenous retinal detachment (RRD) is a significant cause of visual loss and blindness, whereas acquired retinoschisis (RS) is typically a benign and nonprogressive condition characterized by splitting of the neurosensory retina.1, 2 Clinically, there often are differences between these two entities to help differentiate them. RS classically appears more transparent and less mobile compared to RRD and occurs more commonly in the infratemporal retina without retinal corrugations.1,3–5 Despite these differences, localized RRD can appear similar to RS on clinical exam. Various ancillary testing modalities can be utilized to help distinguish the two conditions. On B-scan ultrasonography, RS does not re-appose with scleral depression.3–6 In addition, optical coherence tomography (OCT) can show the splitting of the neurosensory retina compared to the subretinal fluid in a full-thickness detachment.1,7 Occasionally, bullous detachments are difficult to differentiate from bullous schisis cavities on B scan, whereas widefield OCT may not be available to many practices.

RS and RRD typically occur in the far periphery and are therefore technically difficult to capture with standard photography. With the advent of ultra-widefield imaging, as with the Optos 200Tx imaging system (Optos, Dunfermline, Scotland), it is now possible to image the peripheral retina more easily. Ultra-widefield autofluorescence (UAF) imaging can be used to detect functional changes in the retina. Lipofuscin in the retinal pigment epithelium (RPE) is the predominant source of autofluorescence signal in the human retina. The autofluorescence of the RPE is based upon the renewal of photoreceptor outer segments and may be altered by the degree of accumulation and clearance.8 Autofluorescence is decreased when there is a loss of lipofuscin or RPE and increased in the setting of RPE dysfunction.9 Therefore, UAF imaging provides valuable information regarding the function of RPE cells and the viability of the retina by identifying metabolic changes at the level of the RPE and photoreceptor complex.10 Ultra-widefield imaging has the advantage of producing a 200° view of the retina in a single frame, enabling the retinal fundus and periphery to be visualized simultaneously. Of note, RRD causes functional changes in the retina, which are detectable by UAF.8

To our knowledge, there have not been any studies utilizing UAF imaging to distinguish RRD from RS. The purpose of our study is to characterize UAF retinal changes using the Optos device in patients with confirmed diagnosis of RRD compared to those with RS to help differentiate these two entities in the era of multimodal imaging.

Patients and Methods

This retrospective review was approved by the institutional review board of Weill Cornell Medical College (WCMC). The research adhered to the tenets of the Declaration of Helsinki and was conducted in accordance with the Health Insurance Portability and Accountability Act. All patients with the diagnosis of primary RRD or RS at WCMC from 2013 to 2017 were retrospectively reviewed and included in this study.

Eyes were excluded if the quality of the color photograph or UAF prevented reliable evaluation. Eyes were also excluded if there was inadequate follow-up imaging, or if they contained significant peripheral retinal pathology such as diabetic retinopathy or retinal vein occlusions. Baseline information was recorded from the chart review, including the patient's age, gender, and past medical history. Eyes were determined to have RRD or RS based on dilated fundus examination, ultrasound, and OCT imaging consistent with the diagnosis. We sought to characterize and compare UAF findings in our RRD and RS groups. Two retina-trained specialists at WCMC (AO, MG) evaluated the UAF images.

Statistical Analysis

Baseline characteristics, UAF, and OCT imaging characteristics were described for the entire sample (n = 63), as well as by condition type (ie, RRD vs. RS). Continuous variables were described as mean + standard deviation or median (25th percentile; 75th percentile), depending on distribution. Discrete variables were described as frequency (%).

The two-sample t-test and Wilcoxon rank-sum tests, as appropriate based on distribution, were used to assess the relationships between continuous variables of interest and condition type (ie, RRD vs. RS). The chi-square and Fisher's exact tests, as appropriate based on cell counts, were used to assess the association between discrete variables of interest and condition type (ie, RRD vs. RS). The same analyses were carried out in in a subset of RRD patients with macula-off (n = 24). Additionally, in the macula-off subset, the association between imaging characteristics and improvement status at final visit (ie, improve vs. stable/worse) was explored. The Wilcoxon ranked-sum test was used to assess the difference in median change in vision (logMAR) between binary imaging characteristics. Inter-rater reliability of two readers for imaging characteristics was assessed with Cohen's weighted Kappa coefficient and corresponding bootstrapped 95% confidence intervals. All P values were two-sided and statistical significance was evaluated at P values less than .05. Analysis was performed using R Version 3.3.1 (R Foundation for Statistical Computing, Vienna, Austria).

Results

A total of 282 UAFs were reviewed, of which, 53 eyes were included in this study. Thirty-eight eyes had retinal detachment and 25 eyes had RS with a mean length of follow-up of 470 days. Of the eyes with RRD, 63.2% (n = 24) were macula-off. Refer to Table 1 for baseline characteristics. The majority of patients in the RRD group were men (76.3%) compared to (48.0%) in the RS group (P = .042). Median logMAR vision on presentation was 0.00 (Snellen visual acuity [VA]: 20/20) in the RS group and 0.51 (Snellen VA: 20/65) in the RRD group (P < .001). Baseline mean intraocular pressures were 13.8 mm Hg and 14.3 mm Hg in the RS and RRD groups, respectively.

Baseline Characteristics

Table 1:

Baseline Characteristics

Table 2 details the UAF findings of RRD and RS during baseline examination. Eyes were determined to be bullous or not (Figures 1A–1C) from the Optos color photographs. Based on all UAFs reviewed, images were determined to have granular, normal, hypo-, hyper-, or mixed autofluorescence patterns (Figures 2A–2E). The posterior border of the RRD and RS was evaluated separately and determined to have hyper- (Figure 2C), hypo- (Figure 3A), granular (Figure 3B), mixed (Figure 3C), or normal autofluorescence (Figure 2B). Thirty-three eyes with RRD (86.8%) appeared bullous compared to 12 eyes with RS (48%; P = .002). UAF was considered granular in 0% (n = 0) of RRD eyes and 4% (n = 1) of RS eyes, normal in 2.63% (n = 1) of RRD eyes and 68% (n = 17) of RS eyes, hypoautofluorescent in 71.1% (n = 27) of RRD eyes and 16% (n = 4) of RS eyes, hyperautofluorescent in 2.63% (n = 1) of RRD eyes and 4% (n = 1) of RS eyes, and mixed in 23.7% (n = 9) of RRD eyes and 8% (n = 2) of RS eyes (P < .001). When evaluating the posterior leading edge on UAF, 84.2% (n = 32) of patients with RRD had a hyperautofluorescent leading edge (HLE) compared to 25% (n = 6) of patients with RS (P < .001). UAF was homogenous (Figures 2B and 2D) in 65.8% (n = 25) of cases of RRD versus in 92% (n = 23) of cases of RS (P = .037).

UAF Findings of RRD and RS

Table 2:

UAF Findings of RRD and RS

(A) Optos color photograph of bullous retinoschisis (RS). (B) Optos color photograph of non-bullous RS inferotemporally. (C) Optos color photograph of bullous retinal detachment.

Figure 1.

(A) Optos color photograph of bullous retinoschisis (RS). (B) Optos color photograph of non-bullous RS inferotemporally. (C) Optos color photograph of bullous retinal detachment.

(A) Optos ultra-widefield autofluorescence (UAF) showing granular autofluorescence. (B) UAF illustrating a normal autofluorescent inferotemporal retinoschisis cavity with a normal posterior autofluorescent border. (C) UAF illustrating a hypoautofluorescent retinal detachment with a hyperautofluorescent posterior border. (D) UAF illustrating hyperautofluorescence. (E) UAF illustrating mixed autofluorescence.

Figure 2.

(A) Optos ultra-widefield autofluorescence (UAF) showing granular autofluorescence. (B) UAF illustrating a normal autofluorescent inferotemporal retinoschisis cavity with a normal posterior autofluorescent border. (C) UAF illustrating a hypoautofluorescent retinal detachment with a hyperautofluorescent posterior border. (D) UAF illustrating hyperautofluorescence. (E) UAF illustrating mixed autofluorescence.

(A) Optos ultra-widefield autofluorescence (UAF) showing a retinoschisis cavity with a hypoautofluorescent posterior border. (B) Optos UAF showing a granular autofluorescent posterior border. (C) Optos UAF showing a mixed autofluorescent posterior border.

Figure 3.

(A) Optos ultra-widefield autofluorescence (UAF) showing a retinoschisis cavity with a hypoautofluorescent posterior border. (B) Optos UAF showing a granular autofluorescent posterior border. (C) Optos UAF showing a mixed autofluorescent posterior border.

Baseline UAF of the fovea was normal in 100% (n = 25) of RS eyes, whereas in subjects with RRD, baseline UAF of the fovea was normal in 68.6% (n = 24), granular in 2.86% (n = 1), hyperautofluorescent in 15.8% (n = 6), hypoautofluorescent in 2.63% (n = 1), and mixed in 15.8% (n = 6) of eyes (P = .006).

There was excellent agreement (Kappa > 0.90) between the two raters for all variables except homogeneity (Table 3).

Intergrader Reliability

Table 3:

Intergrader Reliability

Among the patients with RRD, 24 (63.2%) presented with macula-off detachment, whereas 20 of these eyes had adequate follow-up data and were analyzed. Sixteen eyes (80%) had improvement of vision at the most recent follow-up, whereas four eyes (20%) had stable or loss of vision. Two eyes (10%) had final vision of worse than 20/200. It did not appear that any of the baseline UAF findings for the detachment, posterior border, or fovea were associated with visual outcomes such as improvement of vision (Table 4) or final vision less than 20/200 (Table 5).

Baseline UAF Associations With Final Visual Acuity Improvement in a Subset of Patients With Macula-Off RRD (n = 20)

Table 4:

Baseline UAF Associations With Final Visual Acuity Improvement in a Subset of Patients With Macula-Off RRD (n = 20)

Baseline UAF Associations With Final VA of 20/200 or Worse in a Subset of Patients With Macula-Off RRD (n = 20)

Table 5:

Baseline UAF Associations With Final VA of 20/200 or Worse in a Subset of Patients With Macula-Off RRD (n = 20)

Discussion

Although RRD can be differentiated from RS by clinical exam alone, it occasionally can be difficult to do so, particularly with regard to localized retinal detachment. In the era of multimodal imaging, various techniques can be used to supplement clinical exam alone to more reliably differentiate these two entities. We used UAF images of the peripheral retina to evaluate for any potential differences between the conditions. To the best of our knowledge, this is the first study to do so.

Based on all UAF reviewed, five common patterns were seen: granular, normal, hypo-, hyper-, or mixed autofluorescence. There was a statistically significant difference in the distribution of UAF patterns between RRD and RS (Table 2; P < .001). The majority of RRD eyes had some degree of hypoautofluorescence (71.1% hypoautofluorescence, 23.7% mixed autofluorescence), whereas the majority of RS eyes appeared to have normal autofluorescence (68%).

The UAF of the posterior border also showed to be significantly different between RRD and RS, with the former exhibiting a high rate of HLE (P < .001). In addition, eyes with RS appeared to have more homogenous UAF when compared to RRD (P = .037) and were also less bullous (48% vs. 86.8%; P = .002).

UAF imaging can be used to detect functional changes in the retina. UAF detects fluorophores, such as lipofuscin, which are located in the RPE.8,11 Accumulation of lipofuscin in RPE cells can lead to enhanced or hyperautofluorescence, such as with altered lipofuscin metabolism or with superimposed RPE cells in age-related macular degeneration.11 Increased levels of UAF can indicate oxidative stress and increased metabolic activity as the RPE becomes preapoptotic.8,12 Hypoautofluorescence occurs from a decrease in lipofuscin or blockage by material anterior to the retina.11

As mentioned, the majority of eyes with RRD in our study were hypoautofluorescent, as was also described by Witmer et al. This is likely due to blocking defect of the overlying subretinal fluid (SRF), particularly in bullous detachments.8 In contrast, only one eye in the RRD group showed normal UAF, whereas the majority of eyes with RS had normal UAF. RS may result from a preexisting peripheral cystoid degeneration13 in the retina, which slowly enlarges. As the retina splits, neurons may be disrupted leading to visual function deficit in the area affected.2,14,15 The RPE typically is not affected and the retina layers remain in opposition to the RPE. Our results support this hypothesis, as the vast majority of our RS cases showed normal UAF. It is possible that some cases of RS showed mixed or hypoautofluorescence due to blocking defect (as in a bullous RS cavity) or due to secondary RPE dysfunction.

An HLE, or posterior hyperautofluorescent area, was also commonly seen in eyes with RRD when compared to RS. This represents shallow SRF and likely a collection of lipofuscin from photoreceptor outer segments, which have been shed and collected in the subretinal space.8 Alternatively, it could represent RPE cells with increased metabolic activity and stress at the border of attached and detached retina. Those eyes with granular UAF changes could result from chronicity or disruption of the RPE and outer retinal anatomy, such as with the inner segment/outer segment junction.8

Eyes with RS also appeared more homogenous compared to RRD. This is likely due to the difference in degree of fluid within regions of a detachment, in addition to its varying effect on the underlying outer retina and RPE.

In our study, preoperative UAF imaging did not appear to be associated with visual outcomes such as improvement in vision (Table 4) or final vision of 20/200 or less (Table 5) in the subset of patients with macula-off RRD. Final vision is dependent on many factors, including preoperative anatomic findings; chronicity; and non-retina related variables, such as cataract formation, glaucoma, and preoperative vision. It is possible that the small number of eyes in the macula-off detachment group limited these results, and that a larger sample would have had different findings.

The limitations of this study include those intrinsic to a retrospective design and a small sample size. Despite this, statistically significant differences between groups were detected.

To our knowledge, this study is the first to utilize UAF imaging to differentiate RRD and RS. Our findings suggest that there are differences between RRD and RS with regard to UAF, UAF of the posterior border, and homogeneity of the area affected. UAF should be considered in the era of multimodal imaging, particularly when clinical exam alone is inadequate to differentiate these two entities. Future investigations with a larger cohort should be made particularly with regard to macula-off RRD to evaluate for certain preoperative UAF prognostic factors.

References

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  2. Zimmerman LE, Spencer WH. The pathologic anatomy of retinoschisis with a report of two cases diagnosed clinically as a malignant melanoma. Arch Ophthalmol. 1960;63:10–19. doi:10.1001/archopht.1960.00950020012002 [CrossRef]13847542
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Baseline Characteristics

RRD (n = 38)RS (n = 25)P Value

Gender
  Male, N (%)29 (76.3%)12 (48%).042
  Female, N (%)9 (23.7%)13 (52%)

Right Eye Affected, N (%)20 (52.6%)12 (48%).919

Mean Age (Years)55.0 + 11.656.4 + 14.2.686

Median Vision Snellen (logMAR)20/65 (0.51)20/20 (0.00)< .001

Macula-on, N (%)14 (36.8%)25 (100%)< .001

UAF Findings of RRD and RS

RRD (n = 38), N (%)RS (n = 25), N (%)P Value

Bullous (From Color Photo), Yes33 (86.8%)12 (48.0%).002

UAF< .001
  Granular0 (0.00%)1 (4.00%)
  Hyper-1 (2.63%)1 (4.00%)
  Hypo-27 (71.1%)4 (16.0%)
  Mixed9 (23.7%)2 (8.00%)
  Normal1 (2.63)17 (68.0%)

UAF of the Posterior Border< .001
  Granular0 (0.00%)1 (4.17%)
  Hyper-32 (84.2%)6 (25.0%)
  Hypo-1 (2.63%)8 (33.3%)
  Mixed1 (2.63%)0 (0.00%)
  Normal4 (10.5%)9 (37.5%)
  UAF, homogenous (yes)25 (65.8%)23 (92.0%).037

Intergrader Reliability

VariableNCohen's Kappa (Weighted)95% CI (Bootstrapped)P Value
Autofluorescence630.920.81–1.00< .0001
Border610.980.93–1.00< .0001
Fovea600.990.97–1.00< .0001
Homogeneity630.420.53–0.63< .0001

Baseline UAF Associations With Final Visual Acuity Improvement in a Subset of Patients With Macula-Off RRD (n = 20)

Stable or Worse Vision (n = 4), N (%)Improvement in Vision (n = 16), N (%)P Value

Bullous.167
  Yes2 (50%)2 (12.5%)
  No2 (50%)14 (87.5%)

UAF (Grader 1)1.000
  Hypo-3 (75.0%)9 (56.2%)
  Mixed1 (25.0%)6 (37.5%)
  Normal0 (0.00%)1 (6.25%)

UAF of the Border (Grader 1)
  Hyper-3 (75.0%)13 (81.2%)
  Hypo-0 (0.00%)1 (6.25%)
  Normal1 (25.0%)2 (12.5%)1.000

UAF of the Fovea (Grader 1)
  Granular0 (0.00%)1 (6.25%)
  Hyper-1 (25.0%)4 (25.0%)
  Mixed2 (50.0%)4 (25.0%)
  Normal1 (25.0%)7 (43.8%).825

Baseline UAF Associations With Final VA of 20/200 or Worse in a Subset of Patients With Macula-Off RRD (n = 20)

Final VA ≥ 20/200 (n = 18), N (%)Final VA < 20/200 (n = 2), N (%)P Value

Bullous.368
  Yes3 (16.7%)1 (50.0%)
  No15 (83.3%)1 (50.0%)

UAF (Grader 1)1.000
  Hypo-11 (61.1%)1 (50.0%)
  Mixed6 (33.3%)1 (50.0%)
  Normal1 (5.56%)0 (0.00%)

UAF of the Border (Grader 1)1.000
  Hyper-14 (77.8%)2 (100%)
  Hypo-1 (5.56%)0 (0.00%)
  Normal3 (16.7%)0 (0.00%)

UAF of the Fovea (Grader 1).521
  Granular1 (5.56%)0 (0.00%)
  Hyper-4 (22.2%)1 (50.0%)
  Mixed5 (27.8%)1 (50.0%)
  Normal8 (44.4%)0 (0.00%)
Authors

From Albert Einstein College of Medicine, Bronx, New York (JBN); the Department of Ophthalmology, Weill Cornell Medical College, New York (MPG, SK, TP, DJD, AO); the Department of Healthcare Policy & Research, Weill Cornell Medicine, New York (GA); and the Department of Ophthalmology, University of Illinois at Chicago, Chicago (RVPC).

Dr. Kiss is a consultant for Optos. Dr. Askin was partially supported by a grant from the Clinical and Translational Science Center at Weill Cornell Medical College (No. 1-UL1-TR002384-01). Dr. Papakostas is a consultant to Alcon and Genentech outside the submitted work. Dr. D'Amico received a departmental grant from Research to Prevent Blindness. The remaining authors report no relevant financial disclosures.

Address correspondence to Anton Orlin, MD, Weill Cornell Medical College, 1305 York Avenue, 11th Floor, New York, NY, 10021; email: ano9028@med.cornell.edu.

Received: August 16, 2018
Accepted: January 17, 2019

10.3928/23258160-20190905-03

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