Ophthalmic Surgery, Lasers and Imaging Retina

Clinical Science 

Prognostic Value of Hyperreflective Material on Visual Acuity in Treatment-Naïve BRVO

Ramesh Venkatesh, MS; Arpitha Pereira, DNB MRCSEd; Sajjan Sangai, MS; Sherina Thomas, MS; Naresh Kumar Yadav, DO, FRCS

Abstract

BACKGROUND AND OBJECTIVE:

To correlate between hyperreflective material (HRM) seen on optical coherence tomography (OCT) and visual outcomes in treatment-naïve acute branch retinal vein occlusion (BRVO).

PATIENTS AND METHODS:

Demographic and OCT features of patients with acute BRVO were analyzed retrospectively. OCT parameters noted were macular edema type, HRM presence and location, and outer retinal layer integrity. Eyes were separated into two groups: Group 1 (BRVO without HRM) and Group 2 (BRVO with HRM).

RESULTS:

Forty-seven eyes (67%) were included in Group 1 and 23 eyes (33%) were included in Group 2. Mean presenting logMAR visual acuity in Groups 1 and 2 was 0.521 ± 0.428 (mean Snellen equivalent = 20/66) and 0.627 ± 0.427 (mean Snellen equivalent = 20/85), respectively. Poor vision at final visit was noted in the BRVO with HRM group (P = .027). More intravitreal injections were required for macular edema resolution in the HRM group (4.83 vs. 2.67).

CONCLUSIONS:

Presence of HRM in BRVO is associated with poorer vision. It can be a useful prognostic biomarker.

[Ophthalmic Surg Lasers Imaging Retina. 2020;51:320–327.]

Abstract

BACKGROUND AND OBJECTIVE:

To correlate between hyperreflective material (HRM) seen on optical coherence tomography (OCT) and visual outcomes in treatment-naïve acute branch retinal vein occlusion (BRVO).

PATIENTS AND METHODS:

Demographic and OCT features of patients with acute BRVO were analyzed retrospectively. OCT parameters noted were macular edema type, HRM presence and location, and outer retinal layer integrity. Eyes were separated into two groups: Group 1 (BRVO without HRM) and Group 2 (BRVO with HRM).

RESULTS:

Forty-seven eyes (67%) were included in Group 1 and 23 eyes (33%) were included in Group 2. Mean presenting logMAR visual acuity in Groups 1 and 2 was 0.521 ± 0.428 (mean Snellen equivalent = 20/66) and 0.627 ± 0.427 (mean Snellen equivalent = 20/85), respectively. Poor vision at final visit was noted in the BRVO with HRM group (P = .027). More intravitreal injections were required for macular edema resolution in the HRM group (4.83 vs. 2.67).

CONCLUSIONS:

Presence of HRM in BRVO is associated with poorer vision. It can be a useful prognostic biomarker.

[Ophthalmic Surg Lasers Imaging Retina. 2020;51:320–327.]

Introduction

One of the commonest causes of retinal vascular disorder after diabetic retinopathy is retinal vein occlusion (RVO). There are two types of RVO, central retinal vein occlusion and branch retinal vein occlusion (BRVO), of which BRVO is more commonly seen.1 Risk factors associated with BRVO include arterial hypertension, glaucoma, diabetes mellitus, hyper viscosity, and old age.2,3 Macular edema and retinal neovascularization are common sequelae of BRVO and can lead to visual impairment.4,5 Visual acuity (VA) is a very sensitive indicator of the oxygen saturation levels at the macula. Better initial VA (≥ 20/50) suggests better macular oxygen saturation levels.6 Generally, BRVO has a good prognosis: 50% to 60% of eyes are reported to have a final VA of 20/50 or better even without treatment.7 One important prognostic factor for final VA in BRVO is initial VA. Studies have shown that the cases of BRVO with an initial VA of 20/200 or worse have a statistically significant poorer visual prognosis than those with an initial VA of 20/50 or better.7,8

Optical coherence tomography (OCT) is a noninvasive imaging tool routinely used to document the severity and type of macular edema in BRVO and to monitor treatment. OCT allows observation of the structural changes in the retina caused by BRVO. Previous studies in literature have identified the presence of subretinal fluid,9–12 foveal hard exudates,13,14 increased number of hyperreflective dots,15 and loss of the photoreceptor layer16,17 on OCT images to be associated with poor visual prognosis. In our retina clinic, we found a few cases of acute BRVO presenting with hyperreflective material (HRM), either intraretinal or subretinal, and having variable visual outcomes. Similarly, presence of intraretinal HRM has been described in diabetic macular edema (DME) as solid-appearing retinal cysts by Liang et al.18 The authors hypothesized that these intraretinal HRMs are mainly composed of fibrin or other inflammatory end products. HRM, underneath either the retina or retinal pigment epithelium, has been described in cases with neovascular age-related macular degeneration (AMD). The presence of central and thick subretinal HRMs with well-defined borders were associated with poorer visual prognosis in eyes with neovascular AMD.19 To the best of our knowledge, there is no published literature on acute BRVO studying the presence and etiopathogenesis of HRM and correlating its presence with the final VA.

With this background, we aimed to study the etiopathogenesis, clinical profile, OCT imaging features, and VA changes in eyes of acute BRVO with or without the presence of HRM.

Patients and Methods

For this retrospective cohort study, all data were collected and analyzed in accordance with the policies and procedures of the institutional review board of Narayana Nethralaya Super specialty eye hospital, Bangalore, India (C-2019-05-003) and the tenets set forth in the Declaration of Helsinki. The retina clinic database was searched for all cases of treatment-naïve BRVO between March 2018 and February 2019. The criteria for inclusion was eyes with treatment-naïve BRVO and a minimum of 3 months' follow-up duration. All other retinopathies mimicking BRVO were excluded from the study. Additionally, patients who had glaucoma and visual field loss, retinal/optic nerve lesion or any other factor (eg, cataract) that could influence visual outcome, unreliable visual fields, photocoagulation prior to the first visit, and inadequate information were excluded. The medical files of all eligible patients were reviewed and the following data were collected: age, gender, involved eye, systemic disease, duration of symptoms, best-corrected VA (BCVA) at presentation and at final follow-up, type of BRVO (major or macular), quadrant involved, clinical features, OCT parameters at presentation and at final follow-up, and treatment offered to the patient. BCVA was recorded in Snellen units and was converted to logarithm of the minimum angle of resolution (logMAR) for statistical analyses.

OCT Features

The central retinal thickness was measured with SD-OCT (Spectralis, Heidelberg Engineering, Heidelberg, Germany). Macular volumetric assessments consisting of 512 A-scans per line with 30° scanning area and 25-line horizontal and vertical raster scans centered at the fovea were performed. In addition, a 12-line foveal centered radial scan was performed for each eye. The following descriptive information was obtained from the OCT scan: presence of macular edema, type of macular edema, presence of HRM at the macula, and location of HRM (intraretinal or subretinal). Macular edema was classified into three types: 1) cystoid macular edema: large fluid-filled cyst-like spaces involving variable depth of the retina with intervening septa mainly confined to the outer retina; 2) spongiform edema: sponge-like retinal swelling mostly confined to the outer retinal layers due to backscattering from intraretinal fluid accumulation; and 3) neurosensory detachment: area of hyporeflectivity confined to the subretinal space. HRM was defined as presence of clumps of hyperreflective material present either in the intraretinal or subretinal space with no shadowing and was considered separate from hyperreflective dots or hard exudates seen on OCT. Quantitative measurements regarding the height of the neurosensory detachment, central retinal thickness, subfoveal choroidal thickness, height, width, and area of HRM were recorded using the automated measurement tool in the Spectralis machine (Heidelberg Engineering, Heidelberg, Germany).

Based on the presence of HRM on SD-OCT at presentation, the patients were categorized into two groups: Group 1 (BRVO without HRM) and Group 2 (BRVO with HRM). The demographic, VA, OCT parameters, and treatment profiles between the two groups were compared at presentation and final follow-up visit.

Statistical Analysis

All data were analyzed with GraphPad Prism software (version 8.1.1 [330] for Windows; GraphPad Software, San Diego, CA). Normal distribution of quantitative variables was checked using the Kolmogorov-Smirnov normality test. Refraction data were converted to logMAR for statistical analysis. Quantitative variables between the two groups were analyzed using the independent t-test and Mann-Whitney U test for parametric and nonparametric data, respectively. Fisher's exact t-test was used to compare the categorical data between the two groups. P values less than .05 were considered statistically significant.

Results

In this retrospective cohort study, 70 eyes of 65 patients diagnosed with treatment-naïve BRVO met the inclusion criteria during the study period. At presentation, 47 (67%) eyes were identified with no HRM while in the remaining 23 (33%) eyes, HRM was noted. The mean ages of the participants in Group 1 and Group 2 were 60.7 ± 12.5 years and 59.1 ± 12.8 years, respectively. Table 1 compares the demographic, clinical, and OCT features between the two groups. The choroid was significantly thicker in the HRM group compared to the non-HRM group at presentation (P = .019). The ELM (P = .032) and EZ (P = .027) layers were discontinuous in the HRM group compared to the non-HRM group. Treatment offered to patients in both groups is also mentioned in Table 1.

Demographic and Clinical Features Between Patients With and Without Hyperreflective Material in Branch Retinal Vein Occlusion at PresentationDemographic and Clinical Features Between Patients With and Without Hyperreflective Material in Branch Retinal Vein Occlusion at Presentation

Table 1:

Demographic and Clinical Features Between Patients With and Without Hyperreflective Material in Branch Retinal Vein Occlusion at Presentation

Table 2 describes the comparisons between Group 1 and Group 2 at the final follow-up visit. In group 1, no HRM was noted in 59 (84%) eyes and in group 2, HRM was noted in 11 (16%) eyes. The mean follow-up interval was 8.12 ± 10.1 months in Group 1 and 8 ± 6.29 months in Group 2, respectively. Three patients developed HRM and converted from Group 1 at presentation to Group 2 at final visit after a mean interval of 8.67 ± 3.79 months. Fifteen of the 23 eyes (65%) in Group 2 showed resolution of the HRM at the final follow-up visit. The mean time interval taken for the HRM to resolve was 2.40 ± 1.12 months. Significantly poor VA was noted in eyes with HRM compared to eyes with no HRM at the final follow-up visit (P = .027). Table 3 describes the subgroup analysis of cases who presented initially with HRM (Group 2) and compared the clinical and OCT features and treatment profiles at the final follow-up visit in eyes where HRM resolved and in eyes where HRM persisted (Figures 1, 2, and 3).

Clinical Features Between Patients With and Without Hyperreflective Material inBranch Retinal Vein Occlusion at Final Visit

Table 2:

Clinical Features Between Patients With and Without Hyperreflective Material inBranch Retinal Vein Occlusion at Final Visit

Subgroup Analysis of Eyes That Presented With Hyperreflective Material (Group 2 Cases)at Their Final Follow-Up Visit

Table 3:

Subgroup Analysis of Eyes That Presented With Hyperreflective Material (Group 2 Cases)at Their Final Follow-Up Visit

Acute branch retinal vein occlusion (BRVO) with intraretinal hyperreflective material: pre- and post-treatment outcomes. (A, B) A 55-year-old female presenting with right eye acute inferotemporal BRVO. Her presenting visual acuity (VA) was 20/120 (0.78 logMAR). Optical coherence tomography image at presentation showed presence of spongiform macular edema with cystoid changes. A clump of hyperreflective material was noted within the intraretinal cyst (white arrow). The external limiting membrane layer and ellipsoid zone (EZ) was continuous. Following three injections of intravitreal anti-vascular endothelial growth factor (bevacizumab), complete resolution of the macular edema was noted with resolution of the intraretinal hyperreflective material. The external limiting membrane and EZ layers were intact following treatment. Her VA improved to 20/80 (0.60 logMAR) at the final follow-up visit.

Figure 1.

Acute branch retinal vein occlusion (BRVO) with intraretinal hyperreflective material: pre- and post-treatment outcomes. (A, B) A 55-year-old female presenting with right eye acute inferotemporal BRVO. Her presenting visual acuity (VA) was 20/120 (0.78 logMAR). Optical coherence tomography image at presentation showed presence of spongiform macular edema with cystoid changes. A clump of hyperreflective material was noted within the intraretinal cyst (white arrow). The external limiting membrane layer and ellipsoid zone (EZ) was continuous. Following three injections of intravitreal anti-vascular endothelial growth factor (bevacizumab), complete resolution of the macular edema was noted with resolution of the intraretinal hyperreflective material. The external limiting membrane and EZ layers were intact following treatment. Her VA improved to 20/80 (0.60 logMAR) at the final follow-up visit.

Pre- and post-treatment outcomes in a patient with acute branch retinal vein occlusion (BRVO) with subretinal hyperreflective material. (A–C) Color fundus image of the left eye in a 60-year-old male using the widefield Optos Daytona showing multiple retinal hemorrhages limited to the superotemporal quadrant, suggestive of acute major vessel BRVO. His presenting visual acuity (VA) was 20/200 (1 logMAR). Pre-treatment optical coherence tomography scans showing the presence of spongiform edema with neurosensory detachment. Within the neurosensory detachment, hyperreflective material was noted (black arrow). The patient was treated with four injections of intravitreal ranibizumab and two injections of intravitreal triamcinolone acetonide. At the final follow-up visit, there was complete resolution of spongiform macular edema with reduction in the height of subretinal fluid. Residual hyperreflective material was noted in the subretinal space (white arrow). The VA showed a one-line improvement at the final follow-up visit at 8 months in the left eye to reach 20/120 (0.78 log units).

Figure 2.

Pre- and post-treatment outcomes in a patient with acute branch retinal vein occlusion (BRVO) with subretinal hyperreflective material. (A–C) Color fundus image of the left eye in a 60-year-old male using the widefield Optos Daytona showing multiple retinal hemorrhages limited to the superotemporal quadrant, suggestive of acute major vessel BRVO. His presenting visual acuity (VA) was 20/200 (1 logMAR). Pre-treatment optical coherence tomography scans showing the presence of spongiform edema with neurosensory detachment. Within the neurosensory detachment, hyperreflective material was noted (black arrow). The patient was treated with four injections of intravitreal ranibizumab and two injections of intravitreal triamcinolone acetonide. At the final follow-up visit, there was complete resolution of spongiform macular edema with reduction in the height of subretinal fluid. Residual hyperreflective material was noted in the subretinal space (white arrow). The VA showed a one-line improvement at the final follow-up visit at 8 months in the left eye to reach 20/120 (0.78 log units).

Treatment outcomes in a patient with acute branch retinal vein occlusion (BRVO) and subretinal hyperreflective material. (A–C) Cropped image of a widefield fundus photograph obtained using the Optos Daytona in a 67-year-old woman shows the presence of acute inferior macular BRVO. Optical coherence tomography image at presentation shows the presence of subretinal fluid, cystoid macular edema, and spongiform edema along the inferior macular branch of the retina. Hyperreflective material is noted in the subretinal space (white arrow). Following treatment with multiple intravitreal anti-vascular endothelial growth factor injections, there was complete resolution of the macular edema. Hyperreflective material was noted to lie underneath the fovea (white arrow) leading to no improvement in the visual acuity (VA) at the final follow-up visit. Her final VA documented in the medical records was 20/120 (0.78 logMAR units).

Figure 3.

Treatment outcomes in a patient with acute branch retinal vein occlusion (BRVO) and subretinal hyperreflective material. (A–C) Cropped image of a widefield fundus photograph obtained using the Optos Daytona in a 67-year-old woman shows the presence of acute inferior macular BRVO. Optical coherence tomography image at presentation shows the presence of subretinal fluid, cystoid macular edema, and spongiform edema along the inferior macular branch of the retina. Hyperreflective material is noted in the subretinal space (white arrow). Following treatment with multiple intravitreal anti-vascular endothelial growth factor injections, there was complete resolution of the macular edema. Hyperreflective material was noted to lie underneath the fovea (white arrow) leading to no improvement in the visual acuity (VA) at the final follow-up visit. Her final VA documented in the medical records was 20/120 (0.78 logMAR units).

Discussion

The results of this study suggest that presence of HRM at presentation, either intraretinal or subretinal, could be associated with poor visual prognosis in eyes with acute BRVO.

There are two distinct types of BRVO identified based on the site of the venous occlusion: 1) major vessel BRVO and 2) macular vessel BRVO. Macular BRVOs are more likely to be associated with macular edema and less likely with retinal neovascularization due to the smaller area of retina affected.20 In this study, a greater proportion of macular vessel occlusions presented with HRM when compared to major vessel BRVOs. The pathogenesis of BRVO involves thrombosis of a retinal vein, resulting in engorgement of the vein throughout its distribution. There is increased intraluminal pressure distal to the obstruction and increased interstitial pressure resulting in transudation of fluid, lipid exudate, and/or heme from the intravascular space to extravascular space. This results in the development of macular edema. A composite mixture of fluid, heme, exudate, and fibrin-like material can get accumulated within the intraretinal cysts or neurosensory detachment, as well. This is being described as the HRM in this study. Deposition of similar hyperreflective material has been previously described in eyes with other retinal or choroidal vascular diseases like DME and neovascular AMD.18,19 However, we found that the HRMs in BRVO were more routinely seen during the early acute stages of the disease compared to HRMs seen in DME or neovascular AMD where they occur during the chronic stages.

HRM was not associated with any systemic disease in our study. On the other hand, systemic diseases like diabetes mellitus and hypertension were commonly encountered in the absent HRM group. This further strengthens our hypothesis that HRM in BRVO occurs due to the vascular changes following the obstruction and not due to the presence of associated systemic diseases like diabetes mellitus and hypertension.

OCT has been an invaluable imaging tool in the diagnosis and management of macular edema in BRVO. Several features seen on the OCT like presence of subretinal fluid, foveal hard exudates, hyperreflective intraretinal dots, and discontinuity of the photoreceptor layer are associated with poor visual prognosis.5,9 In our study, the VAs at the final follow-up were significantly different between the two groups (0.297 ± 0.273 [mean Snellen equivalent = 20/40] in Group 1 and 0.478 ± 0.270 [mean Snellen equivalent = 20/60] in Group 2; P = .027). Eyes with HRM at the final follow-up visit had poor vision compared to eyes with no HRM. Thus, the presence of HRM could possibly be considered as an important visual prognostic marker in addition to other OCT features in acute BRVO.

In other macular conditions like neovascular AMD, the presence of subretinal, thick HRM with well-defined borders is also associated with poor visual prognosis.19

During the last several years, intravitreal anti-VEGF and steroid injections have been the mainstay in the treatment of macular edema following BRVO.7 Even in this study, most of the cases were treated with anti-VEGF injections in both groups. However, we noted a poor response to intravitreal injections in the resolution of macular edema in eyes where the HRM persisted until the final follow-up visit. Liang et al. reported a similar poor response of intravitreal anti-VEGF injections in the resolution of solid-appearing retinal cysts in eyes with DME.18 Pokroy et al. noted poor response to intravitreal bevacizumab (Avastin; Genentech, South San Francisco, CA) injections in eyes with presence of subretinal HRM in neovascular AMD.19 A further subgroup analysis of outcomes of eyes with HRM at presentation showed that in almost two-thirds of the cases, HRM resolution was seen at the final follow-up visit. Persistent HRM was associated with poor visual outcome in this study. In fact, in these eyes the retina and choroid at the macula was thicker and required more intravitreal injections compared to eyes where the HRM resolved at the final visit.

The study shows that eyes without baseline HRM had better visual outcomes, and further, that the poor prognosis was noted in eyes where the HRM persisted. However, we did not perform a further subgroup analysis of eyes with intraretinal or subretinal HRM and its effects on the visual outcomes.

This study has several limitations. First, the retrospective study design and a smaller sample size are its major limitations. Second, the use of bevacizumab, ranibizumab (Lucentis; Genentech, South San Francisco, CA), or intraocular steroids was not exclusive. Comparing the response of HRM positive eyes to different intraocular anti-VEGF or steroid agents would be an interesting area of research. Third, we did not analyze the prognostic value of baseline HRM according to BRVO subgroups (macular vs. major BRVO). Fourth, we did not analyze the baseline HRM OCT characteristics with the final vision. Finally, we did not compare the VA changes between the two groups at visits in between the first and last visit. Our specific aim in the study was to assess whether the persistence of HRM in acute BRVO would have any influence on the final visual outcome.

In conclusion, to the best of our knowledge, this study is the first to assess the prognostic value of HRM on SD-OCT for final BCVA in treatment-naïve BRVO eyes. This study supports the use of HRM as a prognostic biomarker for visual outcome when interpreting OCT in eyes with macular edema following BRVO.

References

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Demographic and Clinical Features Between Patients With and Without Hyperreflective Material in Branch Retinal Vein Occlusion at Presentation

VariableWithout HRM (n = 47)With HRM (n = 23)P Value
Age60.7 ± 12.559.1 ± 12.8.626
Gender (male: female)29:1815:8
Study eye (OD:OS)28:1910:13
Duration of symptoms (days)15.26 ± 3.4214.15 ± 4.21.659
Systemic disease (N, %)Diabetes mellitus15 (32)6 (26).783
Diabetes mellitus15 (32)6 (26).783
Hypertension27 (57)9 (39).204
Heart Disease2 (4)1 (4)> .999
Arthritis2 (4)0> .999
Hypothyroidism1 (2)0> .999
Vasculitis1 (2)0> .999
Systemic disease absent10 (21)11 (48).023
Presenting VA (log MAR), mean Snellen equivalent0.521 ± 0.428, 20/660.627 ± 0.427, 20/85.324
Type of BRVO (N, %)ST BRVO20(43)6(26)
IT BRVO14 (30)5 (22)
SN BRVO1 (2.12)0
IN BRVO00
Superior Macular BRVO8 (17)10 (44)
Inferior Macular BRVO4 (9)2 (9)
Clinical features (N, %)Dense and multiple hemorrhages31 (66)16 (70)> .999
Light and few hemorrhages16 (34)7 (30)> .999
Cotton-wool spots31 (66)11 (48).196
Hard exudates14 (30)3 (13).15
NVE1 (2)0> .999
Vitreous hemorrhage1 (2)0> .999
Presence of macular edema (N, %)46 (98)23 (100)> .999
Type of macular edema (N, %)Spongiform33 (70)19 (83).385
Cystoid44 (94)15 (65).004
NSD16 (34)13 (57).120
Height of NSD (µm)86.6 ± 167186 ± 199.017
CRT (µm)500 ± 190510 ± 186.838
Location of HRM (N, %)Intraretinal8 (35)
Subretinal19 (83)
Subfoveal choroidal thickness (µm)282 ± 67.9330 ± 97.7.019
Treatment with (N, %)Observation2(4)2 (9)
Focal laser4 (9)0
Topical NSAIDS01 (4)
Bevacizumab20 (43)12 (52)
Ranibizumab11 (23)2 (9)
Biosimilar Ranibizumab (Razumab,5 (11)3 (13)
Intas)
IVTA2 (4)3 (13)
Dexamethasone implant3 (6)0

Clinical Features Between Patients With and Without Hyperreflective Material inBranch Retinal Vein Occlusion at Final Visit

VariableWithout HRM (n = 59)With HRM (n = 11)P Value
Final follow-up visit duration (months)8.12 ± 10.18 ± 6.29.567
Presenting VA (log MAR), mean Snellen equivalent0.297 ± 0.273, 20/400.478 ± 0.270, 20/60.027
CRT (μm)321 ± 118365 ± 141.218
Subfoveal choroidal thickness (μm)262 ± 71.6274 ± 95.7.827

Subgroup Analysis of Eyes That Presented With Hyperreflective Material (Group 2 Cases)at Their Final Follow-Up Visit

VariableHRM Persist at Final Visit (n = 8)HRM Resolved at Final Visit (n = 15)P Value
Presenting VA (log MAR), mean Snellen equivalent0.640 ± 0.350, 20/870.184 ± 0.141, 20/31.000
CRT (μm)355 ± 149299 ± 63.6.418
Subfoveal choroidal thickness (μm)304 ± 101272 ± 78.8.515
Mean number of injections4.83 ± 2.152.67 ±1.34.346
Mean follow-up (months)7.75 ± 7.235.87 ± 5.28.780
Authors

From Narayana Nethralaya Super Speciality Eye Hospital, Bangalore, India.

The authors report no relevant financial disclosures.

Address correspondence to Ramesh Venkatesh, MS, Narayana Nethralaya Super Speciality Eye Hospital, #121/C, Chord Road, 1st R block Rajaji Nagar, Bangalore, India 560010; email: vramesh80@yahoo.com.

Received: January 28, 2020
Accepted: April 28, 2020

10.3928/23258160-20200603-02

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