To evaluate the correlation between morphologic changes in the outer retina and visual function after successful repair of rhegmatogenous retinal detachment with macula off.
Observational case series.
settings: Dijon University Hospital. patients: Thirty patients (30 eyes) with successful repair of rhegmatogenous retinal detachment after macula off and a minimum 6-month follow-up after surgery. main outcome measures: Spectral-domain optical coherence tomography (SD-OCT) of the outer retina, fundus autofluorescence (FAF), and microperimetry.
Twenty of 30 eyes presented microstructural changes within the photoreceptor layer (66.7%). Of these, half of the patients (50%) had more than 1 lesion. Disrupted inner segment/outer segment (IS/OS) junction was noted in 16 out of 30 eyes (53.3%), irregular hyporeflectivity in the photoreceptor outer segments (PROS) was observed in 17 eyes (56.7%), external limiting membrane was discontinued in 10 eyes (33.3%), and hyperreflective spots in the outer nuclear layer were observed in 5 eyes (16.7%). FAF changes were detected in only 5 eyes (16.7%). Abnormalities in the IS/OS junction were significantly associated with lower foveal and macular sensitivity, thinner PROS, and global photoreceptor changes ( P = .014, P = .003, P = .006, P < .0001, respectively). Patients with a normal foveal profile showed similar findings.
SD-OCT and microperimetry seem to be appropriate tools to determine the visual and the anatomic recovery of the macula after surgery.
Visual recovery may remain incomplete after rhegmatogenous retinal detachment (RRD), especially in cases of retinal detachments with macula off, even after a successful surgery with a normal-appearing fundus examination. Poor visual acuity, color vision defects, or persistent metamorphopsia may persist over time, suggesting the existence of microstructural macular damage that standard fundus biomicroscopy could not detect.
Recent advances in retinal imaging have improved fundus examinations. Optical coherence tomography (OCT) is a noninvasive real-time system that can be used to explore the retinal structures. Studies using time-domain OCT have associated subretinal persistent fluid, macular edema, and epiretinal membrane with poor visual acuity after retinal detachment. However, these lesions accounted for a minority of poor visual outcomes. Ultrahigh-resolution OCT (UHR-OCT) provided an axial resolution of 3 to 5 μm and better visualization of previously unidentified photoreceptor changes responsible for visual loss in age-related macular degeneration, central serous chorioretinopathy, or macular hole. The development of spectral-domain OCT (SD-OCT) led to a 50-fold higher data acquisition speed, which reduced motion artifacts and dramatically improved visualization of the photoreceptor layer using an axial resolution of 4 to 6 μm. SD-OCT can also be combined with microperimetry to evaluate retinal sensitivity. Therefore, SD-OCT imaging offers new and interesting opportunities to better understand the discordances between anatomic and functional outcomes after retinal detachment surgery.
Several recent studies have identified minimal changes after RRDs, such as disruptions of the photoreceptor inner and outer segment (IS/OS) junction and disruptions of the external limiting membrane (ELM); these abnormalities were correlated to decreased postoperative visual acuity. These findings have prompted us to determine whether photoreceptor damage is a major cause of poor visual recovery after RRD with macula off. We focused most particularly on the ELM, the outer nuclear layer (ONL), the photoreceptor IS/OS junction, and the photoreceptor outer segment layer (PROS). We also compared SD-OCT imaging with preoperative and postoperative visual acuity, with postoperative fundus autofluorescence (FAF), and with macular sensitivity assessed by microperimetry.
Patients and Methods
We retrospectively examined patients who had undergone a successful surgery for a primary RRD involving the macula between January 1, 2007 and December 31, 2009 in 1 academic center. Inclusion criteria were a minimum follow-up period of 6 months after the surgery and written consent of the participants. Exclusion criteria were traumatic or tractional retinal detachment and macula-on RRDs. We also excluded patients with previous ocular diseases, macular abnormalities in the fellow eye, previous macular surgery, or a history of amblyopia. Patients with postoperative media opacities that could affect measurements or interpretations were also excluded.
Preoperative data were age, sex, preoperative visual acuity converted to the logarithm of the minimal angle of resolution (logMAR), time from the onset of symptoms to surgery, lens status, type of surgery, characteristics of the RRD including the number of quadrants involved, and the proliferative vitreoretinopathy grade ( Table 1 ). Patients had a complete ophthalmologic examination including measurement of the best-corrected visual acuity (BCVA) at 4 m with the standard Early Treatment Diabetic Retinopathy Study (ETDRS) chart, a slit-lamp examination, and dilated fundus ophthalmoscopy. On the same day, patients underwent a microperimetry examination with the Spectral OCT/SLO (Opko/Ophthalmic Technologies Inc, Toronto, Ontario, Canada) and macular imaging using the Spectralis HRA-OCT (Heidelberg Engineering, Heidelberg, Germany) using a confocal laser scanning system (SLO). Examinations were conducted by the same experienced investigator (M.P.D.). Postoperative data were the BCVA, the postoperative lens status to detect media opacities, fundus examination, findings of SD-OCT, fundus autofluorescence, and macular sensitivity.
|Number of patients/eyes (n,%)||n = 30|
|Right eyes||19 (67)|
|Left eyes||11 (37)|
|Age (years, mean ± SD [range])||67.3 ± 9.8 [52−83]|
|Duration of symptoms (days, mean ± SD [range])||7.1 ± 3.1 [2−15]|
|Extent of retinal detachment (n,%)|
|1 quadrant||7 (23)|
|2 quadrants||14 (47)|
|3 quadrants||6 (20)|
|4 quadrants||3 (10)|
|Proliferative vitreoretinopathy (n,%) a|
|Grade A||16 (53)|
|Grade B||12 (40)|
|Grade CP||2 (7)|
|Initial and final pseudophakic eyes (n,%)||14 (47); 26 (87)|
|Axial length (mm, mean ± SD)||24.42 ± 1.30|
|Preoperative visual acuity (logMAR, mean ± SD [range])||2.34 ± 0.93 [3−0.5]|
|Scleral buckling||4 (13)|
|PPV air-fluid exchange||24 (80)|
|PPV silicone oil tamponade||2 (7)|
|Postoperative visual acuity (logMAR, mean ± SD [range])||0.25 ± 0.25 [1−0.1]|
|Time between surgery and OCT (months, mean ± SD [range])||23.1 ± 10.3 [7−37]|
|Microperimetry (dB, mean ± SD)|
|Macular sensitivity (12 degrees)||14.15 ± 2.15|
|Foveal sensitivity (4 degrees)||14.04 ± 3.32|
a Grade A: vitreous haze; vitreous pigment clumps; vitreous clusters on inferior retina. Grade B: wrinkling of inner retinal surface; retinal stiffness; vessel tortuosity; rolled and irregular edge of retinal break; decreased mobility of vitreous. Grade CP 1−12: Posterior to equator: focal, diffuse, or circumferential full-thickness folds; subretinal strands.
Macular Imaging with Spectral-Domain Optical Coherence Tomography
The scan protocol consisted of a high-density acquisition of 25 consecutive horizontal B-scans centered on the fovea. B-scans were equally spaced 60 μm apart, covering a central foveal field of 20 × 5 degrees. Lesions in SD-OCT imaging were evaluated by 2 independent observers (M.P.D., C.C.G.). Macular thickness was obtained by automatic segmentation between the inner retinal border and the outermost reflective band (retinal pigment epithelium/Bruch membrane complex). The thickness of the ONL and of the PROS layer required manual segmentation on consecutive B-scans. The PROS thickness was the distance between the retinal pigment epithelium/Bruch membrane complex and the photoreceptor inner-outer segment junction. The thickness of the ONL was measured between the high reflective line of the ELM and the outermost reflection of the outer plexiform layer. The type and number of lesions detected in SD-OCT were as follows: hyperreflectivity spots in the outer nuclear layer, disruption of the external limiting membrane, disruption of the IS/OS junction, and an irregular hyporeflectivity in the PROS.
FAF photography was performed using a band-pass filter for the excitation light centered at 550 nm (bandwidth, 535−585 nm) and a matched barrier filter centered at 665 nm (bandwidth, 615−715 nm). The FAF topographic profile generally follows the distribution of lipofuscin in retinal pigment epithelium (RPE) cells, and a decrease in autofluorescence generally indicates a corresponding loss of or damage to the involved RPE cells. Fundus autofluorescence abnormalities seen in this series were recorded at 4 degrees and 12 degrees.
The recently developed Spectral OCT/SLO (Opko/Ophthalmic Technologies Inc) provides a perimetry of the central visual field with a scale of 0 to 20 decibels (dB) and can detect microscotomata; it also superimposes the microperimetry map onto the retinal thickness map. An eye tracking system is incorporated to compensate for eye movements. In this study, we used Goldmann III stimuli with a presentation time of 200 ms and a 4−2−1 staircase strategy. Twenty-eight locations were tested on a circular grid covering the 12 degrees of the central area. The 4-degree central sensitivity was also recorded. The examination was performed before pupil dilation and started on the fellow eye to limit the learning effect as all patients were inexperienced in automated perimetry. Fixation stability and response reliability (false-positive and false-negative rates) were monitored during the examination. Fixation was “stable” if more than 75% of the fixation points were gathered within a 2-degree central area. Fixation was “unstable” if less than 75% of the points were located inside a 4-degree central circle. Otherwise, fixation was regarded as “relatively unstable.” All our patients had less than 30% false-positive and false-negative responses.
For statistical analysis, preoperative and postoperative BCVA were converted to logMAR value. Patients were split into 2 groups according to their postoperative BCVA: 18 patients in group A with good BCVA (less than 0.3 logMAR) and 12 patients in group B with poor BCVA (0.3 logMAR or higher). Comparisons were performed with the Fisher exact test for dichotomous data. A nonparametric Mann-Whitney test was used for continuous variables such as age or visual acuity. The Spearman rank correlation coefficient was used as a measure of association between non-normally distributed variables, such as retinal sensitivity results, retinal thickness, or the number of lesions in the photoreceptor layer. All analyses were conducted using Prism 5.01 (Graphpad Software, La Jolla, California, USA). The level of statistical significance was set at P < .05 and the tests were 2-tailed.
Sixty-seven patients satisfied all of the study criteria. Thirty-five patients agreed to participate in the study. Five of them were excluded because of media opacities. Finally, 30 eyes of 30 patients (19 men and 11 women) were included; their characteristics are displayed in Table 1 and Table 2 . The follow-up time after surgery was mean ± standard deviation, [range] 23.1 ± 10.3 months [7−37].
|No.||Sex||Eye||Preoperative BCVA (logMAR)||Postoperative BCVA (logMAR)||PROS Irregular Reflectivity||IS/OS Junction Disruption||ELM Disruption||ONL Changes||Other Intraretinal Changes||FAF Abnormality||MP 12 Degrees (dB)||MP 4 Degrees (dB)||Fixation Stability||Macular Thickness (μm)||ONL Thickness (μm)||PROS Thickness (μm)|