Ophthalmic Surgery, Lasers and Imaging Retina

Clinical Science 

Segmental Analysis of Macular Layers in Patients With Rhegmatogenous Retinal Detachment Treated With Perfluoropropane or Silicon Oil

Yasin Sakir Goker, MD; Kemal Yuksel, MD; Miray Faiz Turan, MD; Kenan Sonmez, MD; Kemal Tekin, MD; Pelin Yilmazbas, MD

Abstract

BACKGROUND AND OBJECTIVE:

To determine possible changes in thickness profiles of retinal layers in patients with rhegmatogenous retinal detachment (RRD) treated with perfluoropropane (C3F8) or silicon oil (SiO).

PATIENTS AND METHODS:

Seventy-two eyes of 36 patients were enrolled in this retrospective comparative study. Patients were divided into two groups according to intraocular tamponade: C3F8 or SiO. All study eyes were compared with fellow eyes via spectral-domain optical coherence tomography segment analysis at 6 months postoperatively. Macular layer thicknesses including retinal nerve fiber layer, ganglion cell layer, inner plexiform layer, inner nuclear layer (INL), outer plexiform layer (OPL), outer nuclear layer (ONL), and retinal pigment epithelium were analyzed.

RESULTS:

There was a statistically significant difference between eyes in terms of INL thickness (P = .044) in C3F8 group. Otherwise there was a statistically significant difference between eyes in terms of INL, OPL, and ONL thicknesses (P = .006, P = .048, and P = .004, respectively) in the SiO group.

CONCLUSION:

The findings of the present study show that the tamponade used in RRD surgery can affect the retinal layers differently.

[Ophthalmic Surg Lasers Imaging Retina. 2018;49:41–47.]

Abstract

BACKGROUND AND OBJECTIVE:

To determine possible changes in thickness profiles of retinal layers in patients with rhegmatogenous retinal detachment (RRD) treated with perfluoropropane (C3F8) or silicon oil (SiO).

PATIENTS AND METHODS:

Seventy-two eyes of 36 patients were enrolled in this retrospective comparative study. Patients were divided into two groups according to intraocular tamponade: C3F8 or SiO. All study eyes were compared with fellow eyes via spectral-domain optical coherence tomography segment analysis at 6 months postoperatively. Macular layer thicknesses including retinal nerve fiber layer, ganglion cell layer, inner plexiform layer, inner nuclear layer (INL), outer plexiform layer (OPL), outer nuclear layer (ONL), and retinal pigment epithelium were analyzed.

RESULTS:

There was a statistically significant difference between eyes in terms of INL thickness (P = .044) in C3F8 group. Otherwise there was a statistically significant difference between eyes in terms of INL, OPL, and ONL thicknesses (P = .006, P = .048, and P = .004, respectively) in the SiO group.

CONCLUSION:

The findings of the present study show that the tamponade used in RRD surgery can affect the retinal layers differently.

[Ophthalmic Surg Lasers Imaging Retina. 2018;49:41–47.]

Introduction

Optical coherence tomography (OCT) imaging is commonly used in diagnosing and monitoring retinal diseases. New developments in OCT have improved the quality of the acquired images1 and allow automatic measurements of intraretinal layers. A new update for the Spectralis (Heidelberg Engineering, Heidelberg, Germany), the Heidelberg Eye Explorer mapping software (version 6.0c) allows quantitative measurements of individual retinal layers such as the nerve fiber layer (NFL), ganglion cell layer (GCL), inner plexiform layer (IPL), inner nuclear layer (INL), outer plexiform layer (OPL), outer nuclear layer (ONL), inner segment (IS), outer segment (OS), and retinal pigment epithelium (RPE).2 In this study, we compared the macular layer thicknesses in patients with rhegmatogenous retinal detachment (RRD) treated with perfluoropropane (C3F8) or silicon oil (SiO). The aim was to find out possible changes in thickness profiles of retinal layers related with the type of intraocular tamponade used.

Patients and Methods

Seventy-two eyes of 36 patients were enrolled in this retrospective comparative study, and patients were divided into two groups according to intraocular tamponade: C3F8 or SiO. All patients had macula-off retinal detachment (RD), and all RD cases underwent standard, sutureless, three-port, 23-gauge pars plana vitrectomy (PPV) between September 2014 and December 2015. All surgeries were performed by the same surgeon at a tertiary hospital. All patients received a complete ophthalmic examination, including measurement of best-corrected visual acuity (BCVA) using a Snellen chart, biomicroscopic evaluation of the anterior segment, and dilated fundus examination; all examinations were performed preoperatively and postoperatively on day 1, week 1, and at 1, 3, and 6 months after surgery. Spectral-domain optical coherence tomography (SD-OCT) segment analysis was used to assess each patient at 6 months postoperatively.

Exclusion criteria included the following: axial length (AL) greater than 24 mm and less than 22 mm, traumatic RD, ocular pathologies except retinal detachment, severe proliferative vitreoretinopathy (PVR), and cataract that affected SD-OCT analysis at 6-month evaluation for study eyes. All fellow eyes were normal, had similar AL, and had no history of ocular diseases. Postoperative complications that could affect the retinal layers including high intraocular pressure levels, hypotonia, and long-acting ocular inflammation were also excluded. The symptom duration was defined as the number of days from vision loss to surgery.

All patients provided informed consent prior to surgery, and all the procedures were approved by the institutional ethics committee. This study adheres to the Declaration of Helsinki.

Surgery

All patients underwent standard, sutureless, three-port, 23-gauge PPV with triamcinolone acetonide (TA)-assisted posterior vitreous detachment (PVD), if not already present, cleaning of the vitreous base, and endo-photocoagulation of retinal tears and breaks. Fluid-air exchange was performed through an extrusion cannula, which was followed by the injection of 15% perfluoropropane (C3F8) for superior retinal tears and breaks or 1,000-centistoke SiO for inferior retinal tears and breaks. SiO removal was performed at the fourth month postoperatively. Anatomic success was defined as complete retinal reattachment.

SD-OCT Segmentation

All study eyes were compared with fellow eyes with SD-OCT segment analysis at 6 months postoperatively. All images were taken and assessed by an experienced retinal specialist. To analyze layer thickness estimates, initial intraretinal segmentation was performed using the Heidelberg Eye Explorer software (Version 6.0.0.2). A physician reviewed the results and occasionally corrected the segmentation lines when necessary (semiautomatic segmentation). Segmentation line correction was performed separately for each scan without using any other scan for reference. All central 1 mm macular layer thicknesses including RNFL, GCL, IPL, INL, OPL, ONL, and RPE were analyzed. Central macular thickness (CMT) and inner and outer retinal layer thicknesses (IRL/ORL) were also analyzed. Figures 1 to 3 show an example of retinal layer segmentation with OCT scan.

Central macular thickness, retinal nerve fiber layer, and ganglion cell layer segmentations.

Figure 1.

Central macular thickness, retinal nerve fiber layer, and ganglion cell layer segmentations.

Inner plexiform layer, inner nuclear layer, and outer plexiform layer segmentations.

Figure 2.

Inner plexiform layer, inner nuclear layer, and outer plexiform layer segmentations.

Outer nuclear layer segmentation, as well as retina pigment epithelium, inner retina, and outer retina thicknesses. (A case was from the silicone oil group and spectral-domain optical coherence tomography segmentation at 6 months postoperatively.)

Figure 3.

Outer nuclear layer segmentation, as well as retina pigment epithelium, inner retina, and outer retina thicknesses. (A case was from the silicone oil group and spectral-domain optical coherence tomography segmentation at 6 months postoperatively.)

Statistical Analysis

The Kolmogorov-Smirnov test was applied to assess the normal distribution of data. One-way analysis of variance was used to evaluate homogeneity between groups (P > .05). To compare the measurements between the eyes parametric t-test or nonparametric Mann-Whitney test were performed. The SPSS version 20 (SPSS, Chicago, IL) was used for data analysis, for which P values less than .05 were considered to be statistically significant.

Results

The clinical characteristics of participants are shown in Table 1. Thirty-two eyes of 16 patients were included in the C3F8 group, and 40 eyes of 20 patients were included in the SiO group. The mean ages of the patients were 44.25 years ± 15.80 years (range: 44 years to 66 years) and 56.35 years ± 12.50 years (range: 45 years to 77 years) in the C3F8 and SiO groups, respectively. Symptom duration was 3.92 days ± 1.80 days (range: 2 days to 7 days) versus 4.22 days ± 1.65 days (range: 3 days to 8 days) for patients in the C3F8 and SiO groups, respectively. Therefore, symptom duration did not demonstrate a significant difference between groups (P = .738). The mean AL was 23.04 mm ± 1.10 mm (range: 22.73 mm to 23.95 mm) in the C3F8 group and 23.21 mm ± 1.13 mm (range: 22.77 mm to 23.97 mm) in the SiO group. There was no statistically significant difference between eyes treated with C3F8 or SiO in terms of AL (P = .511).

Participants' Clinical Characteristics

Table 1:

Participants' Clinical Characteristics

The mean RNFL, GCL, IPL, INL, OPL, ONL, and RPE thicknesses of the C3F8 and SiO groups are shown in Tables 2 and 3, respectively. IRL, ORL thicknesses, and CMT are also shown in the tables. There was a statistically significant difference between eyes in terms of INL thickness in C3F8 group (P = .044). Other variables showed no statistically significant difference in the C3F8 group. On the other hand, there was a statistically significant difference between eyes in terms of INL, OPL, and ONL thicknesses (P = .006, P = .048, and P = .004, respectively) in the SiO group. Other variables showed no statistically significant differences in the SiO group.

Retinal Layer Thicknesses of the Perfluoropropane Group

Table 2:

Retinal Layer Thicknesses of the Perfluoropropane Group

Retinal Layer Thicknesses of the Silicone Oil Group

Table 3:

Retinal Layer Thicknesses of the Silicone Oil Group

The mean preoperative BCVA was 0.004 ± 0.006 and improved to 0.177 ± 0.145 postoperatively at 6 months in the C3F8 group (P < .001), and mean preoperative BCVA was 0.005 ± 0.006 and improved to 0.167± 0.143 postoperatively at 6 months in the SiO group (P < .001).

Discussion

Improvements in OCT technologies allow physicians to evaluate and measure thickness of individual intraretinal layers. These quantitative measurements play an important role in the diagnosis and monitoring of many retinal diseases.3–5 Thinning of the RNFL is often noted in myopia,3 glaucoma,4 and diabetic retinopathy.5 Thinning of the GCL reported in glaucoma.6 In age-related macular degeneration, the OS layer gets thinner and the RPE layer gets thicker when vision field defects are present.7 Segmentation also gives physicians information about the prognosis of the disease.8–10 It has been reported that ONL thickness is correlated with visual acuity (VA) in central serous chorioretinopathy.11 The thickness and integrity of the IS and OS may be an important predictor of VA in a wide spectrum of surgical and medical retinal diseases.12–14 Terauchi et al. reported that the increase in the thicknesses of the IS and OS layers during the recovery period of retinal detachment surgery.15 They added that the quantitative analysis of the IS and OS thicknesses may be useful to follow the recovery process.15 Evaluating of intraretinal layers is also important in neurological disease. Thickness of RNFL and the inner retinal layers are reported to change in Parkinsonian syndromes.16

There are a few studies in literature that present retinal segmentation measurements of healthy subjects.17 Huang et al. reported measurements of 30 eyes from 30 normal subjects using the RTVue 100 (Optovue, Fremont, CA).17 However only the inner, outer, and full retinal thicknesses at the foveal central subfield (67.31 μm ± 12.27 μm, 151.67 μm ± 12.96 μm, and 219.33 μm ± 23.19 μm) were presented in their study.17

A RRD causes anatomical disruption of integrity of the retina, resulting in a decrease in the VA. Reattachment of the retina leads to a recovery of retinal layers and vision. However, the degree of visual recovery differs among patients despite successful reattachment in all. It has been reported that the degree of recovery is related to the symptom duration, preoperative VA, macula-off retinal detachment, presence of PVR and may be the type of intraocular tamponade. After a successful repair of RRD with no postoperative complication such as the presence of an epiretinal membrane, cystoid macular edema, retinal folds, and a persistent foveal detachment,18–19 we aim to find out possible changes in thickness profiles of retinal layers related with the type of intraocular tamponade used.

Müller cells are the radial glia of the retina and their nuclei lie within the inner nuclear layer. These cells are the main cells responsible for retinal integrity. In the structural remodeling after retinal detachment and reattachment, Müller cells play an important role. Fisher et al. have observed some cellular alterations in retina after reattachment.20 Vimentin, an intermediate filament protein, extends throughout the cytoplasm of the Müller cells. Vimentin often colocalizes in Müller cells with another intermediate filament protein, glial fibrillary acidic protein (GFAP).20 These intermediate filaments eventually fill the entire cell and make an increase in the volume of the INL thickness. In our study, INL thickness was higher in the study eye than in the fellow eye both in the C3F8 and SiO groups (P < .005).

Müller cells may also have migrate to OPL and ONL. Fisher et al. reported an electron micrograph showing a mitotic figure in the ONL.20 In our study, OPL thickness was higher in the study eye than the fellow eye both in the C3F8 and SiO groups, but it was not statistically significant in the C3F8 group (P = .792 in C3F8 group and P = .048 in the SiO group).

Fisher et al. showed that rods withdraw their terminals from the OPL and the tightly organized layer of terminals found in normal retina is disrupted and decreased in thickness after retinal detachment.20 Rods have lost their deep synaptic invaginations.20 In the SiO group, decrease in ONL thickness was statistically significant, but in the C3F8 group, this quantitative decrease did not demonstrate a statistically significant difference (P = .076 in the C3F8 group and P = .004 in the SiO group). In the light of these findings, we can postulate that SiO could affect retinal layers more than C3F8 as a tamponade.

The limitations of the present study include the relatively small number of patients and its retrospective design. The strength of this study is the quantitative assessment of every retinal layer using SD-OCT.

In conclusion, we propose that not only factors such as disruption of the junction between the inner and outer segments of photoreceptor layer, disrupted external limiting membrane, cystoid macular edema and epiretinal membranes;21–22 but also the intraocular tamponade used, could affect visual recovery after a successful repair of retinal detachment.

References

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Participants' Clinical Characteristics

Perfluoropropane GroupSilicone Oil GroupP Value*
n1620
Age (Years)44.25 ± 15.8 (range: 44 to 66)56.35 ± 12.5 (range: 45 to 77)P = .631
Symptom Duration (Days)3.92 ± 1.80 (range: 2 to 7)4.22 ± 1.65 (range: 3 to 8)P = .738
Axial Length23.04 ± 1.10 (range: 22.73 to 23.95)23.21 ± 1.13 (range: 22.77 to 23.97)P = .511

Retinal Layer Thicknesses of the Perfluoropropane Group

nMean (µm)Standard DeviationP Value*

CMTStudy Eye16291.0047.68.650
Fellow Eye16283.6243.13

RNFLTStudy Eye1618.7510.73.217
Fellow Eye1614.816.40

GCLTStudy Eye1627.0613.28.194
Fellow Eye1620.6214.12

IPLTStudy Eye1626.816.92.337
Fellow Eye1624.009.21

INLTStudy Eye1633.8714.40.044
Fellow Eye1624.3111.13

OPLTStudy Eye1626.186.40.792
Fellow Eye1625.3710.39

ONLTStudy Eye1675.5026.02.076
Fellow Eye1690.0017.78

RPETStudy Eye1616.066.28.926
Fellow Eye1612.254.98

IRLTStudy Eye16207.4345.34.545
Fellow Eye16197.8143.65

ORLTStudy Eye1683.688.51.402
Fellow Eye1685.875.77

Retinal Layer Thicknesses of the Silicone Oil Group

nMean (µm)Standard DeviationP Value*

CMTStudy Eye20280.036.62.881
Fellow Eye20277.950.91

RNFLTStudy Eye2017.607.62.079
Fellow Eye2013.804.84

GCLTStudy Eye2020.8010.91.934
Fellow Eye2020.4513.91

IPLTStudy Eye2023.906.75.721
Fellow Eye2023.008.99

INLTStudy Eye2032.059.81.006
Fellow Eye2023.009.97

OPLTStudy Eye2032.1513.65.048
Fellow Eye2024.959.02

ONLTStudy Eye2069.9523.44.004
Fellow Eye2089.3516.37

RPETStudy Eye2016.8010.80.732
Fellow Eye2015.952.03

IRLTStudy Eye20195.4536.61.884
Fellow Eye20193.3550.67

ORLTStudy Eye2084.4512.98.987
Fellow Eye2084.504.46
Authors

From Ankara Ulucanlar Eye Training and Research Hospital, Ankara, Turkey (YSG, KT, KS, PY); Beyoglu Eye Training and Research Hospital, Istanbul, Turkey (KY); and Adana Numune Eye Training and Research Hospital, Adana, Turkey (MFT).

The authors report no relevant financial disclosures.

Address correspondence to Yasin Sakir Goker, MD, Ulucanlar Eye Training and Research Hospital, Ankara, 06240, Turkey; email: yasingoker5367@hotmail.com.

Received: April 02, 2017
Accepted: September 20, 2017

10.3928/23258160-20171215-06

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