Analysis of Choroidal Thickness Changes in Recurrent Rhegmatogenous Retinal Detachment

doi:10.21203/rs.3.rs-4003023/v1

Purpose: To analyze changes in subfoveal choroidal thickness in patients with recurrent rhegmatogenous retinal detachment (RRD) before and after surgical intervention.

Methods: A retrospective observational study was conducted on patients who underwent surgery for recurrent RRD from November 2019 to March 2023. Choroidal thickness was measured using optical coherence tomography (OCT) at baseline, and then at 2 and 6 months postoperatively. The study analyzed the impact of various factors on choroidal thickness changes.

Results: The study included 33 patients, demonstrating a significant decrease in subfoveal choroidal thickness in the surgical eye compared to the fellow eye over a 6-month period. In the univariate analysis, changes in choroidal thickness were significantly correlated with changes in central retinal thickness (p=0.048) between 0-2 months, and with proliferative vitreoretinopathy (PVR) grade between 2-6 months (p=0.009) and 0-6 months(p=0.02). In the multivariate analysis, an association was found between changes in choroidal thickness from 2 to 6 months and PVR grade(p=0.006)

Conclusion: The findings indicate that surgical reattachment in eyes with recurrent RRD leads to a significant reduction in choroidal thickness. The extent of this reduction is influenced by the severity of PVR, highlighting the importance of considering PVR severity when evaluating surgical outcomes in patients with recurrent RRD.

choroidal thickness

rhegmatogenous retinal detachment

proliferative vitreoretinopathy

optical coherence tomography

The choroid is responsible for maintaining the function of the retina by supplying oxygen and nutrients to the retinal epithelial layer and the optic nerve cell. Previous studies have reported decreased blood flow to the macula after retinal detachment surgery, which has been associated with poor visual acuity after retinal detachment surgery.[1] Given that subfoveal choroidal thickness can be used as a tool to assess ocular blood flow function in the macula, measuring changes in choroidal thickness after retinal detachment surgery is important.[2]

Previous studies of choroidal thickness after rhegmatogenous retinal detachment surgery have reported mixed results, with some reporting increased subfoveal choroidal thickness in rhegmatogenous eyes compared to normal eyes and that choroidal thickness decreases again after retinal adhesion to become non-significantly different from normal eyes,[3, 4] and others reporting decreased choroidal thickness after surgery.[5]

To the best of our knowledge, previous studies investigating choroidal thickness changes in retinal detachment have defined the control as the choroidal thickness of the contralateral eye. This approach stems from the practical limitation of being unable to measure choroidal thickness before retinal detachment occurs in patients with this condition. However, we have previously reported interocular differences in choroidal thickness based on fixation preference patterns. Considering the characteristic prevalence of myopia in retinal detachment, comparing choroidal thickness with that of the contralateral eye could introduce errors.[6]

Therefore, this study aimed to investigate changes in choroidal thickness after surgery in patients with recurrent retinal detachment by measuring the choroidal thickness before the occurrence of recurrent retinal detachment. We also aimed to identify factors influencing these changes in choroidal thickness.

This retrospective observational study was conducted in accordance with the Declaration of Helsinki and was approved by the Institutional Review Board (HPIRB 2023-07-011-001). We included patients diagnosed and treated for recurrent retinal detachment between November 2019 and March 2023. Recurrent retinal detachment was defined as re-detachment of the retina after initial surgery, with stable retinal attachment and maintenance of anatomic success for at least 2 weeks. Patients with high myopia (axial length ≥ 28 mm or spherical equivalent ≤ -6), macular hole retinal detachment, traumatic retinal detachment, age-related macular degeneration, pachychoroidal neovascularization, retinal vascular occlusion, or diabetic retinopathy were excluded as these conditions could affect choroidal thickness.

Baseline choroidal thickness was defined as the choroidal thickness with macular adhesions immediately prior to the time of recurrence detection and examined at 2 and 6 months after reoperation. Choroidal thickness was defined as the distance from the lower part of the retinal pigment epithelial layer to the choroid-sclera interface on the horizontal section of the OCT, and thickness measurement was performed using the method proposed by Manjunath et al[7], and Ban et al[8].(Fig. 1) Manual measurements made by two researchers using manual calipers were compared, and the average of the two measurements was used. If the measurements of the two investigators differed by more than 10%, a third investigator arbitrated and the mean of the values differing by less than 10% was used. The choroidal thickness of the contralateral eye was also measured at the same time point and used as a control for analysis.

In addition to choroidal thickness, factors such as age, gender, slit-lamp examination results, spherical equivalent, surgical methods used during the initial and subsequent surgeries, time until recurrence of retinal detachment after the first surgery, extent of retinal detachment (superior/inferior), presence of macular detachment, and proliferative vitreoretinopathy (PVR) were evaluated. Best corrected visual acuity, intraocular pressure, and central retinal thickness were also examined at each research time point. Spectral-domain optical coherence tomography (SD-OCT) with Enhanced Depth Imaging (EDI) (SPECTRALIS®, Heidelberg Engineering, Heidelberg, Germany) was utilized, measuring choroidal thickness from horizontal scan images crossing the macular center. The average retinal thickness within the central 1000µm area from the OCT macular thickness map was used to determine the central macular thickness.

Statistical analysis

Statistical analysis was conducted using IBM SPSS Statistics version 21.0 (IBM Corp., Armonk, NY, USA). Changes in choroidal thickness over time for both the recurrent and control groups were investigated using Repeated Measures ANOVA, and post hoc analysis was performed to examine the significance of differences between time points (baseline vs. 2 months, 2 months vs. 6 months, baseline vs. 6 months) using Paired-Samples T Test. If Mauchly's test of sphericity was violated in the Repeated Measures ANOVA, degrees of freedom were adjusted using the Greenhouse-Geisser and Huynh-Feldt methods. Pearson’s correlation analysis was conducted to identify factors contributing to changes in choroidal thickness as part of univariate analysis, and Multiple regression with dummy value was used for multivariate analysis. The statistical significance of each factor was set at p value < 0.05, but Bonferroni correction was applied in post hoc analysis to control for Type I errors.

A total of 33 patients were enrolled in the study. The average age of the patients was 54.5 ± 17.3 years, with 20 males and 13 females. At the time of recurrence, the state of the macula was attached in 24 eyes and detached in 9 eyes. Retinal detachment findings showed superior detachment in 9 eyes, inferior detachment in 22 eyes, and both superior and inferior involvement in 2 eyes. At the time of recurrence, 29 eyes were diagnosed with proliferative vitreoretinopathy (PVR), with 6 eyes showing PVR grade a, 12 eyes showing PVR grade b, and 11 eyes showing PVR grade c. The average time to recurrence after the primary surgery was 126.8 days (Table 1).

At the primary surgery, 8 eyes underwent explant buckling, 22 eyes had pars plana vitrectomy (PPV) alone, and 3 eyes had both explant buckling and PPV (Table 2 − 1). During reoperation, 26 eyes received PPV alone, and 7 eyes had both encircling and PPV. The surgical methods and types of tamponades used during reoperation are listed in the tables (Table <link rid="tb3">2</link>–2).

The choroidal thickness for the recurrent and fellow eyes was 201.32 ± 80.54µm and 200.12 ± 78.41 µm at baseline, respectively. At 2 months post-surgery, the measurements were 195.18 ± 72.15µm for the recurrent eye and 198.93 ± 78.85µm for the fellow eye. At 6 months, they were 186.32 ± 72.96µm for the recurrent eye and 197.46 ± 77.63 µm for the fellow eye (Fig. 2). When comparing the choroidal thickness of the recurrent and fellow eyes, a significant decrease in choroidal thickness over time was observed in the recurrent eye, but not in the fellow eye (Repeated Measures ANOVA, Recurrent eye Greenhouse-Geisser: P = 0.009, Huynh-Feldt p = 0.009; Fellow eye Greenhouse-Geisser: P = 0.214, Huynh-Feldt p = 0.213).

In the post hoc analysis, there was no significant difference from baseline to 2 months. However, significant reductions in choroidal thickness were observed in the recurrent eye from baseline to 6 months, and between 2 to 6 months (P = 0.089, p = 0.010, p = 0.012, after applying Bonferroni correction, with a significance level set at p value 0.0167).

In univariate analysis, changes in choroidal thickness showed significant correlations with the amount of change in central retinal thickness and the grade of proliferative vitreoretinopathy (PVR). The change in central retinal thickness demonstrated a significant correlation with a correlation coefficient of 0.347 and a significance probability of 0.048 between 0–2 months. However, no significant correlation was observed between 2–6 months and 0–6 months (p = 0.497, p = 0.26). Proliferative vitreoretinopathy showed a positive correlation with changes in choroidal thickness between 2–6 months and 0–6 months, with correlation coefficients of 0.448 (p = 0.009) and 0.404 (p = 0.02), respectively. No significant correlation was found between 0–2 months (p = 0.229).

In the multivariate analysis, an association was identified between the changes in choroidal thickness from 2 to 6 months and the grade of proliferative vitreoretinopathy (PVR) (ANOVA p = 0.030, Coefficients: PVR grade p = 0.006).

The results of this study showed that the choroidal thickness in eyes with recurrent retinal detachment was statistically significantly reduced compared to the fellow eye six months after surgical treatment. The change in choroidal thickness varied over time but was correlated with the grade of proliferative vitreoretinopathy and the change in central retinal thickness.

Several studies have reported on the changes in choroidal thickness after primary retinal detachment surgery. Some studies have shown a significant increase in subfoveal choroidal thickness immediately after surgery, and from one month post-surgery, the thickness returned to the level of a normal eye [4, 9]. A report from Korea observed a significant decrease in choroidal thickness in the second month after primary retinal detachment surgery, and a significant decrease in choroidal thickness was also observed in the group that had more than 30 days elapse from symptom onset to the day of surgery. This finding aligns with the results of this study. However, a limitation of all previous studies is that they focused on primary retinal detachment and set the control group as choroidal changes in the fellow eye [8].

As the results of this study, changes in choroidal thickness vary over time. In this study, patients who showed recurrence of retinal detachment within two weeks were excluded, as it was difficult to conclude that complete adhesion between the neurosensory retina and the choroid had occurred after the primary surgery. Among the patients enrolled in the study, the longest duration between the first and second surgeries was 1139 days, with a median of 60 days. Therefore, it was assumed that for these patients, the choroidal thickness had stabilized after the initial adhesion between the neurosensory retina and the choroid, and the baseline choroidal thickness was measured after this stabilization.

In this study, the change in central retinal thickness and the change in subfoveal choroidal thickness showed a correlation, with a positive correlation observed between the amount of change in central retinal thickness and the amount of change in subfoveal choroidal thickness within 0–2 months. After that period, no correlation could be found. Among the 33 eyes studied, cystoid macular edema was present in 6 eyes at the 2-month mark and in 17 eyes at the 6-month mark, which may have made it difficult to find a significant relationship between retinal thickness and choroidal thickness after the secondary surgery.

In the multivariate analysis, the amount of change in choroidal thickness significantly decreased according to the grade of proliferative vitreoretinopathy, suggesting that retinal hypoxia and ocular hypoxia itself could have some influence on the decrease in central choroidal thickness. However, as this study did not directly assess the factors mentioned above, it is difficult to draw conclusions.

After retinal detachment, the thickness of the choroid decreased, and one possible mechanism for this could be the effect of silicone oil tamponade. According to previous reports, there are several studies suggesting that the use of silicone oil leads to a decrease in choroidal thickness thereafter [5, 10, 11]. The direct pathophysiological mechanism behind the decrease in central choroidal thickness due to silicone oil has not yet been clarified. However, there are study results suggesting that central retinal degeneration occurs due to the failure of Müller cells to absorb potassium due to silicone oil toxicity. This, in turn, could have a negative impact on the central choroidal blood flow, leading to a decrease in central choroidal thickness [12, 13]. Additionally, there are reports suggesting that the infiltration of silicone oil into the retina can cause neural damage to ganglion and bipolar cell synapses, leading to a decrease in macular function [14]. There are reports suggesting that mechanical stress from silicone oil tamponade and inflammation caused by the subretinal migration of silicone oil can also be contributing factors. [15–17] As other possible mechanism, there are reports that performing laser photocoagulation not only destroys the structure of the retina but also reduces the thickness of the choroid.[18, 19]

The limitations of this study include the small number of subjects, which may limit statistical interpretation, and the lack of analysis on the area of PVR and laser treatment extent, preventing the analysis of choroidal thickness changes according to PVR area and laser treatment area. The inability to clarify the correlation between choroidal thickness and visual function is thought to be due to the retrospective nature and the small number of subjects. Despite these limitations, this study is significant as it is a report to measure the changes in choroidal thickness in the same eye, rather than the contralateral eye, before and after surgery in patients with retinal detachment.

In conclusion, in patients with recurrent retinal detachment, the thickness of the choroid significantly decreased after reattachment of the retina, and the greater the severity of proliferative vitreoretinopathy, the more the choroidal thickness decreased.

Author Contribution

G.C. and K.P. wrote the main manuscript text and S.L. was responsible for creating all tables and figures. All authors reviewed the manuscript.

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Table 1. Characteristics of subject patients

Factors	Results (Mean ± SD)
Sex(Male : Female)	20 : 13
IOP(Pre-OP)	13.52mmHg ± 2.52mmHg
IOP(Post-OP)	18.42mmHg ± 3.24mmHg
Macula on : Macula off	24 : 9
PVR	29
PVR grade a	6
PVR grade b	12
PVR grade c	11
Extent of RRD
Superior	9
Inferior	22
Total	2
Axial length	25.85mm

Values presented behind ± mean standard deviations

IOP = intraocular pressure, RRD = rhegmatous retinal detachment

Table 2-1. Summary of the different surgical technics used (Primary OP)

Surgical technics	Results
Explant buckling alone	8
PPV alone	22
Explant buckling + PPV	3
Tamponades
SF6 gas(20%)	10
C3F8 gas(14%)	3
Silicone oil 1300cst	10
Silicone oil 5700cst	2

Table 2-2. Summary of the different surgical technics used (Secondary OP)

Surgical technics	Results
PPV alone	26
Encircling + PPV	7
Tamponades
SF6 gas(20%)	2
C3F8 gas(14%)	4
Silicone oil 1300cst	21
Silicone oil 5700cst	6

PPV = pars plana vitrectomy

No competing interests reported.

Analysis of Choroidal Thickness Changes in Recurrent Rhegmatogenous Retinal Detachment

Status:

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Abstract

Figures

Introduction

Methods

Statistical analysis

Results

Discussion

Conclusion

Declarations

Author Contribution

References

Tables

Additional Declarations

Status:

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