Changes in retinal layers after pars plana vitrectomy for rhegmatogenous retinal detachment

doi:10.21203/rs.3.rs-3137056/v1

Visual recovery after retinal detachment is often delayed despite surgical success. Changes in retinal thickness have been shown to occur after vitrectomy for retinal detachment and visual acuity seems to be related with these modifications. In this retrospective study we investigated the thickness of retinal layers using optical coherence tomography in patients successfully treated for rhegmatogenous retinal detachment between December 2014 and March 2023. We further investigated possible related clinical and demographic characteristics. A total of 1313 patients were initially identified. Of these, 1282 patients were excluded and finally 31 eyes from 31 patients were included. Twelve months after the surgical procedure the total retinal thickness, in particular, the outer nuclear layer thickness, significantly increased compared to one month postoperatively (respectively, 270.6 ± 34.2 vs. 288.0 ± 29.7, P < 0.001 and 79.5 ± 23.3 vs. 92.9 ± 16.5, P < 0.001). Factors associated with the increase were age, macula off status and the use of SF₆ tamponade (all P < 0.05). No correlation was found between the increase in outer nuclear layer thicknesses and the final visual acuity in pseudophakic patients.

Health sciences/Biomarkers/Predictive markers

Health sciences/Risk factors

Rhegmatogenous retinal detachment (RRD) is a vision-threatening disease, characterized by the separation of the neurosensory retina from the underlying retinal pigment epithelium due to the presence of retinal breaks that allow fluid accumulation from the vitreous cavity into the subretinal space.¹ Pars plana vitrectomy (PPV) is currently the most common procedure used for the treatment of RRD with a success rate of up to 90%.^1–4 However, even in the case of successful surgery and complete anatomic reattachment, the functional recovery can take a long time and may not be complete.^5,6 The reason is not yet perfectly clear but previous studies demonstrated that the detached retina may show a lengthening of the horizontal and bipolar cell processes, a degeneration of photoreceptors and a considerable loss of ganglion cells.⁷ Recent improvements in spectral-domain optical coherence tomography (SD-OCT) facilitated the imaging of microstructural retinal changes that are not clinically observable by fundus biomicroscopy.^6,8–12 Previous studies investigated retinal layers changes in the pre- and post-operative period using SD-OCT, trying also to define prognostic factors that may predict the anatomic and visual outcome.^{2,5–8,13,14} Several authors reported a global retinal thickness decrease, especially in the outer layers, in the immediate postoperative phase and a progressive recovery over time after RRD surgery, in association with visual improvement.^2,5,7,8 Moreover, some authors showed that after RRD surgery the retinal modifications that can be detected on OCT scans are mainly a disruption of the external limiting membrane (ELM), ellipsoid zone (EZ), and cone interdigitation zone (IZ). Moreover, they reported that recovery of the EZ and thickening of the retinal layers in the foveal area in the post-operative period are associated with recovery of best-corrected visual acuity (BCVA).^5,7,15–17 The aim of this study was to investigate the restoration process of the different retinal layers during the first year after successful RRD repair using SD-OCT and, in particular, to assess the correlations of retinal thickness recovery with BCVA.

A total of 1313 patients treated with PPV for RRD were initially identified. Of these, 1282 patients did not satisfy the inclusion/exclusion criteria and were excluded from the final analysis. In particular, 124 presented a retinal detachment caused by proliferative diabetic retinopathy, trauma or posterior uveitis; 153 had either glaucoma, amblyopia or a pre-existing macular disease; 45 presented a recurrence of RRD; 135 patients were treated only with cryopexy; 526 had postoperative retinal alterations, in particular significant epiretinal membrane, macular hole and/or macular oedema; 299 patients did not presented an interpretable OCT at month 1 and 12 after the surgical procedure.

Finally, 31 patients were included in the study. Demographic and surgical characteristics of included patients are reported in Table 1. Mean age was 63 ± 11.6 years, 18 (58.1 %) were male and 13 (41.9 %) were female. Twenty patients (67.7 %) presented a macula off RRD at the time of the procedure. All the 31 patients received gas tamponade, 22 of these (71 %) with C2F6 and 9 patients (29 %) with SF6. Perfluorocarbon liquid (PFCL) was used in the 51.6 % of cases. Fourteen patients (45.2 %) underwent trans-scleral cryopexy and 17 (54.8 %) underwent endolaser to achieve retinopexy.

The retinal layers thickness measured at month 1 (M1) and 12 (M12) follow up visit are reported in Table 2. CMT was significantly increased between M1 and M12 (respectively, 270.6 ± 34.2 vs. 288.0 ± 29.7; P < 0.001). In particular, the ONL and the NFL significantly increased between M1 and M12 (respectively, 79.5 ± 23.3 vs. 92.9 ± 16.5; P < 0.001 and 13.3 ± 2.2 vs. 14.0 ± 2.5; P = 0.03). No significant differences between M1 and M12 were found in GCL, IPL, INL, OPL and RPE (all P > 0.005).

The ANCOVA test showed a significant effect of age, the status of the macula and the type of intraocular tamponade on the change in ONL (Table 3).

We observed a greater increase in CMT between M1 and M12 in older patients (P = 0.002), in patients that presented a macula off RRD (P = 0.001) and in those that received SF6 gas tamponade (P = 0.01). The Pearson correlation test didn’t show any significant correlation between the increase in CMT and BCVA in pseudophakic patients (P = 0.8).

In the present study, we investigated changes of retinal layers thickness after PPV for RRD using SD-OCT. Interestingly, we found a significant increase in CMT 12 months after the surgical procedure. Regarding the analysis of individual layers, a significant increase occurred at the level of the NFL and ONL. In addition, we found that this increase seems to be related with three parameters: the presence of a macula off RRD, older age and the use of SF₆ gas as tamponade. Interestingly, we did not observe any correlation between the increased retinal thickness and BCVA.

The ONL showed the greater increase during the postoperative period. Since it corresponds to the photoreceptors’ nuclei, it can be assumed that a regeneration process may occur at this level. However, we didn’t investigate the atrophy process after retinal detachment. Previous studies investigated this issue comparing the eye affected by RRD with the contralateral one. Several studies showed that atrophy occurs mainly in the outer layers, including ONL, during the first 6 months after the surgical procedure.^2,5,7,8 Thus, it could be assumed that the outer retina is most affected by atrophy.^13,18 Dell'Omo et al. investigated the foveal architectural changes after successful anatomical repair of macula-off RRD.¹⁹ Authors showed a thinning of retinal layers compared to the fellow eye 1 month after the surgery. This difference disappeared at 12 months after surgery. These results are in agreement with those of the present study. However, the study from Dell’Omo and collaborators suffered from the fact that retinal thickness was evaluated manually in a non-reproducible fashion. Another study investigated photoreceptors after RRD using adaptive optics and showed a significant decrease in the density of cones from the first weeks after surgery in both macula-off and macula-on RRD.²⁰ This early alteration could explain the atrophy of the ONL layer in the immediate postoperative period as well as the alterations of the cone interdigitation zone and the ellipsoid zone. At 1-year post-operative follow-up, authors also detected an increase in cone density, that can explain the increase of CMT.

We found a greater increase in CMT in patients with macula-off RRD. Previous studies reported an initial thinning in CMT only in this subset of patients.¹⁹ This finding may help explain our finding since it could be assumed that only patients presenting with initial retinal atrophy subsequently show healing and thus an increase in CMT. On the contrary, those who present a macula-on RDD do not show any alteration of the central retina which is therefore not subject to changes in the postoperative period.¹⁹

We also found a significantly increase of CMT in older patients. To the best of our knowledge, this is the first time that this finding is described. It could be assumed that this more fragile subset of patients presents a greater thinning in the immediate postoperative period, with a subsequent greater increase. However, further studies are needed to investigate this issue.

Interestingly, the use of SF₆ was associated with a greater increase in CMT compared with C₂F₆. To the best of our knowledge there is the first study comparing changes of retinal layers according to the type of gas used as tamponade agent. Inan et al compared gas with silicone oil tamponade and found a greater thinning of the outer layers in the silicone group 12 months after the surgical procedure. However, authors didn’t distinguish between the different gases used.¹⁸

It can be assumed that the mechanical compression exerted by these tamponades leads to some degree of retinal ischemia. C₂F₆ has a longer persistence time than SF₆ and it is possible that this leads to a more important retinal damage which would explain the lower recovery of the photoreceptors. This finding represents the only modifiable factor found in the present study and should be considered in the choice of the tamponade. The main strengths of this study are that the patients were accurately enrolled from a very large sample, the fact that the measurements were carried out in reproducible fashion and a long follow-up duration. Moreover, performing the measurements only on the affected eye, possible biases due to the lack of comparability with the other eye were avoided.

However, it has some limitations that should be taken into account. The main limit is related to relatively small sample size that could have affected the analysis of correlation between changes in retinal thickness and BCVA. In addition, we assessed visual function by BCVA only. Other studies investigating other parameters such as contrast sensitivity or visual field would be interesting to understand if the retinal changes, we observed have an impact on visual function. Finally, in our cohort, no patients had been treated with silicone oil as tamponade. It would be interesting to know if it differs from gases in postoperative retinal changes.

In conclusion, CMT significantly increases after PPV for the treatment of RRD. In particular, the ONL is the retinal layer that increases most in the postoperative period. Factors that had a positive influence on the increase in CMT are older age, macula-off status, and SF₆ tamponade compared to C₂F₆. These findings demonstrate that slow anatomical restoration occurs following RRD particularly when the macula is detached. Finally, the choice of tamponade would seem to play a key role in this process.

Study design and patients

This retrospective multicenter cohort study included patients treated for RRD at two tertiary referral centres (OphtalmoPole de Paris, Hôpital Cochin (Paris, France), Hôpital Hôtel-Dieu (Paris, France) between December 2014 and March 2023. Described research was approved by the ethics committee of the French society of ophthalmology (IRB 00008855) and adhered to the tenets of the declaration of Helsinki. Informed consent was obtained from all subjects included in the study. Consecutive patients that underwent uneventful PPV for primary RRD were screened for enrolment. We included patients, both phakic and pseudophakic, that presented RRD due to single or multiple retinal breaks without significant lens opacification, in order to have an OCT signal good enough to do a retinal segmentation. Eyes that underwent PPV were included as the study eyes. Exclusion criteria were recurrence of RRD, presence of tractional or post-traumatic RRD, presence of diabetic retinopathy, history of uveitis, glaucoma, functional amblyopia and any pre-existing macular pathology. In addition, eyes that presented retinal alterations such as epiretinal membrane, macular oedema and/or macular hole during the follow-up were excluded from the study. Finally, only patients with at least one interpretable OCT 1 and 12 months after the surgical procedure were included.

The following data were extrapolated from medical records: age, sex, preoperative status of the retina (location and characteristics of retinal breaks, presence of peripheral retinal degenerations, presence of vitreous haemorrhage, presence of proliferative vitreoretinopathy), intraocular pressure, lens status, preoperative and postoperative BCVA in logMAR, preoperative and postoperative fundus examination and spectral domain OCT scan.

Surgical procedure

The procedures were performed under general or loco-regional anaesthesia. Three-port 25 or 23 gauge PPV was performed using the Alcon Constellation system (Alcon Laboratories, Inc, Forth Worth, TX) or Stellaris Elite System (Bausch & Lomb, St. Louis, MO, USA) and a contact wide-angle viewing lens (Mini Quad; Volk Optical, Mentor, OH, USA). After central and peripheral vitreous removal, all eyes underwent 360° scleral indentation to shave the vitreous base up to the ora serrata, followed by the removal of vitreous tractions from retinal tears. The choice of using perfluorocarbon liquid (PFCL) as well as the method of retinopexy (cryotherapy or endolaser photocoagulation), the tamponade agent (SF6, C2F6, C3F8, or silicone) and the necessity of suturing the sclerotomies varied according to surgeon's preference. Hypotonizing and corticosteroids eye drops were prescribed after surgery to all patients and were discontinued after one month. Post-operative follow-up included a visit the day after surgery, at one week, 1, 3, 6 and 12 months after surgery.

Image analysis

The SD-OCT images were obtained by Spectralis HRA-OCT (Heidelberg Engineering, Heidelberg, Germany). They were performed by acquiring 49 B-scans in a 20 x 20° area centred on the fovea. Retinal layers thickness was calculated in the central field as defined by the Early Treatment Diabetic Retinopathy Study (1 mm). The integrated analysis software was used to perform automatic OCT segmentation of retinal layer boundaries and thickness measurement: SD-OCT Fast Macular Thickness program (Segmentation Editor; Heidelberg Eye Explorer Spectralis Software Version: 1.9.10.0). A manual error correction was performed if needed. Six different retinal layers were identified by the algorithm: (1) total retinal thickness (CMT); (2) retinal nerve fiber layer (RNFL); (3) ganglion cell layer-inner plexiform layer complex (GCL-IPL); (4) inner nuclear layer-outer plexiform layer complex (INL-OPL); (5) outer nuclear layer (ONL); (6) ellipsoid zone–retinal pigment epithelium complex (EZ-RPE). The inner and outer retinal layers were defined as the distance from the internal limiting membrane to the outer border of the inner nuclear layer and the distance from the inner border of the outer plexiform layer to the RPE, respectively.

Statistical analysis

The R studio software, version 3.6.2 (http://www.r-project.org) was used for data analysis. Values are expressed as mean ± standard deviation for numerical variables, and as percentages for categorical variables. The Shapiro-Wilk test was used to determine normality of data. A paired sample t-test was used to compare normally distributed variables between, while Mann-Whitney U test was used for not normally distributed variables. The ANCOVA test was used to investigate possible the possible effect of demographic, surgical and clinical characteristics on changes in retinal layers thickness. The correlations between thickness of the different retinal layers and postoperative BCVA was evaluated in pseudophakic patients using Pearson correlation analysis. A P value < 0.05 was considered statistically significant.

Acknowledgments

None.

Author contributions

Conceptualization : BJ, FB, PRR ; Data Curation : BJ, FB, FF ; Formal Analysis : FA, AV, EP ; Investigation : BJ, FB, PRR ; Methodology : BJ, FB, PRR, FF, GG ; Supervision : PRR, FB ; Validation : PRR, FB ; Writing – Original Draft Preparation : BJ, FB, PRR, FF, EP, AV ; Writing – Review & Editing : BJ, FB, PRR, FF, EP, AV, FA, GG.

Data availability statement

The data that support the findings of this study are available from the corresponding author, [F.B.], upon reasonable request.

Competing Interests Statement

The authors declare no competing interests.

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	Table 1. Demographic and surgical characteristics of patients treated for rhegmatogenous retinal detachment.
			N (%)
	Age		63 ± 11.6
	Sex
	Female		13 (41.9%)
	Male		18 (58.1%)
	Macula status
	On		11 (35.5%)
	Off		20 (64.5%)
	Lens status
Phakic		15 (48.4%)
Pseudophakic		16 (51.6%)
	Tamponade
	SF6		9 (29%)
	C2F6		22 (71%)
	Retinopexy
	Cryopexy		14 (45.2%)
	Endolaser		17 (54.8%)
	Use of PFCL		15 (48.4%)

Table 2. Foveal retinal thickness measured at month 1 and 12 after RRD surgery
Layer (μm)	M 1 (Mean ± SD)	M 12 (Mean ± SD)	P
CMT	270.6 ± 34.2	288.0 ± 29.7	< 0.001
NFL	13.3 ± 2.2	14.0 ± 2.5	0.03
GCL	17.5 ± 6.4	18.5 ± 6.3	0.1
IPL	22.3 ± 4.5	22.8 ± 4.3	0.3
INL	25.6 ± 7.8	26.0 ± 6.6	0.8
OPL	28.5 ± 8.1	31.1 ± 10.0	0.1
ONL	79.5 ± 23.3	92.9 ±16.5	< 0.001
RPE	14.8 ± 3.0	14.9 ± 1.8	0.8
CMT Central Macular Thickness, NFL Nerve Fiber Layer, GCL Ganglion Cell Layer, IPL Inner Plexiform Layer, INL Inner Nuclear Layer, OPL Outer Plexiform Layer, ONL Outer Nuclear Layer, RPE Retinal Pigment Epithelium. Significant P values (<0.05) are in bold.

Table 3. Effect of demographical, clinical and surgical parameters and the increase of the ONL
Parameters	Correlation Coefficient	Standard Error	P	Confidence Interval
Parameters	Correlation Coefficient	Standard Error	P	Lower Limit	Upper Limit
Age	0.5	0.1	0.001	0.2	0.8
Macula Status (On / Off)	0.5	0.1	0.001	0.2	0.7
Use of PFCL (Yes / No)	-0.2	0.2	0.2	-0.5	0.1
Type of Retinopexy (Cryopexy / Endolaser)	-0.2	0.2	0.1	-0.6	0.1
Tamponade (C2F6/SF6)	-0.4	0.1	0.01	-0.7	-0.1
Sex (Male / Female)	0.3	0.1	0.1	0.0	0.5
Statin Therapy (Yes / No)	0.0	0.2	0.8	-0.3	0.4
Significant P values (<0.05) are in bold.

No competing interests reported.

Changes in retinal layers after pars plana vitrectomy for rhegmatogenous retinal detachment

Status:

Version 1

Abstract

Introduction

Results

Discussion

Methods

Study design and patients

Surgical procedure

Image analysis

Statistical analysis

Declarations

References

Tables

Additional Declarations

Status:

Version 1