OCT Biomarkers Related to Subthreshold Micropulse Laser Treatment Effect in Central Serous Chorioretinopathy

doi:10.21203/rs.3.rs-1513893/v1

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OCT Biomarkers Related to Subthreshold Micropulse Laser Treatment Effect in Central Serous Chorioretinopathy

https://doi.org/10.21203/rs.3.rs-1513893/v1

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Background: To identify the OCT biomarkers related to the anatomical outcomes in eyes with central serous chorioretinopathy (CSCR) after subthreshold micropulse laser (SML) treatment.

Methods: Patients with CSCR underwent SML were enrolled in this retrospective study. Only patients who underwent enhanced depth imaging optical coherence tomography (EDI-OCT) examination before and after SML were selected. Patients were divided into two groups based on whether subretinal fluid (SRF) absorbed or not after SML. Group 1 was the SRF resolved group, and Group 2 was the SRF non-resolved group. Factors including age and gender, duration of symptoms, CSCR history, the height of SRF at baseline, retinal pigment epithelium (RPE) /inner choroid alterations, as well as subfoveal choroidal thickness (SFCT) of the affected eye and the fellow eye before and after SML were recorded and compared between two groups. Longitudinal change of SFCT of a subgroup of patients were analyzed.

Results: A total of 58 eyes of 58 patients were involved in this study. SRF of 31 eyes got completely absorbed, and SRF of 27 eyes was retained after SML. Logistic regression analysis revealed baseline SFCT of the affected eye (OR=1.007, 95% CI: 1.001-1.012, P=0.019) and RPE/inner choroid alterations (OR=25.229, 95% CI: 2.890-220.281, P=0.004) were correlated with SML efficacy. Thirty-three eyes of 33 patients were enrolled in the subgroup analysis. A significant difference of SFCT changes between two groups were demonstrated (P=0.001). The difference of SFCT between baseline and three months after SML was also related to SRF resolution (OR=0.952, 95% CI: 0.915-0.990, P=0.014).

Conclusion: Baseline SFCT, change of SFCT after treatment, and RPE/inner choroid alterations were the OCT biomarkers related to SRF resolution after SML treatment.

subthreshold micropulse laser

central serous chorioretinopathy

OCT biomarkers

choroidal thickness

RPE/inner choroidal alterations

Central serous chorioretinopathy (CSCR) is one of the leading causes of vision problems in the middle-aged population, characterized by subretinal fluid (SRF) with or without pigment epithelial detachment (PED)(1). Although most acute CSCR is self-limited with a recurrence rate of 30–50%, about 15%~20% of acute CSCR converted to chronic type(2–4), characterized by persistent SRF and retina pigment epithelium (RPE) atrophy, leading to permanent damage of photoreceptors. Treatment is recommended for chronic or recurrent CSCR, including photodynamic therapy (PDT), focal laser photocoagulation of leakage point on fluorescein fundus angiography (FFA) images, subthreshold micropulse laser (SML), oral diuretics, and systemic or local carbohydrase inhibitors(5). Anti-vascular endothelial growth factor should be considered when secondary choroidal neovascularization (CNV) is developed(6, 7). Among these treatment options, SML is the only one that does not cause functional damage or structural damage or side effects(8). Considering the self-limiting nature of acute CSCR, the current standard care for it is observation. However, as many studies indicated, even short period fluid accumulation in the subretinal space may cause a certain amount of damage to photoreceptors(9, 10). In order to save photoreceptors from SRF damage, SML was chose to treat the acute CSCR by some clinicians based on its the safety nature. Compared with observation, acute CSCR treated with SML had better visual acuity and higher contrast sensitivity, and less risk of recurrence and progression into chronic version(11).

It is thought SML targets retinal pigment epithelium (RPE) and stimulates functional RPE to drain SRF into choroidal circulation(8). One recent study showed the efficacy of SML is related to RPE function(12): SML is effective for restoring macular anatomy and visual sensitivity in CSCR cases with mild or moderate RPE defects; in contrast, it has only a minimal outcome in CSCR eyes with severe RPE defects. Moreover, previous studies have shown that older age, higher choroidal thickness, and inner choroid attenuation are related to CSCR duration and visual recovery(13–15). However, it is not clear whether these factors are related to anatomic outcomes after SML in CSCR.

The purpose of this study is investigating the optical coherence tomography (OCT) biomarkers related to SML efficacy in CSCR, with particular attention to choroid thickness, RPE alterations and inner choroid attenuation.

Patients diagnosed with CSCR from November 2020 to January 2022 were enrolled in a retrospective study at Eye Center, Second Affiliated Hospital of Zhejiang University. The Institutional Review Board of the Second Affiliated Hospital of Zhejiang University approved the study. The study was performed in accordance with the tenets of the Declaration of Helsinki and compliant with the Health Insurance Portability and Accountability Act of 1996. The need for written informed consent was waived by the Second Affiliated Hospital of Zhejiang University because of the retrospective design and the use of de-identified patient data.

Patients of CSCR, either acute or chronic CSCR, who underwent SML treatment were selected. All patients underwent FFA and OCT angiography (OCTA, OptovueRTVue XR 100; AVANTI, Inc) examination to rule out the presence of CNV. The SML treatment was performed by a single doctor (PPY) with a 577nm micropulse laser mode (Quantel Medical). The laser parameter was set to a 5% duty cycle. The spot size was 160µm. A nine-spot matrix with non-spacing between two spots was chosen. On the micropulse mode, the threshold power was titrated at the arch area. SML was performed on the macular area with SRF. The total laser burns were between 150 and 200.

Macular OCT images (Spectralis OCT, Heidelberg Engineering, Inc., Heidelberg, Germany) obtained under enhanced depth imaging (EDI) mode before and after SML treatment were collected. The exclusion criteria include previous retinal surgery history, ocular trauma, presence of CNV, coexistence of other retinal disorders such as pathologic myopia, and inability to obtain EDI-OCT images due to media opacity or significant eye movements.

Patients were categorized into two groups based on whether SRF was completely absorbed or not after SML. Group 1 is the SRF resolved group, and Group 2 is the SRF non-resolved group. The patients with EDI-OCT images taken at both one month and three months after SML treatment were enrolled in a subgroup analysis for investigating the longitudinal change of SFCT after SML.

Subfoveal choroidal thickness (SFCT) and the height of SRF were measured by FZ using the build-in software of the instrument. If the choroidal-scleral boundary is ambiguous on the OCT images, the case is ruled out from the final analysis. The presence of RPE hyper-transmission defects, irregular PED, and/or inner choroid attenuation on OCT images were defined as RPE/inner choroid alterations (as shown in Fig. 1). The RPE/inner choroid alterations on baseline OCT images were evaluated by two independent graders (FZ and JLH). They were blinded to the grouping. After completing grading, the graders discussed disagreements and produced a consensus. The disagreement was adjudicated by a senior grader (PPY). Demographic information like age and gender, duration of symptoms, and CSCR history was recorded.

All data were described as mean±SD. Chi-square test was used to analyze descriptive data. The continuous data was analyzed by an independent-sample T-test. The means of SFCT measured in different visits were compared with repeated measures analysis of variance (ANOVA). The factors related to the efficacy of SML were analyzed by the logistic regression model. The P value less than 0.05 was recognized as statistically significant. Statistical analysis was performed with IBM SPSS Statistics for Windows, Version 26.0 (IBM Corporation, Armonk, NY, USA).

A total of 58 eyes of 58 patients (47 male) with a mean age of 47.72±8.53 years old were involved in this study. SRF of 31 eyes (53.45%) reached completely absorbed after SML (Group 1), and SRF of 27 eyes (46.55%) was retained after SML (Group 2). There was no difference in age, gender, CSCR history, and patients who got focal laser coagulation performed between the two groups. Compared with Group 1, eyes in Group 2 had thicker SFCT both in the affected eyes (511.81±135.79 vs. 405.97±112.24, P = 0.196) and in the fellow eyes (395.15±115.21 vs. 372.82±116.68, P = 0.888); patients in Group 2 also presented with higher baseline SRF (212.96±124.42 vs. 187.84±121.95, P = 0.942). In Group 2, only one subject was graded as having no RPE/inner choroidal alterations. Statistic differences were found in the duration of symptoms and percentage of patients having RPE/inner choroid alterations between the two groups (Table 1). Logistic regression analysis revealed baseline SFCT of the affected eye (OR = 1.007, 95% CI: 1.001–1.012, P = 0.019) and RPE/inner choroid alterations (OR = 25.229, 95% CI: 2.890-220.281, P = 0.004) were correlated with the resolution of SRF. Other factors including age (OR = 1.051, 95% CI: 0.985–1.121, P = 0.131), gender (OR = 1.056, 95% CI: 0.283–3.945, P = 0.935), duration of symptoms (OR = 1.373, 95% CI: 0.965–1.952, P = 0.078), CSCR history (OR = 2.162, 95% CI: 0.779–6.659, P = 0.134), the height of SRF (OR = 1.002, 95% CI: 0.991–1.006, P = 0.435), and SFCT of the fellow eye (OR = 1.002, 95% CI: 0.997–1.007, P = 0.507) were not predictive factors of SML efficacy.

Table 1

Baseline characteristics of CSCR patients.
	Group 1	Group 2	P value
Age (years)	46.13±8.91	49.56±7.82	0.538
Female/Total	6/31	5/27	0.953
Duration of symptoms (months)	2.42±1.36	4.04±3.85	0.026
With CSCR history/Total	10/31	14/27	0.131
SRF height (µm)	187.84±121.95	212.96±124.42	0.942
SFCT of the diseased eyes (µm)	405.97±112.24	511.81±135.79	0.196
SFCT of the fellow eyes(µm)	372.82±116.68	395.15±115.21	0.888
RPE and inner choroid alterations/Total	15/31	26/27	0.000

Thirty-three eyes of 33 patients with two post-SML EDI-OCT taken were enrolled in the subgroup analysis. In Group 1, the mean SFCT measurements of baseline, one month after SML and three months after SML were 394.06±126.92µm, 363.50±128.58µm, and 347.81±114.70µm, respectively; in Group 2, mean SFCT measurements remained stable with slightly increased at three months after SML (503.53±138.14µm, 501.71±133.01µm, 516.88 ±142.25µm) (Fig. 2). ANOVA demonstrated a significant difference in SFCT changes between the two groups (P = 0.001). The difference between baseline SFCT and 3-month SFCT was also correlated to anatomic outcomes after SML (OR = 0.952, 95% CI: 0.915–0.990, P = 0.014).

This study showed a 53% resolution rate of SRF after SML in CSCR patients. Baseline SFCT of the affected eye and the presence of RPE/inner choroid alterations were the OCT biomarkers related to SML efficacy. The decline of mean SFCT after SML was only noticed in Group 1. By comparison, mean SFCT of Group 2 got slightly increased. The change of SFCT after SML was also identified as a factor influencing the anatomic outcomes of SML in CSCR in the current study.

Unlike traditional laser photocoagulation, SML avoids scarring of RPE and retina by diffusing the heat to surrounding tissue. SML can stimulate SRF absorption by inducing reactions in RPE chromophores, including the possible production of heat shock protein(16). SML has been shown to be effective in both acute and chronic CSCR. Superior visual rehabilitation was noted in SML-treated patients compared to observation in terms of BCVA, contrast sensitivity, and metamorphopsia in acute CSCR(11). Arsan et al. demonstrated SML could significantly increase BCVA and decrease SRF in non-resolving CSCR patients(17). Prasuhn et al. showed decreased central retinal thickness after SML in CSCR patients with persistent SRF either with or without secondary CNV(18). However, compared with half-dose PDT, SML has a lower SRF complete resolution rate(19). The PLACE trial, a multicenter prospective randomized clinical trial designed for chronic CSCR, showed 29% of patients with complete SRF resolution in the SML group and 67% of patients with complete SRF resolution in the half-dose PDT group at 7–8 months after the first treatment(19). In our study, the resolution rate of SRF is 53% after a single SML, which is higher than PLACT trial. The reason might be both acute and chronic CSCR were involved in this study. And Group 1 had much shorter symptoms than group 2, indicating more acute CSCR got resolved after treatment.

Both choroid and RPE contribute to the pathogenesis of CSCR (1). CSCR belongs to the pachychoroid disease spectrum(20). The choroid thickness of the affected eyes in CSCR is much thicker than the healthy eyes and the contralateral eyes(21). Increased choroid thickness indicates hyper-permeability alterations of the choroid and can be recognized as the indicator of disease activity(1, 22). Even though baseline SFCT was not significantly different between the two groups, it acted as a predictor of SRF resolution in our study. The thicker choroid of diseased eyes indicates a worse response to SML, which might be explained by the high activity of CSCR of these patients. Decreased SFCT was noticed after different treatments for CSCR(23–26). Similar alterations of choroid thickness after SML treatment were also reported by other researchers(17, 18). Compared with observation, choroidal thickness was significantly lower in the SML-treated group at eight weeks, sixteen weeks, and six months after treatment in acute CSCR(11). In our study, decreased SFCT was only noticed in the SRF-resolved group (Group 1). The decrease of SFCT may indicate less activity of the disease and improvement of choroidal hyperpermeability after SML treatment. In Group 2, no decrease of SFCT was observed at one month or three months after SML treatment, indicating the prolonged high permeability of choroid, which might be the reason for the persistence of SRF in these eyes. Our findings enhanced the importance of choroid in the pathology and prognosis of CSCR.

Diffuse RPE changes are often observed in chronic CSCR, including RPE detachment, RPE hypertrophy, and RPE atrophy(1). Diffuse RPE atrophy was described in cases of severe chronic CSC, possibly caused by long-term SRF persistent, phachychoroid vessels compression, and inner choroid ischemia(27). If the area of diffuse atrophic RPE alterations more than five disc diameters at the macula, it can be defined as severe chronic CSCR(28). Hypertransmission of RPE on OCT images indicates RPE attenuation or disruption(29). As inner choroid has a direct influence on RPE, inner choroid attenuation may cause ischemia of RPE, which may lead to RPE dysfunction eventually. Since SML was designed to target RPE, RPE and inner choroid alterations might have a certain impact on the treatment effect. This is proven by the fact that only one out of twenty-seven eyes in Group 2 was graded as having no RPE and inner choroid alterations. The presence of RPE/inner choroid alterations was also shown to be a predictive factor related to insufficient response to SML treatment.

A previous study found that age and disease duration were risk factors for persistent SRF after SML in eyes with chronic CSCR(30). But in our study, these two factors were not correlated to SML efficacy. Even symptom duration of Group 1 (2.42±1.361) was less than that of Group 2 (4.04±3.848) significantly, it is not a predictive factor for SRF resolution. The possible explanation is that both acute and chronic CSCR were involved in this study. The rate of acute CSCR in group 1 was higher than that in group2. However, when taking other factors into account, it became less important.

One limitation of this study is that many subjects only had one visit after receiving SML. So only 33 eyes got two EDI-OCT taken after SML and these eyes were selected in the subgroup analysis for investigating longitudinal SFCT change after the treatment. The possible reasons for loss of follow-up include a lack of desire for further treatment after vision rehabilitation and phased lockdown during the pandemic of COVID-19 increased the difficulty of arranging follow-ups. Another limitation of this study is using a single OCT image for choroidal thickness measurement. However, a study has demonstrated that no significant difference between SFCT and the mean of choroidal thickness in the central millimeter of cube scans by using swept-source OCT(31). We have to clarify that the change of choroid we measured in the current study is limited to the central macular region. Whether the change of choroid thickness in a larger area influents treatment effect of SML still needs further investigation.

SML is effective for certain CSCR patients. Thicker baseline SFCT of the affected eye and the presence of RPE/ inner choroid alterations predict unsatisfied outcomes after SML. Failure to observe a decrease in SFCT after SML indicates the likelihood of SRF persistence.

CSCR

central serous chorioretinopathy

SML

subthreshold micropulse laser

EDI

enhanced depth imaging

OCT

optical coherence tomography

SRF

subretinal fluid

RPE

retinal pigment epithelium

SFCT

subfoveal choroidal thickness

PED

pigment epithelial detachment

PDT

photodynamic therapy

FFA

fluorescein fundus angiography

CNV

choroidal neovascularization

Ethics approval and consent to participate

The study was approved by the Institutional Review Board of the Second Affiliated Hospital of Zhejiang University and was conducted in accordance with the Declaration of Helsinki. The need for written informed consent was waived the Institutional Review Board of the Second Affiliated Hospital of Zhejiang University because of the retrospective design and the use of de-identified patient data.

Consent for publication

Not applicable.

Availability of data and materials

The datasets used and analyzed during the current study are available from the corresponding authors on reasonable request.

Competing interests

The authors declare they have no competing interest.

Funding

Research was supported by Zhejiang Natural Science Foundation Project of China (No. LY18H120001), National Natural Youth Science Foundation Project of China (No. 31500795) and Zhejiang University Foundation Project (No. 2020-518052-0054).

Authors' contributions

FZ designed the study, collected and interpreted the data, drafted the initial manuscript, and revised the manuscript. JLH collected and interpreted the data, and critical reviewed the manuscript. ZTS, YL, and YFX collected the data, and critical revised the manuscript. LL performed statistical analysis and critical revised the manuscript. PPY designed the study, supervised data collection and data interpretation, critically reviewed and revised the manuscript. All authors read and approved the final manuscript.

Acknowledgements

Not applicable.

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No competing interests reported.

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OCT Biomarkers Related to Subthreshold Micropulse Laser Treatment Effect in Central Serous Chorioretinopathy

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