Analysis of quantitative OCT and SS-OCTA metrics three months after initiation of intravitreal faricimab for treatment-recalcitrant neovascular AMD

doi:10.21203/rs.3.rs-3755858/v1

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Analysis of quantitative OCT and SS-OCTA metrics three months after initiation of intravitreal faricimab for treatment-recalcitrant neovascular AMD

https://doi.org/10.21203/rs.3.rs-3755858/v1

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Purpose

To utilize optical coherence tomography (OCT) and SS-OCT angiography (SS-OCTA) for quantifying morphological changes seen in eyes with recalcitrant neovascular age-related macular degeneration (nAMD) transitioned to intravitreal faricimab injections during the manufacturer’s recommended induction phase of treatment.

Methods

Fifty-four treatment-recalcitrant patients (60 eyes) were recruited. OCT and SS-OCTA images were obtained at 0 and 3 months. Best corrected visual acuity (BCVA), OCT, pigment epithelial detachment (PED), and macular neovascularization (MNV) parameters were analyzed at baseline and 3 months.

Results

Thirty-two patients (38 eyes) were included in baseline OCT characteristic analysis, 29 patients (35 eyes) in MNV analysis, and 18 patients (21 eyes) in PED analysis. Significant decreases in PED parameters were observed, including PED volume (mean = -19.66%, 95% CI [-36.77, -2.40], p = 0.0114), mean height (mean = -19.16%, 95% CI [-33.50, -4.81], p = 0.0114), and maximum height (mean = -15.28%, 95% CI [-25.59, -4.97], p = 0.0057). Significant decreases in MNV metrics were also observed, including area (mean = -9.06%, 95% CI [-15.45, -2.66], p = 0.0069) and vessel density (mean = -8.23%, 95% CI [-12.46, -4.01], p = 0.0004). BCVA remained stable between baseline and 3 months.

Conclusions

In recalcitrant nAMD patients who were transitioned to faricimab, patients maintained their vision while significant improvements in OCT PED and SS-OCTA MNV parameters were seen during the induction phase.

Health sciences/Diseases/Eye diseases/Retinal diseases

Health sciences/Biomarkers/Prognostic markers

Health sciences/Medical research/Biomarkers/Prognostic markers

Age-related macular degeneration (AMD) is responsible for approximately 5% of blindness worldwide. ¹ Neovascular AMD (nAMD), part of the advanced stage of this disease, is responsible for significant adverse visual outcomes. ² Most of the effective treatments for nAMD antagonize vascular endothelial growth factor (VEGF). However, up to 30% of patients fail to respond to traditional anti-VEGF agents, and such recalcitrant patients may experience persistent subretinal or intraretinal fluid despite anti-VEGF treatment. ^{3, 4}

Faricimab (Vabysmo ®; Roche/Genentech; Basel, Switzerland), a recently approved monoclonal antibody, has shown promise as a tool to control macular neovascularization (MNV) and to extend treatment intervals in patients with nAMD. Faricimab is a bispecific antibody blocking both angiopoietin 2 (Ang-2) and VEGF angiogenesis pathways. ⁵ Ang-2 is thought to be involved in vascular destabilization and inflammation, as well as in sensitizing vessels to VEGF. ⁶ It has been hypothesized that the dual mechanism of action of faricimab allows for greater decreases in vascular leakage and inflammation compared to blockade of either Ang-2 or VEGF alone. ⁵ The TRUCKEE study evaluated the effectiveness of faricimab in real-world patients, both treatment naïve and previously treated. ⁷ After the first injection of faricimab, patients showed significant improvements in best corrected visual acuity (BCVA) and significant decreases in central subfield thickness, which were even more significant after three faricimab injections. ⁷ However, the effects of faricimab had not been studied in patients who were recalcitrant to other intravitreal anti-VEGF agents until very recently. Pandit et al. described 218 eyes of 191 patients that demonstrated stable vision, decreased maximum fibrovascular pigment epithelial detachment (PED) height, decreased mean central foveal thickness, along with decreased subretinal fluid (SRF) and intraretinal fluid (IRF) in patients switched to faricimab from traditional anti-VEGF agents. ⁸ Using the IRIS Registry™, the FARETINA-AMD study investigated real-world early injection interval extension of faricimab in nAMD patients. ⁹ Nearly half of both treatment naïve and previously treated patients had stable vision and were able to be extended past a four week interval within the first four injections. ⁹

In this study, we aimed to identify baseline optical coherence tomography (OCT) features of nAMD treatment-recalcitrant eyes of patients switched to faricimab therapy, quantify early OCT, PED, and OCT angiography (OCT-A) MNV changes in such eyes, and assess changes in BCVA.

This study was a prospective observational case series of consecutive patients with recalcitrant nAMD who were transitioned to faricimab per clinician discretion. Patients were enrolled between 9/14/2022 and 2/7/2023 at our single tertiary care ophthalmology clinic. The tenets of the Declaration of Helsinki were followed, Institutional Review Board approval was obtained, and patients provided written informed consent for obtaining additional Swept-Source (SS) imaging with image data analysis during their treatment.

Recalcitrant patients were defined as patients previously treated with intravitreal anti-VEGF agents (ranibizumab, aflibercept, bevacizumab, or some combination) who were unsuccessfully extended beyond 6-week injection intervals with their previous treatment agent. These patients experienced enlarging PED, recurrent IRF or SRF if extended beyond 6 weeks, or maintained persistent SRF or IRF at 4-week injection intervals. Inclusion criteria comprised of being a recalcitrant nAMD patient consenting to the additional SS imaging and participation in this observational imaging study. Exclusion criteria consisted of any history of photodynamic therapy (PDT).

Recalcitrant nAMD patients who were initiated on a loading-dose regimen of four, monthly, intravitreal faricimab injections, as recommended by the drug manufacturer, were imaged during their treatment visits. These injections were administered at 4-to-6-week intervals based on clinical scheduling availability. OCT and SS-OCTA 3x3 mm and 6x6 mm scans (PLEX Elite 9000; Carl Zeiss Meditec Inc; Dublin, California, USA) were acquired immediately before the first and fourth intravitreal faricimab injections, defined as baseline and 3 months respectively.

Apart from one patient who received baseline imaging five days prior to their first injection, patients who received any consecutive induction-phase intravitreal injections at an interval greater than 6 weeks, or who failed to receive OCT and/or SS-OCTA scans immediately before injections, were excluded from analysis. Patients with presence of vitreous hemorrhage, MNV that was incompletely encompassed in the 6x6 mm SS-OCTA scan, or inability to obtain a high-quality OCT or SS-OCTA scan (signal strength > 6/10) at both timepoints were also excluded from analysis.

OCT features analysis

Baseline prevalence of OCT imaging features of treatment-recalcitrant eyes, including presence versus absence of IRF, SRF, PED, subretinal hyperreflective material (SHRM), hyperreflective foci (HRF), retinal pigment epithelium (RPE) tear, subretinal drusenoid deposits (SDDs), and subfoveal hyper-transmission were compiled.

Macular neovascularization (MNV) analysis

MNV was segmented on SS-OCTA en face images using the standardized “RPE-RPEfit” segmentation on the device manufacturer’s software, as prior work has found this slab to have the greatest inter-reader reproducibility for segmentation of type 1 and type 2 choroidal neovascularization (CNV). ¹⁰ Manual fine-tuning adjustments were made by two graders (AN, MD) when the MNV was not entirely encompassed by this automatic segmentation.

Baseline and 3-month 6x6 mm en face images were used for MNV analysis in FIJI ImageJ 2.9.0/1.53t Java 1.8.0_322 64 bit. ¹¹ Patients without visualized MNV on both baseline and 3-month SS-OCTA scans were excluded from the MNV analysis. Areas of MNV were manually outlined by two graders (AN, MD) at the edges of clear vascular signals to define a region of interest (ROI). If multiple regions of clearly non-contiguous MNV were seen in the image, the MNV was analyzed as a combined but discontinuous ROI with ImageJ. Dice similarity coefficients for the ROIs were calculated between graders, and the mean value was determined to statistically assess overlap of the ROIs as a measurement of inter-grader reliability.

MNV area was calculated as the area covered by the MNV ROI. MNV vessel density (VD) was calculated after image thresholding and binarization with the Huang2 method, an alternative implementation of the Huang method, a fuzzy thresholding method with a noticeable speed advantage constructed by Johannes Schindelin, as the area of the ROI covered by blood vessels divided by the total MNV area. ¹² Total vessel length (TVL) and vessel linear density (VLD; total vessel length divided by MNV area) were calculated with a custom ImageJ macro that summed the lengths of all branches of all vessel skeletons identified by the ImageJ Analyze Skeleton command using the skeletonization of the binarized image. Percent change between the two imaging timepoints was calculated for MNV area, VD, TVL, and VLD. Mean values of these metrics at baseline and 3 months were compared with two-tailed paired t-tests.

The previously described MNV and percent change metrics were also calculated for 3x3 mm scans (9 total) that completely encompassed identified regions of MNV at both baseline and 3-month imaging. All such calculated metrics were compared pairwise to the corresponding 6x6 mm scan metrics from the same eye at the same timepoint using two-tailed paired t-tests to determine if scan size influenced these SS-OCTA metrics.

Pigment epithelial detachment (PED) analysis

The device manufacturer’s prototype “Advanced RPE Analysis” software algorithm and custom code written in Python 3.10.5 (Python Software Foundation; Wilmington, Delaware, USA) were used to segment PEDs from 6x6 mm OCT scans and to calculate PED maximum height, mean height, area, and volume for each image. Patients with solely drusenoid PEDs or PEDs incompletely encompassed within a 6x6 mm image at either timepoint were excluded from the PED analysis. Percent change in PED area, volume, maximum height, and mean height were analyzed. Mean values of these metrics at baseline and 3 months were compared with two-tailed paired t-tests.

Best-corrected visual acuity (BCVA) analysis

Snellen BCVA was recorded by a trained ophthalmic technician at baseline and 3 months. Values were then converted into logarithm of the minimum angle of resolution (logMAR) in order to compare mean values. Chi-squared analysis was used to calculate the change in mean BCVA between imaging timepoints.

Statistics

All statistical comparisons were performed with GraphPad Prism 9.4.1 (Dotmatics, Boston, Massachusetts, USA) at a significance level of alpha equal to 0.05.

Baseline patient characteristics

Fifty-four patients (60 eyes) were evaluated in this study. Twenty-two eyes of 22 patients were excluded from overall analysis (12 eyes of 12 patients for having greater than 6 weeks between consecutive injections, 9 eyes of 9 patients for failure to obtain satisfactory imaging at either timepoint, and 1 eye of 1 patient for MNV that was not fully encompassed in 6x6 mm SS-OCTA imaging). Thirty-eight eyes of 32 patients met all criteria for further analysis. Baseline characteristics of analyzed patient eyes are presented in Table 1.

Baseline OCT imaging characteristics

Baseline and 3-month OCT characteristics of the 38 treatment recalcitrant analyzed eyes are presented in Table 2. At baseline imaging, 18.4% of eyes had IRF, 55.3% had SRF, 21.1% had SHRM, and 73.7% had HRF. Notably, 100% of eyes contained at least 1 PED at baseline (90% fibrovascular, 23% drusenoid, 13% serous). No statistically significant changes in prevalence were seen between baseline and 3 months.

PED metrics

Seventeen of the 38 eyes were excluded from PED analysis (15 for PEDs extending beyond an edge of the 6x6 mm SS-OCT image, and 2 for having purely drusenoid PEDs). Representative images of automatically segmented PEDs with minor manual segmentation adjustments of segmentation are presented in Fig. 1.

For the 21 eyes included in the PED analysis, statistically significant decreases were noted in percent change mean values of PED volume (-19.66%, 95% CI [-36.77, -2.40], p = 0.0114), mean height (-19.16%, 95% CI [-33.50, -4.81], p = 0.0114), and maximum height (-15.28%, 95% CI [-25.59, -4.97], p = 0.0057), with no significant difference in PED area found (p = 0.59).

MNV metrics

Three of the 38 eyes were excluded from MNV analysis due to failure to clearly visualize MNV on both initial and final SS-OCTA images. Representative automatically segmented en face images of MNV with minor manual segmentation adjustments for optimization are presented in Fig. 3.

The Dice similarity coefficient calculated for the 2 graders’ MNV segmentations was 0.88, indicating strong agreement. ¹³

Nine out of 35 MNVs were completely encapsulated by 3x3 mm SS-OCTA scans in the imaged eye. When MNV metrics derived from 6x6 mm SS-OCTA scans and their corresponding 3x3mm SS-OCTA scans were compared, mean values for area (p = 0.13 at baseline; p = 0.15 at 3 months) and VD (p = 0.06 at baseline; p = 0.33 at 3 months) were not different, while mean values for TVL (p = 0.02 at baseline; p = 0.04 at 3 months) and VLD (p = 0.004 at baseline; p = 0.014 at 3 months) were greater for 6x6 mm scans. However, when comparing the percent change in MNV parameters from baseline to 3 months, no SS-OCTA parameters (MNV area, VD, TVL, VLD) showed significant differences (p = 0.63, p = 0.06, p = 0.71, p = 0.38, respectively).

For the 35 eyes included in the MNV analysis, statistically significant decreases were noted in percent change mean values of MNV area (-9.06%, 95% CI [-15.45, -2.66], p = 0.0069) and VD (-8.23%, 95% CI [-12.46, -4.01], p = 0.0004), while no significant changes were found in TVL (p = 0.256) or VLD (p = 0.197).

BCVA results

When converting Snellen to logMAR BCVA, the mean baseline logMAR BCVA was 0.26 while mean 3-month logMAR BCVA was 0.24. Although there were significant changes to both PED and MNV metrics during the induction phase, no significant change in mean BCVA was identified (p = 0.48).

In this study, we evaluated both baseline imaging characteristics and early structural and functional changes in treatment-recalcitrant nAMD patients transitioned to faricimab. Treated eyes universally had PEDs at baseline and most had hyperreflective foci, subretinal drusenoid deposits, and subretinal fluid. Treated eyes experienced significant decreases in PED volume and height, as well as significant reductions in MNV area and vessel density while maintaining stable vision. Such changes demonstrate significant early structural and vascular responses to faricimab in recalcitrant nAMD patients, which may eventually allow for prediction of treatment response in this population.

Changes in PED metrics have previously been reported after a switch from prior-generation anti-VEGF therapies. Major Jr. et al. found a decrease in maximum PED height of 14% at 1 month and 22% at 12 months after switching from bevacizumab or ranibizumab to aflibercept. ¹⁴ Our study’s decrease in maximum PED height of 15.28% at 3 months falls in between these values and is notable to have occurred in aflibercept-resistant eyes. Kanesa-Thasan et al. found a decrease in PED volume of 19% at 18 months in bevacizumab- and ranibizumab-recalcitrant eyes switched to aflibercept, very similar in magnitude to the 19.66% decrease in PED volume we report for aflibercept-resistant eyes switched to faricimab at 3 months. ¹⁵ Of note, within this cohort we observed that as the PED height and volume both decreased, the area at the base of the lesion was shown to increase, suggesting a flattening and spreading mechanism in these treated PEDs.

Changes in OCT-A metrics of MNVs have previously been reported following administration of other anti-VEGF therapies. Forty-eight hours after aflibercept or ranibizumab injection in eyes with nAMD, choroidal neovascularization (CNV) area was found to decrease by 10.5%, and 1 month after administration of aflibercept to treatment-naïve eyes, CNV area decreased by 33.4%, mirroring our reported MNV decrease of 9.06% at 3 months in treatment-recalcitrant eyes. ^{16, 17} Prior studies reported decreased TVL after treatment with earlier anti-VEGF agents over 9.8 months, which we did not find in our study at 3 months, potentially due to differences in follow-up duration and our inclusion of only treatment-recalcitrant eyes. ¹⁸

We also investigated if OCT-A scan dimension (6x6 mm versus 3x3 mm) would alter the values calculated for MNV metrics at each timepoint, or the changes calculated for MNV metrics between timepoints. We attribute our findings that values for TVL and VLD were significantly higher when calculated from 6x6 mm OCT-A scans versus 3x3 mm scans to the effect of differences in the real dimensions of each pixel when skeletonizing images. Pixels in 3x3 mm scans had smaller real dimensions than those in 6x6 mm scans, thus vessels would contribute a greater length to 6x6-mm-measured TVL and VLD. Furthermore, the fact that the percent change in mean values in 3x3 mm SS-OCTA scans from baseline to 3 months did not vary for any MNV metrics (area, VD, VLD, and TVL) suggests that higher resolution 3x3 mm SS-OCTA scans may offer no benefit over 6x6 mm scans when evaluating changes in MNV parameters on the PlexElite 9000 SS-OCTA in our small cohort.

This study had several limitations. First, the strict inclusion criteria used to define treatment-recalcitrant patients both led to a limited number of subjects recruited for this observational study and may limit the generalizability of our results. Patients were excluded if they received any of the faricimab injections out of the 4-to-6-week window in order to preserve a true loading phase. Second, this study was conducted with a limited follow-up period. At this time, we are unable to generalize the results observed during the faricimab loading phase, and whether the noted results are sustained during extended treatment with faricimab. Further investigations examining the sustainability of such results are underway. Third, none of the patients within our recalcitrant cohort had Type 3 MNVs, preventing generalization of our study results to patients who might present with this type of lesion. Fourth, we recognize the importance of inter-eye correlation in the statistical approach. However, given our small sample size of 4 individuals with both eyes included, analyzing correlated eye data with currently recognized methods such as generalized estimating equations (GEE) does not perform well, and as such we are unable to correct for this potential source of bias.¹⁸ Finally, at this time there is not a publicly available segmentation algorithm for OCT instruments that result in flawless PED segmentation. As a result, all images that were analyzed required some manual fine-tuning adjustments to the device’s automatic segmentation. As such, minor imperfections in manual segmentation may remain present in the images that were analyzed in this study.

In conclusion, this study demonstrates that treatment-recalcitrant eyes switched to intravitreal faricimab typically have PEDs, hyperreflective foci, subretinal drusenoid deposits, and subretinal fluid at faricimab initiation. Although the prevalence of such OCT findings did not change over the loading phase, further directions include evaluation of such features after consistent long term faricimab treatment. Furthermore, patients maintain stable vision while PED and MNV OCT and SS-OCTA parameters change significantly during the loading phase of faricimab. Larger 6x6 mm SS-OCTA scans may be suitable for measuring and following changes in MNV parameters despite being lower resolution than 3x3 mm SS-OCTA scans. Future work should explore the imaging and functional changes in treatment-recalcitrant nAMD patients switched to faricimab over a longer follow-up period, and examine the effects of extending treatment intervals for faricimab beyond 4 weeks on OCT and SS-OCTA parameters.

Acknowledgements: None

Conflict of Interest: A.N., None; M.D., None; H.K.B., None; A.B., None; A.M., None; A.T.L, Research PI for REGENXBIO and Apellis; R.G.M., research support from Google Inc. No outside party had any role in study design, data collection or analysis, decision to publish, or preparation of the manuscript.

Funding: This research was funded in part by an unrestricted departmental grant from Research to Prevent Blindness. The sponsor or funding organization had no role in the design or conduct of this research.

Author Contribution Statement: study conception and design: AN, MD, AM, ATL, RGM; data collection: AN, HKB, AB; analysis and interpretation of results: AN, MD, HKB, AB, AM, ATL, RGM; draft manuscript preparation: AN, MD, HKB, ATL, RGM.

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Tables 1 and 2 are available in the Supplementary Files section.

There is conflict of interest

CohortCharacteristicsTable1.xlsx
Table 1: Baseline characteristics of eyes meeting all criteria for further analysis. The mean and standard deviation of the age of patient at first faricimab injection, time from initial treatment to initial faricimab injection, and most recent treatment interval before transition to faricimab are depicted below. The mean and range of number of injections previously received per patient, the gender distribution, and type(s) of previous intravitreal anti-VEGF treatment(s) previously used are also described.
OCTCharacteristicsTable2.xlsx
Table 2: Baseline prevalence outlining presence vs absence of optical coherence tomography (OCT) imaging features of all recalcitrant eyes treated with faricimab that met criteria for analysis.

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You are reading this latest preprint version

Analysis of quantitative OCT and SS-OCTA metrics three months after initiation of intravitreal faricimab for treatment-recalcitrant neovascular AMD

Status:

Version 1

Abstract

Purpose

Methods

Results

Conclusions

Figures

Introduction

Methods

OCT features analysis

Macular neovascularization (MNV) analysis

Pigment epithelial detachment (PED) analysis

Best-corrected visual acuity (BCVA) analysis

Statistics

Results

Baseline patient characteristics

Baseline OCT imaging characteristics

PED metrics

MNV metrics

BCVA results

Discussion

Declarations

References

Tables

Additional Declarations

Supplementary Files

Status:

Version 1