Retinal Vessel Density and Visual Field Changes and Their Correlation Following the Deep Sclerotomy in Primary Open-angle Glaucoma

doi:10.21203/rs.3.rs-3331568/v1

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Retinal Vessel Density and Visual Field Changes and Their Correlation Following the Deep Sclerotomy in Primary Open-angle Glaucoma

https://doi.org/10.21203/rs.3.rs-3331568/v1

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Purpose

To explore any role of the Mitomycin-augmented Non-penetrating Deep Sclerotomy (NPDS) procedure on the retinal microvasculature and visual field and their correlation in POAG eyes.

Methods

22 POAG eyes of 22 patients without previous surgical interventions for glaucoma, whose disease was progressing and/or the intraocular pressure was not at the target level with full topical medication, were allocated to this prospective interventional study. All the patients underwent the non-penetrating deep sclerotomy procedure and followed up for a month. The IOP, Humphery Visual Field (HVF) 30 − 2, RNFL, and the vessel density (VD) of the optic nerve head and macula (by OCTA) were evaluated one day before the surgery and one month after the NPDS procedure.

Results

At the one-month post-op follow-up, the IOP was significantly decreased compared to the pre-op visit (8mmHg vs. 23.5mmHg, p: <0.001). The visual field MD significantly improved one month after the NPDS procedure (-13.06dB vs. -15.44dB, p:0.038), although the PSD did not indicate any significant change. Neither the peripapillary nor the macular VD significantly changed during the study. However, the MD was significantly and positively correlated to the whole image, peripapillary, perifoveal, and parafoveal VD.

Conclusion

The deep sclerotomy procedure is a compelling choice of POAG treatment, which could significantly decrease the IOP and improve the visual field. However, this procedure may not alter the retinal microvasculature in a short period. Nevertheless, the positive correlation between retinal VD and the visual field MD proposes a possible vascular mechanism for the visual field defect in glaucomatous eyes.

POAG

NPDS

OCTA

Vascular Density

Glaucoma

Deep Sclerotomy

Glaucoma is the leading cause of irreversible blindness worldwide, affecting about 79.6 million people in 2020 [1]. Vast varieties of disease with a joint presentation of progressive optic neuropathy mainly due to high intraocular pressure (IOP) described as glaucoma [2]. In addition to medical therapy, various surgery methods such as Trabeculectomy, Deep sclerotomy, and glaucoma valve placement have been introduced and applied for more severe cases [3]

Functional and structural imaging methods are essential in evaluating and following glaucoma patients. Optical Coherence Topography (OCT) and Optical Coherence Tomography Angiography (OCTA) are two novel non-invasive imaging methods to assess the structure of retinal layers and retinal vasculature, respectively [4]. Various studies have demonstrated decreased retinal vasculature density according to glaucoma severity, although the results were not homogenous [5]. It has also been declared that in normal tension glaucoma (NTG), in the absence of significant changes in the retinal nerve fiber layer (RNFL), the peripapillary vessel density (VD) could be declined [6]. These findings confirm the 'vascular concept' of glaucoma pathogenesis, a non-mechanical physiopathology, due to ocular circulation dysregulation and ischemia [7].

The parafoveal deep VD has been negatively correlated with the IOP reduction following an anti-glaucoma medication in a 6-month follow-up [8]. However, another study on the effect of laser trabeculoplasty on the retinal vasculature declared a non-significant change in the macular and peripapillary VD in 6-month post-op follow-up [9]. In contrast, a study on trabeculectomy cases showed a significant increase in optic disk VD in the 6-month post-op visits; however, the VD difference was insignificant in the 1-month follow-up [10]. A prospective study on the effect of deep sclerotomy surgery on the macular and peripapillary structure and vasculature would be valuable in determining the differences between various glaucoma surgeries on retinal structure and circulation.

This prospective study evaluates the macular and peripapillary structure and vasculature of open-angle glaucoma (OAG) cases before and after the Mitomycin-augmented Non-penetrating Deep Sclerotomy to discover the retinal changes following the surgery.

It is a prospective study on Primary Open Angle Glaucoma (POAG) patients at the Nikookari Ophthalmology Center in Tabriz, Iran. Twenty-two patients with the Mitomycin-augmented Non-Penetrating Deep Sclerotomy plan to control their disease progression or lower the IOP were randomly included in the study after getting informed consent and meeting the exclusion and inclusion criteria. One eye of each patient was included in the study. The detailed inclusion and exclusion criteria of the study are mentioned below. All the patients were allocated to the study from March 2021 to March 2022.

Inclusion criteria:

Spherical refractive error less than five diopters and Astigmatism less than three diopters
Open Angle in static gonioscopy
The presence of glaucomatous changes in the Optic disk, such as Neuroretinal rim narrowing or notching or RNFL defect
The presence of visual field defect in a reliable perimetry test

Exclusion Criteria:

Reluctance to continue taking part in the study
Advanced stages of glaucoma
Retinal pathologies affecting the vision, such as diabetic or hypertensive retinopathy.
Significant cataract
History of ocular trauma
History of uveitis
History of past ocular surgery except for the uncomplicated cataract surgery

All the patients underwent ophthalmic examination to determine their IOP (by Goldmann applanation tonometry) before, one day, and one month after the deep sclerotomy surgery. The baseline best corrected visual acuity (BCVA) and cup-to-disk ratio (C/D ratio) were assessed at the primary visit. The Visual field and the retinal vascular density were evaluated through the pre-op and 1-month post-op visits.

The study has been ethically approved by the Research Ethics Committee of the Tabriz University of Medical Sciences with the approval code of IR.TBZMED.REC.1399.384.

Surgical Technique

A single glaucoma surgeon operated on all the patients under general anesthesia. After placing a corneal traction suture with 7/0 silk, the conjunctival fornix-based dissection was done in the superior region of the globe. The superficial scleral flap (rectangular 5*5mm), which represents one-third of the scleral thickness, was next dissected by a blade after Mitomycin C (0.2 mg/ml) saturated sponges had been applied to the sclera for 2 minutes. The deep scleral flap was dissected and excised with an approximate size of 3.5*3.5mm. The Schlemm's canal was unroofed under the deep scleral flap, and the juxtacanalicular trabecular meshwork was peeled. The superficial scleral flap was repositioned and sutured with three 10.0 Naylon, and the conjunctiva was sutured with 10/0 Naylon to the clear cornea.

All the patients stopped using the anti-glaucoma medication immediately after the deep sclerotomy procedure. Patients received Ofloxacin eye drop Q6h for one week, and Betamethasone eye drop Q2h tapered and discontinued through 4 weeks for the operated eye.

Imagings

Patients underwent a 30-2 perimetry by Humphrey Field Analyzer (HFA: Carl Zeiss Meditec, Dublin, CA, USA) at the pre-op and post-op (after one month) visits to determine the Mean Deviation (MD) and Pattern Standard Deviation (PSD) of patients' visual fields. The results with a fixation loss rate higher than 20% and a false negative or false positive rate higher than 15% were considered unreliable; the patients were asked to retry the perimetry.

The AngioVue™ Imaging System (RTVue XR Avanti, Optovue Inc., Fremont, CA, USA) was utilized to obtain the macular and optic disk OCTA before and one month after the surgical procedure. The HD 4.5*4.5 mm program evaluated the peripapillary (1.0 mm wide annulus around the optic nerve head) VD and RNFL thickness. In addition, the HD 6.0*6.0 program helped to evaluate the macular vascular density. The central circle with a 1.0 mm diameter was automatically considered the fovea, and a round annulus with a 2.0 mm width was considered the parafovea region. The 3.0 mm wide round annulus around the parafoveal region was considered the perifoveal region. The system automatically evaluated the vascular density of superficial and deep capillary plexuses, but the mean of these two values was considered the target variable. The OCTA images with a quality score lower than 6/10 or with motion and blinking artifacts were repeated to achieve the appropriate results.

The Alcon OcuScan RxP Ophthalmic Ultrasound System (Alcon Laboratories (U.K.) Ltd) was used to assess the central corneal thickness of patients before the surgery.

Statistical analysis

The statistical analysis of the data was done by IBM SPSS Statistics 25.0. The normally distributed quantitative data were compared using paired student's t-test, and the Wilcoxon and Friedman's two-way tests were utilized for nonparametric data. Spearman and Pearson correlation coefficients were used to study the correlations. Tableau Desktop 2019.4 software was utilized to depict the statistical results.

Ophthalmic examinations and IOP

A total number of 22 eyes of 22 male patients with a mean age of 66.9 (95%CI:61.7-72) were evaluated in the study. The mean baseline IOP of target eyes with full topical medication (Timolol Q12h, Dorzolamide Q12h, Latanoprost Q24h, and Brimonidine Q8h) was 24.8 mmHg (95%CI:22.2-27.4), and the mean central corneal thickness (CCT) was 540.2µm (95%CI:529.5-550.9). The median BCVA of patients in the LogMAR scale was 0.32 (Interquartile range (IQR): 0.23-0.33), and the mean refractive error of patients reported as the spherical equivalence was -1.75 diopters (95%CI: minus (1.12-2.37)). The median C/D ratio was 0.75 (IQR: 0.50-080).

The median IOP of the study eyes was significantly lower compared to the baseline one day and one month after deep sclerotomy surgery (p: <0.001, 8mmHg (IQR:6.75-9) and 8mmHg (IQR:6.75-9.25) respectively). Figure 1 depicts the IOP through the timeline.

Visual field

The pre and post-operation data of Mean Deviation (MD) and Pattern Standard Deviation (PSD) were compared to evaluate the effect of deep sclerotomy on the visual field of patients. The MD was significantly improved after the surgery (p:0.038, -13.06 dB, 95%CI: -(9.61-16.50) compared to -15.44 dB, 95%CI: –(11.20-19.68)), but the PSD has no significant difference compared to the baseline (p:0.865, 7.75 dB, 95%CI: 6.35-9.14 compared to 7.64 dB 95%CI:6.37-8.92). Figure 2 visualizes the comparison of pre-op and post-op visual field indices.

The Pearson correlation coefficient was used to evaluate the correlation between the MD changes and IOP decrease after the deep sclerotomy. The results showed no significant correlation (p:0.422, Pearson Correlation:-0.180).

Peripapillary and Macular Vessel density

The comparison of peripapillary vascular density before and after the surgery showed no significant difference (33.2%, IQR:29.4-39.0 v.s 32.2%, IQR:28.7-40.7 respectively, p:0.329). Detailed data on vascular density in peripapillary OCTA is demonstrated in the Appendix.1 (Supplementary materials).

The Perifoveal (Pre-Op: 37.5%, CI_95%:35.2-39.8 v.s Post-op: 35.6%, CI_95%:32.5-38.7, p:0.125) and Parafoveal (Pre-Op: 40.9%, CI_95%:38.7-43.1 v.s Post-op: 39.0%, CI_95%:35.5-42.5, p:0.250) vascular density was not significantly changed after the surgery. Detailed data on macular OCTA is available in the Appendix.2 (Supplementary materials).

The Spearman correlation coefficient was used to evaluate the correlation of macular and peripapillary vascular density to the MD of the visual field before and after the surgery. At the baseline, only parafoveal and perifoveal VD were significantly correlated with the MD (Correlation coefficient(CC):0.452, p:0.035 and CC:0528, p:0.011, respectively). However, in addition to those two indices, the Whole image and peripapillary VD were significantly correlated to the MD at the follow-up visit. Table 1 shows the more detailed results of the Spearman test. The results show that the lower the vascular density, the worse the mean deviation. So, the damage to the retinal microvascular structure could deteriorate the visual field. The post-op correlation of the optic nerve head and macular VD to the MD could be contemplated in Figure 3.

Table 1 The peripapillary and macular vascular density correlation to the mean deviation of the visual field before and after deep sclerotomy (MD: Mean Deviation)

			Whole Image	Inside Disk	Peripapillary	Foveal	Parafoveal	Perifoveal
MD	Pre-Op	p-value	0.530	0.098	0.375	0.126	0.035	0.011
	Pre-Op	Correlation Coefficient	0.141	0.362	0.199	0.336	0.452	0.528
	Post-Op	p-value	0.001	0.761	0.004	0.776	0.043	0.036
	Post-Op	Correlation Coefficient	0.657	0.069	0.595	0.064	0.435	0.450

To better understand the correlation between the various VD indices and MD, the amount of alteration in VD indices after the surgery was compared to the MD changes in each case. The more detailed results of the mentioned correlation test are demonstrated in Table 2. As declared in the table, the value of MD change was only significantly correlated with the amount of the whole image VD change after the surgery (CC:0.438, p:0.041).

Table 2 The correlation of changes in vascular density and mean deviation after deep sclerotomy. (ΔMD: Changes in Mean Deviation)

VD change		Whole Image	Inside Disk	Peripapillary	Foveal	Parafoveal	Perifoveal
ΔMD	p-value	0.041	0.847	0.444	0.245	0.627	0.994
ΔMD	Correlation Coefficient	0.438	0.044	-0.172	-0.259	0.110	-0.002

Retinal nerve fiber layer

The post-op RNFL thickness and internal limiting membrane (ILM) to retinal pigmented epithelium (RPE) thickness of various regions have been compared to the baseline. As demonstrated in Table 3, the RNFL thickness decrease in Peripapillary (5.5 µm (8.7%), p:0.038), superior hemisphere (3 µm (4.7%), p:0.033), inferior hemisphere (3.2 µm (5.6%), p:0.009), and Nasal-Inferior (8.7 µm (12.9%), p:0.009) is statistically significant after surgery. The Most change has happened in the Nasal-Inferior sector; however, there was no correlated change in the visual field.

Besides, the ILM-RPE thickness has decreased after surgery in the fovea (4.5 µm (1.8%), p:0.045) and perifovea (4 µm (1.5%), p:0.023). Nevertheless, this change (maximum:4.5 µm in the fovea) in the ILM-RPE thickness could not be clinically significant.

Table 3 The RNFL and ILM-RPE thickness comparison before and after deep sclerotomy. (t: Parametric data analyzed by Paired student t-Test, w: Nonparametric data analyzed by Wilcoxon Test)

Glaucoma is a heterogeneous group of diseases with various etiologies with an expected outcome: chronic optic neuropathy and structural changes in the RNFL and ganglion cells leading to visual dysfunction such as impaired visual field and decreased visual acuity. Non-penetrating deep sclerotomy (NPDS) is one of the effective therapeutic interventions with high efficacy in lowering IOP. In a two-year follow-up, Puerto et al. demonstrated a 23.5% IOP decrease following the NPDS [11]. Another study on Chronic POAG cases declared a 45.6% decline in IOP after a month from the NPDS (from 27.7 mmHg at baseline to 15.05 mmHg); however, the longtime (18 months) results showed a final 25.1% decrease in IOP [12]. On the other hand, Our study achieved a 67.75% decrease in IOP after a month from the deep sclerotomy surgery (From 24.8 to 8 mmHg), which is a comparable result to the previous studies.

In addition to the role of therapeutic methods on IOP, their effect on the visual field has been studied. Regarding the impact of the NPDS procedure on Humphery Visual Field (HVF) 30 − 2, a study declared a mean 2.1dB improvement in MD of the test in a 2.5-year postoperative period. Also, they confirmed a 1.4dB rise in PSD two years after the NPDS. However, there were fluctuations in MD and PSD values during the five-year follow-up period of this study [13]. Similarly, Sponsel et al. showed an HVF 30 − 2 MD improvement from − 12.20dB to -10.85 one year after the mitomycin-augmented NPDS [14]. In comparison, the results of our study demonstrate a significant improvement in HVF 30 − 2 MD one month after the NPDS (-13.06 dB, 95%CI: -(9.61–16.50) compared to -15.44 dB, 95%CI: –(11.20-19.68)). Nevertheless, there was no significant change regarding the PSD.

Besides the postoperative functional changes, there could be structural alterations regarding the retinal microvasculature and the thickness of the retinal layer. A prospective study revealed a significantly lower peripapillary vessel density and flow index in glaucomatous eyes than in normal ones. These OCTA indices also correlated highly with the visual field function[15]. Confirming the previous study, Khallouli et al. declared a significant peripapillary vascular damage in manifest glaucoma compared to peri perimetric glaucoma and controls. In addition, this peripapillary vasculature damage was significantly associated with the VF defect. Surprisingly, the peripapillary VD had better diagnostic accuracy than the RNFL and ganglion cell complex (GCC) [16]. A significant correlation between the whole image, peripapillary VD, and MD has been demonstrated in our study, which depicts the crucial role of the optic disk and the peripapillary microvascular condition in the visual field. In addition, the changes in the whole image VD after the surgery were significantly correlated with the MD alterations.

Furthermore, the macular vasculature could be affected by glaucoma. Lu et al. declared a significant decrease in perifoveal and parafoveal VD in early OAG compared to normal people. In the peri perimetric OAG, the perifoveal VD decreased compared to the normal population, although the parafoveal VD was unaffected. It was also suggested that the macular whole image VD and perifoveal VD could have similar diagnostic accuracy to RNFL and GCC [17]. Besides, a significant correlation between the macular VD decrease and a worse visual field has been demonstrated [18]. Similarly, our study showed a significant correlation between higher parafoveal, perifoveal VD, and better MD in HVF 30 − 2 in our cases. This finding could emphasize the role of the macular microvascular structure role on visual field function.

The role of therapeutic procedures on retinal microstructures has been studied through various studies. The medical treatment with latanoprost on 26 treatment-naïve eyes indicated a significant decrease in IOP (26.1%) without a considerable change in macular and peripapillary VD 3 weeks after the treatment initiation. However, the IOP and VD were significantly correlated [19]. A prospective study on 21 POAG patients has demonstrated that one month after the mitomycin-augmented NPDS surgery, the macular and peripapillary VD did not change substantially compared to the baseline[20]. On the other hand, a study on the effect of trabeculectomy surgery on the retinal microvasculature showed a significant increase in peripapillary VD 6 months after the surgery. Nevertheless, there was not such a significant change one month after the surgery, and the macular VD did not show a considerable alteration either 1 or 6 months after the surgery [21]. Confirming, another study on the role of Ahmed glaucoma valve implantation on the optic nerve head vasculature resulted in a significant improvement of peripapillary VD 6 months after the surgery [22].

Regarding the effect of NPDS on the peripapillary and macular microvasculature, our study demonstrated no significant change in the vascular density of either one month after the deep sclerotomy surgery on POAG cases. This result and the comparison to the previous studies suggest a probable time-related effect of anti-glaucoma therapeutic procedures on the retinal microvasculature. The changes in the vascular structure of the retina and optic nerve head could be gradual, which could be missed in early follow-ups after the treatment. So, there should be long-term studies to determine better the exact role of NPDS on the retinal microvasculature condition.

In addition to the vascular components of the retina, neuronal elements such as RNFL could also be altered due to surgical interventions. It has been demonstrated that the mean RNFL thickness of 35 eyes with deep sclerotomy has significantly increased six months after the surgery. Moreover, the RNFL thickness elevation was significantly correlated with the visual field MD improvement [23]. In contrast, another prospective study on 34 glaucomatous eyes undergoing deep sclerotomy revealed no significant change in the RNFL 6 months after the surgery [24]. However, a more recent study on patients with deep sclerotomy or trabeculectomy surgery concluded a slightly significant regional increase in RNFL thickness one month after the procedure [25].

On the contrary, our study showed a significant decrease in Peripapillary, superior hemisphere, inferior hemisphere, and Nasal-Inferior RNFL thickness. Another study on patients with trabeculectomy and NPDS declared a slight RNFL thickening one month after the procedure. However, the RNFL started to get thinned after the third month of follow-up [26].

This study reemphasizes the influential role of non-penetrating deep sclerotomy surgery on medically uncontrolled cases of primary open-angle glaucoma by significantly decreasing IOP and visual field improvement. Also, the results showed that peripapillary and macular vascular density was significantly and positively correlated to the mean deviation in HVF 30 − 2. However, our study failed to show a significant change in the peripapillary and macular microvasculature one month after the surgery. The slow and gradual process of change in the vascular structure could be the reason for this finding, and studies with more extended follow-up periods may explore the exact role of surgery on the retinal microvasculature. The RNFL loss happened in our cases one month after the surgery, which could result from glaucoma progression or an inadvertent intraoperative IOP rise.

The sample size of our study was small, and the follow-up period was short. So, larger studies with more extended follow-up periods could help explore more accurate results.

Funding

This research received no specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Competing Interests

The authors have no relevant financial or non-financial interests to disclose.

Author contributions

All authors contributed to the study's conception and design. N.T., A.M., and B.F. performed clinical evaluations and surgical procedures. M.N., N.T., and A.G. performed the para-clinical evaluations and data collection. A.A. performed the data analysis and wrote the first draft of the manuscript. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Ethics approval

This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Ethics Committee of Tabriz University of Medical Sciences with the approval code of IR.TBZMED.REC.1399.384.

Consent to participate

All the patients enrolled in the study after obtaining written informed consent.

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No competing interests reported.

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Retinal Vessel Density and Visual Field Changes and Their Correlation Following the Deep Sclerotomy in Primary Open-angle Glaucoma

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This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Ethics Committee of Tabriz University of Medical Sciences with the approval code of IR.TBZMED.REC.1399.384.

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