Abstract
AIM
To evaluate the macular microvasculature before and after surgery for idiopathic macular hole (MH) and the association of preoperative vascular parameters with postoperative recovery of visual acuity and configuration.
METHODS
Twenty eyes from 20 patients with idiopathic MH were enrolled. Optical coherence tomography angiography (OCTA) images were obtained before, 2wk, 1, and 3mo after vitrectomy with internal limiting membrane peeling. Preoperative foveal avascular zone (FAZ) area and perimeter and regional vessel density (VD) in both layers were compared according to the 3-month best-corrected visual acuity (BCVA).
RESULTS
The BCVA improved from 0.98±0.59 (logMAR, Snellen 20/200) preoperatively to 0.30±0.25 (Snellen 20/40) at 3mo postoperatively. The preoperative deep VD was smaller and the FAZ perimeter was larger in the 3-month BCVA<20/32 group (all P<0.05). A significant reduction was observed in FAZ parameters and all VDs 2wk postoperatively. Except for deep perifoveal VD, all VDs recovered only to their preoperative values. The postoperative FAZ parameters were lower during follow-up. Decreases in preoperative deep VDs were correlated with worse postoperative BCVA (Pearson's r=-0.667 and -0.619, respectively). A larger FAZ perimeter (Spearman's r=-0.524) and a lower deep perifoveal VD preoperatively (Pearson's r=0.486) were associated with lower healing stage.
CONCLUSION
The status of the deep vasculature may be an indicator of visual acuity in patients with a closed MH. Except for the deep perifoveal region, VD recovers only to preoperative levels.
Keywords: macular microvasculature, macular hole, vitreoretinal surgery, optical coherence tomography angiography
INTRODUCTION
An idiopathic macular hole (MH), caused by tangential traction, can be successfully closed by pars plana vitrectomy with gas-fluid exchange[1]. The anatomic and functional outcomes were further improved by the advent of peeling of the internal limiting membrane (ILM)[2]. However, the postoperative visual acuity (VA) is sometimes poor despite successful anatomic closure[3]–[4]. Long-term restoration of the microstructure and function of the fovea has been evaluated following surgery for idiopathic MH[2]. Previous studies in eyes with MH have focused mainly on disruption of the outer retina, including the external limiting membrane (ELM), the ellipsoid zone (EZ), and the photoreceptors with respect to the visual prognosis[5]–[6].
Recently, researchers demonstrated an association of disorganization of the retinal inner layers (DRIL) with VA in various retinal diseases[7]–[8]. The presence of vitreous cortex, proliferative glial tissue, and retinal hydration has been suggested as factors in the formation of macular holes in histologic studies[9]–[10] and possibly contribute to DRIL. DRIL indicates specific anatomic damage to the structures in the retinal layers that transmit visual data and also a poor inner retinal circulation[11].
With the development of imaging technology, optical coherence tomography angiography (OCTA) provides high-resolution, depth-resolved images for evaluation of the retinal capillary plexuses in eyes with MH in a noninvasive and dye-free manner[12]–[15]. In our previous work, we used a commercially available OCTA device with custom-built imaging software and concluded that disorders in the inner retinal vessels corresponded to disruption of the outer retinal layers and VA in the setting of dysfunctional vasculature[16].
The recovery of the retinal microvasculature in patients with a surgically closed MH remains to be elucidated. Meanwhile, limited information is available regarding quantitative evaluation of the preoperative status of the retinal microvasculature in eyes with MH. Accurate OCTA measurements should correct for ocular magnification and require information on axial length. Until now, no study has accurately quantified the changes that occur in the vasculature of the macula in eyes with MH after surgical treatment or the relationship between preoperative vascular parameters and the postoperative VA.
The aims of this retrospective study were to characterize macular microvasculature in the superficial and deep retinal layers following surgery in patients with idiopathic MH using OCTA and to investigate the association of preoperative microvascular parameters in the inner retina with postoperative best-corrected visual acuity (BCVA) and healing.
SUBJECTS AND METHODS
Ethical Approval
This study was approved by the Ethics Committee at Wenzhou Medical University and complied with the tenets of the Declaration of Helsinki. Informed consent was obtained from all patients.
Subjects
The medical records of patients who had undergone successful MH closure by vitrectomy and ILM peeling in the Fundus Department at the Eye Hospital, Wenzhou Medical University, from June 2018 to May 2020 were reviewed. Each patient underwent a complete ophthalmic examination, including slit-lamp examination, intraocular pressure measurement, fundoscopy, preoperative axial length measurement, OCT (Spectralis; Heidelberg Engineering, Heidelberg, Germany), and OCTA (AngioVue; Optovue, Inc., Fremont, CA, USA). The slit-lamp, fundoscopy, OCT, and OCTA examinations were performed before surgery and 2wk, 1, and 3mo after surgery. The inclusion criterion was a Gass stage 2-3 idiopathic full-thickness MH confirmed on OCT. Eyes with macular disease, such as age-related macular degeneration, epimacular membrane, myopic choroidal neovascularization, a spherical equivalent refractive error >±6.0 diopters, significant cataract (LOCS scale higher than N2, C1, P2)[17] or macular edema after surgery, glaucoma, other marked complications, or a history of intraocular surgery were excluded. Chronic macular holes (defined by visual symptoms of greater than 1y), heavy smokers[18], or patients with systemic disease, such as diabetes, hypertension were also excluded. The patients were divided into groups according to whether or not their 3-month postoperative BCVA was <20/32 or ≥20/32[19].
Image Acquisition and Data Analysis
The AngioVue version 2017.1.0.155 software was used. The macular region was imaged using a central 3×3 mm2 area. Low-quality OCTA images with a scan quality <5/10[20], severe artifacts attributable to poor fixation, or failure of automatic layer segmentation were excluded. The area and perimeter of the foveal avascular zone (FAZ) were determined by the software embedded in the instrument. The vessel density (VD) was calculated as the percentage of pixels with a flow signal greater than the threshold value and automatically measured using custom-built imaging software implemented in MATLAB (Mathworks, Natick, MA, USA)[16],[21]. The mean brightness of the FAZ was taken as the threshold for the retinal vessels. Parafoveal and perifoveal VDs were calculated in the regions of the radius between 0.5 and 0.875 mm and between 0.875 and 1.25 mm, respectively, from the foveal center (Figure 1A, 1B). To reduce the effects of decentration of the FAZ and the artifacts at the edge of the scan, a circular area with a diameter of 2.5 mm was used instead of the entire 3×3-mm2 area.
Figure 1. Macular region analyzed for VD and representative OCT images of DRIL during the post-surgery recovery.
A: Total VD was calculated for the ring-shaped area between a 0.5 and 1.25 mm radius from the fovea center; B: C1 and C2 were 0.5 to 0.875 mm and 0.875 to 1.25 mm radius ring-shaped area from the fovea center, respectively; C, D: Red arrows shows the area where the boundary between the ganglion cell-inner plexiform layer complex, inner nuclear layer and outer plexiform layer cannot be distinguished and is irregular. VD: Vessel density; DRIL: Disorganization of retinal inner layers.
Preoperative minimum diameter of the MH was measured in the OCT images. The postoperative healing stage, i.e., restoration of the photoreceptor layer, was graded from 1 to 3[5]. Grade 1 was assigned when the EZ and ELM were disrupted, grade 2 when the EZ was disrupted but the ELM was restored, and grade 3 when both the ELM and EZ were restored. DRIL was defined as the horizontal extent within the central 2000 µm for which any boundaries between the ganglion cell-inner plexiform layer complex, inner nuclear layer, and outer plexiform layer could not be identified[8]. Two independent observers interpreted the OCTA and OCT images. The observers reached a consensus in all cases.
To eliminate the effect of magnification, the images obtained by OCTA and OCT were corrected by Bennett's formula using the axial length[22]–[23]. The relationship between the OCT image measurements and the actual scan diameter was expressed by the formula t=p×q×s, where t is the actual axial length, p is the magnification factor determined by the camera of the OCT imaging system, q is the magnification factor in relation to the eye, and s is the original measurement obtained from the OCT image. The correction factor q was determined using q=0.01306×(AL–1.82)[23].
Surgical Technique
All procedures were performed by a single surgeon. Standard 3-port pars plana vitrectomy was performed using 23-gauge instruments. Cataract surgery was performed on all 20 phakic eyes. A 31-year-old patient underwent cataract surgery for congenital cataract. A concentration of 0.025% indocyanine green (ICG) was injected into the vitreous cavity and washed out no later than 3 seconds by 23-gauge cutter. Then the ILM was peeled by carefully grasping with forceps without retinal damage to about 4-disc diameters centered on the macula. All patients performed fluid-air exchange with air, and the sclerotomies were sutured. Patients were instructed to remain in a prone position for 3-5d postoperatively.
Statistical Analysis
Independent t-test and Mann-Whitney U test were used to compare continuous variables between the groups. Repeated-measures analysis of variance was used to evaluate differences in the chronologic data. Post multiple comparisons were evaluated using the Bonferroni test. The Pearson correlation test was used to determine the associations between preoperative vascular parameters and postoperative BCVA. The associations between preoperative vascular parameters and postoperative healing stage were evaluated using the Spearman correlation test. All data are expressed as the means±standard deviations and analyzed with SPSS version 22.0 software (IBM Corp., Armonk, NY, USA). logMAR values of 2.0 and 3.0 were assigned for counting fingers and hand motion vision, respectively[24]. P<0.05 indicated statistical significance.
RESULTS
Patient Demographic and Clinical Characteristics
Forty-three eyes of 43 patients with an MH underwent vitrectomy with ILM peeling between June 2018 and May 2020. Twenty-three eyes were excluded (8 for high myopia, 4 for severe cataract that prevented acquisition of high-quality OCTA images, 4 for age-related macular degeneration, 2 for diabetic retinopathy, 2 for myopic choroidal neovascularization, 2 for OCTA images of poor quality, and 1 loss in postoperative follow-up), leaving 20 eyes of 20 patients for inclusion (Table 1). The patients mean age was 59.1±10.1y. Fourteen patients were female (70%) and 6 (30%) were male. The mean preoperative axial length was 23.9±1.1 (range 21.77-25.52) mm. Before surgery, the mean minimum diameter of the hole was 462.9±208.3 (range 206-871) µm.
Table 1. Patient demographic and ophthalmic characteristics.
| Case | Age (y) | Sex | Eye | Stage | Axial length (mm) | Minimum diameter of hole (µm) | Preoperative BCVA | BCVA at 2wk | BCVA 1mo | BCVA 3mo | Healing stage |
| 1 | 31 | F | OS | 3 | 24.46 | 826 | 20/100 | 20/63 | 20/50 | 20/40 | 1 |
| 2 | 60 | M | OD | 2 | 24.79 | 328 | 20/160 | 20/63 | 20/50 | 20/32 | 2 |
| 3 | 57 | F | OS | 3 | 22.95 | 409 | 20/200 | 20/100 | 20/50 | 20/40 | 2 |
| 4 | 49 | F | OD | 2 | 22.63 | 206 | 20/50 | 20/200 | 20/100 | 20/25 | 2 |
| 5 | 63 | F | OS | 2 | 24.26 | 352 | 20/63 | 20/200 | 20/50 | 20/20 | 2 |
| 6 | 68 | M | OS | 2 | 23.2 | 266 | 20/32 | 20/80 | 20/25 | 20/20 | 3 |
| 7 | 61 | F | OD | 3 | 23.34 | 553 | FC/1 m | 20/2000 | 20/200 | 20/200 | 2 |
| 8 | 55 | M | OS | 2 | 24.88 | 331 | 20/500 | 20/63 | 20/63 | 20/63 | 1 |
| 9 | 65 | F | OD | 2 | 25.52 | 223 | 20/40 | 20/40 | 20/32 | 20/25 | 2 |
| 10 | 65 | F | OS | 2 | 22.56 | 285 | 20/1000 | 20/400 | 20/200 | 20/63 | 2 |
| 11 | 69 | M | OD | 2 | 22.61 | 307 | FC/1 m | HM/1 m | 20/100 | 20/50 | 2 |
| 12 | 63 | F | OD | 3 | 21.77 | 574 | 20/125 | 20/100 | 20/50 | 20/40 | 2 |
| 13 | 54 | F | OS | 3 | 22.95 | 871 | 20/100 | 20/63 | 20/25 | 20/20 | 2 |
| 14 | 57 | F | OS | 3 | 23.77 | 695 | FC/1 m | 20/400 | 20/63 | 20/40 | 1 |
| 15 | 47 | M | OS | 3 | 24.85 | 481 | 20/125 | 20/63 | 20/32 | 20/32 | 2 |
| 16 | 46 | F | OD | 2 | 25.5 | 213 | 20/32 | 20/125 | 20/25 | 20/20 | 3 |
| 17 | 65 | F | OS | 3 | 23.84 | 480 | 20/100 | 20/50 | 20/63 | 20/32 | 2 |
| 18 | 72 | M | OS | 3 | 24.53 | 779 | 20/400 | 20/400 | 20/100 | 20/100 | 1 |
| 19 | 63 | F | OD | 3 | 24.47 | 602 | 20/63 | 20/63 | 20/40 | 20/32 | 2 |
| 20 | 72 | F | OD | 3 | 25.41 | 476 | 20/400 | 20/200 | 20/63 | 20/63 | 2 |
F: Female; M: Male; OS: Left eye; OD: Right eye; BCVA: Best-corrected visual acuity.
The logMAR BCVA improved from 0.98±0.59 (range 0.22-2.00, Snellen equivalent 20/200) preoperatively to 0.93±0.64 (range 0.30-3.00, Snellen 20/160) at 2wk, 0.47±0.25 (range 0.15-1.00, Snellen 20/63) at 1mo, and 0.30±0.25 (range 0-1.00, Snellen 20/40) at 3mo postoperatively. Ten patients (50%) had evidence of different degrees of DRIL on OCT images during the post-surgery recovery of MHs (Figure 1C, 1D).
Between-Group Differences in Preoperative Data and Vascular Parameters
There were significant differences in preoperative VA, perimeter of the FAZ, and parafoveal and perifoveal VD in the deep plexus between the group with a 3-month BCVA<20/32 and the group with the 3-month BCVA≥20/32 (Table 2). In the group with the 3-month BCVA<20/32, the preoperative VA was significantly worse, and the perimeter of the FAZ was larger. In the deep capillary layer, the VDs in both regions was smaller. The minimum diameter of the hole and the area of the FAZ were larger, albeit not significantly so. No significant differences were found in patient age, preoperative stage, axial length, or VD in either region of the superficial layer.
Table 2. Comparison of preoperative parameters between eyes with BCVA≥20/32 and eyes with BCVA<20/32 at 3mo postoperatively.
| Variables | BCVA≥20/32 postop. 3mo | BCVA<20/32 postop. 3mo | P a |
| n | 10 | 10 | - |
| Age (y) | 58.0±8.3 | 60.2±12.0 | 0.639 |
| Preoperative stage | 2.4±0.5 | 2.7±0.5 | 0.196 |
| Axial length (mm) | 24.2±1.0 | 23.6±1.2 | 0.251 |
| Minimum diameter of hole (µm) | 402.2±212.1 | 523.5±196.0 | 0.201 |
| Preoperative BCVA (logMAR) | 0.531±0.246 | 1.422±0.491 | 0.001 |
| FAZ area (mm2) | 0.366±0.127 | 0.490±0.164 | 0.076 |
| FAZ perimeter (mm) | 2.5±0.5 | 3.2±0.7 | 0.032 |
| Superficial parafoveal VD (%) | 0.482±0.012 | 0.467±0.035 | 0.211 |
| Superficial perifoveal VD (%) | 0.480±0.012 | 0.463±0.036 | 0.192 |
| Deep parafoveal VD (%) | 0.516±0.039 | 0.468±0.050 | 0.027 |
| Deep perifoveal VD (%) | 0.499±0.038 | 0.456±0.038 | 0.023 |
aIndependent t-test or Mann-Whitney U test were performed as appropriate. BCVA: Best-corrected visual acuity; FAZ: Foveal avascular zone; VD: Vessel density.
Changes in Vessel Density and Foveal Avascular Zone
There were significant changes in all vascular parameters after MH surgery (Table 3). The changes in parafoveal and perifoveal VD in both layers are shown in Figures 2 and 3. Before vitrectomy, the mean parafoveal and perifoveal VD values were 47.4%±2.7% and 47.2%±0.03%, respectively, in the superficial layer and 49.2%±0.05% and 47.7%±0.04%, respectively, in the deep layer. A significant reduction in VD was observed 2wk after surgery. Furthermore, there was evidence of recovery of the macular microvasculature in the superficial plexus at 1 and 3mo postoperatively. In the deep plexus, there was no difference between the preoperative VD and the VD at 1mo postoperatively in either region. The mean perifoveal VD at 3mo postoperatively was even greater than that before surgery.
Table 3. Foveal avascular zone and regional vessel density in the superficial and deep layers.
| Parameters | Preoperative | Postoperative |
P a | ||
| 2wk | 1mo | 3mo | |||
| FAZ | |||||
| Area, mm2 | 0.43±0.16 | 0.19±0.15 | 0.25±0.17 | 0.30±0.17 | <0.001 |
| Perimeter, mm | 2.8±0.7 | 1.7±0.6 | 2.0±0.8 | 2.2 ±0.6 | <0.001 |
| Superficial layer | |||||
| Parafoveal VD, % | 47.4±2.7 | 43.4±0.04 | 45.1±0.03 | 46.8±0.03 | <0.001 |
| Perifoveal VD, % | 47.2±0.03 | 42.8±0.03 | 44.4±0.03 | 46.2±0.03 | <0.001 |
| Deep layer | |||||
| Parafoveal VD, % | 49.2±0.05 | 42.2±0.06 | 48.3±0.04 | 51.6±0.03 | <0.001 |
| Perifoveal VD, % | 47.7±0.04 | 41.3±0.06 | 47.6±0.04 | 51.1±0.03 | <0.001 |
aRepeated-measures analysis of variance. FAZ: Foveal avascular zone; VD: Vessel density.
Figure 2. Macular microvasculature before and after surgery using OCTA and algorithm analysis.
There was a significant reduction in the FAZ area (A) and perimeter (D) during the follow-up period when compared with the preoperative status. The parafoveal and perifoveal VD in the superficial layer (B and E) and deep layer (C and F) show that, with the exception of the deep perifoveal VD, there was a significant reduction in all VD values in both layers at 2wk after surgery with recovery to the preoperative status by 3mo. Each point represents the mean±standard deviation. aP<0.01 and bP≤0.001 vs the preoperative value. FAZ: Foveal vascular zone; OCTA: Optical coherence tomography angiography; VD: Vessel density.
Figure 3. Representative OCTA images for one eye with idiopathic macular hole before and after surgery.
A: Superficial layer; B: Deep layer; C: Horizontal B-scan. The patient is a 65-year-old woman who had an eye with a Gass stage 2 macular hole. Preoperatively, the minimum diameter of the hole was 223 µm. The preoperative Snellen BCVA was 20/40. The 3-month postoperative Snellen BCVA was 20/25 with stage 2 healing. The FAZ area is shown as an example of the macular vasculature. The FAZ area before, 2wk, 1, and 3mo postoperatively was 0.295, 0.253, 0.260, and 0.269 mm2, respectively. BCVA: Best-corrected visual acuity; FAZ: Foveal vascular zone; OCTA: Optical coherence tomography angiography; VD: Vessel density.
The mean preoperative area and perimeter of the FAZ were 0.43 mm2 and 2.8 mm, respectively (Figure 2A, 2D). Significant reductions in the mean values for the FAZ parameters were observed during the follow-up period (Table 3 and Figure 2).
Correlation of Preoperative Vascular Parameters with Postoperative Visual Acuity and Healing Stage
There was a correlation between decreased preoperative parafoveal and perifoveal VD in the deep layer and worse 3-month VA (Pearson's r=-0.667 and -0.619, respectively; Table 4, Figure 4A, 4C). A larger FAZ perimeter (Spearman's r=-0.524) and decreased perifoveal VD preoperatively in the deep layer (Pearson's r=0.486) was associated with lower healing stage of photoreceptor layers (Figure 4B, 4D). There was no correlation between FAZ, superficial vasculature parameters and VA at 3mo after surgery. No correlation was found between preoperative superficial VDs and postoperative healing stage.
Table 4. Correlation of foveal avascular zone and vessel density measurements with 3-month postoperative BCVA and healing stage.
| Preoperative parameters | 3-month BCVAa |
Healing stageb |
||
| r (95%CI) | P | r (95%CI) | P | |
| FAZ | ||||
| Area | 0.308 (-0.07, 0.724) | 0.186 | -0.418 (-0.80, 0.232) | 0.067 |
| Perimeter | 0.394 (0.001, 0.762) | 0.086 | -0.524 (-0.810, -0.078) | 0.018 |
| Superficial layer | ||||
| Parafoveal VD | -0.189 (-0.730, 0.249) | 0.425 | 0.091 (-0.408, 0.550) | 0.701 |
| Perifoveal VD | -0.207 (-0.642, 0.275) | 0.381 | 0.223 (-0.244, 0.620) | 0.344 |
| Deep layer | ||||
| Parafoveal VD | -0.667 (-0.832, -0.386) | 0.001 | 0.330 (-0.142, 0.678) | 0.155 |
| Perifoveal VD | -0.619 (-0.793, -0.420) | 0.004 | 0.486 (0.121, 0.755) | 0.030 |
aPearson correlation test. bSpearman correlation test. BCVA: Best-corrected visual acuity; CI: Confidence interval; FAZ: Foveal avascular zone; VD: Vessel density.
Figure 4. Correlations of vascular parameters with 3-month postoperative BCVA and healing stage.
A, C: Lower preoperative deep parafoveal and perifoveal VD correlated with worse VA; B, D: Larger FAZ perimeter and decreased deep perifoveal VD were associated with poorer healing. BCVA: Best-corrected visual acuity; FAZ: Foveal vascular zone; VD: Vessel density.
DISCUSSION
Several studies have investigated the preoperative configuration of MH using OCT and searched for predictors of the visual outcome after surgery[2],[4],[6]. To the best of our knowledge, postoperative visual recovery has not been evaluated as a predictive parameter by OCTA in eyes with MH. We demonstrated that the preoperative macular microvasculature was denser in eyes with MH that had better VA after surgery, especially in the deep capillaries. Moreover, correlation analysis revealed that a decrease from the preoperative deep capillary VD was strongly correlated with worse postoperative VA. We speculate that this could be attributed to several possible mechanisms[10],[16]. Tornambe[10] proposed the “hydration theory”, whereby during formation of an MH, after the posterior hyaloid has created a retinal defect, vitreous fluid first passes through the inner retina and disrupts homeostasis. Liquid vitreous fluid then accumulates, the MH appears to enlarge, and the inner retinal tissue become swollen, especially in the outer plexiform layer. DRIL was recently identified to be a sign of poor inner retinal circulation[7],[11], indicating disruption of the pathways that transmit visual information from the photoreceptors to the ganglion cells and seemed to be a correlated predictive biomarker for VA in various diseases. We observed a similar phenomenon in a previous study[16]. Given their special watershed-like position, the deep capillaries may be more prone to ischemia and contribute to disruption of the photoreceptor layer and then visual function. The suggested pathophysiologic changes within the inner retinal vasculature, which are supported by histopathologic and imaging studies, collectively may have accounted for the decreased deep blood flow seen in our study.
We quantitively demonstrated recovery of the macular vasculature with magnification correction before and after surgical intervention in eyes with MH. Scupola et al[2] reported significant improvement in retinal function at 3mo after closure of an MH that was confirmed to be maintained at 6 and 12mo by focal electroretinography. Therefore, we compared the microvascular networks in eyes with MH before, 2wk, 1, and 3mo postoperatively. Significant reductions in FAZ parameters were observed 2wk postoperatively, suggesting a movement of foveal tissue toward the central fovea and a centripetal movement when the MH is closed[13]. However, the 2-week postoperative VDs decreased significantly, and the VA improved only slightly, indicating prompt structural recovery but delayed functional repair. Kim et al[14] and Demirel et al[25] reported that the postoperative VD in eyes with a closed MH, particularly in the deep plexus, was lower than that in either fellow eyes or healthy eyes. In the present study, most VD values recovered only to the preoperative status, indicating a lack of functional vascular integrity after surgery. The disrupted microvasculature may impede the dynamic healing process and provide another explanation for the unsatisfactory visual gain after surgery despite successful anatomic closure of the MH.
Correlational analysis revealed a moderate correlation of a decreased deep perifoveal VD and an increased FAZ perimeter with poor healing. The ischemia in inner retinal vasculature is considered to contribute to the disorganization of the outer retina and to lead to poor restoration of the microstructure of the fovea[16].
This study has several limitations. The first is its retrospective design and relatively small sample size. The second relates to the fact that eyes with MH tend to have poorer stable fixation before surgical closure, leading to exclusion of OCTA images with poor quality upon visual inspection.
In conclusion, OCTA analysis before and after surgery in eyes with MH demonstrated the preoperative macular microvasculature and suggests that the status of the deep plexus could predict the postoperative visual outcome. Quantification of the retinal vasculature postoperatively would provide an explanation for the limited visual recovery after surgical closure of MH.
Acknowledgments
Foundations: Supported by the National Natural Science Foundation of China (No.81900910; No.81700884); Natural Science Foundation of Zhejiang Province (No.LQ19H120003; No.LGF21H120005); Key Project Jointly Constructed by Zhejiang Pronvince and Ministry (No.WKJ-ZJ-2037); Basic Scientific Research Project of Wenzhou (No.Y20210194).
Conflicts of Interest: Cheng D, None; Tao JW, None; Yu XT, None; Chen YQ, None; Shen MX, None; Wu MH, None; Yu JF, None; Lian HL, None; Lu Z, None; Shen LJ, None.
REFERENCES
- 1.Tognetto D, Grandin R, Sanguinetti G, Minutola D, Di Nicola M, Di Mascio R, Ravalico G, Macular Hole Surgery Study Group Internal limiting membrane removal during macular hole surgery: results of a multicenter retrospective study. Ophthalmology. 2006;113(8):1401–1410. doi: 10.1016/j.ophtha.2006.02.061. [DOI] [PubMed] [Google Scholar]
- 2.Scupola A, Mastrocola A, Sasso P, Fasciani R, Montrone L, Falsini B, Falsini B, Abed E. Assessment of retinal function before and after idiopathic macular hole surgery. Am J Ophthalmol. 2013;156(1):132–139.e1. doi: 10.1016/j.ajo.2013.02.007. [DOI] [PubMed] [Google Scholar]
- 3.Lai MM, Williams GA. Anatomical and visual outcomes of idiopathic macular hole surgery with internal limiting membrane removal using low-concentration indocyanine green. Retina. 2007;27(4):477–482. doi: 10.1097/01.iae.0000247166.11120.21. [DOI] [PubMed] [Google Scholar]
- 4.Grewal DS, Reddy V, Mahmoud TH. Assessment of foveal microstructure and foveal lucencies using optical coherence tomography radial scans following macular hole surgery. Am J Ophthalmol. 2015;160(5):990–999.e1. doi: 10.1016/j.ajo.2015.08.014. [DOI] [PubMed] [Google Scholar]
- 5.Wakabayashi T, Fujiwara M, Sakaguchi H, Kusaka S, Oshima Y. Foveal microstructure and visual acuity in surgically closed macular holes: spectral-domain optical coherence tomographic analysis. Ophthalmology. 2010;117(9):1815–1824. doi: 10.1016/j.ophtha.2010.01.017. [DOI] [PubMed] [Google Scholar]
- 6.Kusuhara S, Teraoka Escaño MF, Fujii S, Nakanishi Y, Tamura Y, Nagai A, Yamamoto H, Tsukahara Y, Negi A. Prediction of postoperative visual outcome based on hole configuration by optical coherence tomography in eyes with idiopathic macular holes. Am J Ophthalmol. 2004;138(5):709–716. doi: 10.1016/j.ajo.2004.04.063. [DOI] [PubMed] [Google Scholar]
- 7.Babiuch AS, Han M, Conti FF, Wai K, Silva FQ, Singh RP. Association of disorganization of retinal inner layers with visual acuity response to anti-vascular endothelial growth factor therapy for macular edema secondary to retinal vein occlusion. JAMA Ophthalmol. 2019;137(1):38–46. doi: 10.1001/jamaophthalmol.2018.4484. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Zur D, Iglicki M, Feldinger L, Schwartz S, Goldstein M, Loewenstein A, Barak A. Disorganization of retinal inner layers as a biomarker for idiopathic epiretinal membrane after macular surgery-the DREAM study. Am J Ophthalmol. 2018;196:129–135. doi: 10.1016/j.ajo.2018.08.037. [DOI] [PubMed] [Google Scholar]
- 9.Haouchine B, Massin P, Gaudric A. Foveal pseudocyst as the first step in macular hole formation: a prospective study by optical coherence tomography. Ophthalmology. 2001;108(1):15–22. doi: 10.1016/s0161-6420(00)00519-4. [DOI] [PubMed] [Google Scholar]
- 10.Tornambe PE. Macular hole genesis: the hydration theory. Retina. 2003;23(3):421–424. doi: 10.1097/00006982-200306000-00028. [DOI] [PubMed] [Google Scholar]
- 11.Onishi AC, Ashraf M, Soetikno BT, Fawzi AA. Multilevel ischemia in disorganization of the retinal inner layers on projection-resolved optical coherence tomography angiography. Retina. 2019;39(8):1588–1594. doi: 10.1097/IAE.0000000000002179. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Pierro L, Iuliano L, Bandello F. OCT angiography features of a case of bilateral full-thickness macular hole at different stages. Ophthalmic Surg Lasers Imaging Retina. 2016;47(4):388–389. doi: 10.3928/23258160-20160324-16. [DOI] [PubMed] [Google Scholar]
- 13.Akahori T, Iwase T, Yamamoto K, Ra E, Kawano K, Ito Y, Terasaki H. Macular displacement after vitrectomy in eyes with idiopathic macular hole determined by optical coherence tomography angiography. Am J Ophthalmol. 2018;189:111–121. doi: 10.1016/j.ajo.2018.02.021. [DOI] [PubMed] [Google Scholar]
- 14.Kim YJ, Jo J, Lee JY, Yoon YH, Kim JG. Macular capillary plexuses after macular hole surgery: an optical coherence tomography angiography study. Br J Ophthalmol. 2018;102(7):966–970. doi: 10.1136/bjophthalmol-2017-311132. [DOI] [PubMed] [Google Scholar]
- 15.Baba T, Kakisu M, Nizawa T, Oshitari T, Yamamoto S. Regional densities of retinal capillaries and retinal sensitivities after macular hole surgery with internal limiting membrane peeling. Retina. 2020;40(8):1585–1591. doi: 10.1097/IAE.0000000000002637. [DOI] [PubMed] [Google Scholar]
- 16.Cheng D, Shen M, Zhuang X, Lin D, Dai M, Chen S, Lu F, Wang Y. Inner retinal microvasculature damage correlates with outer retinal disruption during remission in behçet's posterior uveitis by optical coherence tomography angiography. Invest Ophthalmol Vis Sci. 2018;59(3):1295–1304. doi: 10.1167/iovs.17-23113. [DOI] [PubMed] [Google Scholar]
- 17.Told R, Ginner L, Hecht A, Sacu S, Leitgeb R, Pollreisz A, Schmidt-Erfurth U. Comparative study between a spectral domain and a high-speed single-beam swept source OCTA system for identifying choroidal neovascularization in AMD. Sci Rep. 2016;6:38132. doi: 10.1038/srep38132. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Tirlapur VG, Gicheru K, Charalambous BM, Evans PJ, Mir MA. Packed cell volume, haemoglobin, and oxygen saturation changes in healthy smokers and non-smokers. Thorax. 1983;38(10):785–787. doi: 10.1136/thx.38.10.785. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Ueda-Consolvo T, Otsuka M, Hayashi Y, Ishida M, Hayashi A. Microperimetric biofeedback training improved visual acuity after successful macular hole surgery. J Ophthalmol. 2015;2015:572942. doi: 10.1155/2015/572942. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Yeung L, Wu WC, Chuang LH, Wang NK, Lai CC. Novel optical coherence tomography angiography biomarker in branch retinal vein occlusion macular edema. Retina. 2019;39(10):1906–1916. doi: 10.1097/IAE.0000000000002264. [DOI] [PubMed] [Google Scholar]
- 21.Cheng D, Chen Q, Wu Y, Yu X, Shen M, Zhuang X, Tian Z, Yang Y, Wang J, Lu F, Shen L. Deep perifoveal vessel density as an indicator of capillary loss in high myopia. Eye (Lond) 2019;33(12):1961–1968. doi: 10.1038/s41433-019-0573-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Kang SH, Hong SW, Im SK, Lee SH, Ahn MD. Effect of myopia on the thickness of the retinal nerve fiber layer measured by cirrus HD optical coherence tomography. Invest Ophthalmol Vis Sci. 2010;51(8):4075. doi: 10.1167/iovs.09-4737. [DOI] [PubMed] [Google Scholar]
- 23.Bennett AG, Rudnicka AR, Edgar DF. Improvements on Littmann's method of determining the size of retinal features by fundus photography. Graefes Arch Clin Exp Ophthalmol. 1994;232(6):361–367. doi: 10.1007/BF00175988. [DOI] [PubMed] [Google Scholar]
- 24.Holladay JT. Proper method for calculating average visual acuity. J Refract Surg. 1997;13(4):388–391. doi: 10.3928/1081-597X-19970701-16. [DOI] [PubMed] [Google Scholar]
- 25.Demirel S, Değirmenci MFK, Bilici S, Yanik Ö, Batıoğlu F, Özmert E, Alp N. The recovery of microvascular status evaluated by optical coherence tomography angiography in patients after successful macular hole surgery. Ophthalmic Res. 2018;59(1):53–57. doi: 10.1159/000484092. [DOI] [PubMed] [Google Scholar]