Abstract
Purpose:
To compare the optical coherence tomography angiography (OCTA) findings of retinal microvasculature in anisometropic amblyopic eyes with fellow eyes.
Methods:
A comparative observational study was conducted in children with unilateral anisometropic amblyopia to compare the OCTA findings of retinal microvasculature between amblyopic and normal fellow eyes. Major outcome measures included superficial vessel density, deep vessel density, and foveal avascular zone (FAZ) parameters (area, perimetry, acircularity index) of amblyopic eye and fellow eye on OCTA.
Results:
The study involved 40 children with a mean age of 10.25 ± 3.07 years. Amblyopic eyes showed significantly reduced vessel density in the superficial and deep plexuses compared to fellow eyes (P < 0.05). Reductions were more pronounced in severe amblyopia, with significant foveal differences in superficial (P = 0.04) and deep layers (P = 0.02). A significant negative correlation was observed between best corrected visual acuity and vessel density.
Conclusion:
This study found reduced retinal vessel density in anisometropic amblyopic eyes, particularly in the superficial and deep capillary plexuses. Vessel density correlates with the severity of amblyopia, suggesting its potential as a biomarker for disease progression and severity.
Keywords: Amblyopia, anisometropic, biomarker, OCTA, retinal microcirculation, vessel density
Amblyopia, commonly known as “lazy eye,” is the leading cause of monocular vision loss in children and is characterized by reduced best corrected visual acuity (BCVA) in one eye due to abnormal visual input during the critical years of visual development.[1] If not identified and treated early, amblyopia can result in permanent vision loss and remains a major global health issue.[2,3] The pathophysiology of amblyopia involves the competition between the two eyes during the neural development of visual pathways. During the sensitive period, a visual imbalance due to one eye receiving poorer input can alter the neural response in the visual cortex, leading to poor development of visual functions.[4] The severity of amblyopia depends on the degree of visual asymmetry and the timing of its onset. Early intervention during the critical period, typically up to eight years of age, can significantly improve visual outcomes, but if left untreated, amblyopia becomes more resistant to treatment with age.[5,6]
Amblyopia is commonly categorized into three primary types: refractive, strabismic, and deprivational. Refractive amblyopia occurs when there is uncorrected refractive error, such as myopia, hypermetropia, or astigmatism, leading to poor visual development in one eye. Strabismic amblyopia arises from misalignment of the eyes (e.g., esotropia or exotropia), where the brain suppresses the misaligned eye to avoid double vision. Deprivational amblyopia results from conditions like cataracts or ptosis that obstruct vision in one eye. Among these, anisometropic amblyopia, caused by unequal refractive power between the eyes, is the second most common cause and often goes undetected because the eyes may appear normal.[7]
Amblyopia not only impairs visual acuity but also affects several aspects of spatial vision, such as contrast sensitivity, stereoacuity (depth perception), and contour detection. Patients with amblyopia may struggle with tasks requiring fine spatial vision, such as reading or detecting three-dimensional images. Binocular vision abnormalities, like limited depth perception, are particularly common in amblyopic individuals.
Optical coherence tomography angiography (OCTA) is an advanced, non-invasive imaging technique that allows detailed visualization of the retinal microvasculature.[8] By detecting movement in blood cells, OCTA can create angiographic images of retinal blood flow, which provides valuable insights into the functional aspects of blood vessels. It uses variations in the OCT signal to distinguish between static tissue and the moving red blood cells in retinal capillaries. This technique has been used extensively in studying macular changes in various eye diseases, including amblyopia, by assessing foveal thickness and retinal layer abnormalities.[9,10,11]
However, while the use of OCTA to explore macular changes in amblyopia has been well documented, there is limited research on the potential changes in retinal microcirculation, particularly in children with anisometropic amblyopia. This study aims to fill that gap by investigating retinal microcirculatory alterations in children with anisometropic amblyopia in comparison with healthy controls, providing insights that could further inform the management and treatment of this condition.
Methods
This comparative observational study was conducted at our eye hospital between June 2022 and December 2023. The institutional ethical committee approval was obtained before beginning the study, and informed consent was obtained from each patient according to the tenets of the Declaration of Helsinki. The study was registered in the Clinical Trials Registry, India (CTRI/2022/08/044578).
Children diagnosed with unilateral anisometropic amblyopia were included, while those with strabismus, deprivation amblyopia, ocular media opacities, or neurological disorders were excluded. After obtaining informed consent, participants underwent a detailed ophthalmic examination, including uncorrected visual acuity and BCVA (LogMAR), anterior segment evaluation using slit-lamp biomicroscopy, and fundus examination with +90D slit-lamp biomicroscopy. We classified mild amblyopia as BCVA between 6/9 and 6/12, moderate amblyopia as BCVA between 6/12 and 6/36, and severe amblyopia as BCVA worse than 6/36. OCTA imaging was performed using Swept Source OCT (DRI-OCT Atlantis, Topcon Corporation), assessing macular thickness, vessel density in the superficial and deep capillary plexus, and foveal avascular zone (FAZ) parameters. Image processing for vessel density analysis was carried out using MATLAB 2020a software, with deep vessel density estimated through binarization and adaptive thresholding techniques.
Sample size calculation
N = {(Zα + Zβ) 2/C2} +3
where C = 0.5 × ln (1 + r/1 − r), r = correlation coefficient – 0.51, Zα = 1.96 at 95% confidence level, Zβ =1.28 at 90% power
Using a 95% confidence level and 90% power, the sample size comes to be a minimum of 40.
Outcome measures
OCTA scan slabs were acquired in 3 × 3 mm and were analyzed with available methods and metrics. Patients whose images had inadequate signal strength, images containing lines or gaps, or motion artifacts were excluded. Superficial capillary plexus was automatically segmented by considering the inner surface as the internal limiting membrane layer and the outer surface as an approximation of the inner plexiform layer. Deep capillary plexus was also automatically segmented, considering the inner surface as the inner plexiform layer and the outer surface as an approximation of the outer plexiform layer. Vessel density was assessed by dividing it into the foveal zone and the parafoveal zone, which is further divided into temporal, nasal, superior, and inferior by the software. OCTA interpretations are then compared with the fellow eyes.
FAZ parameters were evaluated after selecting the icon that detects and outlines the area around the center of the scan with no flow signal and measures its area (mm2), perimeter (mm). Acircularity index (defined as the ratio of the perimeter of the FAZ to the perimeter of a circle with equal area) was also assessed. The scan used for viewing the macula is the Macular Cube 512 × 256 scan. This scan is used to measure macular thickness and create a 3D image of the data.
Statistical analysis
Data entry was made in the Microsoft Excel software in codes, and analysis was performed with Statistical Package for Social Sciences (SPSS-24, IBM software computer package). Categorical variables were expressed as frequencies and percentages. The test of normality was conducted using Kolmogorov-Smirnov and Shapiro-Wilk. Continuous variables were summarized with measures of central tendency (mean and standard deviation). The association between the categorical and continuous variables between the groups was assessed by the Chi-square test and the student “t” test, respectively. Comparisons were made between the amblyopic and fellow eyes to evaluate retinal microcirculatory changes. For all the tests of significance, a P value less than 0.05 was considered statistically significant.
Results
The study involved 40 participants with a mean age of 10.25 ± 3.07 years, and no significant difference in age was observed between the amblyopic and fellow eye groups (P = 1.00). The age distribution was primarily between 11 and 15 years (50%), followed by 6 and 10 years (40%) and 1 and 5 years (10%). Gender distribution was balanced, with 50% male and 50% female participants, and eye involvement was equally distributed between the left and right eyes, each affected in 50% of cases. Statistical analysis revealed no significant differences in age, gender, or eye involvement between the amblyopic and fellow eye groups (P > 0.05). The amblyopic eye had a mean BCVA of 0.531 ± 0.27, while the fellow eye had a mean BCVA of 0. The mean spherical equivalent was −3.25 ± 4.69 and −0.57 ± 1.23 in amblyopic and fellow eyes, respectively.
Table 1 shows the severity and type of amblyopia in the study population. Table 2 summarizes the structural metrics of amblyopic and fellow eyes, including central macular thickness, FAZ area, FAZ perimeter, and acircularity index.
Table 1.
Severity and type of amblyopia in the study population
| Category | Frequency (n) | Percentage (%) |
|---|---|---|
| Severity of amblyopia Mild Moderate Severe |
15 19 6 |
37.50 47.50 15.00 |
| Type of refractive error Astigmatism Hypermetropia Myopia |
14 8 18 |
35.00 20.00 45.00 |
Table 2.
Structural metrics of amblyopic and fellow eyes
| Parameter | Group | Minimum | Maximum | Mean±SD | P |
|---|---|---|---|---|---|
| Central macular thickness (μm) | Amblyopic eye | 254.1 | 262.4 | 257.77±2.80 | 0.83 |
| Fellow eye | 252.1 | 264.2 | 257.61±3.77 | ||
| FAZ area (mm2) | Amblyopic eye | 0.01 | 0.34 | 0.12±0.10 | 0.19 |
| Fellow eye | 0.01 | 1.31 | 0.18±0.27 | ||
| FAZ perimeter (mm) | Amblyopic eye | 0.3 | 3.29 | 1.59±0.86 | 0.86 |
| Fellow eye | 0.32 | 5.26 | 1.63±1.03 | ||
| Acircularity index | Amblyopic eye | 0.18 | 0.89 | 0.49±0.21 | <0.001 |
| Fellow eye | 0.06 | 0.61 | 0.31±0.12 |
FAZ: foveal avascular zone; SD: standard deviation
Significant differences in superficial vessel density were found between the amblyopic and fellow eyes in the whole retina (P = 0.02), parafovea (P < 0.001), nasal (P < 0.001), and temporal regions (P = 0.001). No significant differences were observed in the fovea, superior, or inferior regions. Table 3 shows the comparison of superficial vessel density between amblyopic and fellow eyes.
Table 3.
Comparison of superficial vessel density between amblyopic and fellow eyes
| Vessel density of superficial plexus | Eye | Minimum | Maximum | Mean±SD | P |
|---|---|---|---|---|---|
| Whole | Amblyopic eye | 43.10 | 49.10 | 45.12±1.89 | 0.021 |
| Fellow eye | 42.30 | 49.60 | 46.33±2.66 | ||
| Fovea | Amblyopic eye | 14.60 | 21.40 | 17.23±2.24 | 0.241 |
| Fellow eye | 14.70 | 21.50 | 17.85±2.46 | ||
| Parafovea | Amblyopic eye | 44.15 | 50.65 | 47.18±1.81 | <0.001 |
| Fellow eye | 43.45 | 52.58 | 48.96±2.32 | ||
| Superior | Amblyopic eye | 45.60 | 54.00 | 48.61±2.94 | 0.075 |
| Fellow eye | 44.10 | 54.20 | 49.87±3.31 | ||
| Nasal | Amblyopic eye | 42.20 | 50.00 | 46.45±1.97 | <0.001 |
| Fellow eye | 43.10 | 54.10 | 49.10±3.72 | ||
| Temporal | Amblyopic eye | 41.42 | 49.20 | 46.65±1.89 | 0.001 |
| Fellow eye | 41.70 | 54.10 | 48.99±3.67 | ||
| Inferior | Amblyopic eye | 43.10 | 52.30 | 47.02±2.96 | 0.288 |
| Fellow eye | 41.70 | 53.10 | 47.87±4.06 |
SD: standard deviation
Significant differences in deep vessel density were observed between the amblyopic and fellow eyes in the parafovea, nasal, and temporal regions (P < 0.001). No significant differences were found in the whole retina, fovea, superior, or inferior regions. Table 4 shows the comparison of deep vessel density between amblyopic and fellow eyes.
Table 4.
Comparison of deep vessel density between amblyopic and fellow eyes
| Vessel density of deep plexus | Eye | Minimum | Maximum | Mean±SD | P |
|---|---|---|---|---|---|
| Whole | Amblyopic eye | 52.20 | 57.80 | 54.78±1.67 | 0.385 |
| Fellow eye | 52.20 | 56.50 | 54.46±1.66 | ||
| Fovea | Amblyopic eye | 35.40 | 39.20 | 37.37±1.15 | 0.745 |
| Fellow eye | 35.10 | 39.50 | 37.28±1.43 | ||
| Parafovea | Amblyopic eye | 48.63 | 50.73 | 49.79±0.55 | <0.001 |
| Fellow eye | 48.78 | 52.48 | 50.95±0.87 | ||
| Superior | Amblyopic eye | 50.60 | 54.10 | 52.42±1.12 | 0.730 |
| Fellow eye | 50.80 | 54.10 | 52.50±1.01 | ||
| Nasal | Amblyopic eye | 47.10 | 50.20 | 48.94±0.73 | <0.001 |
| Fellow eye | 47.80 | 54.10 | 51.92±1.66 | ||
| Temporal | Amblyopic eye | 46.70 | 50.20 | 48.83±0.75 | <0.001 |
| Fellow eye | 47.80 | 54.10 | 49.98±1.62 | ||
| Inferior | Amblyopic eye | 47.60 | 50.60 | 48.97±0.95 | 0.064 |
| Fellow eye | 47.80 | 50.90 | 49.39±1.07 |
SD: standard deviation
In the foveal region, superficial vessel density was significantly higher in severe amblyopia (18.366 ± 2.983) compared to moderate (16.315 ± 1.640) and mild amblyopia (17.940 ± 2.257, P = 0.040). Similarly, the deep vessel density in the fovea was highest in moderate amblyopia (37.894 ± 1.161) and showed significant differences (P = 0.020). However, no significant differences in vessel density were observed in other regions or with refractive error types, indicating that vascular changes in amblyopia are localized to the fovea and independent of refractive error.
A significant negative correlation was observed between BCVA and superficial vessel density in the whole, parafovea, nasal, and temporal areas [Fig. 1]. This indicates that as visual acuity worsens, the superficial vessel density decreases across these regions. A significant negative correlation was identified between BCVA and deep vessel density in the parafovea, nasal, and temporal areas [Fig. 2]. This suggests a similar pattern where worsening visual acuity corresponds to reduced deep vessel density in these areas.
Figure 1.
Correlation between BCVA and superficial vessel density in various regions: (a) whole vessel density, (b) parafoveal vessel density, (c) nasal vessel density, (d) temporal vessel density, (e) inferior vessel density, (f) foveal vessel density, and (g) superior vessel density of the superficial plexus. BCVA: best corrected visual acuity
Figure 2.
Correlation between BCVA and vessel density of deep plexus in various regions: (a) whole vessel density, (b) parafoveal vessel density, (c) nasal vessel density, (d) temporal vessel density, (e) inferior vessel density, (f) foveal vessel density, and (g) superior vessel density of the superficial plexus. BCVA: best corrected visual acuity
Discussion
The findings of the present study hypothesize that reduced retinal vessel density in superficial and deep capillary plexuses might be the consequence of underlying amblyopia. The vessel density correlates with amblyopia severity, suggesting its potential as a biomarker for disease progression and severity.
Regarding FAZ parameters, our study found that only the acircularity index was significantly higher in amblyopic eyes compared to fellow eyes, suggesting decreased blood supply to the FAZ in amblyopic eyes. This finding contrasts with the results of Doğuizi et al.,[12] who found no significant differences in FAZ area, acircularity index, or perimeter values between amblyopic and fellow eyes. Additionally, other studies, such as those by Rao et al.,[13] found that the FAZ area and perimeter of hypermetropic ametropic amblyopia eyes were expanded compared to control eyes. These discrepancies could be attributed to variations in measuring instruments used in the studies and differences in the type and severity of amblyopia.
In our study, macular thickness was found to be comparable between amblyopic eyes (257.77 ± 2.808 µm) and fellow eyes (257.61 ± 3.772 µm), which is consistent with the findings of Rao et al.,[13] who reported no significant differences in central macular thickness, macular volume, or early treatment diabetic retinopathy study ring thicknesses in hyperopic ametropic amblyopia eyes compared to control eyes. However, some studies, such as those by Nishikawa et al.[14] and Liu et al.,[15] reported thicker macular retinal thickness in amblyopic eyes compared to control eyes. Rajavi et al.[16] also found significant increases in macular thickness in moderately to severely amblyopic eyes. These inconsistencies could arise from differences in age, sex, and amblyopia types among the study populations.
OCTA analysis revealed that amblyopic eyes exhibited significantly lower vessel density in both the superficial and deep capillary plexuses, particularly in the parafoveal, nasal, and temporal regions, compared to fellow eyes. These results are consistent with previous studies, which found lower vascular density in certain areas of the superficial and deep capillary plexuses in amblyopic eyes.[9,12,14] Conversely, a study by Hamurcu et al.[17] found significant differences only in the superficial capillary plexus vessel density in whole and parafoveal regions, while Cinar et al.[18] did not find significant differences in vessel density between amblyopic and control groups. The discrepancies could be attributed to differences in the OCTA software used or variations in the demographic profiles of participants.
Our findings suggest that the deep capillary plexus is more vulnerable to hypoxic retinal injury due to its distal location from the retinal arterial and choroidal circulations, coupled with higher metabolic demand. The decreased vessel density in amblyopic eyes may be related to abnormal retinal development secondary to inadequate visual experience. While animal models have not shown evidence of this hypothesis, further studies are required to explore this phenomenon. In addition, we observed that the nasal and temporal quadrants of both the superficial and deep vascular layers were predominantly affected in amblyopic eyes. Previous studies by Li et al.[19] and Doğuizi et al.[12] also demonstrated vascular deterioration in myopic and hyperopic eyes, respectively, with regional variations in the macular microcirculation.
We also found a negative correlation between BCVA and vessel density in the parafoveal and nasal deep capillary plexus regions, in line with Doğuizi et al.’s[12] study, which reported a similar negative correlation between BCVA and vascular density in various regions of the fovea and parafovea. Interestingly, our study found a higher prevalence of myopic anisometropia in our sample, but we did not observe a significant correlation between vessel density and the type of refractive error. This contrasts with the study by Lonngi et al.,[9] who reported a significant reduction in vessel density in hyperopic amblyopia. Similarly, studies by Doğuizi et al.[12] and Rao et al.[13] also found significant reductions in vessel density in hyperopic anisometropes. These variations may be explained by differences in sample size or refractive error distribution.
Regarding the relationship between vessel density and the severity of amblyopia, our study found that vessel density in both the superficial and deep vascular layers of the foveal region showed significant differences with the severity of amblyopia. This suggests a correlation between vessel density changes and the severity of amblyopia. However, further studies with larger sample sizes are required to better understand this relationship. Table 5 shows the outline of multiple studies comparing OCTA parameters in different types of amblyopia.
Table 5.
Major studies comparing optical coherence tomography angiography parameters in various types of amblyopia and our findings
| Authors | Type of amblyopia (number of eyes in amblyopic group) | Study results | Our findings |
|---|---|---|---|
| Doğuizi et al.[12] | Hyperopic anisometropic amblyopia (40 eyes) | No significant difference in FAZ parameters; superficial and deep capillary plexus vessel density decreased | FAZ area and central macular thickness were comparable in amblyopic and control eyes; FAZ acircularity index increased; superficial and deep capillary plexus vessel density decreased in the temporal and nasal quadrants of the parafoveal regions |
| Rao et al.[13] | Hyperopic ametropic amblyopia (72 eyes) | FAZ area and perimeter of hypermetropic, ametropic amblyopia eyes were expanded | |
| Sobral et al.[20] | Unilateral strabismic or anisometropic amblyopia (26 eyes) | FAZ area and perimeter of hypermetropic ametropic, and amblyopia eyes were expanded | |
| Lonngi et al.[9] | Strabismic and anisometropic amblyopia (13 eyes) | No significant difference in the FAZ or foveal thickness; superficial and deep capillary plexus vessel density decreased | |
| Nishikawa et al.[14] | Unilateral anisometropia and anisometropia combined with strabismus (22 eyes) | Amblyopic eyes had significantly smaller FAZ area than fellow eyes; superficial and decreased deep capillary plexus vessel density and increased central macular thickness | |
| Cinar et al.[18] | Anisometropic amblyopia (37 eyes) | No significant decrease in vessel density | |
| Chen et al.[21] | Anisometropic amblyopia, strabismic, and bilateral amblyopia (52 anisometropic amblyopia, 16 strabismic and 17 bilateral amblyopia) | Foveal and parafoveal macular vessel density in the superficial capillary plexus was lower in amblyopic eyes; vessel density in anisometropic amblyopia differed the most from controls compared to strabismic and bilateral amblyopia | |
| Ye et al.[22] | Anisometropic amblyopia (27 eyes) |
FAZ size of the amblyopic eyes was larger; the vessel density indices in superficial and deep capillary plexus were lower in amblyopic eyes without a statistical difference. | |
| Karabulut et al.[23] | Strabismic, ametropic, anisometropic, and meridional amblyopia (23 eyes) |
Central macular thickness increased in the amblyopic group; vessel density in both the superficial and deep retinal plexus was significantly lower in amblyopic eyes in all quadrants except the fovea; among different types of amblyopia subgroups, anisometropic amblyopes had significantly higher vessel density at all regions except the fovea | |
| Hamurcu et al.[17] | Unilateral anisometropic amblyopia (18 eyes) | Significant differences were found only in superficial capillary plexus vessel density | |
| Liu et al.[15] | Anisometropic amblyopia (16 eyes) | Central macular thickness increased in amblyopic eyes | |
| Errera et al.[24] | Unilateral strabismic or anisometropic amblyopia or residual amblyopia from early congenital cataract surgery (32 eyes) | Vessel density and perfusion density in the superficial capillary plexus were significantly lower in amblyopic eyes compared to control eyes; the microvascular changes correlated with visual acuity and appeared to be reversible with treatment of amblyopia | |
| Yilmaz et al.[25] | Strabismic amblyopia (15 eyes) | Vessel density of superficial and deep capillary plexus of eyes with amblyopia was lower than that of the companion eye and the age-matched controls; FAZ area was comparable in both groups. | |
| Wong et al.[26] | Strabismic and anisometropic amblyopia (30 eyes) | No difference in FAZ area and vessel density; FAZ circularity was decreased in amblyopic eyes | |
| Araki et al.[27] | Unilateral anisometropic amblyopia with or without strabismus (15 eyes) | FAZ area of superficial capillary plexus was smaller in the amblyopic eyes; no significant difference in the macular vessel density | |
| Pujari et al.[28] | Strabismic amblyopia (10 eyes) | Superficial vascular plexus density centered at the fovea of amblyopic eyes was similar to that of normal eyes |
FAZ: foveal avascular zone
The strength of the study includes the larger sample size compared to the existing studies conducted in the Indian population. The study has some limitations. Eyes with poorer vision might have been more likely to be excluded, due to inadequate scan quality resulting from the inability to fixate well during OCTA acquisition. Vessel density of anisometropes without amblyopia was not compared with the amblyopic group, which would have given a better understanding regarding the hypothesis of the study. The vessel density of choriocapillaris was not studied, which can also show significant changes in amblyopic eyes.
Conclusion
Anisometropic amblyopic eyes exhibit a significant reduction in both superficial and deep vessel density compared to healthy fellow eyes. This suggests that retinal microcirculation may be adversely affected by amblyopia, and vessel density could potentially serve as an indicator of amblyopia severity.
Conflicts of interest:
There are no conflicts of interest.
Funding Statement
Nil.
References
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