Abstract
Background
The purpose of the present study was to evaluate the choroidal characteristics in anisometropic amblyopia.
Methods
This prospective study included individuals with myopic (n = 20) and hyperopic anisometropic amblyopia (n = 30), with their respective fellow eyes and age-matched control eyes. Total choroidal area (TCA), luminal choroidal area (LCA), stromal choroidal area, and choroidal vascularity index (CVI) were calculated in the subfoveal region. Choriocapillaris vessel density (VD) in macular and peripapillary regions was assessed using optical coherence tomography angiography.
Results
The study involved 50 participants with anisometropic amblyopia (mean age 28.44 ± 14.73 years) and 50 age-matched controls. Hyperopic amblyopic eyes had significantly wider LCAs than fellow eyes (p = 0.035) and control eyes (p = 0.048), while the opposite was observed in myopic eyes (p = 0.004 compared to fellow eyes; p = 0.032 compared to control eyes). The CVI showed no significant differences between amblyopic and fellow eyes or between amblyopic and control eyes in both hyperopic and myopic groups (p > 0.05 for both). However, the myopic group exhibited significantly narrower TCA (p = 0.036) and LCA (p = 0.008) than the hyperopic group. Hyperopic eyes demonstrated lower inferior peripapillary VD and higher nasal peripapillary VD compared to fellow eyes (p = 0.007 for both) and control eyes (p = 0.023 and p = 0.014, respectively), with myopic eyes showing no significant inter-eye differences (p > 0.05 for both). Myopic amblyopic eyes had higher inferior peripapillary VD than hyperopic eyes (p = 0.018).
Conclusion
The CVI and macular VD values showed no significant differences between amblyopic and fellow eyes in both groups. However, a difference was observed in peripapillary VDs. This suggests that the peripapillary region may be affected earlier than the macular region in anisometropic amblyopia.
Keywords: Amblyopia, Anisometropia, Choroidal vascularity index, Enhanced‑depth imaging, Optical coherence tomography
Background
Anisometropic amblyopia is a subtype of amblyopia that arises due to a significant refractive difference between the two eyes, leading to chronic monocular blur and subsequent suppression of the image from the defocused eye in binocular vision processing. Although amblyopia is defined as a functional visual impairment without any identifiable structural abnormality, previous studies have reported subtle biometric, retinal, and choroidal alterations in amblyopic eyes [1, 2].
The choroid is pivotal in the pathophysiology of a range of ocular diseases. Efforts to understand the angioarchitecture of the choroid using in vitro methods, such as histology, and microscopy, have been limited in clarifying its vascular structure. Advances in imaging now provide greater insights, with growing research linking choroidal anatomy to various diseases [3]. Optical coherence tomography angiography (OCT-A) is a non-invasive imaging technique that enables visualization of the retinal and choroidal microvasculature without the need for contrast agents. However, its utility is limited in evaluating the deeper layers of the choroid, as it does not provide visualization of the deep choroidal veins [4, 5]. On the other hand, enhanced depth imaging optical coherence tomography (EDI-OCT) holds a significant place in imaging all layers of the choroid. However, like OCT-A, this technique does not directly visualize the deep choroidal veins. Consequently, to assess the overall choroidal vascular status, a parameter derived from the hyporeflective (lumen) and hyperreflective (stroma) areas in the OCT cross-section is used to evaluate the choroidal vascular structures. This parameter is referred to as the choroidal vascularity index (CVI) [6]. The CVI first introduced by Agrawal et al. [7], enables detailed analysis of choroidal vascularization. This technique was developed to specify which part of the choroid is being addressed, to distinguish between the stromal and vascular components of the choroid, as well as to account for the variability inherent in choroidal thickness (CT) measurements [8, 9].
Previous studies revealed that hyperopic anisometropic amblyopic eyes tend to have greater CT than normal eyes [10, 11]. However, most studies have focused on CT alone, providing minimal insight into the architecture of the choroid. A more detailed evaluation of the choroid may assist in better understanding its involvement in the development of amblyopia [12]. Regarding the OCT-A findings in patients with amblyopia, Huang et al. [13] reported that, after adjusting for age, axial length (AL), and spherical equivalents, the vessel density of the superficial capillary plexus (SCP) and deep capillary plexus (DCP) in the whole macula was significantly lower in the amblyopic group compared to the control group. Similarly, Liu et al. [14] found that the macular vessel density of the SCP is lower in anisometropic amblyopic children than in age-matched healthy children. When analyzing the CVI in patients with amblyopia, Oren et al. [15] reported that the amblyopic eyes of patients with anisometropic hypermetropia had larger luminal choroidal area (LCA), CVI, and CT values compared to the fellow eye and control groups. Hui et al. [16] and Guler Alis et al. [17] found lower CVI values in hyperopic anisometropic amblyopic eyes compared to control eyes. To the best of our knowledge, no previous study has directly compared the CVI between myopic and hyperopic anisometropic amblyopic eyes, nor investigated the potential correlation between CVI and OCT-A parameters.
Therefore, this study aimed to address this gap in the literature by comparing the CVI in hyperopic and myopic anisometropic amblyopic eyes with their healthy fellow eyes, age-matched non-amblyopic control eyes, and with each other using OCT. Additionally, the study evaluated the choriocapillaris with OCT-A and investigated potential correlations between OCT-A parameters and CVI to provide a more comprehensive understanding of choroidal vascular changes in anisometropic amblyopia.
Methods
This prospective study assessed the morphological characteristics of the choroid in patients with unilateral anisometropic amblyopia who presented to a tertiary ophthalmology center between January 2023 and July 2024, incorporating an age-matched non-amblyopic control group for comparative analysis. The control group was additionally matched for refractive status, ensuring that hyperopic amblyopic patients were compared with age-matched non-amblyopic hyperopes and myopic amblyopic patients with age-matched non-amblyopic myopes. Ethical approval was granted by the institutional ethics committee (Decision No: 2023/20 − 16; Date:14.06.2023), and informed consent was obtained from all participants or their legal guardians. All study procedures were conducted in adherence to the principles outlined in the Declaration of Helsinki.
Anisometropia was defined as a refractive difference exceeding 1.00 diopters (D) in spherical equivalent or astigmatism between the two eyes [18]. Anisometropic amblyopia was characterized by a reduction of at least two lines in the best-corrected visual acuity (BCVA) of the affected eye, solely attributable to anisometropia and without any other abnormalities identified on clinical examination. Patients and their respective eyes were categorized into two groups: myopic anisometropic amblyopia and hyperopic anisometropic amblyopia. Comparative analyses were conducted across the two groups, as well as between the amblyopic eyes, their fellow eyes, and the age-matched non-amblyopic control eyes.
Participants were eligible for inclusion if they were between 6 and 60 years of age, of any gender, with a diagnosis of anisometropic amblyopia and BCVA of ≥ 20/25 in the fellow eye. The age threshold of 6 years was based on the assumption that refractive status and ocular parameters have generally reached adult-like levels by this age [19, 20]. Exclusion criteria included the presence of organic eye diseases, pathological myopia, bilateral amblyopia, manifest strabismus, eccentric fixation, coexisting nystagmus, prior ocular surgery, trauma, laser treatment, premature birth, neurological conditions, or systemic diseases impacting the retina and choroidal vasculature (e.g., diabetes). Patients with other ocular disorders, including age-related macular degeneration, glaucoma, and lenticular or corneal pathologies, were also excluded. For those with myopic anisometropic amblyopia, additional exclusions applied if retinal changes, such as Bruch membrane rupture or choroidal neovascularization, could interfere with the quality of OCT imaging. None of the adult participants had undergone patching treatment in childhood and had only received refractive correction. Children were included if they were newly diagnosed with amblyopia at the time of evaluation and had not received any previous treatment. For the control group, age-matched non-amblyopic individuals with a BCVA of 20/20 or better in both eyes, a spherical equivalent between − 2.00 D and + 2.00 D, and no history of anisometropia, strabismus, ocular surgery, or systemic diseases affecting the retina or choroidal vasculature were included.
Demographic data were initially recorded for each participant, followed by a comprehensive ophthalmologic assessment. This included assessment of BCVA using the Snellen chart, slit-lamp biomicroscopy (Zeiss, Oberkochen, Germany), orthoptic evaluation (including Hirschberg and cover tests, as well as extraocular movement assessment), intraocular pressure measurement with Goldmann applanation tonometry, fundus examination, and retinal and choroidal multimodal imaging.
Non-cycloplegic refractive error was measured using the Nidek autorefractor-keratometer (RKT-7700, NIDEK Co., Ltd., Gamagori, Japan). Before determining the BCVA for each eye, manifest refraction was performed using a Snellen chart (Auto Chart Projector CP 670; Nidek Co., Ltd., Gamagori, Japan) at 20 feet. Cyclopentolate hydrochloride (1%) (Sikloplejin; Abdi İbrahim, İstanbul, Turkey) was administered to all eyes three times at 5-minute intervals, followed by repeat autorefraction after 30 min to determine the cycloplegic refractive error. Spherical equivalent (SE) was calculated as spherical refractive error + (0.5 × cylindrical refractive error) and logMAR equivalents of the Snellen BCVAs were recorded for further analysis. Axial length was evaluated using non-contact partial coherence laser interferometry (IOL Master®, Carl Zeiss Meditec AG, Jena, Germany).
Spectral-domain OCT imaging was performed with the Spectralis OCT (Heidelberg Engineering, Heidelberg, Germany). For each eye, a horizontal 7 mm line scan centered on the fovea was obtained for further analysis. Central macular thickness (CMT) was measured as the closest distance between the internal limiting membrane and Bruch’s membrane using the caliper measurement, a tool belonging to the Spectralis OCT system. Enhanced depth imaging mode was utilized on the Heidelberg Spectralis® OCT (Heidelberg Engineering). The choroidoscleral interface was defined as the outer border of the choroidal stroma, with all measurements made relative to this interface. Subfoveal CT was measured from Bruch’s membrane to the choroidoscleral interface using a caliper function. The structural features of the 1500 μm-wide nasal-to-temporal subfoveal choroidal region were evaluated using the method described by Agrawal et al. [3]. A public domain software, ImageJ (developed by Wayne Rasband, MD; National Institutes of Health, Bethesda) was used for image binarization [21]. The image was processed by converting it to 8-bit and selecting the choroidal area, which was added to the region of interest (ROI) Manager. Niblack auto-local thresholding and color thresholding were applied to the image, and the resulting areas were combined using the “AND” operation in the ROI Manager. The total choroidal area (TCA) and LCA were measured, and CVI was calculated as (LCA / TCA) × 100, with the stromal choroidal area (SCA) determined by subtracting LCA from TCA. To test the inter-observer reproducibility, the CMT, subfoveal CT, TCA, LCA, SCA, and CVI measurements were performed by three independent masked researchers (S.K., M.K., and C.D.E.). The measurements of the three researchers were averaged and were used in the analysis.
Optical coherence tomography angiography images were acquired using the angio retina scanning mode of the device. The scanning area used in this study was 6 mm × 6 mm, centered on the fovea and optic disc. The choriocapillaris was segmented from Bruch’s membrane to a depth of 10.4 μm beneath it. Vessel density data of the choriocapillaris were automatically provided and recorded within a central 1 mm diameter area from images centered on the fovea, as well as in areas 1 mm superior, nasal, inferior, and temporal to its outermost boundary from images centered on both the fovea and the optic disc [22]. Scans with a signal strength index below 40 or containing motion artifacts and segmentation errors were excluded, and image quality was assessed by two readers (S.K. and M.K.).
The same examination procedures were performed on both amblyopic and fellow eyes by the same physician, conducted at the same time of day while patients were fasting to minimize diurnal variations in line with previous studies [23, 24]. Given that the hyperopic and myopic groups in the study had disparate ALs, magnification correction was applied to OCT and OCT-A measurements using Bennett’s formula to mitigate the effect of AL on the measurements [25].
Statistical analysis
A power analysis based on previous studies on OCT-A parameters and CVI in amblyopic and healthy eyes was conducted using G*Power 3.1.3 (Franz Faul, University of Kiel, Germany) with a two-tailed test, an alpha level of 0.05, and 80% power. The analysis determined that at least 34 eyes per group were required to detect a statistically significant difference. To account for potential dropouts and the broad age distribution, 50 eyes per group were recruited, yielding a total of 150 eyes.
Statistical analyses were performed using SPSS Statistics version 28 (IBM, Armonk, NY, USA). Descriptive statistics were used to summarize the data, with categorical variables expressed as frequencies and percentages, and continuous variables reported as means ± standard deviations. Data normality was evaluated using the Shapiro–Wilk test. The paired samples t-test and Wilcoxon signed-rank test were utilized to compare parameters between amblyopic and fellow eyes within the myopic and hyperopic anisometropic groups. For comparisons with healthy control group, independent samples t-test and Mann-Whitney U test were used. To account for the potential effect of age on choroid, ANCOVA was performed with age as a covariate in comparisons between hyperopic and myopic amblyopic eyes and pairwise comparisons were adjusted using Bonferroni correction. Categorical variables were analyzed using the chi-square test. The intraclass correlation coefficients (ICC) were determined by a two-way mixed effect for observer reliability. To assess the relationship between the scales, Spearman’s correlation was used. To account for multiple correlation analyses, significance levels were adjusted using Bonferroni correction. Statistical significance was set at p < 0.05.
Results
The study population consisted of 50 participants with anisometropic amblyopia, including 15 males (30%) and 35 females (70%), with a mean age of 28.44 ± 14.73 years (range: 6–60 years), along with 50 age-matched non-amblyopic controls. In the amblyopia group, the right eye was affected in 22 participants (44%) and the left eye in 28 (56%). There were no significant differences among the myopic, hyperopic, and control groups in terms of mean age (p = 0.472) or gender distribution (p = 0.805) (Table 1).
Table 1.
Demographic features of the study groups
| Hyperopic Group | Myopic Group | Control Group | p value | |
|---|---|---|---|---|
| Number of patients / eyes, n | 30 / 60 | 20 / 40 | 50 / 50 | − |
| Age, years ± standard deviation | 26.23 ± 12.23 | 31.75 ± 15.20 | 28.99 ± 12.91 | 0.472a |
| Gender, M / F | 9 / 21 | 6 / 14 | 18 / 32 | 0.805b |
| Amblyopic eye, R / L | 11 / 19 | 11 / 9 | - | 0.323b |
F, female; L, left; M, male; R, right
a ANOVA test
b Chi-square test
In both the hyperopic and myopic groups, amblyopic eyes showed significantly worse BCVA and higher absolute SE values compared to their fellow eyes and control eyes (p < 0.001 for all comparisons, except SE in myopic amblyopic vs. control eyes, p = 0.009) (Tables 2 and 3). No significant BCVA difference was found between hyperopic and myopic amblyopic eyes (p = 0.153), though SE differed significantly (p < 0.001) (Table 4).
Table 2.
Comparison of clinical and imaging parameters between amblyopic, fellow and control eyes in hyperopic group
| Parameter, mean ± standard deviation | Hyperopic Group | |||||
|---|---|---|---|---|---|---|
| Amblyopic Eyes | Fellow Eyes | Control Eyes | p1 value (Amblyopic vs. Fellow) | P2 value (Amblyopic vs. Control) | P3 value (Fellow vs. Control) | |
| Best corrected visual acuity, logMAR | 0.45 ± 0.31 | 0.02 ± 0.04 | 0.02 ± 0.03 | <0.001 a | <0.001 b | 0.642c |
| Spherical equivalent, diopters | +4.07 ± 2.03 | +1.44 ± 1.66 | +1.20 ± 0.80 | <0.001 a | <0.001 b | 0.815c |
| Axial length, mm | 22.05 ± 0.94 | 22.76 ± 0.75 | 22.57 ± 0.68 | <0.001 d | 0.004 c | 0.734c |
| Central macular thickness, μm | 222.83 ± 14.66 | 221.73 ± 14.87 | 222.18 ± 14.45 | 0.544a | 0.654b | 0.758b |
| Subfoveal choroidal thickness, μm | 363.80 ± 106.95 | 337.23 ± 105.99 | 334.04 ± 101.84 | 0.077d | 0.068c | 0.689c |
| Choroidal area | ||||||
| Total, μm2 | 1717601.94 ± 528402.53 | 1537688.87 ± 490917.43 | 1567899.98 ± 490917.43 | 0.084d | 0.090c | 0.792c |
| Luminal, μm2 | 1067082.44 ± 265282.33 | 984534.77 ± 276684.07 | 1005548.77 ± 276684.07 | 0.035 d | 0.048 c | 0.713c |
| Stromal, μm2 | 650519.50 ± 271149.078 | 553154.10 ± 224281.84 | 562351.21 ± 224281.84 | 0.060d | 0.059c | 0.674c |
| Choroidal vascular index, % | 63.46 ± 5.61 | 64.85 ± 4.21 | 64.14± 4.32 | 0.082a | 0.092b | 0.801c |
| Choriocapillaris vascular density, % | ||||||
| Macular | ||||||
| Superior parafoveal | 51.27 ± 3.13 | 52.64 ± 3.20 | 52.76 ± 3.14 | 0.098a | 0.104b | 0.612c |
| Temporal parafoveal | 52.20 ± 5.25 | 53.16 ± 3.30 | 52.96 ± 3.20 | 0.344a | 0.287b | 0.743b |
| Inferior parafoveal | 52.88 ± 3.58 | 53.28 ± 2.65 | 53.26 ± 2.98 | 0.610d | 0.589c | 0.682c |
| Nasal parafoveal | 52.17 ± 3.00 | 51.93 ± 4.16 | 51.12 ± 3.46 | 0.773a | 0.658b | 0.771c |
| Foveal | 48.15 ± 12.19 | 49.06 ± 12.35 | 49.24 ± 12.50 | 0.504a | 0.420b | 0.548b |
| Peripapillary | ||||||
| Superior peripapillary | 55.48 ± 7.50 | 56.11 ± 4.73 | 57.01 ± 5.89 | 0.703d | 0.432c | 0.789c |
| Temporal peripapillary | 61.96 ± 10.14 | 61.90 ± 9.65 | 62.10 ± 9.85 | 0.974a | 0.785b | 0.801b |
| Inferior peripapillary | 51.80 ± 9.16 | 52.27 ± 9.09 | 52.19 ± 9.12 | 0.007 d | 0.023 c | 0.675c |
| Nasal peripapillary | 66.37 ± 7.01 | 62.32 ± 8.98 | 63.42 ± 8.90 | 0.007 a | 0.014 b | 0.702c |
a Wilcoxon signed rank test
b Mann-Whitney U test
c Independent samples t test
d Paired samples t-test
Table 3.
Comparison of clinical and imaging parameters between amblyopic, fellow and control eyes in myopic group
| Parameter, mean ± standard deviation | Hyperopic Group | |||||
|---|---|---|---|---|---|---|
| Amblyopic Eyes | Fellow Eyes | Control Eyes | p1 value (Amblyopic vs. Fellow) | P2 value (Amblyopic vs. Control) | P3 value (Fellow vs. Control) | |
| Best corrected visual acuity, logMAR | 0.45 ± 0.31 | 0.02 ± 0.04 | 0.02 ± 0.03 | <0.001 a | <0.001 b | 0.642c |
| Spherical equivalent, diopters | +4.07 ± 2.03 | +1.44 ± 1.66 | +1.20 ± 0.80 | <0.001 a | <0.001 b | 0.815c |
| Axial length, mm | 22.05 ± 0.94 | 22.76 ± 0.75 | 22.57 ± 0.68 | <0.001 d | 0.004 c | 0.734c |
| Central macular thickness, μm | 222.83 ± 14.66 | 221.73 ± 14.87 | 222.18 ± 14.45 | 0.544a | 0.654b | 0.758b |
| Subfoveal choroidal thickness, μm | 363.80 ± 106.95 | 337.23 ± 105.99 | 334.04 ± 101.84 | 0.077d | 0.068c | 0.689c |
| Choroidal area | ||||||
| Total, μm2 | 1717601.94 ± 528402.53 | 1537688.87 ± 490917.43 | 1567899.98 ± 490917.43 | 0.084d | 0.090c | 0.792c |
| Luminal, μm2 | 1067082.44 ± 265282.33 | 984534.77 ± 276684.07 | 1005548.77 ± 276684.07 | 0.035 d | 0.048 c | 0.713c |
| Stromal, μm2 | 650519.50 ± 271149.078 | 553154.10 ± 224281.84 | 562351.21 ± 224281.84 | 0.060d | 0.059c | 0.674c |
| Choroidal vascular index, % | 63.46 ± 5.61 | 64.85 ± 4.21 | 64.14± 4.32 | 0.082a | 0.092b | 0.801c |
| Choriocapillaris vascular density, % | ||||||
| Macular | ||||||
| Superior parafoveal | 51.27 ± 3.13 | 52.64 ± 3.20 | 52.76 ± 3.14 | 0.098a | 0.104b | 0.612c |
| Temporal parafoveal | 52.20 ± 5.25 | 53.16 ± 3.30 | 52.96 ± 3.20 | 0.344a | 0.287b | 0.743b |
| Inferior parafoveal | 52.88 ± 3.58 | 53.28 ± 2.65 | 53.26 ± 2.98 | 0.610d | 0.589c | 0.682c |
| Nasal parafoveal | 52.17 ± 3.00 | 51.93 ± 4.16 | 51.12 ± 3.46 | 0.773a | 0.658b | 0.771c |
| Foveal | 48.15 ± 12.19 | 49.06 ± 12.35 | 49.24 ± 12.50 | 0.504a | 0.420b | 0.548b |
| Peripapillary | ||||||
| Superior peripapillary | 55.48 ± 7.50 | 56.11 ± 4.73 | 57.01 ± 5.89 | 0.703d | 0.432c | 0.789c |
| Temporal peripapillary | 61.96 ± 10.14 | 61.90 ± 9.65 | 62.10 ± 9.85 | 0.974a | 0.785b | 0.801b |
| Inferior peripapillary | 51.80 ± 9.16 | 52.27 ± 9.09 | 52.19 ± 9.12 | 0.007 d | 0.023 c | 0.675c |
| Nasal peripapillary | 66.37 ± 7.01 | 62.32 ± 8.98 | 63.42 ± 8.90 | 0.007 a | 0.014 b | 0.702c |
a Wilcoxon signed rank test
b Mann-Whitney U test
c Independent samples t-test
d Paired samples t-test
Table 4.
Comparison of clinical and imaging parameters between hyperopic and myopic amblyopic eyes
| Parameter, mean ± standard deviation | Amblyopic Eyes | ||
|---|---|---|---|
| Hyperopic | Myopic | p value* | |
| Best corrected visual acuity, logMAR | 0.45 ± 0.31 | 0.63 ± 0.41 | 0.153 |
| Spherical equivalent, diopters | +4.07 ± 2.03 | -3.44 ± 3.32 | <0.001 |
| Axial length, mm | 22.05 ± 0.94 | 24.07 ± 1.23 | <0.001 |
| Central macular thickness, μm | 222.83 ± 14.66 | 233.85 ± 25.72 | 0.042 |
| Subfoveal choroidal thickness, μm | 363.80 ± 106.95 | 346.65 ± 128.77 | 0.32 |
| Choroidal area | |||
| Total, μm2 | 1717601.94 ± 528402.53 | 1383346.61 ± 568160.06 | 0.036 |
| Luminal, μm2 | 1067082.44 ± 265282.33 | 835069.40 ± 296734.43 | 0.008 |
| Stromal, μm2 | 650519.50 ± 271149.078 | 548277.22 ± 286503.29 | 0.155 |
| Choroidal vascular index, % | 63.46 ± 5.61 | 61.74 ± 5.89 | 0.473 |
| Choriocapillaris vascular density, % | |||
| Macular | |||
| Superior parafoveal | 51.27 ± 3.13 | 52.01 ± 4.25 | 0.106 |
| Temporal parafoveal | 52.20 ± 5.25 | 51.39 ± 4.06 | 0.182 |
| Inferior parafoveal | 52.88 ± 3.58 | 52.69 ± 3.79 | 0.769 |
| Nasal parafoveal | 52.17 ± 3.00 | 50.55 ± 4.97 | 0.573 |
| Foveal | 48.15 ± 12.19 | 46.33 ± 12.22 | 0.601 |
| Peripapillary | |||
| Superior peripapillary | 55.48 ± 7.50 | 57.37 ± 5.52 | 0.362 |
| Temporal peripapillary | 61.96 ± 10.14 | 58.20 ± 8.74 | 0.073 |
| Inferior peripapillary | 51.80 ± 9.16 | 57.33 ± 5.25 | 0.018 |
| Nasal peripapillary | 66.37 ± 7.01 | 61.30 ± 9.71 | 0.096 |
* Comparison of hyperopic amblyopic eyes and myopic amblyopic eyes. ANCOVA analysis was performed with age as a covariate and posthoc Bonferroni correction was applied
Axial length measurements reflected the refractive error profiles: hyperopic amblyopic eyes had significantly shorter AL compared to fellow eyes (p < 0.001), control eyes (p = 0.004), and myopic amblyopic eyes (p < 0.001). Conversely, in the myopic group, amblyopic eyes had significantly longer AL than both fellow (p = 0.005) and control eyes (p = 0.010) (Tables 2, 3 and 4). Fellow and control eyes did not differ significantly in BCVA, SE, or AL in either refractive group (p > 0.05).
The measurements demonstrated high reproducibility, with interobserver agreement values of 0.987 for CMT and 0.911 for subfoveal CT. No significant differences in CMT or subfoveal CT were found among amblyopic, fellow, and control eyes in either group (p > 0.05 for all) (Tables 2 and 3). Although subfoveal CT did not significantly differ between hyperopic and myopic amblyopic eyes (p = 0.320), a statistically significant difference was observed in CMT (p = 0.042) (Table 4).
In the hyperopic group, amblyopic eyes exhibited significantly greater LCA compared to both fellow (p = 0.035) and control eyes (p = 0.048). In contrast, myopic amblyopic eyes demonstrated significantly smaller LCA than fellow (p = 0.004) and control eyes (p = 0.032) (Tables 2 and 3). However, no statistically significant differences were observed among amblyopic, fellow, and control eyes in either group with respect to TCA or SCA (p > 0.05 for all comparisons).
The CVI was calculated as 63.46 ± 5.61% in amblyopic eyes, 64.85 ± 4.21% in fellow eyes, and 64.14 ± 4.32% in control eyes in the hyperopic group. The differences between amblyopic and fellow eyes (p = 0.082) and between amblyopic and control eyes (p = 0.092) were not statistically significant (Table 2). In the myopic group, the CVI was 61.74 ± 5.89% in amblyopic eyes, 63.98 ± 4.41% in fellow eyes, and 62.98 ± 4.89 in control eyes (p = 0.075 for amblyopic vs. fellow eyes and p = 0.098 for amblyopic vs. control eyes) (Table 3). No significant differences were observed between fellow and control eyes in any of the choroidal area measurements or CVI values in either the hyperopic or myopic group (p > 0.05 for all comparisons) (Tables 2 and 3). When comparing hyperopic and myopic amblyopic eyes, the myopic group had significantly lower TCA (p = 0.036) and LCA (p = 0.008) (Table 4).
In the hyperopic group, amblyopic eyes exhibited significantly lower inferior peripapillary VD and higher nasal peripapillary VD compared to fellow (p = 0.007 for both) and control eyes (p = 0.023 and p = 0.014, respectively) (Table 2). In contrast, while no significant differences were observed in any quadrant between amblyopic and fellow eyes in the myopic group (p > 0.05 for all), superior peripapillary VD was significantly lower in amblyopic eyes than in control eyes (p = 0.045) (Table 3). No significant differences were found between fellow and control eyes in the microvascular characteristics of the choriocapillaris in the macular and peripapillary regions in either group (p > 0.05 for all comparisons) (Tables 2 and 3). Comparison of the hyperopic and myopic amblyopic eyes revealed higher inferior peripapillary VD in the myopic group (p = 0.018) (Table 4).
In both groups, significant correlations were found among TCA, LCA, SCA, and CVI within amblyopic eyes. However, no significant correlations were identified between choroidal vascularity metrics and OCT-A parameters. Detailed correlation analyses are presented in Fig. 1.
Fig. 1.
Dot plots illustrating the correlation between choroidal vascularity measurements, calculated based on enhanced depth imaging optical coherence tomography, and choriocapillaris vascular density data obtained via optical coherence tomography angiography in the amblyopic eyes of the hyperopic (A) and myopic (B) groups. The size of the cross marks represents the absolute value of the correlation coefficient, while the color indicates the direction of the correlation: red denotes positive correlations and blue denotes negative correlations. Significance levels were adjusted using Bonferroni correction
Discussion
Amblyopia has been linked to structural changes in the choroid [26]. The binarization method, first introduced by Sonoda [27] and later improved by Agrawal [28] has recently offered more objective insights into the structural features of the choroid. This technique allows for a more detailed and precise assessment of the vascular and stromal components of the choroid. The CVI is calculated as the ratio of the LCA to the TCA, serving as an indicator of choroidal vascularity [29].
In the present study, the CVI showed no significant differences between amblyopic and fellow eyes or between amblyopic and control eyes in either the hyperopic or myopic groups. Hyperopic amblyopic eyes exhibited larger LCAs compared to their fellow and control eyes, whereas myopic amblyopic eyes showed the opposite trend. Notably, the myopic group had significantly smaller TCA and LCA than the hyperopic group.
Nishi et al. [30] measured the TCA, LCA, and SCA of the subfoveal choroid using the binarization method in 40 anisohypermetropic amblyopic eyes and their fellow eyes, as well as in 103 age-matched control eyes. Their findings revealed that the TCA was significantly larger in the amblyopic eyes compared to the fellow eyes. Additionally, the luminal-to-stromal ratio was significantly higher in the amblyopic eyes than in both the fellow eyes and the control eyes [30]. Guler Alis et al. [17] investigated the choroidal structure in children with anisometropic amblyopia using a similar method and reported a larger TCA in amblyopic eyes compared to both fellow and control eyes. They also concluded that both amblyopic and fellow eyes exhibited lower CVI values compared to control eyes, which was attributed to a larger SCA and a smaller LCA. Hui et al. [16] evaluated the choroidal characteristics of children with hyperopic anisometropic amblyopia and found significantly greater LCA, SA, and TCA in amblyopic eyes compared to both fellow and control eyes. Although no significant difference in CVI was observed between amblyopic and fellow eyes, CVI values were significantly lower in amblyopic eyes than in control eyes. Similarly, Cevher et al. [12] reported higher TCA, LCA, and SCA, along with lower CVI values in hyperopic anisometropic amblyopic eyes compared to both fellow and control eyes. Although TCA, LCA, and SCA were significantly lower in myopic amblyopic eyes, no significant differences in CVI values were observed among the groups. The discrepancy regarding the CVI values among the studies, could be attributed to differences in sample characteristics, such as age range, inclusion of both hyperopic and myopic subtypes, and the manual measurement approach adopted in our study. While differences in TCA and LCA reached significance, the CVI—being a ratio—may have been less sensitive to changes in absolute vascular and stromal components, especially in a relatively small sample. The lack of significant CVI differences may also reflect the heterogeneity and subclinical nature of choroidal vascular changes in anisometropic amblyopia, highlighting the need for larger, multicenter studies to confirm and clarify these findings within specific populations.
Previous studies suggested that the enlargement of the LCA in amblyopic eyes may be linked to a shorter AL [30, 31]. According to the results of this study, although no significant difference was found in the microvascular features of the choriocapillaris in hyperopic amblyopic eyes compared to the fellow and control eyes—nor in subfoveal CT—, there may have been secondary vascular congestion in the smaller and shorter eye. This could have led to the prominence and enlargement of the lumen in choroidal vessels, particularly in the Haller and Sattler layers. This condition has also been documented in the literature as hyperopic anisometropic amblyopia, which leads to choroidal thickening and an increase in the flow area of choroidal capillaries, along with large and medium-sized vessels [32].
Although not statistically significant, the TCA, LCA, and SCA were slightly larger in the amblyopic eyes of the hyperopic group and smaller in those of the myopic group compared to their respective fellow and control eyes. However, only the difference in LCA reached statistical significance in this study. The smaller SCA and LCA values observed in myopic amblyopic eyes compared to fellow and control eyes may be attributed to a decrease in the choroidal vascular structures per unit area, secondary to increased AL. Additionally, this finding could be explained by alterations in the Haller and Sattler layers, which are drained by larger veins in the sclera—a structure significantly influenced by axial elongation.
The stromal area contains nonvascular smooth muscle [15]. It is proposed that the nonvascular smooth muscle cells in the choroid’s stromal area may differ in quantity, distribution, and function in amblyopic eyes [30, 33, 34]. This leads to dysfunction of the nonvascular smooth muscle, causing an increase in CT and a reduction in the SCA, which indirectly results in an enlargement of the LCA [15]. Although this mechanism is consistent with the results of the present study, the lack of statistical significance in SCA measurements may be due to the limited sample size.
Optical coherence tomography angiography has emerged as the main non-invasive technique for evaluating retino-choroidal vasculature in amblyopic patients [35]. In the present study, the hyperopic amblyopic eyes had significantly lower inferior peripapillary VD and higher nasal peripapillary VD of the choriocapillaris segment compared to fellow and control eyes. When comparing hyperopic and myopic anisometropic amblyopic eyes, the only significant difference in terms of the VD of the choriocapillaris segment observed was in the inferior peripapillary region, where myopic eyes exhibited higher VD values than hyperopic eyes. Cinar et al. [36] conducted a non-invasive assessment of the superficial and deep vascular densities of the retina in amblyopic eyes using OCT-A. Mean vascular densities in both superficial and deep layers in the foveal and parafoveal areas were not significantly different in amblyopic eyes compared to fellow and control eyes. However, when divided into quadrants, vascular densities in the superficial and deep layers were significantly decreased in the parafoveal superior quadrant in amblyopic eyes. Cao et al. [32] used OCT-A to evaluate choroidal features in children with hyperopic anisometropic amblyopia and observed that amblyopic eyes exhibited a greater macular choroidal capillary flow area compared to fellow eyes. Additionally, Sobral et al. [37] conducted a study involving 16 children with strabismic amblyopia, 10 children with anisometropic amblyopia, and 26 healthy subjects. The study revealed a statistically significant decrease in macular vascular density within the SCP and a reduction in optic disc flow area among the amblyopic participants. They stated that the contralateral eyes of children with amblyopia do not exhibit completely normal vascularization [37]. On the other hand, Huang et al. [13] found that whole macular thickness, foveal avascular zone area, and optic disc vessel density were similar among amblyopic eyes (anisometropic or strabismic), fellow eyes, and control eyes. Dereli Can [38] reported that the inside disc VD was significantly lower in amblyopic patients; however, other optic disc OCT-A parameters in the anisometropic amblyopic group did not show significant differences than control eyes. However, the study focused solely on adult patients [38]. Although patients with optic discs displaying abnormal appearances (e.g., tilting or crowding) were excluded from the study, it is possible that cases with minor alterations at the optic disc head were included. This inclusion may have contributed to the statistically significant difference observed between the two groups in the peripapillary area. Repeating the measurements with a larger patient cohort is recommended.
Fellow eyes in both the hyperopic and myopic groups exhibited similar characteristics to healthy controls in the present study. Previously, Stalmakhova et al. [39] reported no significant differences in the vascular parameters of fellow eyes in amblyopic patients compared to healthy controls, suggesting that fellow eyes retain normal vascular characteristics. Other studies have also indicated that retinal vascular density and skeleton length are significantly reduced in amblyopic eyes compared to fellow eyes, whereas fellow eyes themselves do not show significant vascular density differences when compared to healthy controls [40, 41]. In contrast, some studies suggest that subtle vascular abnormalities may still exist in the fellow eyes of unilateral amblyopia, although these changes are not as pronounced as in amblyopic eyes [42]. These discrepancies highlight the complexity of vascular responses in amblyopia and the need for further investigation.
Although several intergroup differences in structural and vascular parameters reached statistical significance, the absolute numerical values for some parameters were relatively close. This suggests that while anisometropic amblyopia may be associated with subtle alterations in ocular morphology and microvasculature, these changes are likely subclinical in nature. Such subtle differences may only be detectable through advanced ocular imaging techniques, reflecting the increased sensitivity of modern diagnostic tools. Further longitudinal studies incorporating functional correlations are needed to clarify the clinical significance of these modest yet statistically significant findings.
This study is subject to several limitations. First, the sample size of the myopic group fell below the minimum number estimated in our power analysis, which may have reduced the statistical power of subgroup comparisons and limited the generalizability of these specific findings. Second, despite efforts to age-match amblyopic and control participants within each refractive group and conduct ANCOVA analysis, the wide age range of the study population may have introduced variability. Third, CT measurements, as well as the TCA, LCA, SCA, and CVI measurements were performed manually due to the absence of automatic choroidal segmentation in the Heidelberg Spectralis OCT system. To eliminate the influence of manual measurements on the results, measurements were conducted by three independent researchers, and the inter-rater agreement of the measurements was evaluated. Moreover, the evaluation of scleral thickness in patients was not performed. Despite all these limitations, the inclusion and comparison of both myopic and hyperopic eyes in the study, the evaluation of the choroid at the capillary level by OCT-A images, and the assessment of the choroid as a whole by calculating CVI through EDI-OCT images enhance the value and strength of this study.
Conclusions
Although no statistically significant difference in CVI was found between hyperopic and myopic amblyopic eyes, significant differences were observed in TCA and LCA in both groups. These results support that hyperopic and myopic amblyopic eyes may display distinct choroidal characteristics. Additional studies with larger sample sizes are needed to further validate these findings.
Acknowledgements
Not applicable.
Abbreviations
- AL
Axial length
- BCVA
Best-corrected visual acuity
- CT
Choroidal thickness
- CMT
Central macular thickness
- CVI
Choroidal vascularity index
- D
Diopters
- DCP
Deep capillary plexus
- EDI
Enhanced depth imaging
- ICC
Intraclass correlation coefficients
- ICGA
Indocyanine green angiography
- LCA
Luminal choroidal area
- OCT
Optical coherence tomography
- OCT-A
Optical coherence tomography angiography
- ROI
Region of interest
- SCA
Stromal choroidal area
- SCP
Superficial capillary plexus
- SE
Spherical equivalent
- TCA
Total choroidal area
Author contributions
Concept: CDE, TÖ, AG; Design: SK, MK, and CDE; Supervision: TÖ, AG; Resource: SK, MK, IK, and CDE; Data Collection and/or Processing: SK, MK, and IK; Analysis and/or Interpretation: CDE and TÖ; Literature Search: SK, and MK; Writing: SK, MK, IK, and CDE; Critical Reviews: TÖ and AG.
Funding
The authors have no relevant financial or non-financial interests to disclose. No funding was received for the study.
Data availability
The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.
Declarations
Ethics approval and consent to participate
Ethical approval was granted by the Dokuz Eylül University Local Ethics Committee (Decision No: 2023/20 − 16; Date:14.06.2023), and informed consent was obtained from all participants or their legal guardians.
Consent for publication
Not Applicable.
Competing interests
The authors declare no competing interests.
Footnotes
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Contributor Information
Seher Köksaldı, Email: seherkoksaldi@gmail.com.
Andrzej Grzybowski, Email: ae.grzybowski@gmail.com.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.