|Year : 2020 | Volume
| Issue : 4 | Page : 255-260
Assessment of choroidal thickness and macular microvascular changes in amblyopic eyes using optical coherence tomography angiography
Sherin H Sadek1, Sherif A Eissa2, Ghada I Gawdat2, Ragai M Hatata1
1 Department of Ophthalmology, Faculty of Medicine, Fayoum University, Fayoum, Egypt
2 Department of Ophthalmology, Faculty of Medicine, Cairo University, Cairo, Egypt
|Date of Submission||17-Apr-2020|
|Date of Decision||31-May-2020|
|Date of Acceptance||04-Jul-2020|
|Date of Web Publication||28-Dec-2020|
MD Sherin H Sadek
Department of Ophthalmology, Faculty of Medicine, Fayoum University, 2/7 Zahraa ELMaadi, Cairo 11435
Source of Support: None, Conflict of Interest: None
Aim This study aimed to assess microvascular and choroidal thickness (CT) changes in cases with unilateral amblyopia and to compare optical coherence tomography angiography parameters with the fellow eyes as well as with age-matched controls.
Study design This is a prospective case–control study.
Patients and methods The study included 44 eyes; 12 eyes had unilateral anisometropic amblyopia compared with their fellow 12 eyes and 20 eyes from normal age-matched controls. Spectral-domain optical coherence tomography angiography was used to assess the vessel density (VD) of the superficial capillary plexus (SCP) and the deep capillary plexus (DCP) in both 3×3 and 6×6 mm scans. In addition, central macular thickness, foveal avascular zone size, and CT were measured.
Results The mean age of amblyopic patients was 25.1±10.8 years with a mean BMI of 22.4±4.7 compared with the mean age of the control group (26.4±2.8 years) with a mean BMI of 21.0±2.1. Amblyopic eyes showed a statistically nonsignificant decrease in subfoveal CT (mean=328.58±34.46 μm) and temporal CT (mean=318.42±33.93 μm) compared with their fellow eyes (321.00±42.41 and 317.33±57.21 μm, respectively) and with the control eyes (subfoveal CT 349.80±72.33 μm and temporal CT 346.50±40.61 μm, P=0.178 and 0.177, respectively). There was a significantly decreased VD in the SCP of amblyopic eyes at the 3 mm scan (P=0.032) with a mean of 43.87±4.67% in the whole image. In addition, DCP VD in the 6 mm scan showed a statistically significant decrease (mean=43.91±7.26%) compared with the fellow and control eyes (P=0.001). The foveal avascular zone size was almost the same in all groups (0.28±0.13 mm2) with no significant difference.
Conclusion Amblyopic eyes showed decreased VD in both SCP and DCP compared with that of the fellow eyes and controls.
Keywords: amblyopia, choroidal thickness, macular microvascular, optical coherence tomography angiography
|How to cite this article:|
Sadek SH, Eissa SA, Gawdat GI, Hatata RM. Assessment of choroidal thickness and macular microvascular changes in amblyopic eyes using optical coherence tomography angiography. Delta J Ophthalmol 2020;21:255-60
|How to cite this URL:|
Sadek SH, Eissa SA, Gawdat GI, Hatata RM. Assessment of choroidal thickness and macular microvascular changes in amblyopic eyes using optical coherence tomography angiography. Delta J Ophthalmol [serial online] 2020 [cited 2022 Jun 26];21:255-60. Available from: http://www.djo.eg.net/text.asp?2020/21/4/255/304939
| Introduction|| |
The most common cause of preventable visual loss in the pediatric age group is amblyopia . The retina and choroid may be involved in the amblyopic process . Thicker subfoveal choroid in amblyopic eyes was observed objectively in optical coherence tomography (OCT) . However, OCT structural parameters in amblyopic eyes are still contradictory .
Optical coherence tomography angiography (OCTA) is a helpful tool to reveal the superficial and deep retinal layer details as well as choriocapillaris. It can be used to measure the vessel density (VD) quantitatively .
The aim of this study was to assess the microvascular and choroidal thickness (CT) changes in unilateral anisometropic amblyopia, compared with those of the fellow eyes and age-matched controls.
| Patients and methods|| |
The study was conducted at Fayoum University Hospitals from April 2018 to September 2018. The study adhered to the tenets of the Declaration of Helsinki and was approved by the Ethics Committee of the University Hospital. All participants signed a written informed consent to participate in the study and for publication of data before enrollment into the study.
This is a prospective, case–control study which included 44 eyes of 32 patients; 12 eyes were amblyopic with their other 12 normal eyes and 20 eyes of normal individuals, which were taken as a control group.
The 12 patients with unilateral anisometropic amblyopia were diagnosed by best-corrected distant visual acuity (BCVA) of more than or equal to two lines worse than the sound eye. The age of the patients ranged between 15 and 39 years. Exclusion criteria included cases with an axial length of more than 27.50 mm or less than 20 mm, history of intraocular surgery, cataract, corneal opacities, intravitreal injections, or any other retinal diseases. The controls were age matched with the same range of axial length, normal fundus, and no systemic diseases.
All cases were subjected to full ophthalmologic examination, including manifest and cycloplegic refraction, BCVA using a standard Early Treatment Diabetic Retinopathy Study (ETDRS) chart at 4 m [Logarithm of the Minimum Angle of Resolution (LogMAR)], fundus examination using indirect ophthalmoscope, axial length (AL) measurement using IOLMaster (Carl Zeiss Meditec, Dublin, California, USA), ocular alignment assessment, and OCTA.
All the eyes were evaluated using spectral-domain OCTA (Avanti RTVue XR; Optovue Inc., Fremont, California, USA). OCTA produces ultrahigh-resolution, three-dimensional images that are displayed as individual layers of retinal vasculature with a scanning speed of about 70 000 A-scans per second. The patients were examined in the sitting position using the internal fixation in alternation with the external fixation (if the patient is poorly fixating). Each scan was acquired in less than 3 s with an axial resolution of ∼5 μm, transverse resolution of ∼15 μm, and 73% more sampling points to give a 6×6 mm scan . Consecutive scans were taken until reaching the high-quality signal scans. The axial imaging depth is 2–3 mm. VD of the superficial capillary plexus (SCP) and deep capillary plexus (DCP) in both 3 mm (304×304 A-lines) and 6 mm (400×400 A-lines) zones, central macular thickness (CMT), foveal avascular zone (FAZ) size as well as CT were measured. CT was measured manually using calipers from the outer portion of the hyper-reflective line corresponding to the retinal pigment epithelium to the chorio-scleral junction at three different locations: at the center of the fovea, 1000 μm temporal to the center of the fovea, and 1000 μm nasal to the center of the fovea. Three comparisons were done: amblyopic eyes versus their fellow eyes, amblyopic eyes versus the eyes of controls, and fellow eyes of amblyopic patients versus eyes of controls.
The collected data were organized, tabulated, and statistically analyzed using SPSS software statistical computer package, version 18 (SPSS Inc., Chicago, Illinois, USA). For quantitative data, the mean and SD were calculated. Kolmogorov–Smirnov test was performed as a test of normality. Kruskal–Wallis test was used in comparing the three groups, while Mann–Whitney U test was performed as a pairwise comparison. Qualitative data were presented as number and percentages and χ2 was used as a test of significance. For interpretation of results of tests of significance, significance was adopted at P value less than or equal to 0.05.
| Results|| |
The 44 eyes of the 32 participants enrolled into the study included 12 patients with unilateral amblyopia (and their normal fellow eyes) and 20 nonamblyopic age-matched controls.
Fifteen patients were women (four in the amblyopic group) and 17 were men (eight in the amblyopic group). The mean age of the amblyopic patients was 25.1±10.8 years with a mean BMI of 22.4±4.7 compared with the mean age of the control group (26.4±2.8 years, P=0.646) with a mean BMI of 21.0±2.1 (P=0.346).
There was a statistically significant difference in the BCVA between the amblyopic group (mean LogMAR BCVA=0.80±0.21) compared with 0.14±0.24 in the fellow eyes (P<0.0001) and 0.03±0.07 in the control group (P<0.0001). There was no significant difference between LogMAR BCVA of the fellow eyes and controls (P=0.187). The spherical equivalent was statistically significantly different between the amblyopic eyes (mean=−7.41±5.44 D) compared with their fellow eyes (−0.77±2.29 D, P<0.0001) and with the control group (−0.49±0.59 D, P<0.0001). However, there was no statistically significant difference in the spherical equivalent between the normal fellow eyes and the control group (P=0.967).
The amblyopic eyes showed a lower statistically significant signal strength index (mean SSI=5.42±2.07) than the control eyes (mean=8.25±0.85). The mean AL of the amblyopic eyes was 24.99±2.21 mm compared with 22.70±0.74 mm in the fellow eyes and 22.83±0.72 mm in the control group. A statistically significant difference was found between the amblyopic eyes and their fellow eyes (P=0.0003) and between the amblyopic eyes and the controls (P=0.0001). However, the difference between the AL of the fellow eyes and controls was nonsignificant (P=0.959).
The CMT was increased in the amblyopic eyes (250.83±29.72 μm) with no significant difference when compared with the fellow eyes (246.67±28.62 μm) and the controls (242.70±15.60 μm) (P=0.454) ([Table 1]). Although the CT showed variations in measurements between the amblyopic and control groups at different locations ([Figure 1]), no statistically significant difference was detected. The subfoveal CT (mean=328.58±34.46 μm) and temporal CT (mean=318.42±33.93 μm) in the amblyopic eyes and their contralateral eyes (321.00±42.41 and 317.33±57.21 μm, respectively) were less than in the control group (mean subfoveal CT=349.80±72.33 μm and temporal CT=346.50±40.61 μm, P=0.178 and 0.177, respectively). Amblyopic eyes showed also a statistically nonsignificant increase in the CT nasally (P=0.807), with a mean thickness of 329.25±39.53 μm compared with 324.75±42.07 μm in their fellow eyes and 323.10±51.56 μm in the control eyes ([Table 1]).
|Table 1 Central macular thickness and choroidal thickness at different locations|
Click here to view
|Figure 1 Choroidal thickness. (a) Left amblyopic eye; central 334 μm and nasal 362 μm. (b) Fellow eye; central 268 μm and nasal 306 μm. (c) Control eye; central 254 μm and nasal 261 μm.|
Click here to view
There was no statistically significant difference in FAZ size of the amblyopic eyes (0.28±0.13 mm2) compared with the control group (0.28±0.12 mm2, P=0.700). The mean VD in the whole image of the SCP at the 3 mm zone (43.87±4.67%) was statistically significantly less (P=0.019), as compared with the control group (47.32±3.14%) ([Table 2]). In addition, there was a statistically significant difference between the whole image (P=0.031) and inferior hemisection (P=0.030) of the three groups. In addition, there was a statistically significant difference between the VD at the inferior hemisection of the amblyopic eyes (43.19±4.98%) and controls (45.91±5.51%, P=0.019) ([Table 2]). At the 6 mm zone, the mean VD of the whole image of SCP was also less in the amblyopic eyes (46.65%, P=0.031) compared with the fellow eyes (48.17%) and the control eyes (50.92%) ([Figure 2] and [Table 3]). By analysis, another statistically significant difference was detected between the VD of the whole image at the SCP (P=0.024) between the amblyopic eyes and controls, inferior hemisection (P=0.007), and also between the three groups at the inferior hemisection (P=0.024).
|Table 2 Vessel density of superficial and deep capillary plexuses at the 3 mm zone|
Click here to view
|Figure 2 Vessel density of the whole image of superficial capillary plexus at 6mm scan of (A) an amblyopic eye 47.4 %, (B) fellow eye 49.7%, (C) control eye 50.9%.|
Click here to view
|Table 3 Vessel density of the superficial and deep capillary plexuses at the 6 mm zone|
Click here to view
There was no significant correlation between the DCP OCTA parameters in the three groups at different sections at the 3 mm zone. However, there was a statistically significant difference between all groups at different sections at the 6 mm zone: whole image (P=0.001), superior hemisection (P=0.002) and inferior hemisection (P=0.001) and also between amblyopic and control eyes (P<0.0001, P=0.001, P<0.0001, respectively, [Table 3]). [Figure 3] illustrates examples of the DCP VD at the 6 mm zone.
|Figure 3 Vessel density of the whole image of deep capillary plexus at 6mm scan of (A) an amblyopic eye 49.8%, (B) fellow eye 54.6%, (C) control eye 60.2%.|
Click here to view
| Discussion|| |
Reviewing the literature, several studies assessed the OCTA structural and blood flow measurements in normal eyes of healthy persons ,. Ghassemi et al.  reported that the mean superficial FAZ area was 0.27 mm2 (which is similar to the present study results), while the deep FAZ area was 0.35 mm2, with no difference between both eyes. The central foveal thickness was 247±21.1 µm. Coscas et al.  analyzed a retrospective chart review of 70 healthy participants with a mean VD and mean FAZ±SD size at the level of the SCP being 52.58±3.22% and 0.28±0.1 mm2, respectively. The mean VD and mean FAZ size at the DCP were 57.87±2.82% and 0.37±0.12 mm2, respectively.
The current study demonstrated the role of OCTA in the evaluation of microvascular parameters and CT changes in anisometropic amblyopic eyes of patients with a mean age of 25.1±10.8 years.
Previous studies have demonstrated that CT in amblyopic eyes was significantly thicker than that in both fellow and control eyes. The choroid may be involved by the amblyopia process, but with no consensus about whether it is structurally abnormal [9-11]. The relation between amblyopia and CT remains unclear. Kara et al.  reported that CT was significantly thicker in amblyopic eyes than in fellow eyes only at 750 µm nasal to the fovea. This finding correlated with the present study, but we measured at 1 mm nasal to the fovea and it was statistically insignificant, maybe due to the small sample size compared with them. These studies were mainly on children while we assessed the subfoveal CT in adult amblyopic patients.
We agreed with El-Hifnawy et al.  in that amblyopic eyes showed increased CMT compared with the fellow normal eyes. However, we found no significant correlation between amblyopia and OCT parameters like Abdulghaffar et al. .
The FAZ size in amblyopic eyes, in the current study, showed no significant difference when compared with the control group. These findings are in agreement with the study of Yilmaz et al. , in which 15 eyes with strabismic amblyopia revealed mean superficial and deep FAZ areas of 0.287 and 0.382 mm2, respectively, with no statistically significant difference compared with the control group. However, Sobral et al.  documented a marginally significant increase in FAZ size of the DCP in amblyopic eyes.
In this study, there was a statistically significant difference between amblyopic and control groups in the SCP and DCP density in both the 3 and 6 mm zones and also when comparing the amblyopic eyes to the fellow eyes. These results agree with Yilmaz et al.  and Lonngi et al. , who reported lower superficial and deep VDs in amblyopic eyes compared with the controls. Yilmaz et al.  hypothesized that the decreased VD in amblyopic eyes may be secondary to retinal or choroid microvasculature alterations, which are secondary to underuse.
In this study, the fellow eye of an amblyopic one also had lower microvascular parameters than the healthy eye. This matches with the findings of previous studies by Sobral et al.  and Meier and Giaschi , which stated that the contralateral eyes of amblyopic children do not have completely normal vascularization.
One of the limitations of this study is the small sample size and the lack of assessment of optic disk vascularization. It is also limited by the poor cooperation of patients due to poor fixation of the amblyopic eye. A software development is recommended for automatic measurement of CT.
| Conclusion|| |
Using OCTA, the amblyopic eyes showed lower VD in both SCP and DCP compared with that of the fellow eyes and controls.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Peterseim MM, Papa CE, Wilson ME, Davidson JD, Shtessel M, Husain M et al.
The effectiveness of the Spot Vision Screener in detecting amblyopia risk factors. J AAPOS 2014; 18:539–542.
Aygit ED, Yilmaz I, Ozkaya A, Alkin Z, Gokyigit B, Yazici AT et al.
Choroidal thickness of children’s eyes with anisometropic and strabismic amblyopia. J AAPOS 2015; 19:237–241.
Bruce A, Pacey IE, Bradbury JA, Scally AJ, Barrett BT. Bilateral changes in foveal structure in individuals with amblyopia. Ophthalmology 2013; 120:395–403.
Zhang Z, Huang X, Meng X, Chen T, Gu Y, Wu Y et al.
In vivo assessment of macula in eyes of healthy children 8 to 16 years old using optical coherence tomography angiography. Sci Rep 2017; 7:8936.
Yilmaz I, Ocak OB, Yilmaz BS, Inal A, Gokyigit B, Taskapili M. Comparison of quantitative measurement of foveal avascular zone and macular vessel density in eyes of children with amblyopia and healthy controls: an optical coherence tomography angiography study. J AAPOS 2017 21:224–228.
Ghassemi F, Mirshahi R, Bazvand F, Fadakar K, Faghihi H, Sabour S. The quantitative measurements of foveal avascular zone using optical coherence tomography angiography in normal volunteers. J Curr Ophthalmol 2017; 29:293–299.
Hashmani N, Hashmani S, Murad A, Baig N. Macular vascular density at the superficial capillary plexus using the optical coherence tomography angiography. Clin Ophthalmol 2019; 13:295–302.
Coscas F, Sellam A, Glacet-Bernard A, Jung C, Goudot M, Miere A et al.
Normative data for vascular density in superficial and deep capillary plexuses of healthy adults assessed by optical coherence tomography angiography. Invest Ophthalmol Vis Sci 2016; 57:211–223.
Kara O, Altintas O, Karaman S, Emre E, Caglar Y. Analysis of choroidal thickness using spectral-domain OCT in children with unilateral amblyopia. J Pediatr Ophthalmol Strabismus 2015; 52:159–166.
Tenlik A, Güler E, Kulak AE, Totan Y, Dervişoğulları MS, Gürağaç FB. Evaluation of choroidal thickness in amblyopia using enhanced depth imaging optical coherence tomography. Curr Eye Res 2015; 40:1063–1067.
Liu Y, Dong Y, Zhao K. A meta-analysis of choroidal thickness changes in unilateral amblyopia. J Ophthalmol 2017; 2017:2915261.
El-Hifnawy MA, Abo-Elkheir AF, Abo-Samra AA, Mohamed KA. Spectral domain optical coherence tomography measurements in amblyopic Egyptian patients. Delta J Ophthalmol 2017; 18:26–31. [Full text]
Abdulghaffar AT, Al-Saadany A, Ibrahim AM. Optical coherence tomography-based comparison of retinal nerve fiber layer thickness and macular thickness in amblyopic and fellow eyes. Delta J Ophthalmol 2019; 20:74–81. [Full text]
Sobral I, Rodrigues TM, Soares M, Seara M, Monteiro M, Paiva C et al.
OCT angiography findings in children with amblyopia. J AAPOS 2018; 22:286–289.
Lonngi M, Velez FG, Tsui I, Seara M, Monteiro M, Paiva C et al.
Spectral-domain optical coherence tomographic angiography in children with amblyopia. JAMA Ophthalmol 2017; 135:1086–1091.
Meier K, Giaschi D. Unilateral amblyopia affects two eyes: fellow eye deficits in amblyopia. Invest Ophthalmol Vis Sci 2017; 58:1779–1800.
[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2], [Table 3]