Methods

This retrospective study was performed at a single center according to the tenets of the Declaration of Helsinki. The study was prospectively approved by Institutional Review Board (Samsung Medical Center Institutional Review Board).

This study involved 96 eyes of 48 healthy children and 54 eyes of 27 healthy adults. The 48 children have participated in multiple studies in the same department. Data were collected from healthy adult subjects who visited our institution for routine eye examinations. However, the previous measurement data were not duplicated and all the measurements were newly performed. Inclusion criteria for children included healthy subjects born at term and with normal birth weights. Only children between the ages of 4 and 10 years were included, as younger children were considered unable to cooperate with OCT examinations. Inclusion criteria for adults included healthy subjects 20–40 years in age. Exclusion criteria for both children and adults included previous eye trauma or eye surgery, refractive error exceeding ±6.0 diopters, and history of any ocular abnormalities, including strabismus, amblyopia, congenital cataract, and vitreoretinal disorders.

All subjects underwent full ophthalmologic assessments, including visual acuity testing, manifest refraction, slit-lamp biomicroscopy, and fundus examination. For children, cycloplegic refractions were additionally performed using retinoscopy after the instillation of 1% cyclopentolate and 0.5% tropicamide. The spherical equivalent was calculated as the sphere plus half a cylinder. In adults, results from manifest refraction were used for analysis, whereas results from cycloplegic refraction were used in children. In children, axial length measurements were additionally performed using interferometry (IOL Master; Carl Zeiss Meditec, La Jolla, California, USA).

Horizontal and vertical enhanced depth imaging OCT crosshair scans were conducted using spectral-domain OCT (Spectralis; Heidelberg Engineering GmbH, Heidelberg, Germany). The choroid was imaged by positioning an OCT camera close enough to the eye to obtain an inverted image, or by using Spectralis enhanced depth imaging by pressing the conversion button provided in the Spectralis software. Measurements were conducted using Heidelberg Eye Explorer software (version 1.7.1.0). To avoid possible overestimation of choroidal thickness in measurements based on 1:1 pixel image, all measurements were performed using 1 μm:1 μm images. Two observers who were experienced in measuring choroidal thickness performed the measurements and the mean value of the 2 measurements was used for analysis.

The measurements of choroidal sub-layers were performed through combined use of 2 recently developed methods for choroidal sub-layer analysis. Among the 2 methods, the measurement in the present study was mainly based on the method developed by Branchini and associates, in which choroidal sub-layers were divided based on a cutoff diameter for large choroidal vessels. In our pilot study, the diameter of large choroidal vessels was relatively small in some children. Thus, the method of Branchini and associates was not directly applied in the present study. The following alterations were made. In the previous study, a 100 μm diameter was used as a cutoff for defining large choroidal vessels. In the present study, the same value was used for adults. However, the diameter of choroidal vessels in children was relatively small. In some eyes, no choroidal vessel within 750 μm distance from the fovea exhibited 100 μm or greater diameter. Given that on OCT images the mean diameter of the smallest large choroidal vessel in healthy children measured approximately 77 μm in our pilot study (range, 52–107 μm; unpublished data), the cutoff for large choroidal vessels in children was defined as 80 μm.

Our methods to evaluate total choroidal thickness and thickness of choroidal sub-layers were almost identical to the methods developed by Branchini and associates ( Figure 1 ). Subfoveal choroidal thickness was defined as the distance from the hyperreflective line of the subfoveal Bruch membrane to the innermost hyperreflective line of the subfoveal chorioscleral interface. The measurements were performed at the following locations: in the horizontal image: at the fovea, 750 μm nasal to the fovea, and 750 μm temporal to the fovea; in the vertical scan image: at the fovea, 750 μm superior to the fovea, and 750 μm inferior to the fovea. The large choroidal vessels measuring 80 μm (children) or 100 μm (adults) or more within closest proximity to the locations of the choroidal thickness measurement lines were identified. Perpendicular lines from the innermost point of the large choroidal vessels were drawn at the same locations, which intersect the choroidal thickness measurement lines. The thickness of the large choroidal vessel layer was measured perpendicularly from the inner border of the sclera to the intersection point on the choroidal thickness measurement lines at all locations. The measurements of the large choroidal vessel layer were subtracted from the total choroidal thickness to obtain the thickness of the medium choroidal vessel layer–choriocapillaris layer. If choroidal vessels exhibiting the cutoff diameter were not observed at the measurement points, a method developed by Sim and associates was used as an alternative. As described in the previous study, the large choroidal vessel layer was defined as the outer choroid, consisting of large hypo-intense spaces representing large vascular luminal spaces. The medium choroidal vessel layer–choriocapillaris layer was defined as the inner choroid consisting of small- to medium-sized hypo-intense spaces, surrounded by hyperintense stroma. The ratio of the thickness of the large choroidal vessel layer to the total choroidal thickness was calculated.

A representative horizontal optical coherence tomography scan image from a child demonstrating choroidal sublayer and choroidal vascular diameter analysis methods. Asterisks (*) indicate large choroidal vessels with ≥80 μm of lumen diameter. The vertical dashed lines indicate choroidal thickness measurement lines, and the horizontal dashed lines indicate imaginary lines dividing the large choroidal vessel layer and medium choroidal vessel layer–choriocapillaris layer. The double-headed arrow (↕) indicates choroidal vascular diameter. At the nasal measurement point (arrowhead), no choroidal vessel exhibited ≥80 μm of lumen diameter. In this case, the 2 choroidal sub-layers were divided based on the method developed by Sim and associates.

The measurement of choroidal vascular diameter was performed based on OCT images ( Figure 1 ). The 3 largest choroidal vessels within 750 μm distance from the fovea were selected, and the diameter of hypo-reflective lumens of each choroidal vessel was measured. When the choroidal thickness measurement lines at 750 μm from the fovea intersected with the choroidal vascular lumen, the vessel was considered to be located within 750 μm distance from the fovea. The measurements were performed for both horizontal and vertical scan images. The mean values of the 6 measurements (3 for horizontal scan image and 3 for vertical scan image) were used in the analysis.

In both children and adults, the association between subfoveal choroidal thickness and thickness of large choroidal vessel layer and medium choroidal vessel layer–choriocapillaris layer, the ratio of the thickness of the large choroidal vessel layer to the total choroidal thickness, and choroidal vascular diameter were analyzed. The association between age and spherical equivalent and the ratio of the thickness of the large choroidal vessel layer to the total choroidal thickness and choroidal vascular diameter was analyzed. The association between large choroidal vessel layer thickness and choroidal vascular layer thickness was estimated. In children, association between axial length and the ratio of the thickness of the large choroidal vessel layer to the total choroidal thickness and choroidal vascular diameter was additionally analyzed. The spherical equivalent, subfoveal choroidal thickness, large choroidal vessel layer thickness, medium choroidal vessel layer–choriocapillaris layer thickness, the ratio of the thickness of the large choroidal vessel layer to the total choroidal thickness, and choroidal vascular diameter was compared between children and adults.

Results

Twenty-six male and 22 female subjects were included in the children group, and 12 male and 15 female subjects were included in the adult group ( Table ). Among the children, the mean age was 6.7 ± 1.9 years (range, 4–10 years). The mean spherical equivalent and axial length of the 96 eyes were −0.44 ± 1.46 diopters (range, −4.50 to +2.75 diopters) and 23.1 ± 0.9 mm (range, 21.8–25.9 mm), respectively. Among the 576 measurements, the method developed by Branchini and associates was used in 514 measurements (89.2%). The remaining 62 measurements (10.8%) were performed using the alternative method. The mean subfoveal choroidal thickness, large choroidal vessel layer thickness, and medium choroidal vessel layer–choriocapillaris layer measurements were 343.8 ± 81.9 μm, 242.2 ± 70.8 μm, and 94.5 ± 27.5 μm, respectively. The mean ratio of the thickness of the large choroidal vessel layer to the total choroidal thickness was 0.71 ± 0.08. The mean choroidal vascular diameter was 103.1 ± 16.0 μm. The subfoveal choroidal thickness was significantly associated with large choroidal vessel layer thickness ( P < .001), medium choroidal vessel layer–choriocapillaris layer ( P = .005), the ratio of the thickness of the large choroidal vessel layer to the total choroidal thickness ( P < .001), and choroidal vascular diameter ( P < .001) ( Figure 2 ). Also, the thickness of the large choroidal vessel layer was significantly associated with choroidal vascular diameter ( P < .001). The association between subfoveal choroidal thickness and the ratio of the thickness of the large choroidal vessel layer to the total choroidal thickness was also found to be significant ( P < .001). There was no association between age, axial length, or spherical equivalent and either the ratio of the thickness of the large choroidal vessel layer to the total choroidal thickness ( P = .874, P = .669, and P = .474, respectively) or choroidal vascular diameter ( P = .988, P = .383, and P = .157, respectively).

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