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Review Article

Past, Present, and Future Concepts of the Choroidal Scleral Interface Morphology on Optical Coherence Tomography

Huynh, Emily MEng*,†; Chandrasekera, Erandi MBBS*,‡,§; Bukowska, Danuta PhD*,†; McLenachan, Samuel PhD*,†; Mackey, David A. MBBS, MD, FRANZCO*,†; Chen, Fred K. MBBS (Hons), PhD, FRANZCO*,†,¶

Author Information
Asia-Pacific Journal of Ophthalmology: January 2017 - Volume 6 - Issue 1 - p 94-103
doi: 10.22608/APO.201698
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Abstract

The posterior coat of the eye comprises the retina, the choroid, and the sclera. Before the 1990s, ophthalmic ultrasonography was the only method to visualize and measure the thickness of these structures in vivo. High-resolution, crosssectional imaging of the choroid only became possible after the development of optical coherence tomography (OCT).1 Although initially neglected, imaging of the choroid is now gaining interest because of the enhanced depth imaging (EDI) technique in spectral domain (SD) OCT and the more recent commercialization of swept source (SS) OCT devices.2 These recent advances enable the visualization of not only the retina but also the layers of the choroid, the choroidal scleral interface (CSI) and, occasionally, the entire thickness of the sclera through to the orbital fat.3

The choroid is a vascular layer within the posterior coat of the eye and it is implicated in the pathophysiology of many posterior segment diseases. The ability to visualize the interface between the choroid and the sclera with SS-OCT and EDI SD-OCT has enabled measurement of choroidal thickness. This parameter is now routinely used clinically to assist diagnosis and monitor treatment response in a variety of chorioretinal diseases.2 Advances in OCT technology have also led to the discovery of the suprachoroidal layer (SCL), a transitional zone between the choroid and sclera. In some cases, the suprachoroidal space (SCS) has been visualized within the SCL.4 Previously, the SCS could only be seen in vivo by ultrasonography in pathologic conditions such as suprachoroidal effusion and suprachoroidal hemorrhage.2,4 The ability to visualize SCS in high resolution in both normal and pathologic conditions has allowed researchers to reveal new insights in its role in health and disease. Studies have suggested that the SCS may be useful for diagnosing and monitoring disease.2 Furthermore, it has been shown to be a potential route for both medical and surgical treatment.2,5 The administration of bevacizumab and triamcinolone into the SCS using a mirocatheter in eyes with age-related macular degeneration (AMD) has been reported to have been performed without any serious complications.6-8 The possibility of retinal surgery in the SCS has been investigated as a potential treatment for glaucoma with the advent of silicone drainage devices, gold micro shunt implants, and supraciliary microstents.2 More recently, the “bionic eye,” a retinal visual prosthesis prototype, has also been implanted into the SCS, demonstrating the suprachoroidal anatomical position as a feasible location for placement of electrode array through minimally invasive and relatively uncomplicated surgery. This technique has been shown to be safe in 3 patients with end-stage retinitis pigmentosa.9

Choroidal thickness is traditionally measured from the outer limit of the Bruch membrane to the posterior boundary of the choroid. Although the concept is straightforward, identifying this boundary in practice is not clear-cut. The presence of the suprachoroid between the choroidal vessels and sclera has been reported by several studies; however, there is a lack of consensus in classifying it as choroidal or scleral in origin. In contrast, layers in the retina as visualized on SD-OCT have been well-defined and a consensus nomenclature for the classification of these layers has been developed to facilitate harmonization of OCT structure terminology.5 However, a universal nomenclature has not been extended to the choroidal and scleral layers, making it difficult to compare the descriptions of this interface across various research groups. Furthermore, the term CSI is often used to describe the posterior boundary in studies reporting choroidal thickness. However, some studies have defined the CSI as a line delineating the inner border of the sclera, whereas others have defined it as a distinct band between the choroidal vessels and sclera. The lack of clarity in the definition of the CSI has led to variation in choroidal thickness measurements, which reduces the precision of this measure.

Therefore, the purpose of this review is to provide an overview of how the choroidal and scleral layers have been visualized and reported in the literature, highlight the discrepancies, and propose a harmonized nomenclature for the anatomic correlates of the zones and layers of the choroid and its outer boundary or interface as seen on OCT.

MATERIALS AND METHODS

References for this review were identified through a comprehensive literature search of MEDLINE and PubMed. In addition, articles and theses thought to be relevant were also selected from the references of the articles generated from the above search. The following key words and combinations of these words were used in compiling the search: “optical coherence tomography,” “choroidal thickness,” “suprachoroid,” “choroidal scleral interface,” “choroidal scleral junction,” “choroidal scleral boundary,” “suprachoroidal space,” “swept source,” and “spectral domain.” Articles were included in the review if they provided a detailed definition and description of the choroidal scleral interface and/or suprachoroidal space with images acquired using EDI SD-OCT or SS-OCT to show where it was located.

HISTOLOGY OF THE CHOROID

The choroid is most commonly described as a 5-layered structure (Fig. 1) consisting of the Bruch membrane, the choriocapillaris, the Sattler small and medium vessels, the Haller large vessels, and the suprachoroid (or suprachoroidal layer).10 The Bruch membrane is an acellular, 5-layered extracellular matrix with a thickness of 2-4 μm.11 The choriocapillaris is a highly anastomosed network of capillaries that is approximately 10 μm thick at the fovea, thinning to about 7 μm in the periphery.10 Below the choriocapillaris is the Sattler medium vessel layer, consisting of arterioles and venules. Underneath this layer is the Haller large vessel layer where choroidal veins and arteries are found. The border between the Sattler and Haller layers is indistinct, as there is no established definition of what is meant by large or medium.12 The extravascular tissue of the vessels, termed the choroidal stroma, consists of collagen and elastic fibers, fibroblasts, nonvascular smooth muscle cells, and numerous giant melanocytes.10 Posterior to the choroidal vessels/stroma is the SCL, which is approximately 30 μm thick and extends from the choroidal stroma to the sclera where the fibers become more compact. It is a transitional zone between the choroid and the sclera,10,13 consisting of 5 to 10 layers of giant melanocytes (Fig. 1C) interspersed between flattened processes of fibroblast cells, embedded in a network of interconnected collagen lamellar fibers.4 When the lamellae separate, the potential space becomes a physical space appearing as the SCS.13 In most healthy eyes, the SCS is a virtual space because the choroid is in close apposition to the sclera. As fluid accumulates in physiological or pathological conditions, it separates and the space becomes real. Depending on whether the Haller and Sattler layers can be delineated and whether the suprachoroid is considered to be of scleral or choroidal origin, the number of choroidal layers can vary from 4 to 6 layers.10

FIGURE 1.
FIGURE 1.:
A, Five layers of the choroid illustrated in an SD-OCT scan. Green dotted lines mark the boundaries of the choroid (from the Bruch membrane to suprachoroidal layer). B, Enlarged image of the OCT scan (from the red box in A) shows 4 hyperreflective bands of the outer retina consisting of the internal limiting membrane (ILM), ellipsoid zone (EZ), inderdigitation zone (IZ), and RPE. Choroidal vessel layers are designated as Sattler and Haller layers distinguished by size of vessel lumen and the outermost layer is the SCL, which consists of densely packed melanocytes and loose connective tissue (C) represented by hyperreflective and hyporeflective structures on OCT (B). Scale bars represent 200 μm.

TECHNOLOGY USED TO IMAGE THE CHOROID

Ultrasonography was first used to examine the eye in 1956. It had applications in evaluating trauma, monitoring and characterizing tumors, detecting vitreoretinal disease, and ocular biometry.14 Pulses of high-frequency acoustic waves are transmitted through the eye and echoes created by reflective ocular structures are received by the ultrasound transducer. The A-mode (amplitude mode) is a 1-dimensional image display of reflected sound waves in which echo amplitude is shown along the vertical axis and echo delay (depth) along the horizontal axis. Juxtaposition of consecutive Amode scans using brightness to represent the amplitude of reflected sound waves creates a cross-sectional image, called the B-mode (brightness mode). The resolution of ultrasound imaging depends directly on the frequency or wavelength of the sound waves used. For a typical clinical ultrasound system, sound waves are in the 10 MHz region and this achieves a spatial resolution of 150 μm in biological tissue. High-frequency ultrasound has also been developed using frequencies of approximately 100 MHz to achieve axial resolution of 15-20 μm. However, high frequencies are strongly attenuated in biological tissues, leading to decreased depth of penetration and failure to image the posterior coat of the eye. As a result, ultrasound for imaging the posterior coat is typically centered at 10-20 MHz, providing an axial resolution of approximately 150-200 μm, which is only useful for visualizing gross changes in the posterior coat.12,14

Optical coherence tomography can be viewed as an optical analog of ultrasound.15 The principal difference between OCT and ultrasound is that light travels faster and its wavelength is much shorter than sound waves, allowing OCT to achieve higher image resolution. However, due to the high velocity of light, it is not possible to measure optical echo amplitude. Instead, OCT uses low coherence interferometry in which the light beam is split into an object arm (which enters the eye) and a reference arm. Analysis of the time delay and amplitude of the interference pattern generated by the backscatter of both beams are used to construct the OCT image. The first OCT device was a time domain system (TDOCT) that was able to acquire 400 A-scans per second with an axial resolution of 8 to 10 μm.16 A broadband light source at 842 nm was used and the mirror in the reference arm was mechanically moved to image at different depths.15 However, the choroid is poorly visualized using a TD-OCT device due to the light scattering from the retinal pigment epithelium (RPE), relatively low signal-to-noise ratio, and limited number of axial scans per B-scan causing lower pixel density.16 The next generation of OCT devices termed SD-OCT incorporated a spectrometer with the interferometer to simultaneously analyze the interference pattern using the Fourier transform.16,17 This technique allows the reference mirror to remain stationary as depth information is frequency encoded. As a result, scan rates of 20,000 to 52,000 A-scans per second and axial resolution of 5 to 7 μm, along with better signalto-noise ratio, can be achieved.16 However, the outer limit of the choroid and sclera cannot be reliably identified, as echoes originating from deeper tissues are more difficult to discern by spectrometer because they have higher frequency modulation than echoes closer to the zero-phase delay line.16 Most SD-OCT devices operate with the inner retina closest to the zero-phase delay line to maximize the sensitivity of the retina and vitreoretinal interface. As a result, the outer choroid is further from the zero-phase delay line with subsequent diminished signal (Fig. 2A). To improve the definition of choroidal structures, Spaide et al developed a technique called EDI using SD-OCT. This is achieved simply by moving the SD-OCT device closer to the eye to invert the image, such that the zero-phase delay line is positioned at the choroidal side of the image frame.18 Although EDI techniques improved the visualization of the choroid and sclera, these structures were not always clearly seen because the central wavelength of the light sources used in SD-OCT devices (ranging from 800-870 nm) is not optimal for deep choroidal tissue penetration (Fig. 2B).19-21 The optimal centered wavelength to image the choroid is 1050-1060, as longer wavelengths exhibit less scatter and can penetrate deeper in the tissue because they are not absorbed by water. These wavelengths are generated by rapidly tuneable laser sources that are employed in SS-OCT systems. In addition, SS-OCT utilizes a single photodiode for the detection of the interferometry signals,21-23 allowing acquisition speeds of 100,000 A-scans per second and axial resolution of approximately 5.3 μm.21 These features of the SS-OCT system improve visualization of the entire thickness of the 3 posterior coats of the eye (Fig. 2C).

FIGURE 2.
FIGURE 2.:
A comparison of OCT sections through the fovea using standard SD-OCT (A), EDI SD-OCT (B), and SS-OCT (C) shows similar clarity in choroidal structures and boundaries between B and C. Note the greater axial scan depth of 2.6 mm (vertical arrow in C) offered by the SS-OCT device as compared with 1.8 mm (vertical arrows in A and B) for SD-OCT. The reduced visibility of the outer choroidal boundary in A is due to the signal-to-noise ratio drop off as a function of distance from zero-phase delay (located at the top of the image). The EDI mode inverses the gradient of the signal-to-noise ratio drop off so that the outer choroidal boundary clarity can be enhanced by placing the zerophase delay at the bottom of the image in B.

Vascular choroidal imaging is best achieved with indocyanine green angiography and fundus fluorescein angiograph.24 They are the gold standard for visualizing choroidal blood flow.24 However, they do not provide cross-sectional anatomical information and are unable to accurately identify the depth of vascular pathology.16 These methods are also invasive because of the need for contrast dye, which has the potential to induce anaphylactic reaction.24 Several noninvasive methods to visualize choroidal blood flow have been developed. Doppler OCT measures the Doppler frequency shift, which is proportional to velocity, in each voxel of an OCT image. The combined Doppler shift and reflectivity data from each voxel allows simultaneous visualization of retinal architecture and blood flow. The so-called OCT angiography (OCTA) can also create an image of vascular anatomy by extracting backscatter light intensity fluctuation data. The variations in the backscattered light generated by moving objects within the blood vessels (eg, red blood cells) provide the contrast for visualizing blood vessels. However, unlike Doppler OCT, which can only measure flow that is oriented transversely to the imaging direction, OCTA can be used to visualize blood vessels irrespective of flow rate (in principle) and orientation.25 Laser Doppler flowmetry can also be useful for subfoveal choroidal circulation.16 However, these modalities can only provide qualitative assessment of the choroidal blood flow but not the extravascular structures.26 Magnetic resonance imaging (MRI) is another noninvasive imaging modality that can provide structural, physiological, and functional information on the choroid.27 However, it is more expensive and lacks in spatial resolution, allowing only 3 layers of the retina/choroid complex to be discriminated.27,28 Its role is limited to imaging of medium and large uveal tumors.

MORPHOLOGY OF THE RETINA AND CHOROID ON POSTERIOR SEGMENT IMAGING

Table 1 shows a summary of the structures visualized using ultrasound and OCT. Advances in choroidal imaging have allowed more detailed visualization of retinal and choroidal structures. The posterior coat of the eye was first visualized through ophthalmic ultrasonography in 1979 by Coleman and Lizzi.14 The ultrasound image appeared to correspond to what was visualized histologically, with the exception of the choroid, which was found to be twice as thick. However, this was hypothesized to be due to the absence of choroidal perfusion postmortem.14 Although the individual layers of the posterior coat in a normal eye are often difficult to delineate on ultrasound, they can be clearly seen in eyes with retinal detachment, infiltrative lesion within the choroid (eg, uveal melanoma and lymphoma), and choroidal detachment. Therefore, the role of ultrasound in precise measurement of choroidal thickness is limited in most clinical situations.

TABLE 1
TABLE 1:
Layers Visualized on Ultrasound and Optical Coherence Tomography Devices

The TD-OCT system was introduced by Huang et al29 in 1991. The first highly reflective layer visualized corresponded to the retinal nerve fiber layer, followed by the inner plexiform and outer plexiform layers as distinct bands of moderate reflectivity.30 Directly below was the hyporeflective outer nuclear layer, followed by a very thin moderate reflective band representing the inner and outer segments of the photoreceptors (IS/OS).30 The brightest and thickest reflective band represents the RPE. Weak reflectivity posterior to the RPE is considered to represent the choriocapillaris and the inner choroidal vessels. The external limiting membrane (ELM), interdigitation zone, Bruch membrane, and choriocapillaris layers are beyond the limits of resolution on the TD-OCT system and are thus blended into the IS/OS and RPE bands, respectively.

The development of SD-OCT in 2002 provided faster and higher resolution imaging, allowing additional layers in the retina to be discerned. Anterior to the RPE, the interdigitation zone, outer segments of the photoreceptors, ellipsoid and myoid zones, ELM, Henle fiber layer, ganglion cell layer, preretinal space, and posterior cortical vitreous were recognized as separate structures. Posterior to the RPE, the choriocapillaris, Haller and Sattler layers, and the choroidal scleral juncture were also more easily visible. All these structures were described by Staurenghi et al, who also proposed a consensus nomenclature and provided descriptions for the retinal structures visualized on SD-OCT.5 Although the choroid could now be seen in SD-OCT images, the signal was weak, making it difficult to reliably visualize its posterior boundary. Hence, the group use a loosely defined term, “the choroid scleral juncture,” to describe the area beneath the large vessel layer.5

In 2008, the EDI technique was developed, which led to the ability to distinguish layers in the outer choroid and sclera. In good quality images, the sclera could be clearly visualized as a thick hyperreflective zone, diminishing in reflectivity below the hyporeflective large choroidal vessels. This improved clarity of the boundary between the choroid and sclera has enabled quantitative analysis of the choroid. The CSI was first defined as the inner boundary of the sclera, which is the most common definition used by studies measuring choroidal thickness. Subsequent studies using EDI techniques noted a hyperreflective band between the outermost limit of the choroidal vessels and the moderately reflective sclera. This band was hypothesized to be the SCL, although some studies referred to this band as the CSI.19,31 Other studies using EDI techniques noted a hyporeflective band adjacent to the sclera, which they hypothesized to be the SCS. Spaide et al also reported the presence of a hyporeflective band under the CSI in some images, which was hypothesized to be the SCS.18 However, the significance of the SCS was not elucidated. Subsequent studies using EDI techniques described the SCS as a variable second layer of the SCL and discussed how its presence would affect choroidal thickness (CT) measurements.32,33

The choroid can also be visualized with the SS-OCT device, which showed the same structures as seen on EDI without sensitivity roll-off across the depth of the scan, inherent within an SD-OCT system. The uniform signal-to-noise ratio and greater scan depth axially in SS-OCT devices reduces image artefact when visualizing SCL in eyes with posterior staphyloma. Swept source OCT also revealed 2 patterns of the SCL if this structure was visible: 1) a single hyperreflective band or 2) a hyperreflective band accompanied by an adjacent hyporeflective band, which represents the SCS.4 Visualization of the CSI may be superior with SS-OCT, with one study reporting feasibility of CT measurement in 100% of eyes imaged with SS-OCT, compared with 73.54% and 68.3% of eyes imaged with EDI and non-EDI SD-OCT, respectively.21

In 2015, Ruiz-Medrano et al visualized the insertion of the inferior oblique muscle in the sclera together with a thin, hyporeflective line parallel to the choroidoscleral boundary, which was hypothesized to be the intrascleral portion of the temporal long posterior ciliary artery. They also observed that vessels in the choroid are hyporeflective due to the higher velocity of blood flow compared with retinal blood vessels, which generate hyperreflective signals.34

Traditionally, choroidal thickness is measured manually as a perpendicular line from the outer boundary of the RPE/Bruch membrane complex to the inner border of the sclera defined as the CSI.12 Measurements are often taken directly underneath the fovea, as the choroid is usually the thickest here.35 The morphology of this interface can vary across the length of the scan and between different types of pathology and different OCT devices.33 Furthermore, the definitions of the different types of CSI also vary in the literature.36 Although the standard deviation in retinal thickness measurements using SD-OCT was reported to be 12.9 μm, it was 77.4 μm in the choroid.26 Variability in choroidal thickness measurements can be attributed to poor image quality, spectrum of pathology of the subject eyes, and inconsistent definition of the outer choroidal boundary.33 The SCL, found between the outer border of the large vessel layer and inner sclera, has caused ambiguity regarding the exact location of the boundary.32 Although multiple algorithms have been proposed for evaluating automated choroidal thickness measurements, there is no gold standard. Such measurements typically exclude the SCL. Whether this layer should be included in choroidal thickness measurements requires further investigation. However, the nomenclature used to describe the choroidal layers can be standardized to avoid confusion for future definitions of the CSI.

Differences in choroidal thickness measurements from SS-OCT versus SD-OCT were generally found to be insignificant.22,37-39 In contrast, differences in pathology caused larger differences in choroidal thickness measurements. In a study by Tan et al, it was found that subfoveal choroidal thickness measurements made using SS-OCT and SD-OCT devices were very similar with mean differences ranging from 7 to 15 μm between any 2 devices.39 Although the reliability was comparable among eyes with retinal diseases and normal eyes, a higher proportion of eyes with disease showed a difference between SS-OCT and SD-OCT greater than or equal to 20 μm.39 A study by Barteselli et al40 that compared SD-OCT with SS-OCT reported that SS-OCT was similar to SD-OCT in visualizing the choroidoscleral boundary (CSB) in 90% of eyes. Eyes were given a grade from 0 to 2 indicating the visibility of the CSB. The average (± standard deviation) grading of 1.81 (± 0.39) was given to SS-OCT and 1.78 (± 0.38) for SD-OCT (P = 0.566). The sharpness of choroidal structures was found to be greater with SS-OCT than SD-OCT (P < 0.001). Matsuo et al39 postulated that choroidal thickness measurements were thicker using SS-OCT because the choroid-scleral border seen on SD-OCT scans may not be the true border. Tan et al22 noticed this phenomenon in some patients in whom there was a hyperreflective region that initially appeared to be the choroid-scleral border on the SDOCT scans, although on closer examination, the true border was seen beyond that point.39 Because differences in choroidal thickness between OCT devices were also found to be smaller among patients with thinner choroids, Tan et al postulated that in eyes with thicker choroids, a signal loss and artefacts and shadows cast by the connective tissues between the vessels might impair visualization of the choroid-scleral border more in SD-OCT than in SS-OCT, thus accounting for the greater variability.22

An important factor in standardizing choroidal thickness measurements is the definition of the CSI.32 The study by Yiu et al32 in 2013 reported that participants with a visible SCL had the greatest differences in choroidal thickness measurements. This suggests that choroidal thickness measurements can be substantially affected by how the CSI is defined. They performed choroidal thickness measurements by using 3 different landmarks to define the posterior boundary and found that choroidal thickness measurements could have a mean difference of up to 70 μm when 3 different boundaries were used to define the outermost limit of the choroid. These 3 posterior boundaries were as follows: 1) posterior vessel border to define vascular CT; 2) outer border of the SCL to define stromal CT; and 3) inner border of the sclera that includes the SCL to define total CT. This study highlighted the potential for systematic error in the reporting of choroidal thickness measurements. Therefore, it is imperative that the CSI be clearly identified in future choroidal studies and that segmentation algorithms differentiate among the 3 types of morphology. It is timely to discuss a standardized definition for the CSI.

THE CHOROIDAL SCLERAL INTERFACE

The CSI is a commonly used term in the choroidal thickness literature. Although it appears in various forms such as the choroidal-scleral junction, sclerochoroidal interface, and choroidoscleral boundary, they all refer to the zone where the choroid meets the sclera. To clearly compare the definition of the CSI in the literature, we will adhere to the guidelines proposed by Staurenghi et al regarding the use of the terminology “band” or “layer” for describing a discrete and defined lamina as opposed to “line,” which is a 1-dimensional structure.5 It is important to clearly define the CSI to enable accurate choroidal thickness measurements that can be compared across studies. In the literature, these terminologies have been used interchangeably, making it difficult to determine how each study has defined the CSI.

The posterior boundary for CT measurements was first defined as the inner surface of the sclera in the pilot study using EDI techniques by Margolis and Spaide,35 which we interpret as a line between the choroidal vessel and scleral bands. Although the SCS was observed in the original description of EDI techniques by Spaide et al,18 this was not included in choroidal thickness measurements. Subsequent studies have adopted this definition for the posterior border of the choroid.22,35,38,41,42 However, some authors have described the CSI as a hyporeflective zone,1,26 whereas others have described it as a hyperreflective zone.43,44 By definition, if the CSI is considered a line, it should not have an intensity descriptive term associated with it. We believe these authors are still referring to the same CSI; however, their description should be interpreted as measuring to the outer border of the hyporeflective choroidal vessels or the inner border of the hyperreflective sclera. Michalewska et al, who imaged the choroid using SS-OCT, were able to clearly visualize the SCL below the choroidal vessels as a hyperreflective band followed by a hyporeflective band.4 However, they defined the CSI as lying between the choroidal vessels and the SCL, aligning with the original definition of the CSI.

Several studies have described the CSI as a hyperreflective band between the choroidal vessels and sclera.19,31,33,45 Maul et al19 defined the CSI as having a width less than or equal to the RPE depending on image quality, whereas other studies described the CSI as a distinct hyperreflective band below the choroidal vessels and if present, above the hyporeflective SCS. For measuring choroidal thickness, Ikuno et al31 used the inner boundary of the CSI as the limit of the choroid, whereas both Maul and Boonarpha33 used the outer boundary of the CSI as the limit of the choroid. In EDI SD-OCT images, Yiu et al observed a hyperreflective band followed by a hyporeflective band between the choroidal vessels and sclera, which they named the choroidal stroma and lamina fusca/SCL, respectively.32 Rather than defining the suprachoroid as originating from the choroid or sclera, Yiu et al proposed 3 definitions for the CSI which were the boundaries posterior to the 1) choroidal vessels (vascular thickness), 2) hyperreflective choroidal stroma (stromal thickness), and 3) hyporeflective SCL (total thickness or lamina thickness).

A review of the literature shows that the CSI has been described as both a boundary and a band. Currently there is no consensus definition and description for the CSI. However, this needs to be standardized so that choroidal thickness can be compared across studies. As the majority of choroidal thickness studies and automatic segmentation algorithms have defined the CSI as a boundary, we believe that it should be considered as a boundary between the choroid and the sclera. Whether this boundary includes or excludes the suprachoroid depends on whether this layer is visible and how this layer is classified by the authors, as there is no universal consensus for its origin yet. Furthermore, examination of the definition and description of the CSI in the literature has highlighted the discordance in the nomenclature for the anatomic correlates of bands visualized in OCT. Correct band assignment is necessary for proper evaluation of both normal and pathological states in the retina.46

HARMONIZATION OF THE TERMINOLOGY IN DESCRIBING THE OUTER CHOROIDAL BOUNDARY

Very few studies are clear about which anatomic correlate visualized on OCT they are referring to when discussing the CSI in text and even fewer studies describe or demonstrate the appearance of the CSI on an OCT image. Often, authors use anatomic landmarks to define the CSI and assume that all readers will interpret these anatomical terms in the same way. For example, “the outer aspect of the lamina fusca, rather than the outer limit of the choroidal vessels, was the landmark used to determine the most distal aspect of the choroid and inner edge of the sclera.”34 However, a review of the literature, as outlined in the Methods section, has shown that a universal naming system for the choroidal and suprachoroidal structures observed in EDI SD-OCT and SS-OCT has yet to be established. In this section, we review the nomenclature and description of the structures visualized in EDI SD-OCT and SS-OCT. Duplicate or derivative works were not included. We also propose a nomenclature for the choroidal layers that is based on histology and harmonizes the terminology used in our review.

The nomenclature we propose for the anatomic correlates visualized on OCT is in the first column of Table 2. Table 2 also shows the nomenclature for the choroidal layers described by the 4 studies included in our review, highlighting the discrepancies in the literature compared with the reference. Papers included in this table provided both a name and a description of the structure visualized and/or demonstrated the structures in figures. All studies to date have defined the anterior boundary of the choroid as the base of the RPE/Bruch complex. However, some studies have called this layer either the RPE18,19 or Bruch membrane.4,33 Nevertheless, all the studies refer to the same structure visualized on OCT and the chosen nomenclature is merely semantics, as the OCT structure representing the RPE and Bruch membrane are usually inseparable under normal conditions.5 The number of choroidal vessel layers identified by studies varies. In some studies, the choroidal vessels are separated into 3 distinct layers, whereas other times they are collectively referred to as the choroidal vessels. However, the posterior boundary of the choroidal vessels is consistent in the literature.

TABLE 2
TABLE 2:
Proposed Nomenclature for Anatomic Landmarks Seen on EDI SD-OCT and SS-OCT Images

If the SCL is present in an OCT image, it is situated between the choroidal vessels and the sclera and visualized as either a single hyperreflective band or as a double structure consisting of a hyperreflective band followed by a hyporeflective band, where the darker band is termed the SCS. It was reported that the SCL was visible in both eyes of 41.8% of the participants in the study by Yiu et al.32 Studies have found that the visibility of the SCL depends on the status and type of disease along with systemic factors such as age.24,33 A number of studies were able to identify the double bands of the SCL. However, the anatomic correlates assigned to them differed among the groups. Povazay et al named the 2 bands the lamina suprachoroidea and the lamina fusca sclera, respectively.45 Yiu et al36 termed them the choroidal stroma and the SCL. According to histology, the choroidal stroma is the extravascular tissue containing collagen and elastic fibers, fibroblasts, nonvascular smooth muscle cells, and numerous large melanocytes that are juxtaposed to the blood vessels.10 Hence, it is considered to be incorporated with the Sattler and Haller layers. To date, no other studies have described the SCL as consisting of only a hyporeflective band. Therefore, we suggest that it is inappropriate to assign this nomenclature to 2 bands. Boonarpha et al called the 2 bands the CSI/SCL and the SCS, respectively.33 According to the reference nomenclature, the SCS is part of the SCL and hence the hyperreflective portion of the double band cannot be termed the SCL. The nomenclature for the 2 bands proposed by Michalewska et al4 aligned with the reference nomenclature.

In general, similar structures are visualized among studies on OCT images. Although some studies have been able to delineate more than 1 band in the choroidal vessels or have noted the presence of the SCL and at times the SCS within it, the choroidal layers visualized among studies are the same. Only the nomenclature used for the layers differs, causing confusion in the literature. Studies that have observed the hyporeflective band within the SCL have agreed that it represents the SCS. However, a review of the literature has revealed that there is currently no consensus nomenclature for the hyperreflective band of the SCL. Some studies have termed the hyperreflective band the CSI. However, as previously discussed, the term CSI should be reserved for the boundary between the choroid and sclera, where the SCL is classified as either of choroidal or scleral origin, if it exists. Others have incorrectly used nomenclature that has already been assigned to another layer. Thus, we propose to refer to this layer as the suprachoroidal stroma. The demarcation of the layers described in Table 2 are shown in the EDI-OCT image in Figure 3A and the relative reflectivity of each structure is shown in the corresponding intensity profile in Figure 3B.

FIGURE 3.
FIGURE 3.:
An SS-OCT image and its corresponding A-scan intensity profile at the fovea. A, SS-OCT image with structures demarcated by colored lines. B, Corresponding intensity profile where the colored lines indicate the beginning of the structures: the retina consists of the neuroretina (NSR) and the RPE. The peaks within the retina (magenta) indicate the 1) ILM, 2) ELM, 3) ellipsoid zone, and 4) RPE. Choroidal vessels (green), suprachoroidal stroma (blue), suprachoroidal space (red), and sclera (cyan) are seen below the retina. Colored lines represent the start of each layer where the average intensity between lines is indicative of the relative reflectivity used to describe OCT images in Table 2.

FUTURE DIRECTIONS

Optical coherence tomography technology will continue to advance, allowing better visualization of the posterior coat of the eye and additional published research on the choroid. It is, therefore, important to establish universal terms for describing choroidal layers and sclera and to standardize nomenclature used in the definition of the boundary between the choroid and sclera, to allow easier comparison between future studies examining choroidal thickness. This would involve defining whether the SCL and the SCS within it belong to the choroid or the sclera. Until then, we suggest that the CSI should be defined as the end of the choroidal vessels for choroidal thickness measurements so that results can be compared with the initial choroidal thickness studies. This is due to the limited signal penetration in eyes with thicker choroids or retinal pathologies that may reduce the likelihood of clearly visualizing the CSI.32 From a functionality perspective, measuring to the posterior vessel border also makes sense because choroidal thickness is usually measured as a marker for choroidal vascular perfusion.32 However, we recommend measuring the thickness of the SCL and SCS separately if observed, as they have potential in the diagnosis and treatment of various conditions.

CONCLUSIONS

As seen in histology, the suprachoroid is a transitional zone containing both choroidal and scleral elements. The border between the choroid and the sclera is, therefore, not well-defined. The definition of the choroidal scleral interface has changed with advancing OCT technology. With TD-OCT, structures beneath the RPE were difficult to discern and thus were collectively termed the choroid. Spectral domain OCT allowed deeper penetration, facilitating distinction between the choroidal vessel layers (choriocapillaris, Haller and Sattler layers) and sometimes the scleral tissue. This expanded the number of choroidal layers that can be visualized and enabled the most posterior layer, the choroid scleral juncture, to be identified. Enhanced depth imaging SD-OCT strengthened the signal deep into the choroid, allowing better delineation of the transition from choroid to sclera. The variable morphology encouraged inconsistency in the naming of the choroidal and scleral structures with multiple research groups simultaneously describing the boundary. Furthermore, the advent of EDI SD-OCT and SS-OCT allowed the visualization of the suprachoroidal layer within which there may be a suprachoroidal space. This imposed a new challenge in the standardization of the choroidal scleral interface definition with the use of inconsistent nomenclature in the literature.

We propose the CSI to be a line representing the posterior boundary of the choroid delineating the choroidal vessel layers from the sclera, rather than a separate layer, to be consistent with histology. Furthermore, the automated segmentation algorithm for the choroid has been developed based on the assumption that the CSI is a line rather than a layer. As research has not yet been able to classify the SCL as originating from the choroid or sclera, we recommend the use of descriptive terms such as hyperreflective and hyporeflective bands to label the SCL.

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Keywords:

choroidoscleral boundary; choroidal thickness; sclerochoroidal boundary; suprachoroidal space; suprachoroidal layer

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