Retinitis pigmentosa (RP) is an inherited retinal dystrophy characterized by the degeneration of retinal pigment epithelium (RPE), loss of photoreceptors, and variable atrophy of the choriocapillaris, leading to localized areas of clinically visible chorioretinal atrophy and, consequently, a dramatic reduction in visual function.1–4 RP usually affects only the eyes, but rarely, systemic associations such as sensorineural deafness in Usher Syndrome and mental retardation, hypogonadism, and polydactyly in Bardet-Biedl and Laurence-Moon syndromes may occur in addition to the visual impairment.5
Clinically, RP is characterized by waxy optic disk pallor, arteriolar narrowing and hyalinization, and mild pigmentary changes, which typically occur in the early course of the disease.1–4 Pigmentary changes are clinically characterized as bone spicules, diffuse granularity, and stippling and clumping of the pigment occurring in response to the degenerating photoreceptors, outer retinal and RPE atrophy, and migration of the RPE cells into the inner retina.1–4
Histopathological studies have confirmed RPE, photoreceptor, and choriocapillaris degeneration localized to the areas of clinically apparent atrophy in RP.1–3 Studies in animal models have also shown that RPE cell loss subsequently leads to choriocapillaris atrophy,6,7 and reduction in the levels of vascular endothelial growth factor (VEGF) derived from the RPE cells is suggested as a causative factor for their degeneration.8
Recent studies have demonstrated the contribution of neurovascular remodeling in the pathogenesis of RP.9,10 Using retinal function imaging technologies, low retinal blood flow velocities have been demonstrated, typically in response to darkness and at a very early stage of the disease, corresponding to the known decrease in retinal vessel diameters on ophthalmoscopic examination of patients with RP.11–14 In addition, altered choroidal hemodynamics has also been reported in patients with RP.14
Efficient and more sensitive spectral-domain optical coherence tomography (SD-OCT) allows for the visualization of the choroid up to the sclera, owing to a better penetration, high-speed acquisition, three-dimensional imaging, image averaging, and resolutions up to a micron scale.16,17 Studies have successfully demonstrated the measurement of choroidal thickness in normal and pathologic states such as age-related macular degeneration, diabetic retinopathy, and central serous chorioretinopathy using different SD-OCT devices.15,18–24 A recent study evaluated choroidal thickness in eyes with RP.25 To the best of our knowledge, however, a description of the morphological changes in the choroid including the analysis of its vascular layers in eyes with RP using SD-OCT imaging has not been performed to date.
Given that the choroid is involved in many posterior segment pathologies, a description of its refined details in terms of its morphology and vasculature may be important clinical parameters for diagnosis and management of retinal diseases. Thus, in view of the clinically observed reductions in the retinal blood vessel diameters and changes in the hemodynamics of retinal and choroidal vessels in patients with RP,11–15,26,27 this study aimed to analyze changes in the morphology and the vascular layers of the choroid in eyes with RP using SD-OCT.
Patients and Methods
A retrospective review identified 14 patients with RP (14 eyes) and 33 healthy subjects (33 eyes) who underwent high-definition one-line raster scanning at the New England Eye Center, Tufts Medical Center, in Boston, Massachusetts, between February 2009 and September 2011.
The diagnostic criteria for RP were based on ophthalmic history, clinical appearance, visual field testing, and in selected cases, fluorescein angiography and electroretinogram (ERG). Patients with concomitant posterior segment pathologies were excluded. Medical chart review was performed to obtain data regarding the type and duration of diagnosis, best corrected visual acuity (BCVA), clinical appearance, and automated central retinal thickness measurements generated by the macular cube scan protocol on SD-OCT. The healthy subjects had a BCVA of 20/20, underwent fundus examination, and were found to have no retinal or choroidal pathology. This study was approved by the institutional review board of Tufts Medical Center and is adherent to the tenets of Declaration of Helsinki.
SD-OCT scanning was performed using Cirrus (Carl Zeiss Meditec, Dublin, CA), which operates at a wavelength of 840 nm. The scanning protocol was the high-definition (HD) one-line raster, which is a 6-mm line scan and consists of 4,096 A-scans, an imaging speed of 27,000 A-scans per second, and 5-μm resolution. It acquires 20 frames at the same retinal location that are then averaged together to increase the signal-to-noise ratio. This allows for a better visualization of the choroid. The images were taken in the usual manner and were not inverted to bring the choroid in closer proximity to the zero-delay line, because image inversion using the Cirrus software results in a low-resolution, pixilated image. The enhanced depth imaging (EDI) protocol, which is a modified form of the HD one-line raster protocol within the Cirrus HD-OCT system in that it sets the choroid closer to the zero-delay line to allow better visualization of the choroid, was not employed in the present study because it was not available on the Cirrus device at the time these scans were performed. All scans had an intensity of 6/10 or greater and were taken as close to the center of the fovea as possible, such that the thinnest point of the macula was imaged in both groups to avoid any discrepancies in the analysis of the morphological features and vascular layers of the choroid due to slight differences in positioning. A single operator trained in acquiring OCT images performed all the imaging. One eye per RP patient that had a clearly identifiable choroid-scleral interface was selected for analysis. For comparison, one eye from each subject in the control group was selected randomly for the purpose of analysis.
Morphological Description of Choroid
Two independent raters experienced in analyzing OCT images evaluated the choroid for morphological characteristics in both groups. A third experienced rater was consulted when the two raters disagreed, and majority determination was used for the purpose of analysis. The clarity of the choroid-scleral interface was examined throughout the 6-mm line scan owing to its importance for accurate choroidal thickness and morphological analysis. The contour and shape of the choroid-scleral interface was evaluated and was labeled as either being (a) convex (or “bowl-shaped”) or (b) S-shaped (having an irregular or concave-convex-concave shape with more than one inflection point). The site of the thickest point of the choroid was identified. The location of this point was compared to the overlying retina. It was defined as being subfoveal when the thickest choroidal point was either exactly beneath the foveal center or within 100 μm nasal and 100 μm temporal to the foveal center. Thus, if the thickest point of the choroid fell within a 200 μm (0.2 mm) region beneath and centered on the foveal center, it was defined as being subfoveal. Where exaggerated thinning of the choroid was observed subjectively, the choroidal thickness was measured (as described below) at that location, and focal thinning was labeled if the choroidal thickness at the measured location was 50% less than that of the mean choroidal thickness in healthy eyes at the corresponding location. The mean choroidal thickness measurements in healthy eyes reported previously29 were used as a reference to define focal thinning in eyes with RP. These definitions of the various features of the choroid have been described previously.30,31
Choroidal Thickness Measurements
Two independent raters experienced in analyzing OCT images measured choroidal thickness perpendicularly from the outer edge of the hyperreflective RPE to the inner border of sclera at the fovea, and at 500 μm intervals up to 2,500 μm temporal and nasal to the fovea (11 locations), using the Cirrus linear measurement tool in both groups. The average of the two observers’ measurements was used for the purpose of analysis.
Large Choroidal Vessel Layer Thickness Measurements
Histologically, the luminal diameter of the large choroidal vessels (including both arteries and veins) in healthy eyes have been measured to range from 28.2 ± 11.2 μm to 37.1 ± 12.5 μm.28 However, since histological analysis may lead to alteration due to postmortem changes or processing artifacts,28 it is difficult to delineate the choroidal vascular layers separately. We conducted a pilot study in which the smallest visible large choroidal vessel at any location, visible in close proximity to the choroid-scleral interface on SD-OCT images of 42 healthy eyes, was measured in the nasal-temporal plane using the Cirrus linear measurement tool by two independent raters experienced in analyzing OCT images. The average measurement of the two observers was calculated. The mean diameter of the smallest visible large choroidal vessels in healthy subjects was 100 μm (range: 86 μm to 108 μm), which was then used as a cut-off for defining a large choroidal vessel for the choroidal vasculature analysis on SD-OCT. This pilot has been described previously.30,31
For the large choroidal vessel layer (Haller’s layer) thickness measurements, the choroidal thickness at the fovea was measured in both groups. A large choroidal vessel measuring at least 100 μm, visible in close proximity to the choroid-scleral interface and located in the closest proximity to the fovea, was selected, and a perpendicular line from the innermost point of that vessel was drawn, intersecting the choroidal thickness measurement line. The large choroidal vessel layer thickness was obtained at the fovea perpendicularly from the inner border of the sclera to the intersection point on the choroidal thickness measurement line. The large choroidal vessel layer thickness was subtracted from the total choroidal thickness to obtain the distance between the large choroidal vessel layer and the Bruch’s membrane–RPE complex, corresponding histologically to the medium choroidal vessel layer (Sattler’s layer) and the choriocapillaris layer (medium choroidal vessel layer–choriocapillaris layer complex). This method is illustrated in Figure 1 and has been described previously.30,31 The ratio of the large choroidal vessel layer thickness to choroidal thickness was calculated to determine the contribution of large choroidal vessel layer to the overall choroidal thickness in both groups. Two independent raters experienced in analyzing OCT images performed all the measurements. The average of the two observers’ measurements was used for the purpose of analysis.
Figure 1. Illustration of the method used to analyze the choroidal vasculature. OCT image of a healthy eye showing analysis of the choroidal vascular layers beneath the fovea. Blue asterisk represents the large choroidal vessel seen in the closest proximity to the fovea, and closest to the choroid-scleral interface, which was used for the large vessel layer measurements in this case. Number in red represent measurements obtained using the Cirrus linear measurement tool. CT = choroidal thickness; LCVL = large choroidal vessel layer.
Data were expressed as mean ± standard error of the mean. Spearman’s correlation was used for assessing the inter-observer correlation. Mann-Whitney test was used to determine the difference in the choroidal thickness and the subfoveal large choroidal vessel layer thickness in both groups. Spearman’s correlation was used to evaluate the association of subfoveal choroidal thickness with central retinal thickness, BCVA, and duration of diagnosis, as well as the association of the subfoveal large choroidal vessel layer thickness with central retinal thickness in eyes with RP. A 95% confidence interval and a 5% level of significance were adopted; therefore, results with a P value less than or equal to 0.05 were considered significant. All statistics were performed using GraphPad Prism 5.0 software for Macintosh (Graph-Pad Software, La Jolla, CA).
The demographic and clinical characteristics of the RP patients and healthy subjects are depicted in Table 1. There was no significant difference between the mean ages (P = .23) and the mean myopic refractive error (P = .41) of the two groups.
Table 1: Demographic and Clinical Characteristics of Study Subjects
Morphological Description of Choroid
A summary of the morphological description of the choroid and representative images with illustration of morphological characteristics in both groups is depicted in Table 2 and Figure 2, respectively.
Table 2: Choroidal Morphological Features of Study Subjects
Figure 2. Analysis of the choroidal morphology in healthy eyes and eyes with retinitis pigmentosa (RP). (A) Representative OCT image of a healthy eye. Note that the choroid is thinnest nasally, thickest beneath the fovea (red arrow) and thins out temporally. Red line represents the smooth, convex (or “bowl”) shape to the border of the choroid and sclera and yellow arrow represents one point of inflection. (B) Representative OCT image of an eye with RP. Note the exaggerated nasal thinning (green arrow) and an irregular or S shape to the border of the choroid and sclera (red line) with more than one inflection point (yellow arrows). The thickest point of the choroid is not under the fovea and is temporally located (red arrow).
Choroidal Thickness Measurements
Mean choroidal thickness at all locations was significantly lower in eyes with RP when compared to healthy eyes (P = .01; Figure 3), All measurements had a strong inter-observer correlation (r = 0.89; P = .001). There was a significant reduction in the subfoveal choroidal thickness in eyes with RP when compared to healthy eyes (P = .04). Mean choroidal thickness in healthy eyes showed a pattern of thinnest choroid nasally, thickening in the subfoveal region and thinning again temporally. This pattern was consistent with prior studies of choroidal thickness in healthy eyes.29 However, the maximal choroidal thickness was not subfoveal, and exaggerated nasal thinning was observed in nine of 14 (64%) eyes with RP.
Figure 3. Choroidal thickness measurements. Representative OCT image of a healthy eye (A) and an eye with retinitis pigmentosa (B) showing choroidal thickness measurements using the Cirrus linear measurement tool at 11 locations (red lines and numbers). (C) Graph of the mean choroidal thickness, showing thinning of the choroid at all locations in eyes with RP, when compared to healthy eyes. P value represents the results of Mann-Whitney test. T = temporal; N = nasal.
There was no association of subfoveal choroidal thickness and central retinal thickness (r = 0.20; P = .8) or subfoveal large choroidal vessel layer thickness and central retinal thickness (r = 0.35; P = .28) in healthy eyes. In eyes with RP, subfoveal choroidal thickness had no association with the duration of disease or BCVA (P = .69 and P = .34, respectively). However, there was a strong positive correlation between subfoveal choroidal thickness and central retinal thickness (r = 0.65; P = .006) and subfoveal large choroidal vessel layer thickness and central retinal thickness (r = 0.55; P = .03), indicating that central retinal thickness decreases as choroidal thickness and large choroidal vessel layer thickness decrease in eyes with RP (Figure 4).
Figure 4. Correlation of central retinal thickness with choroidal thickness and large choroidal vessel layer thickness in eyes with RP. Graphs representing a strong positive correlation between the central retinal thickness and subfoveal choroidal thickness (A) and central retinal thickness and subfoveal large choroidal vessel layer thickness (B). The r and P values represent results of Spearman’s correlation.
Large Choroidal Vessel Layer Thickness Measurements
The mean total choroidal thickness and large choroidal vessel layer thickness were significantly lower in eyes with RP when compared to healthy eyes (Table 3), suggesting a preferential thinning of the choroid favoring the large choroidal vessel layer in eyes with RP. All measurements had a strong inter-observer correlation (r = 0.85; P = .001).
Table 3: Subfoveal Large Choroidal Vessel Layer Thickness Measurements Relative to Subfoveal Total Choroidal Thickness Measurements
Using SD-OCT, the present study demonstrates alterations in the choroidal morphology and a reduction in choroidal thickness in eyes with RP when compared to healthy eyes. It further demonstrates an exaggerated thinning of the choroid favoring the large choroidal vessel layer in eyes with RP. Previous studies have demonstrated the validation of the methods used in the present study to assess the morphology and vascular layers of the choroid in healthy eyes30 and eyes with diabetic retinopathy.31 This is the first study describing the morphology of the choroid and analysis of its vascular layers in eyes with RP using SD-OCT.
The choroid has been evaluated by techniques such as indocyanine green angiography32 and laser Doppler flowmetry,14,32–34 which analyzes the blood flow in the choroidal vessels. These techniques are used as a standard for the assessment of abnormalities in the vessels or blood flow changes, hence providing a better clinical understanding of choroidal changes in various ocular diseases. The advantage of SD-OCT imaging however, is the three-dimensional information and better penetration through the hyperreflective RPE, thereby providing precise anatomic details of the RPE as well as the choroid. The present study showed that the choroid is irregular, concave-convex-concave, or S-shaped; the thickest point of the choroid is not subfoveal; and focal thinning of the choroid typically in the nasal region is observed in eyes with RP. These changes in the choroidal parameters may have relevance clinically when assessing the stage and progression of RP.
Yeoh et al15 previously demonstrated marked thinning of the choroid in inherited retinal dystrophies other than RP using EDI on SD-OCT, while Dhoot et al25 recently described thinning of the choroid in eyes with RP. Based on the stage of the disease and associated genetic factors, the choroid in inherited retinal dystrophies is left with only a residual layer of the large choroidal vessels, due possibly to the loss of both the medium choroidal vessels and choriocapillaris.15 The currently available SD-OCT systems are unable to resolve the choriocapillaris and the medium-sized choroidal vessels, thereby making it difficult to assess these layers separately. Histological studies have determined the choriocapillaris layer to form approximately 5% to 10% of the choroid.35 At the current resolution, while the choriocapillaris and the medium-sized choroidal vessels could not be resolved separately using the Cirrus HD-OCT, the large choroidal vessel layer delineation was achieved in the present study with a strong inter-observer agreement. This study found a significant thinning of the choroid, with a preferential thinning of the large choroidal vessel layer in eyes with RP using the methods described. This was an interesting observation in that previous studies using the conventional histological analysis and animal models of RP have demonstrated degeneration of typically the choriocapillaris in regions of atrophy.1–3,6,7 While the present study did not correlate the degree of choroidal thinning with the genetic data and the severity of the disease, evidence has previously shown that these parameters may in fact contribute to choroidal thinning.15 Such an analysis could not be performed in the present study due to lack of genetic data in most of the RP patients. We hypothesize that the thinning of the large choroidal vessel layer may be due to certain genetic factors or an advanced stage of the disease in our patient population. However, a definite comment cannot be made in this regard, and further studies with a larger sample size are warranted to correlate these parameters with the degree of choroidal vascular changes. In addition, the present study also found a strong positive correlation between subfoveal choroidal thickness and central retinal thickness and the subfoveal large choroidal vessel layer thickness and central retinal thickness, suggesting that retinal and choroidal degeneration occur simultaneously in eyes with RP.
Future imaging technologies such as OCT systems with better resolution and longer wavelengths may provide a better penetration into the choroid and visualization of its vasculature in greater detail.36,37 Doppler OCT may evaluate in detail the volume of the choroid as well as the blood flow within the choroidal vessels.38–40 En-face imaging could allow for three-dimensional visualization of the OCT data in a fundus projection, which could potentially allow for better visualization of the choroidal vascular layers,41 in that the delineation of the medium-sized vessels and choriocapillaris separately may be possible. Such an assessment of the choroidal vasculature may provide better insight into the effects of RP and other disease states on the choroid vasculature.
In inherited retinal dystrophies such as RP, EDI can provide a better view of the choroid-scleral interface,15 given that the hyperreflectance due to the disruption of the RPE in these patients may sometimes obscure a clear view of the choroid-scleral interface. Unfortunately, EDI scans were unavailable for our patients. To control for the plausible discrepancies in our observations and measurements due to an obscure visualization of the choroid-scleral interface in some of our RP patients, this study only selected one eye from each RP patient, in which the choroid-scleral interface was clearly visible for the purpose of analysis.
In conclusion, this study demonstrates an alteration in the choroidal morphology and a reduction in choroidal thickness with preferential thinning of the large choroidal vascular layer thickness in eyes with RP when compared to healthy eyes. This is the first study describing the morphological analysis of the choroid including the evaluation of its vasculature in eyes with RP using SD-OCT. Further studies involving correlation of the disease stage and genetic data with choroidal changes may provide further insight into the involvement of choroid in RP and other inherited retinal dystrophies.
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Demographic and Clinical Characteristics of Study Subjects
|Characteristic||Healthy Subjects||RP Patients|
|No. of patients (eyes)||33 (33)||14 (14)|
|Age (years)||51 (22–79)||46 (21 to 71)|
|Mean myopic refractive error||1.35 (range: 1.20 to 1.75)||1.65 (range: 1.00 to 2.15)|
| Men||16 (48.5%)||3 (21.5%)|
| Women||17 (51.5%)||11 (78.5%)|
| Usher syndrome||N/A||3 (21.4%)|
| Bardet-Beidl syndrome||N/A||1 (7.1%)|
| Autosomal recessive RP||N/A||1 (7.1%)|
| Unspecified form of RP||N/A||9 (64.2%)|
|Mean duration of diagnosis (years)||N/A||17.5 (range: 2 to 55)|
|BCVA||20/20||20/20 to light perception|
| Normal||33 (100%)||0|
| Macular atrophy||N/A||3 (21.4%)|
| CME||N/A||3 (21.4%)|
| RPE atrophy||N/A||8 (57.1%)|
| Bony spicules||N/A||4 (28.5%)|
| Attenuated retinal vessels||N/A||6 (42.8%)|
| Disk pallor||N/A||4 (28.5%)|
Choroidal Morphological Features of Study Subjects
|Choroidal Morphology Feature||% of Healthy Eyes (n = 33)||% of Eyes with RP (n = 14)|
|“Bowl” shape to the choroid-scleral interface (1 point of inflection)||100%||21.4%|
|Clarity of the choroid-scleral interface throughout the 6-mm line scan||79%||75%|
|Thickest point of choroid under the fovea||97%||35.7%|
|Focal thinning of the choroid||0%||64%|
Subfoveal Large Choroidal Vessel Layer Thickness Measurements Relative to Subfoveal Total Choroidal Thickness Measurements
|Choroidal Vessel Parameter||Healthy Eyes (n = 33)||Eyes With RP (n = 14)||P Value|
|CT (μm)||273.4 ± 12.4||229.5 ± 17.8||0.04|
|LCVL thickness (μm)||218.9 ± 14.5||173.1 ± 12.4||0.02|
|MCVL/ choriocapillaris layer complex (μm)||54.5 ± 2.8||57.3 ± 8.0||0.3|
|Ratio of LCVL to CT||0.80 ± 0.01||0.69 ± 0.02||0.001|