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Normative data of outer photoreceptor layer thickness obtained by software image enhancing based on Stratus optical coherence tomography images
U C Christensen, K Kroyer, J Thomadsen, et al. Br J Ophthalmol 2008 92: 800-805

doi: 10.1136/bjo.2007.130500

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Clinical science

Normative data of outer photoreceptor layer thickness obtained by software image enhancing based on Stratus optical coherence tomography images
U C Christensen,1 K Kroyer,1 J Thomadsen,2 T M Jorgensen,2 M la Cour,1 B Sander1
1

Department of Ophthalmology, Glostrup Hospital, University of Copenhagen, Denmark; 2 Department of Optics and Plasma Research, Ris National Laboratory, Roskilde, Denmark Correspondence to: Dr U C Christensen, Department of Ophthalmology, Glostrup Hospital, Nordre Ringvej 57, DK-2600 Glostrup, Denmark; ulrikchristensen@dadlnet.dk Accepted 24 January 2008

ABSTRACT Aim: To present normative data of outer photoreceptor layer thickness obtained by a new semiautomatic image analysis algorithm operating on contrast-enhanced optical coherence tomography (OCT) images. Methods: Eight Stratus OCT3 scans from identical retinal locations from 25 normal eyes were registered and combined to form a contrast-enhanced average image. Utilising the vertical intensity gradients of the enhanced OCT images to demarcate retinal layers, thickness measurements of the outer photoreceptor- and retinal pigment epithelium layer (RPE-OScomplex) were obtained. Additionally backscattered light within the outer nuclear layer (ONL) in the fovea was registered and compared with backscattered light within the ONL in the peripheral part of the macula (Iratio-ONL). Results: The mean RPE-OScomplex thickness in the foveal centre was 77.2 mm (SD = 3.95). The RPE-OScomplex thickness in the superior macula 0.53 mm of the centre was significantly increased as compared with the corresponding inferior retina. In healthy subjects, the IratioONL was 1.06. Conclusions: Contrast-enhanced OCT images enable quantification of outer photoreceptor layer thickness, and normative values may help understanding better the relationship between functional outcome and photoreceptor morphology in retinal diseases.

averaging of a series of repetitive B-scans from identical fundus locations.4 5 By using this software to contrast-enhance OCT images, it is possible to improve the visualisation of smaller intraretinal structures, such as the reflection arising from the photoreceptor inner- and outer segment junction, as compared with standard OCT imaging.4 5 The primary aim of this study is to present normative data of outer photoreceptor layer thickness, obtained by a newly developed semiautomatic quantitative image analysis algorithm operating on contrast-enhanced OCT images. Thus, image data are obtained by the Stratus OCT system which is available in most ophthalmological departments. Besides providing thickness measurements of the photoreceptor layer, the new image-analysis algorithm also provides a measure of the backscattered light arsing from the outer nuclear layer in the foveal centre. This measurement may be relevant in the clinical evaluation of visual function in retinal diseases with induced gliosis. The alignment- and measuring software used in this study is available as shareware upon request to the corresponding author.

METHODS Participants
This methodological study included 25 normal eyes. All subjects had a negative history of previous eye disease and were examined clinically with indirect ophthalmoscopy and documented by fundus images before entering the study. Visual acuity testing was performed using Early Treatment of Diabetic Retinopathy Study (ETDRS) charts with a standard protocol at a distance of 4 m. The ETDRS chart is a logMAR chart where 8488 ETDRS letters correspond to a logMAR value of 0.0 and a Snellen ratio of 20/20.6

Optical coherence tomography (OCT) is currently the gold-standard imaging technique for diagnosing and evaluation of retinal diseases. Until recently, it has not been possible to visualise the subtle intraretinal morphological changes responsible for poor functional results in unfortunate cases, that is after surgery for macula-off retinal detachments or macular hole. Using the widely distributed time-domain Stratus OCT system, it is possible in a non-invasive manner to produce crosssectional images of the retina with 610 mm axialand 15 mm transverse resolutions. Stratus OCT thus enables visualisation of most major intraretinal layers.1 With the introduction of ultrahighresolution OCT scanners (UHR-OCT), which uses a light source with a broader bandwidth than conventional OCT, an axial image resolution of ,3 mm can be obtained.2 Thus, these scanners improve the visualisation of especially outer retinal features to a level where quantitative analyses of the photoreceptor layer are possible.3 Previous studies from our group have shown that improved OCT imaging can be achieved by alignment and
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OCT imaging
All healthy subjects were examined using the OCT3 instrument (Stratus model 3000; Carl Zeiss Meditec, Humphrey Division, Dublin, CA). The subjects underwent scanning after pupil dilation fixating on the internal fixation light during scanning. Using the Line scan acquisition protocol, 20 vertically directed (90u) B-scans from the same location were collected. Each OCT scan was 1024 pixels (2 mm) in depth and 512 pixels (6 mm) in length.
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Clinical science
As previously described in detail, it is possible to reduce speckle noise in OCT images by alignment and averaging of multiple OCT scans from identical retinal locations.5 7 Using this method of enhanced OCT, it is possible to improve the signal-to-noise ratio of the resulting average image by the square root of the number of images used.5 7 In this way, image quality can be increased to the level where the outer retinal layers are clearly discernible (fig 1).4 Because recorded speckle patterns will vary only in cases when the imaging geometry or setup is slightly modified, small movements of the head and saccadic eye movements leading to small axial movements of the retina relative to the image geometry are the basis for suppression of scatter. The selection of images used for software enhancing was based on a visual inspection of qualitatively identicallooking raw scans with a good demarcation of the vitreoretinaland chorioretinal interface and absence of artefacts due to eye movements and pupillary shadowing. Out of the 20 obtained raw scans, eight scans were selected manually for software enhancing.
The central thickness measurement in these cases reflects the thickness of the remaining RPE-OScomplex peripheral to the defect. In cases with larger (.100 mm) central IS/OS defects the algorithm measures the thickness of the remaining central RPEOScomplex layer.

Retinal thickness
The retinal thickness is defined like in standard Stratus OCT software, as the distance from the vitreoretinal interface to the top of the inner hyperreflective IS/OS layer.

Ratio of intensity of backscattered light from the outer nuclear layer (Iratio-ONL)
The ratio of light intensity of the outer nuclear layer (IratioONL) is defined as the pixel light intensity in the central part of retina at the location of the Muller cell cone as compared with a reference pixel light intensity from the ONL in the peripheral part of the macula. This ratio may be of clinical relevance when studying retinal degenerative diseases, where you might find increased backscattered light, indicating high levels of glia tissue. The ratio is calculated based on two 15615 pixel boxes; the first automatically placed by the algorithm 10 pixels above the hyperreflective external limiting membrane in the centre of the scan; the second box placed within the ONL at a location 1500 mm superiorly of the centre. However, the observer is able of modifying the box positions according to the clinical situation.

Quantitative analyses
Windows-based image-processing software was developed in C++ Builder to operate on the contrast-enhanced images in order to trace retinal layers and to quantify descriptive distance measures.8 A shortest cost-path algorithm implemented using so-called dynamic programming was used to extract smooth contours of the desired retinal layers. Specifically, the software provides measurements of the retinal pigment epithelium- and photoreceptor outer segment complex thickness (I), retinal thickness (II) and the intensity of the backscattered light from the outer nuclear layer in the central part of the retina (III) (fig 2).

RESULTS
Normative data were obtained from 25 eyes of 17 subjects, nine women and eight men. The mean age of the normal volunteers was 56.8 years (4568 years). The mean visual acuity was 86 ETDRS letters (7991 letters) corresponding to a Snellen ratio of 20/20. The mean spherical refraction was plano (23.75 sph. to +2.25 sph.). In healthy subjects, the mean thickness of the RPE-OScomplex in the foveal centre was 77.2 mm (SD 3.95). The RPE-OScomplex thickness in corresponding locations 1 mm inferior and 1 mm superior of the centre was 63.76 mm and 67.84 mm, respectively (p,0.001). The RPE-OScomplex thickness in corresponding locations 2 mm inferior and 2 mm superior of the centre was 62.16 mm and 65.36 mm respectively (p = 0.002). Accordingly, the RPE-OScomplex thickness in the superior macula from 0.5 mm to 3 mm of the centre was significantly increased as compared with the corresponding inferior retina (Mann

Thickness of the RPE-OScomplex

The three hyper-reflective layers seen in the outer part of OCT scans of the human retina are thought to arise from the retinal pigment epithelium (RPE), the RPE and photoreceptor outer segment junction (RPE/OS), and the junction between the photoreceptor inner- and outer segments (IS/OS).9 The hyporeflective band between the IS/OS- and RPE/OS layers corresponds to the photoreceptor outer segments (OS) which are longer and thus easier to visualise in the fovea (fig 1). We define the RPE-OScomplex thickness as the distance from the IS/OS line to the outer border of the RPE. In pathological cases with small breaks (,100 mm) in the IS/OS line, the algorithm will ignore the central break by generating a straight line across the defect. Figure 1 Contrast-enhanced optical coherence tomography image of a normal macula. All retinal layers are distinguishable. Enhanced optical coherence tomography imaging especially improves visualisation of the outer retinal structures. GCL, ganglion cell layer; ELM, external limiting membrane; INL, inner nuclear layer; IPL, inner plexiform layer; IS/ OS, photoreceptor inner and outer segment junction; NFL, nerve fibre layer; ONL, outer nuclear layer; OPL, outer plexiform layer; OS, photoreceptor outer segments; RPE, retinal pigment epithelium; RPE/OS, retinal pigment epithelium and photoreceptor outer segment junction. Patient consent has been obtained for publication of this figure.
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Clinical science
Figure 2 (Left) Vertical intensity profile from the central a-scan (no. 256) of a normal macula. The algorithm uses the vertical intensity profile of the contrastenhanced optical coherence tomography image for finding the shortest path between two sets of pixels in the image. (Right) Contrast-enhanced optical coherence tomography image of a normal macula with the lines of the measuring software superimposed. The outer photoreceptor- and retinal pigment epithelium layer (RPE-OScomplex) thickness is measured between the two lines in the outer retina. The retinal thickness (RT) at any point along the 6 mm long scan is calculated between the lines at the vitreoretinal interface and the photoreceptor inner and outer segment junction. The mean pixel light intensity of the outer nuclear layer at the apex of the Muller cell cone in the foveal centre (central box) is compared with reference pixel intensity from the peripheral part of the outer nuclear layer (peripheral box). Patient consent has been obtained for publication of this figure. Whitney rank sum test: p,0.001). Based on the RPE-OScomplex thickness measurements of normal eyes, a thickness profile of the 6 mm long vertically oriented scan was generated. This graphical presentation of the mean RPE-OScomplex thickness profile showed a rise in the central ,1000 mm of the scan, corresponding to the long cone photoreceptor outer segments in this region (fig 3). In healthy subjects, the ratio of intensity of backscattered light from the outer nuclear layer was identical in the central part of the macula as compared with the peripheral part (IratioONL = 1.06). The mean central retinal thickness was 161.5 mm (SD = 15.2). The normative values of the 25 healthy eyes, as obtained by the semiautomatic algorithm on the contrast-enhanced OCT images, are listed in table 1. The validity of the algorithm was tested by assessing the degree of agreement between the algorithm generated foveolar RPE-OScomplex thickness measurements versus caliper assisted thickness measurement on single Stratus OCT images. Additionally, we tested the degree of agreement between foveal retinal thickness measurements obtained from Stratus OCT software and the new algorithm. The caliper measurements were performed on the eight single Stratus OCT raw scans used in the contrast-enhanced image, utilising the built-in software of the OCT machine. The mean of the eight thickness measurements was compared with the measurement obtained Table 1 Characteristics and normative data of 25 healthy eyes obtained by the new algorithm operating on contrast-enhanced stratus OCT images
Normals (n = 25) Mean visual acuity in ETDRS letters (range) Mean spherical refraction in dioptres (range) Algorithm measurements I RPE-OScomplex in the foveola (mm) (SD) RPE-OScomplex 2 mm inferior of foveola (mm) (SD) RPE-OScomplex 1 mm inferior of foveola (mm) (SD) RPE-OScomplex 2 mm superior of foveola (mm) (SD) RPE-OScomplex 1 mm superior of foveola (mm) (SD) II Retinal thickness in the foveola (mm) (SD) III Iratio-ONL Stratus caliper measurements RPE-OScomplex in the foveola (mm) (SD) Retinal thickness in the foveola (mm) (SD) 86 (7991) Plano (23.75 to 2.25)

77.2 (3.95) 62.16 (3.05) 63.76 (3.38) 65.36 (3.77) 67.84 (3.74) 161.5 (15.2) 1.06 (0.11) 75.3 (4.00) 166.3 (15.8)

Figure 3 Mean thickness profile (black line) of the outer photoreceptor layer (outer photoreceptor- and retinal pigment epithelium layer (RPEOScomplex)) of 25 normal eyes as obtained vertically on a 6 mm long contrast-enhanced optical coherence tomography image. Black punctuated lines: 2SD of the mean.
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For comparison reasons, values of foveolar RPE-OScomplex thickness and central retinal thickness, as obtained manually by the Stratus OCT caliper measuring tool, are also provided. ETDRS letters, number of letters seen on the Early Treatment of Diabetic Retinopathy Study Chart (8488 letters corresponds to 20/20); Iratio-ONL, central- versus peripheral pixel light intensity of the outer nuclear layer; RPE-OScomplex, retinal pigment epithelium and photoreceptor outer segment thickness.

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Clinical science
from the enhanced OCT image. All caliper measurements were performed in a masked set-up, that is without any knowledge of the corresponding algorithm generated values. Specifically, measurements of outer photoreceptor layer thickness were obtained by positioning the centre of the caliper-crosses directly at the inner- and outer borders of the hyperreflective layer in the outer retina. Figure 4A,B shows the two scatter diagrams where all data points are near the line of equality. Figure 4C,D shows a plot of the difference between the methods against their mean. We find discrepancies between the Stratus algorithm and the new algorithm of up to 11 mm in foveal retinal thickness measurements, and between the manual caliper method and the automatic algorithm of up to 9 mm in RPE-OScomplex thickness measurements. value when assessing retinal reactions to degenerative diseases or surgical trauma. Thus, increased levels of backscattered light might indicate high levels of glia tissue. Validation analyses compared thickness measurements obtained manually using Stratus OCT software with thickness measurements from our new semiautomatic algorithm. We found discrepancies between the two methods of up to 11 mm in retinal thickness measurements and up to 9 mm in RPE-OScomplex thickness measurements. These small differences are acceptable in daily clinical evaluations; however, the new algorithm has one major advantage over the Stratus caliper measurements in being automatic and independent of observer variations. The method used in this study for suppressing image noise and speckle has previously been presented by Sander and Jrgensen.4 5 By optimising the backscatter of the OCT scans the photoreceptor- and retinal pigment epithelium layers will be clearly visible thus enabling quantitative measurements. Also, the integrity of the IS/OS junction which is an important indicator for restoration of visual function1016 can easily be assessed in the contrast-enhanced OCT images. The methodology of this study of course is limited by possible sampling errors introduced by the alignment- and averaging procedure when sampling the enhanced OCT images. Aligning raw scans which are slightly decentred will lead to misinterpretations of subtle intraretinal changesfor example

DISCUSSION
Contrast-enhanced OCT imaging was capable of quantifying the outer photoreceptor layer in healthy subjects. We have presented normative values of outer photoreceptor layer thickness and demonstrated a difference in outer photoreceptor layer thickness between corresponding areas of inferior and superior macula. Additionally, we have introduced the ratio of intensity of backscattered light from the outer nuclear layer in the central part of the retina as compared with the peripheral part. This ratio is close to 1 in healthy subjects but may have

Figure 4 (A, B) Scatter plots of foveal retinal thickness and foveolar outer photoreceptor- and retinal pigment epithelium layer (RPE-OScomplex) thickness measured with standard Stratus optical coherence tomography (OCT) software and with the new semiautomatic algorithm. (C, D) Difference against the mean for foveal retinal thickness data and foveolar RPE-OScomplex thickness measured using Stratus OCT software and with the new semiautomatic algorithm. The RPE-OScomplex thickness was measured using Stratus OCT software by manually positioning the centre of the calipercrosses directly at the inner- and outer borders of the hyper-reflective layer in the outer retina.
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Clinical science
underestimation of central RPE-OScomplex thickness. Therefore, it is important that each scan used in the image enhancing is selected manually after inspection for qualitative identical images. Scans which are obviously decentred should be rejected. Because the Stratus OCT used in this study does not contain an eye-tracking system, we have no possibility to test for 100% identical retinal scan location, except than to visually inspect and compare the 20 (presumed) identical scans before running the software alignment procedure. However, the basis for noise reduction is that the recorded speckle patterns will wary only in cases when the image geometry is slightly modified; therefore small movements of the retina relative to the imaging geometry during image recording is necessary for increasing the signal-tonoise ratio of the enhanced image. This means that the loci of the A-scans scatter around the ideal scan path and some transverse resolution will be lost in the combined image as compared with that of a singe B-scan. However, due to the increase in signal to noise ratio by 34 times, segmentation and characterisation of the retinal layers is facilitated. Regarding axial measurements multiple scattering events in especially outer retinal layers theoretically may overestimate thickness measurements slightly. We have previously shown that the lateral resolution of the average image is close to 25 mm and the axial resolution below 10 mm, indicating a high-quality image.5 Although ultrahigh-resolution OCT systems give a better resolution,9 these systems will not be available for most ophthalmological departments in the near future. Thus, one important strength of image enhancing as described by Sander and Jrgensen4 5 is that image data are provided by the Stratus OCT, which is found in most ophthalmological departments and large clinics. New spectral-domain OCT (SD-OCT) systems are now available with simultaneous capture of the OCT image and the fundus image (Cirrus HD-OCT, Carl Zeiss Meditec; Spectralis HRA+OCT, Heidelberg Engineering). These systems ensure precise registration between the OCT scan and the fundus image, and are potentially capable of performing these measurements in a more satisfying way by shortening the time over which images are acquired. With such a system, one needs only to perform the axial registration when combining a series of recordings to form an enhanced image. The first report using SD-OCT with multiple B-scan averaging has just recently been published,17 but unfortunately this study is only qualitative and does not provide quantitative measurements of the intraretinal layers. Additionally the caliper tools of the software in these scanners are subject to potentially considerable interobserver variations due to the very small screens allocated when placing the calipers. After considering these possible confounders, it is our experience that quantification of contrast-enhanced images is useful in research and clinical decision-making of retinal diseases where the integrity of the photoreceptor layer and thus central vision may be compromised. The normative values of outer photoreceptor layer thickness (RPE-OScomplex), as presented in this study, therefore may be valuable. Additionally, the normative value of backscattered light the central part of retina (Iratio-ONL) may be valuable when studying retinal reactions to surgical intervention, that is after macula-off retinal detachment or full-thickness macular hole. Besides presenting normative values of the outer photoreceptor layer, we found a significantly thicker outer photoreceptor layer in the superior macula as compared with the inferior macula. To our knowledge, there is no evidence of a difference in retinal morphology between the superior and inferior macula in humans. However,
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our observation supports recent observations of significantly better reading performance in 6u (<1444 mm) of eccentric viewing when using the superior retina as compared with the inferior retina.18 During the conduction of this study, we found that the Stratus OCT algorithm had difficulties in detecting the retinal boundaries used for retinal thickness measurements in some cases. Especially in cases with irregular macular surface configuration or defects/breaks in the normally homogenous IS/OS-line, the Stratus OCT algorithm often showed errorbased patterns. Previous reports have addressed this erroneous retinal thickness measurements in eyes with macular pathology.1922 We found that contrast-enhanced OCT imaging and automated delineation were superior to the Stratus OCT algorithm in detecting the retinal boundaries in these cases. Thus, we expect the new algorithm will find good applicability in cases with retinal pathology, where relatively small errors of the Stratus algorithm may have extensive affects on thickness measurements. In conclusion, the present study for the first time has introduced normative values of outer photoreceptor layer thickness and demonstrated a difference in outer photoreceptor layer thickness between corresponding areas of inferior and superior macula. Our hope is that the objective thickness measurements on contrast-enhanced OCT images can aid assessing and understanding better the relationship between functional outcome and photoreceptor morphology after resolution of retinal diseases involving the macula.
Funding: The Danish Eye Health Society; The Danish Medical Research Council; The John and Birthe Meyer Foundation. Competing interests: None. Ethics approval: Approval was obtained from the local Committee on Biomedical Research Ethics. Patient consent: Informed consent according to the tenets of the Declaration of Helsinki was obtained from all subjects before entering the study

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