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ay,21From the Department of Ophthalmology, General Hospital of Vienna, Medical University of Vienna, Vienna, Austria; the 2Center for Biomedical Engineering and Physics, Christian Doppler Laboratory, Medical University of Vienna, Vienna, Austria.
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Abstract |
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METHODS. One hundred forty eyes with a distinct disease in each of the posterior pole compartments were examined with 3-D UHR OCT. 3-D imaging was performed with a high axial resolution of 3 µm with a compact, commercially available, ultra–broad-bandwidth (160 nm) titanium:sapphire laser at a video rate of up to 25 B-scans/s. Each tomogram consisted of 1024 x 1024 pixels, resulting in 25 megavoxels/s.
RESULTS. 3-D UHR OCT offers high-precision 3-D visualization of macular diseases at all structural levels. The UHR modality allows identification of the contour of the hyaloid membrane, tractive forces of epiretinal membranes, and changes within the inner limiting membrane. The system provides quality 3-D images of the topographic dynamics of traction lines from the retinal surface down to the level of the photoreceptor segments. Intraretinal diseases are identified by their specific location in different layers of the neurosensory ultrastructure. Photoreceptor inner and outer segments are clearly delineated in configuration and size, with a characteristic peak in the subfoveal area. The microarchitecture of choroidal neovascularization is distinctly imaged, related leakage can be identified, and the volume can be quantified.
CONCLUSIONS. High-speed UHR OCT offers unprecedented, realistic, 3-D imaging of ocular diseases at all epi-, intra- and subretinal levels. A complete 3-D data set of the macular layers allows a comprehensive analysis of focal and diffuse diseases, as well as identification of dynamic pathomechanisms.
To evaluate the potential of UHR OCT for enhanced visualization of intraretinal structures and to provide a distinct base for correct interpretation of in vivo ophthalmic UHR OCT tomograms, preclinical studies have been conducted to correlate UHR OCT cross-sectional images of in vivo porcine9 and monkey10 (Macaca fascicularis) retinas with histologic sections of the identical specimen. The results of these comparative studies allow extraction of structural information from in vivo UHR ophthalmic OCT tomograms and substantially reduce the ambiguities in data interpretation. Analogies with histologic features allow correlation of about 10 distinct intraretinal layers with corresponding signals in UHR OCT tomograms. Recently, this novel OCT technology has been used in a clinical setting for the first time, enabling in vivo cross-sectional imaging of macular diseases with an unprecedented axial resolution of 
3 µm, giving the technology unique value in clinical imaging.4 11 12 13
In clinical practice, though, to detect early stage disease, to follow disease progression, and to monitor therapy-induced changes, it is best not to rely on a few B-scans (tomograms) randomly taken at sites that are presumptively chosen during image acquisition. An imaging modality, accomplishing UHR visualization of all intraretinal layers within a few seconds across a volume large enough to include the entire dimension of the investigated disease would clearly have a significant clinical impact on retinal diagnosis. With such a comprehensive 3-D technique, the decision regarding a specific imaging site would not have to be made during the process of data acquisition. Instead, the complete 3-D data volume could ideally be analyzed in more detail and at various locations after image processing, similar to the procedures used in computed tomography or magnetic resonance imaging.
First-generation, UHR OCT systems perform visualization of the tissue microstructure in the so-called time domain. Depth information in this case is obtained as a function of distance or time. State of the art delay lines have been developed to provide high scanning speeds of up to 8 kHz (i.e., 8000 A-scans per second14 ), with the drawback of lower system sensitivity for faster scanning speed and/or broader optical bandwidth to accomplish UHR and longer depth range. A potential alternative to time domain OCT for high-speed imaging is a technique in which the entire spatially resolved tissue reflectance (A-scan) is obtained simultaneously, and no depth scanning is necessary.15 16 17 18 This technique has been referred to in the literature as Fourier domain OCT, spectral domain OCT, frequency domain OCT, and swept source OCT. The technical improvement can be accomplished either by dispersing the interferometric information in space by using a spectrometer setup (also referred to as Fourier domain OCT or spectral domain OCT in the literature) or by encoding information in time by tuning a monochromatic light source in combination with a single photodetector (also referred to in the literature as frequency domain OCT or swept source OCT). The acquisition speed for both approaches—using a spectrometer as a detector or a tuneable light source—is then mainly limited by the read-out rate of the charge-coupled device (CCD) camera or the tuning speed of the light source, respectively. Because of the decoupling of scanning range and electronic detection band width, both approaches offer a significant sensitivity advantage, allowing a dramatic increase in line rate (A-scan rate) without loosing imaging performance in comparison to time domain OCT.19 20 21 Accordingly, OCT with a spectrometer used for detection has recently been demonstrated to offer high speed,22 23 24 UHR,25 26 27 and functional imaging.28 29
One possible approach to performing 3-D retinal imaging is an extension of time domain OCT called en face OCT.30 31 32 33 34 This technique combines the transverse scanning approach of a confocal scanning laser ophthalmoscope (cSLO) with the depth-sectioning capabilities of OCT. This technique represents a cSLO with improved axial resolution by more than one order of magnitude, allowing high transverse resolution en face (also called C-mode scan) imaging. So far, 64 planes in depth, each consisting of 256 x 128 pixels, enabling approximately 2 million voxels (3-D data points)/second, resulting in limited cross-sectional (B-scan) visualization capability and a pixelized tomogram appearance.
In this pilot study, we present the first clinical evaluation of a second generation UHR OCT system with 3-D UHR OCT (3-D UHR OCT), based on Fourier domain OCT, providing video imaging of retinal diseases of all compartments (epiretinal, intra-, subretinal) of the posterior pole of the eye.
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For the present study, the retinal exposure had to account for the ultra–broad-bandwidth light generated by the laser. The ANSI standards36 for retinal exposure account for wavelength, exposure duration, and multiple exposures of the same spot of the retina. Because the laser source generates femtosecond pulses, the laser output was coupled into a 100-m-long optic fiber that was used to provide dispersive stretching of the pulse duration to hundreds of picoseconds. This technique reduces the peak pulse intensities by several orders of magnitude and, because the laser operates at an 80-MHz repetition rate, the output can be handled as a continuous wave. OCT imaging was performed with axial scans at rates ranging from 10,000 to 25,000 Hz, resulting in a retinal exposure time at each point where an axial scan of 40 to 100 µs was acquired. OCT imaging was performed with 800-µW incident optical power in the scanning OCT beam, which is well below the ANSI exposure limits. Each volume, acquired in 2.5 to 6 seconds (depending on the A-scan rate, which was chosen according to the quality of the ocular media of the patients), consisted of 60 tomograms, each comprising 1024 A-scans moving in a transverse direction with 1024 axial pixels, covering a diseased area of approximately 3 x 3 mm (except for the disease shown in Fig. 5 , where 3 x 5 mm was scanned and in Figs. 6A 6B 6C 6D 6E , where 2 x 3 mm was scanned), at a depth of approximately 1 mm. With this incident power, a sensitivity of 95 dB was achieved for all scanning conditions. The sensitivity of the presented technique was measured with an artificial eye consisting of a mirror and 25 mm of water in combination with a neutral-density filter. With the same optical power and bandwidth as is used in clinical in vivo measurements, the density of the optical filter in front of the artificial eye was increased until a signal above the noise could still be distinguished. The maximum of this signal was then used in combination with the variance of the noise and the value of the optical neutral-density filter to calculate the best sensitivity of the system.
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3-µm axial and approximately 15- to 20-µm transverse resolution. One hundred forty eyes with distinct macular diseases of different origins and locations were included. The primary diagnosis was based on a thorough clinical examination that included visual acuity testing, slit lamp examination, and ophthalmoscopy. In cases demonstrating an exudative component clinically, fluorescein angiography (FA) was added to the diagnostic procedure. Eyes were grouped into diseases with a primary epiretinal location including epiretinal membranes and vitreomacular traction, with or without macular hole; an intraretinal disease such as cystoid macular edema, central serous chorioretinopathy, hereditary retinal disease; or an a priori subretinal location, such as age-related macular degeneration with choroidal neovascularization (CNV), dry changes such as drusen or atrophy of the retinal pigment epithelium (RPE), or a serous detachment of the pigment epithelium (PED).
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Analysis of Single UHR OCT Scans from Serial Sections
Figure 2A demonstrates an OCT view of the fundus similar to the one obtained by standard fundus photography, which can be directly reproduced from 3-D UHR OCT data. This OCT view is generated by summing the A-scan signal along the axial direction, resulting in a brightness pixel value for each axial scan, and can be used to register directly the UHR OCT tomograms (Figs. 2C 2D 2E) , in addition to a 3-D representation of the imaged volume (Fig. 2B) . Since each scan of the 60 sections consists of 1024 A-scans with 1024 data points, a single tomographic scan can be extracted and analyzed separately to identify a specific site of interest. Even the architecture of the normal macula varies substantially, depending on the precise location and the distance from the foveal center. When tomographic images from the extrafoveal area, taken at a distance of 1 mm from the foveal center, are selected, the retinal band is homogenous and wide, and no central thinning is seen (Fig. 2C) . However, in the depth of the ganglion cell layer (GCL) and inner plexiform layer (IPL) below the ILM/NFL, abundant areas of focal hyperreflectivity are visible that originate from large-diameter vessels such as arterioles and venules located on the surface of the retina. The solid vascular walls produce distinct zones of reflectance shadows throughout the underlying layers (cf. Figs. 2C 2D , red circles). Otherwise, the 10-layered structure of the retina appears as detailed as seen in conventional two-dimensional (2-D) UHR OCT without any loss of axial resolution. Approaching the juxtafoveal area, the center of the tomogram section becomes thinner with the attenuation of the nerve fiber density (Fig. 2D) . Smaller-caliber blood vessels are located deeper in the retina (i.e., within the inner nuclear layer [INL]) and appear less hyperreflective with a narrower shadow. The tomographic sections from the center of the tomographic series, clearly delineate the central foveal depression (Fig. 2E) . Retinal vessels and associated hyporeflective shadows are completely absent. Characteristic features of the central foveal area are an opacification of the ILM at the deepest location (cf., Figs. 2F and 2G ) of the depression, consistent with a solid structural contact zone between the posterior hyaloid membrane (not visualized), the ILM, and Müller cells (not visualized) on the surface of the fovea and a focal elevation of the external limiting membrane (ELM) and the junctional band between the ISPR and OSPR on the bottom of the foveal retina (cf. Figs. 2F and 2G ). This prominence is due to the increased length of the subfoveal cone outer segments in the foveal center, compared with the relatively shorter OSPR in the extrafoveal retina.
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Subretinal Disease with CNV
Subretinal diseases in age-related macular degeneration can vary, even in the same patient, as documented in the following images. Figure 6A depicts the OCT fundus view, covering the area imaged by 3-D UHR OCT. There is a discrete central swelling of the foveal retina. FA demonstrates active extravasation from a subfoveal neovascular lesion (Fig. 6B) . The locations of the 2-D scans shown in Figures 6C 6D 6E are indicated in the OCT fundus view (Fig. 6A) . 3-D UHR OCT outlines an elevation of the central macular contour and single UHR scans taken through the fovea (Figs. 6C 6D 6E) show the changes associated with CNV. The foveal depression is reduced in depth, but the retinal architecture is completely preserved up to the ELM (Fig. 6C) . Superior to the fovea, the focal detachment is filled with serous fluid (Fig. 6C) . The fluid is located underneath the partially interrupted junctional band between the ISPRs and OSPRs, and the RPE band appears continuous. In the next image, a focal irregularity is identified at the level of the RPE and Bruch’s membrane (Fig. 6D) . The full extent of RPE and Bruch’s membrane erosion is seen in the foveal scan, were the RPE band is absent in the center of the lesion and the neovascular mass has grown through the entrance site and has entered and filled the subretinal space (Fig. 6E) .
The fellow eye (Figs. 6F 6G 6H 6I 6J 6K) shows a central areolar atrophy, clearly outlined by the OCT fundus view (Fig. 6F) as well as indocyanine green angiography (ICGA; Fig. 6G ). Corresponding locations of the scans shown in Figures 6H 6I 6J 6K are indicated in the OCT fundus view (Fig. 6F) . 3-D UHR OCT shows a widened foveal depression of increased depth (Figs. 6H 6I 6J 6K) . Outside the area of RPE atrophy, the retinal architecture is completely preserved down to the photoreceptors and the RPE band. However, there is a sudden change in the retinal structure overlaying the RPE atrophy. The junctional band between the ISPRs and OSPRs is completely lost, as are the overlying retinal structures up to about the IPL (cf. Fig. 6K , red arrows indicating the intact band), a loss of the ELM (cf. Fig. 6K , white arrows indicating the intact ELM), as well as a hyperreflectance window toward the choroids. Only proximal layers (e.g., the GCL) seem relatively well preserved. Due to complete loss of the RPE, consistent with a window defect, UHR OCT imaging reaches deeper into the choroid because there is less absorption and scattering at the melanin-rich RPE layer.
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Discussion |
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In addition, the dynamic forces and distribution of distinct diseases are monitored closely with reconstruction of traction forces and identification of small, localized changes such as the disruption of an epiretinal membrane, the focal break in the ILM membrane and hole operculum, or the penetration site of the CNV through Bruch’s membrane. 3-D angiography is another 3-D imaging method that provides a realistic representation of 3-D structural changes; however, it is restricted to the identification of vascular structures only.37 The retinal thickness analyzer (RTA) is limited to the detection of a surface contour, the epiretinal ILM layer, and a deep contour, the subretinal RPE layer, and does not provide any information about structural changes between these two borders.
The second breakthrough in quality is the high 2-D resolution of the UHR technique which, after the comprehensive 3-D representation, allows a detailed histologic sectioning of each 3-D site of interest. This feature permits insight into the intraretinal consequences of epiretinal traction from cystic changes within the superficial layers down to misalignment of the photoreceptor segments. A detailed scan-by-scan analysis after data acquisition reveals undetected focal changes and details of histologic changes, such as characteristics of macular hole formation or neovascular growth. Diseases can be located in relation to the intraretinal layer, and the primary site of damage can be identified and is correlated to the overall 3-D feature. Most important, the functional consequences of macular disease may be identified, with a precise representation of the photoreceptor integrity and location of the foveola. Small and early changes or changes outside the fovea do not escape the imaging process. Details such as the morphologic differences between cysts with pseudohole formation and lamellar macular holes are of substantial clinical relevance, and conventional OCT allows only a rough differentiation between both entities.38 Early stages of incomplete hole formation can easily be detected in fellow eyes. Such formations may not be imaged by conventional OCT, which is a major diagnostic problem. The accidental orientation and location of the scan set by the examiner has no influence on image quality or detection rate of small lesions, as all sections may be screened retrospectively and, with the high resolution used, any disease within the 3 x 3- or 3 x 5-mm field is identified. A precise quantification of lesions is also provided, such as the diameter and configuration of a macular hole which is an important prognostic factor for surgical intervention and influences the technique selected by the surgeon.39 Chan et al.40 found a so-called stage 0 macular hole in 28% of fellow eyes using advanced conventional OCT techniques. These stage 0 changes are defined as the presence of a preretinal, minimally reflective, thin band inserting obliquely on at least one side of the fovea.40 The topography of such changes is not recognized by 2-D OCT alone, but is identified with all its dynamics by 3-D UHR OCT. The improved resolution of 2-D UHR OCT enables imaging of previously unidentified changes in the photoreceptor morphology associated with macular hole and postoperative repair.11 3-D UHR OCT allows identification of isolated or multiple focal changes as well as their specific distribution throughout the macular area. Visualization of the junction between the ISPR and OSPR was shown to be an important indicator of photoreceptor integrity.11 The level of photoreceptor disturbance clearly determines the functional prognosis of any therapeutic intervention, which becomes a major issue with emerging pharmacologic interventions that have unknown end points of treatment and carry significant costs. High-resolution 3-D OCT is the appropriate noninvasive and precise modality to document the value of selective modern strategies where conventional techniques such as stereoscopic ophthalmoscopy and angiography fail to identify ultrastructural changes and the mechanisms of the therapeutical strategy. Novel pharmacologic modalities (e.g., intravitreal steroids or antiangiogenic agents) avoid mechanical manipulation associated with earlier techniques, such as surgery, laser coagulation, or photodynamic therapy, and work by mechanisms that are neither completely understood nor identified in their tissue interaction. Adequate diagnostic modalities combining a solid stereoscopic evaluation of the treatment effect and a detailed focal resolution of the ultrastructural mechanisms are urgently needed. 3-D UHR OCT characteristics perfectly fulfill this requirement and will allow the clinical development of these new strategies to proceed.
3-D UHR OCT enables unprecedented visualization of all major intraretinal layers, which had previously been possible only with histopathology. Clear visualization of all the major intraretinal layers and the ability to assess changes of retinal morphology associated with retinal diseases in an early stage, especially in the ISPR-OSPR/ELM/RPE complex, promises to have a significant impact on diagnosis and investigation and to provide a better understanding of pathogenesis and evaluation of novel therapy approaches for a variety of macular diseases. The hypothesis is that intraretinal structures that are relevant for the diagnosis and monitoring of early stages of eye diseases can be resolved by the proposed optical biopsy version of 3-D UHR OCT.
It is unlikely that OCT will replace histology or other existing ophthalmic diagnostic modalities. However, from the viewpoint of screening and diagnosis of diseases, the proposed version of OCT may enable significantly new insight into the pathogenesis and therapeutic control of several retinal diseases. The unique features of this developed technology would enable a broad range of research and clinical applications, which may not only complement many of the existing ophthalmic imaging technologies available today, but also may reveal previously unseen intraretinal changes.
This quantum leap in imaging performance is achieved by with a state of the art ultra–broad-bandwidth light source instead of superluminescent diodes. The ultimate availability of this UHR OCT technology strongly depends on the availability of ultra–broad-bandwidth light sources that are suitable for OCT applications.
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Acknowledgements |
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Submitted for publication March 23, 2005; revised April 26, May 20, May 26, 2005; accepted July 21, 2005.
Disclosure: U. Schmidt-Erfurth, None; R.A. Leitgeb, None; S. Michels, None; B. Povaay, None; S. Sacu, None; B. Hermann, None; C. Ahlers, None; H. Sattmann, None; C. Scholda, None; A.F. Fercher, None; W. Drexler, Carl Zeiss Meditec, Inc. (C)
The publication costs of this article were defrayed in part by page charge payment. This article must therefore be marked advertisement in accordance with 18 U.S.C. 
1734 solely to indicate this fact.
Corresponding author: Wolfgang Drexler, Center for Biomedical Engineering and Physics, Christian Doppler Laboratory, Medical University of Vienna, Waehringer Strasse 13, A-1090 Vienna, Austria; wolfgang.drexler{at}meduniwien.ac.at.
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) merged, creating a prominent choroidal ring pattern within the inferior curvature of the ring structure seen in the rotated specimen (G–I and also C, D). (E, H, rectangles) Areas shown at higher magnification in (F) and (I).
