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Abstract
Aim The role of changes at the vitreoretinal interface and vitreomacular traction forces in pathogenesis, and the course of exudative age-related macular degeneration (AMD) need further exploration. This study examines the localisation of adhesion and the direction of traction lines in eyes with exudative AMD.
Methods The cubes 512×128 of Cirrus optical coherence tomography (OCT) and volume scans of Spectralis OCT were reviewed in a consecutive series of patients presenting between December 2008 and March 2009 with vitreomacular adhesion in exudative AMD.
Results 30 eyes of 25 patients with exudative AMD and vitreomacular adhesion were studied. 50% had type III lesions, 46.7% occult and 3.3% predominantly classic lesions. The localisation of the adhesion corresponded in 100% with the area of the neovascularisation (CNV), in 73.3% traction directed towards the CNV and in 83.3% towards the optic disc could be noted. Spectral domain OCT and 3D visualisation enabled clearer localisation of vitreomacular adhesion and definition of resulting traction lines.
Conclusion There is a high prevalence of type III lesions within eyes with vitreomacular adhesions, and complete correspondence between the location of the adhesion and the CNV. There is also a high incidence of vitreopapillary adhesion in these cases, suggesting a possible role in pathogenesis.
- Vitreomacular traction
- age-related macular degeneration
- Optical Coherence Tomography
- spectral domain OCT
- choroidal neovascularisation
- vitreous
- retina
- imaging
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- Vitreomacular traction
- age-related macular degeneration
- Optical Coherence Tomography
- spectral domain OCT
- choroidal neovascularisation
- vitreous
- retina
- imaging
Introduction
Genetic factors, ageing, ischaemia and environment factors1 are considered the main important aetiological factors of age-related macular degeneration (AMD). Still there is an incomplete understanding of the pathogenesis of exudative AMD. Additional important factors influencing the development and course of exudative AMD are changes at the vitreomacular interface which have been confirmed in prior studies. Attached posterior vitreous cortex, partial peripheral posterior vitreous detachment and central adhesions surrounded by shallow detachment of the posterior vitreous cortex were significantly more frequent in exudative AMD than in non-exudative AMD and control eyes.2 3 Several pathways are under discussion as to how the attached posterior vitreous may influence a pathology primarily localised deeper in the area of the retinal pigment epithelium.4 Can traction forces play a role in the development of exudative AMD? In the past, in studies conducted based on time-domain optical coherence tomography (OCT), there was evidence only of vitreoretinal adhesion, although traction was suspected in more than 50% of the cases. The aim of this study was to examine whether the new spectral-domain OCT providing a higher resolution, faster scan acquisition and raster scanning can contribute additional information regarding localisation of vitreomacular adhesion and the direction of traction forces.
Methods
The OCT examinations of patients presenting with various stages of exudative AMD between December 2008 and March 2009 were retrospectively reviewed, and eyes with vitreomacular adhesion (VMA) were included in this study. Eyes with macular diseases other than exudative AMD were excluded, with special regard to diseases accompanied by changes in the vitreomacular interface such as diabetic macular oedema, macular pucker and vitreomacular traction syndrome. Furthermore, highly myopic eyes (<−5.0 dioptres) were excluded. The neovascular lesions were classified according to fluorescein angiographic findings into occult lesions, predominantly classic lesions and type III neovascular lesions (following the new classification of Freund, who suggested this term for retinal angiomatous proliferation (RAP) to distinguish this special type of neovascularisation from the others).5 Evaluated were the first examination within the observation period and a second examination 1 year thereafter.
Distance acuity was tested with ETDRS Charts at a distance of 2 m.
For Cirrus OCT, the macular cube 512×128 program of the Cirrus HD OCT (Carl Zeiss Meditec, Dublin, California) was used. For Spectralis OCT (Heidelberg Engineering, Heidelberg, Germany), the volume 145 sections program, high-speed modus (oversampled twice), was used. An additional five central lines of Cirrus OCT as well as a single high-resolution line through the centre of the lesion of Spectralis OCT were performed. Traction was defined as being present when there was a sharp angulation of the posterior vitreous cortex present at the site of adhesion or a localised deformation of the retinal profile. One year after the first evaluation, the OCT examinations were reviewed once again to show the follow-up of the adhesions. Furthermore, improved visualisation was achieved with ray-traced 3D reconstruction using a custom-made subprogram in Cinema 4D XL 11.0 (Maxon Computer Inc, Thousand Oaks, California). A pseudosegmentation algorithm was implemented using noise-reduction filtering and a stepped colour gradient instead of a ‘look up table.’ The ray-traced shading was backed directly into the texture, resulting in a real-time visualisation using OpenGL.
Results
Thirty eyes of 25 patients were included. The mean age was 77±10.3 (57–93) years, 44% of the patients were male, and 56% were female; 26.7% were treatment-naïve when included in the study, and 73.3% were under treatment with inhibitors of the vascular endothelial growth factor (anti-VEGF); 50% of the lesions were type III, 46.7% were occult lesions, and 3.3% were predominantly classic.
Vitreomacular adhesion surrounded by shallow detachment of the posterior vitreous cortex was located in the fovea in 43.3% and juxtafoveally in 56.7%. In 88.2% of the juxtafoveally localised lesions, a RAP was present. The area of the adhesion corresponded with the localisation of the RAP, even if the lesion extended under the foveal avascular zone. Overall, the area of adhesion corresponded in 100% with the localisation of the CNV. Of these, 73.3% evidenced visible vitreoretinal traction lines directed towards the CNV. In 6.6% under an area of detached vitreous cortex, a second membrane with VMA was present.
Additionally, tight adhesion and traction could be detected on the temporal margin of the optic disc in 83.3%. The posterior vitreous cortex seemed to be split in the area of vitreopapillar adhesion. At the 1-year follow-up examination, 10% of the eyes had developed a detachment of the posterior cortex, 13.3% showed increased traction, and the remaining 76.7% showed an unchanged finding concerning the pathology at the vitreoretinal interface. Meanwhile, 100% of the eyes were under anti-VEGF treatment.
The mean letter score at baseline was 52±31 letters (1–110 letters) and decreased to 48±35 letters (1–116) at month 12. Table 1 presents more detailed distance acuity data.
Distance acuity
Adhesion and traction forces were visible in the OCT scans of both machines. The quality of the single scans with Spectralis OCT exceeded that of the five lines of Cirrus OCT. The quality of the cube/volume scans was sufficient for 3D animation in 83.3% of Cirrus OCT and 13.3% of Spectralis OCT. 3D visualisation was inhibited possibly by the low scan quality in the Cirrus OCT and an expired eye tracker (5 min) before the volume scans were completed with Spectralis OCT (figure 1).
On the left side at the top: Spectralis infrared video images and high-resolution scans. Right side: Cirrus optical coherence tomography high-definition scans (five lines program). In the first row, there is adhesion of the posterior hyaloids surrounded by detachment, in the second row only the temporal side of the posterior hyaloids is detached, and in the third row real traction is visible. In the Spectralis images, the adherence in the area of the optic disc is visible. On the bottom, 3D images are presented, the left image (Spectralis optical coherence tomography) showing the mainly papillary adherence, and the right Cirrus image showing the correlations between traction and CNV.
Discussion
Vitreomacular adhesions were described in a previous study in 36% of eyes with exudative AMD, significantly more frequently than in eyes with non-exudative AMD or control eyes.2 These results were confirmed by Robison, who found VMA in 38% of eyes with exudative AMD,3 and by Lee,6 who found VMA in 22.3% associated with neovascular AMD. These studies used primarily Stratus OCT examinations to verify VMA. Owing to the time-domain technology of Stratus OCT, differentiation between adhesion and traction was difficult, although traction was suspected in more than 50% of the cases. VMA but also signs of traction could clearly be identified in both spectral domain OCT machines, the Spectralis and the Cirrus OCT. Especially in the high-definition scans (five lines 6 mm in length in Cirrus OCT and one single line 8 mm in length in Spectralis OCT) the angulation of the posterior vitreous cortex was clearly visible. Furthermore, the increased length of the scan in Spectralis OCT made the correlation between posterior vitreous cortex and the optic disc obvious. 3D animation helped to visualise the correlations between the localisation of the adhesion and the neovascularisation. Furthermore, 3D shows splitting within the posterior vitreous cortex in the area of vitreo papillary adhesion and traction from different directions. 3D imaging was possible in most (83.3%) of the Cirrus OCT cube scans, but only in 13.3% of Spectralis OCT volume scans of a sufficient scan density was possible.
Spectral domain OCT has not yet been frequently used to show VMT/ VMA: Mojana7 and coworkers have examined 170 eyes of elderly patients with the OTI-Spectral OCT/SLO. They found adhesions in 27.8% of exudative AMD and 24.5% of non-exudative AMD, but traction could be identified in 59% of these eyes in exudative AMD and only 13% in non-exudative AMD. Traction was identified even more frequently in our patients with adhesions in exudative AMD with 73.3%. Mojana7 also described an association of VMT and minimally classic lesions. In our patients, we found 50% of type III lesions (in the former classification frequently exhibiting as minimal classic lesion), a higher incidence than reported in the literature (21–38%).8 The high number of type III lesions within lesions with vitreomacular adhesions is particularly noticeable in this consecutive series of patients, although we performed a retrospective analysis of the data. RAP, or now called type III, lesions are thought to origin from the perifoveal retinal vasculature5 9 explaining the juxtafoveal location of the CNV. However, this is also an area where the vitreous is more adherent, as at the margin of the optic disc and at the ora serrata,10 11 which might influence the development of the CNV. There was 100% agreement of the localisation of the neovascularisation and the adhesion/traction. In larger type III lesions involving the fovea, the adhesion was at the area of the original neovascularisation, which could be verified by reviewing former angiograms.
A follow-up examination of our patients revealed that most changes in vitreomacular interface remained unchanged within 1 year in spite of anti-VEGF treatment. Only 10% exhibited a posterior vitreous detachment, and 13.3% (all lesions located juxtafoveally) showed an increase in traction or the conversion of adhesion to traction. This might indicate that the adhesion is more important in the pathogenesis of neovascular AMD, whereas traction develops later in the course of the disease and might influence further development of the process. Increase in traction was correlated with a decrease in distance acuity (mean of eight letters), whereas posterior vitreous detachment was correlated with an increase in distance acuity (nine letters). Overall distance acuity decreased by three letters within the observation period. The results of this group of selected patients (VMA) were worse than the results of anti-VEGF therapy already published.12 13 This might be caused by the influence of traction on the responsiveness to anti-VEGF treatment, but that needs further exploration. Vitreous detachment occurred in 66.6% in advanced lesions, indicating that in the course of the disease, including scar formation and its effect on the inner retina might cause vitreous detachment. These findings confirm the results of Robison,3 who found an increased incidence of vitreous detachment in advanced lesions. The third case was an occult lesion under anti-VEGF treatment. Vitreous detachment was combined with a decrease in activity and increase in distance acuity. No further injections were required for at least 4 months.
Recently, Sebag et al14 reported on vitreopapillar traction in various diseases and found a high incidence of vitreopapillar adhesion in cases of macular hole, less frequent in cases of non-exudative AMD or macular pucker. We found vitreopapillar adhesions in more than 80% of our exudative AMD patients. Exceedingly tight adhesions on the natural locations of adhesion at the fovea and the optic disc seem to be associated with neovascular AMD. The insertion of the posterior vitreous cortex on the margin of the optic disc revealed a split appearance, possibly a preliminary stage of vitreoschisis.15 16 The thesis that the posterior vitreous cortex might detach in two or more layers in some cases was supported by the presence of two superimposed membranes in 6.6%. Prospective studies, especially including high-risk non-exudative AMD cases or early exudative AMD, have to provide evidence of the interesting details indicated in this study. Furthermore, our attention should concentrate on the area of the optic disc and vitreopapillary adhesions.
In conclusion, we were able to show that the location and the direction of the traction forces visualised by high-technology OCT and 3D OCT correspond in 100% with the origin of the CNV. In about 77%, intravitreal anti-VEGF treatment does not influence vitreomacular adhesion or traction.
References
Footnotes
Presented in part at the annual meeting of the Association for Research in Vision and Ophthalmology, Fort Lauderdale, Florida, 7 May 2009 (5245/A106).
Funding Ludwig Boltzmann Institute of Retinology and Biomicroscopic Lasersurgery.
Competing interests CG is a consultant for Carl Zeiss Meditec and for Maxon Computer Inc.
Patient consent Obtained.
Provenance and peer review Not commissioned; externally peer reviewed.