June 2019
Volume 60, Issue 7
Open Access
Retina  |   June 2019
Longitudinal Association Between Drusen Volume and Retinal Capillary Perfusion in Intermediate Age-Related Macular Degeneration
Author Affiliations & Notes
  • Gregor Sebastian Reiter
    Vienna Clinical Trial Center (VTC), Department of Ophthalmology and Optometry, Medical University of Vienna, Vienna, Austria
  • Reinhard Told
    Vienna Clinical Trial Center (VTC), Department of Ophthalmology and Optometry, Medical University of Vienna, Vienna, Austria
  • Ferdinand Georg Schlanitz
    Vienna Clinical Trial Center (VTC), Department of Ophthalmology and Optometry, Medical University of Vienna, Vienna, Austria
  • Lukas Baumann
    Center for Medical Statistics, Informatics and Intelligent Systems, Medical University of Vienna, Vienna, Austria
  • Ursula Schmidt-Erfurth
    Vienna Clinical Trial Center (VTC), Department of Ophthalmology and Optometry, Medical University of Vienna, Vienna, Austria
  • Stefan Sacu
    Vienna Clinical Trial Center (VTC), Department of Ophthalmology and Optometry, Medical University of Vienna, Vienna, Austria
  • Correspondence: Ursula Schmidt-Erfurth, Department of Ophthalmology and Optometry, Medical University of Vienna, Währinger Gürtel 18-20, Vienna 1090, Austria; ursula.schmidt-erfurth@meduniwien.ac.at
Investigative Ophthalmology & Visual Science June 2019, Vol.60, 2503-2508. doi:10.1167/iovs.18-26237
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      Gregor Sebastian Reiter, Reinhard Told, Ferdinand Georg Schlanitz, Lukas Baumann, Ursula Schmidt-Erfurth, Stefan Sacu; Longitudinal Association Between Drusen Volume and Retinal Capillary Perfusion in Intermediate Age-Related Macular Degeneration. Invest. Ophthalmol. Vis. Sci. 2019;60(7):2503-2508. doi: 10.1167/iovs.18-26237.

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      © ARVO (1962-2015); The Authors (2016-present)

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Abstract

Purpose: To evaluate vascular changes in the superficial and deep retinal capillary plexus (SCP, DCP) and their association with drusen volume changes in intermediate age-related macular degeneration (iAMD).

Methods: Patients with iAMD were examined at baseline and 12 months thereafter. Drusen volume was extracted from 20° × 20° OCT scans using a 3-mm ETDRS grid using a customized algorithm with manual correction. Vessel density (VD) and flow area (FA) were extracted from 3 × 3 mm SD-OCT-A scans after manual correction of the segmentation. Associations were investigated using multiple regression models.

Results: We used 31 eyes of 31 patients for evaluation. The mean age at baseline was 74.9 ± 5.4 years; 26 patients were female. Baseline visual acuity (VA) was 0.05 ± 0.08 logMAR (Snellen equivalent approximately 20/22). The initial mean 3-mm central drusen volume was 0.144 ± 0.136 mm3. A significant association with the signal strength index was consistently found, therefore all capillary measurements were corrected. VD in the same area was 49.88% ± 7.38% and 55.43% ± 9.31% for the SCP and DCP, respectively. The baseline FA resulted in 3.292 ± 0.218 mm2 and 3.433 ± 0.224 mm2 for the SCP and DCP, respectively. No association was found between changes in drusen volume and FA or VD after 12 months (all P > 0.05). VA worsened (P = 0.013) and the foveal FA of the SCP increased significantly (P = 0.014).

Conclusions: No significant association was found between the increase in drusen volume in iAMD and capillary retinal perfusion over a 12-month follow-up. Although VA decreased statistically over this time period, the foveal FA of the SCP increased.

Drusen are a major hallmark of AMD, which is the leading cause of blindness in people older than 60 years in developed countries.1,2 Drusen volume and the retinal pigment epithelium-drusen complex (RPEDC) are under intensive investigation as possible predictors of disease progression when using spectral domain optical coherence tomography (SD-OCT).35 Drusen show a characteristic life cycle with progressive growth, eventually followed by a rapid decrease in volume before conversion.4,6,7 Drusen volume measurements strongly depend on the correct segmentation of Bruch's membrane and the RPE. Automated and manual segmentations show good overall agreement.8,9 However, manual correction of the automated segmentations is still important to achieve precise measurements, particularly considering intraindividual changes in longitudinal studies.4 
OCT-Angiography (OCT-A) has become commercially available and is used for the noninvasive analysis of retinal and choroid vessel morphology and alterations. The choriocapillaris (CC) is the main focus of investigations when OCT-A is used to analyze structures beneath the RPE. The retinal vasculature is subdivided into two main plexus, the superficial retinal capillary plexus (SCP) and the deep retinal capillary plexus (DCP), but the commercial systems divide them by different default settings.10 An intermediate retinal capillary plexus (ICP), which ranges from the outer margin of the inner plexiform layer (IPL) to 20 μm below the IPL, has also been described, but is most commonly integrated into the SCP.11 Spectral domain OCT-A (SD-OCT-A) seems appropriate for the measurement of retinal vessels with good intra- and intervisit reproducibility, in contrast to a lack of in-depth signal strength for the measurement of choroidal vessels exceeding the RPE compared with swept-source OCT-A (SS-OCT-A).1214 Quantifications require a correct segmentation of the retinal layers, which is consistent for healthy eyes, but is often prone to be false for eyes with retinal diseases.10,1517 Nonetheless, vessel density (VD) and the foveal avascular zone have commonly been used to quantify vessel-specific characteristics on OCT-A en face images.1826 Other quantifications, especially for signal loss in order to analyze vessels in the CC, have also been described.27 Recently, investigations reported that VD of the SCP and the DCP measured by OCT-A show alterations in AMD, which become measurable at the stage of intermediate AMD.22 This study was conducted to investigate an association between the changes in drusen volume and the changes in retinal vessels in intermediate AMD. We hypothesized that with disease progression a loss of retinal capillary perfusion might occur which might not be the cause, but a result of drusen regression. 
Methods
This study was conducted following the tenets of the Declaration of Helsinki and the Good Clinical Practice guidelines. Patients with intermediate AMD were included in the study after approval by the ethics committee of the Medical University of Vienna. Each participant gave written informed consent before inclusion. Inclusion criteria was based on the classification by Ferris et al.28 Accordingly, any patient with early AMD, defined as drusen size <125 μm without pigmentary alterations, or late AMD, defined as geographic atrophy or neovascular AMD, including a history of anti-VEGF treatment, were not included. Patients who had had any intraocular surgery except uncomplicated cataract surgery before baseline or any disease that could affect the results of the study were excluded. If both eyes of a patient were eligible for the study, the one with the higher signal strength index (SSI) and better image quality of the OCT-A scan at baseline was used for follow-up. The study was conducted from June 2015 until December 2017. On each visit, participants underwent a best-corrected visual acuity (BCVA) assessment, a complete ophthalmic examination including funduscopy and intraocular pressure measurement using a Goldmann applanation tonometer, SD-OCT (all Spectralis HRA+OCT; Heidelberg Engineering, Heidelberg, Germany) and SD-OCT-A (RTVue XR Avanti; Optovue, Fremont, CA, USA). After a BCVA assessment, pupils of the study eyes were dilated to at least 6 mm with eye drops containing 0.5% tropicamide and 2.5% phenylephrine. A follow-up examination was performed in the same manner 12 months after the baseline examination. 
Imaging Protocol
SD-OCT images were acquired with an OCT device (Heidelberg Engineering) using a 20° × 20° volumetric scan with a resolution of 1024 × 97 (A-scans × B-scans) centered manually on the fovea. The follow-up mode, provided by the system's software, was used to acquire images thereafter. Volumetric scans were exported for initial automated drusen presegmentation. 
SD-OCT-A was performed with a commercially available system (Optovue). A 3 × 3-mm scan centered on the fovea was acquired for retinal vessel assessment. The RTVue XR Avanti acquires a volumetric scan of 304 × 304 A-scans with an A-scan rate of 70 kHz and a center wavelength of 840 nm. Two consecutive volumetric scans were acquired and merged using the system's split-spectrum amplitude decorrelation angiography algorithm (SSADA). Image quality, based on the system's SSI, was checked after every acquisition. If the SSI was ≤50 or if vessels were not quantifiable, images were retaken to ensure sufficient quality for analysis. If the SSI was not reached after three attempts or important motion artifacts or vitreous floaters were still visible, patients were excluded from further imaging. Optovue recommends a minimum SSI of 40 for retinal images. However, different minimum SSIs can be found in the literature, ranging from 40 to 60.11,13,17,20,22 Intra- and intervisit reproducibility of the same device with a coefficient of variation of mostly lower than 5% for the superficial retinal plexus in both healthy and retinal diseases using an SSI >46 have been published.13 Referring to these results, we chose an SSI >50 for this study to ensure correct quantification, also considering the deep retinal capillary plexus. 
SD-OCT and SD-OCT-A Analysis
The SD-OCT volumetric scans acquired were presegmented using a published algorithm.29 Manual correction was performed using the IOWA OCT Explorer 3.6 (The University of Iowa, Iowa, USA). Drusen volume was then computed for an overlying 3-mm Early Treatment Diabetic Retinopathy Study (ETDRS) grid and data from sections one to five were exported (Fig. 1). 
Figure 1
 
Drusen map of an overlaying 3-mm ETDRS grid. Drusen volumes from sections 1 to 5 were extracted for further calculations.
Figure 1
 
Drusen map of an overlaying 3-mm ETDRS grid. Drusen volumes from sections 1 to 5 were extracted for further calculations.
For OCT-A image analysis, the system's software (AngioVue version number 2016.2.0.35; Optovue) was used to automatically segment the superficial and deep retinal plexus. We manually corrected the segmentation if necessary, because segmentation errors have often been highlighted in patients with AMD.10,17 For this purpose, we adjusted the internal limiting membrane (ILM) and the outer margin of the inner plexiform layer (IPL) in every B-scan. The default settings were used to distinguish the SCP from the DCP, which were 3 μm below the ILM to 15 μm below the IPL for the SCP and 15 μm below the IPL to 70 μm below the IPL for the DCP. All volumetric scans were updated with the corrected segmentation and en face images were generated by the software (Fig. 2). VD was extracted using a 3-mm ETDRS grid. VD was defined as the percent of vascularized area in contrast to nonvascularized area in a defined region of interest. FA accounted for the vascularized area without referring to the nonvascularized area. To extract data, we measured flow area in 1- and 3-mm circles centered on the fovea. We further defined the inner 1 mm as the foveal section and the inner 3 mm as the parafoveal section (Fig. 2), which is further subdivided into temporal parafoveal, superior parafoveal, nasal parafoveal, and inferior parafoveal sections. 
Figure 2
 
OCT-A 3 × 3-mm en face images of (A) the SCP with the highlighted (a) foveal and (b) parafoveal sections. (B) The DCP at baseline. (C) Baseline OCT-A B-scan taken from the 3 × 3-mm volumetric scan showing blood flow (red) and segmentations (red and green lines indicate the SCP).
Figure 2
 
OCT-A 3 × 3-mm en face images of (A) the SCP with the highlighted (a) foveal and (b) parafoveal sections. (B) The DCP at baseline. (C) Baseline OCT-A B-scan taken from the 3 × 3-mm volumetric scan showing blood flow (red) and segmentations (red and green lines indicate the SCP).
Statistical Methods
Multiple regression models were calculated to investigate an association between the changes in drusen volume and the changes in vessel quantifications. Changes in FA and changes in VD were used as dependent variables, and changes in drusen volume as well as age at baseline, sex, and eye (left versus right) were used as covariates. Univariate models were computed first to check if the SSI was also a relevant covariate. Multiple regression was computed for VD in all sections of the ETDRS grid (Fig. 1) as well as for FA in both concentric rings around the fovea (Fig. 2), both for the SCP and DCP. The means of the foveal and parafoveal sections were used for the main model. To investigate changes over the follow-up period, paired t-tests were used and significant associated variables were included to correct these results. It should be noted that no correction for multiple testing was performed. 
Results
Study Participants and Baseline Condition
We screened 75 eyes of 49 patients with intermediate AMD for this study. We excluded 12 eyes from the evaluation due to motion artifacts without improvement after three reacquirements. We excluded four eyes due to an SSI ≤50 and no improvement after three reacquirements. We excluded seven eyes due to vitreous floaters. We lost eight eyes to follow-up. Both eyes were eligible for the study in 13 cases and the one with the higher SSI was chosen for follow-up examination. Ultimately, 31 eyes of 31 patients completed the 12-month follow-up examination. Out of these 31 patients, 26 (83.9%) were female. Twenty eyes (64.5%) were right eyes. The mean age at baseline was 74.9 ± 5.4 years and patients had a BCVA of 0.05 ± 0.08 logMAR (Snellen equivalent approximately 20/22). The mean drusen volume in the central 3-mm circle was 0.144 ± 0.136 mm3 at first presentation. VD at baseline in the central 3-mm circle was 49.88% ± 7.38% and 55.43% ± 9.31% for the SCP and the DCP, respectively. The initial FA resulted in 3.292 ± 0.218 mm2 and 3.433 ± 0.224 mm2 for the SCP and the DCP, respectively. OCT-A reached a mean SSI of 63.8 ± 6 for the first visit and 64.7 ± 5.3 at 1 year (P = 0.477 for the paired t-test). 
Influence of SSI on Flow Area and Vessel Density Measurements
The changes in FA in the central 3-mm circle of the SCP and DCP were significantly associated with the changes in SSI (both P < 0.001), and thus the changes in SSI were included in all multiple regression calculations for the FA changes. The changes in VD in the central 3-mm circle of the SCP and the DCP was also significantly associated with changes in SSI (P < 0.001 and P = 0.013, respectively). Hence, the changes in SSI were also included in all multiple models for the vessel density changes. Due to these associations, SSI was also used to correct results in the paired t-tests which were used for the follow-up change investigation. 
Comparison Between Baseline and Follow-Up Examinations
An overview of baseline and the 12-month follow-up data is shown in Table 1. The single sections of the ETDRS grid are presented in Table 2. The results of the paired t-test are shown in Table 1 and Table 2. Mean visual acuity decreased significantly from 0.05 ± 0.08 logMAR (Snellen equivalent approximately 20/22) to 0.1 ± 0.14 logMAR (Snellen equivalent approximately 20/25; P = 0.013). No follow-up changes were found in drusen volume and VD or most measurements for FA (all P > 0.05). However, the foveal FA in the SCP was found to have significantly increased after SSI correction (P = 0.014, Table 2). No changes in SSI could be found after the 12-month follow-up (P > 0.05). 
Table 1
 
Comparison Between Baseline and Follow-Up Data. Vessel Density and Flow Area Data From the Central 3-mm Circle (Mean of Fovea and Parafoveal Sections) and After Signal Strength Index Correction Are Presented
Table 1
 
Comparison Between Baseline and Follow-Up Data. Vessel Density and Flow Area Data From the Central 3-mm Circle (Mean of Fovea and Parafoveal Sections) and After Signal Strength Index Correction Are Presented
Table 2
 
Comparison Between Vessel Density and Flow Area: Baseline and Follow-Up Data
Table 2
 
Comparison Between Vessel Density and Flow Area: Baseline and Follow-Up Data
Association Between Drusen Volume and VD and FA
All models were corrected for SSI due to statistically significant associations between SSI and vessel quantifications. After correction, we found no association between the changes in drusen volume, age, sex, or eye (left vs. right) and changes in vessel density (all P > 0.05). An association was found neither in the superficial retinal plexus nor in the deep retinal plexus. Accordingly, no association between the changes in drusen volume, age, sex or eye (left vs. right) and changes in flow area (all P > 0.05) could be found, either for the superficial retinal plexus or the deep retinal plexus. 
Discussion
This study investigated an association between drusen volume and retinal capillary perfusion. A statistically significant association between the SSI and retinal vessel quantifications was found beforehand. Therefore, all statistical models including paired follow-up t-test were corrected for SSI. Consecutively, we did not find any significant associations between the changes in drusen volume and retinal VD or FA (all P > 0.05). Nevertheless, follow-up analysis showed a significant decrease in visual acuity with a mean worsening of 2.5 letters on the ETDRS chart, equivalent to 0.05 logMAR (P = 0.013). No significant changes over the follow-up period were found in most retinal capillary quantifications, except for a significantly increase of the foveal FA at the SCP (P = 0.014). 
The ganglion cell complex (GCC), which includes the three innermost layers of the retina, the retinal nerve fiber layer (RNFL), the ganglion cell layer (GCL) and the IPL, undergoes thinning in the course of AMD with the most distinct manifestations in late AMD, whereas the RNFL thins only in neovascular AMD.30 Because the SCP is mainly located in the GCC, changes in the retinal vessels may occur even before converting into late AMD and thinning. However, this study did not find such changes in the retinal vessels in a 12-month follow-up of patients with intermediate AMD. 
Segmentation errors are still a limitation for studies using OCT-A in patients with AMD. Segmentation of the inner plexiform layer was found to be disturbed by at least 50 μm in a third of drusen analyzed in one study.17 Even a smaller deviation may alter results—taking into account that the software we used (Optovue) relies on a correct segmentation of the outer margin of the IPL for the quantification of both the superficial and the deep retinal capillary plexus—especially when considering that the default slab of the deep retinal plexus is 55-μm thick. To overcome this limitation, manual correction of the segmentation, although time-consuming, is still inevitable to ensure the highest accuracy of OCT-A analysis. The exclusion of scans which do not show correct segmentation could result in a selection bias, which must be avoided in future OCT-A studies. 
In this study, we used SD-OCT-A instead of SS-OCT-A. The flow impairment could be shown less prone to be false-positive in the CC using a 1050-nm SS-OCT-A.12 However, we only analyzed the retinal vessels without taking the CC into account. As the purpose of this study was to show an association between changes in drusen volume and retinal capillary quantifications, the use of SD-OCT-A seems sufficient, due to good reproducibility of retinal OCT-A images.13 
Some limitations need to be mentioned. The minimum SSI margin chosen for the study was 51, whereas in other studies a margin of 40 to 60 was defined. Because this lower margin reflected the experience of a trained reader, we believe our conditions result in a good balance between gain of data and low quantification errors. Even after excluding 23 eyes due motion artifacts, vitreous floaters and insufficient minimum SSI, we found a statistically significant association between changes in SSI and all vessel quantifications. Therefore, the statistical methods used had to be corrected. The association with the SSI should be examined in further research on vessel quantifications and correction performed if necessary. 
How retinal vessels measured by OCT-A in intermediate AMD change intraindividually over time is still unknown. A 12-month follow-up seems appropriate to verify early changes in retinal vessel quantifications. Noteworthily, no statistically significant changes were found for most parameters, except for foveal FA of the SCP (P = 0.014). Further studies need to reevaluate this result and its association to foveal avascular zone measurements or functional outcomes in intermediate AMD. 
Our study provides data from baseline to 12 months of follow-up. It may be argued that this interval is too long to detect small changes in drusen volume because regression could happen faster than in 12 months or is too short to detect changes in the retinal vessels. Nonetheless, a 12-month follow-up appears as a reasonable tradeoff between these two factors in an exploratory study, investigating an association between drusen volume and retinal vessel perfusion. In order to discover changes during the life cycle of a single druse, further studies will have to cover longer follow-up periods to answer this specific question. Drusen volume seems to constantly increase before a sudden regression may occur.4 Some patients may have already undergone drusen regression in the past and therefore drusen volume remains stable at a low level. These patients may not contribute much for the analysis of the association in the change of retinal vessel quantifications, but nevertheless they still suffer from the same stage of disease according to current classifications. Identification of a subgroup of patients proven to have postregression in contrast to patients with preregression intermediate AMD may be of interest for future studies with larger patient cohorts. 
In conclusion, no association was found between changes in drusen volume, age, sex, or eye (left versus right) and changes in vessel density or flow area (all P > 0.05), either for the SCP or the DCP. Follow-up analyses showed no changes in most vessel quantifications, except for the foveal flow area of the SCP (P = 0.014). Changes in retinal vessels may occur more slowly than anticipated and long-term follow-up data is needed to evaluate these changes. Correction based on SSI changes may become necessary for further studies due to a statistically significant association found between the SSI and vessel quantifications. 
Acknowledgments
Disclosure: G.S. Reiter, None; R. Told, None; F.G. Schlanitz, None; L. Baumann, None; U. Schmidt-Erfurth, None; S. Sacu, None 
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Figure 1
 
Drusen map of an overlaying 3-mm ETDRS grid. Drusen volumes from sections 1 to 5 were extracted for further calculations.
Figure 1
 
Drusen map of an overlaying 3-mm ETDRS grid. Drusen volumes from sections 1 to 5 were extracted for further calculations.
Figure 2
 
OCT-A 3 × 3-mm en face images of (A) the SCP with the highlighted (a) foveal and (b) parafoveal sections. (B) The DCP at baseline. (C) Baseline OCT-A B-scan taken from the 3 × 3-mm volumetric scan showing blood flow (red) and segmentations (red and green lines indicate the SCP).
Figure 2
 
OCT-A 3 × 3-mm en face images of (A) the SCP with the highlighted (a) foveal and (b) parafoveal sections. (B) The DCP at baseline. (C) Baseline OCT-A B-scan taken from the 3 × 3-mm volumetric scan showing blood flow (red) and segmentations (red and green lines indicate the SCP).
Table 1
 
Comparison Between Baseline and Follow-Up Data. Vessel Density and Flow Area Data From the Central 3-mm Circle (Mean of Fovea and Parafoveal Sections) and After Signal Strength Index Correction Are Presented
Table 1
 
Comparison Between Baseline and Follow-Up Data. Vessel Density and Flow Area Data From the Central 3-mm Circle (Mean of Fovea and Parafoveal Sections) and After Signal Strength Index Correction Are Presented
Table 2
 
Comparison Between Vessel Density and Flow Area: Baseline and Follow-Up Data
Table 2
 
Comparison Between Vessel Density and Flow Area: Baseline and Follow-Up Data
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