Among 489 eyes enrolled in the prospective ProgStar Study, a total of 326 were included in the sensitivity analysis of the macula and 322 eyes were included in the analysis of mean sensitivity.
Scatterplots showing the correlation between microperimetric sensitivity with the duration of Stargardt disease (STGD1), the age at onset of STGD1, and the duration of STGD1 symptoms. Univariate linear regression analyses.
The right eye of a 35-year-old man with mean sensitivity of 0.12 dB and best-corrected visual acuity of 77 Early Treatment Diabetic Retinopathy Study letter score (about 20/32 Snellen equivalent). Fixation was within an island of nonatrophic retina on a coregistered fundus autofluorescence image.
eFigure 1: Modified Humphrey 10-2 Pattern (68 Points) for Sensitivity Testing of the Macula.
eFigure 2: Correlation of Visual Acuity with Microperimetric Sensitivity.
eTable 1: Demographic Characteristics by Inclusion in the Analyses.
eTable 2: Macular Sensitivity in Stargardt Disease.
eTable 3: Macular Sensitivity in Stargardt Disease including Patients with Poor Pattern Placement.
eTable 4: Macular Sensitivity in Stargardt Disease and Its Association with Demographic Features including Patients with Poor Pattern Placement.
eTable 5: Macular Sensitivity in Stargardt Disease and Its Association with Visual Acuity including Patients with Poor Pattern Placement. ProgStar Study Team as of 10 Feb 2017
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Schönbach EM, Wolfson Y, Strauss RW, et al. Macular Sensitivity Measured With Microperimetry in Stargardt Disease in the Progression of Atrophy Secondary to Stargardt Disease (ProgStar) Study: Report No. 7. JAMA Ophthalmol. 2017;135(7):696–703. doi:10.1001/jamaophthalmol.2017.1162
How is light sensitivity of the posterior pole compromised in Stargardt disease?
In this multicenter prospective cohort study, microperimetric mean sensitivity was lower in the fovea than in the peripheral macula. Overall mean sensitivity was lower in older patients and those stating longer disease duration. There are cases with obvious discrepancies of low mean sensitivity measurements with good visual acuity; these cases showed foveal sparing on fundus autofluorescence testing.
These findings suggest microperimetry allows a more comprehensive assessment of the function of the central retina, and it may serve as an outcome measure in future clinical trials for Stargardt disease and other macular diseases.
New outcome measures for treatment trials for Stargardt disease type 1 (STGD1) and other macular diseases are needed. Microperimetry allows mapping of light sensitivity of the macula and provides topographic information on visual function beyond visual acuity.
To measure and analyze retinal light sensitivity of the macula in STGD1 using fundus-controlled perimetry (microperimetry).
Design, Setting, and Participants
This was a multicenter prospective cohort study. A total of 199 patients and 326 eyes with molecularly confirmed (ABCA4) STGD1 underwent testing with the Nidek MP-1 microperimeter as part of the multicenter, prospective Natural History of the Progression of Atrophy Secondary to Stargardt Disease (ProgStar) study. Sensitivity of 68 retinal loci was tested, and the mean sensitivity (MS) was determined; each point was categorized as “normal,” “relative,” or “deep” scotoma.
Main Outcomes and Measures
Mean sensitivity and the number of points with normal sensitivity, relative, or deep scotomas.
Mean (SD) patient age was 34.2 (14.7) years, mean (SD) best-corrected visual acuity of all eyes was 47.8 (16.9) Early Treatment Diabetic Retinopathy Study letter score (approximately 20/100 Snellen equivalent), and mean MS of all eyes of all 68 points was 11.0 (5.0) dB. The median number of normal points per eye was 49 (mean [SD], 41.3 [20.8]; range, 0-68); abnormal sensitivity and deep scotomas were more prevalent in the central macula. Mean sensitivity was lower in the fovea (mean [SD], 2.7 [4.4] dB) than in the inner (mean [SD], 6.8 [5.8] dB) and outer ring (mean [SD], 12.7 [5.3] dB). Overall MS per eye was 0.086 dB lower per year of additional age (95% CI, −0.13 to −0.041; P < .001) and 0.21 dB lower per additional year of duration of STGD1 (95% CI, −0.28 to −0.14; P < .001). Longer duration of STGD1 was associated with worse MS (β = −0.18; P < .001), with a lower number of normal test points (β = −0.71; P < .001), and with a higher number of deep scotoma points (β = −0.70; P < .001). We found 11 eyes with low MS (<6 dB) but very good best-corrected visual acuity of at least 72 Early Treatment Diabetic Retinopathy Study letter score (20/40 Snellen equivalent).
Conclusions and Relevance
We provide an extensive analysis of macular sensitivity parameters in STGD1 and demonstrate their association with demographic characteristics and vision. These data suggest microperimetry testing provides a more comprehensive assessment of retinal function and will be an important outcome measure in future clinical trials.
Stargardt disease type 1 (STGD1; OMIM: 248200) is the most common form of juvenile-onset macular dystrophy.1 Pathogenic mutations in the ABCA4 gene lead to atrophic-appearing macular lesions and variable loss of best-corrected visual acuity (BCVA).2 Best-corrected visual acuity can range from 20/20 to 20/400 or worse.3 Measuring the BCVA is a straightforward approach to quantify visual performance and has been widely studied.1,3-5 However, the Progression of Atrophy Secondary to Stargardt disease (ProgStar) study group showed that BCVA is unlikely to be a sensitive outcome measure for treatment trials in STGD1 except in certain subgroups owing to the slow rate of BCVA loss.3,6 Visual field testing is another psychophysical approach, but it misses small scotomas and is often complicated by unstable fixation in macular diseases. Fundus-controlled perimetry (microperimetry) allows for precise sensitivity analysis of the macula by displaying stimuli in preplanned retinal areas.7,8 An eye tracker ensures an exact correlation of macular pathology with functional defects in the Nidek MP-1 microperimeter (MP-1; Nidek Technologies).7 The MP-1 has been shown to be a reliable technique for testing of macular function in longitudinal treatment studies for STGD1.9
In this study, we examined the cross-sectional associations of microperimetric sensitivity data with demographic characteristics and the BCVA in our study cohort with molecularly confirmed STGD1, using data from the baseline examination of the prospective ProgStar study.
The ProgStar study received approval from the Western Institutional Review Board and all institutional review boards of all involved institutions and is in compliance with Health Insurance Portability and Accountability Act of 1996 and the Declaration of Helsinki. Details on all regulatory requirements, the design, organization, inclusion and exclusion criteria, the data collection, and management processes are described in ProgStar Report No. 1.10 This report also details the certification processes, the coordinating, and data management centers, and the strategies to ensure quality and completeness of the examinations and the gradings.
The Nidek MP-1 microperimeter (NAVIS Software 1.7.7 or higher; Nidek Technologies SRL) was used to perform testing. Sensitivity was tested in 68 macular test locations in a pattern comparable with the Humphrey 10-2 pattern (eFigure 1 in the Supplement) using white size 3 stimuli (0.43 arc degrees; comparable with Goldmann III) with a duration of 200 milliseconds on a white monochromatic background and a 4-2 strategy. In the ProgStar study, optical coherence tomography data were used to center the test pattern manually onto the anatomical fovea as accurately as possible following a standard operating procedure.10,11 In cases with foveal atrophy, the graders looked for the point of maximal inner retinal layer convergence and used the adjoining B-scans immediately superior and inferior to the approximate foveal center to determine this center as precisely as possible. Accurate pattern placement is necessary to ensure proper structure-function correlation, ie, to ensure that the central 4 foveal points actually test the function of the foveal region, although this approach leads to exclusion of a significant amount of eyes from the analysis. All tests were performed under almost dark (mesopic) light conditions. The sensitivity at each retinal location was determined by iteratively adjusting the light intensity until the dimmest visible stimulus was found. The sensitivity for each test location was determined on a scale of 0 dB to 20 dB. Test locations with 0 dB (ie, retinal locations where only the brightest stimulus was detected or no stimulus at all was detected) were defined as “deep scotoma,” and test locations with more than 0 dB but less than 12 dB were defined as “relative scotoma.” The ProgStar protocol did not include the testing of normal individuals but based on the literature12,13 and experience to date, loci with 12 dB or higher sensitivity were considered to be normal, near-normal, or at least not substantially abnormal. For simplicity, these test locations with 12 dB to 20 dB are therefore referred to as “normal.” All examinations were performed monocularly, with the contralateral eye patched. The central 4 points were 1.7° away from the anatomical fovea and were grouped as “foveal”; the 12 perifoveal points were at a distance of 3.5° to 4.7° from the center of the anatomical fovea and were grouped as the “inner ring”; and the remainder of the test locations between 5.6° to 10.1° from the fovea were grouped as the “outer ring” (eFigure 1 in the Supplement).
The central reading center categorized the pattern placement on the fovea as “adequate,” “poor,” or “cannot grade.” When the center of the grid was within less than 1° from the anatomical fovea, this was graded as “adequate.” Distances from 1° to less than 2° were “fair.” “Poor” pattern placement means that the grid was improperly placed at a distance of at least 2° from the fovea (eyes with such “poor” placement were excluded from the main analysis).
Linear models with generalized estimating equations were used to estimate the associations between the outcome parameters while accounting for between-eye correlations. Aggregated residuals were used for model assessment. If the assumption of a linear relationship between an independent variable and the outcome variable was not met, piecewise linear models with generalized estimating equations were used where the cutoff value for the final model was determined through iterative model fitting and was the value that yielded the minimum information criteria in the model fit. Multivariable regression models were used including explanatory variables that were significant in univariate analyses, with the appropriate P values ≤ .10.
Between October 21, 2013, and January 30, 2015, a total of 259 patients and 489 eyes were enrolled at 9 centers in the prospective ProgStar study.10 The MP-1 testing was available and graded for 440 eyes. To increase the quality of our data set, 80 eyes with poor pattern placement and 34 eyes with ungradable pattern placement were excluded from the final analysis; a final cohort of 326 eyes (199 participants; 114 women and 85 men) was included. eTable 1 in the Supplement shows the demographic features for all patients and the subgroups. No differences in most characteristics between those with adequate vs poor or ungradable pattern placement were found (with the only exception that in the latter group, African American and Asian ethnicities appeared to be more prevalent). For the qualifying cohort (at least 1 eye with adequate or fair pattern placement), the mean (SD) patients age was 34.2 (14.7) years, and the median BCVA was 43 Early Treatment Diabetic Retinopathy Study (ETDRS) letter score (approximately 20/125; mean [SD], 47.8 [16.9]; range, 20-88). Best-corrected visual acuity was 4.0 ETDRS letter score lower (95% CI, −6.13 to −1.80; P < .001) among patients with poor or ungradable pattern placement.
Figure 1 presents the detailed enrollment count. We present herein the results from the 326 eyes following exclusion of eyes with poor or ungradable pattern placement; data for all 440 eyes are provided in eTables 3-5 in the Supplement.
The median of the mean sensitivity per eye (MS) throughout all 68 points assessed with the MP-1 was 12.4 dB (mean [SD], 11  dB; range, 0- 19.9 dB; n = 322 eyes). The number of normal points and relatively and deeply scotomatous points is shown in Table 1. The median MS was worse when measured in the foveal 4 points (0 dB) and best in the outer ring (14.5 dB). This trend was also reflected by the distribution of deeply scotomatous points, the mean percentage of which among all tested locations was highest at the fovea (73%), intermediate in the inner ring (46%), and smallest in the outer ring (15%) (eTable 2 in the Supplement). Overall, MS measurements were highly correlated between the right and left eyes (overall MS ρ = 0.95; P < .001; n = 124). The correlation of MS between the right and left eye was weaker in the foveal 4 points (foveal MS ρ = 0.75; P < .001; n = 125) than in the inner ring (inner ring MS ρ = 0.91; P < .001; n = 125) or outer ring (outer ring MS ρ = 0.95; P < .001; n = 125). The Pearson correlation coefficient of the BCVA between the right and left eye (BCVA ρ = 0.78; P < .001; n = 127) was similar to that of the foveal MS.
The total number of normal, relatively scotomatous, and deeply scotomatous points among the 68 test locations for each eye showed that the median number of locations with normal sensitivity was higher (median, 49 points; range, 0-68 points) than for points categorized as a relative scotoma (median, 8 points; range, 0-43 points) or deep scotoma (median, 10 points; range, 0-68 points). eTable 3 in the Supplement shows the detailed results from sensitivity testing in the entire cohort including eyes with poor pattern placement.
Table 1 summarizes the association of sensitivity testing with demographic features. Overall MS was 0.086 dB lower per year of additional age (95% CI, −0.13 to −0.041; P < .001) in the univariate model. Better MS of all 68 test locations was significantly associated with younger current patient age (β = −0.09; 95% CI, −0.13 to −0.04; P < .001, Figure 2) and with shorter duration of STGD1 symptoms (β = −0.71; 95% CI, −1.10 to −0.32; P < .001, Figure 2) but not with age at diagnosis of STGD1 older than 18 years (β = 0.014; 95% CI, −1.44 to 1.47; P = .98), race/ethnicity (β = 0.26; 95% CI, −1.75 to 2.27; P = .80), or sex (β = 0.55; 95% CI, −0.86 to 1.96; P = .44). The number of normal test locations (test locations ≥12 dB) was significantly associated with age younger than 50 years, with those patients’ eyes having a mean of 13.4 more normal points (P < .001). A larger number of normal test locations was also associated with shorter duration of STGD1 (P < .001). Similarly, a higher number of deeply scotomatous locations was associated with longer duration of STGD1 symptoms (P < .001) and with an age older than 50 years (P = .004) with their eyes having on average 9.3 additional deep scotomas.
On multivariate analysis accounting for the different demographic measures, duration of STGD1 was the demographic feature associated with most measures of sensitivity in the macular region (Table 1). There were significant associations with the overall MS (β = −0.18; 95% CI, −0.27 to −0.09; P < .001), with the number of normal test locations (β = −0.71; 95% CI, −1.10 to −0.32; P < .001), and the number of deep scotoma points (β = −0.70; 95% CI, 0.37-1.04; P < .001). After accounting for duration of STGD1, there were no longer associations with current age for any of the 3 measures of sensitivity in the macula. eTable 4 in the Supplement presents the results from the entire cohort (including poor pattern placement) which were essentially equivalent.
The association of macular sensitivity and BCVA are presented in Table 2. Best-corrected visual acuity was 1.2 ETDRS letter score lower per 1 dB worse MS (95% CI, 0.75 to 1.64; P < .001). On multivariate analysis simultaneously, including the mean sensitivities in the fovea, in the inner, and in the outer ring, BCVA was 0.62 ETDRS letter score worse per 1 dB less MS among the foveal 4 points (95% CI, 0.1 to 1.14; P = .02); the association was similar for the inner ring where 1 dB decreased MS was associated with 0.59 ETDRS letter score worse BCVA (95% CI, 0.05 to 1.14; P = .03); there was no association of the MS in the outer ring with the BCVA (P = .22). In both the univariate and multivariate analyses, a higher number of deep scotoma points was associated with worse BCVA (β = −0.30; P < .001). eFigure 2 in the Supplement shows these associations in the univariate analysis. Closer analysis of the scatterplot (eFigure 2 in the Supplement) revealed that there are some cases with low MS (<6 dB) but very good BCVA (≥72 ETDRS letter score; ≥20/40). We observed 11 such eyes. Figure 3 shows an illustrative example: all 11 eyes had a small preserved foveal island of nonatrophic retina used for fixation accounting for the good BCVA. However, the preserved island was too small to be covered by any of the central 4 test locations. eTable 5 in the Supplement shows these correlations for the entire cohort.
This study investigated light sensitivity parameters of the macula obtained with fundus-controlled (micro)perimetry in patients with STGD1 and found an overall MS (SD) of 11.0 (5.0) dB. Both the MS and the number of scotomatous points show that the ability to perceive light stimuli of the central retina is reduced in STGD1. Longer duration of symptoms was associated with worse sensitivity of the macula, and the sensitivity parameters correlated with BCVA, although not tightly. Using the MP-1, Testa et al14 reported comparable mean MS results of around 10 dB in a cross-sectional analysis of molecularly confirmed patients with STGD1 with an age at onset of first symptoms younger than 30 years.14 In our cohort, the mean of the MS in all tested locations was 11.0 dB, which is consistent with the report by Testa et al14 given the later age at first symptoms of the disease in our cohort. Later onset of symptoms has been shown to be associated with a milder course of the disease.3 Because macular sensitivity in any tested location should be close to 20 dB in age-matched healthy control individuals,15 our results suggest that the functional deficit in STGD1 is most pronounced in the foveal center, while it is relatively preserved in the peripheral macula.
Our results show that better ability to perceive light stimuli in the macula is significantly associated with younger patient age (P < .001) (univariate analysis) and shorter duration of STGD1 (multivariate analysis). Both a higher overall MS as well as a higher number of test locations categorized as “normal” and a lower number of “deeply scotomatous” points were associated with shorter duration of symptoms and younger patient age. Using the Nidek MP-1, Midena et al15 showed that healthy individuals in their 20s have an MS that is about 1 dB higher than those of healthy people aged 70 to 75 years. The reasons for the age-related decrease of light sensitivity have been attributed to preretinal factors, such as ocular media opacities or smaller pupil size,16 or to neural losses.17 However, this natural decline in sensitivity of the macula is negligible when compared with the loss in sensitivity we found in our STGD1 cohort. According to our cross-sectional results, 1 year of additional reported duration of STGD1 was associated with 0.21 dB lower MS. Therefore, if compared with the Midena et al study,15 a decline in MS throughout 50 years of normal aging is comparable with what we would expect after 5 years in these patients with STGD1. Our results are in accordance with prior reports on better BCVA outcomes in late-onset cases of STGD118 and shorter duration of STGD1.14 Further investigation of longitudinal macular sensitivity data will be conducted in the ProgStar study, differentiating between early- and late-onset cases because patients with an early onset of the disease are expected to have a more rapid decline in visual function.19
We found that better MS is associated with better BCVA. However, there were sporadic cases with eyes with an MS better than 16 dB and a BCVA of less than 40 ETDRS letter score. On the other hand, we encountered 11 eyes with a discrepancy between the BCVA and MS readings, with BCVA of at least 72 ETDRS letter score (approximately 20/40) and MS less than 6 dB. The one example outlined in Figure 3 shows that focally preserved retinal structure as seen on fundus autofluorescence imaging accounts for such cases. A fovea-sparing phenotype of STGD1 has been described, and macular pigment may play an important role in such cases.9,11,20,21 Microperimetry underestimates the true visual acuity potential for this phenotype, whereas BCVA alone does not capture the extensive loss of sensitivity in the rest of the macula.8 Therefore, for a comprehensive assessment of retinal function in STGD1 and possibly in a larger group of macular diseases including age-related macular degeneration, both BCVA and microperimetric sensitivity testing should be considered, although both show strong associations.
Because the visual resolution is highest in the foveal center, where it is limited only by cone spacing,22 we had expected a strong relationship between the MS in the fovea with BCVA. Surprisingly, we found an almost identical association for the inner ring. This suggests that a relatively large area extending to an eccentricity of about 4° from the foveal center is critical for BCVA testing and high-resolution visual perception, possibly with eccentric fixation within 4° from the foveal center.23 It is also possible that our inclusion criteria may account for this finding because they allowed a freedom of 2° grid displacement. Therefore, it is possible that some of the inner ring points were actually in the fovea. On multivariate analysis, the sensitivity in the outer ring did not correlate with BCVA (β = 0.34; P = .22) suggesting that the visual resolution in the outer ring is relatively poor and functional loss of the outer ring area is not associated with additional loss of BCVA.
Our results also show that eyes with less than 20 locations of relative scotoma or less than 20 deep scotoma points were associated with a wide range of BCVA outcomes, from 20 to more than 80 ETDRS letter score. A higher number of deep scotoma points was associated with worse BCVA (β = −0.30; P < .001).
Limitations of the presented research include the cross-sectional nature of the data. The primary outcome parameter of the ProgStar studies is the size of atrophic lesions on fundus autofluorescence testing that resulted in a minimum fundus autofluorescence lesion size as an inclusion criterion. Hence, very early stages of disease without any obvious anatomical changes were not included, and we did not analyze the function of the macula in such cases.
We show that microperimetry is as an important outcome measure for describing the functional status of the macula in STGD1. Our forthcoming longitudinal data may show whether it is useful for also detecting functional change. Microperimetry adds to the information provided by BCVA testing and allows for a more comprehensive assessment of macular function. The microperimetric sensitivity data may also be correlated with the location of the center of fixation. Investigating the correlation of fixation data with sensitivity data of the central macula would permit the identification of a lower threshold of retinal sensitivity beneath which fixation is more liable to become eccentric. In addition, further correlation of the presented data with optical coherence tomographic 24,25 and fundus autofluorescence–derived26,27 measures to show structure-function correlations will be calculated with the longitudinal 12- and 24-months follow-up data from the ProgStar study.10
Corresponding Author: Hendrik P. N. Scholl, MD, Department of Ophthalmology, University of Basel, Mittlere Strasse 91, CH-4031 Basel, Switzerland (email@example.com).
Accepted for Publication: March 20, 2017.
Published Online: May 25, 2017. doi:10.1001/jamaophthalmol.2017.1162
Author Contributions: Dr Scholl had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.
These authors contributed equally to this work: Drs Schönbach, Wolfson and Strauss.
Concept and design: Schönbach, Wolfson, Strauss, Kong, Birch, Sadda, West, Scholl.
Acquisition, analysis, or interpretation of data: Schönbach, Wolfson, Strauss, Ibrahim, Kong, Muñoz, Birch, Cideciyan, Hahn, Nittala, Sunness, Scholl.
Drafting of the manuscript: Schönbach, Muñoz, West, Scholl.
Critical revision of the manuscript for important intellectual content: Schönbach, Wolfson, Strauss, Ibrahim, Kong, Birch, Cideciyan, Hahn, Nittala, Sunness, Sadda, West, Scholl.
Statistical analysis: Wolfson, Kong, Muñoz, Sunness, Sadda, West, Scholl.
Obtained funding: Schönbach, Strauss, West, Scholl.
Administrative, technical, or material support: Strauss, Ibrahim, Birch, Cideciyan, Hahn, Nittala, West, Scholl.
Supervision: Strauss, Birch, Sadda, West, Scholl.
Conflict of Interest Disclosures: All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Dr Scholl is a paid consultant of the following entities: Astellas Institute for Regenerative Medicine; Boehringer Ingelheim Pharma GmbH and Co KG; Daiichi Sankyo Inc; Gerson Lehrman Group; Guidepoint; and Shire. Dr Scholl is member of the Scientific Advisory Board of Gensight Biologics; Vision Medicines Inc; and Intellia Therapeutics Inc. Dr Scholl is member of the Data Monitoring and Safety Board/Committee of the following entities: Genentech Inc/F. Hoffmann-La Roche Ltd; Genzyme Corp/Sanofi, and ReNeuron Group Plc/Ora Inc. These arrangements have been reviewed and approved by the Johns Hopkins University in accordance with its conflict of interest policies. Johns Hopkins University and Bayer Pharma AG have an active research collaboration and option agreement. These arrangements have also been reviewed and approved by the University of Basel in accordance with its conflict of interest policies. Dr Hendrik Scholl is principal investigator of grants at the University of Basel sponsored by the following entities: Acucela Inc; NightstaRx Ltd; and QLT Inc. Grants at University of Basel are negotiated and administered by the institution, which receives them on its proper accounts. Individual investigators who participate in the sponsored project(s) are not directly compensated by the sponsor but may receive salary or other support from the institution to support their effort on the project(s). Dr Sheila West is a scientific technical advisory committee member for the Alcon Research Institute and for Research to Prevent Blindness. Dr Yulia Wolfson is an employee for Optovue Inc. No other disclosures were reported.
Funding/Support: The ProgStar studies are supported by the Foundation Fighting Blindness Clinical Research Institute and a grant to Foundation Fighting Blindness Clinical Research Institute by the US Department of Defense USAMRMC TATRC, Fort Meade, Maryland (grant numbers W81-XWH-07-1-0720 and W81XWH-09-2-0189); Dr Etienne Schönbach is supported by grant LPDS 2015-14 from the Leopoldina Fellowship Program, German National Academy of Sciences. Dr Rupert W. Strauss is supported by grant number J 3383-B23 from the Austrian Science Fund.
Role of the Funder/Sponsor: Foundation Fighting Blindness Clinical Research Institute supported the conduct of the study and data collection. Other funding organizations did not play any role in the design or conduct of the study; collection, management, analysis, interpretation of the data; preparation, review, or approval of the manuscript; nor the decision to submit the manuscript for publication.
Group Information: The ProgStar Study Group members are listed in order of institute:
Chair’s Office, Wilmer Eye Institute, Baltimore, Maryland: Hendrik P.N. Scholl, MD, MA; Rupert W. Strauss, MD; Yulia Wolfson, MD; Millena Bittencourt, MD; Syed Mahmood Shah, MD; Mohamed Ibrahim Ahmed, MD; Etienne Schönbach, MD; Kaoru Fujinami, MD, PhD
Cole Eye Institute, Cleveland, Ohio: Elias Traboulsi, MD; Justis Ehlers, MD; Meghan Marino, MS; Susan Crowe, BS; Rachael Briggs, COA ; Angela Borer, BHA; Anne Pinter, CRA; Tami Fecko; Nikki Brugnoni, BS
Greater Baltimore Medical Center, Towson, Maryland: Janet S. Sunness, MD; Carol Applegate, MLA, CO; Leslie Russell, MAc;
Moorfields Eye Hospital, London, England: Michel Michaelides, MD; Simona Degli Esposti, MD; Anthony Moore ; Andrew Webster, MD; Sophie Connor, BSc; Jade Barnfield, BA; Zaid Salchi, MD; Clara Alfageme, MD; Victoria McCudden; Maria Pefkianaki, MD; Jonathan Aboshiha, MA, MB; Gerald Liew; Graham Holder, PhD; Anthony Robson, PhD; Alexa King, BA; Daniela Ivanova Cajas Narvaez, MSc; Katy Barnard, BS; Catherine Grigg, BSc; Hannah Dunbar, PhD; Yetunde Obadeyi; Karine Girard-Claudon, MST; Hilary Swann, BSc; Avani Rughani, BSc; Charles Amoah, NVQ; Dominic Carrington; Kanom Bibi, BSc; Emerson Ting Co, DMD; Mohamed Nafaz Illiyas; Hamida Begum, BSc; Andrew Carter, BSc; Anne Georgiou, PhD; Selma Lewism BSc; Saddaf Shaheen, PGDip, BSc; Harpreet Shinmar, MSc; Linda Burton, BSc
Moran Eye Center, Salt Lake City, Utah: Paul Bernstein, MD, PhD; Kimberley Wegner, BS; Briana Lauren Sawyer, MS; Bonnie Carlstrom, COA; Kellian Farnsworth, COA; Cyrie Fry, AS, CRA, OCT-C; Melissa Chandler, BS, CRC, OCT-a; Glen Jenkins, BS, COA, CRC, OCT-a; Donnel Creel, PhD
Retina Foundation of the Southwest, Dallas, Texas: David Birch, PhD; Yi-Zhong Wang, PhD; Luis Rodriguez, BS; Kirsten Locke, BS; Martin Klein, MS; Paulina Mejia, BS
Scheie Eye Institute, Philadelphia, Pennsylvania: Artur V. Cideciyan, PhD; Samuel G. Jacobson, MD, PhD; Sharon B. Schwartz, MS, CGC; Rodrigo Matsui, MD; Michaela Gruzensky, MD; Jason Charng, OD, PhD; Alejandro J. Roman, MS;
University of Tübingen, Tübingen, Germany: Eberhart Zrenner, PhD; Fadi Nasser, MD; Gesa Astrid Hahn, MD; Barbara Wilhelm, MD; Tobias Peters, MD; Benjamin Beier, BSc; Tilman Koenig; Susanne Kramer, Dipl. Biol.
The Vision Institute, Paris, France: José-Alain Sahel, MD; Saddek Mohand-Said, MD, PhD; Isabelle Audo, MD, PhD; Caroline Laurent-Coriat, MD; Ieva Sliesoraityte, MD, PhD; Christina Zeitz, PhD ; Fiona Boyard, BS; Minh Ha Tran, BS; Mathias Chapon, COT; Céline Chaumette, COT; Juliette Amaudruz, COT; Victoria Ganem, COT; Serge Sancho, COT; Aurore Girmens, COT
Wilmer Eye Institute, Baltimore, Maryland: Hendrik P.N. Scholl, MD; Rupert W. Strauss, MD; Yulia Wolfson, MD; Syed Mahmood Shah, MD; Mohamed Ibrahim Ahmed, MD; Etienne Schönbach, MD; Robert Wojciechowski, PhD; Shazia Khan, MD; David G. Emmert, BA; Dennis Cain, CRA; Mark Herring, CRA; Jennifer Bassinger, COA; Lisa Liberto, COA
Dana Center Data Coordinating Center, Wilmer Eye Institute, Baltimore, Maryland: Sheila West, PhD; Ann-Margret Ervin, PhD; Beatriz Munoz, MS; Xiangrong Kong, PhD; Kurt Dreger, BS; Jennifer Jones, BA
Doheny Image Reading Center, Doheny Eye Institute, Los Angeles, California: Srinivas Sadda, MD; Michael S. Ip, MD; Anamika Jha, MBS; Alex Ho, BS; Brendan Kramer, BA; Ngoc Lam, BA; Rita Tawdros, BS; Yong Dong Zhou, MD, PhD; Johana Carmona, HS; Akihito Uji, MD, PhD; Amirhossein Hariri, MD; Amy Lock, BS; Anthony Elshafei, BS; Anushika Ganegoda, BS; Christine Petrossian, BS; Dennis Jenkins, MPH; Edward Strnad, BS; Elmira Baghdasaryan, MD; Eric Ito, OD; Feliz Samson, BS; Gloria Blanquel, BS; Handan Akil, MD, FEBOpht; Jhanisus Melendez, MS; Jianqin Lei, MD; Jianyan Huang, MD, PhD; Jonathan Chau, BS; Khalil G. Falavarjani, MD ; Kristina Espino, BS; Manfred Li, BS; Maria Mendoza, BS; Muneeswar Gupta Nittala, MPhil Opt; Netali Roded, BS; Nizar Saleh, MD; Ping Huang, MD, PhD; Sean Pitetta, BS; Siva Balasubramanian, MD, PhD; Sophie Leahy, BA; Sowmya J. Srinivas, MBBS; Swetha B. Velaga, B Opt; Teresa Margaryan, BA ; Tudor Tepelus, PhD; Tyler Brown, BS; Wenying Fan, MD; Yamileth Murillo, BA; Yue Shi, MD, PhD; Srinivas Sadda, MD; Michael S. Ip, MD; Anamika Jha, MBS; Alex Ho, BS; Brendan Kramer, BA; Ngoc Lam, BA; Rita Tawdros, BS; Yong Dong Zhou, MD, PhD; Katherine Aguilar , BS; Cynthia Chan, BS; Lisa Santos, HS; Brian Seo, BA; Christopher Sison, BS; Silvia Perez, BS; Stephanie Chao, HS; Kelly Miyasato, MPH; Julia Higgins, MS; Zoila Luna , MHA; Anita Menchaca, BS; Norma Gonzalez, MA; Vicky Robledo, BS; Karen Carig, BS; Kirstie Baker, HS; David Ellenbogen, BS; Daniel Bluemel, AA; Theo Sanford, BS; Daisy Linares, HS; Mei Tran, BA; Lorane Nava, HS; Michelle Oberoi, BS; Mark Romero, HS; Vivian Chiguil, HS; Grantley Bynum-Bain, BA; Monica Kim, BS; Carolina Mendiguren, MEM; Xiwen Huang, MPH; Monika Smith, HS; Johana Carmona, HS
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