Abstract
Purpose: To report the yearly rate of change in macular function in patients with Stargardt disease type 1 (STGD1) over 24 months and to establish a new volumetric visual function index for use in clinical trials investigating the efficacy on retinal sensitivity. Methods: Design: International, multicenter, prospective cohort study with 5 study visits every 6 months over 24 months. Participants: A total of 233 individuals with genetically confirmed STGD1 (≥1 disease-causing ABCA4 variant). Main Outcome Measures: The total volume (VTOT) beneath the sensitivity surface of a 3-D model of the hill of vision and mean sensitivity (MS) derived from mesopic microperimetry performed with a white stimulus. Changes of VTOT over time and its correlation with the ABCA4 genotype and baseline features. Results: At baseline, 440 eyes (233 patients) with a mean (SD) age of 33.7 (15.0) years, mean (SD) visual acuity of 46.08 (16.03) ETDRS letters were analyzed with an average VTOT of 0.91 decibel-steradian (dB-sr) and an MS of 10.73 dB. The overall mean rate of decrease in sensitivity [95% confidence interval] was 0.077 [0.064, 0.090] dB-sr/y for VTOT and 0.87 [0.72, 1.02] dB/year for MS. The progression rate of VTOT depended on baseline visual function (0.029 dB-sr/year for low and 0.120 dB-sr/year for high baseline VTOT; P < .001) and exhibited a difference in the first vs second year of follow-up (0.065 dB-sr/year vs 0.089 dB-sr/year, respectively; P < .001). The absence of pigmentary abnormalities of the retinal pigment epithelium at baseline was found to be associated with a faster progression rate (P < .001), whereas a significant association with the genotype was not detected (P = .7). Conclusion: In STGD1, both microperimetric outcomes demonstrate statistically significant and clinically meaningful changes after relatively short follow-up periods. Volumetric modeling may be useful in future interventional clinical trials that aim to improve retinal sensitivity or to slow down its decline and for structure-function correlations.
| Original language | English (US) |
|---|---|
| Pages (from-to) | 123-133 |
| Number of pages | 11 |
| Journal | American journal of ophthalmology |
| Volume | 230 |
| DOIs | |
| State | Published - Oct 2021 |
ASJC Scopus subject areas
- Ophthalmology
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In: American journal of ophthalmology, Vol. 230, 10.2021, p. 123-133.
Research output: Contribution to journal › Article › peer-review
}
TY - JOUR
T1 - The Progression of Stargardt Disease Using Volumetric Hill of Vision Analyses Over 24 Months
T2 - ProgStar Report No.15
AU - for the ProgStar Study Group
AU - Schönbach, Etienne M.
AU - Janeschitz-Kriegl, Lucas
AU - Strauss, Rupert W.
AU - Cattaneo, Marco E.G.V.
AU - Fujinami, Kaoru
AU - Birch, David G.
AU - Cideciyan, Artur V.
AU - Sunness, Janet S.
AU - Weleber, Richard G.
AU - Ip, Michael S.
AU - Sadda, Srini Vas R.
AU - Scholl, Hendrik P.N.
N1 - Funding Information: Funding/Support: The ProgStar studies are supported by the Foundation Fighting Blindness (FFB) Clinical Research Institute (Columbia, Maryland, USA) and a grant by the U.S. Department of Defense USAMRMC TATRC to FFB (Fort Meade, Maryland, USA, grant numbers W81‐XWH‐07‐1‐0720 and W81-XWH‐09‐2‐0189). The funding organizations had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication. Financial Disclosures: Dr Schönbach is supported by the German National Academy of Sciences Leopoldina, Grant Number LPDS 2015-14 (Halle, Germany) and the Foundation Fighting Blindness Clinical Research Institute (Columbia, Maryland, USA). Dr Strauss is supported by the Austrian Science Fund (Vienna, Austria; FWF; project number: J 3383-B23) and the Foundation Fighting Blindness Clinical Research Institute (Columbia, Maryland, USA). The departments of ophthalmology, Kepler University Clinic Linz and Medical University Graz are affiliated members of the European Reference Network (ERN) for Orphan diseases (ERN-EYE). Dr Fujinami is a consultant for Astellas Pharma Inc (Tokyo, Japan), Kubota Pharmaceutical Holdings Co, Ltd, Acucela Inc (Tokyo, Japan), Novartis Japan (Tokyo, Japan), Janssen Pharmaceutica Japan (Tokyo, Japan), and Sanofi Genzyme (Cambridge, Massachusetts, USA) and supported by a Grant-in-Aid for Young Scientists (A) of the Ministry of Education, Culture, Sports, Science and Technology, Japan (16H06269), Grant-in-Aid for Scientists to support international collaborative studies of the Ministry of Education, Culture, Sports, Science and Technology, Japan (16KK01930002), National Hospital Organization Network Research Fund, Japan (H30-NHO-Sensory Organs-03), Japan Agency for Medical Research and Development (18ek0109355h0001), Foundation Fighting Blindness Alan Laties Career Development Program (CF-CL-0416-0696-UCL), USA; Health Labour Sciences Research Grant, The Ministry of Health Labour and Welfare, Japan (201711107A), Great Britain Sasakawa Foundation Butterfield Awards, UK. Dr Birch is supported by NIH EY009076 and the Foundation Fighting Blindness Clinical Research Institute (Columbia, Maryland, USA) and is a consultant for AGTC (Alachua, Florida, USA), Iveric (New York, New York, USA), ProQR (Leiden, The Netherlands), Editas (Cambridge, Massachusetts, USA), and Nacuity (Ft. Worth, Texas, USA). Dr Birch is supported by the Foundation Fighting Blindness Clinical Research Institute (FFB CRI, Columbia, Maryland, USA). Dr Sunness is a consultant for Genentech (San Francisco, California, USA), on the scientific advisory board of Acucela (Tokyo, Japan) and Apellis (Crestwood, Kentucky, USA), and on the data safety and monitoring committee for Cell Cure's OpRegen study (Jerusalem, Israel). Dr Weleber and Scott Gillespie are named patent holders for VFMA application and methodology, US Patent US8657446B2. Dr Weleber serves on the Scientific Advisory Board for Applied Genetic Technologies Corporation (Alachua, Florida, USA), serves on the Exdecutive Scientific Advisory Board and as Vice-Chair of The Scientific Advisory Committee for Foundation Fighting Blindness (Columbia, Maryland, USA), and is a consultant for Janssen Research (Raritan, New Jersey, USA). Dr Sadda is a consultant for Allergan (Dublin, Republic of Ireland), CenterVue (Padova, Italy), Genentech (San Francisco, California, USA), Heidelberg Engineering (Heidelberg, Germany), Amgen (Thousand Oaks, California, USA) Merck (Kenilworth, New Jersey, USA), 4DMT (Emeryville, Georgia, USA), Regeneron (Tarrytown, New York, USA), Novartis (Basel, Switzerland), Optos (Dunfermline, UK), and Thrombogenics (Leuven, Belgium). Dr Sadda also receives research instruments from Nidek (Gamagori, Japan), Carl Zeiss Meditec (Dublin, California, USA), CenterVue (Padova, Italy), Optos (Dunfermline, UK), and Topcon (Tokyo, Japan). Dr Scholl is on the data monitoring committee for the following entities: Genentech Inc (San Francisco, CaliforniaA)/F. Hoffmann-La Roche Ltd (CHROMA and SPECTRI trials, Basel, Switzerland); Genzyme Corp (Newark, California, USA)/Sanofi (Paris, France), and ReNeuron Group Plc (Guildford, UK,)/Ora Inc (Andover, Massachusetts, USA). Dr Scholl is on the steering committee of Novo Nordisk (FOCUS trial, Bagsværd, Denmark). Dr Scholl in on the scientific advisory board of the following entities: Astellas Institute for Regenerative Medicine (Chūō, Tokyo); Gensight Biologics (Paris, France); Ionis Pharmaceuticals, Inc (Carlsbad, California, USA); Pharma Research & Early Development (pRED) of F. Hoffmann-La Roche Ltd (Newark, California, USA). Dr Scholl is a consultant for the following entities: Boehringer Ingelheim Pharma GmbH & Co. KG (Ingelheim am Rhein, Germany); Daiichi Sankyo, Inc. (Chūō, Tokyo, Japan); Gerson Lehrman Group (New York, New York, USA); Guidepoint (New York, N ew York, USA). Dr Scholl is co-director of the Institute of Molecular and Clinical Ophthalmology Basel (IOB), which is constituted as a nonprofit foundation and receives funding from the University of Basel, the University Hospital Basel, Novartis, and the government of Basel-Stadt. These arrangements have been reviewed and approved by the Universitätsspital Basel (USB) in accordance with its conflict of interest policies. Dr Scholl receives grant support (Institutional Service Agreements) from the following entities: Acucela Inc; Kinarus AG; NightstaRx Ltd; Ophthotech Corporation; Spark Therapeutics England, Ltd. Grants to investigators at USB are administered by the institution (USB), 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). The following authors have nothing to disclose: Drs Janeschitz-Kriegl, Cattaneo, Cideciyan, and Ip. None of the authors has a commercial conflict of interest related to the content of this manuscript. All authors attest that they meet the current ICMJE criteria for authorship. Funding Information: Funding/Support: The ProgStar studies are supported by the Foundation Fighting Blindness (FFB) Clinical Research Institute (Columbia, Maryland, USA) and a grant by the U.S. Department of Defense USAMRMC TATRC to FFB (Fort Meade, Maryland, USA, grant numbers W81‐XWH‐07‐1‐0720 and W81-XWH‐09‐2‐0189). The funding organizations had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication. Financial Disclosures: Dr Schönbach is supported by the German National Academy of Sciences Leopoldina, Grant Number LPDS 2015-14 (Halle, Germany) and the Foundation Fighting Blindness Clinical Research Institute (Columbia, Maryland, USA). Dr Strauss is supported by the Austrian Science Fund (Vienna, Austria; FWF; project number: J 3383-B23) and the Foundation Fighting Blindness Clinical Research Institute (Columbia, Maryland, USA). The departments of ophthalmology, Kepler University Clinic Linz and Medical University Graz are affiliated members of the European Reference Network (ERN) for Orphan diseases (ERN-EYE). Dr Fujinami is a consultant for Astellas Pharma Inc (Tokyo, Japan), Kubota Pharmaceutical Holdings Co, Ltd, Acucela Inc (Tokyo, Japan), Novartis Japan (Tokyo, Japan), Janssen Pharmaceutica Japan (Tokyo, Japan), and Sanofi Genzyme (Cambridge, Massachusetts, USA) and supported by a Grant-in-Aid for Young Scientists (A) of the Ministry of Education, Culture, Sports, Science and Technology, Japan (16H06269), Grant-in-Aid for Scientists to support international collaborative studies of the Ministry of Education, Culture, Sports, Science and Technology, Japan (16KK01930002), National Hospital Organization Network Research Fund, Japan (H30-NHO-Sensory Organs-03), Japan Agency for Medical Research and Development (18ek0109355h0001), Foundation Fighting Blindness Alan Laties Career Development Program (CF-CL-0416-0696-UCL), USA; Health Labour Sciences Research Grant, The Ministry of Health Labour and Welfare, Japan (201711107A), Great Britain Sasakawa Foundation Butterfield Awards, UK. Dr Birch is supported by NIH EY009076 and the Foundation Fighting Blindness Clinical Research Institute (Columbia, Maryland, USA) and is a consultant for AGTC (Alachua, Florida, USA), Iveric (New York, New York, USA), ProQR (Leiden, The Netherlands), Editas (Cambridge, Massachusetts, USA), and Nacuity (Ft. Worth, Texas, USA). Dr Birch is supported by the Foundation Fighting Blindness Clinical Research Institute (FFB CRI, Columbia, Maryland, USA). Dr Sunness is a consultant for Genentech (San Francisco, California, USA), on the scientific advisory board of Acucela (Tokyo, Japan) and Apellis (Crestwood, Kentucky, USA), and on the data safety and monitoring committee for Cell Cure's OpRegen study (Jerusalem, Israel). Dr Weleber and Scott Gillespie are named patent holders for VFMA application and methodology, US Patent US8657446B2. Dr Weleber serves on the Scientific Advisory Board for Applied Genetic Technologies Corporation (Alachua, Florida, USA), serves on the Exdecutive Scientific Advisory Board and as Vice-Chair of The Scientific Advisory Committee for Foundation Fighting Blindness (Columbia, Maryland, USA), and is a consultant for Janssen Research (Raritan, New Jersey, USA). Dr Sadda is a consultant for Allergan (Dublin, Republic of Ireland), CenterVue (Padova, Italy), Genentech (San Francisco, California, USA), Heidelberg Engineering (Heidelberg, Germany), Amgen (Thousand Oaks, California, USA) Merck (Kenilworth, New Jersey, USA), 4DMT (Emeryville, Georgia, USA), Regeneron (Tarrytown, New York, USA), Novartis (Basel, Switzerland), Optos (Dunfermline, UK), and Thrombogenics (Leuven, Belgium). Dr Sadda also receives research instruments from Nidek (Gamagori, Japan), Carl Zeiss Meditec (Dublin, California, USA), CenterVue (Padova, Italy), Optos (Dunfermline, UK), and Topcon (Tokyo, Japan). Dr Scholl is on the data monitoring committee for the following entities: Genentech Inc (San Francisco, CaliforniaA)/F. Hoffmann-La Roche Ltd (CHROMA and SPECTRI trials, Basel, Switzerland); Genzyme Corp (Newark, California, USA)/Sanofi (Paris, France), and ReNeuron Group Plc (Guildford, UK,)/Ora Inc (Andover, Massachusetts, USA). Dr Scholl is on the steering committee of Novo Nordisk (FOCUS trial, Bagsværd, Denmark). Dr Scholl in on the scientific advisory board of the following entities: Astellas Institute for Regenerative Medicine (Chūō, Tokyo); Gensight Biologics (Paris, France); Ionis Pharmaceuticals, Inc (Carlsbad, California, USA); Pharma Research & Early Development (pRED) of F. Hoffmann-La Roche Ltd (Newark, California, USA). Dr Scholl is a consultant for the following entities: Boehringer Ingelheim Pharma GmbH & Co. KG (Ingelheim am Rhein, Germany); Daiichi Sankyo, Inc. (Chūō, Tokyo, Japan); Gerson Lehrman Group (New York, New York, USA); Guidepoint (New York, N ew York, USA). Dr Scholl is co-director of the Institute of Molecular and Clinical Ophthalmology Basel (IOB), which is constituted as a nonprofit foundation and receives funding from the University of Basel, the University Hospital Basel, Novartis, and the government of Basel-Stadt. These arrangements have been reviewed and approved by the Universitätsspital Basel (USB) in accordance with its conflict of interest policies. Dr Scholl receives grant support (Institutional Service Agreements) from the following entities: Acucela Inc; Kinarus AG; NightstaRx Ltd; Ophthotech Corporation; Spark Therapeutics England, Ltd. Grants to investigators at USB are administered by the institution (USB), 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). The following authors have nothing to disclose: Drs Janeschitz-Kriegl, Cattaneo, Cideciyan, and Ip. None of the authors has a commercial conflict of interest related to the content of this manuscript. All authors attest that they meet the current ICMJE criteria for authorship. Acknowledgments: Complete list of members of the ProgStar Study team as of September 20, 2017: The ProgStar studies consist of the Chair's Office, 9 clinics, 2 resource centers, and 2 affiliated centers with the following members: Chair's Office: Hendrik P.N. Scholl, Rupert W. Strauss, Yulia Wolfson, Millena Bittencourt, Syed Mahmood Shah, Mohamed Ahmed, Etienne Schönbach, Kaoru Fujinami; Cole Eye Institute, Cleveland: Elias Traboulsi, Justis Ehlers, Meghan Marino, Susan Crowe, Rachael Briggs, Angela Borer, Anne Pinter, Tami Fecko, Nikki Burgnoni; Greater Baltimore Medical Center, Towson: Janet S. Sunness, Carol Applegate, Leslie Russell; Moorfields Eye Hospital, London: Michel Michaelides, Simona Degli Esposti, Anthony Moore, Andrew Webster, Sophie Connor, Jade Barnfield, Zaid Salchi, Clara Alfageme, Victoria McCudden, Maria Pefkianaki, Jonathan Aboshiha, Gerald Liew, Graham Holder, Anthony Robson, Alexa King, Daniela Ivanova Cajas Narvaez, Katy Barnard, Catherine Grigg, Hannah Dunbar, Yetunde Obadeyi, Karine Girard-Claudon, Hilary Swann, Avani Rughani, Charles Amoah, Dominic Carrington, Kanom Bibi, Emerson Ting Co, Mohamed Nafaz Illiyas, Hamida Begum, Andrew Carter, Anne Georgiou, Selma Lewism, Saddaf Shaheen, Harpreet Shinmar, Linda Burton; Moran Eye Center, Salt Lake City: Paul Bernstein, Kimberley Wegner, Briana Lauren Sawyer, Bonnie Carlstrom, Kellian Farnsworth, Cyrie Fry, Melissa Chandler, Glen Jenkins, Donnel Creel; Retina Foundation of the Southwest, Dallas: David Birch, Yi-Zhong Wang, Luis Rodriguez, Kirsten Locke, Martin Klein, Paulina Mejia; Scheie Eye Institute, Philadelphia: Artur V. Cideciyan, Samuel G. Jacobson, Sharon B. Schwartz, Rodrigo Matsui, Michaela Gruzensky, Jason Charng, Alejandro J. Roman; University of Tübingen, Tübingen: Eberhart Zrenner, Fadi Nasser, Gesa Astrid Hahn, Barbara Wilhelm, Tobias Peters, Benjamin Beier, Tilman Koenig, Susanne Kramer; The Vision Institute, Paris: José-Alain Sahel, Saddek Mohand-Said, Isabelle Audo, Caroline Laurent-Coriat, Ieva Sliesoraityte, Christina Zeitz, Fiona Boyard, Minh Ha Tran, Mathias Chapon, Céline Chaumette, Juliette Amaudruz, Victoria Ganem, Serge Sancho, Aurore Girmens; The Wilmer Eye Institute, Baltimore: Hendrik P.N. Scholl, Rupert W. Strauss, Yulia Wolfson, Syed Mahmood Shah, Mohamed Ahmed, Etienne Schönbach, Robert Wojciechowski, Shazia Khan, David G. Emmert, Dennis Cain, Mark Herring, Jennifer Bassinger, Lisa Liberto; Dana Center Data Coordinating Center: Sheila West, Ann-Margret Ervin, Beatriz Munoz, Xiangrong Kong, Kurt Dreger, Jennifer Jones; Doheny Image Reading Center: Srinivas Sadda, Michael S. Ip, Anamika Jha, Alex Ho, Brendan Kramer, Ngoc Lam, Rita Tawdros, Yong Dong Zhou, Johana Carmona, Akihito Uji, Amirhossein Hariri, Amy Lock, Anthony Elshafei, Anushika Ganegoda, Christine Petrossian, Dennis Jenkins, Edward Strnad, Elmira Baghdasaryan, Eric Ito, Feliz Samson, Gloria Blanquel, Handan Akil, Jhanisus Melendez, Jianqin Lei, Jianyan Huang, Jonathan Chau, Khalil G. Falavarjani, Kristina Espino, Manfred Li, Maria Mendoza, Muneeswar Gupta Nittala, Netali Roded, Nizar Saleh, Ping Huang, Sean Pitetta, Siva Balasubramanian, Sophie Leahy, Sowmya J. Srinivas, Swetha B. Velaga, Teresa Margaryan, Tudor Tepelus, Tyler Brown, Wenying Fan, Yamileth Murillo, Yue Shi, Katherine Aguilar, Cynthia Chan, Lisa Santos, Brian Seo, Christopher Sison, Silvia Perez, Stephanie Chao, Kelly Miyasato, Julia Higgins, Zoila Luna, Anita Menchaca, Norma Gonzalez, Vicky Robledo, Karen Carig, Kirstie Baker, David Ellenbogen, Daniel Bluemel, Theo Sanford, Daisy Linares, Mei Tran, Lorane Nava, Michelle Oberoi, Mark Romero, Vivian Chiguil, Grantley Bynum-Bain, Monica Kim, Carolina Mendiguren, Xiwen Huang, Monika Smith, Teresa Margaryan, Natalie Sarreal. Publisher Copyright: © 2021 The Authors
PY - 2021/10
Y1 - 2021/10
N2 - Purpose: To report the yearly rate of change in macular function in patients with Stargardt disease type 1 (STGD1) over 24 months and to establish a new volumetric visual function index for use in clinical trials investigating the efficacy on retinal sensitivity. Methods: Design: International, multicenter, prospective cohort study with 5 study visits every 6 months over 24 months. Participants: A total of 233 individuals with genetically confirmed STGD1 (≥1 disease-causing ABCA4 variant). Main Outcome Measures: The total volume (VTOT) beneath the sensitivity surface of a 3-D model of the hill of vision and mean sensitivity (MS) derived from mesopic microperimetry performed with a white stimulus. Changes of VTOT over time and its correlation with the ABCA4 genotype and baseline features. Results: At baseline, 440 eyes (233 patients) with a mean (SD) age of 33.7 (15.0) years, mean (SD) visual acuity of 46.08 (16.03) ETDRS letters were analyzed with an average VTOT of 0.91 decibel-steradian (dB-sr) and an MS of 10.73 dB. The overall mean rate of decrease in sensitivity [95% confidence interval] was 0.077 [0.064, 0.090] dB-sr/y for VTOT and 0.87 [0.72, 1.02] dB/year for MS. The progression rate of VTOT depended on baseline visual function (0.029 dB-sr/year for low and 0.120 dB-sr/year for high baseline VTOT; P < .001) and exhibited a difference in the first vs second year of follow-up (0.065 dB-sr/year vs 0.089 dB-sr/year, respectively; P < .001). The absence of pigmentary abnormalities of the retinal pigment epithelium at baseline was found to be associated with a faster progression rate (P < .001), whereas a significant association with the genotype was not detected (P = .7). Conclusion: In STGD1, both microperimetric outcomes demonstrate statistically significant and clinically meaningful changes after relatively short follow-up periods. Volumetric modeling may be useful in future interventional clinical trials that aim to improve retinal sensitivity or to slow down its decline and for structure-function correlations.
AB - Purpose: To report the yearly rate of change in macular function in patients with Stargardt disease type 1 (STGD1) over 24 months and to establish a new volumetric visual function index for use in clinical trials investigating the efficacy on retinal sensitivity. Methods: Design: International, multicenter, prospective cohort study with 5 study visits every 6 months over 24 months. Participants: A total of 233 individuals with genetically confirmed STGD1 (≥1 disease-causing ABCA4 variant). Main Outcome Measures: The total volume (VTOT) beneath the sensitivity surface of a 3-D model of the hill of vision and mean sensitivity (MS) derived from mesopic microperimetry performed with a white stimulus. Changes of VTOT over time and its correlation with the ABCA4 genotype and baseline features. Results: At baseline, 440 eyes (233 patients) with a mean (SD) age of 33.7 (15.0) years, mean (SD) visual acuity of 46.08 (16.03) ETDRS letters were analyzed with an average VTOT of 0.91 decibel-steradian (dB-sr) and an MS of 10.73 dB. The overall mean rate of decrease in sensitivity [95% confidence interval] was 0.077 [0.064, 0.090] dB-sr/y for VTOT and 0.87 [0.72, 1.02] dB/year for MS. The progression rate of VTOT depended on baseline visual function (0.029 dB-sr/year for low and 0.120 dB-sr/year for high baseline VTOT; P < .001) and exhibited a difference in the first vs second year of follow-up (0.065 dB-sr/year vs 0.089 dB-sr/year, respectively; P < .001). The absence of pigmentary abnormalities of the retinal pigment epithelium at baseline was found to be associated with a faster progression rate (P < .001), whereas a significant association with the genotype was not detected (P = .7). Conclusion: In STGD1, both microperimetric outcomes demonstrate statistically significant and clinically meaningful changes after relatively short follow-up periods. Volumetric modeling may be useful in future interventional clinical trials that aim to improve retinal sensitivity or to slow down its decline and for structure-function correlations.
UR - http://www.scopus.com/inward/record.url?scp=85113781342&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85113781342&partnerID=8YFLogxK
U2 - 10.1016/j.ajo.2021.04.015
DO - 10.1016/j.ajo.2021.04.015
M3 - Article
C2 - 33951446
AN - SCOPUS:85113781342
SN - 0002-9394
VL - 230
SP - 123
EP - 133
JO - American Journal of Ophthalmology
JF - American Journal of Ophthalmology
ER -