Association of Ultra-Widefield Fluorescein Angiography–Identified Retinal Nonperfusion and the Risk of Diabetic Retinopathy Worsening Over Time
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Published:2022-10-01
Issue:10
Volume:140
Page:936
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ISSN:2168-6165
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Container-title:JAMA Ophthalmology
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language:en
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Short-container-title:JAMA Ophthalmol
Author:
Silva Paolo S.12, Marcus Dennis M.34, Liu Danni5, Aiello Lloyd Paul12, Antoszyk Andrew6, Elman Michael7, Friedman Scott8, Glassman Adam R.5, Googe Joseph M.9, Jampol Lee Merrill10, Martin Daniel F.11, Melia Michele5, Preston Carin M.5, Wykoff Charles C.12, Sun Jennifer K.12, Harara Abla M13, Palacios Angela N.13, Berger Brian B.13, Corak Boris13, Luong Bianca13, Jhaveri Chirag D.13, Wilson Daniela Mariel13, Jonna Gowtham13, Gunderson Ivana13, Hosein Kimberly13, Reid Ryan M.13, Chexal Saradha13, Moore Tori13, Seidu Tina A13, Gatavaski Valerie13, Ren Yong13, Stern Bradley A.13, Benvenutti Celia E13, Oude-Reimerink Dinah S13, Shaheen Jenny13, Grybas John13, Vitale-Kuhn Julianne13, Staffne Jessica L.13, Ventimiglia Katie M.13, Allis Megan13, Monk Mary K.13, Thomas Marc E.13, Massu Nicole M.13, Edwards Paul Andrew13, Troszak Tracy A.13, Irons Amber N13, Rego Brittany13, Han Dennis P.13, Dorsey Eleanor13, Nelson Erika13, Sheppard Hannah13, Beringer Joseph R.13, Kim Judy E.13, Keller Kristy L.13, Packard Krissa L.13, Altmann Marriner L.13, Goldberg Mara13, Chen Nickolas13, Winter Pat A.13, Bourgeois Shay13, Jacobo Samantha13, Moebius Stephanie J13, Connor Thomas B.13, Barwick Vicki13, Williams Vesper V.13, Wirostko William J.13, Ghuman A. Thomas13, Leslie Anita H.13, Sharma Ashish G.13, Kiesel Cheryl13, Dyshanowitz Danielle13, Knips Eileen13, Wing Glenn13, Walker Joseph P.13, Raskauskas Paul A.13, Kiesel Raymond K.13, Schlossman Deborah K.13, Weimann Elizabeth S.13, Sharuk George S.13, Kwak Hanna13, Cavallerano Jerry D.13, Rhee Jae W13, Sampani Konstantina13, Tran Katie V13, Bestourous Leila13, Miranda Linette13, Krigman Michael N.13, Stockman Margaret E.13, Arrigg Paul G.13, Cavicchi Robert W.13, Kirby Rita K.13, Glynn Shireen13, Papaconstantinou Steve L.13, Shah Sabera T.13, Murtha Timothy J.13, Carli William13, Finch Autumn K.13, Gentile Angella K.13, Price Angela K.13, Murphy Brittany A13, Rowland Beverly O13, Fleming Christina J.13, Mahr Courtney13, Shore Carol A13, Browning David13, McClain Donna13, Breglio Erica13, Lester Gina M.13, Herby Jenna T.13, Bratcher Kayla A13, Clark Loraine M.13, Jackson Lisa A.13, Watson Lynn13, McOwen Michael D.13, Punjabi Omar S.13, Bojaj Swann J13, Ennis Sarah A.13, Fredenberg Sherry L.13, Jones Taylor S.13, Ragin Teneisha A.13, Balasubramaniam Uma M.13, Ornelas Blanca13, Rodriquez Brenda13, Edwards Carla13, Carns Danielle R.13, Tonner Eileen E.13, Woo Kisung13, Richine Len13, MacCumber Mathew W.13, Merrill Pauline Townsend13, Kociborski Sarah13, Harless Ashley M.13, Harris Charlotte13, White Lorraine13, Maturi Raj K.13, Asher Julie13, Walsh Justin13, Wheeler Jeff13, Milstead Katie13, Oliver Kristina13, Lovelady Lisa13, Anderson Nicholas G.13, Coppola Patricia13, Lince Raul E.13, Shuler R. Keith13, Morris Steve13, Oelrich Sarah M.13, Gardner Brandon S13, Moore Bob13, Cain Dennis13, Donohue Deborah13, Emmert David13, Adeyemo Kemi13, Levin Lisa K.13, Frey Mary13, Rhoton Nick13, Bressler Susan13, Solomon Sharon D.13, Ford Amy L13, Hughes Ashley13, Brewer Alisha N13, Booth JoAnn T13, Lunsford Keven W13, Ukleya Lauren D.13, Burris Russ13, Kingsley Ronald M.13, Almeida Shannon R.13, Icks Sonny13, Shah Vinay A.13, Bergman Vanessa A.13, Castellarin Alessandro A.13, Shook Aimee H.13, Walker Aimee13, Pieramici Dante J.13, Hong Gina13, Avery Kelly13, McKee Kate M13, Giust Matthew13, Munoz Marco A13, Fishbein Sarah13, Camp Alecia B.13, Baker Carl W.13, Baker Jil D13, Sedberry Kylie S.13, Lambert Lynnette F.13, Orr Margaret J.13, Alcaraz Sonya L13, Kettler Samantha13, Caldwell Tracey M.13, Miller Abigail13, Dorr Christine M.13, Hampton G. Robert13, Brown Jamin S.13, Barker Jeffrey P13, Rosenberg Kevin I.13, Kwasniewski Lynn M.13, Sienkiewycz Laurie J.13, Spuches Lisa13, Manley Michelle L.13, Robarge Nicole E.13, DeSantis Stefanie R.13, DeForge Teresa M.13, Brucker Alexander J.13, Kim Benjamin J.13, Berger Jim M.13, DuPont Joan C.13, Drossner Sheri13, Freeman Sara13, Studebaker Ashley13, Payne John F.13, Wells John A.13, Spivey Robbin13, Ogbuewu Tiffany N.13, Swinford Tiffany R.13, Guillory Adrienne13, Hutson Amy13, Schefler Amy C.13, Shah Ankoor R.13, Almanza Belinda A.13, Dives Brenda13, Richter Beau A13, Stoever Cary A.13, Brown David M.13, Foerster Danee13, Garcia David13, Rodriguez Diana13, Park Daniel13, Chen Eric13, Kegley Eric N.13, Quellar Elizabeth13, Twining Garret L13, Koger-Grifaldo Heather13, Ortega Ilsa13, Carranza Jolene13, Major James C.13, Williamson Kimberly13, Burt Lindsay13, Salinas Luis R.13, Wolff Lisa M13, Benz Matthew S.13, Estes Maura A13, James Miranda F13, Berry Meredith13, Vela Melina13, Landaverde Nubia13, Webb Nina A.13, Fish Richard H.13, Kim Rosa Y.13, Yee Rebecca13, Karani Sadia Y13, Supapo Stacy M.13, Dodel Tamara L13, McCoy Tyneisha13, Wong Tien P.13, Sneed Veronica A.13, Barnhart Cassandra J.13, Cantrell Debra13, DuBose Elizabeth L.13, Sharpe Houston P13, Ulrich Jan Niklas13, Bhansali Kanika A13, Esquejo Rona Lyn13, Garg Seema13, Grout Sean13, McKinney Allen13, Bobbitt Brenda J.13, Wendel Ceara L13, Fagan Damanda F.13, Andrews Jacqueline13, Holmes Krystal Nikki13, Seyez Karen L13, Williamson Kimberly A.13, Moinfar Nader13, Walters Paige N.13, Carlton Steve13, Rehling Shannon M13, Williams Shana E13, Reed Tiara L.13, VandeVelde Amber R13, Yeager Frank T.13, Fox Gregory M.13, Batlle Ivan R.13, Bruce Kiersten13, Pippin Katherine13, Ainley Lexie R.13, Singh Ravi S. J.13, Adamo Ashley M13, Guardado Adrian13, Patel Apurva K.13, Puckett Brian S13, Hoerner Christine13, Ma Colin13, Clark David J13, Flato Inessa M13, Cohen Joshua13, Charpentier Margaret E13, Kopfer Marcia13, Peters Mark A.13, Smith Pualani13, Tlucek Paul S.13, Hobbs Stephen13, Ho Stephanie L.13, Metzger Ashley M.13, McCalla Alesia K13, Thompson Amy13, Ringrose Christine13, Sandler Dallas R.13, Leder Henry A.13, Belz Jennifer L.13, Starr JoAnn13, Simmons Jennifer L.13, Orr Peggy R13, Sotirakos Peter13, Singletary Pamela V.13, Cain Terri13, Coffey Teresa13, Carter Tiffany M13, Robinson Twyla J13, Shah Chirag P.13, Cammarata Dominique13, Kruger Jennifer L.13, Colegrove Lindsey13, Graham Margie13, Gleason Shane T.13, Noel Bryan13, Damron Catherine13, Holcomb Diana M.13, Slade Edward A13, Van Arsdall Jeanne13, Bicknell Lisa13, Buck Michelle13, Stone Thomas W.13, Farooq Amina13, Parsons Brook13, Singh Harinderjit13, Ivey Ken13, Foster Lindsay Allison13, Woodward Michele13, Ortiz Siobhan O.13, Bailey Thomas13, Mynampati A Bharani Krishna13, White Cheryl L13, Hamdani Ghulam Shabbir13, Smith Jazzmin N13, Chalam Kakarla V.13, Sambhav Kumar13, Babaria Romesh13, Grover Sandeep13, Carroll Catherine13, Chau Felix Y.13, Lim Jennifer I.13, Talasnik Lauren A13, Janowicz Mark13, Stankovic Natasa13, Berlatsky Sarah L13, Niec Marcia13, Sun Jie13, Johnson Tametha13, Ovando Yesenia13, Nakoski Brenda13, Mein Calvin E.13, Wienecke Christopher Sean13, Castillo Elaine13, Baker Jaynee13, San Roman Jonathan13, Adams Lydia13, Kirschbaum Lita13, Chica Moises A.13, Cloudt Sara L13, Moore Tori R.13, Sabates Felix N.13, Gallimore Gary S.13, Chen Yin C.13, Swann Adrienne C13, Cadwell Deborah M.13, Diddie Kenneth R.13, Boisvert Taryn F.13, Tessau Carrie D13, Bowers Jack13, Nielsen Jared S.13, Rostvold Jay13, Spillman Jamie13, Alliman Kyle J.13, Boender Lisa M.13, Johnson Marilyn A.13, Parker Marianne13, Bix Paula L13, Ridgway Spencer D13, Woehl Tami Jo13, Stonewall Whitney13, Brown Christopher M.13, Lema Gareth M.C.13, Wiechelt Luann13, Yoganathan Pradeepa13, Boglione Sandra L.13, Montesclaros Chris A.13, Mangham Cory13, Karsaliya Gopal13, Le Phillip V.13, Wong Robert W.13, Godfrey Anne Marie13, Kuzmanovic Aleksandra13, Kirker Andrew William13, Harrison Bryan13, Forooghian Farzin13, Elvena Garnet Louise13, Hall Laura J.13, Turhal Bilgin13, Brown Ian13, Kotei Isaac A13, Chen Lina13, Brent Michael Henry13, Moon Michelle13, Sutakovic Olivera13, Chang Angela13, Godfrey Anne-Marie13, Albiani David13, Maberley David A.L.13, Navajas Eduardo Vitor13, Grant Kelly13, Tran Khoi A13, Jovanovic Mira13, Cao Sijia13, Wiens Theresa13, Kozbial Andrzej13, Orlin Anton13, Lenane Courtney Nichole13, Herder Susan P.13, Kiss Szilard13, Reeves Tom13, Cruess Alan F.13, Dean Andrea13, Hoskin-Mott Ann13, Morrison Christine13, Caldwell Meggie D13, Hynes Mitzi13, Gupta R. Rishi13, Durling Stacey13, MacDonnell Trina13, Beck Roy W.13, Baptista Alyssa13, Beaulieu Wesley T.13, Calhoun Claire T.13, Constantine Sharon R.13, Correia Isabella13, Dale Brian B.13, Dupre Simone S.13, Franklin Crystal A.13, Galusic Sandra13, Huggins Meagan13, Hunter Brenda L.13, Johnson Paula A.13, Josic Kristin13, Kelly Brittany13, Maguire Maureen G.13, Meadows Britney13, Stockdale Cynthia R.13, Zokruah Alice13, Bhargava Sangeeta13, Barkmeier Andrew J.13, Baskin Darrell13, Blodi Barbra13, Chew Emily13, Ferris Frederick L.13, Jaffe Glenn J.13, Bressler Neil M.13, Lujan Brandon13, Tolls Dorothy13, Sheridan Daniel13, Pitoc Cloyd M13, Aquino Lizzie Anne C13, Salva Claude Michael G.13, Lewis Drew13, Stainback Jeffery13, Makkena Vijaya13, Winter Katrina13, Mora Adiel13, Harrington Chris13, Vinh Doc-Lap13,
Affiliation:
1. Joslin Diabetes Center, Beetham Eye Institute, Boston, Massachusetts 2. Harvard Department of Ophthalmology, Boston, Massachusetts 3. Southeast Retina Center, Augusta, Georgia 4. Medical College of Georgia, Augusta University, Augusta 5. Jaeb Center for Health Research, Tampa, Florida 6. Charlotte Eye Ear Nose and Throat Associates, Charlotte, North Carolina 7. Elman Retina Group, Baltimore, Maryland 8. Florida Retina Consultants, Lakeland 9. Southeastern Retina Associates, Knoxville, Tennessee 10. Feinberg School of Medicine, Northwestern University, Chicago, Illinois 11. Cole Eye Institute, Cleveland Clinic, Cleveland, Ohio 12. Retina Consultants of Texas, Houston 13. for the DRCR Retina Network
Abstract
ImportancePresence of predominantly peripheral diabetic retinopathy (DR) lesions on ultra-widefield fluorescein angiography (UWF-FA) was associated with greater risk of DR worsening or treatment over 4 years. Whether baseline retinal nonperfusion assessment is additionally predictive of DR disease worsening is unclear.ObjectiveTo assess whether the extent and location of retinal nonperfusion identified on UWF-FA are associated with worsening in Diabetic Retinopathy Severity Scale (DRSS) score or DR treatment over time.Design, Setting, and ParticipantsThis cohort study was a prospective, multicenter, longitudinal observational study with data for 508 eyes with nonproliferative DR and gradable nonperfusion on UWF-FA at baseline. All images were graded at a centralized reading center; 200° ultra-widefield (UWF) color images were graded for DR at baseline and annually for 4 years. Baseline 200° UWF-FA images were graded for nonperfused area, nonperfusion index (NPI), and presence of predominantly peripheral lesions on UWF-FA (FA PPL).InterventionsTreatment of DR or diabetic macular edema was at investigator discretion.Main Outcomes and MeasuresAssociation of baseline UWF-FA nonperfusion extent with disease worsening, defined as either 2 or more steps of DRSS worsening within Early Treatment Diabetic Retinopathy Study fields on UWF-color images or receipt of DR treatment.ResultsAfter adjusting for baseline DRSS, the risk of disease worsening over 4 years was higher in eyes with greater overall NPI (hazard ratio [HR] for 0.1-unit increase, 1.11; 95% CI, 1.02-1.21; P = .02) and NPI within the posterior pole (HR for 0.1-unit increase, 1.35; 95% CI, 1.17-1.56; P < .001) and midperiphery (HR for 0.1-unit increase, 1.08; 95% CI, 1.00-1.16; P = .04). In a multivariable analysis adjusting for baseline DRSS score and baseline systemic risk factors, greater NPI (HR, 1.11; 95% CI, 1.02-1.22; P = .02) and presence of FA PPL (HR, 1.89; 95% CI, 1.35-2.65; P < .001) remained associated with disease worsening.Conclusions and RelevanceThis 4-year longitudinal study has demonstrated that both greater baseline retinal nonperfusion and FA PPL on UWF-FA are associated with higher risk of disease worsening, even after adjusting for baseline DRSS score and known systemic risk. These associations between disease worsening and retinal nonperfusion and FA PPL support the increased use of UWF-FA to complement color fundus photography in future efforts for DR prognosis, clinical care, and research.
Publisher
American Medical Association (AMA)
Cited by
18 articles.
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