Association of Ultra-Widefield Fluorescein Angiography–Identified Retinal Nonperfusion and the Risk of Diabetic Retinopathy Worsening Over Time-Reference-Cited by-同舟云学术

Association of Ultra-Widefield Fluorescein Angiography–Identified Retinal Nonperfusion and the Risk of Diabetic Retinopathy Worsening Over Time

Published:2022-10-01 Issue:10 Volume:140 Page:936
ISSN:2168-6165
Container-title:JAMA Ophthalmology
language:en
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 &lt; .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 &lt; .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)

Subject

Ophthalmology

Link

https://jamanetwork.com/journals/jamaophthalmology/articlepdf/2795372/jamaophthalmology_silva_2022_oi_220047_1668627022.76032.pdf

Reference36 articles.

1. Grading diabetic retinopathy from stereoscopic color fundus photographs—an extension of the modified Airlie House classification: ETDRS report number 10.;Early Treatment Diabetic Retinopathy Study Research Group;Ophthalmology,1991

2. Proposed international clinical diabetic retinopathy and diabetic macular edema disease severity scales.;Wilkinson;Ophthalmology,2003

3. Ultra wide field fluorescein angiography guided targeted retinal photocoagulation (TRP).;Reddy;Semin Ophthalmol,2009

4. Diabetic retinopathy severity and peripheral lesions are associated with nonperfusion on ultrawide field angiography.;Silva;Ophthalmology,2015

5. Patterns of peripheral retinal and central macula ischemia in diabetic retinopathy as evaluated by ultra-widefield fluorescein angiography.;Sim;Am J Ophthalmol,2014

Cited by 18 articles. 订阅此论文施引文献订阅此论文施引文献，注册后可以免费订阅5篇论文的施引文献，订阅后可以查看论文全部施引文献

1. Imaging Modalities for Assessing the Vascular Component of Diabetic Retinal Disease: Review and Consensus for an Updated Staging System;Ophthalmology Science;2024-05

2. Advantages of the Utilization of Wide-Field OCT and Wide-Field OCT Angiography in Clinical Practice;Diagnostics;2024-02-01

3. Correlations between Retinal Microvascular Parameters and Clinical Parameters in Young Patients with Type 1 Diabetes Mellitus: An Optical Coherence Tomography Angiography Study;Diagnostics;2024-02-01

4. Recent Developments in Visualization of the Vasculature in the Living Eye;Reference Module in Neuroscience and Biobehavioral Psychology;2024

5. Association between macrophage-like cell density and ischemia metrics in diabetic eyes;Experimental Eye Research;2023-12