Longitudinal Imaging of Microvascular Remodelling in Proliferative Diabetic Retinopathy Using Adaptive Optics Scanning Light Ophthalmoscopy

Overview

Journal Ophthalmic Physiol Opt

Date 2016 Jan 25

PMID 26803289

Citations 22

Authors

Toco Yuen Ping Chui

Alexander Pinhas

Alexander Gan

Moataz Razeen

Nishit Shah

Eric Cheang

Chun L Liu

Alfredo Dubra

Richard B Rosen

Affiliations

Soon will be listed here.

Abstract

Purpose: To characterise longitudinal changes in the retinal microvasculature of type 2 diabetes mellitus (T2DM) as exemplified in a patient with proliferative diabetic retinopathy (PDR) using an adaptive optics scanning light ophthalmoscope (AOSLO).

Methods: A 35-year-old T2DM patient with PDR treated with scatter pan-retinal photocoagulation at the inferior retina 1 day prior to initial AOSLO imaging along with a 24-year-old healthy control were imaged in this study. AOSLO vascular structural and perfusion maps were acquired at four visits over a 20-week period. Capillary diameter and microaneurysm area changes were measured on the AOSLO structural maps. Imaging repeatability was established using longitudinal imaging of microvasculature in the healthy control.

Results: Capillary occlusion and recanalisation, capillary dilatation, resolution of local retinal haemorrhage, capillary hairpin formation, capillary bend formation, microaneurysm formation, progression and regression were documented over time in a region 2° superior to the fovea in the PDR patient. An identical microvascular network with same capillary diameter was observed in the control subject over time.

Conclusions: High-resolution serial AOSLO imaging enables in vivo observation of vasculopathic changes seen in diabetes mellitus. The implications of this methodology are significant, providing the opportunity for studying the dynamics of the pathological process, as well as the possibility of identifying highly sensitive and non-invasive biomarkers of end organ damage and response to treatment.

Citing Articles

Measurement of retinal blood flow precision in the human eye with multimodal adaptive optics imaging.

Raghavendra A, Damani A, Oechsli S, Magder L, Liu Z, Hammer D Biomed Opt Express. 2024; 15(8):4625-4641.

PMID: 39346998 PMC: 11427214. DOI: 10.1364/BOE.524944.

Detection of capillary abnormalities in early diabetic retinopathy using scanning laser ophthalmoscopy and optical coherence tomography combined with adaptive optics.

Torm M, Pircher M, Bonnin S, Johannesen J, Klefter O, Schmidt M Sci Rep. 2024; 14(1):13450.

PMID: 38862584 PMC: 11166634. DOI: 10.1038/s41598-024-63749-7.

Twenty-five years of clinical applications using adaptive optics ophthalmoscopy [Invited].

Morgan J, Chui T, Grieve K Biomed Opt Express. 2023; 14(1):387-428.

PMID: 36698659 PMC: 9841996. DOI: 10.1364/BOE.472274.

Progress of Imaging in Diabetic Retinopathy-From the Past to the Present.

Horie S, Ohno-Matsui K Diagnostics (Basel). 2022; 12(7).

PMID: 35885588 PMC: 9319818. DOI: 10.3390/diagnostics12071684.

Differentiating Microaneurysm Pathophysiology in Diabetic Retinopathy Through Objective Analysis of Capillary Nonperfusion, Inflammation, and Pericytes.

An D, Tan B, Yu D, Balaratnasingam C Diabetes. 2022; 71(4):733-746.

PMID: 35043147 PMC: 9375447. DOI: 10.2337/db21-0737.

References

Kempen J, OColmain B, Leske M, Haffner S, Klein R, Moss S . The prevalence of diabetic retinopathy among adults in the United States. Arch Ophthalmol. 2004; 122(4):552-63. DOI: 10.1001/archopht.122.4.552. View

Forouzan O, Yang X, Sosa J, Burns J, Shevkoplyas S . Spontaneous oscillations of capillary blood flow in artificial microvascular networks. Microvasc Res. 2012; 84(2):123-32. DOI: 10.1016/j.mvr.2012.06.006. View

Scholfield C, McGeown J, Curtis T . Cellular physiology of retinal and choroidal arteriolar smooth muscle cells. Microcirculation. 2007; 14(1):11-24. DOI: 10.1080/10739680601072115. View

Burns S, Elsner A, Chui T, Vannasdale Jr D, Clark C, Gast T . In vivo adaptive optics microvascular imaging in diabetic patients without clinically severe diabetic retinopathy. Biomed Opt Express. 2014; 5(3):961-74. PMC: 3959854. DOI: 10.1364/BOE.5.000961. View

Chui T, Dubow M, Pinhas A, Shah N, Gan A, Weitz R . Comparison of adaptive optics scanning light ophthalmoscopic fluorescein angiography and offset pinhole imaging. Biomed Opt Express. 2014; 5(4):1173-89. PMC: 3985984. DOI: 10.1364/BOE.5.001173. View

Dubra A, Sulai Y . Reflective afocal broadband adaptive optics scanning ophthalmoscope. Biomed Opt Express. 2011; 2(6):1757-68. PMC: 3114240. DOI: 10.1364/BOE.2.001757. View

Bernardes R, Nunes S, Pereira I, Torrent T, Rosa A, Coelho D . Computer-assisted microaneurysm turnover in the early stages of diabetic retinopathy. Ophthalmologica. 2009; 223(5):284-91. DOI: 10.1159/000213638. View

Yu T, Mitchell P, Berry G, Li W, Wang J . Retinopathy in older persons without diabetes and its relationship to hypertension. Arch Ophthalmol. 1998; 116(1):83-9. DOI: 10.1001/archopht.116.1.83. View

Chui T, VanNasdale D, Burns S . The use of forward scatter to improve retinal vascular imaging with an adaptive optics scanning laser ophthalmoscope. Biomed Opt Express. 2012; 3(10):2537-49. PMC: 3470005. DOI: 10.1364/BOE.3.002537. View

10.

Joussen A, Poulaki V, Le M, Koizumi K, Esser C, Janicki H . A central role for inflammation in the pathogenesis of diabetic retinopathy. FASEB J. 2004; 18(12):1450-2. DOI: 10.1096/fj.03-1476fje. View

11.

Kohner E, Porta M . Vascular abnormalities in diabetes and their treatment. Trans Ophthalmol Soc U K (1962). 1980; 100(3):440-4. View

12.

Chen S, Chou P, Lee A, Lee F, Hsu W, Liu J . Microaneurysm number and distribution in the macula of Chinese type 2 diabetics with early diabetic retinopathy: a population-based study in Kinmen, Taiwan. Acta Diabetol. 2009; 47(1):35-41. DOI: 10.1007/s00592-009-0095-6. View

13.

Wong T, Klein R, Sharrett A, Couper D, Klein B, Hubbard L . Cerebral white matter lesions, retinopathy, and incident clinical stroke. JAMA. 2002; 288(1):67-74. DOI: 10.1001/jama.288.1.67. View

14.

Snodderly D, Weinhaus R, Choi J . Neural-vascular relationships in central retina of macaque monkeys (Macaca fascicularis). J Neurosci. 1992; 12(4):1169-93. PMC: 6575794. View

15.

Li W, YANOFF M, Liu X, Ye X . Retinal capillary pericyte apoptosis in early human diabetic retinopathy. Chin Med J (Engl). 1998; 110(9):659-63. View

16.

Kohner E, Stratton I, Aldington S, Turner R, Matthews D . Microaneurysms in the development of diabetic retinopathy (UKPDS 42). UK Prospective Diabetes Study Group. Diabetologia. 1999; 42(9):1107-12. DOI: 10.1007/s001250051278. View

17.

Weinhaus R, Burke J, Delori F, Snodderly D . Comparison of fluorescein angiography with microvascular anatomy of macaque retinas. Exp Eye Res. 1995; 61(1):1-16. DOI: 10.1016/s0014-4835(95)80053-0. View

18.

Chui T, Gast T, Burns S . Imaging of vascular wall fine structure in the human retina using adaptive optics scanning laser ophthalmoscopy. Invest Ophthalmol Vis Sci. 2013; 54(10):7115-24. PMC: 3813321. DOI: 10.1167/iovs.13-13027. View

19.

Sulai Y, Scoles D, Harvey Z, Dubra A . Visualization of retinal vascular structure and perfusion with a nonconfocal adaptive optics scanning light ophthalmoscope. J Opt Soc Am A Opt Image Sci Vis. 2014; 31(3):569-79. PMC: 4465430. DOI: 10.1364/JOSAA.31.000569. View

20.

Chui T, VanNasdale D, Elsner A, Burns S . The association between the foveal avascular zone and retinal thickness. Invest Ophthalmol Vis Sci. 2014; 55(10):6870-7. PMC: 4214206. DOI: 10.1167/iovs.14-15446. View