Ocular fundus changes and association with systemic conditions in systemic lupus erythematosus

Abstract

Systemic lupus erythematosus (SLE) is an autoimmune disease that affects multiple organs and systems. Ocular involvement is estimated to manifest in one-third of individuals with SLE, of which lupus retinopathy and choroidopathy represent the severe subtype accompanied by vision impairment. Advancements in multimodal ophthalmic imaging have allowed ophthalmologists to reveal subclinical microvascular and structural changes in fundus of patients with SLE without ocular manifestations. Both ocular manifestations and subclinical fundus damage have been shown to correlate with SLE disease activity and, in some patients, even precede other systemic injuries as the first presentation of SLE. Moreover, ocular fundus might serve as a window into the state of systemic vasculitis in patients with SLE. Given the similarities of the anatomy, physiological and pathological processes shared among ocular fundus, and other vital organ damage in SLE, such as kidney and brain, it is assumed that ocular fundus involvement has implications in the diagnosis and evaluation of other systemic impairments. Therefore, evaluating the fundus characteristics of patients with SLE not only contributes to the early diagnosis and intervention of potential vision damage, but also holds considerate significance for the evaluation of SLE vasculitis state and prediction of other systemic injuries.

Keywords: central nervous system; kidney; multimodal imaging; ocular fundus; systemic damage; systemic lupus erythematosus.

Figure 1

Ocular fundus lesions of patients with systemic lupus erythematosus (SLE). (A) Retinal microangiopathy with cotton-wool spots (red arrows) and small flame-shaped hemorrhage (blue arrow). (B) Branch retinal vein occlusion with tortuous and dilated veins, as well as notable hemorrhage. (C) Lupus choroidopathy with serous retinal detachment and subretinal fluid (green arrow). (D) Optic disc edema and obvious hemorrhage.

Figure 2

Multimodal imaging in a patient with lupus retinopathy [(A–F): images were taken at the first presentation; (G, H): images were taken after treatment]. (A) Wide-field image by montage with the traditional fundus camera demonstrated the multiple clustered cotton-wool spots (yellow arrow) and hemorrhage dots (blue circles), as well as white vascular sheathing (white arrow) (Zeiss VISUCAM 500, Carl Zeiss Meditec AG, Jena, Germany). (B) Wide-field fundus fluorescein angiography revealed marked area of capillary non-perfusion and vaso-occlusions, as well as vascular leakage (green arrow) and hyper-fluorescent foci (red circle) (Optos^® California device). (C, D) Optical coherence tomography (OCT) showed the irregular retinal structure and notably edema of the retinal nerve fiber layer (violet arrow). (E) Imaging the ocular fundus with the non-contact ultra-wide-field pseudocolor fundus camera, enabling capturing the retinal images up to 200°C (Optos^® California device). (F) OCT-angiography (OCTA) revealed significant flow void, which corresponds to the area of non-perfusion area. (G) Ultra-wide-field pseudocolor fundus photograph showed the stable condition of ocular fundus after laser photocoagulation (Daytona, Optos PLC, Dunfermline, United Kingdom). (H) OCTA detected the areas of angiogenesis and recanalization (red arrows) 10 months after the first presentation and 6 months after the laser treatment (OCT and OCTA images were taken using VG200, Svision Imaging, Ltd, Luoyang, China).

Figure 3

Measurement of retinal thickness with swept source optical coherence tomography (OCT) and vasculature parameters with OCT-angiography (OCTA) to detect the subclinical changes in a patient with SLE (Images were taken using BM400K BMizar, TowardPi Medical Technology Co., Ltd, Beijing, China). (A, B) Infrared image coupled OCT with automated segmentation of retinal layers [line red: internal limiting membrane (ILM); line orange: retinal nerve fiber layer (RNFL); line yellow: inner nuclear layer; line green: outer nuclear layer; dark red: Bruch’s membrane]. (C) A wide-field OCTA image of retinal superficial capillary plexus from ILM to the inner plexiform layer. (D) Measurements of fovea avascular zone (FAZ) parameters, including area, acircularity, and FAZ vessel density—300 μm. (E) Vessel densities of four quadrants of the parafoveal and perifoveal area. (F) The vessel density map of the wide-field OCTA image. (G) An image of radial peripapillary RNFL capillary plexus. (H) Peripapillary RNFL thickness map. (I) Peripapillary RNFL vessel density map.

Figure 4

The similar pathogenesis among ocular fundus, kidney, and brain damage in SLE. The common pathogenic factors, including immune-complex deposition, endothelial dysfunction, activation of RAAS, secondary hypertension, and existence of antiphospholipid antibodies may contribute to the damage of kidney, ocular fundus, and brain, which have a similar anatomy. SLE, systemic lupus erythematosus; RAAS, renin–angiotensin–aldosterone system; RBC, red blood cell.