Detection of Choroidal Hypoperfusion in Giant Cell Arteritis Using Swept-Source Optical Coherence Tomographic Angiography

Clinical Correspondence Section Editors: Robert Avery, DO Karl C. Golnik, MD Caroline Froment, MD, PhD An-Guor Wang, MD Detection of Choroidal Hypoperfusion in Giant Cell Arteritis Using Swept-Source Optical Coherence Tomographic Angiography Edward S. Lu, BA, Amy Yuan, MD, Devon A. Cohen, MD, Raviv Katz, BS, John B. Miller, MD, Eric D. Gaier, MD, PhD G iant cell arteritis (GCA) is an immune-mediated vasculitis of medium-sized to large-sized arteries that predominantly affects adults older than 50 years with high morbidity and mortality if untreated. Giant cell arteritis affects the short posterior ciliary arteries supplying the prelaminar and laminar portions of the optic nerve head, resulting in acute vision loss and pallid nerve edema characteristic of arteritic anterior ischemic optic neuropathy (1). Other hallmark symptoms of GCA include headache, myalgias, fatigue, fever, weight loss, or jaw claudication. Fluorescein angiography (FA) classically demonstrates delayed or incomplete choroidal filling in the acute phase of GCA (2). Optical coherence tomography angiography (OCTA), a noninvasive tool for imaging of laminar blood flow, provides high-resolution, three-dimensional segmentation of the chorioretinal microvasculature into the superficial capillary plexus (SCP), deep capillary plexus (DCP), and choriocapillaris (CC) (3). Although FA has historically been the standard imaging modality for chorioretinal vascular Department of Ophthalmology (ESL, DAC, RK, JBM, EDG), Massachusetts Eye and Ear Infirmary, Boston, Massachusetts; Department of Ophthalmology (ESL, DAC, RK, JBM, EDG), Harvard Medical School, Boston, Massachusetts; Harvard Retinal Imaging Lab (ESL, RK, JBM), Boston, Massachusetts; Department of Ophthalmology (AY), University of Washington School of Medicine, Seattle, Washington; Department of Ophthalmology (EDG), Boston Children’s Hospital, Boston, Massachusetts; Picower Institute for Learning and Memory (EDG), Massachusetts Institute of Technology, Cambridge, Massachusetts. J. B. Miller: Lions Clubs International Foundation grant 530 125. E. D. Gaier: NIH K08 EY030164, Children’s Hospital Ophthalmology Foundation. The sponsor or funding organization had no role in the design or conduct of this research. J. B. Miller: Alcon, Zeiss, Sunovion, Allergan, and Genentech. E. D. Gaier: Luminopia, Inc (scientific advisor, equity, and patent) and Stoke Therapeutics, Inc (consultant). The remaining authors report no conflicts of interest. Posted history: This manuscript was previously posted to MedRxiv: https://doi.org/10.1101/2021.05.21.21257605. Off-label use: Triton, Topcon, Tokyo, Japan; off-label use under an IRB-approved protocol. Address correspondence to Eric D. Gaier, MD, PhD, Pediatric NeuroOphthalmology Service, Harvard Medical School, Boston Children’s Hospital, 300 Longwood Avenue, Boston, MA 02115; E-mail: eric. [e-mail] Lu et al: J Neuro-Ophthalmol 2023; 43: e117-e119 pathology, OCTA is a promising alternative to dye-based angiography. A woman in her late 70s with a history of rheumatoid arthritis presented with sudden vision loss in the right eye 1 day before, with jaw claudication, headache, scalp tenderness, and weight loss. On examination, visual acuities were counting fingers in the right eye and 20/30 in the left eye. There was a brisk relative afferent pupillary defect in the right eye and a dense inferior arcuate defect in the left eye on visual field testing (Fig. 1F; inset). Funduscopic examination revealed pallid optic disc edema that was circumferential in the right eye and most prominent superonasally in the left eye (Fig. 1A, F). Inflammatory markers and platelets (PLT) were elevated (ESR 119 mm/hour, C-reactive protein [CRP] 75 mg/L, and PLT 748 K/mL). Right temporal artery biopsy was positive for GCA. Fluorescein angiography demonstrated a large, sharply demarcated area of choroidal filling delay involving the temporal fundus in the right eye (Fig. 1B). The left eye also demonstrated a large, sharply demarcated area of delayed choroidal perfusion centrally that extended inferiorly and temporally (Fig. 1G). Late frames showed full eventual choroidal filling in these areas and leakage at the optic nerve head in both eyes (not shown). SCP and DCP segmentation of en face swept-source (SS)-OCTA images demonstrated reduced angiographic signal in the perfusion beds of small cilioretinal arteries (Fig. 1C, H, I; green arrows). There was a reduction in the SCP density temporally in the right eye, potentially signifying an early consequence of ganglion cell layer and retinal nerve fiber layer atrophy. Notably, segmentation of the CC demonstrated decreased perfusion in the same distribution as the choroidal filling delay observed on FA (Fig. 1E, J). The patient was treated with intravenous methylprednisolone and transitioned to an oral prednisone taper. Follow-up examination 6 months later revealed visual acuities of no light perception in the right eye and improvement to 20/25 in the left eye with stable visual field defects. For comparison, we present 1 patient without visual symptoms, and biopsy-proven GCA who was imaged with SS-OCTA as a control (Fig. 2). The patient was a e117 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Clinical Correspondence FIG. 1. A woman in her 70s with GCA causing sudden vision loss in the right eye. Fundus images of the right (A) and left (F) eyes. Automated perimetry (30-2) of the left eye (F; inset). FA images taken in the midphase (1:21) and early phase (0:25) for the right (B) and left (G) eyes, respectively. En face SS-OCTA 6 · 6-mm images with laminar segmentation of the superficial capillary plexus (C, H), deep capillary plexus (D, I), and choriocapillaris (E, J) for the right and left eyes, respectively (Triton, Topcon, Tokyo, Japan; off-label use under an IRB-approved protocol). Insets depict B-scan images through the fovea with segmented area highlighted in blue. Red arrows outline matching boundaries of perfusion/nonperfusion on FA and SS-OCTA. Green arrows indicate decreased angiographic signal in the perfusion beds of small cilioretinal arteries. FA, fluorescein angiography; GCA, giant cell arteritis; SS-OCTA, swept-source optical coherence tomographic angiography. woman in her 70s referred by her neurologist to evaluate for ophthalmic signs suggestive of GCA in the setting of elevated inflammatory markers (ESR 65 mm/hour and CRP 111 mg/L), jaw claudication (confounded by active dental disease), weight loss, and headaches with scalp tenderness. The patient denied visual changes. FA was obtained given her atypical clinical presentation, and no choroidal filling defects were found. Subsequent right temporal artery biopsy was positive, and the patient was treated with corticosteroids. Choroidal filling delay demonstrated by IV dye-based angiography is a highly suggestive finding of GCA in the right clinical context due to hypoperfusion of the posterior ciliary arteries (2). As such, FA serves as a useful ancillary tool in the evaluation of GCA, particularly in mild cases. Optical coherence tomography angiography has the potential to serve as a practical alternative to FA. FA testing has several limitations, including the need for a licensed practitioner to place an IV and administer fluorescein, the longer time required to complete the test, adverse reactions to fluorescein dye, and the inability to repeat FA testing in the event of poor image quality until the dye is excreted. On the other hand, OCTA is fast, easy to capture, and noninvasive (3). Thus, OCTA may enable more expedient assessment of choroidal perfusion than dye-based angiography to facilitate the diagnosis and treatment of GCA in select cases. e118 We previously reported 4 GCA cases in which spectraldomain (SD)-OCTA demonstrated superficial peripapillary dilation and retinal capillary perfusion defects that corresponded to visual field loss in the acute phase (4). Two patients in the series had choroidal perfusion abnormalities evident on FA, yet SD-OCTA analysis of the choroid and CC (performed on the same day as FA) showed no signal abnormality in those corresponding regions. This case suggests SS-OCTA may offer improved resolution of deeper retinal and choroidal vessels as compared with SD-OCTA and thus might be better suited to capture alterations in choroidal perfusion. Tran et al (5) reported the first definitive case of choroidal hypoperfusion secondary to GCA imaged using SS-OCTA to offer a direct comparison with FA and indocyanine green angiography. The case depicted a large Amalric choroidal infarct similar to the right eye in this case (Fig. 1A–E). Notably, Tran et al used a different SS-OCTA device (Plex-Elite 9000; Carl Zeiss Meditec, Dublin, CA) than the one used in our study and allowed for direct OCTA imaging of the full choroid. Although their findings are similar to our findings, there are likely to be differences between SS-OCTA devices that influence sensitivity in detecting subretinal perfusion abnormalities. This case demonstrates comparability between SSOCTA and FA in detecting choroidal ischemia in GCA. There are many advantages of SS-OCTA over FA, including ease and expedience of obtaining imaging in the acute setting that is highly relevant in clinical scenarios of Lu et al: J Neuro-Ophthalmol 2023; 43: e117-e119 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Clinical Correspondence FIG. 2. SS-OCTA images from a GCA-positive, control patient in her 70s without ocular involvement. Fundus images of the right (A) and left (F) eyes. Fluorescein angiography (FA) images taken in the early phase (0:17) and midphase (0:46) for the right (B) and left (G) eyes, respectively. En face SS-OCTA 6 · 6-mm images with laminar segmentation of the superficial capillary plexus (C, H), deep capillary plexus (D, I), and choriocapillaris (E, J) for the right and left eyes, respectively. Horizontal lines on SS-OCTA images are due to motion artifact. GCA, giant cell arteritis. SS-OCTA, Swept-source optical coherence tomography angiography. suspected GCA. Further study evaluating SS-OCTA as a diagnostic tool in screening for choroidal perfusion abnormalities in suspected GCA cases would be of great value. REFERENCES 1. Hayreh SS. Anterior ischaemic optic neuropathy. II. Fundus on ophthalmoscopy and fluorescein angiography. Br J Ophthalmol. 1974;58:964–980. 2. Siatkowski RM, Gass JD, Glaser JS, Smith JL, Schatz NJ, Schiffman J. Fluorescein angiography in the diagnosis of giant cell arteritis. Am J Ophthalmol. 1993;115:57–63. Lu et al: J Neuro-Ophthalmol 2023; 43: e117-e119 3. Spaide RF, Fujimoto JG, Waheed NK, Sadda SR, Staurenghi G. Optical coherence tomography angiography. Prog Retin Eye Res. 2018;64:1–55. 4. Gaier ED, Gilbert AL, Cestari DM, Miller JB. Optical coherence tomographic angiography identifies peripapillary microvascular dilation and focal non-perfusion in giant cell arteritis. Br J Ophthalmol. 2018;102:1141–1146. 5. Tran AQ, Yannuzzi NA, Motulsky EH, Zhou XY, Galor A, Dubovy SR, Rosenfeld PJ, Lam BL. Swept-source optical coherence tomography angiography of an amalric choroidal infarction in a rare presentation of giant cell arteritis with bilateral corneal edema. Ophthalmic Surg Lasers Imaging Retina. 2018;49:e157–e160. e119 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited.