West Nile virus (WNV) infection is a worldwide distributed arboviral disease that may cause severe neurologic disease, usually in association with advanced age and diabetes.1–3 Bilateral multifocal chorioretinitis, with typical clinical and angiographic features of chorioretinal lesions and a self-limited disease course, has been recognized as the most common ocular manifestation of WNV infection.1–4 Retinal vascular involvement also has been described including retinal hemorrhages, retinal vascular sheathing, retinal vascular leakage on fluorescein angiography (FA), and, rarely, occlusive retinal vasculitis. Most documented cases of occlusive retinal vasculitis occurred in elderly patients with diabetes mellitus and were associated with severe irreversible visual loss.3,5–9 The presence of occlusive retinal vasculitis can be suspected on clinical examination, but FA is necessary to confirm the diagnosis and assess the extent of retinal capillary nonperfusion.
Optical coherence tomography angiography (OCTA) is a new, noninvasive imaging modality that has already shown to be clinically useful in evaluating foveal microvascular changes in a wide variety of retinal vascular diseases.10–13 We report herein OCTA findings in a patient with WVN chorioretinitis and associated occlusive retinal vasculitis.
A 65-year-old man with diabetes and a history of fever of unknown origin 2 weeks earlier presented with sudden blurring of vision in both eyes. Best-corrected visual acuity (BCVA) was 20/50 in the right eye (OD) and 20/200 in the left eye (OS). Slit-lamp examination showed fine keratic precipitates, 1+ cells in the anterior chamber, and 1+ vitreous haze bilaterally. Intraocular pressure was 10 mm Hg in both eyes. Dilated fundus examination showed in both eyes a few retinal hemorrhages and microaneurysms, as well as multiple deep, round, atrophic chorioretinal lesions in the posterior pole and midperiphery, with some lesions showing central pigmentation (Figures 1A and 1B). There were also patchy areas of ischemic retinal whitening with arteriolar narrowing and sheathing OS (Figure 1B). FA confirmed the presence of bilateral inactive multifocal chorioretinitis with a target-like appearance and linear clustering of chorioretinal lesions (Figures 1C and 1D). The perifoveal capillary arcade appeared to be slightly disrupted OD (Figure 1C). There was a marked disruption of the perifoveal capillary arcade with enlarged and irregular foveal avascular zone and diffuse staining and leakage of perifoveal arterioles and venules OS (Figure 1D). Indocyanine green angiography showed hypofluorescent choroidal spots with more lesions than those appreciated clinically or by FA (Figures 1E and 1F). Fundus autofluorescence showed multiple well-delineated, uniformly hypoautofluorescent or centrally hyperautofluorescent and peripherally hypoautofluorescent spots (Figures 1G and 1H). Spectral-domain optical coherence tomography (SD-OCT) OD showed focal involvement of the outer retina and retinal pigment epithelium corresponding to a focus of chorioretinitis (Figure 1I). There were paracentral focal hyperreflective lesions extending from the inner limiting membrane to the outer plexiform layer OS corresponding to the patchy areas of ischemic retinal whitening seen clinically (Figure 1J). There also were focal alterations of the outer retina.
(A, B) Fundus photography shows mild nonproliferative diabetic retinopathy with a few retinal hemorrhages and microaneurysms in both eyes, as well as bilateral multiple round atrophic chorioretinal lesions, with central pigmentation in some of them (arrowhead). There are patchy areas of ischemic retinal whitening with arteriolar narrowing and sheathing in the left eye (B) (arrows). (C, D) Mid-phase fluorescein angiograms show bilateral inactive multifocal chorioretinitis with a target-like appearance (orange arrowheads) and linear clustering of chorioretinal lesions (orange arrows). The perifoveal capillary arcade appears to be slightly disrupted in the right eye (C). In the left eye, there was a marked disruption of the perifoveal capillary arcade with enlarged and irregular foveal avascular zone and diffuse staining and leakage of perifoveal arterioles and venules (D). (E, F) Late-phase indocyanine green angiograms show hypofluorescent choroidal spots with more lesions than those appreciated clinically or by fluorescein angiography. (G, H) Fundus autofluorescence shows multiple well-delineated, uniformly hypoautofluorescent or centrally hyperautofluorescent and peripherally hypoautofluorescent spots. (I) Spectral-domain optical coherence tomography (OCT) of the right eye showed focal involvement of the outer retina and retinal pigment epithelium corresponding to a focus of chorioretinitis (blue arrow). In the left eye, there are paracentral focal hyperreflective lesions extending from the inner limiting membrane to the outer plexiform layer corresponding to the patchy areas of ischemic retinal whitening seen clinically (green arrows), and focal alterations of the outer retina (pink arrows) (J). Swept-source OCT angiogram of the right eye shows multiple small, hypointense nonperfusion areas (asterisks) and a few microaneurysms (yellow arrows) and telangiectatic vessels involving both the superficial (K) and deep (L) capillary plexuses. OCT angiogram of the left eye shows extensive well-delineated, hypointense nonperfusion areas (asterisks) and perifoveal capillary arcade disruption (white triangles) in the superficial capillary plexus (M) and larger nonperfusion areas (asterisks), capillary rarefaction, and diffuse capillary network attenuation and disorganization in the deep capillary plexus, with a significant degree of projection artifact from the superficial capillary plexus (N).
Swept-source OCT angiogram (DRI OCT Triton plus; Topcon, Tokyo, Japan) OD showed small, hypointense nonperfusion areas and a few microaneurysms and telangiectatic vessels involving both the superficial and deep capillary plexuses (Figures 1K and 1L). OCT angiogram OS showed extensive well-delineated, hypointense nonperfusion areas and perifoveal capillary arcade disruption in the superficial capillary plexus (SCP). In the deep capillary plexus (DCP), there were larger nonperfusion areas of capillary hypoperfusion, capillary rarefaction, and diffuse capillary network attenuation and disorganization, with a marked degree of projection artifact from the SCP (Figures 1M and 1N).
A diagnosis of WNV-associated chorioretinitis with occlusive retinal vasculitis was considered and was confirmed by demonstration of WNV specific immunoglobulin M in a serum sample using the immunoglobulin M antibody-capture enzyme-linked immunoabsorbent assay. Systemic work-up showed that the patient did not have any fluctuations on his glucose level or on his blood pressure measures. The patient was treated with topical corticosteroids.
One month after initial presentation, BCVA remained unchanged OD and had improved to 20/100 OS. The patchy areas of ischemic retinal whitening OS had cleared (Figure 2A), and SD-OCT showed the resolution of hyperreflective lesions, with residual diffuse thinning of the retinal inner and outer plexiform layers, and persistent alterations of the outer retina (Figure 2B). OCTA findings remained unchanged with persistence of hypoperfused areas in both the superficial and deep capillary plexuses.
(A) Fundus photograph of the left eye 1 month after initial presentation shows resolution of retinal whitening. (B) Spectral-domain optical coherence tomography shows complete resolution of the hyperreflective lesions with residual diffuse thinning of the inner and outer plexiform retinal layers, as well as persistent alterations of the outer retina.
To the best of our knowledge, our report is the first to noninvasively evaluate the ability of OCTA to image the microvascular structures in a diabetic patient with bilateral WNV-associated chorioretinitis. Our patient also exhibited clinical and FA findings suggestive of associated occlusive retinal vasculitis OS. Although FA remains the gold standard for assessing occlusive and nonocclusive retinal vasculitis, it is invasive, costly, time-consuming, and has a substantially limited depth-resolution due to light scattering phenomenon. Swept-source OCTA was obviously superior to FA in detecting and analyzing the ischemic retinal capillary changes in our patient with WNV-associated chorioretinitis and occlusive retinal vasculitis. The OCTA evaluation of superficial and deep networks separately allowed us detecting differential involvement of the two layers. There was a marked loss of retinal capillary perfusion in both plexuses, with the DCP more severely involved than the SCP. The distribution and extent of areas of capillary nonperfusion in the superficial and deep capillary plexuses on OCTA appeared to be closely related to the acute ischemic patchy, white retinal areas seen clinically and to focal hyperreflective areas at the inner and middle retinal layers on swept-source SD-OCT.
Follow-up examination OS showed the resolution of acute patchy retinal whitening, persistence of retinal capillary nonperfusion on OCTA, and subsequent development of retinal atrophy on SD-OCT associated with irreversible visual loss.
In this patient with bilateral mild nonproliferative diabetic retinopathy and typical WNV multifocal chorioretinitis, unilateral occlusive retinal vasculitis in the form of arteriolar occlusions more likely resulted from WNV infection than from diabetic retinopathy, although diabetes mellitus might contribute to the development of the occlusive event. Conversely, the retinal capillary changes observed on FA and OCTA in OD appeared to be primarily diabetic in nature, although a contributory role of WNV cannot be excluded.
This case shows that OCTA may be a valuable tool for assessing noninvasively occlusive retinal vasculitis associated with WNV infection. OCTA allows an accurate detection and precise delineation of areas of retinal capillary nonperfusion in both the SCP and DCP. Additional studies with larger number of patients are needed to further improve our understanding of the retinal vascular changes that may occur in patients with WNV infection to clarify the role of OCTA in evaluating chorioretinal disease severity and in assessing predictive factors of visual outcome.
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