- Brief report
- Open Access
Wide-field fluorescein and indocyanine green angiography findings in the eyes with Vogt-Koyanagi-Harada disease
© The Author(s). 2017
Received: 16 May 2017
Accepted: 5 July 2017
Published: 11 July 2017
The purpose of this study is to report wide-field angiography findings before and after steroid therapy in a case with bilateral Vogt-Koyanagi-Harada (VKH) disease.
A 44-year-old woman presented with bilateral blurred vision and metamorphopsia accompanied by symptoms of headache and tinnitus. The baseline best-corrected visual acuity was 20/20 in both eyes. Ophthalmic examination revealed a shallow anterior chamber and panuveitis accompanied by multiple serous retinal detachments in both eyes and ciliochoroidal detachments in the left eye. Wide-field fluorescein angiograms showed hyperfluorescene indicating pooling corresponding to multiple serous retinal detachments in the posterior lesion and vascular leakage in the peripheral retina and choroid, resolved after steroid tapering therapy. Interestingly, wide-field indocyanine angiograms revealed narrowing of choroidal vessels in the acute phase and its normalization with resolution of inflammation after the therapy.
Eyes with Vogt-Koyanagi-Harada disease had peripheral chorioretinal vascular leakage and choroidal vessel narrowing in the acute phase. Wide-field angiography is a useful tool to reveal peripheral chorioretinal findings and assess diameters and density of choroidal vessels.
Vogt-Koyanagi-Harada (VKH) disease is defined as a bilateral glanulomatous panuveitis with or without extraocular manifestations such as meningismus, tinnitus, perception deafness, cerebrospinal fluid pleocytosis, alopecia, poliosis, and depigmentation of the skin . In the acute phase, several widespread ocular manifestations including swelling of the optic disc, multiple serous retinal detachments, thickening of the choroid, and ciliochoroidal detachments were observed [1, 2]. Adequate doses of corticosteroids soon after the disease onset often resolve the ocular and systemic manifestations . Several previous reports [2, 4] have shown fluorescein angiography (FA) and indocyanine green angiography (ICGA) findings in the eyes with VKH disease. However, no reports described peripheral findings in the eyes with VKH disease using wide-field FA and ICGA. In the current case report, we evaluated the wide-field FA and ICGA findings before and after steroid therapy in the eyes with VKH disease as well as the clinical observations.
Binarization of wide-field indocyanine green angiography images
Densities of retinal and choroidal vessels
Time of measurement
In the current case report, we performed wide-field FA and ICGA using Optos California before and after steroid therapy in the eyes with VKH disease, which revealed peripheral chorioretinal lesions and enabled densitometry of retinal and choroidal vessels by binarization of wide-field ICGA images. We found that peripheral findings as well as posterior findings were observed in this patient. Recent reports described that wide-field imaging was useful to identify peripheral lesions in diabetic retinopathy (DR)  and age-related macular degeneration [7, 8] and assess progression of diseases such as DR and retinitis pigmentosa [6, 9]. There are no reports describing wide-field angiography findings in the eyes with VKH disease. However, several reports [10–12] described ciliochoroidal detachments using UBM the same as in the current patient, indicating that the peripheral lesions also were involved in the eyes with VKH disease. Therefore, wide-field angiography was useful to evaluate the wider area than conventional FA and ICGA.
We previously reported  that binarization of wide-field ICGA images enabled quantification of choroidal vessel density in the eyes with central serous chorioretinopathy. In the current report, the same method was used to evaluate the change before and after the therapy in the eyes with VKH disease. Although a subtraction of FA images from the ICGA images had failed because of intensive hyperfluorescent signals related to subretinal pooling of fluorescein dye, we could recognize the decreased densities using binarization of wide-field ICGA in the acute phase and those recoveries after the therapy in both posterior and peripheral lesions. Kim et al.  reported that parafoveal capillary density using OCT angiography images in the eyes with uveitis was significantly lower than in the healthy controls. In addition, Hirooka et al.  reported that macular mean blur rate using laser speckle flowgraphy significantly increased after treatment accompanied with a decrease of central choroidal thickness in the eyes with VKH disease. Taken together, in the eyes with VKH disease, the inflammation causes vascular hyperpermeability and diffuse infiltration of lymphocytes and fluids into the choroidal stroma, resulting in a marked choroidal thickening . Then, the choroidal vessels are compressed by the increased hydrostatic pressure in the choroidal stroma and the blood flow might be decreased . In the current case, the densities in both the posterior and peripheral lesions in the acute phase were lower than those after the therapy. Future studies with more samples should be needed to confirm this result and elucidate underlying pathogenesis.
The current study has several limitations. First, this is just a case report. With large samples, a quantification of choroid vessels density by which fluorescein signals were subtracted from the ICGA images should be examined. Second, there were no appropriate controls, which means age-matched controls with neither any inflammation nor retinal or choroidal diseases.
In conclusion, the current case report showed that wide-field angiograms revealed not only that peripheral lesion was involved in the eyes with VKH disease but also that the vessel diameters and the vessel density in the peripheral lesion decreased in the acute phase. A future studies with a large sample size is needed for further understanding of the pathogenesis of VKH disease.
This study was supported by a Grant-in-Aid for Scientific Research (C) 15K10875 (Y.H.), 60273447 (M.Y), 25462758 (T.Y.), and Scientific Research (B) 15H04997 (Y.O.) from the Japan Society for the Promotion of Science, Tokyo, Japan. Y.H. also was supported by the Mochida Memorial Foundation, Takeda Science Foundation, Suzuken Memorial Foundation, and Santen Pharmaceutical’s Founder.
RK, YH, NN, and KS collected the data. YH wrote the main manuscript text. TY, MY, and YO supervised the work. All authors read and approved the final manuscript.
Consent for publication
An informed consent for publication was obtained from the patient.
The authors declare that they have no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
- Moorthy RS, Inomata H, Rao NA (1995) Vogt-Koyanagi-Harada syndrome. Surv Ophthalmol 39:265–292View ArticlePubMedGoogle Scholar
- Bouchenaki N, Herbort CP (2001) The contribution of indocyanine green angiography to the appraisal and management of Vogt-Koyanagi-Harada disease. Ophthalmology 108:54–64View ArticlePubMedGoogle Scholar
- Lai T, Chan R, Chan C et al (2009) Effects of the duration of initial oral corticosteroid treatment on the recurrence of inflammation in Vogt-Koyanagi-Harada disease. Eye 23:543–548View ArticlePubMedGoogle Scholar
- Chee SP, Jap A, Cheung CM (2010) The prognostic value of angiography in Vogt-Koyanagi-Harada disease. Am J Ophthalmol 150:888–893View ArticlePubMedGoogle Scholar
- Hirahara S, Yasukawa T, Kominami A et al (2016) Densitometry of choroidal vessels in eyes with and without central serous chorioretinopathy by wide-field indocyanine green angiography. Am J Ophthalmol 166:103–111View ArticlePubMedGoogle Scholar
- Silva PS, Cavallerano JD, Haddad NM et al (2015) Peripheral lesions identified on ultrawide field imaging predict increased risk of diabetic retinopathy progression over 4 years. Ophthalmology 122:949–956View ArticlePubMedGoogle Scholar
- Writing Committee for the OPTOS Peripheral RetinA (OPERA) study (Ancillary Study of Age-Related Eye Disease Study 2), Domalpally A, Clemons TE, Danis RP et al (2017) Peripheral Retinal Changes Associated with Age-Related Macular Degeneration in the Age-Related Eye Disease Study 2: Age-Related Eye Disease Study 2 Report Number 12 by the Age-Related Eye Disease Study 2 Optos Peripheral RetinA (OPERA) Study Research Group. Ophthalmology 124:479–487View ArticleGoogle Scholar
- Suetsugu T, Kato A, Yoshida M et al (2016) Evaluation of peripheral fundus autofluorescence in eyes with wet age-related macular degeneration. Clin Ophthalmol 10:2497–2503View ArticlePubMedPubMed CentralGoogle Scholar
- Ogura S, Yasukawa T, Kato A et al (2014) Wide-field fundus autofluorescence imaging to evaluate retinal function in patients with retinitis pigmentosa. Am J Ophthalmol 158:1093–1098View ArticlePubMedGoogle Scholar
- Kawano Y, Tawara A, Nishioka Y et al (1996) Ultrasound biomicroscopic analysis of transient shallow anterior chamber in Vogt-Koyanagi-Harada syndrome. Am J Ophthalmol 121:720–723View ArticlePubMedGoogle Scholar
- Gohdo T, Tsukahara S (1996) Ultrasound biomicroscopy of shallow anterior chamber in Vogt-Koyanagi-Harada syndrome. Am J Ophthalmol 122:112–114View ArticlePubMedGoogle Scholar
- Kishi A, Nao-i N, Sawada A (1996) Ultrasound biomicroscopic findings of acute angle-closure glaucoma in Vogt-Koyanagi-Harada syndrome. Am J Ophthalmol 122:735–737View ArticlePubMedGoogle Scholar
- Kim AY, Rodger DC, Shahidzadeh A et al (2016) Quantifying retinal microvascular changes in uveitis using spectral-domain optical coherence tomography angiography. Am J Ophthalmol 171:101–112View ArticlePubMedGoogle Scholar
- Hirooka K, Saito W, Namba K et al (2015) Relationship between choroidal blood flow velocity and choroidal thickness during systemic corticosteroid therapy for Vogt-Koyanagi-Harada disease. Graefes Arch Clin Exp Ophthalmol 253:609–617View ArticlePubMedGoogle Scholar