Extensive Chorioretinal Atrophy in Vogt Koyanagi Harada Disease
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1 Extensive Chorioretinal Atrophy in Vogt Koyanagi Harada Disease Shozo Sonoda, Kumiko Nakao and Norio Ohba Department of Ophthalmology, Kagoshima University Faculty of Medicine, Kagoshima, Japan Purpose: To report extensive chorioretinal atrophy during the long-term course of Vogt Koyanagi Harada (VKH) disease not treated properly in the initial phase. Cases: Four patients with VKH disease were examined more than 10 years after onset of the disease. Observations: They presented initially with classic features of VKH disease, except 1 patient who had developed bilateral, acute angle-closure glaucoma as the initial sign. Two patients received systemic corticosteroid therapy at the acute phase of the disease. During the followup of years subsequent to onset, these patients had chronic recurrent anterior uveitis with apparently stable depigmented fundus. Eventually, they developed diffuse, extensive chorioretinal atrophy that resulted in severe visual loss. One patient had an unusual familial occurrence of the disease. Conclusions: Failure to prescribe proper corticosteroid therapy in the initial phase of VKH disease may lead to chronic recurrent uveitis. Long-standing uveitic reactions may eventually result in severe visual loss due to extensive chorioretinal degeneration. Jpn J Ophthalmol 1999;43: Japanese Ophthalmological Society Key Words: Chorioretinal atrophy, corticosteroid therapy, recurrent uveitis, Vogt Koyanagi Harada disease. Introduction Received: August 13, 1998 Address correspondence and reprint requests to: Shozo SONODA, MD, Department of Ophthalmology, Kagoshima University Faculty of Medicine, Sakuragaoka , Kagoshima , Japan Vogt Koyanagi Harada (VKH) disease is a bilateral, diffuse granulomatous uveitis that is probably due to an autoimmune pathomechanism directed against melanocytes. The acute panuveitis is usually resolved in months with early administration of systemic corticosteroid. Choroidal and extraocular depigmentation follow and there are no further episodes. However, improper initial therapy may sometimes lead to chronic recurrent anterior uveitis that may be resistant to corticosteroid therapy and cause vision-threatening complications, such as cataract, glaucoma, and subretinal neovascularization. 1 6 Extensive chorioretinal atrophy is also occasionally observed many years after the onset of disease. 7 9 We report herein, 4 additional cases of such late complications years after onset of the disease. One case had a rare familial occurrence of the disease. Case Reports Of 135 patients with VKH disease seen between 1978 and 1997 in the Kagoshima University Hospital, the following 4 cases developed severe chorioretinal atrophies more than 10 years after onset of the disease. The clinical information of these cases is summarized in Table 1. Case 1 A 66-year-old woman first noted acute visual blurring in 1980 at the age of 53 years and was treated subsequently by a local doctor with the diagnosis of VKH disease. The bilateral acute inflammation regressed with systemic corticosteroids tapered over 6 months. During subsequent years, the patient had exacerbations of anterior uveal reactions about twice each year, and was treated with a variable dose and Jpn J Ophthalmol 43, (1999) 1999 Japanese Ophthalmological Society /99/$ see front matter Published by Elsevier Science Inc. PII S (98)
2 114 Jpn J Ophthalmol Vol 43: , 1999 Table 1. Cases of Chorioretinal Atrophy as a Late Complication of Vogt Koyanagi Harada Disease Sex Age of Onset (y) Treatment Extraocular Clinical Course Recurrence Complication Years After Onset Visual Outcome Last Examination Ophthalmoscopic Findings Both Eyes With Symmetric Changes Sonoda, Nakao, & Ohba Case 1 F 53 Classic Intravenous steroid Case 2 F 65 Acute glaucoma Topical steroid Case 3 M 18 Classic Oral steroid vitiligo, hearing loss Headache, Case 4 M 41 Classic Unknown Headache, tinnitus, Inomata [6] Case 1 F 21 Classic Steroid Alopecia,, dysacousia, Hayakawa [7] Case 1 M 40 Classic Oral steroid Case 2 M 33 Classic Oral steroid loss of hairs,, vitiligo headache, (twice/year) Cataract 13 VA: 0.05, 0.6 Orange-red appearance, peripapillary chorioretinal atrophy, peripheral Dalen- Fuchs nodules Glaucoma, cataract 14 VA: blind, 0.3 peripheral field defect Unknown Cataract 34 VA: 0.2, 0.1 annular scotoma, subnormal ERG, night blindness (protracted) Cataract, glaucoma Glaucoma, rubeosis (several times/y) Sunset-glow appearance, peripapillary chorioretinal atrophy, Dalen-Fuchs nodules, optic atrophy Sunset-glow appearance, peripheral bone spicule pigments, narrowed retinal vessels 25 VA: blind, LP Posterior pigment proliferations, optic atrophy, bone spicule pigment clumps, Dalen- Fuchs nodules 26 VA: LP, blind Enucleations due to ocular pain, histophathologic findings: disappearance of choroidal melanocytes, epithelioid cells in the lesion, plasma cells, lymphocytes accumulated, choroidal neovascularizations 12 VA: 1.2, 1.2 peripheral field defect, subnormal ERG, DA defect Diffuse chorioretinal atrophy 17 VA: 0.9, 0.4 Multiple ovoid atrophic foci, confluent depigmented areas, bone spicule pigment clumps Remarks Familial occurrence (continued) 114
3 S. SONODA ET AL. 115 CHORIORETINAL ATROPHY IN VKH DISEASE Table 1. Continued Sex Age of Onset (y) Treatment Extraocular Clinical Course Recurrence Complication Years After Onset Visual Outcome Last Examination Ophthalmoscopic Findings Both Eyes With Symmetric Changes Hayakawa 9 Case 1 F 28 Classic Oral steroid Case 2 F 43 Classic Steroid Case 3 F 42 Classic Oral steroid Hayakawa 8 Case 1 M 36 Classic Topical steroid loss of hairs, loss of hairs,, dysacousia, vitiligo, dysacousia 12 VA: 1.0, 0.9 midperiphery depression, subnormal ERG (three times/y) (for 15 y) (once/y, for 10 y) 17 VA: 1.2, 1.2 midperiphery depression, subnormal ERG 23 VA: 0.1, 0.6 peripheral depression, elevated DA thresholds, extinct ERG Cataract 17 VA: 1.0, 1.0 superior field defect, subnormal ERG, delayed DA Posterior synechiae, chorioretinal atrophy, with pigmentations and depigmentations Partial sunset-glow appearance, midperiphery, chorioretinal atrophy, with pigmentation and atrophic foci Posterior synechiae, posterior sunset-glow, chorioretinal atrophy, with pigment clumps and Dalen-Fuchs nodules Widespread chorioretinal atrophy, bone spicule pigments, peripapillary whitish atrophy DA: dark adaptation, HM: hand movement, LP: light perception, VA: visual acuity (right eye, left eye). Remarks 115
4 116 of topical or systemic corticosteroid taper. The recurrent anterior uveitis caused a progressive decrease in bilateral visual acuity. The patient visited us 13 years after the onset of disease. On presentation, she also complained of persistent tinnitus and of the eyebrows. Best visual acuity was RE: 0.05 and LE: 0.6. Corneas were clear. Anterior chambers had 11 cells. Irides and anterior chamber angles were unremarkable. Lenses had posterior subcapsular opacities. Ophthalmoscopy revealed the Jpn J Ophthalmol Vol 43: , 1999 characteristic orange-red appearance of both fundi. There were peripapillary chorioretinal areas of atrophy with some pigment clumps and multiple, yellow, discrete areas of chorioretinal atrophy in the midperiphery (Figure 1A). Case 2 A 79-year-old woman had severe pain in the forehead, tinnitus, ocular pain, and bilateral visual loss in Figure 1. Fundus photographs (A: case 1, B: case 2, C: case 3, D: case 4) illustrating extensive chorioretinal degeneration.
5 S. SONODA ET AL. 117 CHORIORETINAL ATROPHY IN VKH DISEASE 1981, when aged 65 years, and was referred to us 3 weeks later. She presented with features of acute angle-closure glaucoma; namely, perilimbal injection, shallow anterior chamber with numerous cells and flares, partial posterior synechiae, unidentified angle structure, and elevated intraocular pressure. Iridectomy relieved symptoms and normalized the intraocular pressure. During the acute phase of the disease no corticosteroid therapy was performed because of the delayed diagnosis of VKH disease. Six months later, ophthalmoscopy revealed the sunset-glow appearance of the posterior fundus and gray-white pigments in the periphery. At that time she had vitiligo over her head and mild hearing loss. In subsequent years, she was followed up by doctors in our affiliated hospital and had recurrent anterior uveal inflammation that was resistant to corticosteroids. The patient returned to our University Hospital in 1996 at the age of 79 years, 14 years after the onset of VKH disease. Best visual acuity was RE: blind and LE: 0.3 with aphakic correction. Anterior segments and intraocular pressure were unremarkable. Fundus changes were symmetric in both eyes. Chorioretinal atrophy was so marked in the peripapillary and juxtapapillary areas that the choroidal vessels were barely detectable. Optic disks appeared pale, being more prominent in the left eye (Figure 1B). There was multiple, ovoid, yellow-white well-circumscribed chorioretinal scarring in the inferior fundi. Figure 2 illustrates right visual field at the ages of 68 and 79 years. Case 3 A 52-year-old man first noted bilateral acute visual loss and headache in 1964 at the age of 18 years. The disease was diagnosed as VKH disease by a local doctor. He recovered in a few months with oral corticosteroid administration, but reported that during the subsequent 30 years he had suffered slow, progressive bilateral decrease in visual acuity. From about 48 years of age, he had experienced difficulty in night vision as well, and at that time he was diagnosed as having retinitis pigmentosa by another local doctor. He visited us in 1998 at the age of 52 years because of further progressive visual losses. On presentation, he appeared physically healthy. Best visual acuity was RE: 0.2 and LE: 0.1, both eyes being pseudophakic. Panel D-15 test revealed blue-yellow defect in both eyes. Goldmann perimetry showed bilateral annular scotoma and peripheral field constriction (Figure 3). Results of scotopic electroretinogram were subnormal. Corneas were clear. A few inflammatory cells were present bilaterally in the anterior chamber. Pupils were round but sluggish to light. Irides and vitreous cavities were unremarkable. Ophthalmoscopy revealed bilateral diffuse chorioretinal atrophy, retinal pigment clumps of bone spi- Figure 2. Case 2: Goldmann perimetry in right eye, at 68 and 79 years of age, measured 3 and 14 years after onset, respectively.
6 118 Jpn J Ophthalmol Vol 43: , 1999 Figure 3. Case 3 at 52 years of age. Goldmann perimetry in both eyes, measured 34 years after disease onset. cule pattern in the midperiphery, and narrowed retinal artery (Figure 1C). Laboratory tests for HLA revealed HLA-DR4. Case 4 A 66-year-old man complained of severe visual losses during the last 25 years. He had been followed-up by a local ophthalmologist. According to his statement, he first noted in 1964, at the age of 41 years, acute profound visual losses accompanied by headache, tinnitus, and irritable scalp hairs. At that time he was said to have bilateral severe uveitis, which regressed in a few months, leaving of scalp hairs. Whether he received corticosteroid therapy was. Subsequently, inflammatory symptoms and signs recurred many times, and complicated cataracts and glaucoma had developed. The patient was referred to us in 1989 because of further progression of visual losses. The right eye was blind and the left eye had only light perception. Pupils were irregularly dilated with posterior synechiae and reacted poorly to light. No active inflammatory signs could be identified bilaterally in either the anterior or posterior ocular segments. Ophthalmoscopic examinations disclosed pale optic disks, widespread chorioretinal degenerative changes with proliferated pigment clumps, and narrow retinal vessels (Figure 1D). There was familial occurrence of VKH disease. His son had developed acute, bilateral uveitis preceded by headache in 1989 at the age of 35 years. The disease was compatible with the clinical features of VKH disease, and it resolved in 3 months after initial high-dose intravenous corticosteroids followed by oral tapering, leaving a sunset-glow appearance of the fundi. A 4-year follow-up study showed no further episode. The father and son, both affected by VKH disease, had no other physical ailments. There was no other contributory family history. The results of HLA typing were as follows. Affected father: A2, A24/B39, Bw54/Cw1, Cw7/DR4; nonaffected mother: A24, A31/B7, B15/Cw3, Cw7/DR1, DR4; affected son: A24, A31/Bw54, B15/Cw1, Cw3/DR4. Discussion The cases described above featured bilateral severe visual loss and extensive chorioretinal atrophy due to chronic recurrent uveitis. The disease is unequivocally diagnosed as VKH disease from the initial symptoms and signs, followed by the orange-red or sunset-glow appearance of the fundus and extraocular depigmentation, such as and vitiligo, VKH disease usually presents with a limited period of acute severe panuveitis and regresses in months with favorable visual recovery and no further episode, but it may sometimes show recurrences. When the disease recurs for a long time, complications, such as cataract, glaucoma, and subretinal neovascularization, may occur. 1 6 Our patients had long-standing anterior uveal reactions and
7 S. SONODA ET AL. 119 CHORIORETINAL ATROPHY IN VKH DISEASE eventually had severe visual losses, even complete blindness, at examinations years after onset of the disease. A literature search enables one to identify 7 cases, all reported from Japan, 7 9 whose clinical features are summarized in Table 1. The previously reported cases are consistent with our cases and indicate that they initially presented with classic features of VKH disease and that more than 10 years later they had severe visual loss due to extensive chorioretinal atrophy with pigment proliferation and migration in the retina. Vogt Koyanagi Harada disease is recognized as an immune-mediated disease that primarily affects melanocytes. Hence, systemic administration of corticosteroid, first advocated in the late 1960s 10 is the current therapeutic measure that significantly alters the course and prognosis of the disease. Early aggressive use of systemic corticosteroid followed by slow tapering over several months is recommended. 11 However, if the timing, doses, and tapering of therapeutic regimen are not managed properly, anterior uveitis may be recurrent and become resistant to corticosteroid; in fact, some of our cases did not receive corticosteroid therapy at the early phase of disease. Chronic anterior uveitis may result in serious inflammatory events in the retina as well as choroid, as evidenced by a histopathologic study 12 demonstrating that chronic inflammation of the choroid damages Bruch s membrane and retinal pigment epithelium and, hence, leads to chorioretinal degeneration with pigment proliferation. The incidence of extensive, severe chorioretinal atrophy in VKH disease remains undefined; it may be more uncommon after the introduction of standardized corticosteroid therapy. In any event, it is recommended that patients be followed up for many years, in particular those who had a chronic course of the disease. The present observations warrant further discussion. One of our cases presented with distinct features of bilateral acute angle-closure glaucoma. The diagnosis of VKH disease and proper corticosteroid therapy in the early phase of the disease were delayed, which might have led to the long-standing anterior uveitis in this case; it is documented in the literature that occasional cases of VKH disease may develop acute angle-glaucoma as an initial clinical sign As regards familial occurrence of VKH disease, an extensive literature search identifies 2 reports, each describing VKH disease in monozygotic twins. 16,17 One of the cases described here, an elderly man, had a son who was affected with VKH disease. This is, to our knowledge, the first report of the disease over two successive generations. Immunogenetic predisposition to VKH disease has been well-defined for its significant association with specific HLA genes. 18 It is of interest in this connection that the present familial cases shared HLA-DR4, an HLA class II antigen susceptible to VKH disease. It remains to be elucidated why the incidence of familial VKH disease is rare. References 1. Sugiura S. Vogt Koyanagi Harada disease. Jpn J Ophthalmol 1978;22: Ohno S, Char DH, Kimura SJ, O Connor GR. Vogt-Koyanagi-Harada disease. Am J Ophthalmol 1977;83: Beniz J, Forseter DJ, Lean JS, Smith RE, Rao NA. Variations in clinical features of the Vogt-Koyanagi-Harada disease. Retina 1991;11: Ohno S, Minakawa R, Matsuda H. Clinical studies of Vogt Koyanagi Harada s disease. Jpn J Ophthalmol 1988;32: Moorthy RS, Inomata H, Rao NA. Vogt-Koyanagi-Harada disease. Surv Ophthalmol 1995;39: Inomata H, Minei M, Taniguchi Y, Nishimura F. Choroidal neovascularization in long-standing case of Vogt-Koyanagi- Harada disease. Jpn J Ophthalmol 1983;27: Hayakawa M, Takahashi H, Yamaguchi T, Konyama W, Kato K, Nakajima A. Chorioretinal atrophy in the long course of Harada s disease. Ganka Rinsho Iho (Jpn Rev Clin Ophthalmol) 1989;83: Hayakawa M, Takahashi H, Kato K, Nakajima A. Clinical course of protracted Harada s disease over seventeen-year period. Ganka Rinsho Iho (Jpn Rev Clin Ophthalmol) 1990; 84: Hayakawa M, Iwasaki Y, Murakami A, et al. Fate of chorioretinal atrophy and visual impairment in protracted cases of Harada s disease. Ganka Rinsho Iho (Jpn Rev Clin Ophthalmol) 1990;84: Masuda K, Tanishima T. Harada s disease. A new therapeutic approach. Rinsho Ganka (Jpn J Clin Ophthalmol) 1969;23: Sasamoto Y, Ohno S, Matsuda H. Studies on corticosteroid therapy in Vogt-Koyanagi-Harada disease. Ophthalmologica 1990;201: Perry HD, Font RL. Clinical and histopathologic observations in severe Vogt-Koyanagi-Harada syndrome. Am J Ophthalmol 1977;83: Shirato S, Hayashi K, Masuda K. Acute angle closure glaucoma as an initial sign of Harada s disease. Report of two cases. Jpn J Ophthalmol 1980;24: Hatta M, Kumagaya I, Takeda H, Nomatsu I. Increased ocular tension as initial sign of disease of Harada. Rinsho Ganka (Jpn J Clin Ophthalmol) 1968;22: Watanabe T. Harada s disease with an onset mimicking acute angle-closure glaucoma. Ganka Rinsho Iho (Jpn Rev Clin Ophthalmol) 1971;65: Itoh S, Kurimoto S, Kouno T. Vogt-Koyanagi-Harada disease in monozygotic twins. Int Ophthalmol 1992;16: Rutzen AR, Ortega-Larrocea G, Schwab IR, Rao NA. Simultaneous onset of Vogt-Koyanagi-Harada syndrome in monozygotic twins. Am J Ophthalmol 1995;119: Ohno S. Immunological aspects of Behçet s and Vogt- Koyanagi-Harada s diseases. Trans Ophthalmol Soc UK 1981; 101:
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