trophy, macroreticular dystrophy, and fundus pulverulentus together as pattern dystrophy of the retinal pigment epithelium
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1 - ACTA OPHTHALMOLOGICA SCANDINAVICA 1997 Reticular dystrophy of the retinal pigment epithelium and choroidal neovascularization A fluorescein and ICGV study Filippo Marano, August F. Deutman2, Alfred J. L. G. Pinckers2, Albert L. Aandekerk2 and Wilhelmina J. Rijneveld3 Institute of OphthalmologyL, University of Catania, Catania, Italy, Institute of Ophthalmology2, University Hospital Nijmegen, Nijmegen and Westfries Gasthuis3, Hoorn, The Netherlands ABSTRACT. We report the clinical history of 2 patients affected with reticular dystrophy of the retinal pigment epithelium and central choroidal neovascularization. With time, spontaneous reduction of the subretinal fluid associated with consequent improvement of the visual acuity has been noted in our first case. The second patient showed a stable fibrotic subfoveal choroidal neovascularization. Conventional fluorescein angiography and indocyanine green videoangiography findings are illustrated. The differential diagnosis between other reticular pigmented lesions often associated with choroidal neovascularization is discussed. Key words: reticular dystrophy of the RPE - choroidal neovascularization - fluorescein angiography - ICGV. Acta Ophthalmol. Scand. 1997: 75: ystrophia reticularis laminae pig- D mentosae retinae has been described for the first time by Sjogren in 1950 as an autosomal, recessively inherited disease. A network of hyperpigmentation, resembling a fishing net with knots, located in the pigmented layer of the retina, and a presumed unaffected choriocapillaris are typical findings of this uncommon disease. In the reported family, Sjogren also noted spherophakia with myopia and luxated lenses, partial atrophy of the iris, scleral staphyloma, convergent strabismus, and a gradual disintegration of the hyperpigmented net over a long period. Deaf-mutism and choreatiform behaviour were also reported in some cases. Deutman & Riimke (1969) described a second family, and confirmed the recessive inheritance of the disease. Other authors (Alezzandrini 1971; Hsieh et al. 1977; Kingham et al. 1978) reported families with a kind of reticular dystrophy and an autosomal dominant trait. Marmor & Byers (1977) grouped these recessive and dominant dystrophies with butterfly-shaped dys- trophy, macroreticular dystrophy, and fundus pulverulentus together as pattern dystrophy of the retinal pigment epithelium. Except for Sjogren s family, the visual prognosis in this kind of dystrophy of the retinal pigment epithelium seems to be relatively good, at least in the early stages (Pinckers 1988). In this report we describe the clinical history of 2 patients affected with reticular dystrophy of the retinal pigment epithelium that developed choroidal neovascularization (CNV). Fluorescein angiography and indocyanine green videoangiography (ICGV) findings are herein presented. The differential diagnosis between other reticular pigmented lesions often associated with choroidal neovascularization is also discussed. Case Reports Case 1 A 36-year-old man was seen for the firs1 time in September 1993 because of a sudden visual loss in his left eye. Best cor- rected visual acuity was 0.8 in the right eye and 0.12, associated with metamorphopsia, in the left eye. Biomicroscopy showed a normal anterior segment in both eyes, IOP was found in the normal range. Fundus examination showed a bilateral symmetrical reticular pattern at the posterior pole extending concentrically beyond the vascular arcade and nasally to the optic disc. This pattern, localized in the deeper layers of the retina, showed a yellowish appearance in the posterior pole and a dark color more peripherally, expecially nasal to the disc. Optic nerve head and retinal vessels were normal. Examination of his left fundus showed a small macular detachment of the sensory retina with suspected CNV. Both ERG and EOG (light peak/dark ratio was 2.48 in the right eye and 2.81 in the left eye) were in the normal range. Only an aspecific modification of the colour vision (no axis subtype) was present in the right eye, while a combined acquired red-greenhlue-yellow deficit with anomaloscopic diminished red sensitivity has been noted in the left eye. This is consistent with photoreceptor misalignment at the posterior pole. He is the youngest son of healthy consanmeous parents. The ophthalmic examination was unremarkable in his elderly brother. Conventional fluorescein angiography revealed the typical aspect of fehdar dystrophy of the retinal pigment epithelium described for the first time by Sjogren in A bilateral symmetrical hypofluorescent reticular net with an evident dark spot at the junctions, resembling a fishing net with knots associated with a central diffuse hypopigmentation, was noted. Moreover, localized subfoveal leakage concomitant with CNV was de- 22
2 ACTA OPHTHALMOLOGICA SCANDINAVICA ' Fig. 1. (Case I). The composite shows the hypofluorescent reticular net resembling afishing net with knots associated with a central diffuse hypopigmentation. A subfoveal hyperfluorescent area concomitant with a small CNV is also evident. finitively present on fluorescein angiography (Fig. 1). Because of the central localization no laser treatment was advised. Three months later, the visual acuity was spontaneously improved. It was 0.8 in the right eye and 0.3, associated with less metamorphopsia, in the left eye. Fundus examination revealed a reduction of the subretinal fluid in the left eye confirmed by the fluorescein angiogram (Fig. 2). ICGV performed 2 months later did not show any hyperfluorescent area significant of an active CNV. However. a diffuse hypofluorescent central area associated with the typical hypofluorescent reticular pattern more peripherally was present in the late phases (Fig. 3). During the last visit in December 1994, visual acuity had no significant changes. Fundus examination showed a completely dry subfoveal lesion. Case 2 A 53-year-old woman was referred in November 1995 because of a reticular hyperpigmented pattern in both fundi with suspected CNV in her left eye. Best corrected visual acuity was 0.7 in the right eye and 0.6 with metamorphopsia in the left eye. The anterior segment examination was unremarkable. IOP was normal. Fundus examination showed a bilateral hyperpigmented reticular pattern in the macular area and nasally to the optic nerve head. A small subfoveal whitish lesion surrounded by a circular hyperpigmented ring was present in the left eye. The EOG was abnormal in both eyes (light peak/dark ratio was 1.52 in the right eye and 1.64 in the left eye). Colour vision: anomaloscope equation showed a zone slightly enlarged towards red in the right eye, and a symmetrical enlargement toward green and red in the left eye. Light discrimination was within the age limits. General medical condition was unremarkable. The family history did not reveal any significant information. Digital fluorescein angiography clearly showed the symmetrical hypofluorescent reticular pattern with knots surrounded by a diffuse hyperfluorescent area. Thk%- ' brotic subretinal lesion was hyperfluorescent during the early phases, showing no leakage in the late phases. ICGV-displayed a normal arterio-venous choroidal filling. Whereas the hyperpigmented net was not evident during the entire choroidal angiography, 45 min after the injection of the dye a diffuse central dark area appeared at the posterior pole. Bilateral, tiny hyperfluorescent dots were also observed (Fig. 4).
3 - ACTA OPHTHALMOLOGICA SCANDINAVICA 1997 Fig. 2. (Case 1). Fluorescein angiography shows reduction of the subretinal leakage in the late phases. Left: September Right: 3 months later Fig. 3. (Case I). In the late phases, ICGV shows a dilt'use hypofluorescent central area associated with the typical hypofluorescent reticular pattern more peripherically. No sign of dye leakagc is noted in the foveal re- Igion.
4 ACTA OPHTHALMOLOGICA SCANDINAVICA Fig. 4. (Case 2). Top left: red-free digital fundus photography. Top right: digital fluorescein angiography shows fibrotic CNV surrounded by pigmented reticular pattern, and circular diffuse hyperfluorescence. Bottom left: Early phases of ICGV. Bottom right: in the very late phases (45 min) an irregular hypofluorescent area surrounds the macula and optic nerve head. Discussion The pigmented reticular arrangement seems to be an aspecific response to different stimuli. It has been reported in several conditions like pattern dystrophy, gyrate atrophy (Deutman et al. 1978), chronic progressive external ophthalmoplegia (Bastiaensen 1978), myotonic dystrophy (Hayasaka et al. 1984), pseudoxanthoma elasticum (McDonald et al. 1988) mucopolysaccharidoses type 11 (Delleman et al. 1985), and age-related macular degeneration (Gass 1973). The differential diagnosis between the recessive type of reticular dystrophy and all the other disorders presenting a reticular pigmented pattern should be made on the basis of the following considerations: development of a bilateral symmetrical reticular pattern early in life; concentric growth from the center to the periphery; hypofluorescent reticular pattern resembling a fishing net with knots associated with surrounding hypopigmentation on fluorescein angiography; a good visual acuity at least in the early stage, and an autosomal recessive inheritance. Ruling out of eventually associated systemic diseases is also necessary. In pathologies where the RPE is involved, CNV can occur. To our knowledge, only Taillanter-Francoz et al. (1981) reported a 13-year-old girl affected with Sjogren s reticular dystrophy and CNV. Shiono et al. (1990) described 25 -
5 - ACTA OPHTHALMOLOGICA SCANDINAVICA I997 a family in which one member showed a reticular hypofluorescent lesion extending in the macular area and nasal to the disc in both eyes associated with bilateral CNV. However, a dominant trait was noted in the affected family by these investigators. Reticular-like pigmentary patterns in patients affected with pseudoxanthoma elasticum and CNV have also been reported by McDonald et al. (1988). In their article, while 67% of patients with reticular pigmentary changes developed the ingrowth of choroidal new vessels, only 10 h had CNV in absence of pigmentary pattern. Gass (1973) reported a high percentage of macular disciform detachment in patients affected with drusen and varying degrees of a reticular pigmented network in the equatorial area of the fundus (Fig. 5). In our patients, besides the reticular dystrophy, the ingrowth of a small subfoveal CNV has been noted in case 1. A spontaneous improvement of the visual acuity with time was concomitant with a reduction of the subretinal fluid. Visual acuity improved and the neovascukarization appeared to be fibrotic. Differently, in case 2 a quiet fibrotic macular CNV has been observed. The morphologic alteration of the dystrophic RPE, including pigment accumulation and rarefaction associated with probab\e changes in Bruchs membrane can lead to the ingrowth of choroidal new vessels from an apparently healthy choriocapillaris. A consequent anomalous production of chemotactic factors stimulating a macrophage migration could be taken into account. In an experimental rat model for retinitis pigmentosa the observed RPE changes demonstrated a progressive breakdown of the pigment epithelial cell junctions (Caldwell et al. 1982). These findings might partially explain how the neovascular net reaches the subretinal space. In both cases, ICGV showed a well defined hypofluorescent irregular central area associated with a reticular dark pattern in the midperiphery completely evident in the very late phase (42 min). During the relatively normal arterio-venous phase only small pigmented clumps were noted. Unexpectedly, the central hypofluorescent pattern seen in ICGV hardly can be compared with the hyperfluorescent area, due to the extensive hypopigmentation of the RPE evident on fluorescein angiography (compare Fig. 1 and Fig. 3, Fig. 4, top right and bottom right). In the midperiphery, where the pigmented reticular network is still clearly present (case I), fluorescein angiography and ICG show similar findings. We also noted hyperfluorescent white dots diffusely spread in the macular area and in correspondence with the hypofluorescent peripherical reticular pattern. No sign of dye leakage was noted in the foveal reglon. Lacking histopathologic studies aboul indocyanine green dye localization after its injection, it is quite difficult to exactly Fig. 5. Age-related macular CNV associated with drusen and peripheral pigmented network. explain the cause of the central hypofluorescence. According to the physicochemical properties of the indocyanine green dye (Cherrick et al. 1960; Benson Kues 1978), either a partially damaged or atrophic choriocapillaris (Amalric 1987) or a lower binding of the dye in the extravascular space might be present. Also, a late blocked choroidal fluorescence caused by an abnormal deposition of any material in the deeper layer of the retina, not revealed on fluorescein angiography, could be taken into account. In summary, the ingrowth of CNV can lead to a further loss of visual acuity in patients affected with reticular dystrophy of the WE. The pathogenetic course of this complication remains unknown, although it is generally accepted that diseased WE can give rise to CNV formation. Once this vision threatening complication occurs new approaches, like surgical membrane removal (Thomas et al. 1993) and radiation therapy (Bergink et al. 1992,1994), have been used as alternatives to laser photocoagulation in the hope of reducing further visual loss. Finally, ICGV may be useful in the study of this rare retinal disease, but further investigations are necessary to understand the unclear ICG patterns. References Alezzandrini AA (197 I): La retino-tluoresceinografia an las alteraciones del epitelio pigmentario de la retina. Arch Oftal B Aires 46: Amalric P (1987): Reticular dystrophy: a minor sign of chronic choroid ischemia. Ophtalmologie I : Bastiaensen LA (1978): Pigment changes of the retina in chronic progressive external ophthalmoplegia. Acta Ophthalmol (Copenh) 62 (Suppl 138): Benson RC & Kues HA (1978): Fluorescence properties of indocyanine green as related 10 XilgQgXphy.Ph~SN\eh%b\~3. \59-\\63. Bergink GJ, Deutman AF & van Daal WAJ (1992): Radiation therapy for subfoveal choroidal neovascular membranes in agerelated macular degeneration: a pitot study. Int Ophthalmol suppl vol 16: 16. Bergink GJ, Deutman AF, van den Broek JFCM, van Daal WAJ & van.der Maazen RWM (1994): Radiation therapy for subfoveal choroidal neovascular membranes in age-related macular degeneration. A pilot study. Graefe s Arch Clin Exp Ophthalmol 232: Caldwell RB, McLaughlin BJ & Boykins LG (1982): Intramembrane changes in retinal pigment epithelial cell junction of the dystropic rat retina. Invest Ophthalmol Vis Sci 23;
6 ACTA OPHTHALMOLOGICA SCANDINAVICA Cherrick GR, Stein SW, Leevy CM & Davidson CS (1 960): lndocyanine green: observations on its physical properties, plasma decay, and hepatic extraction. J Clin Invest 39: Delleman JW & de Jong PTVM (1985): Pigment epithelial pattern dystrophy: a peripheral type. Br J Ophthalmol 69: Deutman AF & Riimke AML (1969): Reticular dystrophy of the retinal pigment epithelium. Arch Ophthalmol82: 4-9. Deutman AF, Sengers RCA & Trybels JMF (1978): Gyrate atrophy of the choroid and retina with reticular pigmentary dystrophy and ornithine-ketoacid-transaminase deficiency. Int Ophthalmol 1: Fishman GA, Woolf MB, Goldberg MF & Busse B (1976): Reticular tapeto-retinal dystrophy. As a possible late stage of Sjogren s reticular dystrophy. Br J Ophthalmol60: Gass JMD (1973): Drusen and disciform macular detachment and degeneration. Arch Ophthalmol 90: Hayasaka S, Kiyosawa M, Katsumata S, Honda M, Fdkase S & Mizuno K (1984): Ciliary and retinal changes in myotonic dystrophy. Arch Ophthalmol 102: Hsieh RC, Fine BS & Lyons JS (1977): Patterned dystrophies of the retinal pigment epithelium. Arch Ophthalmol95: Kingham JD, Fenzl RE, Willerson D & Aaberg TM (1978): Reticular dystrophy of the retinal pigment epithelium. Arch Ophthalmol96: Marmor MF & Byers B (1977): Pattern dystrophy of the pigment epithelium. Am J Ophthalmol 84: McDonald HR, Schatz H & Aaberg TM (1988): Reticular-like pigmentary pattern in pseudoxanthoma elasticum. Ophthalmology 95: Pinckers A (1988): Patterned dystrophies of the retinal pigment epithelium - A review. Ophthal Paed Genet 9: Schiono T, Ishikawa A, Hara S & Tamai M (1990): Pattern dystrophy of the retinal pigment epithelium. Retina 10: Sjiigren H (1950): Dystrophia reticularis laminae pignientosae retinae. Acta Ophthalmol (Copenh) 28: Taillanter-Francoz N, Remy C, Bonnet M & Baserer T (1981): Choroidal neovessels associated with reticular dystrophy of the pigment epithelium (case report). Bull Soc Ophtalmol Fr 81: Thomas MA, Grand MG, Williams DF, Lee CM, Pesin SR & Lowe MA (1992): Surgical management of subfoveal choroidal neovascularization. Ophthalmology 99: Received on December 4th, Corresponding uuthor: Prof. A. F. Deutman Institute of Ophthalmology P.O. Box HB - Nijmegen, The Netherlands. Tel: + 31-(0) Fax: (0)
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