Mechanisms of Inflammatory Response in Sympathetic Ophthalmia and Vkh Syndrome

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MECHANISMS OF INFLAMMATORY RESPONSE IN SYMPATHETIC OPHTHALMIA AND VKH SYNDROME NARSING A. RAG Los Angeles, California SUMMARY sympathetic ophthalmia. Moreover, the inciting Although the iucitiug events in the pathogenesis of event for the two entities is different: the develop­ sympathetic ophthalmia and Vogt-Koyanagi-Harada ment of intraocular inflammation in sympathetic (VKH) syndrome are different, these two forms of ophthalmia requires a penetrating ocular injury, but bilateral granulomatous uveitis share several clinical, no traumatic event is required for the development histopathological and immunohistochemical features, of VKH syndrome. The latter usually follows including their association with HLA types and in their prodromal symptoms and signs suggestive of a in vitro T-cell response to retinal antigens. These systemic viral infection. In addition, although it clinical and immunopathological features indicate that appears that extraocular manifestations such as there is an underlying T -cell-mediated autoimmunity to vitiligo, alopecia, poliosis, meningismus and dysacu­ uveaVretinai antigens in the development of these sis are relatively more frequent in VKH syndrome, forms of uveitis. Both forms exhibit preservation of there are studies revealing the presence of similar the choriocapillaris and retina despite extensive inflam­ manifestations in sympathetic ophthalmia?,4 matory cell infiltration in the choroid. Recent experi­ The typical histopathological features seen in the mental studies suggest that this preservation of early phases of both sympathetic ophthalmia and choriocapillaris could be the result of anti-inflammatory VKH syndrome include a granulomatous inflamma­ products secreted by the retinal pigment epithelium, tion that primarily involves the choroid, with a including transforming growth factor-beta and a novel similar albeit milder inflammatory infiltrate that protein called retinal pigment epithelial protective involves the iris and ciliary body. However, the protein that is known to suppress the phagocyte choroid is the site where several characteristic generation of superoxide. Such suppression of the features are observed, including: (1) diffuse lympho­ oxidant release in the choroidal inflammation could cytic infiltration interrupted at multiple sites with help protect the uvea from necrotic change and collections of epithelioid cells and few multinu­ preserve the choriocapillaris from inflammatory cell cleated giant cells; (2) the presence of pigment in infiltration. the epithelioid cells and giant cells in the absence of apparent choroidal necrosis; (3) sparing of the Although sympathetic ophthalmia and Vogt-Koya­ choriocapillaris from inflammatory cell infiltration; nagi-Harada (VKH) syndrome are two distinct and (4) preservation of retinal pigment epithelium clinical entities, they share virtually identical histo­ (RPE) and retina except at the sites of Dalen-Fuchs' pathological features, fluorescein angiographic find­ nodules and other foci where RPE junctions are ings and association with HLA antigens of DR4, disrupted. These disrupted RPE cells are commonly DRw53 and Bw54.1 However, whereas VKH syn­ detected by fluorescein angiography as focal leaks at drome has a predilection for darkly pigmented races the level of RPE. - Asians, Hispanics, Native Americans and Asian Sympathetic ophthalmia and VKH syndrome also Indians2 - no racial predilection is observed in share several immunopathological features, such as infiltration of primarily T-lymphocytes in the chor­ From: A. Ray Irvine, Jr, Ophthalmic Pathology Laboratory. Doheny Eye Institute, University of Southern California, School oid. In both entities, most of these infiltrated cells of Medicine, Los Angeles, California, USA. exhibit the markers of helper and suppressor/ Correspondence to: Narsing A. Rao, MD, Doheny Eye cytotoxic cells, along with class II MHC molecules.5,6 Institute, 1450 San Pablo Street DVRC-211, Los Angeles, CA 90033-1088, USA. Similar molecules are also noted on the activated Eye (1997) 11, 213-216 © 1997 Royal College of Ophthalmologists 214 N. A. RAO macrophages along with various adhesion molecules, appears that the formation of these epithelioid cells including intercellular adhesion molecule-l.6 More­ requires the presence of activated T-cells in the over, in both entities the choroidal infiltrates inflammatory lesion. Moreover, the cytokines of T­ generate various pro-inflammatorycytokines? Over­ cells, such as the interleukins IL-2, IL-4, IL-6, IL-8 all, these immunohistological features suggest a and IL-lO, interferon gamma and others, are also delayed type of hypersensitivity (T-cell-mediated) known to modulate epithelioid cell formation and the mechanism in the induction and/or perpetuation of maintenance and resolution of the granulomatous the uveal inflammation,possibly directed to the uveal inflammation?1 Granuloma formation is also modu­ melanocytes or other antigens in the uveal tract.4,8 lated by the level of class II MHC molecule Once initiated, an immune response against a tissue expression by the macrophages. Adhesion molecules target, such as in the uvea, can lead to the further displayed on the macrophages and vascular endothe­ release of various sequestered self-antigens, against lium may also contribute to the development of which self-tolerance has never been established. granulomatous inflammation.6 Release of such antigens can lead to the perpetuation The metabolic products released at the site of of uveitis, even though the initiating trigger may be inflammation are found either to accentuate granu­ directed to a restricted response to a single specific loma development or to suppress formation of target.9,lO epithelioid cell granulomas and the associated chronic inflammatory process.12 Studies on experi­ mental granulomatous uveitis have revealed GRANULOMATOUS INFLAMMATIONS OF enhancement of the granulomatous process in the THE UVEA presence of lip oxygenase metabolic products of AA. The cellular and molecular mechanisms leading to In contrast cyclo-oxygenase products are noted to development of granulomatous uveitis are poorly suppress granuloma formation.lO Such modulation of understood. However, the role of macrophages, T­ granulomatous inflammation in the presence of AA cells and their cytokines, melanocytes, vascular metabolites could be the result of altered macro­ endothelial cells and arachidonic acid (AA) metabo­ phage expression of MHC class II molecules. More­ lites in the initiation, maintenance and resolution of over, lipoxygenase products of AA are important the granulomatous inflammation is becoming clear. inflammatory mediators with pro-inflammatory func­ In general the granulomatous uveitis can be classified tions of chemotaxis, vasodilation and induction of as either hypersensitivity type or foreign body type. lysosomal enzyme release.13 The latter is rarely observed and usually results from T-cells cause pathological changes through their traumatic events associated with retained foreign ability to produce cytokines, which can recruit material. The hypersensitivity granulomas usually additional T-cells, macrophages and other phagocytic result either from an infectious agent such as cells, including eosinophilic leucocytes. All these cells mycobacteria, or from a non-infectious aetiology, are present in the uveal tracts of patients with such as an autoimmune disorder, mediated by either sympathetic ophthalmia and all may cause tissue T-cells or immune complexes. damage if not properly regulated. Additionally, a Hypersensitivity granulomas show three charac­ subset of T-Iymphocytes, cytotoxic T-cells, may cause teristic microscopic patterns: zonal, sarcoidal or these pathological changes directly. diffuse. These three patterns may indicate an under­ lying mechanism of granuloma formation. The zonal pattern of granulomatous uveitis consists of a central TISSUE INJURY IN UVEITIS area of necrosis surrounded by zones of different Several kinds of experimentally induced uveitis in infiltrating inflammatory cells, such as epithelioid animals have revealed the importance of macro­ cell/histiocytes, lymphocytes and other inflammatory phages and other phagocytic inflammatory cells in cells, including fibroblasts. Such a zonal pattern is inducing tissue damage, although T-cells are required seen in tuberculosis and other infectious diseases. for the induction of uveitis. These phagocytes cause The sarcoidal pattern consists of a collection of necrosis of the tissue and amplify the inflammation epithelioid cells without necrosis. Typically such a by releasing various secretory products, including pattern is observed in sarcoidosis. The diffuse pattern proteases, AA metabolites and free radicals. The reveals collections, primarily of lymphocytes, free radicals are potent cytotoxic agents that throughout the choroid and the anterior uvea with primarily cause peroxidation of lipid cell membranes focal collections of epithelioid cells. This pattern is at the site of their release. The free radicals that commonly seen in immune-mediated granulomas cause such tissue damage are mostly derived from such as sympathetic ophthalmia and VKH syndrome. the oxygen metabolite superoxide and its derived In granulomatous uveitis, the epithelioid cells agents such as hydrogen peroxide, hypochlorous acid represent modifiedmacrophages displaying primarily and hydroxyl radicals.14 Nitric oxide, another mole­ the morphological features of secretory functions. It cule released by the activated macrophages,
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