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Vogt–Koyanagi–Harada Syndrome: a Rheumatologic Perspective

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Vogt–Koyanagi–Harada Syndrome: a Rheumatologic Perspective REVIEW Vogt–Koyanagi–Harada syndrome: a rheumatologic perspective Vogt–Koyanagi–Harada (VKH) syndrome is an idiopathic systemic inflammatory disorder that affects various melanocyte-containing structures, including the eyes, meninges, inner ear and skin. It classically leads to bilateral chronic granulomatous diffuse uveitis, and its extraocular manifestation can include sensorineural hearing loss, meningitis, and cutaneous findings of vitiligo, poliosis (loss of hair pigment) and alopecia. Ethnicity/racial background and HLA genotype play a strong role in the pathogenesis of VKH syndrome. The inflammatory process is not completely understood, but recent studies have pointed to several potential autoantigen targets, and have also demonstrated the role IL-23 plays in inducing the differentiation of Th17 cells and the subsequent production of IL-17. The success in preserving the vision of VKH syndrome patients hinges on early diagnosis and aggressive treatment that includes immunomodulatory therapy, and as a result ophthalmologists are increasingly referring such patients to rheumatologists for management. It is therefore necessary for the rheumatologists to be familiar with VKH syndrome and its clinical aspects and management. Although the role of biologics in the treatment of VKH syndrome has yet to be investigated, it is possible that such treatments may prove beneficial, given what is currently known about the pathogenesis of the disease. 1 KEYWORDS: ankylosing spondylitis n chorioretinitis n HLA-DRB1*04 n IL-23 Jonathan Lipps & n immunomodulatory therapy n poliosis n sensorineural hearing n Th17 lymphocytes Muhammad Asim Khan2,† n uveitis n vitiligo n Vogt–Koyanagi–Harada syndrome †Author for correspondence 1Ohio State University College The increasingly close collaboration between Vogt–Koyanagi–Harada syndrome is an idio- of Medicine, Columbus, ophthalmologists and rheumatologists is greatly pathic systemic inflammatory disease that was OH, USA 2 aiding the early diagnosis and more effective reported in the early 20th Century [6], although Case Western Reserve interdisciplinary management of patients it was first described in the 10th Century by University, MetroHealth with inflammatory eye involvement associ- the famous Arab scientist and ophthalmologist Medical Center, Cleveland, ated with many multisystem diseases [1–3]. For Ali ibn Isa in his landmark textbook on oph- OH, USA example, occurrence of acute anterior uveitis thalmology, Notebook of the Oculists [7], and Fax: +1 216 778 8376 in patients with ankylosing spondylitis and later by another Arab physician, Mohammad [email protected] related spondylo arthropathies is more painful Al-Ghafiqi, in the 12th Century [6]. It is an and frightening for these patients than their autoimmune disorder of melanocyte proteins back pain and stiffness, so that most of them that occurs in genetically susceptible individu- will urgently seek ophthalmology consultation. als and affects various melanocyte-containing Ophthalmologists are increasingly referring structures, including the eyes, meninges, inner to rheumatologists those patients with acute ear and skin [5,8,9]. It classically leads to bilateral anterior uveitis who have rheumatological chronic granulomatous diffuse uveitis, sensori- complaints, especially the subset that possesses neural hearing loss, meningitis and cutaneous HLA-B27 [1,2]. Furthermore, they are also refer- findings of vitiligo, poliosis (loss of hair pigment) ring patients with many other forms of non- and alopecia [4,5,10,11]. infectious chronic ocular inflammation that require immunomodulatory therapy (IMT) Epidemiology owing to increasing reliance on rheumatologists The prevalence of VKH syndrome varies by for the management of such therapy [3]. ethnic/racial population groups, and is one of Vogt–Koyanagi–Harada (VKH) syndrome is the more common causes of chronic noninfec- one such disease that requires IMT for its optimal tious uveitis in some parts of the world [4,10–14]. management, and failure to do so portends a poor For example, it is the leading cause of nonin- prognosis [4,5]. It is therefore necessary for the rheu- fectious uveitis in Brazil [14], the second most matologists to be familiar with its clinical aspects, common cause in Saudi Arabia [10], and the pathogenesis and appropriate management. third most common cause of chronic uveitis 10.2217/IJR.10.2 © 2010 Future Medicine Ltd Int. J. Clin. Rheumatol. (2010) 5(2), 255–263 ISSN 1758-4272 255 REVIEW Lipps & Khan Vogt–Koyanagi–Harada syndrome: a rheumatologic perspective REVIEW (behind sarcoidosis and Behcet’s disease) in peptide (TRP)-1, TRP-2, gp100/PMel-17 and Japan, where it represents 6–9% of cases in uve- MART-1/MelanA, are some of the most studied itis clinics [12]. It tends to affect pigmented races in VKH syndrome pathogeneis [8,20–23]. Along (East and Southeast Asian and Middle Eastern with tyrosinase, which catalyzes the oxidation populations, as well as Hispanics and Native of tyrosine in the process of melanization, this Americans) more commonly than Caucasians protein family may be the leading candidate for of European descent, but the disease is rare autoantigen target in VKH syndrome. Studies among sub-Saharan Africans [9], indicating have demonstrated that T lymphocytes iso- that more is involved in the pathogenesis of the lated from the peripheral blood of VKH syn- disease than just the skin pigmentation. The drome patients show significant proliferation changing population demographics are result- when compared with those of healthy control ing in increasing incidence of VKH syndrome in subjects upon in vitro exposure to tyrosinase regions with higher percentages of Hispanic and family proteins [19]. Furthermore, Yamaki et al. Asian (including Middle Eastern) populations. have demonstrated that rats immunized with For example, a report indicates 7% prevalence TRP-1 and TRP-2 show both ocular inflam- of VKH syndrome at a uveitis tertiary refer- mation similar to that of humans afflicted with ral center in southern California versus 1–4% VKH syndrome, as well as histological changes prevalence nationwide [15]. The disease usually in the skin and meninges [20]. However, a subse- strikes between the third and fifth decades of life, quent ana lysis of microsatellite polymorphisms although there are also rare reports of its occur- in the tyrosinase gene family in 87 Japanese rence in children [16]. Familial cases are rare [17]. VKH syndrome patients and 122 healthy It is two-times more common in women than controls failed to show any increased risk men, although this trend does not appear to hold attributed to the gene family [21]. Other auto- true in Japan [4,18,19]. antigens, such as KU-MEL-1 [22] and Lens epithelium-derived growth factor [23], have Pathogenesis also been identified as possibly being involved Etiopathogenesis of VKH syndrome is not well in the pathogenesis of VKH syndrome via an understood; it tends to occur in genetically IgG-mediated process. susceptible individuals, but a trigger, which is Less is known about the trigger that leads as yet unknown, is needed to initiate a CD4+ to dysregulation of the immune system in the T cell-mediated autoimmune process against development of the disease. The leading hypoth- an unidentified autoantigen expressed in mela- esis is that exposure to a virus causes a T-cell nocytes [8,9,19–23]. A systemic inflammatory response against autoantigens by molecular cascade follows, affecting the meninges, uveal mimicry. The idea that VKH syndrome may tract, inner ear and epidermis. There is a strong have a viral trigger is not new, as it has long been association with HLA-DR4 [24], and in particu- noted that the first phase of VKH syndrome is lar the allele HLA-DRB1*0405 [14,25]. This allele often marked by a prodromal period suggestive codes for amino acid substitutions in the anti- of an acute viral infection. Epstein–Barr virus gen-binding groove, presumably affecting the DNA has previously been isolated from the vit- immune function of the antigen-presenting cells reous and cerebrospinal fluid (CSF) of patients + and their interaction with the cytotoxic CD4 with VKH syndrome [26,27], and a more recent T cells. The association with HLA-DR4 holds study by Sugita et al. showed that a cytomegalo- true for multiple ethnic/racial groups [14,18,25]; virus infection could produce T cells that cross- however, there is also a secondary association react with tyrosinase [28]. Also supporting the with other MHC class II alleles – most notably virus-as-trigger hypothesis are case reports of HLA-DR1 [14,24]. simultaneous onset of the disease in coworkers, Perhaps the most successful research into friends and neighbors, all of whom reported a the etiology of VKH syndrome to date is the flu-like prodromal phase [29]. work carried out in identifying an autoantigen The inflammatory cascade in VKH syndrome target. Logically, the identification of melano- has been described as being a CD4+ T cell- cytes as a potential target in VKH syndrome is dependent process within the environment of a consistent with both the cutaneous findings of T helper (Th)1 cytokine profile. Sakaguchiet al. vitiligo/poliosis in VKH syndrome patients and demonstrated that T-cell clones isolated from the the increased prevalence of the disease in more aqueous humor of VKH syndrome patients pro- heavily pigmented groups. Melanocyte differ- duced greater amounts of IL-6, IL-8 and IFN-g entiation proteins, such as tyrosinase-related when compared with T-cell clones from healthy 256 Int. J. Clin. Rheumatol. (2010) 5(2) future science group REVIEW Lipps & Khan Vogt–Koyanagi–Harada syndrome: a rheumatologic perspective REVIEW donor peripheral blood mononuclear cells [30]. dysacousia, vertigo and tinnitus are all typical Of major interest is the recent finding that findings [4,5,36–42]. Meningismus is the most IL-23, through its induction of the formation common of the extraocular signs, but indi- of IL-17-producing CD4+ T cells, is responsible vidual presentations of VKH syndrome vary for the autoimmune inflammatory response in greatly among individuals and ethnic groups. VKH syndrome [31].
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