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Uveitic Macular Edema C Fardeau, E Champion, N Massamba and REVIEW P Lehoang

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Uveitic Macular Edema C Fardeau, E Champion, N Massamba and REVIEW P Lehoang Eye (2016) 30, 1277–1292 © 2016 Macmillan Publishers Limited, part of Springer Nature. All rights reserved 0950-222X/16 www.nature.com/eye Uveitic macular edema C Fardeau, E Champion, N Massamba and REVIEW P LeHoang Abstract Macular edema (ME) may complicate anterior, etiologies. Uveitis is the fifth leading cause of intermediate, and posterior uveitis, which may visual impairment in developed countries and be because of various infectious, neoplastic or responsible for about 20% of legal blindness.1,2 autoimmune etiologies. BRB breakdown is ME is the main condition associated with vision involved in the pathogenesis of Uveitic ME loss in uveitis, decreasing the visual acuity (VA) (UME). Optical coherence tomography has to o20/40 in about one-third of posterior uveitis become a standard tool to confirm the diag- patients.3,4 Panuveitis and intermediate uveitis nosis of macular thickening, due to its non- usually occur in conjunction with ME, with an invasive, reproducible, and sensitive features. incidence of 66% and 65%, respectively.4 fl Retinal uorescein and indocyanine green The most common known causes of Uveitis angiography is helpful to study the macula and Macular Edema (UME) are HLA B27 positive screen for associated vasculitis, detect ischemic anterior uveitis, juvenile idiopathic arthritis, areas and preretinal, prepapillary or choroidal intermediate uveitis due to sarcoidosis, multiple neovascular complications, and it may provide sclerosis, and pars-planitis, infections, posterior information about the etiology and be needed uveitis due to systemic diseases such as to assess the therapeutic response. UME due to sarcoidosis, Behcet's disease, or due to intra- fi an infection or neoplastic in ltration may ocular dysimmunity such as Irvine Gass fi require a speci c treatment. If it remains syndrome post-cataract surgery, Birdshot persistent or occurs in other etiologies, immu- retinochoroidopathy (retinal vasculitis and nomodulatory treatments may be needed. depigmented choroiditis associated with Intravitreal, subconjunctival, or subtenon cor- HLA-A29), sympathic ophthalmia, and ticosteroids are widely used. Their local use is Department of infectious retinitis.5 Ophthalmology, Reference contraindicated in glaucoma patients and lim- ME is a significant risk factor for visual loss in Centre for Rare Diseases, ited by their short-lasting action. In case of uveitis: it has indeed been shown that 45% of Hôpital Pitié-Salpêtrière, bilateral sight-threatening chronic posterior University Hospital patients with posterior uveitis presented with a uveitis, systemic treatments are usually Department of Vision and decrease in VA, and 28% of them also had needed, and corticosteroids are used as the Disability, Pierre and Marie a ME.4 Curie University, Paris VI, standard first-line therapy. In order to reduce Therefore in posterior uveitis, ME is the most 47-83 Boulevard de the daily steroid dose, immunosuppressive or common complication and the main cause of l'Hôpital, Paris, France immunomodulatory agents may be added, decreased VA. For example in Birdshot some of them being now available intravitre- Correspondence: retinochoriopathy, a 5-year cumulative incidence ally. Ongoing prospective studies are assessing Dr C Fardeau, Department of cystoid ME (CME) of 50% has been shown in biotherapies and immunomodulators to deter- of Ophthalmology, eyes free of CME at baseline.6 Reference Centre for Rare mine their safety and efficacy in this indication. When uveitis and ME are associated, the Diseases, Hôpital Pitié- Eye (2016) 30, 1277–1292; doi:10.1038/eye.2016.115; Salpêtrière, University visual prognosis depends on the status of the published online 3 June 2016 Hospital Department of outer retinal layers, and uveitis duration, type, Vision and Disability, Pierre and etiology. A low VA (o20/60) has been and Marie Curie University, found respectively in 64% and 28% of cases of Paris, 75013, France Introduction Tel: +0033142163207; panuveitis and intermediate uveitis alone, and Fax: +0033142163218. Macular edema (ME) is characterized by a respectively 59% and 85% of them also had E-mail: christine.fardeau@ retinal thickening in the macular area due to the a ME.4 aphp.fr breakdown of the blood-retinal barrier (BRB). UME secondary to anterior and intermediate Extracellular fluid accumulates in the intraretinal uveitis can benefit from an early management Received: 23 September area or collects in the subretinal space. including work-up and efficient treatment in 2015 Accepted in revised form: Inflammatory ME may complicate anterior, secondary care center. Chronic, bilateral UME 23 April 2016 intermediate or posterior uveitis that may be due associated with posterior uveitis usually needs a Published online: to various infectious, neoplastic, or autoimmune step-wise approach with immunosuppressive 3 June 2016 Uveitic macular edema C Fardeau et al 1278 therapy, which may be best managed easily in a tertiary perfusion, while the retinal vessels used to remain intact care center. as shown using retinal angiography.13 The BRB integrity also depends on other retinal cell types. On one hand, Müller cells, the main type of retinal Pathophysiology of UME glial cells, establish connections between the different The main cause of macular thickening in inflammatory retinal cell layers and have multiple functions including conditions is inflammatory ME. However, other causes maintaining the homeostasis of the retinal extracellular can increase the macular thickness in ocular inflammation milieu through aquaporins and transmembrane condition, such as (1) inflammatory choroidal potassium channels (Kir). The latter are located on cell vascularization, (2) vitreo-macular traction by interdigitations in the inner retina around retinal inflammatory epiretinal membrane, (3) contiguity with capillaries that allow water and potassium transfer to the papillary edema, (4) central serous chorioretinopathy retinal capillaries. Changes in potassium transport lead to exacerbated by the use of steroid therapy. neuronal hyperexcitability and edema. Müller cells also Inflammatory ME is due to breakdown of the BRB.The have a neuroprotective role through the release of BRB is mainly formed of tight junctions between neurotrophic factors, glutamate uptake and degradation, endothelial cells of non-fenestrated capillaries and retinal synthesis of the antioxidant glutathione. They release pigment epithelial (RPE) cells. Tight junction proteins immunomodulatory cytokines including interleukins include zonula occludens, occludins, and VE-cadherins. (ILs)-1, -13, -4, and -10 which are involved in retinal At the level of retinal capillary endothelium, the inner homeostasis. However, activated Müller cells may also BRB breakdown may be due to many factors including synthesize pro-inflammatory cytokines. Moreover, Müller vascular endothelium growth factor (VEGF), a signal cell dysfunction impairs glutamate catabolism and protein produced by cells stimulating vasculogenesis and dysregulate ion homeostasis, contributing to the angiogenesis that is extensively produced by Müller cells. development of a retinal edema and neuronal death. VEGF modulates occludin and VE-cadherin adhesion and On the other hand, the inner and outer plexiform layers expression; its interaction with its receptor induces a of the retina contain numerous synaptic vesicles and are cascade of intracellular phosphorylations causing the composed of bipolar, ganglion, and amacrine cells that degradation of tight junction proteins. Occludin and are involved in the BRB function. cadherin phosphorylation, induced by pro-inflammatory cytokines and metalloproteinases secreted by leukocytes, Imaging in UME promotes leukocyte migration through intact capillary walls into surrounding body tissue. Diapedesis is a Diagnosis is usually made based on imaging examination. chemotactic process corresponding to the migration of Functional signs usually include a drop in near VA; a leukocyte toward the retinal tissue and involving their macular syndrome may be associated with a type of adhesion to the activated endothelium, through the micropsia, metamorphopsia, and positive relative expression of various adhesion proteins, including scotoma or blurred vision like looking through a water selectins and ICAM-1 and a conformational change in drop. The visual loss may be highly variable, but in cases integrin.7,8 with chronic degeneration of the outer retina, the visual Factors other than VEGF promoting the BRB effects may be significant. When an acute macular breakdown include pro-inflammatory cytokines such as ischemia is associated, like in Behcet's disease, the TNF-α, IL-1, TGF-β, angiotensin II, as well as adenosine, decrease in VA may persist despite appropriate histamine, and glucose.7,8 Increased levels of IL-6 and IL-8 emergency treatment administration. have been found in the aqueous humor of patients with Optical coherence tomography (OCT) is the gold intermediate uveitis.9 standard technique for the diagnosis of ME, regardless of At the level of RPE, the outer layer of the BRB, the its etiology, since it is non-invasive, reproducible, and adhesion between photoreceptors and the RPE is sensitive. It accurately quantifies the retinal macular maintained through active transport mechanisms, mainly thickness using mapping, may show fluid accumulation from the trans-epithelial space to the extraretinal space. either at the inner (Figures 1 and 2) or outer plexiform That could be damaged in acute inflammatory conditions layer (Figure 3), a non-uniform
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