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Choroidal and Adnexal Extranodal Marginal Zone B-Cell Eye (2013) 27, 828–835 & 2013 Macmillan Publishers Limited All rights reserved 0950-222X/13 www.nature.com/eye 1 2 1 CLINICAL STUDY Choroidal and P Loriaut , F Charlotte , B Bodaghi , D Decaudin3, V Leblond4, C Fardeau1, adnexal extranodal L Desjardins5, P Lehoang1 and N Cassoux5 marginal zone B-cell lymphoma: presentation, imaging findings, and therapeutic management in a series of nine cases Abstract Purpose To describe the clinical and Eye (2013) 27, 828–835; doi:10.1038/eye.2013.74; imaging presentation, pitfalls in the published online 19 April 2013 1Department of Ophthalmology, diagnosis of choroidal extranodal marginal Pitie´ -Salpe´ trie` re Hospital, zone B-cell lymphoma of mucosa-associated Keywords: choroid; extranodal marginal zone Paris, France lymphoid tissue (MALT), as well as the B-cell lymphoma of mucosa-associated therapeutic management and prognosis. lymphoid tissue; MALT 2 Department of Pathology, Methods A retrospective case review of nine Pitie´ -Salpe´ trie` re Hospital, Paris, France choroidal MALT lymphomas was performed. Initial clinical presentation and imaging Introduction 3Department of findings of these histologically confirmed Non-Hodgkin lymphoma (NHL) is a general Hematology, Institut Curie cases of lymphoma were analyzed. Treatment term for a large group of malignancies of Paris, Paris, France methods, time to diagnosis, systemic work- lymphoid tissue. Although it usually affects the up, and treatment prognosis were assessed. lymphatic system, extranodal sites are common 4Department of Hematology, Results Initial presentation was essentially and may involve almost all tissues. Although Pitie´ -Salpe´ trie` re Hospital, blurred vision. The features described on lymphoma of the ocular region is a relatively Paris, France examination were: anterior and posterior rare condition, NHL is the most common type scleritis, iridocyclitis, choroidal infiltration, and typically involves mucosa-associated 5 Department of Ophthalmic and exudative retinal detachment. lymphoid tissue (MALT). MALT lymphoma Oncology, Institut Curie, Fluorescein and indocyanine green usually involves the conjunctiva, lacrimal Paris, France angiography as well as ultrasonography and gland, and orbit, but intraocular choroidal Correspondence: optic coherence tomography provided involvement is rare and has rarely been P Loriaut, Department of arguments in favor of the diagnosis. Biopsy reported. As the initial presentation is Ophthalmology, Pitie´ - sites included conjunctiva, Tenon’s capsule, frequently nonspecific and insidious,1–3 this Salpe´ trie` re Hospital, deep scleral tissue, episclera, lacrimal gland, form of MALT lymphoma is particularly ˆ 47-83 bd de l’hopital, and choroid. Treatment mostly consisted difficult to diagnose and treat. Based on a better 75013 Paris, France Tel: +33 7 6055 5115; of a combination of chemotherapy and knowledge of this condition, clinicians may be Fax: +33 1 4216 3203; radiotherapy. The mean time to diagnosis able to recognize this disease at an early stage, E-mail: patrickloriaut@ was 12 months. at which treatment may prevent systemic hotmail.com Conclusions Owing to the insidious onset dissemination of the disease or transformation of these tumors and their ability to simulate into a more aggressive lymphoma.4–6 In this Received: 1 June 2012 other conditions, the diagnosis is commonly study, we report the clinical findings, medical Accepted in revised form: 7 March 2013 delayed. The prognosis is generally good imaging, and therapeutic management of Published online: 19 April and treatment is effective in the case of nine patients with a histologically confirmed 2013 localized lymphoma. diagnosis of choroidal MALT lymphoma. Choroidal MALT lymphoma P Loriaut et al 829 Patients and methods patients. Two patients had bilateral eye involvement. Mean initial visual acuity was 20/50. Mean final acuity This study is a retrospective case review of nine was 20/50. Nine patients presented progressive painless consecutive patients with choroidal MALT lymphoma. visual impairment and one patient reported isolated All patients were seen in a referral center between 1998 retrobulbar headache. Other symptoms included and 2010. Patients’ medical records were reviewed for metamorphopsia and floaters. Clinical findings are the following inclusion criteria: histologically confirmed summarized in Table 1. Examination of the anterior diagnosis of MALT lymphoma, primary choroidal segment revealed chemosis in two patients and involvement. Evidence of MALT lymphoma was iridocyclitis with pseudohypopyon in two other patients. based on a set of arguments such as morphology, One eye had features of anterior scleritis. In one patient, immunohistochemistry, and molecular biology. the initial presentation also included red eye and Choroidal involvement was documented clinically and epiphora. All nine patients had choroidal infiltrates on ultrasonography and fluorescein angiography. on fundus examination (Figure 1). The other features on All patients were referred to our center after failure of initial examination were: exudative retinal detachment first-line medical management. The following data (three cases), choroidal thickening (three cases), macular were collected for each patient: age, gender, general choroidal neovascularization (one case), optic disc comorbidity, presenting clinical features, initial treatment swelling (two cases), and venous stasis retinopathy (one method and investigations, visual acuity testing, case). slit-lamp and fundus examination, medical or surgical All patients underwent fluorescein angiography, interventions, and locoregional and systemic staging which confirmed fundus examination findings in every assessment. Pathological examination included case (Figures 1 and 2). On fluorescein angiography, biopsy, grading, and classification of the lymphoma, patients typically had localized or diffuse thickening of conventional histology, immunohistochemistry, and PCR the choroid with heterogeneous hyperfluorescence and for immunoglobulin light chain gene rearrangement. alterations or migrations of retinal pigment epithelium The time to diagnosis was defined as the time elapsed (tiger-like pattern). These choroidal lesions remained between onset of symptoms and histological diagnosis of hypofluorescent on ICG angiography. The eye with the marginal zone lymphoma. At final follow-up, remission venous stasis retinopathy was confused with extrinsic status, relapse, and survival were assessed. Disease was compression. B-scan ultrasonography was performed in considered resolved when patients did not present any all cases and showed diffuse, irregular scleral thickening, recurrence of initial features or any other lymphoma site isoechoic to normal choroid, possibly associated with (or systemic spread) at last follow-up, corresponding swelling of Tenon’s capsule and conjunctiva (2/10) to criteria of complete remission. (Figure 2). These features were confirmed by orbital MRI, showing a hyperintense area of thickened choroid with mild gadolinium enhancement. Detailed angiographic Results findings are summarized in Table 2. Two patients Nine patients (11 eyes) with choroidal MALT lymphoma underwent extensive laboratory and imaging were identified. Mean age at presentation was 56 years investigations (that gave negative results) for suspicion (median, 54 years; range: 40–73 years). Mean follow-up of acute uveitis. They were subsequently treated with was 74.2 months (median 60 months; range: 6–156 topical and systemic corticosteroids, with only temporary months). Follow-up was longer than 5 years for five improvement of visual acuity. Complementary Table 1 Demographic data and clinical findings Age Follow-up Diagnosis Case (years) Sex (months) Symptoms Examination findings Initial VA Final VA delay (months) 1 73 F 6 BV, metamorphopsia Chemosis, SRD 20/32 20/50 9 2 46 M 84 BV, floaters CI, white dots 20/100 20/32 2 3 63 M 60 BV CI, ERD 20/125 20/100 18 4 54 F 144 BV, headache CI, SRD 20/32 20/50 6 5 64 F 12 BV Chemosis, pseudo-hypopion, CI 20/4000 LP 12 6 54 F 120 BV CI, optic disc swelling 20/40 20/32 24 7 40 M 156 BV, red eye, epiphora Anterior uveitis, anterior scleritis, CI 20/25 20/20 18 8 53 F 53 BV ERD, CI 20/200 NLP 3 9 57 M 33 BV Optic disc swelling, stasis retinopathy, 20/63 20/40 17 uveal effusion, SRD Abbreviations: BV, blurred vision; CI, choroidal infiltration; ERD, exsudative retinal detachment; LP, light perception; NLP, no light perception; SRD, serous retinal detachment; VA, visual acuity. Eye Choroidal MALT lymphoma P Loriaut et al 830 Figure 1 Fundus photography of bilateral choroidal involvement of choroidal MALT lymphoma. In the left eye (upper left): posterior choroidal infiltration. In right the eye (upper right): exsudative retinal detachment with peripheral cream-colored choroidal infiltrates. On the bottom left, green-light fundus photography of choroidal infiltrates; on the bottom right, same eye fluorescein angiography (1 : 02) showing the same features. investigations in one patient in this series with systemic chemotherapy in three patients. Chemotherapy metamorphopsia and vision loss showed features protocols used various combinations of drugs, mostly of unilateral macular choroidal neovascularization associated with rituximab. These protocols are reported (Figure 3). The initial diagnosis was that of age-related in Table 3. Patients were treated with 30 Gy of irradiation macular degeneration and the patient underwent in 1.5 Gy fractions over 4 weeks. repeated intravitreal anti-VEGF therapy. Persistent complete
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