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Normal EOG in BD and ARB

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Normal EOG in BD and ARB Normal Electrooculography in Best Disease and Autosomal Recessive Bestrophinopathy Abbreviated Title: Normal EOG in BD and ARB Kamron N Khan, PhD, FRCOphth1-3 Farrah Islam, FCPS, FRCS.2 Graham E Holder,PhD1,2 Anthony Robson,PhD1,2 Andrew R Webster, MD(Res) , FRCOphth1,2 Anthony T Moore, FRCS, FRCOPhth1,2,4 Michel Michaelides, MD(Res), FRCOphth1,2 1. University College London Institute of Ophthalmology, University College London, London, UK. 2. Medical Retina Service, Moorfields Eye Hospital, London, UK. 3. Department of Ophthalmology, Leeds Institute of Molecular Medicine, St James' University Hospital, Beckett St, Leeds, UK. 4. Ophthalmology Department, University of California San Francisco Medical School, San Francisco, California, USA. Corresponding authors: Kamron Khan and Michel Michaelides at address 1 above. Email: [email protected] and [email protected] Grants/ Financial Disclosure: National Institute for Health Research Biomedical Research Centre at Moorfields Eye Hospital National Health Service Foundation Trust and UCL Institute of Ophthalmology (UK; KNK, ARW, ATM, MM), Fight For Sight (UK; ARW, MM, OAM), Moorfields Eye Hospital Special Trustees (UK; MM), the Foundation Fighting Blindness (FFB, USA; ARW, ATM, MM), Retinitis Pigmentosa Fighting Blindness (UK; ARW, ATM, MM), and the Wellcome Trust (099173/Z/12/Z; ARW, MM). Michel Michaelides is supported by an FFB Career Development Award. This research has been funded/supported by the National Institute for Health Research Rare Diseases Translational Research Collaboration (NIHR RD-TRC). The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR or the Department of Health.” 1 Proprietary Interest : None CONFLICT OF INTEREST: No conflicting relationship exists for any of the authors. KEY WORDS Autosomal Recessive Best Retinopathy. Best related Retinopathy. Electrooculography. Retina. Retinal dystrophy. SUMMARY STATEMENT The Bestrophinopathies are a group of inherited eye disorders that arise from either dominant or recessive mutations in the BEST1 gene. Electrooculography is invaluable in the diagnosis of Best disease (BD) and autosomal recessive bestrophinopathy (ARB), as a reduced Arden ratio is a highly penetrant feature of disease. We demonstrate that EOG phenotype in BD and ARB is more variable than currently appreciated. 2 Normal Electrooculography in Best Disease and Autosomal Recessive Bestrophinopathy Abstract Purpose: To evaluate the electrooculogram (EOG) in a large series of patients with Best disease (BD) and autosomal recessive Bestrophinopathy (ARB). Methods: A retrospective review of consecutive cases at Moorfields Eye Hospital, London, United Kingdom. Patients with BD or ARB who, after electrophysiological testing, had a normal or atypical EOG light rise were identified. Main outcome measure was EOG amplitude, clinical phenotype and genotype. Results: 113 patients were identified with likely disease-causing sequence variants in BEST1 (99 BD, 14 ARB). EOGs had been performed in 75 patients. 20 patients (27%) had no detectable light rise (Arden ratio of 100%) and 49 (65%) had Arden ratios of between 100-165%. Six patients (8%) were found to have an EOG light rise of >165%. No cases demonstrated significant interocular asymmetry in EOG amplitude. Conclusions: The current work provides significant clinical evidence that the EOG phenotype in BD and ARB is more variable than currently appreciated. As a normal EOG may occur in the presence of a classical fundus appearance, the consequences of BEST1 mutation may be independently expressed, possibly mediated via differential effects on intracellular calcium homeostasis. 3 Normal Electrooculography in Best Disease and Autosomal Recessive Bestrophinopathy Introduction The Bestrophinopathies are a group of inherited eye disorders that arise from either dominant or recessive mutations in the BEST1 gene. The clinical spectrum of disorders include (i) diseases predominantly affecting the macula - Best disease (BD) and Adult Vitelliform Macular Dystrophy (AVMD); (ii) generalised retinal involvement - Autosomal Dominant Vitreoretinochoroidopathy (ADVIRC) and Retinitis Pigmentosa (RP); and (iii) diseases with retinal and anterior segment involvement – autosomal recessive Bestrophinopathy (ARB) and Microcornea, Rod-cone dystrophy, Cataract and posterior Staphyloma (MRCS).1-7 In addition to the phenotypic heterogeneity some of the bestrophinopathies display significant variation in penetrance of the clinical phenotype.8 However, one endophenotype, the absent or reduced electrooculogram (EOG) light rise, is reported to be almost fully penetrant.9 This electrophysiological parameter arises as the cornea is positively charged relative to the negative retina thus creating a dipole through the eye that can be measured with surface electrodes. The light rise reflects a progressive depolarisation of the basal membrane of the retinal pigment epithelium (RPE) in response to a change from scotopic to photopic adaptation. Although the underlying molecular basis for the change in EOG with illumination is not known, it is almost always reduced in patients with BEST1 mutations. The present report investigates the EOG findings in a large cohort of patients with BD and ARB. Methods A retrospective review of the genetic database at Moorfields Eye Hospital, London, United Kingdom was undertaken to identify all patients with either bi-allelic or heterozygous mutations in BEST1 and a compatible clinical phenotype. Within this group only those who had undergone electrophysiological testing at our own institution were investigated further. Patients with a normal or atypical EOG light rise were then identified. 4 The EOG testing was performed to be consistent with ISCEV standards.10 Normative EOG data were obtained by testing 30 individuals aged between 30 and 60 years of age with no known ocular abnormalities. One eye from each normal subject was randomly selected and used to establish the normative data. In brief, EOG testing was performed with surface electrodes placed at the medial and lateral canthi of each eye. Thirty degree eye movements were recorded for 10 seconds of each minute during 15 minutes of dark adaptation, followed by a further 10–15 minutes in full-field (Ganzfeld) light adaptation (100 cd/m2). The amplitudes of the light peak and dark trough were directly measured and the light peak:dark trough ratio expressed as a percentage. Pattern electroretinograms (PERGs) and full-field ERGs (FFERGs) were used to assess macular function and generalised retinal function respectively.11, 12 All clinical electrophysiological assessments were analysed by one of two consultant electrophysiologists (GH or AR) masked to the molecular diagnosis. A clinical diagnosis was made based on the fundoscopic appearance together with findings on optical coherence tomography (OCT) and fundus autofluorescence (FAF) (excitation wavelength 488 nm; Spectralis, Heidelberg Engineering, Heidelberg, Germany). A genetic diagnosis was determined by DNA sequencing (Manchester Regional Genetics Laboratory). Genomic DNA was extracted from peripheral blood (Qiagen Blood DNA extraction kit, Qiagen, Crawley, UK) and used as the template for bidirectional Sanger sequencing analysis of the entire coding regions of BEST1, including the splice donor and acceptor sites. Results The EOG Arden ratios in the normal subjects ranged from 180% to 435% (median 267%, SD 50% n=30). For this study we considered an Arden ratio of less than 165% to be abnormal (2SD below the mean). 5 A total of 113 patients were identified with likely disease-causing sequence variants in BEST1 (99 BD, 14 ARB). Electrophysiological testing had been performed in 75 patients. Three groups were identified. 20 patients (27%) had no detectable light rise (Arden ratio of 100%), whilst 49 cases (65%) had Arden ratios of between 100-165%. Six patients (8%) were found to have an EOG light rise of >165% and will be described in detail below. No cases were identified with sufficient asymmetry in Arden ratios to cause eyes of the same patient to be categorised differently. Patient 1 was diagnosed with BD aged 8 based on bilateral typical macular vitelliform lesions. He later presented with reduced vision in his right eye due to macular scarring from a presumed occult choroidal neovascular membrane and underwent EOG testing aged 39. Arden ratios were 220% right and 180% left. FFERGs were normal and symmetrical, indicating no evidence of generalised retinal dysfunction. PERG P50 component was mildly subnormal on the right consistent with mild right macular dysfunction. The diagnosis of BD was thereby questioned and PRPH2 gene screening was initiated but no pathogenic variants were identified. BEST1 screening revealed a heterozygous missense amino-acid substitution (p.Arg25Trp) previously associated with BD.13 Patient 2 was diagnosed with BD as a teenager when her vision deteriorated in both eyes. The diagnosis was questioned when she was seen between the ages of 28-36 due to an atypical macular appearance. OCT imaging demonstrated focal choroidal excavation alongside subretinal deposit and fluid. The FFERG was normal, but the PERG P50 component was reduced, left more than right in keeping with macular dysfunction. Eye movement artefacts disrupted accurate grading of the EOG but an adequate light rise and dark trough were noted, consequently this patient was reported to have a normal EOG and included in this cohort. Screening BEST1 identified the variant p.Lys30Asn,
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