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Multifocal Electroretinography Changes at the 1-Year Follow-Up in a Cohort of Diabetic Macular Edema Patients Treated with Ranib

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Multifocal Electroretinography Changes at the 1-Year Follow-Up in a Cohort of Diabetic Macular Edema Patients Treated with Ranib Doc Ophthalmol (2017) 135:85–96 DOI 10.1007/s10633-017-9601-2 ORIGINAL RESEARCH ARTICLE Multifocal electroretinography changes at the 1-year follow- up in a cohort of diabetic macular edema patients treated with ranibizumab Marc Baget-Bernaldiz . Pedro Romero-Aroca . Angel Bautista-Perez . Joaquin Mercado Received: 14 November 2016 / Accepted: 11 July 2017 / Published online: 4 August 2017 Ó The Author(s) 2017. This article is an open access publication Abstract response density and the best-corrected visual acuity Purpose To determine the changes in the multifocal (BCVA). electroretinogram (mfERG) at 1 year in a clinical series Results Eyes with cystic and spongiform DME of diabetic macular edema (DME) patients treated with showed better response density with respect to the ranibizumab (RNBZ) using a pro re nata protocol. serous type (p \ 0.001) at baseline. Similarly, eyes Methods We analyzed a clinical series of 35 eyes of with high IS/OS and ELM preservation rates showed 35 patients with DME at baseline and after treating higher initial response density compared to the others them with RNBZ over 1 year, in order to determine (p \ 0.001). Eyes with moderate DR had better the change in the macular function, which was response density compared to those with severe and assessed by means of the response density and the proliferative DR (p = 0.001). At the beginning of the implicit time of the first-order kernel (FOK) P1 wave study, those eyes with proliferative and severe DR of the mfERG at the foveola (R1), fovea (R2) and showed longer implicit times with respect to those parafovea (R3). These electrophysiological parame- with moderate DR (p = 0.04). The response density ters were studied taking into account different inde- significantly increased in eyes that anatomically pendent variables, such as DME type, degree of restored the IS/OS and the ELM after being treated diabetic retinopathy (DR), level of preservation of with RNBZ (both p \ 0.001). Similarly, eyes with both the ellipsoid zone (IS/OS) and the external spongiform DME further improved the response limiting membrane (ELM) and changes in central density with respect to those with cystic and serous retinal thickness (CRT) and total macular volume DME (p \ 0.001). On the contrary, eyes with hard (TMV). We also studied the relationship between the exudates showed less improvement in their response density at the end of the study (p \ 0.001). We observed a significant relationship between BCVA M. Baget-Bernaldiz Á P. Romero-Aroca (&) Á and the response density achieved at the end of the A. Bautista-Perez Á J. Mercado study (p = 0.012). Eyes with severe and proliferative Ophthalmic Service, University Hospital Sant Joan, Reus, DR significantly shortened implicit time compared to Spain e-mail: [email protected]; those with moderate DR (p = 0.04). [email protected] Conclusions The multifocal electroretinogram allowed us to differentiate groups of eyes with DME M. Baget-Bernaldiz Á P. Romero-Aroca Á according to their electrophysiological profile, both A. Bautista-Perez Á J. Mercado Institut de Investigacio Sanitaria Pere Virgili [IISPV], initially and after being treated with RNBZ. Ranibi- University Rovira and Virgili, Tarragona, Spain zumab increased the response density in all DME 123 86 Doc Ophthalmol (2017) 135:85–96 types included in the study, with a maximum response The aim of this study was to evaluate the macular in those eyes with spongiform type. Once treated with functional status using the mfERG in a population of RNBZ, the macular electrophysiological activity type 2 diabetic patients with DME over a 1-year improved in eyes that had a well-preserved ellipsoid follow-up of treatment with RNBZ. We believe that zone and ELM. The presence of hard exudates was a this study will increase our understanding of certain limitation to the response density achieved at the physiological mechanisms involved in the clinical foveola. response to RNBZ by determining the electrophysio- logical response of the macula. Keywords Multifocal electroretinogram Á Retinal density of response Á Implicit time Á Diabetic macular edema Á Diabetic retinopathy Á Ellipsoid zone Á Methods External limiting membrane Á Central retinal thickness Á Total macular volume Study design A prospective clinical study was conducted from Introduction January 1, 2014, to December 31, 2014, including a total of 35 eyes of 35 Caucasian patients with DME. Diabetic macular edema (DME) is the leading cause of visual acuity loss in diabetic patients [1]. Clinical Ethical adherence manifestations include the presence of fluid or lipids (hard exudates) in the macula, with an increase in its This study was conducted in accordance with local volume and thickness. legal requirements (the local ethics committee of Optical coherence tomography (OCT) is the tech- Hospital Universitari Sant Joan de Reus, approval no. nique most often used during follow-up for DME and 11-05-26/proj5), and with the revised guidelines of the helps to determine the need for continued treatment. Declaration of Helsinki. Informed consent was There are different pathophysiological mechanisms obtained from all participants in the study. involved in the genesis of DME. Several studies have emphasized the role of vascular endothelial growth factor (VEGF) after having observed an increase in its Power of the study levels in the vitreous of patients with diabetic retinopathy (DR). It increases the retinal vascular We estimate the detection of a 95% increase in risk permeability that can lead to DME [2]. Currently, the with an accuracy interval of 3%. The calculations were majority of treatments for DME target VEGF to block based on the consideration of variables involving two its action. Ranibizumab (RNBZ) is a selective anti- possible random errors in their determination. VEGF drug used in this treatment. Several studies 1. Response density of the FOK P1 wave: to allow have demonstrated its safety and efficacy in the for technical mistakes, a possible error was treatment of this disease [3, 4]. considered of 20 nanovolts per degree squared Multifocal electroretinography (mfERG) is a non- (nV/deg2) for every ring studied. invasive test that allows us to assess the functional 2. Error in measuring the thickness of the retina with status of the macula. Patients must fix their eyes on the optical coherence tomography (OCT), with a central part of the monitor, and the macula is sampling error of 5 microns, was considered due stimulated by a sequence of scaled hexagonal flashes to possible failure of the technique used. of light projected onto it. The matrices most com- monly used in clinical practice are 103 and 61 hexagons. In our study, we chose the latter, aiming Inclusion criteria to shorten the scanning time and thus minimize artifacts due to patient fatigue. The mfERG is taken Type 2 DM patients with naı¨ve DME diagnosed as under conditions of light adaptation in order to obtain clinically significant macular edema with foveal an electrophysiological response from the cones [5]. center involvement [6]. 123 Doc Ophthalmol (2017) 135:85–96 87 Exclusion criteria hexagonal matrix of 61 flicker lights, transitioning from white to dark in high frequency (75 Hz); this pattern of stimulation was presented under photopic • Patients with type 1 DM conditions to achieve electrophysiological responses • Patients with cataracts or other opacities of the cone and bipolar cells. The correct fixation of • Patients with uncontrolled glaucoma or previous each tested eye was monitored by external ocular surgery observation. • Patients with tractional DME The basic mfERG response includes a first negative • Patients with macular ischemia wave (N1) followed by a positive wave (P1). The set of • Patients with previous nephropathy, stroke or N1–P1 biphasic waveforms is known as the first-order myocardial infarction kernel (FOK) or first-order response [10]. The two electrophysiological variables selected in Methods our study to assess the electrophysiological responses at the foveola, fovea and parafovea were the response Diabetic macular edema was diagnosed by a retina density and the implicit time of the P1 wave of the specialist in the Ophthalmology service. All exami- first-order kernel (FOK). The first ring (R1) corre- nations were made at baseline, at 6 and at 12 months sponds to 0° to 2° of the visual field (foveola), the of follow-up and included BCVA, biomicroscopy, second ring (R2) corresponds to 2° to 5° of the visual fluorescein angiography (FA), optical coherence field (fovea), and the third (R3) corresponds to 5° to tomography (OCT) and multifocal electroretinogra- 10° of the visual field (parafovea). phy (mfERG). The response density is the amplitude achieved per OCT was taken using a TOPCON 3D OCT-2000, unit of area measured in nanovolts per square degree and we determined the central retinal thickness (CRT), (nV/deg2). It quantifies the amplitude obtained in each the total macular volume (TMV), the level of preser- ring, considering its size. It is at its maximum at the vation of both the inner segment/outer segment foveola since that is the macular region with the (ellipsoid zone) and the external limiting membrane highest cone density, and decreases with the eccen- (ELM) and the presence of hard exudates (HE) in the tricity because the cone density is reduced by the same fovea. proportion. The implicit time is the time it takes to We evaluated quantitatively both the ellipsoid zone reach the maximum amplitude in every macular region and the ELM by measuring the traceable segments for studied. each layer in the fovea. Both layers were classified for These three rings are affected by DME and are each eye as having high, medium or low preservation responsible for the changes in BCVA. rate. The level of preservation for each layer was high Normal electrophysiological values in the present when it could be measured between 66 and 100% of study are: their length (1000–1500 microns), medium if it was Response density: between 33 and 66% (500–1000 microns) and low if it was less than 33% (\500 microns) [7].
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