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Long-Term Repeatability and Reproducibility of Phosphene Characteristics in Chronically Implanted Argus II Retinal Prosthesis Subjects

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Long-Term Repeatability and Reproducibility of Phosphene Characteristics in Chronically Implanted Argus II Retinal Prosthesis Subjects Long-term Repeatability and Reproducibility of Phosphene Characteristics in Chronically Implanted Argus II Retinal Prosthesis Subjects YVONNE H-L. LUO, JOE JIANGJIAN ZHONG, MONICA CLEMO, AND LYNDON DA CRUZ PURPOSE: Previously published literatures of acute (Second Sight Medical Products Inc., Sylmar, CA, USA) studies on few subjects have shown contradictory evi- retinal prosthesis system has been implanted in an dence on the reproducibility and characteristics of the increasing number of patients.1 However, despite this elicited phosphenes, despite using the same stimulating growing clinical use, data describing the features of artifi- parameters with epiretinal electrode arrays. In this study, cial vision perceived by the users remain scarce in the we set out to investigate the long-term repeatilibity and published literature.2–5 The idea of developing useful reproducibility of phosphenes in subjects chronically vision by epiretinal electrical stimulation hinges on the implanted with the Argus II retinal prosthesis (Second premise that stimulation with a single electrode gives rise Sight Medical Products, Inc., Sylmar, CA, USA). to a discrete focal percept in a retinotopic manner. DESIGN: Retrospective interventional case series and Simultaneous stimulation with multiple electrodes reliability study. therefore theoretically leads to perception of a pattern in METHODS: Six Argus II subjects of >5 years implanta- concordance with the pattern defined by the stimulating tion from a single site participated. The 4-electrode clus- electrodes.3 ter (‘‘quad’’) closest to fovea was stimulated in each In earlier studies, Rizzo and associates have called into subject with a fixed biphasic current. Perceived phos- question the consistency and reproducibility of phosphenes phenes were depicted relative to subjective visual field elicited by patterned epiretinal microelectrode stimula- center. The stimulus was applied at reducing time inter- tion.4 In a study involving 5 end-stage RP patients and 1 vals from 20 minutes to 1 second. Two sets of stimula- patient with normal retina, only 48% of the single- tions were performed on the same day and 2 further sets electrode stimulations and 32% of the multielectrode stim- repeated on a separate visit >1 week apart. ulations elicited visual percepts that matched the electrical RESULTS: Each subject depicted phosphenes of consis- stimulation patterns. Of the single-electrode stimulations, tent shapes and sizes, and reported seeing the same colors 3 subjects reported ‘‘a line’’ on some occasions, while ‘‘clus- with the fixed stimulating parameters, irrespective of the ters of 2 or 3 images’’ were seen on other occasions. In interstimuli intervals. However, there is a wide intersubject particular, the authors reported that only 66% (out of 99 variation in the phosphene characteristics. Four subjects stimulations) of the elicited visual percepts were reproduc- drew phosphenes in the same visual field quadrant, as ible in 3 RP patients on 2 separate trials, despite using the predicted by the quad-fovea location. Two subjects depicted same stimulating parameters to activate the same elec- phosphenes in the same hemifield as the expected locations. trodes. Such inconsistencies in the form and reproduc- CONCLUSION: Phosphenes for each subject were ibility of phosphenes would seriously undermine the consistently reproducible in all our chronically implanted formation of pixelated vision. subjects. This has important implications in the develop- In this study, we set out to investigate the consistency ment of long-term pixelated prosthetic vision for future and reproducibility of phosphenes elicited in a cohort of devices. (Am J Ophthalmol 2016;170:100–109. Ó subjects chronically implanted with the Argus II system 2016 Elsevier Inc. All rights reserved.) at a single site. All of the subjects described have had the device implanted and functioning for more than 5 years. INCE ENTERING THE COMMERCIAL MARKET AS A retinal prosthetic device for the treatment for end- Ò S stage retinitis pigmentosa (RP), the Argus II METHODS Accepted for publication Jul 20, 2016. SUBJECT INCLUSION/EXCLUSION CRITERIA: This is a From the NIHR Biomedical Research Centre for Ophthalmology (Y.H- L.L., J.J.Z., M.C., L.d.C.) and Vitreoretinal Service (Y.H-L.L., L.d.C.), single-center prospective study. All but 1 subject from Moorfields Eye Hospital NHS Foundation Trust, London, United our center implanted with the Argus II retinal pros- Kingdom. thesis system as part of the phase I/II clinical trial Inquiries to Yvonne H-L. Luo, NIHR Biomedical Research Centre for Ophthalmology, Moorfields Eye Hospital NHS Foundation Trust, 162 (clinicaltrials.gov identifier: NCT00407602) took part City Road, London EC1V 2PD, UK; e-mail: [email protected] in the study (n ¼ 6). One subject was excluded, as his 100 © 2016 ELSEVIER INC.ALL RIGHTS RESERVED. 0002-9394/$36.00 http://dx.doi.org/10.1016/j.ajo.2016.07.021 TABLE 1. Demographics and Operation Dates of the Participating Chronically Implanted Argus II Retinal Prosthesis Subjects Year of Age at Time of Subject ID Diagnosis Operation Operation (y) 001 Retinitis pigmentosa 2008 70 003 Retinitis pigmentosa 2008 72 005 Retinitis pigmentosa 2009 55 006 Choroideremia 2009 66 007 Retinitis pigmentosa 2009 63 009 Retinitis pigmentosa 2009 45 device ceased to function after he developed retinal detachment and thick macular pucker as a result of a FIGURE 1. Red-free fundus photograph of the microelectrode fall. The participating subjects’ demographics and oper- array of a chronically implanted Argus II retinal prosthesis sub- ation dates are shown in Table 1.Thestudywas ject (ID: 007). The designated quad for stimulation consisted of electrodes E07E08F07F08 (enclosed in white square). The approved by the institutional review boards and ethics fovea location is estimated to be 15.5 degrees temporal and committee, and adhered to the tenets of the Declara- 1.5 degrees inferior to the center of the optic disc. The quad- tion of Helsinki. fovea relation is calculated from the estimated fovea location, to the center of the stimulated quad. SELECTION OF STIMULATING ELECTRODES AND PA- RAMETERS: For each subject, a cluster of 4 electrodes (hereinafter referred to as a ‘‘quad’’) closest to the fovea, which were functioning with thresholds within the safety was performed, to assess the contact between the stimu- charge density limit, was selected for stimulation, and the lating electrodes and the retinal surface. The selected elicited phosphenes characterized for the purpose of this quad, quad-retina relation, quad threshold, and stimulating study (Figure 1). current for each subject were as shown in Table 2. An estimated location of the fovea was made on the fundus photograph (taken at the outset of the study) and PHOSPHENES DEPICTION: To record the phosphenes was used for each subject as a reference point, measuring perceived by each subject, we constructed a wall covered 15.5 6 1.1 degrees from the center of the optic disc hori- with smooth-surface black mats. The subjects were first zontally and À1.5 6 0.9 degrees vertically.6 The foveal po- asked to stand up and stretch out both arms fully to touch sition was estimated, as there were no remaining features of the black wall, so that their shoulders were square, facing the fovea on color photographs, fluorescein angiograms, or the wall. The standing position of each subject was then optical coherence tomography (OCT) scans owing to se- adjusted so that the distance between the front of their vere end-stage RP. eyes and the wall equaled 30 cm. Next, the subjects were Once the designated quad was chosen, the stimulating asked to point with the index finger of both hands simulta- current for each subject was arbitrarily set to be 100 mA neously on the black wall, to where they believed the cen- above the threshold (measured within the last 6 months) ter of their visual field was, while keeping their head and initially, and then adjusted according to the strength of eyes pointing straight ahead. A stack of white A4-size response and comfort level reported by the subject. We papers (in landscape layout) was then placed underneath aimed to elicit a clear, definite visual percept without the index fingers of each subject and pinned to the wall, causing any discomfort or physical ‘‘tingling’’ sensation so that the index fingers were pointing at the center of for each subject. Default settings for the Argus II retinal the top sheet of paper (ie, the center of the paper was prosthesis system Clinical Fitting System (CFS) employed approximating the proclaimed center of each subject’s for device fitting and standard testing were likewise used for visual field). A drawing pin with a protruding cylindrical this study, which generate cathodic-first, charge-balanced head was then inserted at the point where their index fin- biphasic square waves to avoid tissue damage from charge gers contacted with the wall, so as to mark the location of build-up. These default waveform parameters were as fol- the proclaimed visual field center. lows: phase width of 0.46 ms, interphase duration of 0 sec- During the experiment, the subjects were asked to posi- onds, and total stimulation duration of 250 ms at the tion themselves according to the setup above, hold onto frequency of 20 Hz.7 Swept-source OCT (DRI OCT-1 the preplaced drawing pin head, and adjust their head Atlantis; TOPCON, Topcon Medical Systems, Tokyo, and eye position until they felt the center of their visual Japan) imaging through the
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