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Short-Term Changes in the Photopic Negative Response Following Intraocular Pressure Lowering in Glaucoma

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Short-Term Changes in the Photopic Negative Response Following Intraocular Pressure Lowering in Glaucoma Glaucoma Short-Term Changes in the Photopic Negative Response Following Intraocular Pressure Lowering in Glaucoma Jessica Tang,1,2 Flora Hui,1 Xavier Hadoux,1 Bernardo Soares,3 Michael Jamieson,3 Peter van Wijngaarden,1–3 Michael Coote,1–3 and Jonathan G. Crowston1,2,4,5 1Glaucoma Research Unit, Centre for Eye Research Australia, Royal Victorian Eye and Ear Hospital, Melbourne, Australia 2Ophthalmology, Department of Surgery, The University of Melbourne, Melbourne, Australia 3Royal Victorian Eye and Ear Hospital, Melbourne, Australia 4Centre for Vision Research, Duke-NUS Medical School, Singapore, Singapore 5Singapore Eye Research Institute, Singapore National Eye Centre, Singapore, Singapore Correspondence: Jessica Tang, PURPOSE. To evaluate the short-term changes in inner retinal function using the photopic Glaucoma Research Unit, Centre for negative response (PhNR) after intraocular pressure (IOP) reduction in glaucoma. Eye Research Australia, Royal Victorian Eye and Ear Hospital, METHODS. Forty-seven participants with glaucoma who were commencing a new or addi- Level 7, Peter Howson Wing, 32 tional IOP-lowering therapy (treatment group) and 39 participants with stable glau- Gisborne St, East Melbourne, VIC coma (control group) were recruited. IOP, visual field, retinal nerve fiber layer thick- 3002, Australia; ness, and electroretinograms (ERGs) were recorded at baseline and at a follow-up visit [email protected]. (3 ± 2 months). An optimized protocol developed for a portable ERG device was used Received: August 29, 2019 to record the PhNR. The PhNR saturated amplitude (Vmax), Vmax ratio, semi-saturation Accepted: June 16, 2020 constant (K), and slope of the Naka–Rushton function were analyzed. Published: August 7, 2020 RESULTS. A significant percentage reduction in IOP was observed in the treatment group Citation: Tang J, Hui F, Hadoux X, (28 ± 3%) compared to the control group (2 ± 3%; P < 0.0001). For PhNR Vmax, there et al. Short-term changes in the was no significant interactionF ( 1,83 = 2.099, P = 0.15), but there was a significant differ- photopic negative response ence between the two time points (F1,83 = 5.689, P = 0.019). Post hoc analysis showed following intraocular pressure a significant difference between baseline and 3 months in the treatment group (mean lowering in glaucoma. Invest difference, 1.23 μV; 95% confidence interval [CI], 0.24–2.22) but not in the control group Ophthalmol Vis Sci. 2020;61(10):16. https://doi.org/10.1167/iovs.61.10.16 (0.30 μV; 95% CI, 0.78–1.38). K and slope were not significantly different in either group. Improvement beyond test–retest variability was seen in 17% of participants in the treat- ment group compared to 3% in the control group (P = 0.007, χ 2 test). CONCLUSIONS. The optimized protocol for measuring the PhNR detected short-term improvements in a proportion of participants following IOP reduction, although the majority showed no change. Keywords: electroretinography, glaucoma, pressure lowering, photopic negative response here is a growing body of evidence suggesting that, However, a similar number of studies have found no T prior to irreversible cell death, compromised retinal visual field improvement after IOP lowering.13–17 A recent ganglion cells (RGCs) enter a dysfunctional state that may analysis of short-term visual field changes in 255 individ- partially recover under certain conditions.1,2 This concept uals enrolled in the Early Manifest Glaucoma Trial found of RGC recovery is not new. In 1985, Spaeth3 argued that that small improvements in sensitivity were just as common the adequacy of intraocular pressure (IOP) therapy in glau- as small deteriorations in both the untreated and treated coma could not be certain unless there were accompanying groups.17 These apparently contradictory findings may be improvements in the visual field or optic disc. explained by the inherent variability18 and perimetric learn- Although it is well established that lowering IOP can ing19 that confounds visual field interpretation; thus, it delay visual field progression in the long term,4,5 there is remains to be determined if short-term functional improve- conflicting evidence regarding visual field recovery in glau- ment can be detected with perimetry. coma. Both Paterson et al.6 and Flammer et al.7 separately On the other hand, experimental and clinical stud- showed increases in visual sensitivity following acetazo- ies using electrophysiological tests have provided more lamide administration in a subset of glaucoma patients. Prata compelling evidence for RGC recovery associated with IOP and colleagues8 observed improvements in visual field mean reduction. Experimental models of glaucoma have demon- deviation as well as contrast sensitivity 4 weeks after lower- strated partial reversal of functional loss following IOP ing IOP with topical medications. Others have demonstrated lowering measured using the pattern electroretinogram visual field improvement following laser trabeculoplasty9 (PERG),20,21 scotopic threshold response (STR),22–24 and and surgical IOP reduction.8,10–12 photopic negative response (PhNR).25 This improvement in Copyright 2020 The Authors iovs.arvojournals.org | ISSN: 1552-5783 1 This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License. Downloaded from iovs.arvojournals.org on 09/23/2021 Change in PhNR After Pressure Lowering in Glaucoma IOVS | August 2020 | Vol. 61 | No. 10 | Article 16 | 2 function may be enhanced with diet restriction,26 exercise,27 tonometry, SAP, optical coherence tomography, and ERG 28 and nicotinamide (vitamin B3). recordings, were performed at baseline and follow-up at 3 In humans, several studies have observed PERG recovery months (±2-month window period) in both groups. in a subpopulation of glaucoma patients after IOP lower- 29–31 ing with topical medication and surgery, with one study Full-Field ERG Recording finding greater improvement in those with early 29disease. The PhNR may similarly improve after IOP treatment in The ERG setup, recording, and analysis have been described glaucoma patients. In their pilot study, Niyadurupola et al.32 previously.34–36 Following pupil dilation using 0.5% tropi- reported short-term PhNR recovery in a small cohort of camide (Mydriacyl; Alcon Laboratories, Macquarie Park, patients after a significant pressure reduction (greater than NSW, Australia), a DTL-like electrode (22/1 dtex; Shieldex 25% of baseline), which was not evident in patients with Trading, Palmyra, NY, USA) was placed along the lower lid stable IOP. margin, with reference and ground Grass gold cup skin elec- The practical advantages of the PhNR over the PERG trodes (AstroNova, West Warwick, RI, USA) placed on the (e.g., not requiring refractive correction or clear optics33), temple and forehead, respectively. together with the accessibility of recording using a portable Participants were adapted to background light before electroretinogram (ERG) device (RETeval; LKC Technologies, the stimuli were delivered with the RETeval device. Stimuli Gaithersburg, MD, USA),34–36 make the PhNR an attractive consisted of brief, red flashes (13 stimulus strengths from alternative to monitor RGC function in the clinic. We have 0.07 to 4.5 cd·s/m2 in 0.15-log unit increments) on a steady recently made a number of modifications to the ERG record- blue background (peak wavelength, 470 nm; photopic lumi- ing and test protocols with the RETeval to reduce inter- nance, 10 cd/m2). Fifty flashes per stimulus strength were test variability.34–36 In this study, we sought to determine delivered at 2 Hz. All raw ERG traces were extracted and whether the optimized protocol can reliably detect changes processed offline using MATLAB (MathWorks, Natick, MA, in the PhNR shortly after IOP lowering in glaucoma and USA). Baseline detrending using a third-order polynomial to compare corresponding changes on standard automated was performed as previously described.35 perimetry (SAP). The amplitudes of the following parameters were extracted from the average trace: a-wave, defined as the trough in the time window 0 to 30 ms and measured from METHODS baseline; b-wave, defined as the maximum after the a-wave and measured from the a-wave trough to peak; and the The research followed the tenets of the Declaration of PhNR, defined as the trough after the b-wave in the time Helsinki and was approved by the Human Research Ethics window 55 to 90 ms from flash onset and measured from Committee at the Royal Victorian Eye and Ear Hospi- the baseline. Where two or more troughs were seen, the tal, Melbourne, Australia (13/1121H). Participants were most negative trough was chosen as the PhNR, which is in recruited from two sites: public outpatient clinics at the line with International Society for Clinical Electrophysiology Royal Victorian Eye and Ear Hospital or a private ophthal- of Vision recommendations.37 mology clinic (Melbourne Eye Specialists). Informed consent The PhNR and b-wave amplitude were plotted as a func- was obtained from all participants prior to examination. tion of log stimulus strength (Fig. 1). The Naka–Rushton n n n The treatment group was comprised of glaucoma equation, defined as V = Vmax × I /(I + K ), where V is suspects or manifest glaucoma patients deemed by the treat- the amplitude, I is the stimulus strength, Vmax is the maxi- ing glaucoma specialist to require new or additional IOP- mum saturating amplitude, n is the slope, and K is the semi- lowering treatment due to high IOP or evidence of progres- saturation constant, was fitted to the data in MATLAB using sion on visual field; they were recruited and baseline tested a robust, nonlinear, least-squares method with a bi-square prior to initiating therapy. Glaucoma patients who were weight to reduce the influence of outlier data points. Vmax, deemed stable by the treating specialist and not requir- K, slope, and Vmax ratio, defined as PhNR Vmax over b-wave ing a change in treatment at the time of study recruitment Vmax, were analyzed.
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