Shortened Pattern Electroretinogram Latency and Impaired Autoregulatory Dynamics to Steady-State Stimuli in Patients With Multiple Sclerosis.
Journal
Journal of neuro-ophthalmology : the official journal of the North American Neuro-Ophthalmology Society
ISSN: 1536-5166
Titre abrégé: J Neuroophthalmol
Pays: United States
ID NLM: 9431308
Informations de publication
Date de publication:
01 03 2021
01 03 2021
Historique:
pubmed:
25
1
2020
medline:
12
11
2021
entrez:
25
1
2020
Statut:
ppublish
Résumé
The steady-state pattern electroretinogram (PERG) is a sensitive measure of retinal ganglion cell (RGC) function that includes within-test progressive changes-adaptation-reflecting RGC autoregulatory dynamics. Comprehensive PERG assessment in patients with multiple sclerosis (MS) (with or without optic neuritis [ON]) may provide unique information about RGC dysfunction and its progression, as well as a comparison between functional loss and structural loss as measured by optical coherence tomography (OCT). The goal of this project was to measure steady-state PERG components and their associations with intraretinal layer thicknesses in MS. One hundred forty eyes of 70 patients with relapsing-remitting MS and 126 eyes of 63 age- and sex-matched healthy control subjects (HC) were investigated using a new-generation PERG method and ultrahigh-resolution OCT. Of MS eyes, there were 30 eyes with ON (MSON), 22 non-ON fellow eyes (MSFE), and 88 non-ON MS eyes (MSNON). PERG amplitude, phase (latency), and adaptation of amplitude and phase were measured and correlated with OCT-determined thicknesses of intraretinal layers. The average PERG amplitude in MSON eyes was significantly lower than MSFE (P = 0.007), MSNON (P = 0.002), and HC (P < 0.001). The PERG amplitude in MSFE eyes was also significantly lower than HC (P = 0.039). The PERG latency in MSON eyes was significantly shorter than in MSFE (P = 0.001), MSNON (P = 0.002), and HC (P < 0.001). The PERG latency in MSFE (P = 0.007) and MSNON (P = 0.002) was significantly shorter than in HC. However, no significant differences were found between MSFE and MSNON (P > 0.05). PERG adaptation of amplitude in MSON was significantly lower than that in MSNON (P = 0.039) and HC (P = 0.037). Both the amplitude and latency in the MS eyes were significantly correlated with the thicknesses of the macular retinal nerve fiber layer (mRNFL) and ganglion cell-inner plexiform layer (GCIPL). Shortened PERG latency and impaired autoregulatory dynamics occurred in MS, suggesting preferential dysfunction of small, slower RGC axons and decreased ability of RGC to autoregulate their gain in response to PERG stimulus. The established relations of PERG measurements with intraretinal thickness measurements suggested that PERG losses were primarily associated with GCIPL and mRNFL thinning.
Sections du résumé
BACKGROUND
The steady-state pattern electroretinogram (PERG) is a sensitive measure of retinal ganglion cell (RGC) function that includes within-test progressive changes-adaptation-reflecting RGC autoregulatory dynamics. Comprehensive PERG assessment in patients with multiple sclerosis (MS) (with or without optic neuritis [ON]) may provide unique information about RGC dysfunction and its progression, as well as a comparison between functional loss and structural loss as measured by optical coherence tomography (OCT). The goal of this project was to measure steady-state PERG components and their associations with intraretinal layer thicknesses in MS.
METHODS
One hundred forty eyes of 70 patients with relapsing-remitting MS and 126 eyes of 63 age- and sex-matched healthy control subjects (HC) were investigated using a new-generation PERG method and ultrahigh-resolution OCT. Of MS eyes, there were 30 eyes with ON (MSON), 22 non-ON fellow eyes (MSFE), and 88 non-ON MS eyes (MSNON). PERG amplitude, phase (latency), and adaptation of amplitude and phase were measured and correlated with OCT-determined thicknesses of intraretinal layers.
RESULTS
The average PERG amplitude in MSON eyes was significantly lower than MSFE (P = 0.007), MSNON (P = 0.002), and HC (P < 0.001). The PERG amplitude in MSFE eyes was also significantly lower than HC (P = 0.039). The PERG latency in MSON eyes was significantly shorter than in MSFE (P = 0.001), MSNON (P = 0.002), and HC (P < 0.001). The PERG latency in MSFE (P = 0.007) and MSNON (P = 0.002) was significantly shorter than in HC. However, no significant differences were found between MSFE and MSNON (P > 0.05). PERG adaptation of amplitude in MSON was significantly lower than that in MSNON (P = 0.039) and HC (P = 0.037). Both the amplitude and latency in the MS eyes were significantly correlated with the thicknesses of the macular retinal nerve fiber layer (mRNFL) and ganglion cell-inner plexiform layer (GCIPL).
CONCLUSIONS
Shortened PERG latency and impaired autoregulatory dynamics occurred in MS, suggesting preferential dysfunction of small, slower RGC axons and decreased ability of RGC to autoregulate their gain in response to PERG stimulus. The established relations of PERG measurements with intraretinal thickness measurements suggested that PERG losses were primarily associated with GCIPL and mRNFL thinning.
Identifiants
pubmed: 31977664
pii: 00041327-202103000-00011
doi: 10.1097/WNO.0000000000000894
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
60-68Informations de copyright
Copyright © 2020 by North American Neuro-Ophthalmology Society.
Déclaration de conflit d'intérêts
The authors report no conflicts of interest.
Références
Lanzillo R, Cennamo G, Criscuolo C, Carotenuto A, Velotti N, Sparnelli F, Cianflone A, Moccia M, Brescia Morra V. Optical coherence tomography angiography retinal vascular network assessment in multiple sclerosis. Mult Scler. 2018;24:1706–1714.
Ikuta F, Zimmerman HM. Distribution of plaques in seventy autopsy cases of multiple sclerosis in the United States. Neurology. 1976;26:26–28.
Toussaint D, Périer O, Verstappen A, Bervoets S. Clinicopathological study of the visual pathways, eyes, and cerebral hemispheres in 32 cases of disseminated sclerosis. J Clin Neuroophthalmol. 1983;3:211–220.
Nolan RC, Akhand O, Rizzo JR, Galetta SL, Balcer LJ. Evolution of visual outcomes in clinical trials for multiple sclerosis disease-modifying therapies. J Neuroophthalmol. 2018;38:202–209.
Porciatti V. The mouse pattern electroretinogram. Doc Ophthalmol. 2007;115:145–153.
Guy J, Feuer WJ, Porciatti V, Schiffman J, Abukhalil F, Vandenbroucke R, Rosa PR, Lam BL Retinal ganglion cell dysfunction in asymptomatic G11778A: Leber hereditary optic neuropathy. Invest Ophthalmol Vis Sci. 2014;55:841–848.
Porciatti V, Ventura LM. Retinal ganglion cell functional plasticity and optic neuropathy: a comprehensive model. J Neuroophthalmol. 2012;32:354–358.
Monsalve P, Triolo G, Toft-Nielsen J, Bohorquez J, Henderson AD, Delgado R, Miskiel E, Ozdamar O, Feuer WJ, Porciatti V. Next generation PERG method: expanding the response dynamic range and capturing response adaptation. Transl Vis Sci Technol. 2017;6:5.
Ventura LM, Porciatti V, Ishida K, Feuer WJ, Parrish RK. Pattern electroretinogram abnormality and glaucoma. Ophthalmology. 2005;112:10–19.
Monsalve P, Ren S, Jiang H, Wang J, Kostic M, Gordon P, Porciatti V. Retinal ganglion cell function in recovered optic neuritis: faster is not better. Clin Neurophysiol. 2018;129:1813–1818.
Rodriguez-Mena D, Almarcegui C, Dolz I, Herrero R, Bambo MP, Fernandez J, Pablo LE, Garcia-Martin E. Electropysiologic evaluation of the visual pathway in patients with multiple sclerosis. J Clin Neurophysiol. 2013;30:376–381.
Hokazono K, Raza AS, Oyamada MK, Hood DC, Monteiro ML. Pattern electroretinogram in neuromyelitis optica and multiple sclerosis with or without optic neuritis and its correlation with FD-OCT and perimetry. Doc Ophthalmol. 2013;127:201–215.
Banitt MR, Ventura LM, Feuer WJ, Savatovsky E, Luna G, Shif O, Bosse B, Porciatti V. Progressive loss of retinal ganglion cell function precedes structural loss by several years in glaucoma suspects. Invest Ophthalmol Vis Sci. 2013;54:2346–2352.
Ventura LM, Porciatti V. Restoration of retinal ganglion cell function in early glaucoma after intraocular pressure reduction: a pilot study. Ophthalmology. 2005;112:20–27.
Porciatti V, Bosse B, Parekh PK, Shif OA, Feuer WJ, Ventura LM. Adaptation of the steady-state PERG in early glaucoma. J Glaucoma. 2014;23:494–500.
Fadda A, Di RA, Martelli F, Marangoni D, Batocchi AP, Giannini D, Parisi V, Falsini B. Reduced habituation of the retinal ganglion cell response to sustained pattern stimulation in multiple sclerosis patients. Clin Neurophysiol. 2013;124:1652–1658.
Saidha S, Al-Louzi O, Ratchford JN, Bhargava P, Oh J, Newsome SD, Prince JL, Pham D, Roy S, van Zijl P, Balcer LJ, Frohman EM, Reich DS, Crainiceanu C, Calabresi PA. Optical coherence tomography reflects brain atrophy in multiple sclerosis: a four-year study. Ann Neurol. 2015;78:801–813.
Saidha S, Syc SB, Ibrahim MA, Eckstein C, Warner CV, Farrell SK, Oakley JD, Durbin MK, Meyer SA, Balcer LJ, Frohman EM, Rosenzweig JM, Newsome SD, Ratchford JN, Nguyen QD, Calabresi PA. Primary retinal pathology in multiple sclerosis as detected by optical coherence tomography. Brain. 2011;134:518–533.
Balcer LJ, Baier ML, Cohen JA, Kooijmans MF, Sandrock AW, Nano-Schiavi ML, Pfohl DC, Mills M, Bowen J, Ford C, Heidenreich FR, Jacobs DA, Markowitz CE, Stuart WH, Ying GS, Galetta SL, Maguire MG, Cutter GR. Contrast letter acuity as a visual component for the multiple sclerosis functional composite. Neurology. 2003;61:1367–1373.
Porciatti V, Ventura LM. Normative data for a user-friendly paradigm for pattern electroretinogram recording. Ophthalmology. 2004;111:161–168.
Wei Y, Jiang H, Shi Y, Qu D, Gregori G, Zheng F, Rundek T, Wang J. Age-related alterations in the retinal microvasculature, microcirculation, and microstructure. Invest Ophthalmol Vis Sci. 2017;58:3804–3817.
Shao Y, Jiang H, Wei Y, Shi Y, Shi C, Wright CB, Sun X, Vanner EA, Rodriguez AD, Lam BL, Rundek T, Baumel BS, Gameiro GR, Dong C, Wang J. Visualization of focal thinning of the ganglion cell-inner plexiform layer in patients with mild cognitive impairment and alzheimer's disease. J Alzheimers Dis. 2018;64:1261–1273.
Tan J, Yang Y, Jiang H, Liu C, Deng Z, Lam BL, Hu L, Oakley J, Wang J. The measurement repeatability using different partition methods of intraretinal tomographic thickness maps in healthy human subjects. Clin Ophthalmol. 2016;10:2403–2415.
Toft-Nielsen J, Bohorquez J, Ozdamar O. Innovative pattern reversal displays for visual electrophysiological studies. Conf Proc IEEE Eng Med Biol Soc. 2011;2011:2009–2012.
Ito H, Ogawa M, Sunaga S. Evaluation of an organic light-emitting diode display for precise visual stimulation. J Vis. 2013;13:6.
Chiappa KH. Pattern-shift visual, brainstem auditory and short-latency somatosensory evoked potentials in multiple sclerosis. Ann N Y Acad Sci. 1984;436:315–327.
Evangelou N, Konz D, Esiri MM, Smith S, Palace J, Matthews PM. Size-selective neuronal changes in the anterior optic pathways suggest a differential susceptibility to injury in multiple sclerosis. Brain. 2001;124:1813–1820.
Porciatti V, Burr DC, Morrone MC, Fiorentini A. The effects of aging on the pattern electroretinogram and visual evoked potential in humans. Vis Res. 1992;32:1199–1209.
Fadda A, Di RA, Parisi V, Stifano G, Balestrazzi E, Riva CE, Falsini B. Lack of habituation in the light adapted flicker electroretinogram of normal subjects: a comparison with pattern electroretinogram. Clin Neurophysiol. 2009;120:1828–1834.
Porciatti V, Ventura LM. Adaptive changes of inner retina function in response to sustained pattern stimulation. Vis Res. 2009;49:505–513.
Porciatti V, Sorokac N, Buchser W. Habituation of retinal ganglion cell activity in response to steady state pattern visual stimuli in normal subjects. Invest Ophthalmol Vis Sci. 2005;46:1296–1302.