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      Relationship between pattern electroretinogram and optic disc morphology in glaucoma

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      PLoS ONE

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          Abstract

          Purpose

          To evaluate the relationship between pattern electroretinogram (PERG) and optic disc morphology in glaucoma suspect and glaucoma.

          Methods

          Eighty-six eyes of glaucoma suspect and 145 eyes of manifest glaucoma subjects were included in this study. Average peripapillary retinal nerve fiber layer (RNFL) thickness was obtained with spectral-domain optical coherence tomography, and optic disc imaging was performed using the Heidelberg Retinal Tomograph (HRT). Visual function was evaluated with perimetry (SITA and frequency doubling technology) and PERG. Scatter plots and correlation coefficients were evaluated between visual function and RNFL thickness or optic disc structure.

          Results

          Scatter plots of PERG and perimetry according to RNFL thickness change showed that PERG started to decrease earlier than did perimetry. The differences between linear and logarithmic R 2 were largest for the scatter plot of SITA 24–2 (linear R 2 = 0.415; logarithmic R 2 = 0.443) and the smallest for P50 amplitude of PERG (linear R 2 = 0.136, logarithmic R 2 = 0.138). In glaucoma suspect, HRT parameters such as cup shape measure (CSM) and linear cup-disc ratio (CDR) had significant correlations with PERG amplitudes ( P = 0.016 for P50 and 0.049 for N95 in CSM, P = 0.012 for P50 in CDR). However, in glaucoma patients, mean RNFL thickness was associated with PERG amplitude ( P = 0.011 for P50 and 0.002 for N95).

          Conclusions

          PERG deterioration occurred earlier than did perimetry according to RNFL thickness decrease. PERG amplitudes were significantly correlated with disc morphology in glaucoma suspect. These results suggest that PERG can detect ganglion cell dysfunction before the cells die.

          Related collections

          Most cited references 31

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          Optic nerve damage in human glaucoma. II. The site of injury and susceptibility to damage.

          We examined the histologic structure of the optic nerve head in 15 eyes of nine persons with a known glaucoma history. All had been seeing eyes, varying from normal visual acuity and visual field to advanced glaucoma damage. The site of damage to nerve fibers is the scleral lamina cribrosa, where there is local blockage of axonal transport. Early cup size increase prior to definite field loss results from loss of nerve fibers, not from damage to astrocytic glial cells of the nerve head. No selective damage to nerve head capillaries is seen in mildly damaged specimens. Scanning electron microscopic analysis suggests that the structure of the lamina cribrosa is an important determinant of the degree of susceptibility to damage by elevated intraocular pressure.
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            Number of ganglion cells in glaucoma eyes compared with threshold visual field tests in the same persons.

            To compare the number of retinal ganglion cells (RGCs) topographically mapped with specific visual field threshold test data in the same eyes among glaucoma patients. Seventeen eyes of 13 persons with well-documented glaucoma histories and Humphrey threshold visual field tests (San Leandro, CA) were obtained from eye banks. RGC number was estimated by histologic counts of retinal sections and by counts of remaining axons in the optic nerves. The locations of the retinal samples corresponded to specific test points in the visual field. The data for glaucoma patients were compared with 17 eyes of 17 persons who were group matched for age, had no ocular history, and had normal eyes by histologic examination. The mean RGC loss for the entire retina averaged 10.2%, indicating that many eyes had early glaucoma damage. RGC body loss averaged 35.7% in eyes with corrected pattern SD probability less than 0.5%. When upper to lower retina RGC counts were compared with their corresponding visual field data within each eye, a 5-dB loss in sensitivity was associated with 25% RGC loss. For individual points that were abnormal at a probability less than 0.5%, the mean RGC loss was 29%. In control eyes, the loss of RGCs with age was estimated as 7205 cells per year in persons between 55 and 95 years of age. In optic nerves from glaucoma subjects, smaller axons were significantly more likely to be present than larger axons (R2 = 0.78, P<0.001). At least 25% to 35% RGC loss is associated with statistical abnormalities in automated visual field testing. In addition, these data corroborate previous findings that RGCs with larger diameter axons preferentially die in glaucoma.
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              Ganglion cell losses underlying visual field defects from experimental glaucoma.

              To investigate the relationship between ganglion cell losses and visual field defects caused by glaucoma. Behavioral perimetry and histology data were obtained from 10 rhesus monkeys with unilateral experimental glaucoma that was induced by argon laser treatments to their trabecular meshwork. After significant visual field defects had developed, the retinas were collected for histologic analysis. The ganglion cells were counted by light microscopy in cresyl violet-stained retina sections, and the percentage of ganglion cell loss (treated to control eye counts) was compared with the depth of visual field defect (treated to control eye thresholds) at corresponding retinal and perimetry test locations. Sensitivity losses as a function of ganglion cell losses were analyzed for Goldmann III, white and Goldmann V, and short- and long-wavelength perimetry test stimuli. The relationship between the proportional losses of ganglion cells and visual sensitivity, measured with either white or colored stimuli, was nonlinear. With white stimuli, the visual sensitivity losses were relatively constant (approximately 6 dB) for ganglion cell losses of less than 30% to 50%, and then with greater amounts of cell loss the visual defects were more systematically related to ganglion cell loss (approximately 0.42 dB/percent cell loss). The forms of the neural-sensitivity relationships for visual defects measured with short- or long-wavelength perimetry stimuli were similar when the visual thresholds were normalized to compensate for differences in expected normal thresholds for white and colored perimetry stimuli. Current perimetry regimens with either white or monochromatic stimuli do not provide a useful estimate of ganglion cell loss until a substantial proportion have died. The variance in ganglion cell loss is large for mild defects that would be diagnostic of early glaucoma and for visual field locations near the fovea where sensitivity losses occur relatively late in the disease process. The neural-sensitivity relationships were essentially identical for both white and monochromatic test stimuli, and it therefore seems unlikely that the higher sensitivity for detecting glaucoma with monochromatic stimuli is based on the size-dependent susceptibility of ganglion cells to injury from glaucoma.
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                Author and article information

                Contributors
                Role: Data curationRole: Formal analysisRole: Writing – original draft
                Role: ConceptualizationRole: Formal analysisRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Writing – review & editing
                Role: ConceptualizationRole: SupervisionRole: Validation
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                7 November 2019
                2019
                : 14
                : 11
                Affiliations
                Department of Ophthalmology, Seoul St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea
                National Taiwan University Hospital, TAIWAN
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Article
                PONE-D-19-14182
                10.1371/journal.pone.0220992
                6837750
                31697709
                © 2019 Jeon et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Page count
                Figures: 6, Tables: 6, Pages: 14
                Product
                Funding
                The authors received no specific funding for this work.
                Categories
                Research Article
                Medicine and Health Sciences
                Ophthalmology
                Eye Diseases
                Glaucoma
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Neurons
                Afferent Neurons
                Retinal Ganglion Cells
                Biology and Life Sciences
                Neuroscience
                Cellular Neuroscience
                Neurons
                Afferent Neurons
                Retinal Ganglion Cells
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Neurons
                Ganglion Cells
                Retinal Ganglion Cells
                Biology and Life Sciences
                Neuroscience
                Cellular Neuroscience
                Neurons
                Ganglion Cells
                Retinal Ganglion Cells
                Biology and Life Sciences
                Anatomy
                Ocular System
                Ocular Anatomy
                Optic Disc
                Medicine and Health Sciences
                Anatomy
                Ocular System
                Ocular Anatomy
                Optic Disc
                Medicine and Health Sciences
                Ophthalmology
                Biology and Life Sciences
                Anatomy
                Head
                Eyes
                Medicine and Health Sciences
                Anatomy
                Head
                Eyes
                Biology and Life Sciences
                Anatomy
                Ocular System
                Eyes
                Medicine and Health Sciences
                Anatomy
                Ocular System
                Eyes
                Medicine and Health Sciences
                Diagnostic Medicine
                Diagnostic Radiology
                Tomography
                Research and Analysis Methods
                Imaging Techniques
                Diagnostic Radiology
                Tomography
                Medicine and Health Sciences
                Radiology and Imaging
                Diagnostic Radiology
                Tomography
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Neurons
                Ganglion Cells
                Biology and Life Sciences
                Neuroscience
                Cellular Neuroscience
                Neurons
                Ganglion Cells
                Biology and Life Sciences
                Physiology
                Electrophysiology
                Medicine and Health Sciences
                Physiology
                Electrophysiology
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                All relevant data are within the paper and its Supporting Information files.

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