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Electroretinograms of eyes with Stickler syndrome

June 2020
Documenta Ophthalmologica 140(5)

June 2020
140(5)

DOI:10.1007/s10633-019-09739-x

Authors:

Hiroyuki Kondo

University of Occupational and Environmental Health

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Purpose To determine the characteristics of the full-field electroretinograms (ERGs) of eyes with Stickler syndrome. Methods Twenty-two eyes of 14 Japanese patients from nine families with Stickler syndrome were studied. All of the patients were found to have mutations in the COL2A1 gene and had undergone ERG recordings. The ERGs from one of the two eyes were compared to 11 eyes of 11 normal control subjects who were matched by age, sex, and refractive error. Results One patient had non-recordable ERGs under both scotopic and photopic conditions. For the remaining 13 patients, the amplitudes of the b-waves of the scotopic combined, rod, and cone responses were significantly smaller than those of the control subjects (P = 0.0001, P = 0.015, P = 0.0006, respectively). The implicit times of the b-wave of the scotopic combined and photopic responses were significantly prolonged (P = 0.0037 and P = 0.0126). The age was inversely and significantly correlated with the amplitudes of the scotopic combined a-wave (P = 0.0184) and b-wave (P = 0.0076) in 13 eyes. The amplitudes of the scotopic combined b-wave amplitudes were not significantly correlated with the refractive error. Conclusions The reduced or absent full-field ERGs in eyes with Stickler syndrome indicate that the physiology of the entire retina was negatively altered. The greater reduction in the ERGs with increasing age suggests that the physiological alterations of the retina are progressive.

Clinical findings of three patients with Stickler syndrome. The images (a–c), (d, e) and (f, g) are from Patient 5, Patient 2 and Patient 1, respectively (see Table 1). Fundus photographs (a, d, e, f) show severe myopic changes associated with localized retinal degeneration along the retinal vessels and around the optic nerve head (d), and localized vitreous veil changes (f). Fluorescein angiography of Patient 5 shows dark spots due to vitreous opacities but retinal changes are unremarkable (b). Optical coherence tomographic image of Patient 5 shows shallow foveal pit (c). Fundus autofluorescence image shows relatively preserved autofluorescence in spite of the decreased electroretinograms (g)

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Full-field electroretinograms (ERGs) of patients with Stickler syndrome. LE left eye. Control subject: a 28-year-old man with a refractive error of − 10.0 diopters

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Correlation of a- and b- wave amplitudes of the dark-adapted 200 ERG responses with the patients’ age and refractive error in 13 eyes with Stickler syndrome. The age of the patients was inversely and significantly correlated with the amplitudes of the a-wave (a; r = − 0.64, P = 0.0184) and b-wave (b; r = − 0.70, P = 0.0076). The refractive error was not significantly correlated with the a-wave amplitude (c; r = 0.31, P = 0.31) and the b-wave amplitude (d; r = 0.13, P = 0.68)

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ORIGINAL RESEARCH ARTICLE

Electroretinograms of eyes with Stickler syndrome

Hiroyuki Kondo .Kazushi Fujimoto .Mamika Imagawa .Kazuma Oku .

Itsuka Matsushita .Takaaki Hayashi .Tatsuo Nagata

Received: 21 May 2019 / Accepted: 20 November 2019 / Published online: 28 November 2019

ÓSpringer-Verlag GmbH Germany, part of Springer Nature 2019

Abstract

Purpose To determine the characteristics of the full-

ﬁeld electroretinograms (ERGs) of eyes with Stickler

syndrome.

Methods Twenty-two eyes of 14 Japanese patients

from nine families with Stickler syndrome were

studied. All of the patients were found to have

mutations in the COL2A1 gene and had undergone

ERG recordings. The ERGs from one of the two eyes

were compared to 11 eyes of 11 normal control

subjects who were matched by age, sex, and refractive

error.

Results One patient had non-recordable ERGs under

both scotopic and photopic conditions. For the

remaining 13 patients, the amplitudes of the b-waves

of the scotopic combined, rod, and cone responses

were signiﬁcantly smaller than those of the control

subjects (P= 0.0001, P= 0.015, P= 0.0006, respec-

tively). The implicit times of the b-wave of the

scotopic combined and photopic responses were

signiﬁcantly prolonged (P= 0.0037 and

P= 0.0126). The age was inversely and signiﬁcantly

correlated with the amplitudes of the scotopic com-

bined a-wave (P= 0.0184) and b-wave (P= 0.0076)

in 13 eyes. The amplitudes of the scotopic combined

b-wave amplitudes were not signiﬁcantly correlated

with the refractive error.

Conclusions The reduced or absent full-ﬁeld ERGs

in eyes with Stickler syndrome indicate that the

physiology of the entire retina was negatively altered.

The greater reduction in the ERGs with increasing age

suggests that the physiological alterations of the retina

are progressive.

Keywords Full-ﬁeld electroretinograms Stickler

syndrome Myopia Wagner vitreoretinopathy 

Cone-rod dystrophy

Introduction

Stickler syndrome (OMIM 108300, 604841, 609508,

614134, and 614284) is an inherited systemic disorder

that affects the eye, cartilage, and articular tissues [1].

The systemic features affected include mid-facial

hypoplasia, degenerated cartilage, and sensory hearing

impairments [2]. The ocular ﬁndings are characterized

Electronic supplementary material The online version of

this article (https://doi.org/10.1007/s10633-019-09739-x) con-

tains supplementary material, which is available to authorized

users.

H. Kondo (&)K. Fujimoto M. Imagawa 

K. Oku I. Matsushita T. Nagata

Department of Ophthalmology, University of

Occupational and Environmental Health, 1-1, Iseigaoka,

Yahatanishiku, Kitakyushu 807-8555, Japan

e-mail: kondohi@med.uoeh-u.ac.jp

T. Hayashi

Department of Ophthalmology, The Jikei University

School of Medicine, Tokyo, Japan

123

Doc Ophthalmol (2020) 140:233–243

https://doi.org/10.1007/s10633-019-09739-x(0123456789().,-volV)(0123456789().,-volV)

Content courtesy of Springer Nature, terms of use apply. Rights reserved.

ULTRA-WIDE FIELD FUNDUS AUTOFLUORESCENCE IMAGING OF EYES WITH STICKLER SYNDROME

Article

Full-text available

Jul 2020
RETINA-J RET VIT DIS

Purpose: To determine the characteristics of fundus autofluorescence (FAF) images and visual functions in eyes with Stickler syndrome using ultra-widefield FAF images. Methods: Forty-six eyes of 26 patients with mutations in the COL2A1 gene underwent ultra-widefield FAF imaging. The eyes were categorized into three types; no signs of abnormal AF, predominantly hyperfluorescent AF (hyper-AF), and predominantly hypofluorescent AF (hypo-AF). Goldmann perimetry was performed on 34 eyes, and line-scan images of the abnormal AF lesions were obtained by swept-source optical coherence tomography in 4 eyes. Results: Abnormal AF lesions were found in 37 eyes of 21 (80.7%) of the 26 patients. Hyper-AF was found in 15 eyes and hypo-AF was found in 22 eyes. The FAF changes corresponded with the funduscopically observed radial paravascular retinal degeneration. The average age at the examination was significantly younger in patients who had eyes with hyper-AF or no abnormal AF than in those with hypo-AF (12.8 vs. 28.4 years; P = 0.009). Abnormal AF-associated visual field defects were found in 5/10 (50%) eyes with hyper-AF and 17/18 (94%) eyes with hypo-AF. Hyper-AF changes tended to appear before retinal changes were detectable by fluorescein angiography. An absence of the ellipsoid zone and the outer nuclear layer and a thinning of the overall retinal thickness were found corresponding to the hypo-AF lesions in the swept source optical coherence tomography images. Conclusion: Abnormal FAF is characteristic of eyes with Stickler syndrome. Age-related alterations of the FAF was associated with visual field defects and disruption of the photoreceptors and retinal pigment epithelial cells.

Transient electroretinographic abnormalities that mimic those of KCNV2 retinopathy: a case report

Article

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Oct 2021
DOC OPHTHALMOL

Purpose The purpose of this report was to describe the case of a 68-year-old male patient with stage IV colon cancer who exhibited electroretinographic abnormalities that are similar to those of KCNV2 retinopathy. Methods The patient presenting with photophobia, reduced visual acuity, and poor general conditions, the onset of which occurred ten days before presentation, was examined using fundoscopy, full-field electroretinography, blood tests, and abdominal computed tomography. Results The patient’s decimal best-corrected visual acuity (BCVA) was 0.4 in each eye. Fundoscopy showed bull's eye-like maculopathy in both eyes. Electroretinographic findings were similar to the characteristic findings of KCNV2 retinopathy: Rod electroretinogram showed delayed and preserved b-wave amplitudes; bright-flash electroretinogram showed double troughs of a-waves; b/a ratios shown by bright-flash electroretinogram were higher than those shown by standard-flash electroretinogram; and both cone and 30-Hz flicker electroretinograms showed extinguished responses. His serum potassium level increased to 6.2 mmol/L (normal range 3.6–4.8 mmol/L) owing to hydronephrosis resulting from disseminated carcinoma. After performing an emergency surgery to treat this condition, the serum potassium level immediately decreased to a normal range. Eleven days after presentation, rod and standard/bright-flash electroretinography showed improvement in the implicit time of the rod b-waves and the a-waves. Unexpectedly, the responses recorded by cone and 30-Hz flicker electroretinography became normal. The symptoms and maculopathy disappeared, and his BCVA improved to 1.2. Conclusions The abnormal electroretinographic findings might be associated with the transient increase in serum potassium level.

Severe foveal hypoplasia and macular degeneration in Stickler syndrome caused by missense mutation in COL2A1 gene

Article

Apr 2022

Background: The aim is to determine the retinal changes in patients with Stickler syndrome caused by a p.R565C missense mutation of the COL2A1 gene. Methods: We reviewed the clinical records of 10 eyes of six patients from two families with the Stickler syndrome. The members of both families were heterozygous for the p.R565C mutation. The clinical features including the visual acuity, fundus appearances, fundus autofluorescence (FAF), optical coherence tomographic (OCT) images, and electroretinograms were examined. Results: Myopia of -12 diopters (D) to -24 D with an average of -16.8 D was observed in 9 eyes of the 5 patients. The FAF images showed different degrees of hyper and hypoautofluorescent patterns in the macula in all but the two youngest patients (7 of 9 eyes, 78%). The OCT images showed the absence of a foveal pit and destruction of the outer retinal layers in the macular area in all patients. The ellipsoid zone (EZ) in the macular region was disrupted in eight eyes (80%) of which seven were fovea sparing. Conclusion: Two families with Stickler syndrome with the p.R565C mutation showed more severe foveal hypoplasia, macular degeneration, and extensive retinal degeneration. A correlation of the OCT and FAF images with the genotype is helpful in determining the prognosis of Stickler syndrome.

Retinal Features of Family Members With Familial Exudative Vitreoretinopathy Caused By Mutations in KIF11 Gene

Article

Full-text available

Jun 2021

Purpose: To determine the clinical characteristics of patients and family members with familial exudative vitreoretinopathy (FEVR) caused by mutations in the KIF11 gene. Methods: Twenty-one patients from 10 FEVR families with mutations in the KIF11 gene were studied. The retinal and systemic features were examined. The genetic analyses performed included Sanger sequencing of the KIF11 gene, whole exome sequencing, as well as array comparative genomic hybridization (CGH) analysis and multiple ligation probe assay (MLPA). Results: Sequence analysis revealed seven different KIF11 mutations. Array CGH with MLPA revealed two different exon deletions. All probands had advanced FEVR with retinal detachments (RDs) and microcephaly with or without developmental disabilities. Patients with bilateral RDs were more frequently associated with developmental disabilities (P = 0.023). Multimodal imaging of the family members revealed that six of nine patients without RDs (66%) had varying degrees of chorioretinopathy. The retinal folds in FEVR patients were associated with severe retinal avascularization. However, funduscopic changes in the peripheral retina were unremarkable in family members without RDs. A score representing the peripheral vascular anomalies determined from the fluorescein angiograms was lower than that of control eyes of patients with mutations of the Wnt signaling genes (P = 0.0029). Conclusions: The probands with KIF11 mutations were associated with severe ocular and systemic pathologies, whereas affected family members showed highly variable clinical manifestations. Peripheral vascular anomalies can often be unremarkable in eyes without RDs. Translational relevance: These findings highlight more diverse mechanisms that underlie the pathological changes in patients with FEVR.

Autosomal recessive Stickler syndrome associated with homozygous mutations in the COL9A2 gene

Article

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Background: Stickler syndrome is a hereditary disorder of collagen tissues causing ocular, auditory, orofacial, and joint manifestations. Ocular findings typically include vitreous degeneration, high myopia, retinal detachment, and cataract. Many subjects demonstrate sensorineural or conductive hearing loss. The inheritance is autosomal dominant with mutations in COL2A1, COL11A1, or COL11A2 or autosomal recessive due to mutations in COL9A1, COL9A2, or COL9A3. We describe a family with Stickler syndrome caused by homozygous loss-of-function mutations in COL9A2. Methods: Two brothers from a consanguineous family were examined with genetic testing, visual acuity, Goldmann perimetry, full-field and multifocal electroretinography (ffERG, mERG), optical coherence tomography (OCT), fundus autofluorescence (FAF), fundus photography, and pure-tone audiograms. Results: Both subjects were homozygous for the mutation c.1332del in COL9A2. Their parents were heterozygous for the same mutation. The boys demonstrated reduced visual acuity, vitreous changes and myopia. The proband was operated for retinal detachment and cataract in one eye. FfERG revealed reduced function of both rods and cones and mERG showed reduced macular function. No morphological macular changes were found by OCT or FAF. Both brothers have severe sensorineural hearing loss with down-sloping audiograms but only subtle midface hypoplasia and no, or mild joint problems. Conclusion: Only a few families with Stickler syndrome caused by COL9A2 mutations have been reported. We confirm previous descriptions with a severe ocular and auditory phenotype but mild orofacial and joint manifestations. Moreover, we demonstrate reduced macular and overall retinal function explaining the reduced visual acuity in patients with Stickler syndrome also without retinal complications.

WAGNER syndrome: anatomic, functional and genetic characterization of a Portuguese family

Article

Full-text available

Jan 2018
GRAEF ARCH CLIN EXP

Purpose: To report the clinical (anatomic and functional) and genetic findings of Wagner Syndrome (WS) in a Portuguese family. Methods: Nine members of the family agreed to be examined. All had complete clinical eye examinations. The proband and selected patients underwent color fundus photography, spectral domain optical coherence tomography (SD-OCT), automatic static white-on-white computerized perimetry, and electrophysiology assessment (flash ERG, multifocal(mf) ERG and dark adaptometry). A pedigree was constructed based on interviews with known affected subjects. Genomic DNA samples derived from venous blood were collected from all affected family members examined. Results: Twenty-eight family members are affected. This family has the typical features of Wagner Syndrome, namely an empty vitreous cavity with veils, mild myopia and cataract. Four examined patients underwent vitreoretinal surgery due to abnormal peripheral vitreoretinal adhesions with peripheral retinal traction (n = 3). Retinal detachment was observed in 5 of the examined subjects. Four of them occurred between the ages of 5 and 15 years. Chorioretinal atrophy is also a frequent finding which results in moderate to severe visual field and advanced rod-cone dystrophy from younger ages, also confirmed by absence of scotopic function on dark adaptation. The macular dysfunction on mfERG was profound and of early onset. A heterozygous mutation in intron 7 of the VCAN gene (c.4004-1G > A) was found. Conclusions: We described a rare autosomal dominant vitreoretinopathy with near complete penetrance in a Portuguese family. Abnormal peripheral vitreoretinal adhesions, retinal detachment and chorioretinal atrophy are present in most of the examined individuals at young ages. Early onset of advanced visual field and electrophysiologic abnormalities were observed in this family. We also added relevant information to the literature by reporting our experience in surgical management of Wagner Syndrome patients with, and at risk of, retinal detachment.

Novel mutations in the COL2A1 gene in Japanese patients with Stickler syndrome

Article

Full-text available

Jul 2016

Stickler syndrome is an inherited connective tissue disorder that affects the eyes, cartilage and articular tissues. The phenotypes of Stickler syndrome include congenital high myopia, retinal detachment, premature joint degeneration, hearing impairment and craniofacial anomalies, such as cleft palate and midline facial hypoplasia. The disease is genetically heterogeneous, and the majority of the cases are caused by mutations in the COL2A1 gene. We examined 40 Japanese patients with Stickler syndrome from 23 families to determine whether they had mutations in the COL2A1 gene. This analysis was conducted by examining each patient’s genomic DNA by Sanger sequencing. Five nonsense, 4 splicing and 8 deletion mutations in the COL2A1 gene were identified, accounting for 21 of the 23 families. Different mutations of the COL2A1 gene were associated with similar phenotypes but with different degrees of expressivity.

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Erratum to: ISCEV Standard for full-field clinical electroretinography (2015 update)

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This document, from the International Society for Clinical Electrophysiology of Vision (ISCEV), presents an updated and revised ISCEV Standard for full-field clinical electroretinography (ffERG or simply ERG). The parameters for Standard flash stimuli have been revised to accommodate a variety of light sources including gas discharge lamps and light emitting diodes. This ISCEV Standard for clinical ERGs specifies six responses based on the adaptation state of the eye and the flash strength: (1) Dark-adapted 0.01 ERG (rod ERG); (2) Dark-adapted 3 ERG (combined rod-cone standard flash ERG); (3) Dark-adapted 3 oscillatory potentials; (4) Dark-adapted 10 ERG (strong flash ERG); (5) Light-adapted 3 ERG (standard flash "cone" ERG); and (6) Light-adapted 30 Hz flicker ERG. ISCEV encourages the use of additional ERG protocols for testing beyond this minimum standard for clinical ERGs.

Analysis of donor splice signals in different organisms

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We present here a new algorithm for functional site analysis. It is based on four main assumptions: each variation of nucleotide composition makes a different contribution to the overall binding free energy of interaction between a functional site and another molecule; nonfunctioning site-like regions (pseudosites) are absent or rare in genomes; there may be errors in the sample of sites; and nucleotides of different site positions are considered to be mutually dependent. In this algorithm, the site set is divided into subsets, each described by a certain consensus. Donor splice sites of the human protein-coding genes were analyzed. Comparing the results with other methods of donor splice site prediction has demonstrated a more accurate prediction of consensus sequences AG/GU(A,G), G/GUnAG, /GU(A,G)AG, /GU(A,G)nGU, and G/GUA than is achieved by weight matrix and consensus (A,C)AG/GU(A,G)AGU with mismatches. The probability of the first type error, El, for the obtained consensus set was about 0.05, and the probability of the second type error, E2, was 0.15. The analysis demonstrated that accuracy of the functional site prediction could be improved if one takes into account correlations between the site positions. The accuracy of prediction by using human consensus sequences was tested on sequences from different organisms. Some differences in consensus sequences for the plant Arabidopsis sp., the invertebrate Caenorhabditis sp., and the fungus Aspergillus sp. were revealed. For the yeast Saccharomyces sp. only one conservative consensus, /GUA(U,A,C)G(U,A,C), was revealed (El = 0.03, E2 = 0.03). Yeast is a very interesting model to use for analysis of molecular mechanisms of splicing.

Autosomal Recessive Stickler Syndrome in Two Families Is Caused by Mutations in the COL9A1 Gene

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To investigate COL9A1 in two families suggestive of autosomal recessive Stickler syndrome and to delineate the associated phenotype. The probands of two consanguineous autosomal recessive Stickler families were evaluated for homozygosity using SNP microarray in one and haplotype analysis in the other. Subsequently, the entire COL9A1 open reading frame was analyzed by DNA sequencing in all members of the respective families. Several family members were investigated for dysmorphic features as well as ophthalmic, audiologic, and radiologic abnormalities. A novel homozygous COL9A1 mutation (p.R507X) was identified in two affected Turkish sisters, and the previously published mutation (p.R295X) was found in a Moroccan boy. Ophthalmic assessment revealed myopia, cataracts, distinct vitreous changes, progressive chorioretinal degeneration, and exudative and rhegmatogenous retinal detachments. All three had sensorineural hearing loss and epiphyseal dysplasia. Intervertebral disc bulging was observed in one patient and in two heterozygous carriers of the p.R507X mutation. A second, novel mutation was identified in COL9A1, causing autosomal recessive Stickler syndrome together with the previously described nucleotide change in two separate families. Although the overall phenotype was comparable to autosomal dominant Stickler, vitreous changes that may enable recognition of patients who are likely to carry mutations in COL9A1 were identified, and exudative retinal detachment was observed as a new finding in Stickler syndrome.

Foveal Hypoplasia in Patients with Stickler Syndrome

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Purpose: To determine the microstructure of the fovea in patients with Stickler syndrome using imaging by spectral-domain optical coherence tomography (SD OCT) and swept-source OCT. Design: Retrospective case series study. Participants: A total of 39 eyes of 25 patients with genetically confirmed Stickler syndrome were studied. Methods: All of the patients had mutations in the COL2A1 gene and were diagnosed with Stickler syndrome. Cross-sectional OCT images, OCT angiography (OCTA), and en face OCT images were assessed. The ratio of the foveal inner retinal layer (fIRL) thickness to the parafoveal inner retinal layer (pIRL) thickness, the ratio of the foveal outer retinal layer (fORL) thickness to the parafoveal outer retinal layer (pORL) thickness, and the size of the foveal avascular zone (FAZ) were determined. Main outcome measures: The degree of foveal hypoplasia and the best-corrected visual acuity in patients with Stickler syndrome. Results: A persistence of the inner retinal layers in the fovea with an fIRL/pIRL ratio >0.2 was present in 32 of the 39 eyes (82%). Optical coherence tomography angiography showed that the FAZ was smaller, 0 to 0.19 mm(2), than that of normal eyes, in 25 eyes of 17 patients who underwent OCTA. There was no significant correlation between the visual acuities and the fIRL/pIRL ratios. Conclusions: A mild foveal hypoplasia with a persistence of the IRL is characteristic of eyes with Stickler syndrome. The visual acuities were not correlated with the fIRL/pIRL ratios.

Effect of axial length on full-field and multifocal electroretinograms: Effect of axial length on full-field and multifocal ERGs Sachidanandam, Ravi and Sen

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Purpose: The aim was to investigate the effect of axial length on full-field electroretinogram (ffERG) and multifocal electroretinogram (mfERG) in young Indian subjects. Methods: One hundred subjects (44 male) with refractive errors from +0.50 to -18.00 DS and no myopic retinopathy underwent axial length measurement. ffERG was measured, which included scotopic and photopic responses according to International Society for Clinical Electrophysiology of Vision (ISCEV) guidelines. The mfERG was recorded after correcting for refractive error according to ISCEV standards. The dark-adapted and light-adapted parameters of ffERG and N1, P1 parameters of six rings in mfERG were analysed with axial length, controlled for refractive error. The subjects were divided into seven groups based on axial length. The b/a ratio of dark-adapted and light-adapted 3.0 ffERG and P1/N1 ratio of mfERG amplitudes were analysed for seven groups of axial length. Results: The axial length ranged from 21.79 to 30.55 mm. Significant negative correlations were noted for ffERG and mfERG amplitudes, whereas implicit times showed minimal delay with increase in axial length. In ffERG, the scotopic responses were more decreased compared to photopic responses. In mfERG, P1 and N1 amplitudes were significantly decreased in all the rings in all groups and more reduction was noted in the central ring compared to peripheral rings. The P1 amplitudes were more affected as compared to N1 amplitudes. The light-adapted and dark-adapted 3.0 ERG b/a ratio and P1/N1 ratio for seven axial length groups did not show statistically significant difference. The ERG parameters were not significant with refractive error. Conclusion: This study quantifies the relationship of axial length with ffERG and mfERG parameters in a young Indian population. Although the amplitudes were reduced significantly, the implicit times were not significantly affected. The ERG parameters were more related to axial length than refractive error. Hence, interpretation of ffERG and mfERG parameters needs careful consideration in subjects with increasing axial length.

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