Skip to main content
Top
Published in: Documenta Ophthalmologica 3/2020

01-06-2020 | Original Research Article

A novel method for electroretinogram assessment in patients with central retinal vein occlusion

Authors: Neda Sefandarmaz, Soroor Behbahani, Alireza Ramezani

Published in: Documenta Ophthalmologica | Issue 3/2020

Login to get access

Abstract

Purpose

Central retinal vein occlusion (CRVO) is the second most common retinal vascular disorder after diabetic retinopathy that affects the eyes. We propose a method for distinction of normal and central CRVO eyes based on electroretinogram (ERG).

Methods

Seventeen patients with CRVO in one eye were analyzed. Their ERG signals were collected in six different stimuli, including four records in the darkness (dark-adapted 0.01, dark-adapted 3.0, dark-adapted oscillatory potentials, and dark-adapted 10) and two records in brightness (light-adapted 3.0 and light-adapted 30 Hz flicker). Nonlinear features such as Hurst exponent (HE) and approximate entropy (ApEn) were extracted from healthy and CRVO eyes. Finally, a parabolic mapping and two criteria (theta angle and the density of points) were proposed to distinguish the groups.

Results

For ApEn, the P values of dark-adapted 3.0 oscillatory (P = 0.0433) and flicker (P = 0.0425) confirmed significant differences between the groups. For HE, the P values of dark-adapted 3.0 oscillatory (P = 0.0421) and flicker 30 Hz (P = 0.0402) confirmed differences between the healthy and CRVO groups. The P values of theta angle for dark-adapted 3.0 (P = 0.0199), dark-adapted oscillatory (P = 0.0265), dark-adapted 10.0 (P = 0.0166), light-adapted 3.0 (P = 0.0411), and flicker (P = 0.0361) showed significant differences. Using the density criterion, the statistical test demonstrated a significant difference between the groups in dark-adapted 3 (P = 0.0038), dark-adapted oscillatory (P = 0.0102), dark-adapted 10.0 (P = 0.0071), light-adapted 3.0 (P = 0.0319), and flicker 30 Hz (P = 0.0076).

Conclusion

The proposed features have made it possible to distinguish between healthy and CRVO eyes. This method could be helpful in some cases with no definite diagnosis or to estimate the severity of CRVO.
Literature
1.
go back to reference Uhumwangho OM, Itina EI (2015) Retinal diseases in a tertiary hospital in Southern Nigeria. J West Afr Coll Surg 5(2):1–16PubMedPubMedCentral Uhumwangho OM, Itina EI (2015) Retinal diseases in a tertiary hospital in Southern Nigeria. J West Afr Coll Surg 5(2):1–16PubMedPubMedCentral
2.
go back to reference Wittström E (2017) Central retinal vein occlusion in younger Swedish adults: case reports and review of the literature. Open Ophthalmol J 11:89–102PubMedPubMedCentral Wittström E (2017) Central retinal vein occlusion in younger Swedish adults: case reports and review of the literature. Open Ophthalmol J 11:89–102PubMedPubMedCentral
3.
go back to reference Rogers S, McIntosh RL, Cheung N et al (2010) The prevalence of retinal vein occlusion: pooled data from population studies from the United States, Europe, Asia, and Australia. Ophthalmology 117:313–319PubMedPubMedCentral Rogers S, McIntosh RL, Cheung N et al (2010) The prevalence of retinal vein occlusion: pooled data from population studies from the United States, Europe, Asia, and Australia. Ophthalmology 117:313–319PubMedPubMedCentral
4.
go back to reference Prisco D, Marcucci R (2002) Retinal vein thrombosis: risk factors, pathogenesis, and therapeutic approach. Pathophysiol Haemost Thromb 32(5–6):308–311PubMed Prisco D, Marcucci R (2002) Retinal vein thrombosis: risk factors, pathogenesis, and therapeutic approach. Pathophysiol Haemost Thromb 32(5–6):308–311PubMed
5.
go back to reference Lahey JM, Tunc M, Kearney J et al (2002) Laboratory evaluation of hypercoagulable states in patients with central retinal vein occlusion who are less than 56 years of age. Ophthalmology 109(1):126–131PubMed Lahey JM, Tunc M, Kearney J et al (2002) Laboratory evaluation of hypercoagulable states in patients with central retinal vein occlusion who are less than 56 years of age. Ophthalmology 109(1):126–131PubMed
6.
go back to reference Hayreh SS, Klugman MR, Podhajsky P, Kolder HE (1989) Electroretinography in central retinal vein occlusion: correlation of electroretinographic changes with pupillary abnormalities. Graefes Arch Clin Exp Ophthalmol 227(6):549–561PubMed Hayreh SS, Klugman MR, Podhajsky P, Kolder HE (1989) Electroretinography in central retinal vein occlusion: correlation of electroretinographic changes with pupillary abnormalities. Graefes Arch Clin Exp Ophthalmol 227(6):549–561PubMed
7.
go back to reference Williamson TH, Keating D, Bradnam M (1997) Electroretinography of central retinal vein occlusion under scotopic and photopic conditions: what to measure? Acta Ophthalmol Scand 75(1):48–53PubMed Williamson TH, Keating D, Bradnam M (1997) Electroretinography of central retinal vein occlusion under scotopic and photopic conditions: what to measure? Acta Ophthalmol Scand 75(1):48–53PubMed
8.
go back to reference Larsson J, Andreasson S, Bauer B (1998) Cone b-wave implicit time as an early predictor of rubeosis in central retinal vein occlusion. Am J Ophthalmol 125(2):247–249PubMed Larsson J, Andreasson S, Bauer B (1998) Cone b-wave implicit time as an early predictor of rubeosis in central retinal vein occlusion. Am J Ophthalmol 125(2):247–249PubMed
9.
go back to reference Larsson J, Bauer B, Andréasson S (2000) The 30-Hz flicker cone ERG for monitoring the early course of central retinal vein occlusion. Acta Ophthalmol Scand 78(2):187–190PubMed Larsson J, Bauer B, Andréasson S (2000) The 30-Hz flicker cone ERG for monitoring the early course of central retinal vein occlusion. Acta Ophthalmol Scand 78(2):187–190PubMed
10.
go back to reference Montzka DP, Brucker AJ, Quinn GE (1991) Electroretinogram interpretation in central retinal vein occlusion. Ophthalmology 98(12):1837–1844PubMed Montzka DP, Brucker AJ, Quinn GE (1991) Electroretinogram interpretation in central retinal vein occlusion. Ophthalmology 98(12):1837–1844PubMed
11.
go back to reference Sakaue H, Katsumi O, Hirose T (1989) Electroretinographic findings in fellow eyes of patients with central retinal vein occlusion. Arch Ophthalmol 107(10):1459–1462PubMed Sakaue H, Katsumi O, Hirose T (1989) Electroretinographic findings in fellow eyes of patients with central retinal vein occlusion. Arch Ophthalmol 107(10):1459–1462PubMed
12.
go back to reference Johnson MA, Marcus S, Elman MJ et al (1988) Neovascularization in central retinal vein occlusion: electroretinographic findings. Arch Ophthalmol 106(3):348–352PubMed Johnson MA, Marcus S, Elman MJ et al (1988) Neovascularization in central retinal vein occlusion: electroretinographic findings. Arch Ophthalmol 106(3):348–352PubMed
13.
go back to reference Hassan-Karimi H, Jafarzadehpur E, Blouri B, Hashemi H, Sadeghi AZ, Mirzajani A (2012) Frequency domain electroretinography in retinitis pigmentosa versus normal eyes. J Ophthalmic Vis Res 7(1):34–38PubMedPubMedCentral Hassan-Karimi H, Jafarzadehpur E, Blouri B, Hashemi H, Sadeghi AZ, Mirzajani A (2012) Frequency domain electroretinography in retinitis pigmentosa versus normal eyes. J Ophthalmic Vis Res 7(1):34–38PubMedPubMedCentral
14.
go back to reference Gauvin M, Lina J-M, Lachapelle P (2014) Advance in ERG analysis: from peak time and amplitude to frequency, power, and energy. BioMed Res Int, Article ID, p 246096 Gauvin M, Lina J-M, Lachapelle P (2014) Advance in ERG analysis: from peak time and amplitude to frequency, power, and energy. BioMed Res Int, Article ID, p 246096
15.
go back to reference Nair SS, Joseph KP (2014) Chaotic analysis of the electroretinographic signal for diagnosis. BioMed Res Int, Article ID, p 503920 Nair SS, Joseph KP (2014) Chaotic analysis of the electroretinographic signal for diagnosis. BioMed Res Int, Article ID, p 503920
16.
go back to reference Bornschein H, Goodman G, Gunkel RD (1957) Temporal aspects of the human electroretinogram: a study of the implicit time-amplitude relationship of the b-wave. AMA Arch Ophthalmol 57(3):386–392PubMed Bornschein H, Goodman G, Gunkel RD (1957) Temporal aspects of the human electroretinogram: a study of the implicit time-amplitude relationship of the b-wave. AMA Arch Ophthalmol 57(3):386–392PubMed
17.
go back to reference Barraco R, Bellamonte L, Brai M (2007) Time-frequency behavior of the a-wave of the human electroretinogram. IFMBE proceedings 16:919–922 Barraco R, Bellamonte L, Brai M (2007) Time-frequency behavior of the a-wave of the human electroretinogram. IFMBE proceedings 16:919–922
18.
go back to reference Barraco R, Persano Adorno D, Brai M, Tranchina L (2014) A comparison among different techniques for human ERG signals processing and classification. Phys Med 30:86–95PubMed Barraco R, Persano Adorno D, Brai M, Tranchina L (2014) A comparison among different techniques for human ERG signals processing and classification. Phys Med 30:86–95PubMed
19.
go back to reference Miguel JM, Boquete L, Ortega S, Cordero CA, Barea R, Blanco R (2012) MfERG LAB: software for processing multifocal electroretinography signals. Comput Methods Programs Biomed 108(1):377–387PubMed Miguel JM, Boquete L, Ortega S, Cordero CA, Barea R, Blanco R (2012) MfERG LAB: software for processing multifocal electroretinography signals. Comput Methods Programs Biomed 108(1):377–387PubMed
20.
go back to reference Miguel Jimenez JM, Ortega S, Boquete L, Rodríguez-Ascariz JM, Blanco R (2011) Multifocal ERG wavelet packet decomposition applied to glaucoma diagnosis. BioMed Eng Online 10(37):37PubMedPubMedCentral Miguel Jimenez JM, Ortega S, Boquete L, Rodríguez-Ascariz JM, Blanco R (2011) Multifocal ERG wavelet packet decomposition applied to glaucoma diagnosis. BioMed Eng Online 10(37):37PubMedPubMedCentral
21.
go back to reference Nair SS, Paul Joseph K (2014) Wavelet-based electroretinographic signal analysis for diagnosis. Biomed Signal Process Control 9:37–44 Nair SS, Paul Joseph K (2014) Wavelet-based electroretinographic signal analysis for diagnosis. Biomed Signal Process Control 9:37–44
22.
go back to reference Crevier DW, Meister M (1998) Synchronous period-doubling in flicker vision of salamander and man. J Neurophysiol 79(4):1869–1878PubMed Crevier DW, Meister M (1998) Synchronous period-doubling in flicker vision of salamander and man. J Neurophysiol 79(4):1869–1878PubMed
23.
go back to reference Molaie M, Falahian R, Gharibzadeh S, Jafari S, Sprott JC (2014) Artificial neural networks: powerful tools for modeling chaotic behavior in the nervous system. Front Comput Neurosci 8(40):40PubMedPubMedCentral Molaie M, Falahian R, Gharibzadeh S, Jafari S, Sprott JC (2014) Artificial neural networks: powerful tools for modeling chaotic behavior in the nervous system. Front Comput Neurosci 8(40):40PubMedPubMedCentral
24.
go back to reference McCulloch DL, Marmor MF, Brigell MG, Hamilton R, Holder GE, Tzekov R, Bach M (2015) ISCEV Standard for full-field clinical electroretinography. Doc Ophthalmol 130:1–12PubMed McCulloch DL, Marmor MF, Brigell MG, Hamilton R, Holder GE, Tzekov R, Bach M (2015) ISCEV Standard for full-field clinical electroretinography. Doc Ophthalmol 130:1–12PubMed
25.
go back to reference Marmor MF, Fulton AB, Holder GE, Miyake Y, Brigell M, Bach M (2009) ISCEV Standard for full-field clinical electroretinography (2008 update). Doc Ophthalmol 118:69–77PubMed Marmor MF, Fulton AB, Holder GE, Miyake Y, Brigell M, Bach M (2009) ISCEV Standard for full-field clinical electroretinography (2008 update). Doc Ophthalmol 118:69–77PubMed
26.
go back to reference Singh A, Kaur J (2016) Approximate entropy (ApEn) based heart rate variability analysis. Indian J Sci Technol 9(47):1–4 Singh A, Kaur J (2016) Approximate entropy (ApEn) based heart rate variability analysis. Indian J Sci Technol 9(47):1–4
27.
go back to reference Kamath C (2015) Entropy measures of irregularity and complexity for surface electrocardiogram time series in patients with congestive heart failure. J Adv Comput Res 6(4):1–11 Kamath C (2015) Entropy measures of irregularity and complexity for surface electrocardiogram time series in patients with congestive heart failure. J Adv Comput Res 6(4):1–11
28.
go back to reference Natarajan K, Acharya RU, Alias F, Tiboleng T, Puthusserypady SK (2004) Nonlinear analysis of EEG signals at different mental states. BioMed Eng OnLine 3:7PubMedPubMedCentral Natarajan K, Acharya RU, Alias F, Tiboleng T, Puthusserypady SK (2004) Nonlinear analysis of EEG signals at different mental states. BioMed Eng OnLine 3:7PubMedPubMedCentral
29.
go back to reference Blythe DAJ, Haufe S, Müller K-R, Nikulin VV (2014) The effect of linear mixing in the EEG on Hurst exponent estimation. NeuroImage 99:377–387PubMed Blythe DAJ, Haufe S, Müller K-R, Nikulin VV (2014) The effect of linear mixing in the EEG on Hurst exponent estimation. NeuroImage 99:377–387PubMed
30.
go back to reference Adeli H, Dastidar SG, Dadmehr N (2007) A wavelet-chaos methodology for the analysis of EEGs and EEG sub-bands to detect seizure and epilepsy. IEEE Trans Biomed Eng 54(2):205–211PubMed Adeli H, Dastidar SG, Dadmehr N (2007) A wavelet-chaos methodology for the analysis of EEGs and EEG sub-bands to detect seizure and epilepsy. IEEE Trans Biomed Eng 54(2):205–211PubMed
31.
32.
go back to reference Kannathal N, Chee J, Er K, Lim K, Tat OH (2014) Chaotic analysis of epileptic EEG signals. In: Proceeding of the 15th international conference on biomedical engineering, pp 652–654 Kannathal N, Chee J, Er K, Lim K, Tat OH (2014) Chaotic analysis of epileptic EEG signals. In: Proceeding of the 15th international conference on biomedical engineering, pp 652–654
33.
go back to reference Behbahani S, Moridani MK (2015) Nonlinear Poincaré analysis of respiratory. Bratisl Med J 116(7):426–432 Behbahani S, Moridani MK (2015) Nonlinear Poincaré analysis of respiratory. Bratisl Med J 116(7):426–432
34.
go back to reference Moridani MK, Pouladian M (2009) Detection ischemic episodes from electrocardiogram signal using wavelet transform. J Biomed Sci Eng 2(04):239 Moridani MK, Pouladian M (2009) Detection ischemic episodes from electrocardiogram signal using wavelet transform. J Biomed Sci Eng 2(04):239
35.
go back to reference Behbahani S, Nasrabadi AM (2009) Applications of fuzzy similarity index method in the processing of hypnosis. J Biomed Sci Eng 2(5):359–362 Behbahani S, Nasrabadi AM (2009) Applications of fuzzy similarity index method in the processing of hypnosis. J Biomed Sci Eng 2(5):359–362
36.
go back to reference Behbahani S, Nasrabadi AM (2013) The relation of susceptibility levels of hypnosis and different mental tasks. Signal Image Video Process 7(4):1–9 Behbahani S, Nasrabadi AM (2013) The relation of susceptibility levels of hypnosis and different mental tasks. Signal Image Video Process 7(4):1–9
37.
go back to reference Behbahani S, Dabanloo NJ, Nasrabadi AM, Dourado A (2016) Prediction of epileptic seizures based on heart rate variability. Technol Health Care 24(6):795–810PubMed Behbahani S, Dabanloo NJ, Nasrabadi AM, Dourado A (2016) Prediction of epileptic seizures based on heart rate variability. Technol Health Care 24(6):795–810PubMed
38.
go back to reference Behbahani S, Dabanloo NJ, Nasrabadi AM, Dourado A (2016) Classification of ictal and seizure-free HRV signals with focus on lateralization of epilepsy. Technol Health Care 23(1):43–54 Behbahani S, Dabanloo NJ, Nasrabadi AM, Dourado A (2016) Classification of ictal and seizure-free HRV signals with focus on lateralization of epilepsy. Technol Health Care 23(1):43–54
39.
go back to reference Matsui Y, Katsumi O, Sakaue H, Hirose T (1994) Electroretinogram b/a wave ratio improvement in central retinal vein obstruction. Br J Ophthalmol 78:191–198PubMedPubMedCentral Matsui Y, Katsumi O, Sakaue H, Hirose T (1994) Electroretinogram b/a wave ratio improvement in central retinal vein obstruction. Br J Ophthalmol 78:191–198PubMedPubMedCentral
40.
go back to reference Breton ME, Schueller AW, Montzka DP (1991) Electroretinogram b-wave implicit time and b/a wave ratio as a function of intensity in central retinal vein occlusion. Ophthalmology 98(12):1845–1853PubMed Breton ME, Schueller AW, Montzka DP (1991) Electroretinogram b-wave implicit time and b/a wave ratio as a function of intensity in central retinal vein occlusion. Ophthalmology 98(12):1845–1853PubMed
41.
go back to reference Yasuda S, Kachi S, Kondo M, Ushida H, Uetani R, Terui T, Piao C-H, Terasaki H (2011) Significant correlation between electroretinogram parameters and ocular vascular endothelial growth factor concentration in central retinal vein occlusion eyes. Investig Ophthalmol Vis Sci 52:5737–5742 Yasuda S, Kachi S, Kondo M, Ushida H, Uetani R, Terui T, Piao C-H, Terasaki H (2011) Significant correlation between electroretinogram parameters and ocular vascular endothelial growth factor concentration in central retinal vein occlusion eyes. Investig Ophthalmol Vis Sci 52:5737–5742
42.
go back to reference Sabates R, Hirose T, McMeel JW (1983) Electroretinography in the prognosis and classification of central retinal vein occlusion. Arch Ophthalmol 101(2):232–235PubMed Sabates R, Hirose T, McMeel JW (1983) Electroretinography in the prognosis and classification of central retinal vein occlusion. Arch Ophthalmol 101(2):232–235PubMed
43.
go back to reference Ferman-Attar G, Rotenstreich Y (2011) The diagnostic significance of the ERG a/b ratio in retinal disorders. Investig Ophthalmol Vis Sci 52:6073 Ferman-Attar G, Rotenstreich Y (2011) The diagnostic significance of the ERG a/b ratio in retinal disorders. Investig Ophthalmol Vis Sci 52:6073
Metadata
Title
A novel method for electroretinogram assessment in patients with central retinal vein occlusion
Authors
Neda Sefandarmaz
Soroor Behbahani
Alireza Ramezani
Publication date
01-06-2020
Publisher
Springer Berlin Heidelberg
Published in
Documenta Ophthalmologica / Issue 3/2020
Print ISSN: 0012-4486
Electronic ISSN: 1573-2622
DOI
https://doi.org/10.1007/s10633-019-09742-2

Other articles of this Issue 3/2020

Documenta Ophthalmologica 3/2020 Go to the issue